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1 1 Conservation Biology for All EDITED BY : Navjot S. Sodhi AND * Department of Department of Biological Sciences, National University of Singapore Organismic and Evolutionary Biology, Harvard University (*Address while the book was prepared) Paul R. Ehrlich Department of Biology, Stanford University 1 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

2 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 3 Great Clarendon Street, Oxford DP 26 OX Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide in Oxford New York Auckland Cape Town Dar es Salaam Hong Kong Karachi Kuala Lumpur Madrid Melbourne Mexico City Nairobi New Delhi Shanghai Taipei Toronto fi ces in With of Argentina Austria Brazil Chile Czech Republic France Greece Guatemala Hungary Italy Japan Poland Portugal Singapore South Korea Switzerland Thailand Turkey Ukraine Vietnam Oxford is a registered trade mark of Oxford University Press in the UK and in certain other countries Published in the United States by Oxford University Press Inc., New York # Oxford University Press 2010 The moral rights of the authors have been asserted Database right Oxford University Press (maker) First published 2010 Reprinted with corrections 2010 Available online with corrections, January 2011 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, without the prior permission in writing of Oxford University Press, or as expressly permitted by law, or under terms agreed with the appropriate reprographics rights organization. Enquiries concerning reproduction outside the scope of the above should be sent to the Rights Department, Oxford University Press, at the address above You must not circulate this book in any other binding or cover and you must impose the same condition on any acquirer British Library Cataloguing in Publication Data Data available Library of Congress Cataloging in Publication Data Data available Typeset by SPI Publisher Services, Pondicherry, India Printed in Great Britain on acid-free paper by CPI Antony Rowe, Chippenham, Wiltshire – 19 – 955423 – 2 (Hbk.) ISBN 978 – 0 – – 955424 – 9 (Pbk.) 19 0 – ISBN 978 3579108642 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

3 1 Contents Dedication xi xii Acknowledgements List of Contributors xiii Foreword Georgina Mace xvii Introduction Navjot S. Sodhi and Paul R. Ehrlich 1 Paul R. Ehrlich Introduction Box 1: Human population and conservation ( )2 )3 Paul R. Ehrlich Introduction Box 2: Ecoethics ( 1: Conservation biology: past and present Curt Meine 7 7 1.1 Historical foundations of conservation biology )8 Box 1.1: Traditional ecological knowledge and biodiversity conservation ( Fikret Berkes fi eld 12 1.2 Establishing a new interdisciplinary 1.3 Consolidation: conservation biology secures its niche 15 16 1.4 Years of growth and evolution Box 1.2: Conservation in the Philippines ( Mary Rose C. Posa )19 21 1.5 Conservation biology: a work in progress 21 Summary 22 Suggested reading Relevant websites 22 2: Biodiversity Kevin J. Gaston 27 2.1 How much biodiversity is there? 27 33 2.2 How has biodiversity changed through time? 2.3 Where is biodiversity? 35 2.4 In conclusion 39 Navjot S. Sodhi )40 Box 2.1: Invaluable biodiversity inventories ( 41 Summary 41 Suggested reading Revelant websites 42 3: Ecosystem functions and services 45 Cagan H. Sekercioglu 45 3.1 Climate and the Biogeochemical Cycles 3.2 Regulation of the Hydrologic Cycle 48 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

4 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do vi CONTENTS 3.3 Soils and Erosion 50 51 3.4 Biodiversity and Ecosystem Function )52 Robert M. Pringle Box 3.1: The costs of large-mammal extinctions ( Mark S. Boyce Box 3.2: Carnivore conservation ( )54 )55 Box 3.3: Ecosystem services and agroecosystems in a landscape context ( Teja Tscharntke 57 3.5 Mobile Links )58 Box 3.4: Conservation of plant-animal mutualisms ( Priya Davidar Box 3.5: Consequences of pollinator decline for the global food supply ( Claire Kremen )60 64 3.6 Nature ’ s Cures versus Emerging Diseases 65 3.7 Valuing Ecosystem Services 66 Summary 67 Relevant websites Acknowledgements 67 4: Habitat destruction: death by a thousand cuts William F. Laurance 73 4.1 Habitat loss and fragmentation 73 73 4.2 Geography of habitat loss Box 4.1: The changing drivers of tropical deforestation ( )75 William F. Laurance 76 4.3 Loss of biomes and ecosystems Box 4.2: Boreal forest management: harvest, natural disturbance, and climate change ( )80 Ian G. Warkentin ‐ use intensi fi 4.4 Land 82 cation and abandonment Benjamin S. Halpern, Carrie V. Kappel, Box 4.3: Human impacts on marine ecosystems ( )83 Fiorenza Micheli, and Kimberly A. Selkoe 86 Summary 86 Suggested reading 86 Relevant websites 5: Habitat fragmentation and landscape change 88 Andrew F. Bennett and Denis A. Saunders 88 5.1 Understanding the effects of landscape change 90 5.2 Biophysical aspects of landscape change 92 5.3 Effects of landscape change on species Andrew F. Bennett Box 5.1: Time lags and extinction debt in fragmented landscapes ( and Denis A. Saunders )92 96 5.4 Effects of landscape change on communities 99 5.5 Temporal change in fragmented landscapes 99 5.6 Conservation in fragmented landscapes Box 5.2: Gondwana Link: a major landscape reconnection project ( Andrew F. Bennett 101 and Denis A. Saunders ) ) 102 Paul R. Ehrlich Box 5.3: Rewilding ( 104 Summary 104 Suggested reading 104 Relevant websites 6: Overharvesting Carlos A. Peres 107 108 6.1 A brief history of exploitation 110 6.2 Overexploitation in tropical forests © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

5 1 CONTENTS vii 6.3 Overexploitation in aquatic ecosystems 113 115 6.4 Cascading effects of overexploitation on ecosystems sheries ( Daniel Pauly Box 6.1: The state of fi 118 ) 120 6.5 Managing overexploitation ) 121 Box 6.2: Managing the exploitation of wildlife in tropical forests ( Douglas W. Yu 126 Summary 126 Relevant websites 7: Invasive species 131 Daniel Simberloff ) Daniel Simberloff Box 7.1: Native invasives ( 131 Daniel Simberloff ) 132 Box 7.2: Invasive species in New Zealand ( 7.1 Invasive species impacts 133 7.2 Lag times 143 7.3 What to do about invasive species 144 Summary 148 Suggested reading 148 Relevant websites 148 8: Climate change 153 Thomas E. Lovejoy 153 8.1 Effects on the physical environment 8.2 Effects on biodiversity 154 Box 8.1: Lowland tropical biodiversity under global warming ( Navjot S. Sodhi ) 156 158 8.3 Effects on biotic interactions 159 8.4 Synergies with other biodiversity change drivers 8.5 Mitigation 159 Box 8.2: Derivative threats to biodiversity from climate change ( Paul R. Ehrlich ) 160 161 Summary 161 Suggested reading 161 Relevant websites 9: Fire and biodiversity 163 David M. J. S. Bowman and Brett P. Murphy 164 fi 9.1 What is re? 164 re in geological time fi 9.2 Evolution and 165 9.3 Pyrogeography David M. J. S. Bowman and Brett P. Murphy ) 167 Box 9.1: Fire and the destruction of tropical forests ( re 167 fi climate patterns decoupled by – 9.4 Vegetation 9.5 Humans and their use of fi re 170 David M. J. S. Bowman and Brett P. Murphy ) 171 Box 9.2: The grass- fi re cycle ( fi s giant ) 173 ’ Box 9.3: Australia reweeds ( David M. J. S. Bowman and Brett P. Murphy 173 9.6 Fire and the maintenance of biodiversity re regimes 176 9.7 Climate change and fi 177 Summary 178 Suggested reading 178 Relevant websites Acknowledgements 178 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

6 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do viii CONTENTS 10: Extinctions and the practice of preventing them Stuart L. Pimm and Clinton N. Jenkins 181 181 10.1 Why species extinctions have primacy 182 (Jennifer B.H. Martiny) Box 10.1: Population conservation 10.2 How fast are species becoming extinct? 183 10.3 Which species become extinct? 186 187 10.4 Where are species becoming extinct? 10.5 Future extinctions 192 10.6 How does all this help prevent extinctions? 195 196 Summary 196 Suggested reading 196 Relevant websites 11: Conservation planning and priorities 199 Thomas Brooks 11.1 Global biodiversity conservation planning and priorities 199 204 11.2 Conservation planning and priorities on the ground Güven Eken, Box 11.1: Conservation planning for Key Biodiversity Areas in Turkey ( _   I g lu, Murat Ataol, Murat Bozdo an, Özge Balk g ı z, Süreyya sfendiyaro Dicle Tuba K ld ) 209 ı ray Lise ı l ı ı ç, and Y 11.3 Coda: the completion of conservation planning 213 214 Summary Suggested reading 214 214 Relevant websites Acknowledgments 215 12: Endangered species management: the US experience 220 David. S. Wilcove 220 12.1 Identi cation fi Box 12.1: Rare and threatened species and conservation planning in Madagascar Claire Kremen, Alison Cameron, Tom Allnutt, and Andriamandimbisoa ( fi 221 Raza ) mpahanana Box 12.2: Flagship species create Pride ( 223 ) Peter Vaughan 226 12.2 Protection 12.3 Recovery 230 12.4 Incentives and disincentives 232 12.5 Limitations of endangered species programs 233 Summary 234 234 Suggested reading 234 Relevant websites ed landscapes fi 13: Conservation in human-modi 236 Lian Pin Koh and Toby A. Gardner ” wild nature “ cation and the concept of fi 13.1 A history of human modi 236 Box 13.1: Endocrine disruption and biological diversity ( 237 ) J. P. Myers fi ‐ 13.2 Conservation in a human modi 240 ed world 242 13.3 Selectively logged forests 243 13.4 Agroforestry systems © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

7 1 CONTENTS ix 13.5 Tree plantations 245 Box 13.2: Quantifying the biodiversity value of tropical secondary forests and exotic 247 Jos Barlow tree plantations ( ) 13.6 Agricultural land 248 Matthew Struebig, Box 13.3: Conservation in the face of oil palm expansion ( ) 249 Ben Phalan, and Emily Fitzherbert Box 13.4: Countryside biogeography: harmonizing biodiversity and agriculture 251 ) Jai Ranganathan and Gretchen C. Daily ( 13.7 Urban areas 253 254 13.8 Regenerating forests on degraded land 255 fi 13.9 Conservation and human livelihoods in modi ed landscapes 256 13.10 Conclusion Summary 257 Suggested reading 257 Relevant websites 258 14: The roles of people in conservation 262 fi C. Anne Claus, Kai M. A. Chan, and Terre Satter eld uence on ecosystems 14.1 A brief history of humanity ’ 262 sin fl 14.2 A brief history of conservation 262 Box 14.1: Customary management and marine conservation ( C. Anne Claus, Kai 264 M. A. Chan, and Terre Satter fi eld ) Box 14.2: Historical ecology and conservation effectiveness in West Africa ( C. Anne Claus, eld ) 265 fi Kai M. A. Chan, and Terre Satter 14.3 Common conservation perceptions 265 re ( Paul R. Ehrlich ) 267 Box 14.3: Elephants, animal rights, and Camp fi 269 environment relations ‐ 14.4 Factors mediating human Box 14.4: Conservation, biology, and religion ( 270 ) Kyle S. Van Houtan 273 14.5 Biodiversity conservation and local resource use 14.6 Equity, resource rights, and conservation 275 276 ) Priya Davidar Box 14.5: Empowering women: the Chipko movement in India ( 278 14.7 Social research and conservation Summary 281 281 Relevant websites 281 Suggested reading 15: From conservation theory to practice: crossing the divide Madhu Rao and Joshua Ginsberg 284 Box 15.1: Swords into Ploughshares: reducing military demand for wildlife products 285 ( Lisa Hickey, Heidi Kretser, Elizabeth Bennett, and McKenzie Johnson ) 286 ) Tony Whitten Box 15.2: The World Bank and biodiversity conservation ( Heather Tallis, Joshua H. Goldstein, Box 15.3: The Natural Capital Project ( 288 ) and Gretchen C. Daily 15.1 Integration of Science and Conservation Implementation 290 Box 15.4: Measuring the effectiveness of conservation spending ( Matthew Linkie and Robert J. Smith ) 291 292 15.2 Looking beyond protected areas Karl Didier ) 293 Box 15.5: From managing protected areas to conserving landscapes ( © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

8 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do x CONTENTS 15.3 Biodiversity and human poverty 293 297 ) Tom Clements Box 15.6: Bird nest protection in the Northern Plains of Cambodia ( ) Box 15.7: International activities of the Missouri Botanical Garden ( Peter Raven 301 15.4 Capacity needs for practical conservation in developing countries 303 15.5 Beyond the science: reaching out for conservation 304 305 15.6 People making a difference: A Rare approach 305 15.7 Pride in the La Amistad Biosphere Reserve, Panama 306 15.8 Outreach for policy 306 15.9 Monitoring of Biodiversity at Local and Global Scales ı Box 15.8: Hunter self-monitoring by the Isoseño-Guaran ́ in the Bolivian ) 307 Chaco ( Andrew Noss Summary 310 Suggested reading 310 Relevant websites 310 s toolbox – principles for the design and analysis ’ 16: The conservation biologist of conservation studies 313 Corey J. A. Bradshaw and Barry W. Brook ’ 314 biodiversity 16.1 Measuring and comparing ‘ Toby Gardner ) 314 Box 16.1: Cost effectiveness of biodiversity monitoring ( 316 ) David Bickford Box 16.2: Working across cultures ( 319 16.2 Mensurative and manipulative experimental design ) Box 16.3: Multiple working hypotheses ( 321 Corey J. A. Bradshaw and Barry W. Brook 324 Box 16.4: Bayesian inference ( Corey J. A. Bradshaw and Barry W. Brook ) 16.3 Abundance Time Series 326 328 16.4 Predicting Risk 16.5 Genetic Principles and Tools 330 331 Noah K. Whiteman Box 16.5: Functional genetics and genomics ( ) 333 16.6 Concluding Remarks Corey J. A. Bradshaw and Barry W. Brook ) 334 Box 16.6: Useful textbook guides ( Summary 335 335 Suggested reading 335 Relevant websites Acknowledgements 336 341 Index © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

9 1 Dedication NSS: To those who have or want to make the difference. PRE: To my mentors — Charles Birch, Charles Michener, and Robert Sokal. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

10 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: Acknowledgements Wren Wirth, and the Mertz Gilmore Foundation NSS thanks the Sarah and Daniel Hrdy Fellowship for their support. We thank Mary Rose C. Posa, Pei in Conservation Biology (Harvard University) and Xin, Ross McFarland, Hugh Tan, and Peter Ng the National University of Singapore for support for their invaluable assistance. We also thank while this book was prepared. He also thanks Ian Sherman, Helen Eaton, and Carol Bestley at Naomi Pierce for providing him with an of ce. fi Oxford University Press for their help/support. PRE thanks Peter and Helen Bing, Larry Condon, © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

11 1 List of Contributors  gan Murat Bozdo Tom Allnutt g a Derne Do   g i, Hürriyet Cad. 43/12 Dikmen, Ankara, tal Sciences, Policy and Department of Environmen Turkey. Management, 137 Mulford Hall, University of Califor- . nia, Berkeley, CA 94720-3114, USA Corey J. A. Bradshaw Environment Institute, School of Earth and Environ- Murat Ataol mental Sciences, University of Adelaide, South Aus-   g g Do a Derne i, Hürriyet Cad. 43/12 Dikmen, Ankara, tralia 5005 AND South Australian Research and Turkey . Development Institute, P.O. Box 120, Henley Beach, ı Özge Balk z South Australia 5022, Australia. Do  g a Derne  g i, Hürriyet Cad. 43/12 Dikmen, Ankara, Barry W. Brook Turkey . Environment Institute, School of Earth and Environmen- Jos Barlow tal Sciences, University of Adelaide, South Australia Lancaster Environment Centre, Lancaster University, 5005, Australia. . Lancaster, LA1 4YQ, UK Thomas Brooks Andrew F. Bennett Center for Applied Biodiversity Science, Conservation School of Life and Environmental Sciences, Deakin International, 2011 Crystal Drive Suite 500, Arling- University, 221 Burwod Highway, Burwood, VIC ton VA 22202, USA; World Agroforestry Center . 3125, Australia (ICRAF), University of the Philippines Los Baños, Laguna 4031, Philippines; AND School of Geography Elizabeth Bennett and Environmental Studies, University of Tasmania, Wildlife Conservation Society, 2300 Southern Boule- Hobart TAS 7001, Australia. vard., Bronx, NY 10464-1099, USA. Alison Cameron Fikret Berkes Max Planck Institute for Ornithology, Eberhard- Natural Resources Institute, 70 Dysart Road, University Gwinner-Straße, 82319 Seewiesen, Germany. of Manitoba, Winnipeg MB R3T 2N2, Canada. Kai M. A. Chan David Bickford Institute for Resources, Environment and Sustainability, Department of Biological Sciences, National University University of British Colum bia, Vancouver, British of Singapore, 14 Science Drive 4, Singapore 117543, Columbia V6T 1Z4, Canada. Republic of Singapore. C. Anne Claus David M. J. S. Bowman Departments of Anthropology and Forestry & Envi- School of Plant Science, University of Tasmania, Private ronmental Studies, Yale University,10 Sachem Street, Bag 55, Hobart, TAS 7001, Australia. New Haven, CT 06511, USA. Mark S. Boyce Tom Clements Department of Biological Sciences, University of Wildlife Conservation Society, Phnom Penh, Cambodia. Alberta, Edmonton, Alberta T6G 2E9, Canada. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

12 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: LIST OF CONTRIBUTORS xiv _  Gretchen C. Daily Isfendiyaro Süreyya glu   Center for Conservation Biology, Department of Biology, a Derne g Do g i, Hürriyet Cad. 43/12 Dikmen, Ankara, and Woods Institute, 371 Serra Mall, Stanford Univer- Turkey. sity, Stanford, CA 94305-5020, USA. Clinton N. Jenkins Nicholas School of the Environment, Duke University, Priya Davidar Box 90328, LSRC A201, Durham, NC 27708, USA. School of Life Sciences, Pondicherry University, Kalapet, Pondicherry 605014, India. McKenzie Johnson Wildlife Conservation Society, 2300 Southern Boule- Karl Didier vard, Bronx, NY 10464-1099, USA. Wildlife Conservation So ciety, 2300 Southern Boule- vard, Bronx, NY 10464-1099, USA. Carrie V. Kappel National Center for Ecological Analysis and Synthe- Paul R. Ehrlich sis, 735 State Street, Santa Barbara, CA 93101, USA. Center for Conservation Biology, Department of Biol- ogy, Stanford University, Stanford, CA 94305-5020, ı Dicle Tuba K ı ç l USA.   Do g i, Hürriyet Cad. 43/12 Dikmen, Ankara, g a Derne Turkey. Güven Eken   i, Hürriyet Cad. 43/12 Dikmen, Ankara, Do g a Derne g Lian Pin Koh Turkey. Institute of Terrestrial Ecosystems, Swiss Federal In- stitute of Technology (ETH Zürich), CHN G 74.2, Emily Fitzherbert Universitätstrasse 16, Zurich 8092, Switzerland. Institute of Zoology, Zoological Society of London, Regent ’ s Park, London, NW1 4RY, UK. Claire Kremen Department of Environmental Sciences, Policy and Toby A. Gardner Management, 137 Mulford Hall, University of Cali- Department of Zoology, University of Cambridge, fornia, Berkeley, CA 94720-3114, USA. Downing Street, Cambridge, CB2 3EJ, UK AND Heidi Kretser Departamento de Biologia, Universidade Federal de Wildlife Conservation Society, 2300 Southern Boule- Lavras, Lavras, Minas Gerais, 37200-000, Brazil. vard, Bronx, NY 10464-1099, USA. Kevin J. Gaston William F. Laurance Department of Animal & Plant Sciences, University Smithsonian Tropical Research Institute, Apartado of Shef eld, S10 2TN, UK. fi fi eld, Shef 0843-03092, Balboa, Ancón, Republic of Panama. Joshua Ginsberg Matthew Linkie Wildlife Conservation Society, 2300 Southern Boule- Fauna & Flora International, 4th Floor, Jupiter House, vard, Bronx, NY 10464-1099, USA. Station Road, Cambridge, CB1 2JD, UK. Joshua H. Goldstein ı Y ray Lise ı ld Human Dimensions of Natural Resources, Warner   a Derne Do g g i, Hürriyet Cad. 43/12 Dikmen, Ankara, College of Natural Resources, Colorado State Univer- Turkey. sity, Fort Collins, CO 80523-1480, USA. Thomas E. Lovejoy Benjamin S. Halpern The H. John Heinz III Center for Science, Economics National Center for Ecological Analysis and and the Environment, 900 17th Street NW, Suite 700, Synthesis, 735 State Street, Santa Barbara, CA Washington, DC 20006, USA. 93101, USA. Jennifer B. H. Martiny Lisa Hickey Department of Ecology and Evolutionary Biology, Wildlife Conservation Society, 2300 Southern Boule- University of California, Irvine, CA 92697, USA. vard, Bronx, NY 10464-1099, USA. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

13 1 LIST OF CONTRIBUTORS xv Curt Meine Madhu Rao Aldo Leopold Foundation/International Crane Wildlife Conservation Society Asia Program 2300 Foundation, P.O. Box 38, Prairie du Sac, WI S. Blvd., Bronx, New York, NY 10460, USA. 53578, USA. Peter Raven Fiorenza Micheli fi Missouri Botanical Garden, Post Of ce Box 299, St. fi c Hopkins Marine Station, Stanford University, Paci Louis, MO 63166-0299, USA. Grove, CA 93950, USA. Andriamandimbisoa Raza fi mpahanana Réseau de la Biodiversité de Madagascar, Wildlife Brett P. Murphy Conservation Society, Villa Ifanomezantsoa, Soavim- School of Plant Science, University of Tasmania, Pri- bahoaka, Boîte Postale 8500, Antananarivo 101, Ma- vate Bag 55, Hobart, TAS 7001, Australia. dagascar. J. P. Myers Terre Satter fi eld Environmental Health Sciences, 421 E Park Street, Institute for Resources, Environment and Sustainabil- Charlottesville VA 22902, USA. ity, University of British Columbia, Vancouver, Brit- Andrew Noss ish Columbia V6T 1Z4, Canada. Proyecto Gestión Integrada de Territorios Indigenas Denis A. Saunders WCS-Ecuador, Av. Eloy Alfaro N37-224 y Coremo CSIRO Sustainable Ecosystems, GPO Box 284, Can- Apartado, Postal 17-21-168, Quito, Ecuador. berra, ACT 2601, Australia. Daniel Pauly Cagan H. Sekercioglu Seas Around Us Project, University of British Colum- Center for Conservation Biology, Department of Biology, bia, Vancouver, British Columbia, V6T 1Z4, Canada. Stanford University, Stanford, CA 94305-5020, USA. Carlos A. Peres Kimberly A. Selkoe School of Environmental Sciences, University of East National Center for Ecological Analysis and Synthe- Anglia, Norwich, NR4 7TJ, UK. sis, 735 State Street, Santa Barbara, CA 93101, USA. Ben Phalan Daniel Simberloff Conservation Science Group, Department of Zoology, Department of Ecology and Evolutionary Biology, University of Cambridge, Downing Street, Cam- University of Tennessee, Knoxville, TN 37996, bridge, CB2 3EJ, UK. USA. Stuart L. Pimm Robert J. Smith Nicholas School of the Environment, Duke University, Durrell Institute of Conservation and Ecology, Box 90328, LSRC A201, Durham, NC 27708, USA. University of Kent, Canterbury, Kent, CT2 7NR, Mary Rose C. Posa UK. Department of Biology, National University of Singa- Navjot S. Sodhi pore, 14 Science Drive 4, Singapore 117543, Republic Department of Biological Sciences, National Univer- of Singapore. sity of Singapore, 14 Science Drive 4, Singapore Robert M. Pringle 117543, Republic of Singapore AND Department of Department of Biology, Stanford University, Stan- Organismic and Evolutionary Biology, Harvard Uni- ford, CA 94305, USA. versity, Cambridge, MA 02138, USA. Jai Ranganathan Matthew Struebig National Center for Ecological Analysis and Synthe- School of Biological & Chemical Sciences, Queen sis, 735 State Street, Suite 300 Santa Barbara, CA Mary, University of London, Mile End Road, London, 93109, USA. E1 4NS, UK. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

14 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: xvi LIST OF CONTRIBUTORS Ian G. Warkentin Heather Tallis Biology, Memorial Univer- – Environmental Science The Natural Capital Project, Woods Institute for the sity of Newfoundland, Corner Brook, Newfoundland Environment, 371 Serra Mall, Stanford University, and Labrador A2H 6P9, Canada. Stanford, CA 94305-5020, USA. Noah K. Whiteman Teja Tscharntke Department of Organismic and Evolutionary Biol- Agroecology, University of Göttingen, Germany. ogy, Harvard University, Cambridge, MA 02138, USA. Kyle S. Van Houtan Tony Whitten Department of Biology, O W Rollins Research Ctr, The World Bank, Washington, DC, USA. 1st Floor, 1510 Clifton Road, Lab# 1112 Emory David Wilcove University AND Center for Ethics, 1531 Dickey Department of Ecology and Evolutionary Biology, Drive, Emory University, Atlanta, GA 30322, Princeton University, Princeton, NJ 08544-1003, USA. USA. Peter Vaughan Douglas W. Yu Rare, 1840 Wilson Boulevard, Suite 204, Arlington, School of Biological Sciences, University of East VA 22201, USA. Anglia, Norwich, NR4 7TJ, UK. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

15 1 Foreword 2010 was named by the United Nations to be the servation biology relevant to and applicable by International Year of Biodiversity, coinciding all is therefore a key task. with major political events that set the stage for It is in this context that Navjot Sodhi and Paul a radical review of the way we treat our environ- Ehlrich have contributed this important book. ment and its biological riches. So far, the reports Covering all aspects of conservation biology have been dominated by recon fi rmations that from the deleterious drivers, through to the im- people and their lifestyles continue to deplete pacts on people, and providing tools, techniques, the earth s biodiversity. We are still vastly over- ’ and background to practical solutions, the book spending our natural capital and thereby depriv- provides a resource for many different people ing future generations. If that were not bad and contexts. Written by the world s leading ex- ’ enough news in itself, there are no signs that perts you will fi nd clear summaries of the latest actions to date have slowed the rate of depletion. literature on how to decide what to do, and then In fact, it continues to increase, due largely to how to do it. Presented in clear and accessible growing levels of consumption that provide in- text, this book will support the work of many creasingly unequal bene ts to different groups of fi people. There are different kinds of conservation people. actions, at different scales, and affecting different It is easy to continue to delve into the patterns parts of the biosphere, all laid out clearly and and processes that lie at the heart of the problem. concisely. But it is critical that we also start to do everything There is something in here for everyone who is, we can to reverse all the damaging trends. These or wishes to be, a conservation biologist. I am actions cannot and should not be just the respon- sure you will all be inspired and better informed sibility of governments and their agencies. It to do something that will improve the prospects must be the responsibility of all of us, including for all, so that in a decade or so, when the world scientists, wildlife managers, naturalists, and in- community next examines the biodiversity ac- deed everyone who cares so that future genera- nitely be taking a turn for fi counts, things will de tions can have the same choices and the same the better! opportunity to marvel at and bene t from nature, fi Georgina Mace CBE FRS as our generation has had. We all can be involved Imperial College London in actions to improve matters, and making con- 18 November 2010 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

16 1 Introduction Navjot S. Sodhi and Paul R. Ehrlich Our actions have put humanity into a deep envi- (e.g. food, medicines, pollination, pest control, ronmental crisis. We have destroyed, degraded, and fl ood protection). – s natural habitats ’ and polluted Earth indeed, Habitat loss and pollution are particularly uence of virtually all of them have felt the in fl acute in developing countries, which are of spe- the dominant species. As a result, the vast major- cial concern because these harbor the greatest ity of populations and species of plants and ani- species diversity and are the richest centers of key working parts of human life support – mals endemism. Sadly, developing world conserva- – are in decline, and many are already systems fi cult to afford an tion scientists have found it dif extinct. Increasing human population size and authoritative textbook of conservation biology, consumption per person (see Introduction Box which is particularly ironic, since it is these 1) have precipitated an extinction crisis – the countries where the rates of habitat loss are high- , which is comparable to “ sixth mass extinction ” est and the potential bene fi ts of superior informa- past extinction events such as the Cretaceous- tion in the hands of scientists and managers are Tertiary mass extinction 65 million years ago therefore greatest. There is also now a pressing that wiped out all the dinosaurs except for the need to educate the next generation of conserva- birds. Unlike the previous extinction events, tion biologists in developing countries, so that which were attributed to natural catastrophes hopefully they are in a better position to protect including volcanic eruptions, meteorite impact their natural resources. With this book, we intend and global cooling, the current mass extinction to provide cutting-edge but basic conservation is exclusively humanity s fault. Estimates indicate ’ science to developing as well as developed coun- that numerous species and populations are cur- try inhabitants. The contents of this book are rently likely being extinguished every year. But freely available on the web. yet. all is not lost – Since our main aim is to make up-to-date conser- Being the dominant species on Earth, humans vation knowledge widely available, we have invit- have a moral obligation (see Introduction Box 2) ed many of the top names in conservation biology to ensure the long-term persistence of rainfor- c topics. Overall, this book repre- fi to write on speci ests, coral reefs, and tidepools as well as sagua- sents a project that the conservation community ro cacti, baobab trees, tigers, rhinos, pandas, has deemed worthy of support by donations of ies, and a birds of paradise, morpho butter fl time and effort. None of the authors, including plethora of other creatures. All these landmarks ourselves, will gain fi nancially from this project. and life make this planet remarkable – our It is our hope that this book will be of relevance imagination will be bankrupt if wild nature is and use to both undergraduate and graduate stu- – even if civilization could survive obliterated dents as well as scientists, managers, and person- the disaster. In addition to moral and aesthetic nel in non-governmental organizations. The book sh reason to preserve fi reasons, we have a sel should have all the necessary topics to become a – nature it provides society with countless and required reading for various undergraduate and invaluable goods and absolutely crucial services graduate conservation-related courses. English is 1 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

17 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 2 CONSERVATION BIOLOGY FOR ALL Introduction Box 1 Human population and conservation Paul R. Ehrlich mined and smelted today, water and petroleum The size of the human population is must come from lower quality sources, deeper approaching 7 billion people, and its most wells, or (for oil) from deep beneath the ocean fundamental connection with conservation is and must be transported over longer distances, simple: people compete with other animals, ‐ all at ever greater environmental cost. which unlike green plants cannot make their The tasks of conservation biologists are made Homo sapiens uses, own food. At present more dif cult by human population growth, as fi coopts, or destroys close to half of all the food is readily seen in the I=PAT equation (Holdren available to the rest of the animal kingdom (see and Ehrlich 1974; Ehrlich and Ehrlich 1981). Introduction Box 1 Figure). That means that, in Impact (I) on biodiversity is not only a result of essence, every human being added to the population size (P), but of that size multiplied population means fewer individuals can be by af uence (A) measured as per capita fl supported in the remaining fauna. consumption, and that product multiplied by But human population growth does much another factor (T), which summarizes the more than simply cause a proportional decline political economic ‐ technologies and socio ‐ in animal biodiversity – since as you know, we arrangements to service that consumption. degrade nature in many ways besides More people surrounding a rainforest reserve competing with animals for food. Each in a poor nation often means more individuals additional person will have a disproportionate invading the reserve to gather fi rewood or negative impact on biodiversity in general. The bush meat. More people in a rich country may fi rst farmers started farming the richest soils ‐ road vehicles (ORVs) assaulting mean more off they could fi nd and utilized the richest and most the biota – especially if the ORV manufacturers accessible resources fi rst (Ehrlich and Ehrlich are politically powerful and can successfully 2005). Now much of the soil that people fi rst ght bans on their use. As poor countries ’ fi farmed has been eroded away or paved over, populations grow and segments of them and agriculturalists increasingly are forced to fl become more af uent, demand rises for meat turn to marginal land to grow more food. and automobiles, with domesticated animals Equally,deeperandpoorer oredepositsmustbe continues Human beings consuming resources. Photograph by Mary Rose Posa. Introduction Box 1 Figure continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

18 1 INTRODUCTION 3 Introduction Box 1 (Continued) to humanely lower birth rates until population growth stops and begins a slow decline toward a competing with or devouring native biota, cars sustainable size (Daily 1994). et al. causing all sorts of assaults on biodiversity, and both adding to climate disruption. Globally, as a growing population demands greater quantities of plastics, industrial chemicals, REFERENCES pesticides, fertilizers, cosmetics, and medicines, Anonymous. (2008). Welcome to the Anthropocene. the toxi fi cation of the planet escalates, Chemical and Engineering News ,3. 86 , bringing frightening problems for organisms Daily, G. C. and Ehrlich, A. H. (1994). Optimum human ranging from polar bears to frogs (to say population size. Population and Environment , 15 , nothing of people!) (see Box 13.1). 475. – 469 In sum, population growth (along with Ehrlich, P. R. and Ehrlich, A. H. (1981). Extinction: the escalating consumption and the use of causes and consequences of the disappearance of environmentally malign technologies) is a major . Random House, New York, NY. species driver of the ongoing destruction of Ehrlich, P. R. and Ehrlich, A. H. (2005). One with Nineveh: populations, species, and communities that is a politics, consumption, and the human future , (with new salient feature of the Anthropocene afterword). Island Press, Washington, DC. (Anonymous 2008). Humanity, as the dominant Ehrlich, P. R. and Ehrlich, A. H. (2008). The Dominant animal (Ehrlich and Ehrlich 2008), simply out Animal: human evolution and the environment . Island ’ competes other animals for the planet s Press, Washington, DC. productivity, and often both plants and animals Holdren J. P. and Ehrlich, P. R. (1974). Human population for its freshwater. While dealing with more American Scientist , 62 , and the global environment. limited problems, it therefore behooves every – 292. 282 conservation biologist to put part of her time into restraining those drivers, including working Introduction Box 2 Ecoethics Paul R. Ehrlich The landethic simply enlargesthe boundariesof scale institutions that try (and ‐ wielded by large the community to include soils, waters, plants, sometimes succeed) to control broad aspects of ... andanimals,orcollectively:theland .AldoLeo- our global civilization. Those institutions pold (1949) include governments, religions, transnational corporations, and the like. To ignore these As you read this book, you should keep in mind power relations is, in essence, to ignore the that the problem of conserving biodiversity is most important large scale issues, such as ‐ replete with issues of practical ethics – agreed ‐ conservation in the face of further human upon notions of the right or wrong of actual population growth and of rapid climate change behaviors (Singer 1993; Jamieson 2008). If issues that demand global ethical discussion. – civilization is to maintain the ecosystem services scale ecoethical dilemmas are ‐ Small (Chapter 3) that can support a sustainable commonly faced by conservation biologists. society and provide virtually everyone with a Should we eat shrimp in a restaurant when we reasonable quality of life, humanity will need ’ t determine its provenance? Should we can to focus much more on issues with a signi cant fi become more vegetarian? Is it legitimate to fl y ecoethics . ” “ conservation connection, around the world in jet aircraft to try and Ultimately everything must be examined persuade people to change a lifestyle that ” personal “ from common ‐ scale small ying around the world in jet aircraft? fl includes ecoethical decisions to the ethics of power How should we think about all the trees cut continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

19 . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: Conservation Biology for All Introduction Box 2 (Continued) down to produce the books and articles we ve ’ poor, while striving to limit aggregate con- written? These sorts of decisions are poignantly sumption by humanity. discussed by Bearzi (2009), who calls for Start a global World War II type mobilization • conservation biologists to think more carefully to shift to more benign energy technologies about their individual decisions and set a better wide and thus reduce the chances of a world ‐ example where possible. Some personal conservation disaster caused by rapid climate – such as how many decisions are not so minor change. children to have. But ironically Bearzi does not • Judge technologies not just on what they do bearing decisions, even though discuss child ‐ people and the organ- for people but also to especially in rich countries these are often the support isms that are key parts of their life ‐ most conservation signi cant ethical decisions fi ‐ systems. an individual makes. Educate students, starting in kindergarten, • cult ethical Ecotourism is a hotbed of dif fi about the crucial need to preserve biodiversity issues, some incredibly complex, as shown in ’ empathy not just to all and expand peoples Box 14.3. But perhaps the most vexing ethical human beings but also to the living elements in questions in conservation concern con fl icts the natural world. between the needs and prerogatives of peoples Most conservation biologists view the task of ‐ and non human organisms. This is seen in issues preserving biodiversity as fundamentally one of like protecting reserves from people, where in ethics (Ehrlich and Ehrlich 1981). Nonetheless, the extreme some conservation biologists plead long experience has shown that arguments for strict exclusion of human beings based on a proposed ethical need to preserve (e.g. Terborgh 2004), and by the debates over our only known living relatives in the entire the preservation of endangered organisms and universe, the products of incredible traditional rights to hunt them. The latter is evolutionary sequences billions of years in exempli fi ed by complex aboriginal extent, have largely fallen on deaf ears. Most “ ” subsistence whaling issues (Reeves 2002). ecologists have therefore switched to While commercial whaling is largely admittedly risky instrumental arguments for responsible for the collapse of many stocks, conservation (Daily 1997). What proportion of aboriginal whaling may threaten some of the conservation effort should be put into remnants. Does one then side with the whales promoting instrumental approaches that might or the people, to whom the hunts may be an back fi re or be effective in only the short or important part of their tradition? Preserving tactical issue. middle term is an ethical ‐ the stocks by limiting aboriginal takes seems One of the best arguments for emphasizing the ecoethical thing to do, since it allows for the instrumental is that they can at least traditional hunting to persist, which will not buy time for the necessarily slow happen if the whales go extinct. Tradition is a cultural evolutionary process of coal mining or land development tricky thing – changing the norms that favor attention to may be family traditions, but ecoethically those reproducible capital and property rights to occupations should end. the near exclusion of natural capital. Perhaps most daunting of all is the task of ” Some day Aldo Leopold ’ s “ Land Ethic getting broad agreement from diverse cultures may become universal – until then on ecoethical issues. It has been suggested that conservation biologists will face many ethical Millennium Assessment of wide ‐ a world challenges. (MAHB) be established to, Human Behavior among other things, facilitate discussion and debate (Ehrlich and Kennedy 2005). My own views of the basic ecoethical paths that should REFERENCES be pursued follow. Others may differ, but if we ’ don t start debating ecoethics now, the current Bearzi, G. (2009). When sword fi sh conservation biologists ethical stasis will likely persist. – ,1 eat sword 2. fi sh. Conservation Biology , 23 Daily, G. C., ed. (1997). Nature ’ s services: societal depen- • Work hard to humanely bring human popu- . Island Press, Washington, dence on natural ecosystems lation growth to a halt and start a slow decline. DC. • Reduce overconsumption by the already rich while increasing consumption by the needy continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

20 1 5 INTRODUCTION (Continued) Introduction Box 2 . Oxford Univer- Sand county almanac Leopold, A. (1949). Ehrlich, P. R. and Ehrlich, A. H. (1981). Extinction: the sity Press, New York, NY. causes and consequences of the disappearance of spe- Reeves, R. R. (2002). The origins and character of cies. Random House, New York, NY. whaling: a global review. aboriginal subsistence ’ ‘ Ehrlich, P. R. and Kennedy, D. (2005). Millennium 106. – ,71 32 , Mammal Review assessment of human behavior: a challenge to scientists. Singer, P. (1993). Practical ethics. 2nd edn. University Press, 563. , 309 Science , 562 – Cambridge, UK. Ethics and the environment: an in- Jamieson, D. (2008). Terborgh, J. (2004). Requiem for nature . Island Press, troduction . Cambridge University Press, Cambridge, UK. Washington, DC. Saunders. They also examine biophysical aspects of kept at a level comprehensible to readers for landscape change, and how such change affects po- whom English is a second language. pulations, species, and communities. The book contains 16 chapters, which are brief- ly introduced below: Chapter 6. Overharvesting Chapter 1. Conservation biology: past and present Biodiversity is under heavy threat from anthropo- genic overexploitation (e.g. harvest for food or dec- In this chapter, Curt Meine introduces the discipline oration or of live animals for the pet trade). For by tracing its history. He also highlights the inter- example, bushmeat or wild meat hunting is imperil- disciplinary nature of conservation science. ing many tropical species as expanding human po- Chapter 2. Biodiversity pulations in these regions seek new sources of Kevin J. Gaston de fi nes biodiversity and lays out the protein and create potentially pro fi table new ave- obstacles to its better understanding in this chapter. nues for trade at both local and international levels. In this Chapter, Carlos A. Peres highlights the effects Chapter 3. Ecosystem functioning and services of human exploitation of terrestrial and aquatic In this chapter, Cagan H. Sekercioglu recapitulates biomes on biodiversity. natural ecosystem functions and services. Chapter 7. Invasive species Chapter 4. Habitat destruction: death by a Daniel Simberloff presents an overview of invasive thousand cuts species, their impacts and management in this chapter. William F. Laurance provides an overview of con- Chapter 8. Climate change temporary habitat loss in this chapter. He evaluates patterns of habitat destruction geographically and Climate change is quickly emerging as a key issue in contrasts it in different biomes and ecosystems. He the battle to preserve biodiversity. In this chapter, also reviews some of the ultimate and proximate Thomas E. Lovejoy reports on the documented im- factors causing habitat loss. pacts of climate change on biotas. Chapter 5. Habitat fragmentation and landscape Chapter 9. Fire and biodiversity change Evolutionary and ecological principles related to Conceptual approaches used to understand conser- conservation in landscapes subject to regular vation in fragmented landscapes are summarized in fi res are presented in this chapter by David M. J. S. this chapter by Andrew F. Bennett and Denis A. Bowman and Brett P. Murphy. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

21 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: 6 CONSERVATION BIOLOGY FOR ALL conserving biodiversity in human-modi fi ed land- Chapter 10. Extinctions and the practice of scapes. preventing them Stuart L. Pimm and Clinton N. Jenkins explore why Chapter 14. The roles of people in conservation extinctions are the critical issue for conservation The effective and sustainable protection of biodiver- science. They also list a number of conservation sity will require that the sustenance needs of native options. people are adequately considered. In this chapter, C. fi eld Anne Claus, Kai M. A. Chan, and Terre Satter Chapter 11. Conservation planning and priorities highlight that understanding human activities and In this chapter, Thomas Brooks charts the history, human roles in conservation is fundamental to effec- state, and prospects of conservation planning and tive conservation. prioritization in terrestrial and aquatic habitats. He Chapter 15. From conservation theory to practice: focuses on successful conservation implementation crossing the divide s conceptual frame- planned through the discipline ’ work of vulnerability and irreplaceability. Madhu Rao and Joshua Ginsberg explore the implementation of conservation science in this chap- Chapter 12. Endangered species management: the ter. US experience s toolbox ’ Chapter 16. The conservation biologist – In this chapter, David S. Wilcove focuses on principles for the design and analysis of conserva- endangered species management, emphasizing the tion studies United States of America (US) experience. Because In this chapter, Corey J. A. Bradshaw and Barry the US has one of the oldest and possibly strongest W. Brook, discuss measures of biodiversity patterns laws to protect endangered species, it provides an followed by an overview of experimental design and illuminating case history. associated statistical paradigms. They also present fi ed Chapter 13. Conservation in human-modi the analysis of abundance time series, assessments landscapes of species endangerment, and a brief introduction ’ to genetic tools to assess the conservation status of Lian Pin Koh and Toby A. Gardner discuss the species. challenges of conserving biodiversity in degraded and modi ed landscapes with a focus on the tropi- fi Each chapter includes boxes written by various cal terrestrial biome in this chapter. They highlight experts describing additional relevant material, ed fi the extent to which human activities have modi case studies/success stories, or personal perspec- natural ecosystems and outline opportunities for tives. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

22 1 CHAPTER 1 Conservation biology: past 1 and present Curt Meine Our job is to harmonize the increasing kit of tioners remain embedded within a process of c tools and the increasing recklessness in fi scienti change that has challenged conservation “ in the using them with the shrinking biotas to which ’ even while extending conservation ” old sense, s they are applied. In the nature of things we are core commitment to the future of life, human and mediators and moderators, and unless we can non-human, on Earth. help rewrite the objectives of science we are pre- There is as yet no comprehensive history of destined to failure. conservation that allows us to understand the Aldo Leopold (1940; 1991) — s ’ causes and context of conservation biology emergence. Environmental ethicists and histor- Conservation in the old sense, of this or that ians have provided essential studies of particular resource in isolation from all other resources, is conservation ideas, disciplines, institutions, indi- not enough. Environmental conservation based viduals, ecosystems, landscapes, and resources. on ecological knowledge and social understand- Yet we still lack a broad, fully integrated account ing is required. of the dynamic coevolution of conservation sci- Raymond Dasmann (1959) — ence, philosophy, policy, and practice (Meine Conservation biology is a mission-driven disci- 2004). The rise of conservation biology marked a pline comprising both pure and applied science. ” at the intersection of these rallying point “ new We feel that conservation biology is a new ... domains; exactly how, when, and why it did so fi eld, or at least a new rallying point for biologists are still questions awaiting exploration. wishing to pool their knowledge and techniques to solve problems. Michael E. Soulé and Bruce A. Wilcox (1980) — 1.1 Historical foundations of conservation biology s emergence, com- ’ Since conservation biology Conservation biology, though rooted in older sci- eld has rightly empha- fi mentary on (and in) the fi c, professional, and philosophical traditions, enti sized its departure from prior conservation gained its contemporary de fi nition only in the thread science and practice. However, the main ” “ mid-1980s. Anyone seeking to understand the — the description, explanation, appre- of the fi eld history and growth of conservation biology thus biological ciation, protection, and perpetuation of fi eld has formed faces inherent challenges. The diversity can be traced much further back through too recently to be viewed with historical detach- the historical tapestry of the biological sciences fl uid ment, and the trends shaping it are still too and the conservation movement (Mayr 1982; s practi- ’ to be easily traced. Conservation biology 1 Adapted from Meine, C., Soulé, M., and Noss, R. F. (2006). A mission ‐ driven discipline ” : the growth of conservation biology. “ , 20 , 631 – 651. Conservation Biology 7 © Oxford University Press 2010. All rights reserved. For permissions please email: academic[email protected]

23 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 8 McIntosh 1985; Grumbine 1996; Quammen 1996). tions of respect for the natural world both within That thread weaves through related themes and and beyond the Western experience (see Box 1.1 concepts in conservation, including wilderness and Chapter 14). Long before environmentalism protection, sustained yield, wildlife protection began to reshape “ conservation in the old sense ” and management, the diversity-stability hypoth- — prior even to the Progressive Era in the 1960s esis, ecological restoration, sustainability, and — the conservation movement of the early 1900s ecosystem health. By focusing on the thread itself, foundations of conservation biology were being conservation biology brought the theme of laid over the course of biology s epic advances ’ biological diversity to the fore. “ discovery of over the last four centuries. The In so doing, conservation biology has recon- s phrase) was the diversity ” (to use Ernst Mayr ’ nected conservation to deep sources in Western driving force behind the growth of biological natural history and science, and to cultural tradi- thought. “ Hardly any aspect of life is more Box 1.1 Traditional ecological knowledge and biodiversity conservation Fikret Berkes James Bay, Quebec, Canada (see Box 1.1 Conservation biology is a discipline of Western Figure). In the Peruvian Andes, the centre of science, but there are other traditions of origin of the potato, the Quetchua people conservation in various parts of the world (see maintain a mosaic of agricultural and natural also Chapter 14). These traditions are based on areas as a biocultural heritage site with some local and indigenous knowledge and practice. 1200 potato varieties, both cultivated and wild. Traditional ecological knowledge may be ned as a cumulative body of knowledge, fi de practice and belief, evolving by adaptive processes and handed down through generations by cultural transmission. It is experiential knowledge closely related to a way generational, based on oral ‐ of life, multi transmission rather than book learning, and hencedifferentfrom scienceinanumberof ways. Traditional knowledge does not always result in conservation, just as science does not always result in conservation. But there are a number of ways in which traditional knowledge and practice may lead to conservation outcomes. First, sacred groves and other sacred areas are Paakumshumwaau Biodiversity Reserve in James Box 1.1 Figure protected through religious practice and Bay, Quebec, Canada, established at the request of the Cree Nation enforced by social rules. UNESCO s (the United ’ of Wemindji. Photograph by F. Berkes. c and Cultural Nations Educational, Scienti fi Organization) World Heritage Sites network In some cases, high biodiversity is explainable includes many sacred sites, such as Machu in terms of traditional livelihood practices that Picchu in Peru. Second, many national parks maintain a diversity of varieties, species and have been established at the sites of former landscapes. For example, Oaxaca State in sacred areas, and are based on the legacy of Mexico exhibits high species richness despite traditional conservation. Alto Fragua Indiwasi the absence of of fi cial protected areas. This National Park in Colombia and Kaz Daglari may be attributed to the diversity of local and National Park in Turkey are examples. Third, ‐ indigenous practices resulting in multi new protected areas are being established at functional cultural landscapes. In many parts of the request of indigenous peoples as a the world, agroforestry systems that rely on the safeguard against development. One example cultivation of a diversity of crops and trees is the Paakumshumwaau Biodiversity Reserve in together (as opposed to modern continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

24 1 9 CONSERVATION BIOLOGY: PAST AND PRESENT (Continued) Box 1.1 The objective of formal protected areas monocultures), seem to harbor high species is biodiversity conservation, whereas richness. There are at least three mechanisms traditional conservation is often practiced that help conserve biodiversity in the use of for livelihood and cultural reasons. Making agroforestry and other traditional practices: biodiversity conservation relevant to most of Land use regimes that maintain forest • the world requires bridging this gap, with an patches at different successional stages con- emphasis on sustainability, equity and a serve biodiversity because each stage repre- diversity of approaches. There is international sents a unique community. At the same time, interest in community ‐ conserved areas as a such land use contributes to continued ecosys- class of protected areas. Attention to time ‐ tem renewal. tested practices of traditional conservation • The creation of patches, gaps and mosaics can help develop a pluralistic, more enhance biodiversity in a given area. In the inclusive de fi nition of conservation, and study of landscape ecology, the principle is that build more robust constituencies for low and intermediate levels of disturbance conservation. often increase biodiversity, as compared to disturbed areas. ‐ non • Boundaries between ecological zones are SUGGESTED READING characterized by high diversity, and the creation of new edges (ecotones) by disturbance en- , 2nd edn. Routledge, Berkes, F. (2008). Sacred ecology hances biodiversity, but mostly of “ edge ‐ loving ” New York, NY. species. Overlaps and mixing of plant and ani- mal species produce dynamic landscapes. characteristic than its almost unlimited diversi- For example, Alfred Russel Wallace (1863) warned ” “ Indeed, there is ty, wrote Mayr (1982:133). against the “ extinction of the numerous forms of life hardly any biological process or phenomenon which the progress of cultivation invariably en- where diversity is not involved. ” tails ” and urged his scienti fi c colleagues to assume This “ discovery ” unfolded as colonialism, the the responsibility for stewardship that came with Industrial Revolution, human population growth, knowledge of diversity. expansion of capitalist and collectivist economies, The s rst edition of George Perkins Marsh fi ’ and developing trade networks transformed Man and Nature appeared the following year. In human social, economic, political, and ecological cation, and fi his second chapter, “ Transfer, Modi relationships ever more quickly and profoundly ” Extirpation of Vegetable and of Animal Species, (e.g. Crosby 1986; Grove 1995; Diamond 1997). Marsh examined the effect of humans on biotic ’ sca- Technological change accelerated humanity diversity. Marsh described human beings as a pacity to reshape the world to meet human needs and surveyed human ” new geographical force “ fi ed tensions along and desires. In so doing, it ampli impacts on plants, insects, minute organisms, “ ” basic philosophical fault lines: mechanistic/organ- aquatic animals, ” reptiles, birds, and fi sh, “ ic; utilitarian/reverential; imperialist/arcadian; re- quadrupeds. “ ”“ All nature, ” he wrote, is linked “ ductionism/holism (Thomas et al. 1956; Worster together by invisible bonds, and every organic 1985). As recognition of human environmental im- creature, however low, however feeble, however th century philosophers, pacts grew, an array of 19 dependent, is necessary to the well-being of some scientists, naturalists, theologians, artists, writers, other among the myriad forms of life with which and poets began to regard the natural world within the Creator has peopled the earth. ” He concluded an expanded sphere of moral concern (Nash 1989). his chapter with the hope that people might © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

25 Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: 10 CONSERVATION BIOLOGY FOR ALL “ learn to put a wiser estimate on the works of New concepts from ecology and evolutionary th creation (Marsh 1864). Through the veil of 19 ” fi biology began to lter into conservation and the century language, modern conservation biolo- resource management disciplines during the early th century. Proto-conservation biologists ” “ gists may recognize Marsh, Wallace, and others 20 from this period include Henry C. Cowles, as common intellectual ancestors. whose pioneering studies of plant succession ’ Marsh s landmark volume appeared just as the and the fl ora of the Indiana Dunes led him into post-Civil War era of rampant resource exploita- active advocacy for their protection (Engel 1983); tion commenced in the United States. A generation Victor Shelford, who prodded his fellow ecolo- s book undergirded the Progressive ’ later, Marsh gists to become active in establishing biologically Era reforms that gave conservation in the United representative nature reserves (Croker 1991); Ar- States its modern meaning and turned it into thur Tansley, who similarly advocated establish- a national movement. That movement rode ment of nature reserves in Britain, and who in Theodore Roosevelt ’ s presidency into public con- 1935 contributed the concept of the “ ecosystem ” sciousness and across the American landscape. to science (McIntosh 1985; Golley 1993); Charles Conservationists in the Progressive Era were fa- (1927) provided Animal Ecology Elton, whose text mously split along utilitarian-preservationist the foundations for a more dynamic ecology lines. The utilitarian Resource Conservation Ethic, nition of food chains, food webs, through his de fi realized within new federal conservation agencies, trophic levels, the niche, and other basic concepts; cient, scienti was committed to the ef fi cally in- fi Joseph Grinnell, Paul Errington, Olaus Murie, and formed management of natural resources, to pro- fi other eld biologists who challenged prevailing vide the greatest good to the greatest number for “ notions on the ecological role and value of preda- (Pinchot 1910:48). By contrast, the ” the longest time tors (Dunlap 1988); and biologists who sought to Romantic-Transcendental Preservation Ethic, place national park management in the USA on a overshadowed but persistent through the Progres- sound ecological footing (Sellars 1997; Shafer sive Era, celebrated the aesthetic and spiritual 2001). Importantly, the crisis of the Dust Bowl in value of contact with wild nature, and inspired North America invited similar ecological critiques campaigns for the protection of parklands, refuges, of agricultural practices during the 1930s (Worster forests, and “ wild life. ” 1979; Beeman and Pritchard 2001). Callicott (1990) notes that both ethical camps By the late 1930s an array of conservation con- ‘ were “ essentially human-centered or anthropo- soil erosion, watershed degradation, cerns — ... ’ centric (and) regarded human beings or urban pollution, deforestation, depletion of fi sh- human interests as the only legitimate ends and brought academ- — eries and wildlife populations nonhuman natural entities and nature as a whole ic ecologists and resource managers closer Moreover, the science upon which both ” as means. th century re- together and generated a new awareness of con- relied had not yet experienced its 20 c volutions. Ecology had not yet united the scienti fi servation s ecological foundations, in particular ’ understanding of the abiotic, plant, and animal the signi cance of biological diversity. In 1939 fi components of living systems. Evolutionary biolo- Aldo Leopold summarized the point in a speech gy had not yet synthesized knowledge of genetics, to a symbolically appropriate joint meeting of the population biology, and evolutionary biology. Ge- Ecological Society of America and the Society of ology, paleontology, and biogeography were just American Foresters: beginning to provide a coherent narrative of the temporal dynamics and spatial distribution of life The emergence of ecology has placed the on Earth. Although explicitly informed by the nat- economic biologist in a peculiar dilemma: ural sciences, conservation in the Progressive with one hand he points out the accumu- Era was primarily economic in its orientation, re- fi ndings of his search for utility, or lack lated ductionist in its tendencies, and selective in its of utility, in this or that species; with the application. other he lifts the veil from a biota © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

26 1 11 CONSERVATION BIOLOGY: PAST AND PRESENT limnology, marine biology, and biogeography so complex, so conditioned by interwoven (Mayr 1982). As these advances accrued, main- cooperations and competitions, that no man taining healthy connections between the basic can say where utility begins or ends. No sciences and their application in resource man- ’ without the tongue in species can be ‘ rated elds proved challenging. It fell to a fi agement the cheek; the old categories of ‘ useful ’ and c researchers, inter- fi diverse cohort of scienti ‘ harmful have validity only as conditioned ’ preters, and advocates to enter the public policy by time, place, and circumstance. The only fi gures as Rachel fray (including such notable sure conclusion is that the biota as a whole is Carson, Jacques-Yves Cousteau, Ray Dasmann, useful, and (the) biota includes not only G. Evelyn Hutchinson, Julian Huxley, Eugene plants and animals, but soils and waters as and Howard Odum, and Sir Peter Scott). Many well (Leopold 1991:266 – 67). uence through their of these had worldwide in fl ” the biota as a whole “ With appreciation of came writings and students, their collaborations, and greater appreciation of the functioning of ecolog- their ecological concepts and methodologies. ical communities and systems (Golley 1993). For Working from within traditional disciplines, gov- Leopold and others, this translated into a rede fi - ernment agencies, and academic seats, they stood s aims: away from the nar- ’ nition of conservation at the complicated intersection of conservation row goal of sustaining outputs of discrete — science, policy, and practice a place that would commodities, and toward the more complex ne conservation biology. come to de fi goal of sustaining what we now call ecosystem More pragmatically, new federal legislation in health and resilience. the USA and a growing body of international As conservation ’ s aims were thus being rede- agreements expanded the role and responsibilities ned, its ethical foundations were being recon- fi of biologists in conservation. In the USA the Na- sidered. The accumulation of revolutionary tional Environmental Policy Act (1970) required ’ biological insights, combined with a generation s analysis of environmental impacts in federal deci- experience of fragmented policy, short-term eco- sion-making. The Endangered Species Act (1973) nomics, and environmental decline, yielded Leo- called for an unprecedented degree of scienti c fi s assertion of an Evolutionary-Ecological ’ pold involvement in the identi cation, protection, and fi Land Ethic (Callicott 1990). A land ethic, Leopold recovery of threatened species (see Chapter 12). wrote, “ enlarges the boundaries of the communi- Other laws that broadened the role of biologists ty to include soils, waters, plants, and animals, or in conservation and environmental protection in- changes the role of collectively: the land “ ;it ” clude the Marine Mammal Protection Act (1972), Homo sapiens from conqueror of the land-commu- the Clean Water Act (1972), the Forest and Range- nity to plain member and citizen of it ” (Leopold land Renewable Resources Planning Act (1974), 1949:204). These ethical concepts only slowly the National Forest Management Act (1976), and fi sheries management, gained ground in forestry, the Federal Land Policy Management Act (1976). wildlife management, and other resource man- At the international level, the responsibilities of agement disciplines; indeed, they are contentious biologists were also expanding in response to the still. adoption of bilateral treaties and multilateral In the years following World War II, as con- agreements, including the UNESCO (United Na- sumer demands increased and technologies tions Educational, Scienti c and Cultural Organi- fi evolved, resource development pressures grew. zation) Man and the Biosphere Programme Resource managers responded by expanding (1970), the Convention on International Trade in their efforts to increase the yields of their particu- Endangered Species of Wild Fauna and Flora fi c lar commodities. Meanwhile, the pace of scienti (CITES) (1975), and the Convention on Wetlands change accelerated in disciplines across the Ramsar Con- of International Importance (the “ biological spectrum, from microbiology, genetics, ) (1975). In 1966 the International Union ” vention systematics, and population biology to ecology, for the Conservation of Nature (IUCN) published © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

27 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 12 inventories of threatened species. rst it “ red list ” fi ” c basis fi rm scienti fi “ . Constructing that ” work In short, the need for rigorous science input into researchers and practi- and attracted — — required conservation decision-making was increasing, tioners from varied disciplines (including Ehren- conservation was changing. of even as the science feld himself, whose professional background was This state of affairs challenged the traditional in medicine and physiological ecology). The com- orientation of resource managers and research mon concern that transcended the disciplinary biologists alike. : its extent, role, biological diversity boundaries was value, and fate. By the mid-1970s, the recurring debates within theoretical ecology over the relationship between 1.2 Establishing a new interdisciplinary species diversity and ecosystem stability were eld fi intensifying (Pimm 1991; Golley 1993; McCann In the opening chapter of Conservation Biology: An 2000). Among conservationists the theme of di- Evolutionary-Ecological Perspective , editors Michael s day, began to ’ versity, in eclipse since Leopold Soulé and Bruce Wilcox (1980) described conser- re-emerge. In 1951, renegade ecologists had cre- vation biology as a mission-oriented discipline “ ated The Nature Conservancy for the purpose of comprising both pure and applied science. The ” protecting threatened sites of special biological phrase (or crisis-driven ) was soon crisis-oriented and ecological value. In the 1960s voices for di- added to the list of modi ers describing the fi versity began to be heard within the traditional eld (Soulé 1985). This characterization fi emerging conservation A Different fi elds. Ray Dasmann, in the prevail- of conservation biology as a mission-oriented, (1968: vii) lamented “ Kind of Country ing trend toward uniformity and made the case ” crisis-driven, problem-solving fi eld resonates with “ and for for the preservation of natural diversity ” echoes of the past. The history of conservation cultural diversity as well. Pimlott (1969) detected and environmental management demonstrates “ a sudden stirring of interest in diversity ... Not fi elds (or that the emergence of problem-solving until this decade did the word diversity, as an elds) invari- fi new emphases within established ecological and genetic concept, begin to enter the ably involves new interdisciplinary connections, vocabulary of the wildlife manager or land-use new institutions, new research programs, and Hickey (1974) argued that wildlife ecol- ” planner. new practices. Conservation biology would fol- ogists and managers should concern themselves low this pattern in the 1970s, 1980s, and 1990s. ” with cally fi a scienti “ ; that all living things “ Biological In 1970 David Ehrenfeld published should ” sound wildlife conservation program Conservation , an early text in a series of publications “ encompass the wide spectrum from one-celled that altered the scope, content, and direction of plants and animals to the complex species we call conservation science (e.g. MacArthur and Wilson birds and mammals. Conservation scientists and ” 1963; MacArthur and Wilson 1967; MacArthur advocates of varied backgrounds increasingly 1972; Soulé and Wilcox 1980; CEQ 1980; Frankel framed the fundamental conservation problem 1983; Harris et al. and Soulé 1981; Schonewald-Cox in these new and broader terms (Farnham 2002). 1984; Caughley and Gunn 1986; Soulé 1986; Soulé As the theme of biological diversity gained had also Biological Conservation 1987a) (The journal traction among conservationists in the 1970s, the begun publication a year earlier in England). In his key components of conservation biology began to preface Ehrenfeld stated, Biologists are beginning “ coalesce around it: to forge a discipline in that turbulent and vital area where biology meets the social sciences and huma- Within the sciences proper, the synthesis of “ nities ” . Ehrenfeld recognized that the acts of con- · knowledge from island biogeography and popula- servationists are often motivated by strongly tion biology greatly expanded understanding of the but cautioned that the ” “ humanistic principles, distribution of species diversity and the phenomena rm fi practice of conservation must also have a of speciation and extinction. scienti c basis or, plainly stated, it is not likely to fi © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

28 1 13 CONSERVATION BIOLOGY: PAST AND PRESENT in situ and The fate of threatened species (both Evolution s work ’ ) (Frankel and Soulé 1981). Soulé · ) and the loss of rare breeds and plant germ- ex situ on that volume led to the convening of the First plasm stimulated interest in the heretofore neglected International Conference on Conservation Biology (and occasionally even denigrated) application of in September 1978. The meeting brought together genetics in conservation. an odd assort- “ what looked from the outside like Driven in part by the IUCN red listing process, ment of academics, zoo-keepers, and wildlife con- · captive breeding programs grew; zoos, aquaria, and servationists (Gibbons 1992). Inside, however, ” botanical gardens expanded and rede ned their role fi the experience was more personal, among indivi- as partners in conservation. duals who had come together through important, and often very personal, shifts in professional prio- Wildlife ecologists, community ecologists, and · rities. The proceedings of the 1978 conference were limnologists were gaining greater insight into the Conservation Biology: An Evolutionary- published as role of keystone species and top-down interactions Ecological Perspective (Soulé and Wilcox 1980). The in maintaining species diversity and ecosystem conference and the book initiated a series of meet- health. eld for its ings and proceedings that de fi ned the fi Within forestry, wildlife management, range · growing number of participants, as well as for sheries management, and other ap- management, fi those outside the immediate circle (Brussard plied disciplines, ecological approaches to resource 1985; Gibbons 1992). management gained more advocates. Attention to the genetic dimension of conserva- Advances in ecosystem ecology, landscape ecolo- · tion continued to gain momentum into the early gy, and remote sensing provided increasingly so- 1983). Meanwhile, et al. 1980s (Schonewald-Cox phisticated concepts and tools for land use and awareness ofthreats tospecies diversityand causes conservation planning at larger spatial scales. of extinction was reaching a broader professional As awareness of conservation ssocialdimensions ’ · and public audience (e.g. Ziswiler 1967; Iltis 1972; increased, discussion of the role of values in science Terborgh 1974; Ehrlich and Ehrlich 1981). In partic- became explicit. Interdisciplinary inquiry gave rise to ular, the impact of international development po- environmental history, environmental ethics, ecolog- licies on the world ’ s species-rich, humid tropical ical economics, and other hybrid fi elds. forests was emerging as a global concern. Field keystone indivi- As these trends unfolded, “ biologists, ecologists, and taxonomists, alarmed duals also had special impact. Peter Raven and ” by the rapid conversion of the rainforests and — Paul Ehrlich (to name two) made fundamental witnesses themselves to the loss of research sites contributions to coevolution and population began to sound alarms (e.g. and study organisms — biology in the 1960s before becoming leading et al. Gómez-Pompa 1972; Janzen 1972). By the proponents of conservation biology. Michael early 1980s, the issue of rainforest destruction was gure in the emergence of conser- fi Soulé, a central highlighted through a surge of books, articles, and vation biology, recalls that Ehrlich encouraged fi c reports (e.g. Myers 1979, 1980; NAS 1980; scienti his students to speculate across disciplines, and NRC 1982; see also Chapter 4). had his students read Thomas Kuhn s ’ The Struc- During these years, recognition of the needs of c Revolutions fi ture of Scienti (1962). The intellectual s poor and the developing world was ’ the world led Soulé to adopt population biology syntheses in prompting new approaches to integrating conser- conservation biology (around 1976) the term for his vation and development. This movement was own synthesizing efforts. embodied in a series of international programs, For Soulé, that integration especially entailed meetings, and reports, including the Man and the the merging of genetics and conservation (Soulé Biosphere Programme (1970), the United Nations 1980). In 1974 Soulé visited Sir Otto Frankel while Conference on the Human Environment held in on sabbatical in Australia. Frankel approached Stockholm (1972), and the World Conservation Soulé with the idea of collaborating on a volume Strategy (IUCN 1980). These approaches eventu- Conservation and on the theme (later published as sustainable ally came together under the banner of © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

29 Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 14 fi ned in the report of , especially as de development resource management agencies, and international the World Commission on Environment and De- development organizations (Soulé 1987b). velopment (the Brundtland Report ” ) (WCED “ In retrospect, the rapid growth of conservation 1987). The complex relationship between devel- fl biology re ected essential qualities that set it opment and conservation created tensions within fi fi apart from predecessor and af elds: liated conservation biology from the outset, but also Conservation biology rests upon a scienti fi c foun- drove the search for deeper consensus and inno- · dation in systematics, genetics, ecology, and evolu- vation (Meine 2004). tionary biology. As the Modern Synthesis A Second International Conference on Conser- rearranged the building blocks of biology, and new vation Biology convened at the University of Mi- insights emerged from population genetics, devel- chigan in May 1985 (Soulé 1986). Prior to the opmental genetics (heritability studies), and island meeting, the organizers formed two committees biogeography in the 1960s, the application of to consider establishing a new professional socie- biology in conservation was bound to shift as well. ty and a new journal. A motion to organize the ’ s pri- This found expression in conservation biology Society for Conservation Biology (SCB) was ap- mary focus on the conservation of genetic, species, proved at the end of the meeting (Soulé 1987b). and ecosystem diversity (rather than those ecosys- One of the Society ’ s fi rst acts was to appoint tem components with obvious or direct economic Conser- David Ehrenfeld editor of the new journal value). (Ehrenfeld 2000). vation Biology Conservation biology paid attention to the entire The founding of SCB coincided with planning · biota; to diversity at all levels of biological organiza- for the National Forum on BioDiversity, held tion; to patterns of diversity at various temporal and 24, 1986 in Washington, DC. The – September 21 spatial scales; and to the evolutionary and ecological forum, broadcast via satellite to a national processes that maintain diversity. In particular, and international audience, was organized by emerging insights from ecosystem ecology, distur- the US National Academy of Sciences and bance ecology, and landscape ecology in the 1980s the Smithsonian Institution. Although arranged shifted the perspective of ecologists and conserva- ’ independently of the process that led to SCB s tionists, placing greater emphasis on the dynamic creation, the forum represented a convergence nature of ecosystems and landscapes (e.g. Pickett fi c expertise, and of conservation concern, scienti and White 1985; Forman 1995). interdisciplinary commitment. In planning the Conservation biology was an interdisciplinary, cer with the fi event, Walter Rosen, a program of · systems-oriented, and inclusive response to conser- National Research Council, began using a con- vation dilemmas exacerbated by approaches that biological diversity tracted form of the phrase . The were too narrowly focused, fragmented, and exclu- began its etymological biodiversity abridged form sive (Soulé 1985; Noss and Cooperrider 1994). career. It provided an interdisciplinary home for those in The forum Bio- s proceedings were published as ’ established disciplines who sought new ways to or- diversity (Wilson and Peter 1988). The wide impact fi c information, and who fol- ganize and use scienti of the forum and the book assured that the land- lowed broader ethical imperatives. It also reached scape of conservation science, policy, and action beyond its own core scienti fi c disciplines to incorpo- would never be the same. For some, conservation rate insights from the social sciences and humanities, biology appeared as a new, unproven, and unwel- from the empirical experience of resource managers, come kid on the conservation block. Its adherents, and from diverse cultural sources (Grumbine 1992; however, saw it as the culmination of trends long Knight and Bates 1995). latent within ecology and conservation, and as a Conservation biology acknowledged its status as necessary adaptation to new knowledge and a · an inherently “ ” fi eld. Soulé (1985) as- value-laden gathering crisis. Conservation biology quickly “ ethical norms are a genuine part of serted that gained its footing within academia, zoos and bo- ” Noss (1999) regarded this as conservation biology. t conservation groups, tanical gardens, non-pro fi © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

30 1 CONSERVATION BIOLOGY: PAST AND PRESENT 15 a distinguishing characteristic, noting an “ overarch- funding priorities and encouraged those interest- ing normative assumption in conservation bio- ed in the new fi eld. A steady agenda of confer- logy ... that biodiversity is good and ought to be ences on biodiversity conservation brought ’ Leopold s land ethic and related appeals preserved. ” cials, resource together academics, agency of fi to intergenerational responsibilities and the intrinsic managers, business representatives, international value of non-human life motivated growing numbers aid agencies, and non-governmental organiza- of conservation scientists and environmental ethicists tions. In remarkably rapid order, conservation (Ehrenfeld 1981; Samson and Knopf 1982; Devall and biology gained legitimacy and secured a profes- Sessions 1985; Nash 1989). This explicit recognition sional foothold. ’ of conservation biology s ethical content stood Not, however, without resistance, skepticism, in contrast to the usual avoidance of such considera- eld grew, com- fi and occasional ridicule. As the tions within the sciences historically (McIntosh 1980; plaints came from various quarters. Conservation Barbour 1995; Barry and Oelschlaeger 1996). biology was caricatured as a passing fad, a re- sponse to trendy environmental ideas (and mo- close link- Conservation biology recognized a “ · mentarily available funds). Its detractors regarded between biodiversity conservation and eco- ” age it as too theoretical, amorphous, and eclectic; too nomic development and sought new ways to promiscuously interdisciplinary; too enamored of sustainability became improve that relationship. As fi models; and too technique-de cient and data-poor the catch-all term for development that sought to to have any practical application (Gibbons 1992). blend environmental, social, and economic goals, Conservation biologists in North America were conservation biology provided a new venue at the accused of being indifferent to the conservation intersection of ecology, ethics, and economics (Daly traditions of other nations and regions. Some saw and Cobb 1989). To achieve its goals, conservation old wine “ conservation biology as merely putting biology had to reach beyond the sciences and gener- in a new bottle ” and dismissing the rich experience ate conversations with economists, advocates, poli- of foresters, wildlife managers, and other resource cy-makers, ethicists, educators, the private sector, managers (Teer 1988; Jensen and Krausman 1993). and community-based conservationists. itself was just too broad, or confusing, Biodiversity Conservation biology thus emerged in response or ” “ thorny a term (Udall 1991; Takacs 1996). to both increasing knowledge and expanding Such complaints made headlines within the demands. In harnessing that knowledge and c journals and re fi scienti ected real tensions fl meeting those demands, it offered a new, within resource agencies, academic departments, integrative, and interdisciplinary approach to and conservation organizations. Conservation bi- conservation science. ology had indeed challenged prevalent para- digms, and such responses were to be expected. eld, Ehrenfeld (1992: 1625) fi Defending the new 1.3 Consolidation: conservation biology fi Conservation biology is not de ned by a wrote, “ secures its niche discipline but by its goal — to halt or repair the In June 1987 more than 200 people attended the undeniable, massive damage that is being done to ecosystems, species, and the relationships of hu- rst annual meeting of the Society for Conserva- fi mans to the environment. ... Many specialists in a tion Biology in Bozeman, Montana, USA. The fi nd it dif fi fi host of elds cult, even hypocritical, to rapid growth of the new organization ’ s member- rmly in continue business as usual, blinders fi ship served as an index to the expansion of the place, in a world that is falling apart. ” eld generally. SCB tapped into the burgeoning fi interest in interdisciplinary conservation science Meanwhile, a spate of new and complex con- among younger students, faculty, and conserva- servation issues were drawing increased attention tion practitioners. Universities established new to biodiversity conservation. In North America, the Northern Spotted Owl ( Strix occidentalis caur- courses, seminars, and graduate programs. Scien- ) became the poster creature in deeply ina fi ti c organizations and foundations adjusted their © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

31 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: 16 CONSERVATION BIOLOGY FOR ALL contentious debates over the fate of remaining ush of excitement in establishing fl Amid the old-growth forests and alternative approaches to conservation biology, it was sometimes easy to forest management; the Exxon Valdez oil spill and overlook the challenges inherent in the effort. its aftermath put pollution threats and energy Ehrenfeld (2000) noted that the nascent eld was fi policies on the front page; the anti-environmental, ” Friction was inherent not controversy-rich. “ movement gained in “ Wise Use anti-regulatory ” ’ only in conservation biology s relationship to political power and in fl uence; arguments over related eld itself. Some of fi elds, but within the fi livestock grazing practices and federal rangeland this was simply a result of high energy applied to policies pitted environmentalists against ran- a new endeavor. Often, however, this re fl ected chers; perennial attempts to allow oil develop- deeper tensions in conservation: between sustain- ment within the Arctic National Wildlife Refuge able use and protection; between public and pri- continued; and moratoria were placed on com- vate resources; between the immediate needs of shing of depleted stocks of northern mercial fi people, and obligations to future generations and cod (Alverson et al. 1994; Yaffee 1994; Myers other life forms. Conservation biology would be et al. 2002; Jacobs 2003). et al. 1997; Knight the latest stage on which these long-standing ten- At the international level, attention focused on sions would express themselves. the discovery of the hole in the stratospheric Other tensions re fl ected the special role that ozone layer over Antarctica; the growing scien- conservation biology carved out for itself. c consensus about the threat of global warm- fi ti Conservation biology was largely a product of ing (the Intergovernmental Panel on Climate American institutions and individuals, yet sought fi Change was formed in 1988 and issued its rst to address a problem of global proportions (Meffe assessment report in 1990); the environmental 2002). Effective biodiversity conservation en- legacy of communism in the former Soviet bloc; tailed work at scales from the global to the local, and the environmental impacts of international and on levels from the genetic to the species to the aid and development programs. In 1992, 172 na- community; yet actions at these different scales tions gathered in Rio de Janeiro at the United and levels required different types of informa- Nations Conference on Environment and Devel- tion, skills, and partnerships (Noss 1990). Profes- “ ” ). Among the pro- opment (the Earth Summit sionals in the new fi fi rmly grounded eld had to be ducts of the summit was the Convention on within particular professional specialties, yet con- Biological Diversity. In a few short years, the versant across disciplines (Trombulak 1994; Noss scope of biodiversity conservation, science, and 1997). Success in the of biodiversity con- practice policy had expanded dramatically (e.g. McNeely servation was measured by on-the-ground im- et al. 1990; Lubchenco et al. 1991). science pact, yet the of conservation biology was obliged (as are all sciences) to undertake rigorous To some degree, conservation biology had de- research and to de fi ne uncertainty (Noss 2000). fi ned its own niche by synthesizing scienti fi c dis- eld value-laden “ Conservation biology was a ” fi ciplines, proclaiming its special mission, and adhering to explicit ethical norms, yet sought to gathering together a core group of leading scien- c advance conservation through careful scienti fi tists, students, and conservation practitioners. analysis (Barry and Oelschlager 1996). These ten- fi However, the lling a niche that fi eld was also sions within conservation biology were present at was rapidly opening around it. It provided a birth. They continue to present important meeting ground for those with converging inter- challenges to conservation biologists. They also ests in the conservation of biological diversity. It give the fi eld its creativity and vitality. was not alone in gaining ground for interdisci- plinary conservation research and practice. It joined restoration ecology, landscape ecology, ag- 1.4 Years of growth and evolution roecology, ecological economics, and other new fi elds in seeking solutions across traditional aca- Although conservation biology has been an eld only since the mid-1980s, it is fi organized demic and intellectual boundaries. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

32 1 CONSERVATION BIOLOGY: PAST AND PRESENT 17 possible to identify and summarize at least sever- Even as conservation biologists have honed al salient trends that have shaped it since. tools for designing protected area networks and managing protected areas more effectively (see Chapter 11), they have looked beyond reserve 1.4.1 Implementation and transformation boundary lines to the matrix of surrounding Conservation biologists now work in a much lands (Knight and Landres 1998). Conservation biologists play increasingly important roles in eld than existed at the time of more elaborate fi fi de ning the biodiversity values of aquatic eco- its founding. Much of the early energy and de- — systems, private lands, and agroecosystems. The bate — in conservation biology focused on ques- result is much greater attention to private land tions of the genetics and demographics of small conservation, more research and demonstration populations, population and habitat viability, landscape fragmentation, reserve design, and at the interface of agriculture and biodiversity management of natural areas and endangered conservation, and a growing watershed- and species. These topics remain close to the core of community-based conservation movement. Con- servation biologists are now active across the eld has grown conservation biology, but the fi entire landscape continuum, from wildlands to around them. Conservation biologists now tend agricultural lands and from suburbs to cities, exibly, at varied scales and in to work more fl where conservation planning now meets urban varied ways. In recent years, for example, more design and green infrastructure mapping (e.g. attention has focused on landscape permeability and connectivity, the role of strongly interacting Wang and Moskovits 2001; CNT and Openlands species in top-down ecosystem regulation, and Project 2004). the impacts of global warming on biodiversity (Hudson 1991; Lovejoy and Peters 1994; Soulé 1.4.2 Adoption and integration and Terborgh 1999; Ripple and Beschta 2005; Since the emergence of conservation biology, the 2007; Pringle 2008; see Chapters 5 Pringle et al. conceptual boundaries between it and other and 8). elds have become increasingly porous. Re- fi Innovative techniques and technologies (such fi elds searchers and practitioners from other as computer modeling and geographic informa- s circle, ’ have come into conservation biology tion systems) have obviously played an impor- adopting and applying its core concepts while tant role in the growth of conservation biology. contributing in turn to its further development. The most revolutionary changes, however, have Botanists, ecosystem ecologists, marine biolo- involved the reconceptualizing of science ’ s role in gists, and agricultural scientists (among other conservation. The principles of conservation biol- s groups) were underrepresented in the fi eld ’ ogy have spawned creative applications among early years. The role of the social sciences in con- conservation visionaries, practitioners, planners, servation biology has also expanded within the 1997; Adams 2005). and policy-makers (Noss et al. et al. eld (Mascia fi 2003). Meanwhile, conserva- To safeguard biological diversity, larger-scale tion biology ndings fi s concepts, approaches, and ’ and longer-term thinking and planning had to ” permeation “ elds. This fi ltered into other fi have take hold. It has done so under many rubrics, fl (Noss 1999) is re ected in the number of biodi- including: adaptation of the biosphere reserve versity conservation-related articles appearing in concept (Batisse 1986); the development of gap the general science journals such as and Science 1993); the movement toward et al. analysis (Scott , and in more specialized ecological and Nature ecosystem management and adaptive manage- resource management journals. Since 1986 sever- ment (Grumbine 1994b; Salafsky et al. 2001; al new journals with related content have ap- 2002); ecoregional planning and anal- Meffe et al. peared, including Ecological Applications (1991), ogous efforts at other scales (Redford 2003); et al. (1998), the on-line Journal of Applied Ecology the and the establishment of marine protected areas journal Conservation Ecology (1997) (now called et al. 2001). and networks (Roberts © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

33 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 18 CONSERVATION BIOLOGY FOR ALL Ecology and Society ), Frontiers in Ecology and the Blue Ocean Institute, and the Pew Institute for Environment (2003), and Conservation Letters Ocean Science. (2008). Interest in freshwater conservation biology has uence of conservation biology is even The in fl fi also increased as intensi ed human demands more broadly evident in environmental design, continue to affect water quality, quantity, distri- planning, and decision-making. Conservation bution, and use. Conservationists have come to biologists are now routinely involved in land-use appreciate even more deeply the essential hydro- and urban planning, ecological design, landscape logical connections between groundwater, sur- architecture, and agriculture (e.g. Soulé 1991; Nas- face waters, and atmospheric waters, and the sauer 1997; Babbitt 1999; Jackson and Jackson impact of human land use on the health and 2002; Miller and Hobbs 2002; Imhoff and Carra biological diversity of aquatic ecosystems (Leo- 2003; Orr 2004). Conservation biology has spurred pold 1990; Baron et al. 2002; Glennon 2002; Hunt activity within such emerging areas of interest as and Wilcox 2003; Postel and Richter 2003). Con- conservation psychology (Saunders 2003) and servation biologists have become vital partners conservation medicine (Grifo and Rosenthal in interdisciplinary efforts, often at the water- 1997; Tabor et al. 2001; Aguirre et al. 1997; Pokras shed level, to steward freshwater as both an 2002). Lidicker (1998) noted that et al. conserva- “ essential ecosystem component and a basic tion needs conservation biologists for sure, but it human need. also needs conservation sociologists, conservation political scientists, conservation chemists, conser- 1.4.4 Building capacity vation economists, conservation psychologists, and conservation humanitarians. ” Conservation At the time of its founding, conservation biology biology has helped to meet this need by catalyzing was little known beyond the core group of scien- tists and conservationists who had created it. communication and action among colleagues eld is broadly accepted and well repre- Now the fi across a wide spectrum of disciplines. sented as a distinct body of interdisciplinary knowledge worldwide. Several textbooks ap- peared soon after conservation biology gained 1.4.3 Marine and freshwater conservation its footing (Primack 1993; Meffe and Carroll biology 1994; Hunter 1996). These are now into their sec- has been s Conservation biology ’ “ permeation ” ond and third editions. Additional textbooks especially notable with regard to aquatic ecosys- have been published in more specialized subject tems and marine environments. In response to areas, including insect conservation biology maximum sus- long-standing concerns over “ (Samways 1994), conservation of plant biodiver- tained yield sheries management, protection fi ” et al. 1995), forest biodiversity sity (Frankel of marine mammals, depletion of salmon stocks, (Hunter and Seymour 1999), conservation genet- degradation of coral reef systems, and other is- 2002), marine conservation ics (Frankham et al. sues, marine conservation biology has emerged biology (Norse and Crowder 2005), and tropical as a distinct focus area (Norse 1993; Boersma 2007). conservation biology (Sodhi et al. na 1998; fi 1996; Bohnsack and Ault 1996; Sa Academic training programs in conservation Thorne-Miller 1998; Norse and Crowder 2005). biology have expanded and now exist around the The application of conservation biology in marine et al. 1995; Rodrí- world (Jacobson 1990; Jacobson environments has been pursued by a number of guez 2005). The interdisciplinary skills of et al. non-governmental organizations, including conservation biologists have found acceptance ’ SCB s Marine Section, the Ocean Conservancy, within universities, agencies, non-governmental the Marine Conservation Biology Institute, the organizations, and the private sector. Funders Center for Marine Biodiversity and Conservation s ’ have likewise helped build conservation biology at the Scripps Institution of Oceanography, the capacity through support for students, academic © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

34 1 19 CONSERVATION BIOLOGY: PAST AND PRESENT c roots of biodiversity conservation are scienti fi programs, and basic research and eld projects. fi obviously not limited to one nation or continent Despite such growth, most conservation biologists (see Box 1.2). Although the international conser- would likely agree that the capacity does not near- vation movement dates back more than a centu- ly meet the need, given the urgent problems in ry, the history of the science from an international biodiversity conservation. Even the existing sup- perspective has been inadequately studied (Blan- port is highly vulnerable to budget cutbacks, din 2004). This has occasionally led to healthy changing priorities, and political pressures. debate over the origins and development of con- servation biology. Such debates, however, have 1.4.5 Internationalization not hindered the trend toward greater interna- Conservation biology has greatly expanded its tional collaboration and representation within international reach (Meffe 2002; Meffe 2003). The eld (e.g. Medellín 1998). fi the Box 1.2 Conservation in the Philippines Mary Rose C. Posa a burgeoning human population. The Conservation biology has been referred to as a Philippines has thus been pegged as a top “ ” (Wilson 2000). As discipline with a deadline hotspot ” for terrestrial and conservation “ the rapid loss and degradation of ecosystems marine ecosystems, and there are fears that it accelerates across the globe, some scientists could be the site of the fi rst major extinction — in effect, writing suggest a strategy of triage spasm (Heaney and Mittermeier 1997; Myers off countries that are beyond help (Terborgh et al. 2000; Roberts et al. 2002). Remarkably, 1999). But are there any truly lost causes in and despite this precarious situation, there is conservation? evidence that hope exists for biodiversity biodiversity ‐ The Philippines is a mega conservation in the Philippines. country with exceptionally high levels of Indication of the growing valuation of endemism (~50% of terrestrial vertebrates and biodiversity, sustainable development and 60% of vascular plants; Heaney and – 45 environmental protection can be seen in Mittermeier 1997). However, centuries of different sectors of Philippine society. Stirrings exploitation and negligence have pushed its of grassroots environmental consciousness ecosystems to their limit, reducing primary began in the 1970s, when marginalized forest cover [less than 3% remaining; FAO communities actively opposed unsustainable (Food and Agriculture Organization of the commercial developments, blocking logging United Nations) 2005], decimating mangroves trucks, and protesting the construction of large (>90% lost; Primavera 2000), and severely dams (Broad and Cavanagh 1993). After the 100% – damaging coral reefs (~5% retaining 75 1986 overthrow of dictator Ferdinand Marcos, live cover; Gomez 1994), leading to a high et al. a revived democracy fostered the emergence of number of species at risk of extinction [~21% of civil society groups focused on environmental vertebrates assessed; IUCN (International Union issues. The devolution of authority over natural for Conservation of Nature and Natural resources from central to local governments Resources) 2006]. Environmental degradation also empowered communities to create and has also brought the loss of soil fertility, enforce regulations on the use of local pollution, and diminished sheries fi resources. There are now laudable examples productivity, affecting the livelihood of millions ‐ where efforts by communities and non of rural inhabitants. Efforts to preserve governmental organizations (NGOs) have biodiversity and implement sound made direct impacts on conserving endangered environmental policies are hampered by 2008). et al. species and habitats (Posa entrenched corruption, weak governance and Driven in part by public advocacy, there has opposition by small but powerful interest also been considerable progress in groups. In addition, remaining natural environmental legislation. In particular, the resources are under tremendous pressure from continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

35 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 20 CONSERVATION BIOLOGY FOR ALL Box 1.2 (Continued) complacency, that positive progress has been National Integrated Protected Areas System Act a conservation worst “ — made in the Philippines provides for stakeholder involvement in ”— suggests that there are case scenario protected area management, which has been a grounds for optimism for biodiversity key element of success for various reserves. conservation in tropical countries worldwide. ‐ Perhaps the best examples of where people centered resource use and conservation have come together are marine protected areas REFERENCES (MPAs) managed by coastal communities across the country — a survey of 156 MPAs reported Alcala, A. C. and Russ, G. R. (2006). No ‐ take marine that 44.2% had good to excellent management sheries management in the Philip- reserves and reef fi (Alcala and Russ 2006). pines: a new people power revolution. Ambio 35 , , Last, but not least, there has been renewed 254. – 245 interest in biodiversity research in academia, Broad, R. and Cavanagh, J. (1993). Plundering paradise: increasing the amount and quality of the struggle for the environment in the Philippines . biodiversity information (see Box 1.2 Figure). University of California Press, Berkeley, CA. Labors of eld researchers result in hundreds of fi Dutson,G. C. L., Magsalay,P. M., and Timmins, R. J. (1993). additional species yet to be described, and The rediscovery of the Cebu Flowerpecker Dicaeum some rediscoveries of species thought to be quadricolor , with notes on other forest birds on Cebu, owerpecker extinct (e.g. Cebu fl Dicaeum Philippines. 243. – , 235 3 , Bird Conservation International ; Dutson 1993). There are et al. quadricolor FAO (Food and Agriculture Organization of the United increasing synergies and networks among Nations) (2005). Global forest resources assessment conservation workers, politicians, community . Forestry 2005, Country report 202: Philippines leaders, park rangers, researchers, local people, Department, FAO, Rome, Italy. and international NGOs, as seen from the Gomez, E. D., Aliño, P. M., Yap, H. T., Licuanan, W. Y. growth of the Wildlife Conservation Society of (1994). A review of the status of Philippine reefs. Marine the Philippines, which has a diverse ,62 68. – 29 , Pollution Bulletin membership from all these sectors. Heaney, L. and Mittermeier, R. A. (1997). The Philippines. 140 In R. A. Mittermeier, G. P. Robles, and C. G. Mittermeier, eds Megadiversity: earth s biologically wealthiest ’ 120 – 255. CEMEX, Monterrey, Mexico. , pp. 236 nations 100 IUCN (International Union for Conservation of Nature and Natural Resources) (2006). 2006 IUCN Red List of 80 threatened species . www.iucnredlist.org. 60 Myers, N.,Mittermeier,R.A.,Mittermeier,C.G.,daFonseca, G. A. B., and Kent, J. (2000). Biodiversity hotspots for 40 858. – ,853 403 , Nature conservation priorities. 20 Posa, M. R. C., Diesmos, A. C., Sodhi, N. S., and Brooks, Number of publications 0 T. M. (2008). Hope for threatened biodiversity: lessons , 231 58 240. – from the Philippines. BioScience , 1985 1995 2000 2005 1990 1980 Primavera, J. H. (2000). Development and conservation of Year Philippine mangroves: Institutional issues. Ecological 106. , Economics – 35 ,91 Box 1.2 Figure Steady increase in the number of publications on Roberts, C. M., McClean, C. J., Veron, J. E. N., et al. (2002). Philippine biodiversity and conservation, obtained from searching – three ISI Web of Knowledge databases for the period 1980 2007. Marine biodiversity hotspots and conservation priorities for tropical reefs. 295 , 1280 – 1284. , Science Terborgh, J. (1999). Requiem for nature . Island Press, While many daunting challenges remain Washington, DC. especially in the area of conservation of Wilson, E. O. (2000). On the future of conservation biology. populations (Chapter 10) and ecosystems – 3. Conservation Biology , 14 ,1 services (Chapter 3), and there is no room for © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

36 1 CONSERVATION BIOLOGY: PAST AND PRESENT 21 This growth is re fl ected in the expanding institu- 1.5 Conservation biology: a work tional and membership base of the Society for in progress Conservation Biology. The need to reach across These trends (and no doubt others) raise impor- national boundaries was recognized by the foun- tant questions for the future. Conservation biolo- Conservation ders of the SCB. From its initial issue gy has grown quickly in a few brief decades, yet Biology included Spanish translations of article ab- most conservation biologists would assert that ed its editorial fi stracts. The Society has diversi s sake is hardly justi ’ growth for growth ed. As fi board, recognized the accomplishments of leading disciplines and organizations become more conservation biologists from around the world, structured, they are liable to equate mere expan- and regularly convened its meetings outside the sion with progress in meeting their missions (Eh- cant move toward greater interna- fi USA. A signi renfeld 2000). Can conservation biology sustain tional participation in the SCB came when, in 2000, its own creativity, freshness, and vision? In its the SCB began to develop its regional sections. collective research agenda, is the fi eld asking, and answering, the appropriate questions? Is it performing its core function — providing reliable 1.4.6 Seeking a policy voice c information on biological and useful scienti fi in the most effec- — diversity and its conservation Conservation biology has long sought to de ne fi tive manner possible? Is that information making an appropriate and effective role for itself in shap- ” “ need to be constituencies a difference? What ing public policy (Grumbine 1994a). Most who more fully involved and engaged? call themselves conservation biologists feel obli- While continuing to ponder such questions, con- gated to be advocates for biodiversity (Oden- servation biologists cannot claim to have turned baugh 2003). How that obligation ought to be s diversity. Yet the ’ eld fi back the threats to life lled has been a source of continuing debate fi ful has contributed essential knowledge at a time fi within the eld. Some scientists are wary of play- when those threats have continued to mount. It ing an active advocacy or policy role, lest their has focused attention on the full spectrum of objectivity be called into question. Conversely, biological diversity, on the ecological processes biodiversity advocates have responded to the ef- that maintain it, on the ways we value it, and on fect that “ if you don ’ t use your science to shape steps that can be taken to conserve it. It has brought ” policy, we will. c knowledge, long-range perspectives, and fi scienti s inherent mix of science Conservation biology ’ a conservation ethic into the public and profession- and ethics all but invited such debate. Far from c al arenas in new ways. It has organized scienti fi Conservation Biology avoiding controversy, ’ s information to inform decisions affecting biodiver- founding editor David Ehrenfeld built dialogue sity at all levels and scales. In so doing, it has on conservation issues and policy into the journal helped to reframe fundamentally the relationship has regularly at the outset. Conservation Biology between conservation philosophy, science, and published letters and editorials on the question of practice. values, advocacy, and the role of science in shaping policy. Conservation biologists have not achieved fi nal resolution on the matter. Perhaps in the end it is irresolvable, a matter of personal judgment in- Summary volving a mixture of scienti fi ccon fi dence levels, Conservation biology emerged in the mid-1980s uncertainty, and individual conscience and re- · as a new fi eld focused on understanding, protecting, is the key word, as ” “ sponsibility. Responsibility and perpetuating biological diversity at all scales all parties to the debate seem to agree that advoca- and all levels of biological organization. cy, to be responsible, must rest on a foundation of Conservation biology has deep roots in the solid science and must be undertaken with honesty · growth of biology over several centuries, but its and integrity (Noss 1999). © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

37 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 22 CONSERVATION BIOLOGY FOR ALL Alverson, W. S., Kuhlman, W., and Waller, D. M. (1994). fl emergence re ects more recent developments in an Wild forests: conservation biology and public policy . Island array of biological sciences (ecology, genetics, evo- Press, Washington, DC. lutionary biology, etc.) and natural resource man- s mandate and the birth of urban Babbitt, B. (1999). Noah ’ elds (forestry, wildlife and sheries fi fi agement , 677 678. Conservation Biology – 13 , bioplanning. management, etc.). Barbour, M. G. (1995). Ecological fragmentation in Conservation biology was conceived as a “ mis- Uncommon ground: toward the Fifties. In W. Cronon, ed. · fi sion-oriented ” eld based in the biological sciences, – reinventing nature , pp. 233 255. W. W. Norton, New York. but with an explicit interdisciplinary approach that Baron, J. S., Poff, N. L., Angermeier, P. L., (2002). et al. incorporated insights from the social sciences, hu- Meeting ecological and societal needs for freshwater. manities, and ethics. , 1247 12 , 1260. – Ecological Applications Barry, D. and Oelschlaeger, M. (1996). A science for surviv- Since its founding, conservation biology has · al: values and conservation biology. , Conservation Biology greatly elaborated its research agenda; built stronger 911. – , 905 10 fi elds and disciplines; ex- connections with other Batisse, M. (1986). Developing and focusing the Biosphere tended its reach especially into aquatic and marine Nature and Resources , 22 Reserve concept. – 11. ,2 environments; developed its professional capacity A green and Beeman, R. S. and Pritchard, J. A. (2001). for training, research, and eld application; become fi permanent land: ecology and agriculture in the twentieth an increasingly international fi eld; and become in- . University Press of Kansas, Lawrence, Kansas. century creasingly active at the interface of conservation sci- Blandin, P. (2004). Biodiversity, between science and ethics. ence and policy. In S. H. Shakir, and W. Z. A. Mikhail, eds Soil zoology for sustainable development in the 21st Century 49. – , pp. 17 Eigenverlag, Cairo, Egypt. Boersma, P. D. (1996). Maine conservation: protecting the Suggested reading exploited commons. Society for Conservation Biology Farnham, T. J. (2007). s Legacy: Origins of ’ Saving Nature , 6. – ,1 3 Newsletter · . Yale University Press, the Idea of Biological Diversity Boersma, P. D., Kareiva, P., Fagan, W. F., Clark, J. A., and New Haven. Hoekstra, J. M. (2001). How good are endangered The Song of the Dodo: Island Bioge- Quammen, D. (1996). 650. – , 643 51 BioScience species recovery plans? , · . Simon and Schuster, ography in an Age of Extinctions Bohnsack, J. and Ault, J. (1996). Management strategies to New York. – ,73 9 , Oceanography conserve marine biodiversity. 81. Correction Lines: Essays on Land, Meine, C. (2004). Brussard, P. (1985). The current status of conservation biolo- · Leopold, and Conservation . Island Press, Washington, DC. – ,9 11. gy. Bulletin of the Ecological Society of America , 66 Minteer, B. A. and Manning, R. E. (2003). Reconstructing Conser- Callicott, J. B. (1990). Whither conservation ethics? · Conservation: Finding Common Ground . Island Press, 20. , – vation Biology ,15 4 Washington, DC. Caughley, G. and Gunn, A. (1986). Conservation biology in theory and practice . Blackwell Science, Cambridge, Massachusetts. CNT (Center For Neighborhood Technologies) and Open- Relevant website Natural connections: green infrastruc- lands Project (2004). ture in Wisconsin, Illinois, and Indiana . (Online) Available Society for Conservation Biology: http://www.conbio. · at http://www.greenmapping.org. (Accessed February org/ 2006). CEQ (Council On Environmental Quality) (1980). Environ- 1980: the eleventh annual report of the CEQ . mental quality — fi ce, Washington, DC. US Government Printing Of REFERENCES Croker, R. A. (1991). Pioneer ecologist: the life and work of Adams, J. S. (2005). The future of the wild: radical conservation . Smithsonian Institution Press, Victor Ernest Shelford . Beacon Press, Boston, Massachusetts. for a crowded world Washington, DC. Aguirre, A. A., Ostfeld, R. S., Tabor, G. M., House, C., and Crosby, A. W. (1986). Ecological imperialism: the biological Pearl, M. C. (2002). Conservation medicine: ecological health . Cambridge University expansion of Europe, 900 – 1900 . Oxford University Press, New York. in practice Press, New York. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

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40 1 25 CONSERVATION BIOLOGY: PAST AND PRESENT Ripple, W. J. and Beschta, R. L. (2005). Linking wolves and Noss, R. F. (1990). Indicators for monitoring biodiversity: a 55 plants: Aldo Leopold on trophic cascades. , , BioScience – , 4 364. Conservation Biology , 355 hierarchical approach. 621. – 613 Noss, R. F. (1997). The failure of universities to produce Roberts, C. M., Halpern, B., Palumbi, S. R., and Warner, R. , Conservation Biology conservation biologists. , 11 R. (2001). Designing marine reserve networks: why 1269. 1267 – small, isolated protected areas are not enough. Conserva- Noss, R. F. (1999). Is there a special conservation biology? 17. – ,10 2 , tion Biology in Practice , 113 – 122. Ecography , 22 Rodríguez, J. P., Simonetti, J. A., Premoli, A., and Marini, Noss, R. F. (2000). Science on the bridge. Conservation Biol- M. Â. (2005). Conservation in Austral and Neotropical ogy , 14 , 333 – 335. America: building scienti fi c capacity equal to the chal- s ’ Noss, R. 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M. (2008). Elephants as agents of habitat creation Soulé, M. E. (1980). Thresholds for survival: criteria for – for small vertebrates at patch scale. Ecology , 89 ,26 33. maintenance of tness and evolutionary potential. In fi Pringle, R. M., Young, T. P., Rubenstein, D. I., and Mccauly, Conservation biology: M. E. Soulé, and B. A. Wilcox, eds D. J. (2007). Herbivore-initiated interaction cascades and , pp. 151 – 170. Sinauer an evolutionary-ecological perspective their modulation by primary productivity in an African Associates, Sunderland, Massachusetts. savanna. Proceedings of the National Academy of Sciences of BioSci- Soulé, M. E. (1985). What is conservation biology? , 193 the United States of America 104 – 197. , 734. – , 727 35 , ence Quammen, D. (1996). The song of the dodo: island biogeogra- Conservation biology: the science of Soulé, M. E., ed. (1986). . Simon and Schuster, New phy in an age of extinctions . Sinauer Associates, Sunderland, scarcity and diversity York. 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41 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: 26 CONSERVATION BIOLOGY FOR ALL Thorne-Miller, B. (1998). The Living Ocean: Understanding Soulé, M. E. (1987b). History of the Society for Conserva- , 2nd ed. Island Press, and Protecting Marine Biodiversity tion Biology: how and why we got here. Conservation Washington, DC. Biology 1 ,4 – , 5. Trombulak, S. C. (1994). Undergraduate education and the Soulé, M. E. (1991). Land use planning and wildlife main- next generation of conservation biologists. Conservation tenance: guidelines for preserving wildlife in an urban 591. – , 589 , Biology 8 , landscape. Journal of the American Planning Association , Sierra 89. Udall, J. R. (1991). Launching the natural ark. – ,80 7 – 57 323. , 313 Wallace, A. R. (1863). On the physical geography of the Soulé, M. E. and Terborgh, J., eds (1999). Continental conser- Journal of the Royal Geographical Malay Archipelago. vation: scienti c foundations of regional reserve networks . fi , 217 33 Society of London , 234. – Washington, DC., Island Press. Wang, Y. and Moskovits, D. K. (2001). Tracking fragmen- Soulé, M. E. and Wilcox, B. A., eds (1980). Conservation tation of natural communities and changes in land cover: biology: an evolutionary-ecological perspective . Sinauer, applications of Landsat data for conservation in an Sunderland, Massachusetts. urban landscape (Chicago Wilderness). Tabor, G. M., Ostfeld, R. S., Poss, M., Dobson, A. P., and Conservation Aguirre, A. A. (2001). Conservation biology and the , 835 – 843. , Biology 15 health sciences. In M. E. Soulé and G. H. Orians, eds . Biodiversity Wilson, E. O. and Peter, F. M., eds (1988). , Conservation biology: research priorities for the next decade National Academy Press, Washington, DC. – 173. Island Press, Washington, DC. pp. 155 WCED (World Commission On Environment and Devel- Takacs, D. (1996). The idea of biodiversity: philosophies of . Oxford University opment) (1987). Our common future paradise . Johns Hopkins University Press, Baltimore, Press, Oxford, UK. Maryland. Dust bowl: the southern plains in the Worster, D. (1979). Teer, J. G. (1988). Review of Conservation biology: the . Oxford University Press, New York. 1930s Journal of Wildlife Man- science of scarcity and diversity. s economy: a history of ecological ’ Nature Worster, D. (1985). , 570 agement , – 572. 52 ideas . Cambridge University Press, Cambridge, UK. Terborgh, J. (1974). Preservation of natural diversity: Yaffee, S. L. (1994). The wisdom of the spotted owl: policy BioScience the problem of extinction prone species. , 24 , lessons for a new century . Island Press, Washington, 722. – 715 DC. Thomas, W. L. Jr., Sauer, C. O., Bates, M., and Mumford, L. Ziswiler, V. (1967). Extinct and vanishing animals: a biolo- . Univer- Man (1956). s role in changing the face of the Earth ’ gy of extinction and survival . Springer-Verlag, New sity of Chicago Press, Chicago, Illinois. York. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

42 1 CHAPTER 2 Biodiversity Kevin J. Gaston Biological diversity or biodiversity (the latter term The scale of the variety of life is dif fi cult, and the variety of is simply a contraction of the former) is perhaps impossible, for any of us truly to visua- life , in all of its many manifestations. It is a broad rst attempt fi lize or comprehend. In this chapter I unifying concept, encompassing all forms, levels to give some sense of the magnitude of biodiver- and combinations of natural variation, at all levels sity by distinguishing between different key ele- of biological organization (Gaston and Spicer ments and what is known about their variation. nition 2004). A rather longer and more formal de fi Second, I consider how the variety of life has is given in the international Convention on changed through time, and third and fi nally Biological Diversity (CBD; the de fi nition is how it varies in space. In short, the chapter will, provided in Article 2), which states that inevitably in highly summarized form, address “‘ Biological diversity ’ means the variability the three key issues of how much biodiversity among living organisms from all sources includ- there is, how it arose, and where it can be found. , terrestrial, marine and other aquatic ing, inter alia ecosystems and the ecological complexes of which 2.1 How much biodiversity is there? they are part; this includes diversity within species, ” between species and of ecosystems .Whichever Some understanding of what the variety of life fi de nition is preferred, one can, for example, comprises can be obtained by distinguishing be- speak equally of the biodiversity of some given tween different key elements. These are the basic area or volume (be it large or small) of the land or building blocks of biodiversity. For convenience, sea, of the biodiversity of a continent or an ocean they can be divided into three groups: genetic basin, or of the biodiversity of the entire Earth. diversity, organismal diversity, and ecological Likewise, one can speak of biodiversity at present, diversity (Table 2.1). Within each, the elements at a given time or period in the past or in the future, are organized in nested hierarchies, with those or over the entire history of life on Earth. higher order elements comprising lower order Elements of biodiversity (focusing on those levels that are most commonly used). Modi fi ed from Heywood and Baste Table 2.1 (1995). Ecological diversity Organismal diversity Biogeographic realms Domains or Kingdoms Phyla Biomes Families Provinces Genera Ecoregions Ecosystems Species Habitats Genetic diversity Subspecies Populations Populations Populations Individuals Individuals Chromosomes Genes Nucleotides 27 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

43 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 28 ones. The three groups are intimately linked and eggs (diploid) develop into females and unfertil- share some elements in common. ized eggs (haploid) become males, hence the lat- ter have the minimal achievable single chromosome in their cells (Gould 1991). Humans 2.1.1 Genetic diversity have 46 chromosomes (22 pairs of autosomes, and one pair of sex chromosomes). Genetic diversity encompasses the components of Within a species, genetic diversity is commonly the genetic coding that structures organisms (nu- cleotides, genes, chromosomes) and variation in measured in terms of allelic diversity (average the genetic make-up between individuals within a number of alleles per locus), gene diversity (het- population and between populations. This is the erozygosity across loci), or nucleotide differences. Large populations tend to have more genetic di- raw material on which evolutionary processes act. versity than small ones, more stable populations Perhaps themostbasic measure of genetic diversity uctuate, and popu- fl more than those that wildly — is genome size the amount of DNA (Deoxyribo- ’ lations at the center of a species geographic range chromosomes ’ nucleicacid) inone copy ofa species often have more genetic diversity than those at (also called the C-value). This can vary enormous- ly, with published eukaryote genome sizes ranging the periphery. Such variation can have a variety between 0.0023 pg (picograms) in the parasitic mi- fl uences, including on pro- of population-level in crosporidium and 1400 Encephalitozoon intestinalis tness components, behav- ductivity/biomass, fi ior, and responses to disturbance, as well as pg in the free-living amoeba Chaos chaos (Gregory uences on species diversity and ecosystem fl in 2008). These translate into estimates of 2.2 million 2008). et al. processes (Hughes and 1369 billion base pairs (the nucleotides on op- posing DNA strands), respectively. Thus, even at this level the scale of biodiversity is daunting. Cell 2.1.2 Organismal diversity size tends to increase with genome size. Humans Organismal diversity encompasses the full taxo- have a genome size of 3.5 pg (3.4 billion base pairs). nomic hierarchy and its components, from indi- Much of genome size comprises non-coding viduals upwards to populations, subspecies and DNA, and there is usually no correlation between species, genera, families, phyla, and beyond to genome size and the number of genes coded. The kingdoms and domains. Measures of organismal genomes of more than 180 species have been diversity thus include some of the most familiar completely sequenced and it is estimated that, for expressions of biodiversity, such as the numbers example, there are around 1750 genes for the bacte- of species (i.e. species richness). Others should be fl ria Haemophilus in uenzae and 3200 for Escherichia better studied and more routinely employed than ,19000 Saccharomycescerevisiae ,6000fortheyeast coli they have been thus far. for the nematode Caenorhabditis elegans , 13 500 for Starting at the lowest level of organismal diver- y fl 25 000 for the fruit  ,and Drosophila melanogaster sity, little is known about how many individual Arabidopsis thaliana ,themouse Mus muscu- the plant organisms there are at any one time, although this , brown rat Rattus norvegicus lus and human Homo is arguably an important measure of the quantity . There is strong conservatism of some genes sapiens and variety of life (given that, even if sometimes acrossmuchofthediversityoflife.Thedifferencesin only in small ways, most individuals differ from geneticcomposition of species give us indications of one another). Nonetheless, the numbers must be theirrelatedness,andthusimportantinformationas extraordinary. The global number of prokaryotes to how the history and variety of life developed. 30 cells — many 6x10 has been estimated to be 4 – Genes are packaged into chromosomes. The million times more than there are stars in the number of chromosomes per somatic cell thus with a produc- visible universe (Copley 2002) — far observed varies between 2 for the jumper ant 30 cells per annum (Whitman et tion rate of 1.7 x 10 and 1260 for the adders-tongue Myrmecia pilosula al. 1998). The numbers of protists is estimated at . The ant species re- fern Ophioglossum reticulatum 2 7 4 individuals per m (Finlay 2004). 10  10 produces by haplodiploidy, in which fertilized © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

44 1 BIODIVERSITY 29 Impoverished habitats have been estimated to plying standard species concepts, in culturing the 5 2 , and individual nematodes per m have 10 vast majority of these organisms and thereby ap- 2 7 6  per m , possi- 10 more productive habitats 10 fi cation techniques, and by plying classical identi 19 8 2 has ;10 per m bly with an upper limit of 10 the vast numbers of individuals. Indeed, depend- been suggested as a conservative estimate of the ing on the approach taken, the numbers of pro- global number of individuals of free-living nema- karyotic species estimated to occur even in very todes (Lambshead 2004). By contrast, it has small areas can vary by a few orders of magni- been estimated that globally there may be less than et al. tude (Curtis 2002; Ward 2002). The rate of 11 breeding birds at any one time, fewer than 17 10 reassociation of denatured (i.e. single stranded) 2003). et al. for every person on the planet (Gaston DNA has revealed that in pristine soils and sedi- Individual organisms can be grouped into rela- ments with high organic content samples of 30 to 3 correspond to c. 3000 to 11 000 different tively independent populations of a species on the 100 cm 4 different prokary- genomes, and may contain 10 fl ow and some level of genet- basis of limited gene otic species of equivalent abundances (Torsvik ic differentiation (as well as on ecological criteria). et al. 2002). Samples from the intestinal microbial The population is a particularly important ele- ora of just three adult humans contained repre- fl ment of biodiversity. First, it provides an impor- sentatives of 395 bacterial operational taxonomic tant link between the different groups of elements units (groups without formal designation of tax- of biodiversity (Table 2.1). Second, it is the scale at onomic rank, but thought here to be roughly which it is perhaps most sensible to consider lin- equivalent to species), of which 244 were previ- kages between biodiversity and the provision of ously unknown, and 80% were from species that — ecosystem services (supporting services e.g. nu- have not been cultured (Eckburg et al. 2005). Like- trient cycling, soil formation, primary production; wise, samples from leaves were estimated to har- provisioning services — e.g. food, freshwater, bor at least 95 to 671 bacterial species from each of e.g. timber and fi ber, fuel; regulating services — nine tropical tree species, with only 0.5% com- climate regulation, fl ood regulation, disease regu- mon to all the tree species, and almost all of the lation, water puri fi e.g. cation; cultural services — bacterial species being undescribed (Lambais aesthetic, spiritual, educational, recreational; et al. 2006). On the basis of such fi ndings, global MEA 2005). Estimates of the density of such po- prokaryote diversity has been argued to comprise pulations and the average geographic range sizes possibly millions of species, and some have sug- of species suggest a total of about 220 distinct gested it may be many orders of magnitude more et al. populations per eukaryote species (Hughes than that (Fuhrman and Campbell 1998; Dykhui- 1997). Multiplying this by a range of estimates of et al. zen 1998; Torsvik 2004). et al. 2002; Venter the extant numbers of species, gives a global total 9 populations (Hughes et al. 1997), Although much more certainty surrounds es- of 1.1 to 6.6 x 10 one or fewer for every person on the planet. The timates of the numbers of eukaryotic than pro- gure is essentially unknown, fi accuracy of this karyotic species, this is true only in a relative and with major uncertainties at each step of the calcu- not an absolute sense. Numbers of eukaryotic lation, but the ease with which populations can be species are still poorly understood. A wide vari- eradicated (e.g. through habitat destruction) sug- ety of approaches have been employed to esti- gests that the total is being eroded at a rapid rate. mate the global numbers in large taxonomic People have long pondered one of the impor- groups and, by summation of these estimates, tant contributors to the calculation of the total how many extant species there are overall. number of populations, namely how many differ- These approaches include extrapolations based ent species of organisms there might be. Greatest on counting species, canvassing taxonomic ex- uncertainty continues to surround the richness of perts, temporal patterns of species description, prokaryotes, and in consequence they are often proportions of undescribed species in samples, ignored in global totals of species numbers. This well-studied areas, well-studied groups, species- culties in ap- fi is in part variously because of dif abundance distributions, species-body size © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

45 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 30 CONSERVATION BIOLOGY FOR ALL distributions, and trophic relations (Gaston fi ed, complete and maintained database single uni 2008). One recent summary for eukaryotes of valid formal names. However, probably about gives lower and upper estimates of 3.5 and 108 2 million extant species are regarded as being million species, respectively, and a working fi g- known to science (MEA 2005). Importantly, this ure of around 8 million species (Table 2.2). Based total hides two kinds of error. First, there are on current information the two extremes seem instances in which the same species is known fi rather unlikely, but the working gure at least under more than one name (synonymy). This is seems tenable. However, major uncertainties more frequent amongst widespread species, surround global numbers of eukaryotic species which may show marked geographic variation in particular environments which have been in morphology, and may be described anew re- poorly sampled (e.g. deep sea, soils, tropical peatedly in different regions. Second, one name forest canopies), in higher taxa which are ex- may actually encompass multiple species (hom- tremely species rich or with species which are onymy). This typically occurs because these spe- very dif fi cult to discriminate (e.g. nematodes, cies are very closely related, and look very similar arthropods), and in particular functional groups (cryptic species), and molecular analyses may be which are less readily studied (e.g. parasites). A fi rm their differences. required to recognize or con widearrayoftechniquesisnowbeingemployed Levels of as yet unresolved synonymy are un- to gain access to some of the environments that doubtedly high in many taxonomic groups. In- have been less well explored, including rope deed, the actual levels have proven to be a key climbing techniques, aerial walkways, cranes issue in, for example, attempts to estimate the and balloons for tropical forest canopies, and global species richness of plants, with the highly remotely operated vehicles, bottom landers, sub- variable synonymy rate amongst the few groups marines, sonar, and video for the deep ocean. that have been well studied in this regard making Molecular and better imaging techniques are dif fi cult the assessment of the overall level of also improving species discrimination. Perhaps synonymy across all the known species. Equally, cantly, however, it seems highly most signi fi however, it is apparent that cryptic species probable that the majority of species are para- abound, with, for example, one species of neo- sites, and yet few people tend to think about tropical skipper butter fl y recently having been biodiversity from this viewpoint. shown actually to be a complex of ten species How many of the total numbers of species have (Hebert et al. 2004). been taxonomically described remains surpris- New species are being described at a rate ingly uncertain, in the continued absence of a of about 13 000 per annum (Hawksworth and Estimates (in thousands), by different taxonomic groups, of the overall global numbers of extant eukaryote Table 2.2 fi species. Modi Arroyo (1995) and May (2000). ‐ ed from Hawksworth and Kalin Overall species fi gure Working Accuracy of working Low gure fi High very poor ‘ Protozoa ’ 200 60 100 300 very poor ‘ ’ 1000 150 Algae Plants good 320 300 500 Fungi 2700 200 1500 moderate very poor 500 100 1000 Nematodes 4650 moderate Arthropods 101 200 2375 moderate 120 100 200 Molluscs Chordates 50 50 good 55 Others 800 200 250 moderate very poor 7790 3535 107 655 Totals © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

46 1 BIODIVERSITY 31 Kalin-Arroyo 1995), or about 36 species on the tems, ecoregions, provinces, and on up to biomes average day. Given even the lower estimates of and biogeographic realms (Table 2.1). This is an overall species numbers this means that there is important dimension to biodiversity not readily little immediate prospect of greatly reducing the captured by genetic or organismal diversity, and numbers that remain unknown to science. This is in many ways is that which is most immediately particularly problematic because the described apparent to us, giving the structure of the natural species are a highly biased sample of the extant and semi-natural world in which we live. How- biota rather than the random one that might en- ever, ecological diversity is arguably also the least able more ready extrapolation of its properties to satisfactory of the groups of elements of biodiver- all extant species. On average, described species sity. There are two reasons. First, whilst these tend to be larger bodied, more abundant and elements clearly constitute useful ways of break- more widespread, and disproportionately from ing up continua of phenomena, they are dif cult fi temperate regions. Nonetheless, new species con- to distinguish without recourse to what ultimate- tinue to be discovered in even otherwise relative- ly constitute some essentially arbitrary rules. For ly well-known taxonomic groups. New extant example, whilst it is helpful to be able to label fi sh species are described at the rate of about different habitat types, it is not always obvious 130 – 160 each year (Berra 1997), amphibian spe- precisely where one should end and another cies at about 95 each year (from data in Frost begin, because no such beginnings and endings 2004), bird species at about 6 – 7 each year (Van really exist. In consequence, numerous schemes Rootselaar 1999, 2002), and terrestrial mammals have been developed for distinguishing between 30 each year (Ceballos and Ehrlich 2009). – at 25 many elements of ecological diversity, often with Recently discovered mammals include marsu- wide variation in the numbers of entities recog- pials, whales and dolphins, a sloth, an elephant, nized for a given element. Second, some of the primates, rodents, bats and ungulates. elements of ecological diversity clearly have both Given the high proportion of species that have abiotic and biotic components (e.g. ecosystems, yet to be discovered, it seems highly likely that ecoregions, biomes), and yet biodiversity is de- there are entire major taxonomic groups of organ- . fi ned as the variety of life isms still to be found. That is, new examples of Much recent interest has focused particularly higher level elements of organismal diversity. on delineating ecoregions and biomes, principal- This is supported by recent discoveries of possi- ly for the purposes of spatial conservation ble new phyla (e.g. Nanoarchaeota), new orders planning (see Chapter 11), and there has thus (e.g. Mantophasmatodea), new families (e.g. As- been a growing sense of standardization of the pidytidae) and new subfamilies (e.g. Martiali- schemes used. Ecoregions are large areal units nae). Discoveries at the highest taxonomic levels containing geographically distinct species as- have particularly served to highlight the much semblages and experiencing geographically dis- greater phyletic diversity of microorganisms tinct environmental conditions. Careful compared with macroorganisms. Under one clas- fi ed 867 terrestrial mapping schemes have identi cation 60% of living phyla consist entirely or fi si et al. ecoregions (Figure 2.1 and Plate 1; Olson largely of unicellular species (Cavalier-Smith et al. 2001), 426 freshwater ecoregions (Abell 2004). Again, this perspective on the variety of 2008), and 232 marine coastal & shelf area ecor- life is not well re fl ected in much of the literature egions (Spalding et al. 2007). Ecoregions can in on biodiversity. turn be grouped into biomes, global-scale bio- geographic regions distinguished by unique col- lections of species assemblages and ecosystems. 2.1.3 Ecological diversity Olson et al. (2001) distinguish 14 terrestrial The third group of elements of biodiversity en- biomes, some of which at least will be very fa- miliar wherever in the world one resides (tropi- compasses the scales of ecological differences cal & subtropical moist broadleaf forests; from populations, through habitats, to ecosys- © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

47 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All 32 CONSERVATION BIOLOGY FOR ALL (2001). Figure 2.1 The terrestrial ecoregions. Reprinted from Olson et al. tropical & subtropical dry broadleaf forests; Westerlies, Trades and Coastal boundary), which tropical & subtropical coniferous forests; tem- are then subdivided, on the basis principally perate broadleaf & mixed forests; temperate co- of biogeochemical features, into a further 12 niferous forests; boreal forest/taiga; tropical & biomes (Antarctic Polar, Antarctic Westerly subtropical grasslands, savannas & shrublands; Winds, Atlantic Coastal, Atlantic Polar, Atlantic temperate grasslands, savannas & shrublands; Trade Wind, Atlantic Westerly Winds, Indian fl ooded grasslands & savannas; montane grass- Ocean Coastal, Indian Ocean Trade Wind, Paci c fi lands & shrublands; tundra; Mediterranean for- c Trade Wind, Paci fi c Polar, Paci fi Coastal, Paci c fi ests, woodlands & scrub; deserts & xeric Westerly Winds), and then into a fi ner 51 units shrublands; mangroves). (Longhurst 1998). At a yet coarser spatial resolution, terrestrial and aquatic systems can be divided into bio- 2.1.4 Measuring biodiversity geographic realms. Terrestrially, eight such realms are typically recognized, Australasia, Given the multiple dimensions and the complex- Antarctic, Afrotropic, Indo-Malaya, Nearctic, ity of the variety of life, it should be obvious that et al. Neotropic, Oceania and Palearctic (Olson there can be no single measure of biodiversity 2001). Marine coastal & shelf areas have been (see Chapter 16). Analyses and discussions of divided into 12 realms (Arctic, Temperate biodiversity have almost invariably to be framed c, fi North Atlantic, Temperate Northern Paci in terms of particular elements or groups of ele- c, Central fi Tropical Atlantic, Western Indo-Paci ments, although this may not always be apparent c, Eastern Indo-Paci fi c, Tropical Indo-Paci fi from the terminology being employed (the term Eastern Paci fi c, Temperate South America, ‘ biodiversity ’ is used widely and without explicit Temperate Southern Africa, Temperate Austra- cation to refer to only some subset of the fi quali et al. lasia, and Southern Ocean; Spalding variety of life). Moreover, they have to be framed 2007). There is no strictly equivalent scheme ” in terms either of number “ ” or of “ heterogeneity for the pelagic open ocean, although one has measures of biodiversity, with the former disre- divided the oceans into four primary units (Polar, garding the degrees of difference between the © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

48 1 33 BIODIVERSITY occurrences of an element of biodiversity and the 2.2 How has biodiversity changed latter explicitly incorporating such differences. through time? For example, organismal diversity could be ex- The Earth is estimated to have formed, by the pressed in terms of species richness, which is a accretion through large and violent impacts of number measure, or using an index of diversity numerous bodies, approximately 4.5 billion that incorporates differences in the abundances of years ago (Ga). Traditionally, habitable worlds the species, which is a heterogeneity measure. are considered to be those on which liquid The two approaches constitute different re- water is stable at the surface. On Earth, both the sponses to the question of whether biodiversity atmosphere and the oceans may well have started is similar or different in an assemblage in which a to form as the planet itself did so. Certainly, life is small proportion of the species comprise most of thought to have originated on Earth quite early in the individuals, and therefore would predomi- – its history, probably after about 3.8 4.0 Ga, when nantly be obtained in a small sample of indivi- impacts from large bodies from space are likely to duals, or in an assemblage of the same total have declined or ceased. It may have originated number of species in which abundances are in a shallow marine pool, experiencing intense more evenly distributed, and thus more species radiation, or possibly in the environment of a would occur in a small sample of individuals deeper water hydrothermal vent. Because of the (Purvis and Hector 2000). The distinction be- subsequent recrystallisation and deformation of tween number and heterogeneity measures is the oldest sediments on Earth, evidence for early also captured in answers to questions that re fl ect life must be found in its metabolic interaction taxonomic heterogeneity, for example whether the with the environment. The earliest, and highly above-mentioned group of 10 skipper butter fl ies controversial, evidence of life, from such indirect ve skipper species is as biodiverse as a group of fi geochemical data, is from more than 3.83 billion and fi ve swallowtail species (e.g. Hendrickson years ago (Dauphas 2004). Relatively unam- et al. and Ehrlich 1971). biguous fossil evidence of life dates to 2.7 Ga In practice, biodiversity tends most commonly (López-García et al. 2006). Either way, life has to be expressed in terms of number measures of thus been present throughout much of the Earth ’ s organismal diversity, often the numbers of a given existence. Although inevitably attention tends to taxonomic level, and particularly the numbers of fall on more immediate concerns, it is perhaps species. This is in large part a pragmatic choice. worth occasionally recalling this deep heritage in Organismal diversity is better documented and the face of the conservation challenges of today. often more readily estimated than is genetic diver- For much of this time, however, life comprised sity, and more fi nely and consistently resolved Precambrian chemosynthetic and photosynthetic than much of ecological diversity. Organismal prokaryotes, with oxygen-producing cyanobac- diversity, however, is problematic inasmuch as teria being particularly important (Labandeira the majority of it remains unknown (and thus 2005). Indeed, the evolution of oxygenic photo- studies have to be based on subsets), and precisely synthesis, followed by oxygen becoming a major how naturally and well many taxonomic groups component of the atmosphere, brought about a are themselves delimited remains in dispute. dramatic transformation of the environment Perhaps most importantly it also remains but on Earth. Geochemical data has been argued to one, and arguably a quite narrow, perspective on suggest that oxygenic photosynthesis evolved biodiversity. before 3.7 Ga (Rosing and Frei 2004), although Whilst accepting the limitations of measuring others have proposed that it could not have arisen biodiversity principally in terms of organismal before c.2.9 Ga (Kopp 2005). et al. diversity, the following sections on temporal These cyanobacteria were initially responsible and spatial variation in biodiversity will follow for the accumulation of atmospheric oxygen. This this course, focusing in many cases on species in turn enabled the emergence of aerobically richness. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

49 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 34 CONSERVATION BIOLOGY FOR ALL metabolizing eukaryotes. At an early stage, eu- to address its associated biases to determine those karyotes incorporated within their structure aer- actual patterns. The best fossil data are for marine obically metabolizing bacteria, giving rise to invertebrates and it was long thought that these eukaryotic cells with mitochondria; all anaerobi- principally demonstrated a dramatic rise in diver- cally metabolizing eukaryotes that have been cant periods of fi sity, albeit punctuated by signi studied in detail have thus far been found to stasis and mass extinction events. However, ana- have had aerobic ancestors, making it highly lyses based on standardized sampling have likely that the ancestral eukaryote was aerobic markedly altered this picture (Figure 2.2). They (Cavalier-Smith 2004). This was a fundamentally identify the key features of change in the numbers important event, leading to heterotrophic micro- of genera (widely assumed to correlate with spe- organisms and sexual means of reproduction. cies richness) as comprising: (i) a rise in richness Such endosymbiosis occurred serially, by simpler from the Cambrian through to the mid-Devonian and more complex routes, enabling eukaryotes to  ( 400 million years ago, Ma); (ii) a large 525 – diversify in a variety of ways. Thus, the inclusion extinction in the mid-Devonian with no clear re- of photosynthesizing cyanobacteria into a eu- –  400 covery until the Permian ( 300 Ma); (iii) a karyote cell that already contained a mitochon- large extinction in the late-Permian and again in drion gave rise to eukaryotic cells with plastids  250 – 200 Ma); and (iv) a rise in the late-Triassic ( and capable of photosynthesis. This event alone richness through the late-Triassic to the present ’ s would lead to dramatic alterations in the Earth 200 2008). ( 0 Ma; Alroy –  et al. ecosystems. Whatever the detailed pattern of change in di- Precisely when eukaryotes originated, when versity through time, most of the species that fi ed, and how congruent was the they diversi have ever existed are extinct. Across a variety of fi cation of different groups remains un- diversi groups (both terrestrial and marine), the best clear, with analyses giving a very wide range of present estimate based on fossil evidence is that dates (Simpson and Roger 2004). The uncertainty, the average species has had a lifespan (from its which is particularly acute when attempting to appearance in the fossil record until the time it understand evolutionary events in deep time, re- disappeared) of perhaps around 1 10 Myr – sults principally from the inadequacy of the fossil (McKinney 1997; May 2000). However, the varia- record (which, because of the low probabilities of bility both within and between groups is very fossilization and fossil recovery, will always tend marked, making estimation of what is the overall to underestimate the ages of taxa) and the dif - fi fi average dif cult. The longest-lived species that is culties of correctly calibrating molecular clocks so well documented is a bryozoan that persisted as to use the information embodied in genetic from the early Cretaceous to the present, a period sequences to date these events. Nonetheless, of approximately 85 million years (May 2000). If there is increasing convergence on the idea that the fossil record spans 600 million years, total most known eukaryotes can be placed in one of species numbers were to have been roughly con- ve or six major clades — Unikonts (Opisthokonts fi stant over this period, and the average life span of and Amoebozoa), Plantae, Chromalveolates, Rhi- individual species were 1 10 million years, then – 2005; Roger and et al. zaria and Excavata (Keeling c instant the extant species would at any speci fi Hug 2006). – 2% of those that have ever have represented 0.2 Focusing on the last 600 million years, attention lived (May 2000). If this were true of the present shifts somewhat from the timing of key diversi fi - time then, if the number of extant eukaryote spe- cation events (which becomes less controversial) cies numbers 8 million, 400 million might once per se to how diversity has changed through time have existed. (which becomes more measurable). Arguably the The frequency distribution of the numbers of critical issue is how well the known fossil record time periods with different levels of extinction is ects the actual patterns of change that took re fl markedly right-skewed, with most periods hav- place and how this record can best be analyzed ing relatively low levels of extinction and a © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

50 1 BIODIVERSITY 35 800 600 400 Number of genera 200 0 Ng S O Cm Tr J K Pg P C D 100 400 500 200 0 300 Time (Ma) ‐ Changes in generic richness of marine invertebrates over the last 600 million years based on a sampling Figure 2.2 standardized analysis of the fossil et al. (2008) with permission from AAAS (American Association for the Advancement of Science). record. Ma, million years ago. Reprinted from Alroy minority having very high levels (Raup 1994). lion years (Erwin 1998), and the resultant assem- The latter are the periods of mass extinction blages have invariably had a markedly different – 95% of species that were extant are es- when 75 composition from those that preceded a mass fi - timated to have become extinct. Their signi extinction, with groups which were previously cance lies not, however, in the overall numbers highly successful in terms of species richness of extinctions for which they account (over the being lost entirely or persisting at reduced last 500 Myr this has been rather small), but in the numbers. hugely disruptive effect they have had on the development of biodiversity. Clearly neither ter- fi restrial nor marine biotas are in nitely resilient to 2.3 Where is biodiversity? environmental stresses. Rather, when pushed be- yond their limits they can experience dramatic Just as biodiversity has varied markedly through collapses in genetic, organismal and ecological time, so it also varies across space. Indeed, one diversity (Erwin 2008). This is highly signi fi cant can think of it as forming a richly textured land given the intensity and range of pressures that and seascape, with peaks (hotspots) and troughs have been exerted on biodiversity by humankind, (coldspots), and extensive plains in between (Fig- and which have drastically reshaped the natural ure 2.3 and Plate 2, and 2.4 and Plate 3; Gaston world over a suf ciently long period in respect to fi 2000). Even locally, and just for particular groups, available data that we have rather little concept of the numbers of species can be impressive, with what a truly natural system should look like for example c.900 species of fungal fruiting bodies (Jackson 2008). Recovery from past mass extinc- recorded from 13 plots totaling just 14.7 ha (hect- tion events has invariably taken place. But, whilst are) near Vienna, Austria (Straatsma and Krisai- this may have been rapid in geological terms, it Greilhuber 2003), 173 species of lichens on a has nonetheless taken of the order of a few mil- single tree in Papua New Guinea (Aptroot © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

51 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: 36 CONSERVATION BIOLOGY FOR ALL Figure 2.3 Global richness patterns for birds of (a) species, (b) genera, (c) families, and (d) orders. Reprinted from Thomas (2008). et al. 1997), 814 species of trees from a 50 ha study plot sive inventory of all of the species that are present et al. 1992), in Peninsular Malaysia (Manokaran fi (microorganisms typically remain insuf ciently 850 species of invertebrates estimated to occur at documented even in otherwise well studied a sandy beach site in the North Sea (Armonies areas), knowledge of the basic patterns has been and Reise 2000), 245 resident species of birds developing rapidly. Although long constrained recorded holding territories on a 97 ha plot in to data on higher vertebrates, the breadth of or- Peru (Terborgh et al. 1990), and 200 species of > ganisms for which information is available has mammals occurring at some sites in the Amazo- been growing, with much recent work particular- nian rain forest (Voss and Emmons 1996). ly attempting to determine whether microorgan- Although it remains the case that for no even isms show the same geographic patterns as do moderately sized area do we have a comprehen- other groups. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

52 1 BIODIVERSITY 37 Figure 2.4 Global species richness patterns of birds, mammals, and amphibians, for total, rare (those in the lower quartile of range size for each group) and threatened (according to the IUCN criteria) species. Reprinted from Grenyer et al. (2006). 180 Ma) is important in ex-  Gondwana from 2.3.1 Land and water plaining why there are more species in terrestrial 2  340.1 million km (67%), the The oceans cover systems than in marine ones. Finally, the extreme 2 (33%), and freshwaters  land 170.3 million km fragmentation and isolation of freshwater bodies 2 (0.3%; with  1.5 million km (lakes and rivers) seems key to why these are so diverse for their 2 under ice and permanent another 16 million km area. 2 as wetlands, soil water snow, and 2.6 million km and permafrost) of the Earth ’ s surface. It would therefore seem reasonable to predict that the 2.3.2 Biogeographic realms and ecoregions oceans would be most biodiverse, followed by Of the terrestrial realms, the Neotropics is gener- the land and then freshwaters. In terms of num- ally regarded as overall being the most biodi- bers of higher taxa, there is indeed some evidence verse, followed by the Afrotropics and Indo- that marine systems are especially diverse. For Malaya, although the precise ranking of these example, of the 96 phyla recognized by Margulis tropical regions depends on the way in which and Schwartz (1998), about 69 have marine repre- organismal diversity is measured. For example, sentatives, 55 have terrestrial ones, and 60 have for species the richest realm is the Neotropics for freshwater representatives. However, of the spe- amphibians, reptiles, birds and mammals, but for cies described to date only about 15% are marine families it is the Afrotropics for amphibians and and 6% are freshwater. The fact that life began in mammals, the Neotropics for reptiles, and the the sea seems likely to have played an important Indo-Malayan for birds (MEA 2005). In parts, role in explaining why there are larger numbers ect variation in the histories these differences re fl of higher taxa in marine systems than in terrestri- of the realms (especially mountain uplift and cli- al ones. The heterogeneity and fragmentation of mate changes) and the interaction with the emer- the land masses (particularly that associated gence and spread of the groups, albeit perhaps of with the breakup of the “ supercontinent ” © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

53 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 38 The Table 2.3 ve most species rich terrestrial ecoregions for each of four vertebrate groups. AT – Afrotropic, IM – Indo ‐ Malaya, fi – – Neotropic. Data from Olson NA Nearctic, and NT et al. (2001). Reptiles Birds Mammals Amphibians Northern Indochina ‐ Veracruz Sierra Madre de Oaxaca Peten 1 Northwestern Andean subtropical forests (IM) moist forests (NT) pine ‐ oak forests (NT) montane forests (NT) Northern Indochina Southwest Amazon 2 Eastern Cordillera real Southwest Amazon moist forests (NT) subtropical forests moist forests (NT) montane forests (IM) (NT) 3 Napo moist forests (NT) Napo moist forests Albertine Rift montane Sierra Madre Oriental pine ‐ forests (AT) oak forests (NA) (NT) 4 Southwest Amazon Southern Paci fi c dry Central Zambezian Miombo Southwest Amazon moist forests (NT) woodlands (AT) forests (NT) moist forests (NT) Northern Acacia Central Zambezian ‐ 5 Choco ‐ Darien moist Central American forests (NT) pine ‐ oak forests Miombo woodlands Commiphora bushlands & thickets (AT) (NT) (AT) richness (and some other elements of organismal complicated by issues of geographic consistency diversity) towards lower (tropical) latitudes. in the de nition of higher taxonomic groupings. fi Several features of this gradient are of note: fi c and Central The Western Indo-Paci (i) it is exhibited in marine, terrestrial and fresh- fi Indo-Paci c realms have been argued to be a waters, and by virtually all major taxonomic center for the evolutionary radiation of many groups, including microbes, plants, invertebrates groups, and are thought to be perhaps the global and vertebrates (Hillebrand 2004; Fuhrman et al. hotspot of marine species richness and endemism 2008); (ii) it is typically manifest whether biodi- 2002). With a shelf area (Briggs 1999; Roberts et al. 2 , which is considered to be a versity is determined at local sites, across large of 6 570 000 km signi fl uence, it has more than 6000 spe- cant in fi regions, or across entire latitudinal bands; (iii) it cies of molluscs, 800 species of echinoderms, 500 has been a persistent feature of much of the species of hermatypic (reef forming) corals, and history of life on Earth (Crane and Lidgard sh (Briggs 1999). fi 4000 species of 2008); (iv) the peak of diversity 1989; Alroy et al. At the scale of terrestrial ecoregions, the most is seldom at the equator itself, but seems often to speciose for amphibians and reptiles are in the be displaced somewhat further north (often at  N); (v) it is commonly, though far from Neotropics, for birds in Indo-Malaya, Neotropics  30 20 – universally, asymmetrical about the equator, in- and Afrotropics, and for mammals in the Neo- creasing rapidly from northern regions to the tropics, Indo-Malaya, Nearctic, and Afrotropics equator and declining slowly from the equator (Table 2.3). Amongst the freshwater ecoregions, to southern regions; and (vi) it varies markedly those with globally high richness of freshwater in steepness for different major taxonomic fi sh include the Brahmaputra, Ganges, and fl groups with, for example, butter ies being Yangtze basins in Asia, and large portions of more tropical than birds. the Mekong, Chao Phraya, and Sitang and Irra- Although it attracts much attention in its own waddy; the lower Guinea in Africa; and the right, it is important to see the latitudinal pattern Paraná and Orinoco in South America (Abell in species richness as a component of broader 2008). et al. spatial patterns of richness. As such, the mechan- isms that give rise to it are also those that give rise 2.3.3 Latitude to those broader patterns. Ultimately, higher spe- cies richness has to be generated by some combi- Perhaps the best known of all spatial patterns in nation of greater levels of speciation (a cradle of biodiversity is the general increase in species © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

54 1 39 BIODIVERSITY diversity), lower levels of extinction (a museum progressively to decrease with distance from sea of diversity) or greater net movements of geo- level (above or below) and to show a pronounced graphic ranges. It is likely that their relative im- fi rst increases hump-shaped pattern in which it portance in giving rise to latitudinal gradients and then declines (Angel 1994; Rahbek 1995; varies with taxon and region. This said, greater et al. 2008). The latter pattern tends Bryant levels of speciation at low latitudes and range to become more apparent when the effects of expansion of lineages from lower to higher variation in area have been accounted for, and is latitudes seem to be particularly important probably the more general, although in either et al. 2007). More 2006; Martin et al. (Jablonski case richness tends to be lowest at the most proximally, key constraints on speciation and ex- extreme elevations or depths. tinction rates and range movements are thought Microbial assemblages can be found at consid- to be levels of: (i) productive energy, which in fl u- erable depths (in some instances up to a few kilo- ence the numbers of individuals that can be sup- meters) below the terrestrial land surface and the ported, thereby limiting the numbers of species fl oor, often exhibiting unusual metabolic cap- sea that can be maintained in viable populations; abilities (White et al. 2004). et al. Hondt ’ 1998; D fl uences mutation (ii) ambient energy, which in Knowledge of these assemblages remains, how- rates and thus speciation rates; (iii) climatic vari- ever, extremely poor, given the physical chal- ation, which on ecological time scales in fl uences lenges of sampling and of doing so without the breadth of physiological tolerances and contamination from other sources. dispersal abilities and thus the potential for pop- ulation divergence and speciation, and on evolu- uences extinctions (e.g. fl tionary time scales in 2.4 In conclusion through glacial cycles) and recolonizations; and (iv) topographic variation, which enhances the Understanding of the nature and scale of biodi- likelihood of population isolation and thus speci- versity, of how it has changed through time, and 2005; Clarke and et al. ation (Gaston 2000; Evans of how it varies spatially has developed immea- Gaston 2006; Davies et al. 2007). surably in recent decades. Improvements in the levels of interest, the resources invested and the application of technology have all helped. In- 2.3.4 Altitude and Depth deed, it seems likely that the basic principles are in the main well established. However, Variations in depth in marine systems and alti- much remains to be learnt. The obstacles are tude in terrestrial ones are small relative to the fourfold. First, the sheer magnitude and com- areal coverage of these systems. The oceans aver- plexity of biodiversity constitute a huge chal- age c.3.8 km in depth but reach down to 10.9 km lenge to addressing perhaps the majority of (Challenger Deep), and land averages 0.84 km in questions that are posed about it, and one that elevation and reaches up to 8.85 km (Mt. Everest). is unlikely to be resolved in the near future. Nonetheless, there are profound changes in or- Second, the biases of the fossil record and the ganismal diversity both with depth and altitude. apparent variability in rates of molecular evolu- This is in large part because of the environmental tion continue to thwart a better understanding of differences (but also the effects of area and isola- the history of biodiversity. Third, knowledge of tion), with some of those changes in depth or the spatial patterning of biodiversity is limited altitude of a few hundred meters being similar by the relative paucity of quantitative sampling to those experienced over latitudinal distances of of biodiversity over much of the planet. Finally, several hundred kilometers (e.g. temperature). the levels and patterns of biodiversity are In both terrestrial and marine (pelagic and ben- being profoundly altered by human activities thic) systems, species richness across a wide vari- (see Box 2.1 and Chapter 10). ety of taxonomic groups has been found © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

55 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 40 Box 2.1 Invaluable biodiversity inventories Navjot S. Sodhi sh, birds, fi ies, freshwater fl 43%) in butter – (34 This chapter de nes biodiversity. Due to fi and mammals. Due to low endemism in massive loss of native habitats around the Singapore, all of these extinctions likely globe (Chapter 4), biodiversity is rapidly being represented population than species eroded (Chapter 10). Therefore, it is critical to extinctions (see Box 10.1). Using extinction data understand which species will survive human (2003) also from Singapore, Brook et al. onslaught and which will not. We also need to projected that if the current levels of comprehend the composition of new deforestation in Southeast Asia continue, communities that arise after the loss or between 13 – 42% of regional populations could disturbance of native habitats. Such a be lost by 2100. Half of these extinctions could “ peek ” into the past. determination needs a represent global species losses. That is, which species were present before the Fragments are becoming a prevalent feature habitat was disturbed. Perhaps naturalists in inmostlandscapesaroundtheglobe(Chapter5). the 19th and early 20th centuries did not Very little is known about whether fragments realize that they were doing a great service to ‐ can sustain forest biodiversity over the long future conservation biologists by publishing term. Using an old species inventory, Sodhi et al. species inventories. These historic inventories (2005) studied the avifaunal change over 100 they can be used as — are treasure troves years (1898 – 1998) in a four hectare patch of rain baselines for current (and future) species loss forestinSingapore(SingaporeBotanicGardens). and turnover assessments. Over this period, many forest species (e.g. green case scenario in Singapore represents a worst ‐ 2 Calyptomena viridis broadbill ( ); Box 2.1 Figure) tropical deforestation. This island (540 km ) has were lost, and replaced with introduced species lost over 95% of its primary forests since 1819. such as the house crow ( Corvus splendens ). By Comparing historic and modern inventories, 1998, 20% of individuals observed belonged to et al. Brook (2003) could determine losses in introduced species, with more native species vascular plants, freshwater decapod expected to be extirpated from the site in the ies, freshwater fl crustaceans, phasmids, butter future through competition and predation. This fi sh, amphibians, reptiles, birds, and mammals. study showsthat small fragments decline intheir They found that overall, 28% of original species value for forest birds over time. were lost in Singapore, probably due to deforestation. Extinctions were higher Box 2.1 Figure Green broadbill. Photograph by Haw Chuan Lim. continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

56 1 BIODIVERSITY 41 (Continued) Box 2.1 also be included in these as such can be The old species inventories not only help in used to determine the effect of abundance understanding species losses but also help on species persistence. All these checklists determine the characteristics of species that are should be placed on the web for wide vulnerable to habitat perturbations. Koh et al. dissemination. Remember, like antiques, (2004) compared ecological traits (e.g. body species inventories become more valuable size) between extinct and extant butter ies in fl with time. Singapore. They found that butter ies species fl restricted to forests and those which had high larval host plant speci city were particularly fi REFERENCES vulnerable to extirpation. In a similar study, but on angiosperms, Sodhi et al. (2008) found Brook, B. W., Sodhi, N. S., and Ng, P. K. L. (2003). that plant species susceptible to habitat Catastrophic extinctions follow deforestation in disturbance possessed traits such as Nature , 420 424 423. – Singapore. , dependence on forests and pollination by Koh, L. P., Sodhi, N. S., and Brook, B. W. (2004). Prediction mammals. These trait comparison studies may extinction proneness of tropical butter Conservation ies. fl assist in understanding underlying Biology 1578. , 18 , 1571 – mechanisms that make species vulnerable to Sodhi, N.S., Lee, T. M., Koh, L. P., and Dunn, R. R. extinction and in preemptive identi fi cation (2005). A century of avifaunal turnover in a small of species at risk from extinction. , tropical rainforest fragment. Animal Conservation The above highlights the value of species 8 , 217 – 222. inventories. I urge scientists and amateurs Sodhi, N. S., Koh, L. P., Peh, K. S. et al. H. ‐ (2008). to make species lists every time they visit a Correlates of extinction proneness in tropical angios- site. Data such as species numbers should perms. Diversity and Distributions , 14 ,1 – 10. Biodiversity is variably distributed across Summary · the Earth, although some marked spatial gra- Biodiversity is the variety of life in all of its many dients seem common to numerous higher taxonomic · manifestations. groups. This variety can usefully be thought of in terms of The obstacles to an improved understanding of · · three hierarchical sets of elements, which capture biodiversity are: (i) its sheer magnitude and com- different facets: genetic diversity, organismal diver- plexity; (ii) the biases of the fossil record and the sity, and ecological diversity. apparent variability in rates of molecular evolution; nition no single measure of biodi- There is by de fi (iii) the relative paucity of quantitative sampling · versity, although two different kinds of measures over much of the planet; and (iv) that levels and (number and heterogeneity) can be distinguished. patterns of biodiversity are being profoundly al- Pragmatically, and rather restrictively, biodiver- tered by human activities. · sity tends in the main to be measured in terms of number measures of organismal diversity, and espe- cially species richness. Suggested reading Biodiversity has been present for much of the · history of the Earth, but the levels have changed Gaston, K. J. and Spicer, J. I. (2004). Biodiversity: an · introduction , 2nd edition. Blackwell Publishing, Oxford, dramatically and have proven challenging to docu- UK. ment reliably. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

57 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 42 CONSERVATION BIOLOGY FOR ALL World atlas of Groombridge, B. and Jenkins, M. D. (2002). Clarke, A. and Gaston, K. J. (2006). Climate, energy and · . s living resources in the 21st century ’ biodiversity: earth Proceedings of the Royal Society of London Series diversity. University of California Press, London, UK. B 2266. – , 2257 273 , , – , 572 415 574. Nature Copley, J. (2002). All at sea. Levin, S. A., ed. (2001). Encyclopedia of biodiversity, Vols. · fi Crane, P. R. and Lidgard, S. (1989). Angiosperm diversi - Academic Press, London, UK. 1 – 5. cation and paleolatitudinal gradients in Cretaceous MEA (millennium Ecosystem Assessment) (2005). Eco- · 246 , Science oristic diversity. fl 678. – , 675 systems and human well-being: current state and trends, Curtis, T. P., Sloan, W. T., and Scannell, J. W. (2002). Island Press, Washington, DC. Volume 1. 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(Suppl. 1), 105 , my of Sciences of the United States of America Proceedings of the National Academy of Sciences of the United 11465. 11458 – 6763. – , 6758 91 , States of America (2005). The tree et al. Keeling, P. J., Burger, G., Durnford, D. G., et al. Roberts, C. M., McClean, C. J., Veron, J. E. N., (2002) , – , 670 20 of eukaryotes. 676. Trends in Ecology and Evolution Marine biodiversity hotspots and conservation priorities Kopp, R. E., Kirschvink, J. L., Hilburn, I. A., and Nash, C. Z. 295 , 1280 – 1284. , Science for tropical reefs. (2005). The Paleoproterozoic snowball Earth: A climate © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

59 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All 44 CONSERVATION BIOLOGY FOR ALL Torsvik, V., Øvreås, L., and Thingstad, T. F. (2002). Pro- - fi Roger, A. J. and Hug, L. A. (2006). The origin and diversi karyotic diversity-magnitude, dynamics, and controlling cation of eukaryotes: problems with molecular phyloge- , 1064 296 , Science factors. 1066. – Philosophical nies and molecular clock estimation. van Rootselaar, O. (1999). New birds for the world: Transactions of the Royal Society of London B , 361 , , species discovered during 1980 1999. , 12 – Birding World 1039 – 1054. 286 – 293. Rosing, M. T. and Frei, R. (2004). U-rich Archaean sea- fl oor van Rootselaar, O. (2002). New birds for the world: 3700 Ma sediments from Greenland - indications of > species described during 1999 oxygenic photosynthesis. Earth and Planetary Science Birding World – 2002. , – 244. , 217 Letters , 237 – , 428 15 431. Simpson, A. G. B. and Roger, A. J. (2004). The real ‘ king- Venter, J. C., Remington, K., Heidelberg, J. F., et al. (2004). of eukaryotes. Current Biology doms – , 14 ’ , R693 R696. Environment genome shotgun sequencing of the (2007). Marine Spalding, M. D., Fox, H. E., Allen, G. R., et al. – Sargasso Sea. Science , 304 ,66 74. ecoregions of the world: a bioregionalisation of coastal Voss, R. S. and Emmons, L. H. (1996). Mammalian diversity 57 , 573 – 583. , BioScience and shelf areas. in Neotropical lowland rainforests: a preliminary Straatsma, G. and Krisai-Greilhuber, I. (2003). Assemblage assessment. Bulletin of the American Museum of Natural structure, species richness, abundance and distribution ,1 – , History 115. 230 of fungal fruit bodies in a seven year plot-based survey Ward, B. B. (2002). How many species of prokaryotes are Mycological Research near Vienna. 640. – , 632 107 , Proceedings of the National Academy of Sciences of the there? Terborgh, J., Robinson, S. K., Parker, T. A. III, Munn, C. A., – , 10234 , United States of America 99 10236. and Pierpont, N. (1990). Structure and organization White, D. C., Phelps, T. J., and Onstott, T. C. (1998). What ’ s of an Amazonian forest bird community. Ecological Current Opinion in Microbiology , up down there? , 238. – , 213 Monographs 60 1 , 286 – 290. et al. Thomas, G. H., Orme, C. D., Davies, R. G., (2008). Whitman, W. B., Coleman, D. C., and Wiebe, W. J. (1998). Regional variation in the historical components of global Prokaryotes: the unseen majority. Proceedings of the avian species richness. Global Ecology and Biogeography , , National Academy of Sciences of the United States of America , 340 17 351. – 6583. – , 6578 95 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

60 1 CHAPTER 3 Ecosystem functions and services Cagan H. Sekercioglu In our increasingly technological society, people may not know what an ecosystem is, the proper give little thought to how dependent they are on s ecosystems is critical to ’ functioning of the world the proper functioning of ecosystems and the human survival, and understanding the basics of fl crucial services for humanity that ow from ecosystem services is essential. Entire volumes them. Ecosystem services are “ the conditions have been written on ecosystem services (Nation- and processes through which natural ecosystems, al Research Council 2005; Daily 1997), culminat- and the species that make them up, sustain and ing in a formal, in-depth, and global overview by ” (Daily 1997); in other words, ll human life ful fi hundreds of scientists: the Millennium Ecosystem “ the set of ecosystem functions that are useful to Assessment (2005a). It is virtually impossible to list humans ” (Kremen 2005). Although people have all the ecosystem services let alone the natural been long aware that natural ecosystems help products that people directly consume, so support human societies, the explicit recognition this discussion presents a brief introduction to is relatively recent of “ ecosystem services ” ecosystem function and an overview of critical (Ehrlich and Ehrlich 1981a; Mooney and Ehrlich ecosystem services. 1997). Since the entire planet is a vast network of integrated ecosystems, ecosystem services range 3.1 Climate and the Biogeochemical Cycles from global to microscopic in scale (Table 3.1; Ecosystem services start at the most fundamental Millennium Ecosystem Assessment 2005a). level: the creation of the air we breathe and the Ecosystems purify the air and water, generate supply and distribution of water we drink. oxygen, and stabilize our climate. Earth would Through photosynthesis by bacteria, algae, fi not be t for our survival if it were not for plants plankton, and plants, atmospheric oxygen is that have created and maintained a suitable at- mostly generated and maintained by ecosystems mosphere. Organisms decompose and detoxify and their constituent species, allowing humans detritus, preventing our civilization from being and innumerable other oxygen-dependent organ- buried under its own waste. Other species help to isms to survive. Oxygen also enables the atmo- create the soils on which we grow our food, and itself via the oxidation of sphere to ” “ clean recycle the nutrients essential to agriculture. Myr- compounds such as carbon monoxide (Sodhi iad creatures maintain these soils, play key roles et al. 2007) and another form of oxygen in the in recycling nutrients, and by so doing help to ozone layer, protects life from the sun ’ s carcino- mitigate erosion and oods. Thousands of animal fl genic, ultraviolet (UV) rays. species pollinate and fertilize plants, protect them the Global biogeochemical cycles consist of “ from pests, and disperse their seeds. And of transport and transformation of substances in course, humans use and trade thousands of the environment through life, air, sea, land, and plant, animal and microorganism species for ice ” (Alexander et al. 1997). Through these cycles, food, shelter, medicinal, cultural, aesthetic and the planet ’ s climate, ecosystems, and creatures many other purposes. Although most people 45 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

61 Table 3.1 Ecosystem services, classi ed according to the Millennium Ecosystem Assessment (2003), and their ecosystem service providers. ‘ Functional fi ’ units ik) of ecosystem service providers; spatial scale indicates the scale(s) of operation refer to the unit of study for assessing functional contributions ( ∫ of the service. Assessment of the potential to apply this conceptual framework to the service is purposefully conservative and is based on the degree t o which the contributions of individual species or communities can currently be quanti ed (Kremen 2005). fi Potential to apply this conceptual framework for Ecosystem service providers/ Functional units Spatial scale trophic level Service ecological study Populations, Aesthetic, cultural Low All biodiversity Local ‐ global species, communities, ecosystems Diverse species Populations, Medium Ecosystem goods global Local ‐ species, communities, ecosystems Biogeochemical cycles, micro ‐ UV protection Biogeochemical Low Global organisms, plants cycles, functional groups cation fi ‐ organisms, plants Biogeochemical Puri Micro ‐ Regional Medium (plants) cycles, of air global populations, species, functional groups Flood mitigation Communities, Vegetation Local ‐ regional Medium habitats Vegetation Communities, Local ‐ regional Medium Drought mitigation habitats Climate stability Vegetation Communities, Medium Local ‐ global habitats Insects, birds, mammals Pollination Populations, Local High species, functional groups Pest control Populations, Invertebrate parasitoids and Local High species, predators and vertebrate predators functional groups cation of water Vegetation, soil micro ‐ organisms, fi Puri Populations, regional Medium to high* ‐ Local species, organisms, aquatic aquatic micro ‐ functional invertebrates groups, communities, habitats Detoxi fi cation and Leaf litter and soil invertebrates, soil Populations, regional Medium ‐ Local decomposition of ‐ micro ‐ species, organisms, aquatic micro wastes functional organisms groups, communities, habitats Soil generation and Leaf litter and soil invertebrates, soil Populations, Medium Local ‐ fi xing ‐ micro soil fertility organisms, nitrogen species, plants, plant and animal functional production of waste products groups Seed dispersal Ants, birds, mammals Populations, High Local species, functional groups * Waste ‐ water engineers ‘ design ’ microbial communities; in turn, wastewater treatments provide ideal replicated experiments for ecological work (Graham and Smith 2004 in Kremen 2005).

62 1 47 ECOSYSTEM FUNCTIONS AND SERVICES and warming both exacerbate the problem as for- are tightly linked. Changes in one component can est ecosystems switch from being major carbon have drastic effects on another, as exempli fi ed by 2004; et al. sinks to being carbon sources (Phat the effects of deforestation on climatic change IPCC 2007). If fossil fuel consumption and defor- et al. (Phat 2004). The hydrologic cycle is one estation continue unabated, global CO emissions that most immediately affects our lives and it is 2 are expected to be about 2 4 times higher than at – treated separately below. present by the year 2100 (IPCC 2007). As climate As carbon-based life forms, every single organ- and life have coevolved for billions of years and ism on our planet is a part of the global carbon interact with each other through various feedback cycle. This cycle takes place between the four main )inthe mechanisms (Schneider and Londer 1984), rapid reservoirs of carbon: carbon dioxide (CO 2 atmosphere; organic carbon compounds within climate change would have major consequences organisms; dissolved carbon in water bodies; and ’ for the planet s life-support systems. There are carbon compounds inside the earth as part of soil, now plans under way for developed nations to limestone (calcium carbonate), and buried organic fi nance the conservation of tropical forests in the matter like coal, natural gas, peat, and petroleum developing world so that these forests can contin- (Alexander 1997). Plants play a major role in et al. ue to provide the ecosystem service of acting as through photosynthesis xing atmospheric CO fi carbon sinks (Butler 2008). 2 and most terrestrial carbon storage occurs in forest Changes in ecosystems affect nitrogen, phos- 2000). The global carbon et al. trees (Falkowski et al. phorus, and sulfur cycles as well (Alexander cycle has been disturbed by about 13% compared 1997; Millennium Ecosystem Assessment 2005b; to the pre-industrial era, as opposed to 100% or Vitousek 1997). Although nitrogen in its et al. ) makes up 80% of the atmo- more for nitrogen, phosphorous, and sulfur cycles gaseous form (N 2 sphere, it is only made available to organisms et al. (Falkowski 2000). Given the dominance of through nitrogen fi xation by cyanobacteria in carbon in shaping life and in regulating climate, aquatic systems and on land by bacteria and however, this perturbation has already been algae that live in the root nodules of lichens and enough to lead to signi fi cant climate change with 1997). Eighty million legumes (Alexander et al. worse likely to come in the future [IPCC (Intergov- fi cially fi tons of nitrogen every year are xed arti ernmental Panel on Climate Change) 2007]. , methane (CH ), and by industry to be used as fertilizer (Millennium Because gases like CO 4 2 O) trap the sun ’ s heat, especially nitrous oxide (N Ecosystem Assessment 2005b). However, the ex- 2 ’ s emitted by the long-wave infrared radiation that cessive use of nitrogen fertilizers can lead to nu- the warmed planet, the atmosphere creates a nat- trient overload, eutrophication, and elimination ural “ greenhouse ” (Houghton 2004). Without this of oxygen in water bodies. Nitrogen oxides, greenhouse effect, humans and most other organ- regularly produced as a result of fossil fuel com- isms would be unable to survive, as the global bustion, are potent greenhouse gases that mean surface temperature would drop from the increase global warming and also lead to smog,   – C (IPCC 2007). Ironically, Cto 19 current 14 breakdown of the ozone layer, and acid rain the ever-rising consumption of fossil fuels during 1997). Similarly, although sulfur et al. (Alexander the industrial age and the resultant increasing is an essential element in proteins, excessive emission of greenhouse gases have created the sulfur emissions from human activities lead to opposite problem, leading to an increase in the sulfuric acid smog and acid rain that harms peo- magnitude of the greenhouse effect and a conse- ple and ecosystems alike (Alexander 1997). et al. quent rise in global temperatures (IPCC 2007). Phosphorous (P) scarcity limits biological nitro- concentrations Since 1750, atmospheric CO gen fi xation (Smith 1992). In many terrestrial eco- 2 have increased by 34% (Millennium Ecosystem systems, where P is scarce, specialized symbiotic Assessment 2005a) and by the end of this century, fungi (mycorrhizae) facilitate P uptake by plants average global temperature is projected to rise by (Millennium Ecosystem Assessment 2005b). Even   C (IPCC 2007). Increasing deforestation 6.4 – 1.8 though P is among the least naturally available of © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

63 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 48 major nutrients, use of phosphorous in arti cial fi (2007): improvement of extractive water supply, fertilizers and runoff from animal husbandry improvement of in-stream water supply, water often also leads to eutrophication in aquatic sys- damage mitigation, provision of water-related tems (Millenium Ecosystem Assessment 2005b). cultural services, and water-associated support- The mining of phosphate deposits and their addi- ing services (Figure 3.1). Although 71% of the tion to terrestrial ecosystems as fertilizers repre- planet is covered by water, most of this is seawa- sents a six fold increase over the natural rate of ter un fi t for drinking or agriculture (Postel et al. mobilization of P by the weathering of phosphate 1996). Fresh water not locked away in glaciers rock and by plant activity (Reeburgh 1997). and icecaps constitutes 0.77% of the planet s ’ P enters aquatic ecosystems mainly through ero- cient water (Shiklomanov 1993). To provide suf fi sion, but no-till agriculture and the use of hedge- fresh water to meet human needs via industrial rows can substantially reduce the rate of this desalination (removing the salt from seawater) process (Millenium Ecosystem Assessment 2005a). would cost US$3 000 billion per year (Postel and Carpenter 1997). Quantity, quality, location, and timing of water provision determine the scale and impact of 3.2 Regulation of the Hydrologic Cycle et al. 2007). These hydrologic services (Brauman One of the most vital and immediate services of attributes can make the difference between water ecosystems, particularly of forests, rivers and as a blessing (e.g. drinking water) or a curse (e.g. wetlands, is the provisioning and regulation of oods). Water is constantly redistributed through fl water resources. These services provide a vast the hydrologic cycle. Fresh water comes down range of bene ts from spiritual to life-saving, fi as precipitation, collects in water bodies or is cation of hydrologic ser- illustrated by the classi fi absorbed by the soil and plants. Some of the et al. ve broad categories by Brauman fi vices into ows unutilized into the sea or seeps into fl water Hydrologic service Hydrologic attribute Ecohydrologic process (what the beneficiary receives) (direct effect of the ecosystem) (what the ecosystem does) Local climate interactions Quantity Diverted water supply: (surface and ground water water for municipal, Water use by plants storage and flow) agricultural, commercial, industrial, thermoelectric power Environmental filtration generation uses Quality In situ water supply: (pathogens, nutrients, Soil stabilization water for hydropower, salinity, sediment) recreation, transportation, Chemical and biological supply of fish and other additions/subtractions freshwater products Water damage mitigation: Soil development water for hydropower, recreation, transportation, Ground surface Location supply of fish and other modification (ground/surface, freshwater products up/downstream, in/out of Surface flow path alteration Spiritual and aesthetic: channel) provision of religious, River bank development educational, tourism values Supporting: Control of flow speed Water and nutrients to support Timing vital estuaries and other Short-and long-term water (peak flows, base flows, habitats, preservation of storage velocity) options Seasonality of water use The effects of hydrological ecosystem processes on hydrological services. Reprinted from Brauman et al. (2007). Figure 3.1 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

64 1 49 ECOSYSTEM FUNCTIONS AND SERVICES underground aquifers where it can remain for extent (Day et al. 2007). The impact of the 24 millennia unless extracted by people; mining this December 2004 tsunami in Southeast Asia “ fossil groundwater is often unsustainable and is ” would have been reduced if some of the hard- a serious problem in desert regions like Libya est-hit areas had not been stripped of their man- (Millennium Ecosystem Assessment 2005c). The 2005; et al. grove forests (Dahdouh-guebas cycle is completed when water vapor is released Danielsen 2005). These observations support et al. back into the atmosphere either through evapora- waru “ analytical models in which thirty trees ” tion from land and water bodies or by being re- Hibiscus tiliaceus ( ) planted along a 100 m by leased from plants (transpiration) and other 1 meter band reduced the impact of a tsunami organisms. Rising environmental temperatures by 90% (Hiraishi and Harada 2003), a solution are expected to increase evaporation and conse- fi more effective and cheaper than arti cial barriers. quent precipitation in some places and raise the Hydrologic regulation by ecosystems begins fi res in other places, likelihood of droughts and with the rst drop of rain. Vegetation layers, fi both scenarios that would have major conse- especially trees, intercept raindrops, which grad- quences for the world ’ s vegetation (Wright ually descend into the soil, rather than hitting it 2005). These changes in turn can lead to further directly and leading to erosion and oods. By fl climatic problems, affecting agriculture and com- intercepting rainfall and promoting soil develop- munities worldwide. Ecosystems, particularly ment, vegetation can modulate the timing of forests, play major roles in the regulation of the fl ows and potentially reduce ooding. Flood mit- fl hydrologic cycle and also have the potential to igation is particularly crucial in tropical areas moderate the effects of climate change. Tropical where downpours can rapidly deposit enormous forests act as heat and humidity pumps, transfer- amounts of water that can lead to increased ero- ring heat from the tropics to the temperate zones oods, and deaths if there is little natural sion, fl and releasing water vapor that comes back as 2007). et al. forest to absorb the rainfall (Bradshaw 2007). Extensive tropical defores- rain (Sodhi et al. Studies of some watersheds have shown that na- tation is expected to lead to higher temperatures, fl tive forests reduced ood risks only at small reduced precipitation, and increased frequency of scales, leading some hydrologists to question di- droughts and fi res, all of which are likely to reduce ood reduction fl rectly connecting forest cover to tropical forest cover in a positive feedback loop fi (Calder and Aylward 2006). However, in the rst (Sodhi et al. 2007). global-scale empirical demonstration that forests Forest ecosystems alone are thought to regulate ood risk and severity in are correlated with fl ’ approximately a third of the planet s watersheds developing countries, Bradshaw (2007) esti- et al. on which nearly fi ve billion people rely (Millen- mated that a 10% decrease in natural forest area nium Ecosystem Assessment 2005c). With in- would lead to a fl ood frequency increase between creasing human population and consequent 8% increase in total – 4% and 28%, and to a 4 ood fl water pollution, fresh water is becoming an in- duration at the country scale. Compared to natu- creasingly precious resource, especially in arid ral forests, however, afforestation programs or areas like the Middle East, where the scarcity of oods, or may forest plantations may not reduce fl icts fl water is likely to lead to increasing local con ood volume due to road construc- even increase fl st century (Klare 2001; Selby 2005). in the 21 tion, soil compaction, and changes in drainage Aquatic ecosystems, in addition to being vital regimes (Calder and Aylward 2006). Non-native fi sources of water, sh, waterfowl, reeds, and plantations can do more harm than good, partic- other resources, also moderate the local climate ularly when they reduce dry season water fl ows oods, tsunamis, and fl and can act as buffers for 2005). et al. (Scott other water incursions (Figure 3.1). For example, Despite covering only 6% of the planet ’ s sur- the ooding following Hurricane Katrina would fl face, tropical forests receive nearly half of the have done less damage if the coastal wetlands world s rainfall, which can be as much as 22 500 ’ surrounding New Orleans had had their original fi mm during ve months of monsoon season in © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

65 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 50 India (Myers 1997). In Southeast Asia, an intact farming can result in the loss of half the soil old-growth dipterocarp forest intercepts at least nutrients in less than a decade (Bolin and Cook 35% of the rainfall, while a logged forest inter- 1983), a loss that can take centuries to restore. In spp.) Elaeis cepts less than 20%, and an oil palm ( arid areas, the replacement of native deep-rooted plantation intercepts only 12% (Ba 1977). As a plants with shallow-rooted crop plants can lead consequence, primary forest can moderate sea- to a rise in the water table, which can bring soil fl ow and availability bet- sonal extremes in water salts to the surface (salinization), cause waterlog- ter than more intensive land uses like plantation ging, and consequently result in crop losses forestry and agriculture. For example, primary 1993). et al. (Lefroy ve times forest in Ivory Coast releases three to fi Soil provides six major ecosystem services as much water at the end of the dry season com- 1997): et al. (Daily pared to a coffee plantation (Dosso 1981). How- Moderating the hydrologic cycle. · ever, it is dif fi cult to make generalizations about Physical support of plants. · hydrologic response in the tropics. For example, Retention and delivery of nutrients to plants. · local soil and rainfall patterns can result in a Disposal of wastes and dead organic matter. · 65-fold variation in tropical natural sedimentation Renewal of soil fertility. · rates (Bruijnzeel 2004). This underlines the impor- Regulation of major element cycles. · tance of site-speci fi c studies in the tropics, but Every year enough rain falls to cover the planet most hydrologic studies of ecosystems have with one meter of water (Shiklomanov 1993), but taken place in temperate ecosystems (Brauman ’ thanks to soil s enormous water retention capacity, 2007). et al. most of this water is absorbed and gradually released to feed plants, underground aquifers, and rivers. However, intensive cultivation, by low- 3.3 Soils and Erosion ering soil ’ s organic matter content, can reduce this Without forest cover, erosion rates skyrocket, and oods, erosion, pollution, and fl capacity, leading to many countries, especially in the tropics, lose et al. further loss of organic matter (Pimentel 1995). astounding amounts of soil to erosion. World- Soil particles usually carry a negative charge, 2 of land (the area of USA wide, 11 million km which plays a critical role in delivering nutrient and Mexico combined) are affected by high rates cations (positively-charged ions) like Ca2 , þ ,K þ of erosion (Millennium Ecosystem Assessment þ , NH4 Na et al. to plants (Daily þ , and Mg2 þ 2005b). Every year about 75 billion tons of soil 1997). To deliver these nutrients without soil are thought to be eroded from terrestrial ecosys- would be exceedingly expensive as modern hy- 40 times faster than the average tems, at rates 13 – droponic (water-based) systems cost more than rate of soil formation (Pimentel and Kounang ’ sOf fi ce of Urban US$250 000 per ha (Canada et al. (1995) estimated that in the 1998). Pimentel Agriculture 2008; Avinash 2008). Soil is also criti- th century about a third of the second half of the 20 ltering and purifying water by removing cal in fi s arable land was lost to erosion. This ’ world contaminants, bacteria, and other impurities means losing vital harvests and income (Myers et al. (Fujii 2001). Soils harbor an astounding di- 1997), not to mention losing lives to malnutrition versity of microorganisms, including thousands and starvation. Soil is one of the most critical but of species of protozoa, antibiotic-producing bac- also most underappreciated and abused elements teria (which produce streptomycin) and fungi of natural capital, one that can take a few years to (producing penicillin), as well as myriad inverte- ’ lose and millennia to replace. A soil s character is brates, worms and algae (Daily et al. 1997). These determined by six factors: topography, the nature organisms play fundamental roles in decompos- of the parent material, the age of the soil, soil ing dead matter, neutralizing deadly pathogens, organisms and plants, climate, and human activi- and recycling waste into valuable nutrients. Just et al. 1997). For example, in the tropics, ty (Daily fi xed by soil organisms like the nitrogen © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

66 1 51 ECOSYSTEM FUNCTIONS AND SERVICES Rhizobium bacteria amounts to about 100 million 2003) can lessen wind ero- et al. practices (Gomes metric tons per year (Schlesinger 1991). It would cost sion substantially. Montane areas are especially at least US$320 billon/year to replace natural nitro- prone to rapid erosion (Milliman and Syvitski et al. 1997). gen fertilization with fertilizers (Daily 1992), and revegetation programs are critical in O(Nitrous ,N As the accelerating release of CO such ecosystems (Vanacker et al. 2007). Interest- 2 2 Oxide), methane and other greenhouse gases in- ingly, soil carbon buried in deposits resulting es climate (IPCC 2007), the soil s ’ creasingly modi fi from erosion, can produce carbon sinks that can capacity to store these molecules is becoming even offset up to 10% of the global fossil fuel emissions (Berhe et al. 2007). However, erosion also more vital. Per area, soil stores 1.8 times the carbon of CO 2 lowers soil productivity and reduces the organic and 18 times the nitrogen that plants alone can carbon returned to soil as plant residue (Gregor- store (Schlesinger 1991). For peatlands, soil carbon et al. 1998). Increasing soil carbon capacity by ich storage can be 10 times greater than that stored by 5 15% through soil-friendly tillage practices not – the plants growing on it and peatland fi res release into the atmosphere only offsets fossil-fuel carbon emissions by a massive amounts of CO 2 (Page and Rieley 1998). roughly equal amount but also increases crop s vital importance, 17% of the ’ Despite soil yields and enhances food security (Lal 2004). Earth ’ s vegetated land surface (Oldeman 1998) An increase of one ton of soil carbon pool in or 23% of all land used for food production degraded cropland soils may increase crop yield [FAO (Food and Agriculture Organization of the by 20 to 40 kilograms per ha (kg/ha) for wheat, United Nations) 1990] has experienced soil deg- 10 to 20 kg/ha for maize, and 0.5 to 1 kg/ha for radation since 1945. Erosion is the best-known cowpeas (Lal 2004). example of the disruption of the sedimentary cycle. Although erosion is responsible for releas- ing nutrients from bedrock and making them 3.4 Biodiversity and Ecosystem Function available to plants, excessive wind and water erosion results in the removal of top soil, the loss The role of biodiversity in providing ecosystem of valuable nutrients, and deserti fi cation. The di- services is actively debated in ecology. The diver- sity of functional groups (groups of ecologically rect costs of erosion total about US$250 billion per equivalent species (Naeem and Li 1997)), is as year and the indirect costs (e.g. siltation, obsoles- important as species diversity, if not more so (Kre- cence of dams, water quality declines) approxi- mately $150 billion per year (Pimentel et al . men 2005), and in most services a few dominant cient preventive measures would cost 1995). Suf fi et al. species seem to play the major role (Hooper 1995). et al. only 19% of this total (Pimentel 2005). However, many other species are critical The loss of vegetative cover increases the ero- for ecosystem functioning and provide “ insur- sional impact of rain. In intact forests, most rain against disturbance, environmental change, ” ance and the decline of the dominant species (Tilman water does not hit the ground directly and tree 2007). As for et al. 2004; Hobbs et al. 1997; Ricketts roots hold the soil together against being washed many other ecological processes, it was Charles away (Brauman 2007), better than in logged et al. forest or plantations (Myers 1997) where roads fi Darwin who rst wrote of this, noting that several can increase erosion rates (Bruijnzeel 2004). The distinct genera of grasses grown together would expansion of farming and deforestation have produce more plants and more herbage than a doubled the amount of sediment discharged single species growing alone (Darwin 1872). into the oceans. Coral reefs can experience high rmed that increased bio- fi Many studies have con diversity improves ecosystem functioning in mortality after being buried by sediment dis- plant communities (Naeem and Li 1997; Tilman fi charge (Pandol et al. 2003; Bruno and Selig 1997). Different plant species capture different 2007). Wind erosion can be particularly severe in desert ecosystems, where even small increases in resources, leading to greater ef fi ciency and higher vegetative cover (Hupy 2004) and reduced tillage 1996). Due to the et al. productivity (Tilman © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

67 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 52 Box 3.1 The costs of large mammal extinctions ‐ Robert M. Pringle When humans alter ecosystems, large mammals rst species to disappear. They are typically the fi are hunted for meat, hides, and horns; they are harassed and killed if they pose a threat; they require expansive habitat; and they are susceptible to diseases, such as anthrax, rinderpest, and distemper, that are spread by domestic animals. Ten thousand years ago, humans played at least a supporting, if not leading, role in extinguishing most of the large mammals in the Americas and Australia. Over the last 30 years, we have extinguished many mammal populations (and currently ‐ large the — threaten many more) in Africa and Asia two continents that still support diverse Box 3.1 Figure 1 , shown Peromyscus leucopus White-footed mice ( assemblages of these charismatic creatures. with an engorged tick on its ear) are highly competent reservoirs for Lyme The ecological and economic consequences disease. When larger mammals disappear, mice often thrive, increasing disease risk. Photograph courtesy of Richard Ostfeld Laboratory. of losing large ‐ mammal populations vary depending on the location and the ecological role of the species lost. The loss of carnivores has induced trophic cascades: in the absence of top predators, herbivores can multiply and deplete the plants, which in turn drives down the density and the diversity of other species (Ripple and Beschta 2006). Losing large herbivores and their predators can have the opposite effect, releasing plants and producing compensatory increases in the populations of smaller herbivores (e.g. rodents: Keesing 2000) and their predators (e.g. snakes: McCauley et al. 2006). Such increases, while not necessarily detrimental Box 3.1 Figure 2 Ecotourists gather around a pair of lions in themselves, can have unpleasant consequences ’ s Ngorongoro Crater. Ecotourism is one of the most Tanzania powerful driving forces for biodiversity conservation, especially in (see below). tropical regions where money is short. But tourists must be managed Many species depend on the activities of in such a way that they do not damage or deplete the very resources particular large mammal species. Certain they have traveled to visit. Photograph by Robert M. Pringle trees produce large fruits and seeds apparently adapted for dispersal by large browsers These examples and others suggest that the et al. 2008). Defecation by large (Guimarães loss of large mammals may precipitate mammals deposits these seeds and provides extinctions of other taxa and the relationships food for many dung beetles of varying degrees of among them, thus decreasing the diversity of specialization. In East Africa, the disturbance both species and interactions. Conversely, caused by browsing elephants creates habitat protecting the large areas needed to conserve dwelling lizards (Pringle 2008), while for tree ‐ large mammals may often serve to conserve the the total loss of large herbivores dramatically the greater diversity of smaller organisms — altered the character of an ant ‐ plant symbiosis via so ‐ called umbrella effect. a complex string of species interactions The potential economic costs of losing large et al. 2008). (Palmer mammals also vary from place to place. Because continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

68 1 53 ECOSYSTEM FUNCTIONS AND SERVICES (Continued) Box 3.1 could deal a crippling — rhinoceroses in Asia cattle do not eat many species of woody plants, blow to efforts to salvage the greater portion the loss of wildlife from rangelands can result in of biodiversity. bush encroachment and decreased pastoral tability. Because some rodents and their fi pro parasites are reservoirs and vectors of various REFERENCES human diseases, increases in rodent densities may increase disease transmission (Ostfeld and Guimarães, P. R. J., Galleti, M., and Jordano, P. (2008). Mills 2007; Box 3.1 Figure 1). Perhaps most Seed dispersal anachronisms: rethinking the fruits importantly, because large mammals form the extinct megafauna ate. PloS One , 3 , e1745. basis of an enormous tourism industry, the loss Keesing, F. (2000). Cryptic consumers and the ecology of of these species deprives regions of an , an African savanna. 50 , 205 BioScience 215. – important source of future revenue and foreign McCauley, D. J., Keesing, F., Young, T. P., Allan, B. F., and exchange (Box 3.1 Figure 2). Pringle, R. M. (2006). Indirect e ffects of large herbivores on Arguably, the most profound cost of losing , 2663. – , 2657 87 Ecology snakes in an African savanna. large mammals is the toll that it takes on our Ostfeld, R. S., and Mills, J. N. (2007). Social behavior, ability to relate to nature. Being large mammals borne pathogens. In J. O. demography, and rodent ‐ ourselves, we nd it easier to identify and fi Rodent societies , Wolff and P. W. Sherman, eds sympathize with similar species they behave — pp. 478 – 486. University of Chicago Press, Chicago, IL. “ in familiar ways, hence the term charismatic Palmer, T. M., Stanton, M. L., Young, T. P., et al. (2008). While only a handful of large ” megafauna. plant mutualism follows the loss of ‐ Breakdown of an ant mammal species have gone globally extinct in Science large mammals from an African savanna. , , 319 the past century, we are dismantling many 195. 192 – species population by population, pushing Pringle, R. M. (2008). Elephants as agents of habitat creation them towards extinction. At a time when we , 89 for small vertebrates at the patch scale. Ecology, desperately need to mobilize popular support 26 33. – for conservation, the loss over the next 50 years Ripple, W. J. and Beschta, R. L. (2006). Linking a cougar great apes — of even a few emblematic species catastrophic regime shift in decline, trophic cascade, and in central Africa, polar bears in the arctic, Biological Conservation Zion National Park. 133 , 397 , – 408. “ sampling-competition effect ” the presence of (Macarthur 1955; Hooper et al. 2005; Vitousek more species increases the probability of having and Hooper 1993; Worm 2006). et al. a particularly productive species in any given eld experiments have con- Greenhouse and fi environment (Tilman 1997). Furthermore, differ- fi rmed that biodiversity does increase ecosystem ent species ecologies lead to complementary re- ’ productivity, while reducing uctuations in pro- fl source use, where each species grows best under a 1996). et al. 1995; Tilman et al. ductivity (Naeem fi c range of environmental conditions, and speci Although increased diversity can increase the different species can improve environmental con- fl uctuations of individual species, di- population ditions for other species (facilitation effect; Hoop- versity is thought to stabilize overall ecosystem 2005). Consequently, the more complex an et al. er 2000; Tilman 1996) and et al. functioning (Chapin ecosystem is, the more biodiversity will increase make the ecosystem more resistant to perturba- ecosystem function, as more species are needed to tions (Pimm 1984). These hypotheses have been fully exploit the many combinations of environ- fi eld experiments, where species- con fi rmed in mental variables (Tilman 1997). More biodiverse rich plots showed less yearly variation in produc- ecosystems are also likely to be more stable and tivity (Tilman 1996) and their productivity during fi more ef cient due to the presence of more path- a drought year declined much less than species- ways for energy fl ow and nutrient recycling poor plots (Tilman and Downing 1994). Because © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

69 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 54 Box 3.2 Carnivore conservation Mark S. Boyce invariably swift and involves killing those Predation by carnivores can alter prey population abundance and distribution, and individuals responsible for the depredation, but furthermore such incidents of human these predator effects have been shown to fl ‐ in uence many aspects of community ecology. driven predation usually result in fear management actions that seldom consider the Examples include the effect of sea otters that kill and eat sea urchins reducing their cance of the carnivores in fi ecological signi abundance and herbivory on the kelp forests question. that sustain diverse near Another consideration that often plays a shore marine ‐ fi c. Likewise, major role in carnivore conservation is public communities of the North Paci subsequent to wolf (see Box 3.2 Figure) opinion. Draconian methods for predator control, including aerial gunning and poisoning recovery in Yellowstone National Park (USA), elk have become preferred prey of wolves of wolves by government agencies, typically erce public opposition. Yet, some meets with resulting in shifts in the distribution and fi abundance of elk that has released vegetation livestock ranchers and hunters lobby to have from ungulate herbivory with associated the carnivores eradicated. Rural people who increases in beavers, song birds, and other are at risk of depredation losses from carnivores plants and animals. usually want the animals controlled or Yet, carnivore conservation can be very eliminated, whereas tourists and broader challenging because the actions of carnivores publics usually push for protection of the often are resented by humans. Carnivores carnivores. depredate livestock or reduce abundance of Most insightful are programs that change human management practices to reduce the wildlife valued by hunters thereby coming into ict with humans. Some larger species fl direct con probability of con fl ict. Bringing cattle into of carnivores can prey on humans. Every year, areas where they can be watched during people are killed by lions in Africa, children are calving can reduce the probability that bears or killed by wolves in India, and people are killed or wolves will kill the calves. Ensuring that mauled by cougars and bears in western North garbage is unavailable to bears and other large carnivores reduces the risk that America (see also Box 14.3). Retaliation is carnivores will become habituated to humans and consequently come into con fl ict. Livestock ranchers can monitor their animals ‐ country areas and can dispose of in back dead animal carcasses to reduce the risk of depredation. Killing those individuals that are known to depredate livestock can be an effective approach because individuals sometimes learn to kill livestock whereas most carnivores in the population take only wild prey. Managing recreational access to selected trails and roads can be an effective tool for reducing con fl icts between large carnivores and people. Finding socially acceptable methods of predator control whilst learning to live in proximity with large carnivores is the key challenge for carnivore Canis lupus Grey wolf ( Box 3.2 Figure ). Photograph from www. all-about-wolves.com. conservation. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

70 1 55 ECOSYSTEM FUNCTIONS AND SERVICES Although it makes intuitive sense that the spe- more species do better at utilizing and recycling cies that dominate in number and/or biomass are nutrients, in the long-term, species-rich plots are more likely to be important for ecosystem func- better at reducing nutrient losses and maintain- 2004), in some tion (Raffaelli 2004; Smith et al. 1996; Vitousek and et al. ing soil fertility (Tilman cases, even rare species can have a role, for Hooper 1993). Box 3.3 Ecosystem services and agroecosystems in a landscape context Teja Tscharntke may encourage environment friendly Agroecosystems result from the transformation agriculture. This is why governments of natural ecosystems to promote ecosystem ecosystem service ‐ implement payment for ‐ fi ts people fi services, which are de ned as bene programs such as the agri ‐ environment obtain from ecosystems (MEA 2005). Major schemes in the European Community or the challenges in managing ecosystem services are oods on fl Chinese programs motivated by large that they are not independent of each other et al. the Yangtze River (Tallis 2008). and attempts to optimize a single service (e.g. In addition, conservation of most services reforestation) lead to losses in other services needs a landscape perspective. Agricultural (e.g. food production; Rodriguez et al. 2006). land use is often focused on few species and Agroecosystems such as arable elds and fi local processes, but in dynamic, human ‐ grasslands are typically extremely open dominated landscapes, only a diversity of ecosystems, characterized by high levels of insurance species may guarantee resilience, i.e. input (e.g. labour, agrochemicals) and output the capacity to re organize after disturbances ‐ (e.g. food resources), while agricultural (see Box 3.3 Figure). Biodiversity and associated management reduces structural complexity ecosystem services can be maintained only in and associated biodiversity. complex landscapes with a minimum of near ‐ s agroecosystems deliver a number ’ The world natural habitat (in central Europe roughly 20%) of key goods and services valued by society such supporting a minimum number of species fi as food, feed, bre, water, functional dispersing across natural and managed systems biodiversity, and carbon storage. These services 2005). For example, pollen (Tscharntke et al. ‐ may directly contribute to human well being, beetles causing economically meaningful for example through food production, or just damage in oilseed rape (canola) are naturally indirectly through ecosystem processes such as controlled by parasitic wasps in complex but natural biological control of crop pests ed landscapes. Similarly, high not in simpli fi (Tscharntke et al. 2007) or pollination of crops levels of pollination and yield in coffee and 2007). Farmers are mostly et al. (Klein interested in the privately owned, marketable pumpkin depend on a high diversity of bee goods and services, while they may also species, which is only available in produce public goods such as aesthetic heterogeneous environments. The landscape landscapes or regulated water levels. Finding context may be even more important for local ‐ win solutions that serve both private win biodiversity and associated ecosystem services economic gains in agroecosystems and public than differences in local management, for ‐ term conservation in agricultural long example between organic and conventional ‐ cult (but see Steffan fi landscapes is often dif fi elds with or without farming or between crop ‐ lasting Dewenter et al. 2007). The goal of long near ‐ natural fi eld margins, because the ecosystem services providing sustainable organisms immigrating into agroecosystems human well ‐ being may become compromised ‐ wide species pool may from the landscape by the short ‐ term interest of farmers in compensate for agricultural intensi fi cation at a increasing marketable services, but incentives 2005). local scale (Tscharntke et al. continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

71 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 56 Box 3.3 (Continued) Disturbance d) a) b Y a e) b) b Y complexity Number of species a Biological control Decreasing landscape f) c) b Y a Hypothesized responses to disturbance on ecosystem services such as biological control and pollination by native natural Box 3.3 Figure c) and recover of biological control and pollination after ‐ enemies and pollinators in different landscapes, showing how beta diversity (a disturbance (d ‐ f) change with landscape heterogeneity. Adapted from Tscharntke et al. (2007). a) and d) Intensely used monotonous landscape with a small available species pool, giving a low general level of ecosystem services, a greater dip in the service after a disturbance and an ecosystem that is unable to recover. b) and e) Intermediate landscape harboring slightly higher species richness, rendering deeper dip and slower return from a somewhat lower maximum level of biological control or pollination after a disturbance. c) and f) Heterogeneous landscape with large species richness, mainly due to the higher beta diversity, rendering high maximum level of the service, and low dip and quick return after a disturbance. high beta diversity coping with the spatial and The turnover of species among patches (the temporal heterogeneity in a real world under dissimilarity of communities creating high beta Global Change. level ‐ diversity, in contrast to the local, patch alpha diversity) is the dominant driver of wide biodiversity. Beta diversity ‐ landscape re fl ects the high spatial and temporal REFERENCES heterogeneity experienced by communities at a Klein, A. ‐ M., Vaissière, B. E., Cane. J. H., et al. (2007). landscape scale. Pollinator or biocontrol species Importance of pollinators in changing landscapes for thatdonot contribute tothe service inone patch Proceedings of the Royal Society of London world crops. may be important in other patches, providing , 274 – 313. , 303 B spatial insurance through complementary MEA (2005). Millenium Ecosystem Assessment. Island resource use (see Box 3.3 Figure). Sustaining Press, Washington, DC. ecosystem services in landscapes depends on a continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

72 1 57 ECOSYSTEM FUNCTIONS AND SERVICES (Continued) Box 3.3 practical conservation and economic development. Rodriguez, J. J., Beard, T. D. Jr, Bennett, E. M., et al. (2006). Proceedings of the National Academy of Sciences of the Trade ‐ offs across space, time, and ecosystem services. 105 United States of America , , 9457 – 9464. , Ecology and Society , 28 (online). 11 Tscharntke, T., Klein, A. ‐ Dewen- ‐ M., Kruess, A., Steffan Steffan ‐ Dewenter, I., Kessler, M., Barkmann, J., et al. ter, I, and Thies, C. (2005). Landscape perspectives on (2007). Tradeoffs between income, biodiversity, and ‐ agricultural intensi ecosystem fi cation and biodiversity ecosystem functioning during tropical rainforest con- Ecology Letters service management. – 874. , 8 , 857 version and agroforestry intensi fi cation. Proceedings of et al. Tscharntke, T., Bommarco, R., Clough, Y., (2007). the National Academy of Sciences of the United States Conservation biological control and enemy , 4973 104 , of America 4978 – diversity on a landscape scale. Biological Control , Tallis, H., Kareiva, P., Marvier, M., and Chang, A. (2008). 43 – 309. , 294 An ecosystem services framework to support both example, in increasing resistance to invasion increasingly vital over the entire range of habitats (Lyons and Schwartz 2001). A keystone species and systems, from diverse forest stands seques- et al. better in the long-term (Bolker is one that has an ecosystem impact that is dis- tering CO 2 et al. 1995; Hooper 2005; but see Tallis and Kar- proportionately large in relation to its abundance eiva 2006) to forest-dwelling native bees coffee ’ (Hooper et al. 1996; see Boxes 2005; Power et al. pollination services increasing coffee production 3.1, 3.2, and 5.3). Species that are not thought of as in Costa Rica (Ricketts . 2004; also see Box et al keystones can turn out to be so, some- ” typical “ 3.3). With accelerating losses of unique species, et al. 1993). times in more ways than one (Daily humanity, far from hedging its bets, is moving Even though in many communities only a few ever closer to the day when we will run out of species have strong effects, the weak effects of options on an increasingly unstable planet. many species can add up to a substantial stabiliz- effects over ing effect and seemingly “ weak ” broad scales can be strong at the local level (Ber- low 1999). Increased species richness can “ insure ” 3.5 Mobile Links against sudden change, which is now a global Mobile links ” are animal species that provide “ phenomenon (Parmesan and Yohe 2003; Root critical ecosystem services and increase ecosys- 2003). Even though a few species may et al. tem resilience by connecting habitats and ecosys- make up most of the biomass of most functional tems as they move between them (Gilbert 1980; groups, this does not mean that other species are Lundberg and Moberg 2003; Box 3.4). Mobile 1999). Species may act et al. unnecessary (Walker links are crucial for maintaining ecosystem func- like the rivets in an airplane wing, the loss of each tion, memory, and resilience (Nystrm and Folke unnoticed until a catastrophic threshold is passed 2001). The three main types of mobile links: ge- (Ehrlich and Ehrlich 1981b). netic, process, and resource links (Lundberg and s footprint on the planet increases As humanity ’ Moberg 2003), encompass many fundamental and formerly stable ecosystems experience con- ecosystem services (Sekercioglu 2006a, 2006b). stant disruptions in the form of introduced spe- Pollinating nectarivores and seed dispersing fru- cies (Chapter 7), pollution (Box 13.1), climate givores are genetic links that carry genetic mate- change (Chapter 8), excessive nutrient loads, rial from an individual plant to another plant or fi res (Chapter 9), and many other perturbations, to a habitat suitable for regeneration, respectively the insurance value of biodiversity has become © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

73 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 58 Box 3.4 Conservation of plant animal mutualisms ‐ Priya Davidar abioticmeansincreaseinthe community(Wright Plant ‐ animal mutualisms such as pollination 2007b). et al. and seed dispersal link plant productivity and Habitat fragmentation is another process that ow fl ecosystem functioning, and maintain gene can disrupt mutualistic interactions by reducing in plant populations. Insects, particularly bees, the diversity and abundance of pollinators and are the major pollinators of wild and crop seed dispersal agents, and creating barriers to plants worldwide, whereas vertebrates such as pollen and seed dispersal (Cordeiro and Howe birds and mammals contribute 2001, 2003; Aguilar 2006). et al. disproportionately to dispersal of seeds. About ‐ Plant animal mutualisms form webs or 1200 vertebrate and 100 000 invertebrate te to the maintenance of networks that contribu species are involved in pollination (Roubik biodiversity. Specialized interactions tend to be 1995; Buchmann and Nabhan 1996). Pollinators ed interactions where nested within generaliz are estimated to be responsible for 35% of generalists interact more with each other than by et al. 2007) and global crop production (Klein chance, whereas specialists interact with 90% of the reproduction of wild plants – for 60 generalists (Bascompte and Jordano 2006). 2007). It is estimated that feral et al. (Kremen Interactions are usually asymmetric, where one and managed honey bee colonies have partner is more dependent on the other thanvice ‐ declined by 25% in the USA since the 1990s, versa. These characteristics allow for the and globally about 200 species of wild persistence of rare specialist species. Habitat loss vertebrate pollinators might be on the verge of pters 4 and 5), hunting and fragmentation (Cha 1998). The et al. Wardell extinction (Allen ‐ (Chapter 6) and other factors can disrupt widespread decline of pollinators and mutualistic networks and result in loss of consequently pollination services is a cause for biodiversity. Models suggest that structured concern and is expected to reduce crop networks are less resilient to habitat loss than productivity and contribute towards loss of randomly generated communities (Fortuna and biodiversity in natural ecosystems (Buchmann Bascompte 2006). and Nabhan 1996; Kevan and Viana 2003). Therefore maintenance of contiguous forests Habitat loss, modi cation and the fi and intact functioning ecosystems is needed to indiscriminate use of pesticides are cited as sustain mutualistic interactions such as major reasons for pollinator loss (Kevan and pollination and seed dispersal. For agricultural Viana 2003). This alarming trend has led to the production, wild biodiversity needs to be International Initiative for the creation of an “ preserved in the surrounding matrix to Conservation and Sustainable use of promote native pollinators. ” as a key element under the Pollinators Convention on Biodiversity, and the International Union for the Conservation of REFERENCES Nature has a task force on declining pollination in the Survival Service Commission. Aguilar, R., Ashworth, L., Galetto, L., and Aizen, M. A. Frugivores tend to be less specialized than (2006). Plant reproductive susceptibility to habitat frag- pollinatorssincemanyanimalsincludesomefruit mentation: review and synthesis through a meta ‐ analy- in their diet (Wheelwright and Orians 1982). 9 Ecology Letters 980. – , 968 sis. Decline of frugivores from overhunting and loss et al. (1998). Allen ‐ Wardell, G., Bernhardt, P., Bitner, R., of habitat, can affect forest regeneration The potential consequences of pollinator declines on the 2007a). Hunting pressure (Wright et al. conservation of biodiversity and stability of food crop differentially affects recruitment of species, , ,8 – 17. 12 Conservation Biology yields. where seeds dispersed by game animals Bascompte, J. and Jordano, P. (2006). The structure of game animals and by decrease, and small non ‐ animal mutualistic networks. In M. Pascual and ‐ plant continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

74 1 59 ECOSYSTEM FUNCTIONS AND SERVICES (Continued) Box 3.4 world crops. Proceedings of the Royal Society of London J. Dunne, eds Ecological networks , pp. 143 – 159. Oxford , – B 274 , 303 313. University Press, Oxford, UK. Kremen, C., Williams, N. M., Aizen, M. A., (2007). et al. Buchmann, S. L. and Nabhan, G. P. (1996). The forgotten Pollination and other ecosystem services produced by pollinators . Island Press, Washington, DC. mobile organisms: a conceptual framework for the Cordeiro, N. J. and Howe, H. F. (2001). Low recruitment of use change. effects of land 314. – , 299 ‐ Ecology Letters , 10 trees dispersed by animals in African forest fragments. Roubik, D. W. (1995). Pollination of cultivated plants in the , 1733 15 , Conservation Biology – 1741. tropics . Bulletin 118. FAO, Rome, Italy. Cordeiro, N. J. and Howe, H. F. (2003). Forest fragmenta- Wheelwright, N. T. and Orians, G. H. (1982). Seed dispersal tion severs mutualism between seed dispersers and an by animals: contrasts with pollen dispersal, problems of Proceedings of the National endemic African tree. terminology, and constraints on coevolution. American Academy of Sciences of the United States of America , – , 402 119 , Naturalist 413. 100 , 14052 14056. – Wright, S. J., Hernandez, A., and Condit, R. (2007a). The Fortuna, M. A. and Bascompte, J. (2006). Habitat loss and bushmeat harvest alters seedling banks by favoring ‐ animal mutualistic networks. the structure of plant lianas, large seeds and seeds dispersed by bats, birds 9 , 281 , Ecology Letters – 286. 371. , , 363 Biotropica and wind. – 39 Kevan, P. G. and Viana, B. F. (2003). The global decline of (2007b). The Wright, S. J., Stoner, K. E., Beckman, N., et al. Biodiversity 8. – ,3 4 , pollination services. plight of large animals in tropical forests and the conse- et al. (2007). Klein, A ‐ M., Vaissiere, B. E., Cane, J. H., Biotropica quencesforplantregeneration. Importance of pollinators in changing landscapes for 291. , 39 ,289 – (Box 3.4). Trophic process links are grazers, such uence one another (Lundberg and Moberg fl in as antelopes, and predators, such as lions, bats, 2003). The long-distance migrations of many and birds of prey that in fl uence the populations species, such as African antelopes, songbirds, of plant, invertebrate, and vertebrate prey (Boxes ) waterfowl, and gray whales ( Eschrichtius robustus 3.1 and 3.2). Scavengers, such as vultures, are are particularly important examples of critical crucial process links that hasten the decomposi- mobile links. However, many major migrations tion of potentially disease-carrying carcasses are disappearing (Wilcove 2008) and nearly (Houston 1994). Predators often provide natural two hundred migratory bird species are threatened pest control (Holmes 1979). Many animals, et al. or near threatened with extinction (Sekercioglu such as fi sh-eating birds that nest in colonies, are 2007). resource links that transport nutrients in their Dispersing seeds is among the most important fi cant re- droppings and often contribute signi functions of mobile links. Vertebrates are the main sources to nutrient-deprived ecosystems (Ander- seed vectors for fl owering plants (Regal 1977; Tiff- son and Polis 1999). Some organisms like ney and Mazer 1995), particularly woody species woodpeckers or beavers act as physical process (Howe and Smallwood 1982; Levey et al. 1994; linkers or et al. (Jones ” ecosystem engineers “ Jordano 2000). This is especially true in the tropics fl ooding large 1994). By building dams and where bird seed dispersal may have led to the areas, beavers engineer ecosystems, create new emergence of owering plant dominance (Regal fl wetlands, and lead to major changes in species 1977; Tiffney and Mazer 1995). Seed dispersal is composition (see Chapter 6). In addition to con- thought to bene fi t plants in three major ways suming insects (trophic linkers), many wood- (Howe and Smallwood 1982): peckers also engineer their environment and Escape from density-dependent mortality caused build nest holes later used by a variety of other · by pathogens, seed predators, competitors, and her- 1993). Through mobile links, species (Daily et al. bivores (Janzen-Connell escape hypothesis). distant ecosystems and habitats are linked to and © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

75 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 60 Chance colonization of favorable but unpredict- owering plant species and three fl s ’ the world · able sites via wide dissemination of seeds. quarters of food crops (Nabhan and Buchmann c sites that are partic- fi Directed dispersal to speci 1997), are the most important group of pollina- · ularly favorable for establishment and survival. tors (Box 3.3). In California alone, their services are estimated to be worth $4.2 billion (Brauman Although most seeds are dispersed over short and Daily 2008). However, bee numbers world- distances, long-distance dispersal is crucial (Cain wide are declining (Nabhan and Buchmann 1997) et al. 2000), especially over geological time scales (Box 3.5). In addition to the ubiquitous European during which some plant species have been calcu- ), native bee species that Apis mellifera honeybee ( lated to achieve colonization distances 20 times depend on natural habitats also provide valuable higher than would be possible without vertebrate fi ed by Costa Rican services to farmers, exempli et al. 2000). Seed dispersers seed dispersers (Cain forest bees whose activities increase coffee yield play critical roles in the regeneration and restora- by 20% near forest fragments (Ricketts et al . 2004). tion of disturbed and degraded ecosystems (Wun- Some plant species mostly depend on a single derle 1997; Chapter 6), including newly-formed 1993) or a few (Rathcke 2000) pollinator et al. (Parra volcanic soils (Nishi and Tsuyuzaki 2004). species. Plants are more likely to be pollinator-lim- Plant reproduction is particularly pollination- et al. 2004) and a ited than disperser-limited (Kelly limited in the tropics relative to the temperate survey of pollination experiments for 186 species zone (Vamosi et al. 2006) due to the tropics great- showed that about half were pollinator-limited er biodiversity, and up to 98% of tropical rain- (Burd 1994). Compared to seed dispersal, pollina- forest trees are pollinated by animals (Bawa tion is more demanding due to the faster ripening 1990). Pollination is a critical ecosystem function 2004). et al. owers (Kelly fl rates and shorter lives of for the continued persistence of the most biodi- Seed disperser and pollinator limitation are often verse terrestrial habitats on Earth. Nabhan and more important in island ecosystems with fewer Buchmann (1997) estimated that more than 1200 species, tighter linkages, and higher vulnerability vertebrate and about 289 000 invertebrate species to disturbance and introduced species. Island plant fl owering are involved in pollinating over 90% of species are more vulnerable to the extinctions of plant species (angiosperms) and 95% of food their pollinators since many island plants have lost crops. Bees, which pollinate about two thirds of Box 3.5 Consequences of pollinator decline for the global food supply Claire Kremen extreme risk of relying on a single pollinator to Both wild and managed pollinators have s crop species. ’ provide services for the world cant declines in recent years. suffered signi fi ve percent of globally important fi Seventy ‐ Managed , the most important Apis mellifera crops rely on animal pollinators, providing up source of pollination services for crops around to 35% of crop production (Klein 2007). et al. the world, have been diminishing around the At the same time, although records are sorely globe (NRC 2006), particularly in the US where lacking for most regions, comparisons of recent colony numbers are now at < 50% of their 1950 ‐ 1980) records have with historical (pre levels. In addition, major and extensive colony cant regional declines in species fi indicated signi losses have occurred over the past several years richness of major pollinator groups (bees and in North America and Europe, possibly due to hover fl ies in Britain; bees alone in the Foster ‐ diseases as well as other factors (Cox et al. 2006). Large Netherlands) (Biesmeijer et al. 2007; Stokstad 2007), causing shortages reductions in species richness and abundance of and rapid increases in the price of pollination bees have also been documented in regions of services (Sumner and Boriss 2006). These recent s ’ high agricultural intensity in California trends in honey bee health illustrate the continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

76 1 61 ECOSYSTEM FUNCTIONS AND SERVICES Box 3.5 (Continued) reasons, we may indeed face more serious 2002; Klein and Central Valley (Kremen et al. shortages of pollinators in the future. Kremen unpublished data). Traits associated A recent, carefully analyzed, global assessment fl y declines in with bee, bumble bee and hover of the economic impact of pollinator loss (e.g. fl Europe included oral specialization, slower total loss of pollinators worldwide) estimates our (univoltine) development and lower dispersal vulnerability (loss of economic value) at Euro 153 ‐ et al. (non migratory) species (Biesmeijer 2006; billion or 10% of the total economic value of Goulson 2008). Specialization is also et al. 2009). et al. annual crop production (Gallai indicated as a possible correlate of local Although total loss of pollination services is both extinction in pollinator communities studied unlikely to occur and to cause widespread famine across a disturbance gradient in Canada; if it were to occur, it potentially has both serious communities in disturbed habitat contained economic and human health consequences. For fi cantly more generalized species than signi s of the world produce example, some region those associated with pristine habitats (Taki bodied bees were more ‐ and Kevan 2007). Large s pollinator ’ large proportions of the world ‐ sensitive to increasing agricultural dependent crops — such regions would s Central Valley, ’ cation in California fi intensi experience more severe economic consequences ‐ visit and ominously, bees with the highest per from the loss of pollinators, although growers pollination ef ciencies were also most likely to fi and industries would undoubtedly quickly go locally extinct with agricultural respond to these changes in a variety of ways et al. 2005). intensi cation (Larsen fi passing the principle economic burden on to Thus, in highly intensive farming regions, consumers globally (Southwick and Southwick such as California s Central Valley, that ’ et al. 2009). Measures of the impacts 1992; Gallai contribute comparatively large amounts to on consumers (consumer surplus) are of the same global food production (e.g. 50% of the world – 310 billion based order of magnitude (Euro 195 supply of almonds), the supply of native bee on reasonable estimates for price elasticities, pollinators is lowest in exactly the regions 2009) as the impact on total economic et al. Gallai where the demand for pollination services is value of crop production. Nutritional et al. 2002) and highest. Published (Kremen fi xed and more consequences may be more recent studies (Klein et al. unpublished data) serious than economic consequences, due to the clearly show that the services provided by wild ses to economic change. likely plasticity of respon bee pollinators are not suf cient to meet the fi Pollinator ‐ dependent crop species supply not only demand for pollinators in these intensive up to 35% of crop production by weight (Klein regions; such regions are instead entirely 2007), but also provide essential vitamins, et al. reliant on managed honey bees for pollination fi nutrients and ber for a healthy diet and provide services. If trends towards increased et al. et al. 2009; Kremen diet diversity (Gallai cation continue elsewhere fi agricultural intensi 2007). The nutritional consequences of total 2006), then et al. (e.g. as in Brazil, Morton pollinator loss for human health have yet to be pollination services from wild pollinators are ed; however food recommendations for fi quanti highly likely to decline in other regions minimal daily portions of fruits and vegetables et al. 2008). At the same time, global (Ricketts known and already often not met in ‐ are well food production is shifting increasingly towards diets of both developed and underdeveloped dependent foods production of pollinator ‐ countries. 2008), increasing our need for et al. (Aizen managed and wild pollinators yet further. REFERENCES ‐ Global warming, which could cause mis matches between pollinators and the plants Aizen, M. A., Garibaldi, L. A., Cunningham, S. A., and they feed upon, may exacerbate pollinator Klein, A. M. (2008). Long ‐ term global trends in crop et al. decline (Memmott 2007). For these yield and production reveal no current pollination continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

77 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 62 (Continued) Box 3.5 Memmott, J., Craze, P. G., Waser, N. M., and Price, shortage but increasing pollinator dependency. Current 18 , 1572 – 1575. Biology , M. V. (2007). Global warming and the disruption (2006). Biesmeijer, J. C., Roberts, S. P. M., Reemer, M., et al. of plant , Ecology Letters pollinator interactions. ‐ ‐ Parallel declines in pollinators and insect pollinated plants in 10 – 717. , 710 Britain and the Netherlands. 354. – 313 , ,351 Science , et al. Morton, D. C., DeFries, R. S., Shimabukuro, Y. E., (2007). et al. Foster, D. L., Conlan, S., Holmes, E. C., Cox ‐ (2006). Cropland expansion changes deforestation dy- A metagenomic survey of microbes in honey bee colony namics in the southern Brazilian Amazon. Proceedings 318 , 287. collapse disorder. – , 283 Science of the National Academy of Sciences of the United ‐ M., Settele, J., and Vaissière, B. E. Gallai, N., Salles, J. 14641. – , 14637 103 , States of America (2009). Economic valuation of the vulnerability of world NRC (National Research Council of the National agriculture confronted with pollinator decline. Ecologi- Status of Pollinators in North Academies) (2006). , 810 cal Economics 821. – 68 , . National Academy Press, America Goulson, D., Lye, G. C., and Darvill, B. (2008). Decline and Washington, DC. Annual Review of Ento- conservation of bumblebees. Ricketts, T. H., Regetz, J., Steffan et al. ‐ Dewenter, I., , 53 , 191 mology 208. – (2008) Landscape effects on crop pollination services: et al. Klein, A. M., Vaissièrie, B., Cane, J. H., (2007). are there general patterns? , Ecology Letters Importance of crop pollinators in changing landscapes , 499 11 515. – Proceedings of the Royal Society of for world crops. Southwick, E. E. and Southwick, L. Jr. (1992). Estimating the 274 313. – , 303 , London B economic value of honey bees (Hymenoptera: Apidae) as Kremen,C.,Williams,N.M.,andThorp,R.W.(2002).Crop Journal of agricultural pollinators in the United States. isk from agricultural inten- pollination from native bees at r 633. ,621 – , Economic Entomology 85 si fi cation. Proceedings of the National Academy of Sciences Stokstad, E. (2007). The case of the empty hives. Science , – , 16812 99 16816. , of the United States of America 972. – , 970 316 et al. Kremen, C., Williams, N. M., Aizen, M. A., (2007). conomics and the ‐ Sumner, D. A. and Boriss, H. (2006). Bee Pollination and other ecosystem services produced by Giannini Foundation of Agricul- leap in pollination fees. mobile organisms: a conceptual framework for the tural Economics Update , 9 ,9 – 11. Ecology Letters , 10 , 299314. ‐ effects of land use change. Taki, H. and Kevan, P. G. (2007). Does habitat loss Larsen, T. H., Williams, N. M., and Kremen, C. (2005). Extinc- affect the communities of plants and insects equally tion order and altered communi ty structure rapidly disrupt ndings. in plant ‐ pollinator interactions? Preliminary fi 8 , Ecology Letters ecosystem functioning. ,538 547. – Biodiversity and Conservation , 16 – , 3147 3161. their ability to self-pollinate and have become 1989). In the US et al. crops every year (Pimentel completely dependent on endemic pollinators alone, despite the US$25 billion spent on pesticides (Cox and Elmqvist 2000). Pollination limitation annually (Naylor and Ehrlich 1997), pests destroy due to the reduced species richness of pollinators 37% of the potential crop yield (Pimentel et al. on islands like New Zealand and Madagascar (Far- 1997). However, many pests have evolved resis- et al. 2004) can signi fi cantly reduce fruit sets wig tance to the millions of tons of synthetic pesticide and probably decrease the reproductive success of sprayed each year (Pimentel and Lehman 1993), dioecious plant species. largely due to insects ’ short generation times and Predators are important trophic process links their experience with millions of years of coevolu- and can control the populations of pest species. tion with plant toxins (Ehrlich and Raven 1964). For millennia, agricultural pests have been compet- Consequently, these chemicals poison the environ- ing with people for the food and ber plants that fi ment (Carson 1962), lead to thousands of wildlife feed and clothe humanity. Pests, particularly her- fatalities every year, and by killing pests natural ’ s 50% of humanity ’ bivorous insects, consume 25 – enemies faster than the pests themselves, often lead © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

78 1 63 ECOSYSTEM FUNCTIONS AND SERVICES to the emergence of new pest populations (Naylor (Prakash et al. 2003) and where vultures contrib- and Ehrlich 1997). As a result, the value of natural ute to human and ecosystem health by getting rid pest control has been increasingly recognized of refuse (Pomeroy 1975), feces (Negro 2002), et al. worldwide, some major successes have been 2003). and dead animals (Prakash et al. achieved, and natural controls now form a core Mobile links also transport nutrients from one “ integrated pest management component of ” habitat to another. Some important examples are (IPM) that aims to restore the natural pest-predator geese transporting terrestrial nutrients to wetlands balance in agricultural ecosystems (Naylor and et al. (Post 1998) and seabirds transferring marine Ehrlich 1997). productivity to terrestrial ecosystems, especially in Species that provide natural pest control range coastal areas and unproductive island systems from bacteria and viruses to invertebrate and (Sanchez-pinero and Polis 2000). Seabird drop- vertebrate predators feeding on insect and rodent pings (guano) are enriched in important plant nu- 2004; Seker- et al. pests (Polis 2000; Perfecto et al. trients such as calcium, magnesium, nitrogen, cioglu 2006b). For example, a review by Holmes phosphorous, and potassium (Gillham 1956). Mur- (1990) showed that reductions in moth and but- phy (1981) estimated that seabirds around the 5 4 to 10 tons of phosphorous y populations due to temperate forest birds fl ter world transfer 10 from sea to land every year. Guano also provides 70% at low insect densi- was mostly between 40 – an important source of fertilizer and income to 60% at intermediate densities, and 0 10% – ties, 20 – many people living near seabird colonies. at high densities. Although birds are not usually Scavengers and seabirds provide good exam- thought of as important control agents, avian ples of how the population declines of ecosystem control of insect herbivores and consequent re- service providers lead to reductions in their ser- ductions in plant damage can have important vices (Hughes et al. 1997). Scavenging and sh- fi economic value (Mols and Visser 2002). Take- eating birds comprise the most threatened avian kawa and Garton (1984) calculated avian control functional groups, with about 40% and 33%, re- of western spruce budworm in northern Wa- spectively, of these species being threatened or shington State to be worth at least US$1820/ 2 /year. To make Beijing greener for the 2008 near threatened with extinction (Sekercioglu km Olympics without using chemicals, entomolo- et al. 2004). The large declines in the populations gists reared four billion parasitic wasps to get of many scavenging and fi sh-eating species mean rid of the defoliating moths in less than three that even if none of these species go extinct, their months (Rayner 2008). Collectively, natural ene- services are declining substantially. Seabird losses mies of crop pests may save humanity at least US can trigger trophic cascades and ecosystem shifts $54 billion per year, not to mention the critical (Croll et al. 2005). Vulture declines can lead to the importance of natural controls for food security emergence of public health problems. In India, and human survival (Naylor and Ehrlich 1997). Gyps vulture populations declined as much as Promoting natural predators and preserving their 2003). Vultures et al. 99% in the 1990s (Prakash native habitat patches like hedgerows and forests compete with feral dogs, which often carry rabies. may increase crop yields, improve food security, As the vultures declined between 1992 and 2001, and lead to a healthier environment. the numbers of feral dogs increased 20-fold at a Often underappreciated are the scavenging 2003). Most et al. garbage dump in India (Prakash and nutrient deposition services of mobile links. ’ of world s rabies deaths take place in India (World Scavengers like vultures rapidly get rid of rotting Health Organization 1998) and feral dogs replacing carcasses, recycle nutrients, and lead other ani- vultures is likely to aggravate this problem. mals to carcasses (Sekercioglu 2006a). Besides Mobile links, however, can be double-edged their ecological signi cance, vultures are particu- fi swords and can harm ecosystems and human po- larly important in many tropical developing pulations, particularly in concert with human countries where sanitary waste and carcass dis- related poor land-use practices, climate change, posal programs may be limited or non-existent and introduced species. Invasive plants can spread © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

79 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 64 via native and introduced seed dispersers (Larosa traditional, rural communities to urban areas, and 1985; Cordeiro et al. 2004). Land use change et al. disappearing cultures and languages mean that the can increase the numbers of mobile links that dam- priceless ethnobotanical knowledge of many cul- age distant areas, such as when geese overload tures is rapidly disappearing in parallel with the et al. wetlands with excessive nutrients (Post impending extinctions of many medicinal plants 1998). Climate change can lead to asynchronies in due to habitat loss and overharvesting (Millenni- insect emergence and their predators timing of um Ecosystem Assessment 2005a). Some of the et al. 2006), and in fl breeding (Both owering and rainforest areas that are being deforested fastest, their pollinators lifecycles (Harrington 1999) et al. like the island of Borneo, harbor plant species that (Chapter 8). produce active anti-HIV (Human Immunode fi - Mobile links are often critical to ecosystem func- ciency Virus) agents (Chung 1996; Jassim and that pro- “ tioning as sources of external memory ” Naji 2003). Doubtlessly, thousands more useful mote the resilience of ecosystems (Scheffer et al. and vital plant compounds await discovery in the 2001). More attention needs to be paid to mobile forests of the world, particularly in the biodiverse links in ecosystem management and biodiversity tropics (Laurance 1999; Sodhi et al. 2007). However, conservation (Lundberg and Moberg 2003). This is without an effective strategy that integrates com- especially the case for migrating species that face munity-based habitat conservation, rewarding countless challenges during their annual migra- of local ethnobotanical knowledge, and scienti c fi tions that sometimes cover more than 20 000 kilo- research on these compounds, many species, the meters (Wilcove 2008). Some of the characteristics local knowledge of them, and the priceless cures that make mobile links important for ecosystems, they offer will disappear before scientists discover such as high mobility and specialized diets, also them. make them more vulnerable to human impact. As with many of nature s services, there is a fl ip ’ Protecting pollinators, seed dispersers, predators, side to the medicinal bene ts of biodiversity, fi scavengers, nutrient depositors, and other mobile namely, emerging diseases ( Jones 2008). et al. links must be a top conservation priority to prevent The planet s organisms also include countless ’ collapses in ecosystem services provided by these diseases, many of which are making the transi- vital organisms (Boxes 3.1 3.5). – tion to humans as people increasingly invade the habitats of the hosts of these diseases and con- sume the hosts themselves. Three quarters of human diseases are thought to have their origins s Cures versus Emerging ’ 3.6 Nature in domestic or wild animals and new diseases are Diseases emerging as humans increase their presence in While many people know about how plants pre- formerly wilderness areas (Daily and Ehrlich vent erosion, protect water supplies, and “ clean the et al 1996; Foley . 2005). Some of the deadliest , how bees pollinate plants or how owls reduce air ” diseases, such as monkeypox, malaria, HIV and rodent activity, many lesser-known organisms not Ebola, are thought to have initially crossed from only have crucial ecological roles, but also produce central African primates to the people who unique chemicals and pharmaceuticals that can hunted, butchered, and consumed them (Hahn s lives. Thousands of plant ’ literally save people 2005; Rich et al. . 2009). et al et al. 2000; Wolfe species are used medically by traditional, indige- Some diseases emerge in ways that show the ’ nous communities worldwide. These peoples eth- dif fi culty of predicting the consequences of dis- nobotanical knowledge has led to the patenting, by turbing ecosystems. The extensive smoke from pharmaceutical companies, of more than a quarter – 1998 forest fi res in Southeast the massive 1997 of all medicines (Posey 1999), although the indige- Asia is thought to have led to the fruiting failure nous communities rarely bene fi t from these pa- of many forest trees, forcing frugivorous bats to tents (Mgbeoji 2006). Furthermore, the eroding of switch to fruit trees in pig farms. The bats, which traditions worldwide, increasing emigration from host the Nipah virus, likely passed it to the pigs, © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

80 1 65 ECOSYSTEM FUNCTIONS AND SERVICES from which the virus made the jump to people Collectively, the conditions leading to and result- (Chivian 2002). Another classic example from ing from tropical deforestation, combined with Southeast Asia is the Severe Acute Respiratory climate change, human migration, agricultural Syndrome (SARS). So far having killed 774 peo- cking create the intensi fi cation, and animal traf fi ple, the SARS coronavirus has been recently dis- perfect storm for the emergence of new diseases covered in wild animals like the masked palm as well as the resurgence of old ones. In the face of ) and raccoon dog ( Paguma larvata civet ( Nyctereu- rapid global change, ecologically intact and rela- teus procyonoides ) that are frequently consumed tively stable communities may be our best weap- . 2003). SARS- by people in the region (Guan et al on against the emergence of new diseases. like coronaviruses have been discovered in bats . 2005) and the virus was probably passed et al (Li to civets and other animals as they ate fruits 3.7 Valuing Ecosystem Services partially eaten and dropped by those bats (Jamie Ecosystems and their constituent species provide H. Jones, personal communication). It is probable an endless stream of products, functions, and ser- fi that SARS made the nal jump to people through vices that keep our world running and make our such animals bought for food in wildlife markets. existence possible. To many, even the thought of The recent emergence of the deadly avian in fl u- putting a price tag on services like photosynthesis, enza strain H5N1 provides another good example. puri cation of water, and pollination of food crops fi Even though there are known to be at least 144 may seem like hubris, as these are truly priceless fl u, only a few strains kill people. strains of avian services without which not only humans, but most However, some of the deadliest pandemics have of lifewould perish.A distinguished economistput been among these strains, including H1N1, H2N, it best in response to a seminar at the USA Federal and H3N2 (Cox and Subbarao 2000). H5N1, the Trade Commission, where the speaker down- cause of the recent bird fl u panic, has a 50% fatality played the impact of global warming by saying rate and may cause another human pandemic. agriculture and forestry “ accounted for only three At low host densities, viruses that become too .Theecon- ” percentoftheUSgrossnationalproduct deadly, fail to spread. It is likely that raising do- omist ’ s response was: “ What does this genius think mestic birds in increasingly higher densities led to (Naylor and Ehrlich 1997). we ’ re going to eat? ” the evolution of higher virulence in H5N1, as it Nevertheless, in our nancially-driven world, fi became easier for the virus to jump to another we need to quantify the trade-offs involved in host before it killed its original host. There is also land use scenarios that maximize biodiversity con- a possibility that increased invasion of wilderness servation and ecosystem services versus scenarios areas by people led to the jump of H5N1 from wild that maximize pro fi t from a single commodity. birds to domestic birds, but that is yet to be proven. Without such assessments, special interests repre- Malaria, recently shown to have jumped from senting single objectives dominate the debate and chimpanzees to humans (Rich et al . 2009), is per- sideline the integration of ecosystem services into haps the best example of a resurging disease that et al the decision-making process (Nelson . 2009). increases as a result of tropical deforestation Valuing ecosystem services is not an end in itself, . 2005; Ya- (Singer and Castro 2001; Foley et al rst step towards integrating these ser- fi but is the suoka and Levins 2007). Pearson (2003) calculat- vices into public decision-making and ensuring the ed that every 1% increase in deforestation in the continuity of ecosystems that provide the services Amazon leads to an 8% increase in the population (Goulder and Kennedy 1997; National Research of the malaria vector mosquito ( Anopheles dar- Council 2005; Daily et al. 2009). Historically, eco- lingi ). In addition, some immigrants colonizing system services have been mostly thought of as deforested areas brought new sources of malaria free public goods, an approach which has too fre- (Moran 1988) whereas other immigrants come quently led to the “ tragedy of the commons ” from malaria-free areas and thus become ideal where vital ecosystem goods like clean water hosts with no immunity (Aiken and Leigh 1992). © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

81 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 66 have been degraded and consumed to extinction versity they harbor, and the services they collec- (Daily 1997). Too often, ecosystem services have tively provide are truly priceless, market-based been valued, if at all, based on “ marginal utility ” and other quantitative approaches for valuing (Brauman and Daily 2008). When the service (like fi le of nat- ecosystem services will raise the pro clean water) is abundant, the marginal utility of one s services in the public consciousness, inte- ’ ure additional unit can be as low as zero. However, as grate these services into decision-making, and the service becomes more scarce, the marginal utility help ensure the continuity of ecosystem contribu- of each additional unit becomes increasingly valu- tions to the healthy functioning of our planet and able (Goulder and Kennedy 1997). Using the mar- its residents. ginal value for a service when it is abundant drastically underestimates the value of the service as it becomes scarcer. As Benjamin Franklin wryly Summary ’ s dry, we know the worth observed, “ When the well Ecosystem services are the set of ecosystem func- ” of water. · tions that are useful to humans. As the societal importance of ecosystem services These services make the planet inhabitable by becomes increasingly appreciated, there has been · supplying and purifying the air we breathe and the a growing realization that successful application water we drink. of this concept requires a skilful combination of Water, carbon, nitrogen, phosphorus, and sulfur biological, physical, and social sciences, as well as · are the major global biogeochemical cycles. Disrup- the creation of new programs and institutions. The oods, droughts, tions of these cycles can lead to fl fi c community needs to help develop the scienti climate change, pollution, acid rain, and many other necessary quantitative tools to calculate the value environmental problems. of ecosystem services and to present them to the Soils provide critical ecosystem services, especial- et al. 2009). A promising decision makers (Daily · ly for sustaining ecosystems and growing food example is the InVEST (Integrated Valuation of crops, but soil erosion and degradation are serious Ecosystem Services and Tradeoffs) system problems worldwide. 2009; Nelson 2009) developed by the et al. (Daily Higher biodiversity usually increases ecosystem Natural Capital Project (www.naturalcapital.org; · ef fi ciency and productivity, stabilizes overall eco- see Box 15.3). However, good tools are valuable system functioning, and makes ecosystems more fi cult goal is only if they are used. A more dif resistant to perturbations. convincing the private and public sectors to Mobile link animal species provide critical eco- incorporate ecosystem services into their deci- · system functions and increase ecosystem resilience sion-making processes (Daily et al. 2009). Never- by connecting habitats and ecosystems through theless, with the socio-economic impacts and their movements. Their services include pollination, human costs of environmental catastrophes, seed dispersal, nutrient deposition, pest control, and such as Hurricane Katrina, getting bigger and scavenging. more visible, and with climate change and related Thousands of species that are the components of carbon sequestration schemes having reached · ecosystems harbor unique chemicals and pharma- a prominent place in the public consciousness, ceuticals that can save people s lives, but traditional ’ the value of these services and the necessity of knowledge of medicinal plants is disappearing and maintaining them has become increasingly main- many potentially valuable species are threatened stream. with extinction. Recent market-based approaches such as pay- Increasing habitat loss, climate change, settle- ments for Costa Rican ecosystem services, wet- · ment of wild areas, and wildlife consumption facili- land mitigation banks, and the Chicago Climate tate the transition of diseases of animals to humans, Exchange have proven useful in the valuation of and other ecosystem alterations are increasing the ecosystem services (Brauman and Daily 2008). prevalence of other diseases. Even though the planet s ecosystems, the biodi- ’ Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

82 1 67 ECOSYSTEM FUNCTIONS AND SERVICES Valuation of ecosystem services and tradeoffs Bawa, K. S. (1990). Plant-pollinator interactions in Tropical · Rain-Forests. , Annual Review of Ecology and Systematics helps integrate these services into public decision- 21 , 399 – 422. making and can ensure the continuity of ecosystems Berhe, A. A., Harte, J., Harden, J. W., and Torn, M. S. that provide the services. fi cance of the erosion-induced terrestrial (2007). The signi carbon sink. BioScience , 57 , 337 – 46. Berlow, E. L. (1999). Strong effects of weak interactions in 398 ecological communities. Nature , 34. – , 330 Relevant websites The major biogeochemi- Bolin, B. and Cook, R. B., eds (1983). Millennium Ecosystem Assessment: http://www.mil- . Wiley, New York. cal cycles and their interactions · lenniumassessment.org/ Bolker, B.M., Pacala, S. W., Bazzaz, F. A., Canham, C.D., and Intergovernmental Panel on Climate Change: http:// Levin, S. A. (1995). Species diversity and ecosystem re- · www.ipcc.ch/ sponse to carbon dioxide fertilization: conclusions from a Ecosystem Marketplace: http://www.ecosystemmar- ,373 Global Change Biology temperate forest model. , 1 381. – · ketplace.com/ Both, C., Bouwhuis, S., Lessells, C. M., and Visser, M. E. United States Department of Agriculture, Forest Service (2006). Climate change and population declines in a · Website on Ecosystem Services: http://www.fs.fed.us/ 83. – ,81 long-distance migratory bird. Nature , 441 ecosystemservices/ Bradshaw, C. J. A., Sodhi, N. S., Peh, K. S.-H., and Brook, B. Ecosystem Services Project: http://www.ecosystemser- W. (2007). Global evidence that deforestation ampli fi es · vicesproject.org/index.htm fl ood risk and severity in the developing world. Global Change Biology , 2379 – 2395. 13 , Natural Capital Project: http://www.naturalcapital- · Brauman, K. A., and G. C. Daily. (2008). Ecosystem project.org Human services. In S. E. Jorgensen and B. D. Fath, ed. Carbon Trading: http://www.carbontrading.com/ · , pp. 1148 Ecology 1154. Elsevier, Oxford, UK. – Brauman, K. A., Daily, G. C., Duarte, T. K., and Mooney, H. A. (2007). The nature and value of ecosys- Acknowledgements tem services: an overview highlighting hydrologic services. , Annual Review of Environment and Resources I am grateful to Karim Al-Khafaji, Berry Brosi, Paul R. 32 ,67 – 98. Ehrlich, Jamie H. Jones, Stephen Schneider, Navjot Sodhi, Bruijnzeel, L. A. (2004). Hydrological functions of tropical Tanya Williams, and especially Kate Brauman for their Agriculture forests: not seeing the soil for the trees? valuable comments. I thank the Christensen Fund for , 104 228. Ecosystems and Environment – , 185 their support of my conservation and ecology work. Bruno, J. F. and Selig, E. R. (2007). Regional decline of coral fi cover in the Indo-Paci c: timing, extent, and subregional , PLoS One comparisons. , e711. 2 Burd, M. (1994). Bateman ’ s principle and plant reproduc- tion: the role of pollen limitation in fruit and seed set. REFERENCES ,81 60 , Botanical Review 109. – nancial chaos, donors pledge Butler, R. (2008). Despite fi Aiken, S. R. and Leigh, C. H. (1992). Vanishing rain forests . $100M for rainforest conservation. http://news.mongabay. Clarendon Press, Oxford, UK. com/2008/1023-fcpf.html. Alexander, S. E., Schneider, S. H., and Lagerquist, K. Cain, M. L., Milligan, B. G., and Strand, A. E. (2000). Long- (1997). The interaction of climate and life. In G. C. distance seed dispersal in plant populations. American Daily, ed. 92. Island Press, s Services Nature , pp. 71 – ’ , Journal of Botany 87 , 1217 1227. – Washington DC. fl Calder, I. R. and Aylward, B. (2006). Forest and oods: Anderson, W. B. and Polis, G. A. (1999). Nutrient fl uxes Moving to an evidence-based approach to watershed from water to land: seabirds affect plant nutrient status ood management. and integrated fl , Water International , 324 32. 118 – , Oecologia on Gulf of California islands. – 31 ,87 99. Avinash, N. (2008). Soil no bar: Gujarat farmers going hi- Urban agricul- fi Canada ’ sOf ce of Urban Agriculture (2008). tech. 24 July . , The Economic Times ture notes . City Farmer, Vancouver, Canada. Bio-economics of trees in native Malayan Ba, L. K. (1977). Carson, R. (1962). Silent Spring .HoughtonMif fl in, Boston, . Department of Botany, University of Malaya, forest MA. Kuala Lumpur. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

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86 1 71 ECOSYSTEM FUNCTIONS AND SERVICES Sekercioglu, C. H. (2006b). Increasing awareness of avian Postel, S. L., Daily, G. C., and Ehrlich, P. R. (1996). Human , 21 , Trends in Ecology and Evolution ecological function. , Science , appropriation of renewable fresh water. 271 471. – 464 788. 785 – Sekercioglu, C. H. (2007). Conservation ecology: area et al. Power, M. E., Tilman, D., Estes, J. A., (1996). Current trumps mobility in fragment bird extinctions. Challenges in the quest for keystones. BioScience , 46 , Biology R286. – , R283 17 , – 609 620. Sekercioglu, C. H., Daily, G. C., and Ehrlich, P. R. (2004). . (2003). et al Prakash, V., Pain, D. J., Cunningham, A. A., Ecosystem consequences of bird declines. Proceedings of Catastrophic collapse of Indian White-backed Gyps ben- the National Academy of Sciences of the United States of galensis and Long-billed Gyps indicus vulture popula- – , 18042 101 , America 18047. 90. – , 381 109 , Biological Conservation tions. Selby, J. (2005). 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88 1 CHAPTER 4 Habitat destruction: death by a thousand cuts William F. Laurance 4.1 Habitat loss and fragmentation Humankind has dramatically transformed much ’ s surface and its natural ecosystems. of the Earth Habitat destruction occurs when a natural habitat, This process is not new it has been ongoing for — such as a forest or wetland, is altered so dramati- but it has accelerated sharply over the — millennia cally that it no longer supports the species it origi- last two centuries, and especially in the last sev- nally sustained. Plant and animal populations are eral decades. destroyed or displaced, leading to a loss of biodi- Today, the loss and degradation of natural ha- versity (see Chapter 10). Habitat destruction is bitats can be likened to a war of attrition. Many considered the most important driver of species natural ecosystems are being progressively razed, extinction worldwide (Pimm and Raven 2000). bulldozed, and felled by axes or chainsaws, until Few habitats are destroyed entirely. Very often, only small scraps of their original extent survive. habitats are reduced in extent and simultaneously Forests have been hit especially hard: the global fragmented, leaving small pieces of original habi- area of forests has been reduced by roughly half tat persisting like islands in a sea of degraded over the past three centuries. Twenty- ve nations fi land. In concert with habitat loss, habitat frag- have lost virtually all of their forest cover, and mentation is a grave threat to species survival another 29 more than nine-tenths of their forest et al. 2002; et al. (Laurance 2002; Sekercioglu (MEA 2005). Tropical forests are disappearing Chapter 5). 2 roughly a year (Figure 4.1) — at up to 130 000 km Globally, agriculture is the biggest cause of hab- elds a minute. Other ecosystems fi 50 football itat destruction (Figure 4.2). Other human activ- are less imperiled, and a few are even recover- ities, such as mining, clear-cut logging, trawling, ing somewhat following past centuries of overex- and urban sprawl, also destroy or severely degrade ploitation. habitats. In developing nations, where most habi- Here I provide an overview of contemporary tat loss is now occurring, the drivers of environ- habitat loss. Other chapters in this book descr- mental change have shifted fundamentally in ibe the many additional ways that ecosystems recent decades. Instead of being caused mostly by are being threatened — by overhunting (Chapter small-scale farmers and rural residents, habitat 6), habitat fragmentation (Chapter 5), and climate loss, especially in the tropics, is now substantially but change (Chapter 8), among other causes — driven by globalization promoting intensive agri- my emphasis here is on habitat destruction culture and other industrial activities (see Box 4.1). . I evaluate patterns of habitat destruction per se geographically and draw comparisons among different biomes and ecosystems. I then consider 4.2 Geography of habitat loss some of the ultimate and proximate factors that drive habitat loss, and how they are changing Some regions of the Earth are far more affected by today. habitat destruction than others. Among the most 73 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

89 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: 74 CONSERVATION BIOLOGY FOR ALL The aftermath of slash Figure 4.1 ‐ and ‐ burn farming in central Amazonia. Photograph by W. F. Laurance. ” , imperiled are the so-called biodiversity hotspots “ and degraded, are examples of biodiversity hot- which contain high species diversity, many locally spots. Despite encompassing just a small fraction endemic species (those whose entire geographic s land surface, hotspots may ( < 2%) of the Earth ’ range is con fi ned to a small area), and which have sustain over half of the world ’ s terrestrial species lost at least 70% of their native vegetation (Myers 2000). et al. (Myers et al. 2000). Many hotspots are in the tropics. The Many islands have also suffered heavy habitat Atlantic forests of Brazil and rainforests of West loss. For instance, most of the original natural Africa, both of which have been severely reduced habitat has already been lost in Japan, New Extent of land area cultivated globally by the year 2000. Reprinted from MEA (2005). Figure 4.2 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

90 1 HABITAT DESTRUCTION: DEATH BY A THOUSAND CUTS 75 Box 4.1 The changing drivers of tropical deforestation William F. Laurance Tropical forests are being lost today at an alarming pace. However, the fundamental (b) (b) (b) drivers of tropical forest destruction have changed in recent years (Rudel 2005; Butler and Laurance 2008). Prior to the late 1980s, deforestation was generally caused by rapid human population growth in developing nations, in concert with government policies for rural development. These included agricultural loans, tax incentives, and road construction. Such initiatives, especially evident in countries such as Brazil and Indonesia, uxes of colonists fl promoted large in into frontier areas and often caused dramatic forest loss. Box 4.1 Figure scale ‐ Changing drivers of deforestation: Small More recently, however, the impacts of rural cultivators (a) versus industrial road construction (b) in Gabon, central Africa. Photograph by W. F. Laurance. peoples on tropical forests seem to be stabilizing (see Box 4.1 Figure). Although nancial fi At the same time, globalized many tropical nations still have considerable markets and a worldwide commodity boom are population growth, strong urbanization creating a highly attractive environment for trends (except in Sub Saharan Africa) mean ‐ the private sector. Under these conditions, that rural populations are growing more crops, livestock, and large ‐ scale agriculture — slowly, and are even declining in some tree plantations by corporations and wealthy — ‐ areas. The popularity of large ‐ scale frontier landowners is increasingly emerging as the colonization programs has also waned. biggest direct cause of tropical deforestation If such trends continue, they could begin (Butler and Laurance 2008). Surging demand to alleviate some pressures on forests for grains and edible oils, driven by the global scale farming, hunting, and from small ‐ thirst for biofuels and rising standards of living wood gathering (Wright and Muller ‐ fuel ‐ in developing countries, is also spurring this landau 2006). trend. In Brazilian Amazonia, for instance, ‐ scale ranching has exploded in recent large (a) (a) (a) years, with the number of cattle more than tripling (from 22 to 74 million head) since 1990 (Smeraldi and May 2008), while industrial soy farming has also grown dramatically. Other industrial activities, especially logging, mining, and petroleum development, are also playing a critical but indirect role in forest 2008). destruction (Asner etal. 2006; Finer etal. These provide a key economic impetus for forest building (see Box 4.1 Figure), which in turn road ‐ allows in fl uxes of colonists, hunters, and miners into frontier areas, often leading to rapid forest disruption and cycles of land speculation. continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

91 . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 76 Box 4.1 (Continued) threats to wilderness, biodiversity, and indigenous REFERENCES PLoS One peoples. , doi:10.1371/journal.pone.0002932. Asner, G. P., Broadbent, E., Oliveira, P., Keller, M., Knapp, Rudel, T. K. (2005). Changing agents of deforestation: D., and Silva, J. (2006). Condition and fate of logged initiated to enterprise driven processes, from state ‐ Proceedings of the National forests in the Amazon. – Land Use Policy 24 1970 ,35 41. 2000. – , Academy of Sciences of the United States of America . The cattle realm: Smeraldi, R. and May, P. H. (2008). 12950. 103 , 12947 – a new phase in the livestock colonization of Butler, R. A. and Laurance, W. F. (2008). New strategies Brazilian Amazonia . Amigos da Terra, Amazônia for conserving tropical forests. Trends in Ecology and Brasileira, São Paulo, Brazil. Evolution , 23 , 469 – 72. Wright, S. J. and Muller ‐ Landau, H. C. (2006). The Finer, M., Jenkins, C., Pimm, S., Kean, B., and Rossi, C. , 38 future of tropical forest species. Biotropica , (2008). Oil and gas projects in the western Amazon: – 301. 287 Zealand, Madagascar, the Philippines, and Java palm or rubber plantations (MacKinnon 2006; (WRI 2003). Other islands, such as Borneo, Suma- Laurance 2007; Koh and Wilcove 2008; see Box tra, and New Guinea, still retain some original 13.3). Older agricultural frontiers, such as those in habitat but are losing it at alarming rates (Curran Europe, eastern China, the Indian Subcontinent, 2004; MacKinnon 2006). et al. and eastern and midwestern North America, Most areas of high human population density often have very little native vegetation remaining have suffered heavy habitat destruction. Such (Figure 4.2). areas include much of Europe, eastern North America, South and Southeast Asia, the Middle East, West Africa, Central America, and the Ca- 4.3 Loss of biomes and ecosystems ribbean region, among others. Most of the biodi- 4.3.1 Tropical and subtropical forests versity hotspots occur in areas with high human density (Figure 4.3) and many still have rapid A second way to assess habitat loss is by contrast- 2000). Human et al. population growth (Cincotta ing major biomes or ecosystem types (Figure 4.4). populations are often densest in coastal areas, Today, tropical rainforests (also termed tropical many of which have experienced considerable moist and humid forests) are receiving the greatest losses of both terrestrial habitats and nearby attention, because they are being destroyed coral reefs. Among others, coastal zones in Asia, so rapidly and because they are the most biologi- northern South America, the Caribbean, Europe, cally diverse of all terrestrial biomes. Of the rough- 2 and eastern North America have all suffered se- of tropical rainforest that ly 16 million km vere habitat loss (MEA 2005). originally existed worldwide, less than 9 million 2 Finally, habitat destruction can occur swiftly in remains today (Whitmore 1997; MEA 2005). km areas with limited human densities but rapidly The current rate of rainforest loss is debated, with expanding agriculture. Large expanses of the different estimates ranging from around 60 000 2 2 Amazon, for example, are currently being cleared 2002) to 130 000 km per year et al. (Achard km for large-scale cattle ranching and industrial (FAO 2000). Regardless of which estimate one ad- soy farming, despite having low population den- heres to, rates ofrainforest lossare alarmingly high. 2001). Likewise, in some et al. sities (Laurance Rates of rainforest destruction vary consider- relatively sparsely populated areas of Southeast s ’ ably among geographic regions. Of the world Asia, such as Borneo, Sumatra, and New Guinea, three major tropical regions, Southeast Asian for- forests are being rapidly felled to establish oil- ests are disappearing most rapidly in relative © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

92 1 77 HABITAT DESTRUCTION: DEATH BY A THOUSAND CUTS 25) and three major tropical wildernesses ‐ Human population density in 1995 within 25 recognized biodiversity hotspots (numbered 1 Figure 4.3 et al. 2000 © Nature Publishing Group. C). Reprinted from Cincotta ‐ (labeled A terms (Figure 4.5), while the African and New gion as a whole is buffered by the vastness of the World tropics have somewhat lower rates of per- Amazon. Likewise, in tropical Africa, forest loss is 2004). Such cent-annual forest loss (Sodhi et al. severe in West Africa, montane areas of East averages, however, disguise important smaller- Africa, and Madagascar, but substantial forest scale variation. In the New World tropics, for ex- still survives in the Congo Basin (Laurance 1999). ample, the Caribbean, MesoAmerican, and An- Other tropical and subtropical biomes have dean regions are all suffering severe rainforest suffered even more heavily than rainforests loss, but the relative deforestation rate for the re- (Figure 4.4). Tropical dry forests (also known as Fraction of potential area converted (%) 100 80 70 90 –100 102030405060 Mediterranean forests, woodlands, and scrub Temperate forest steppe and woodland Temperate broadleaf and mixed forest Tropical and sub-tropical dry broadleaf forests Flooded grasslands and savannas Tropical and sub-tropical grasslands, savannas, and shrublands Tropical and sub-tropical coniferous forests Deserts Montane grasslands and shrublands Tropical and sub-tropical moist broadleaf forests Temperate coniferous forests Loss by 1950 Boreal forests Loss between 1950 and 1990 Tundra Projected loss by 2050 to 1990, with projected losses up to 2050. Reprinted from MEA (2005). Estimated losses of major terrestrial biomes prior to 1950 and from 1950 Figure 4.4 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

93 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 78 Figure 4.5 Tropical rainforests in Southeast Asia are severely imperiled, as illustrated by this timber operation in Indonesian Borneo. Photograph by W. F. Laurance. ests and woodlands, temperate broadleaf and monsoonal or deciduous forests) have been se- mixed forests, and temperate forest-steppe and verely reduced, in part because they are easier woodlands have all suffered very heavy losses to clear and burn than rainforests. For instance, (Figure 4.4), given the long history of human along Central America fi c coast, much less ’ s Paci settlement in many temperate regions. By 1990 than 1% of the original dry forest survives. Losses more than two-thirds of Mediterranean forests of dry forest have been nearly as severe in Mada- and woodlands were lost, usually because they gascar and parts of Southeast Asia (Laurance were converted to agriculture (MEA 2005). In the 2005). et al. 1999; Mayaux eastern USA and Europe (excluding Russia), old- Mangrove forests, salt-tolerant ecosystems that growth broadleaf forests (>100 years old) have grow in tropical and subtropical intertidal zones, 2000), al- et al. nearly disappeared (Matthews have also been seriously reduced. Based on though forest cover is now regenerating in countries for which data exist, more than a third many areas as former agricultural lands are aban- of all mangroves were lost in the last few decades th century (MEA 2005). From 1990 to doned and their formerly rural, farming-based of the 20 2000, over 1% of all mangrove forests were lost populations become increasingly urbanized. annually, with rates of loss especially high in In the cool temperate zone, coniferous forests 2005). Such losses et al. Southeast Asia (Mayaux have been less severely reduced than broadleaf are alarming given the high primary productivity fi and mixed forests, with only about a fth being of mangroves, their key role as spawning and lost by 1990 (Figure 4.4). However, vast expanses fi sh rearing areas for economically important of coniferous forest in northwestern North Amer- and shrimp species, and their importance for ica, northern Europe, and southern Siberia are sheltering coastal areas from destructive storms being clear-felled for timber or pulp production. and tsunamis (Danielsen et al. 2005). As a result, these semi-natural forests are con- verted from old-growth to timber-production for- fi ed stand ests, which have a much-simpli 4.3.2 Temperate forests and woodlands structure and species composition. Large expanses of coniferous forest are also burned each year Some ecosystems have suffered even worse de- 2000). et al. (Matthews struction than tropical forests. Mediterranean for- © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

94 1 HABITAT DESTRUCTION: DEATH BY A THOUSAND CUTS 79 Figure 4.6 African savannas are threatened by livestock overgrazing and conversion to farmland. Photograph by W. F. Laurance. in recent decades, and rates of loss remain very 4.3.3 Grasslands and deserts high (Klink and Machado 2005). Grasslands and desert areas have generally suf- fered to a lesser extent than forests (Figure 4.4). Just 10 – 20% of all grasslands, which include the 4.3.4 Boreal and alpine regions savannas of Africa (Figure 4.6), the cer- llano and Boreal forests are mainly found in broad conti- ecosystems of South America, the steppes of rado nental belts at the higher latitudes of North Central Asia, the prairies of North America, and America and Eurasia. They are vast in Siberia, the spinifex grasslands of Australia, have been the largest contiguous forest area in the world, permanently destroyed for agriculture (White as well as in northern Canada. They also occur at et al. 2000; Kauffman and Pyke 2001). About a high elevations in more southerly areas, such as s deserts have been converted third of the world ’ the European Alps and Rocky Mountains of to other land uses (Figure 4.4). Included in this 2 North America. Dominated by evergreen coni- of seasonally gure is the roughly 9 million km fi ned to cold, moist fi fers, boreal forests are con dry lands, such as the vast Sahel region of Africa, climates and are especially rich in soil carbon, that have been severely degraded via deserti fi ca- because low temperatures and waterlogged soils tion (Primack 2006). inhibit decomposition of organic material (Mat- Although deserts and grasslands have not et al. thews 2000). fared as badly as some other biomes, certain re- Habitat loss in boreal forests has historically gions have suffered very heavily. For instance, been low (Figure 4.4; Box 4.2). In Russia, howev- less than 3% of the tallgrass prairies of North er, legal and illegal logging activity has grown America survive, with the remainder having rapidly, with Siberia now a major source of tim- 2000). been converted to farmland (White et al. ber exports to China, the world s largest timber ’ In southern Africa, large expanses of dryland are importer. In Canada, nearly half of the boreal fi being progressively deserti ed from overgrazing forest is under tenure for wood production. In by livestock (MEA 2005). In South America, more addition, fi re incidence is high in the boreal savannas, than half of the biologically-rich cerrado 2 2 of boreal forest zone, with perhaps 100 000 km , have which formerly spanned over 2 million km et al. 2000). burning each year (Matthews elds and cattle pastures fi been converted into soy © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

95 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 80 Like boreal forests, tundra is a vast ecosystem such as taiga grasslands (Figure 4.7), have also 2 globally) that has – (spanning 9 13 million km suffered little loss. However, all boreal ecosystems been little exploited historically (Figure 4.4) are vulnerable to global warming (see Chapter 8; (White et al. 2000). Unlike permafrost areas, tun- Box 4.2). Boreal forests, in particular, could decline dra ecosystems thaw seasonally on their surface, if climatic conditions become signi fi cantly warm- becoming important wetland habitats for water- er or drier, leading to an increased frequency or fowl and other wildlife. Other boreal habitats, res (see Box 4.2, Chapter 9). fi severity of forest Box 4.2 Boreal forest management: harvest, natural disturbance, and climate change Ian G. Warkentin fi res has led to a 2.3% rise in human ‐ ignited Until recently, the boreal biome has largely been etal. annual decrease in forest cover (Achard ignored in discussions regarding the global 2006, 2008). impacts of habitat loss through diminishing forestcover. Eventsintropical regions duringthe past four decades were far more critical due to the high losses of forest and associated species (Dirzo and Raven2003). While there are ongoing concerns about tropical forest harvest, the implications of increasing boreal forest exploitation now also need to be assessed, particularly in the context of climate change. (Bradshaw . 2009) Warnings suggest that etal forest managers shouldnot overlook the services provided by the boreal ecosystem, especially carbon storage (Odling ‐ Smee 2005). Ranging across northern Eurasia and North America, the boreal biome constitutes one third of all current forest cover on Earth and is home to nearly half Box 4.2 Figure An example of harvesting in the Boreal forest. of the remaining tracts of extensive, intact Photograph by Greg Mitchell. forests. Nearly 30% of the Earth s terrestrial ’ The biggest challenge for boreal managers stored carbon is held here, and the boreal may may come from the warmer and drier weather, uence onmeanannual global fl well have more in with a longer growing season, that climate temperature than any other biome due to its latitude change models predict for upper ‐ fl ectivity (albedo) properties and sunlight re ecosystems (IPCC 2001). The two major drivers evapotranspiration rates (Snyder etal. 2004). fi of boreal disturbance dynamics ( re and insect Conversion of North America s boreal forest to ’ infestation) are closely associated with weather other land cover types has been limited (e.g. <3% conditions (Soja etal. 2007) and predicted to be in Canada; Smith and Lee 2000). In Finland and both more frequent and intense over the next Sweden forest cover has expanded during recent etal. century (Kurz ‐ ignited 2008); more human decades, but historic activities extensively reduced fi res are also predicted as access to the forest fi ’ s boreal forests for and modi ed the region expands (Achard 2008). Increased harvest, etal. commercial purposes, leaving only a small fi re and insect infestations will raise the rates of etal. 2001; proportion as natural stands (Imbeau carbon loss to the atmosphere, but climate see Box 4.2 Figure). Conversely, there has been a models also suggest that changes to albedo and rapid expansion of harvest across boreal Russia evapotranspiration due to these disturbances during the past 10 15 years leading to broad – etal. will offset the lost carbon stores (Bala shifts from forest to other land cover types (MEA maintaining large non forested boreal — ‐ 2007) 2005). Forest cover loss ac ross European Russia is sites potentially may cool the global climate associated with intens ive harvest, mineral more than the carbon storage resulting from ation, while in Siberian exploitation and urbaniz reforestation at those sites. However, to Russia the combination of logging and a sharp manage the boreal forest based solely on one continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

96 1 HABITAT DESTRUCTION: DEATH BY A THOUSAND CUTS 81 Box 4.2 (Continued) Imbeau, L., Mönkkönen, M., and Desrochers, A. (2001). ecosystem service would be reckless. For term effects of forestry on birds of the Long ‐ example, many migratory songbirds that eastern Canadian boreal forests: a comparison depend upon intact boreal forest stands for , 15 with Fennoscandia. , Conservation Biology breeding also provide critical services such as 1162. – 1151 insect predation, pollen transport and seed IPCC (Intergovernmental Panel on Climate Change) dispersal (Sekercioglu 2006) in habitats c basis fi Climate change 2001: the scienti (2001). . extending from boreal breeding grounds, to Contribution of Working Group I to the Third migratory stopovers and their winter homes Assessment Report of the Intergovernmental Panel in sub tropical and tropical regions. Thus ‐ on Climate Change. Cambridge University Press, boreal forest managers attempting to meet New York, NY. climate change objectives (or any other single Kurz, W. A., Stinson, G., Rampley, G. J., Dymond, C. C., goal) must also consider the potential costs and Neilson, E. T. (2008). Risk of natural disturbances for biodiversity and the multiple services at s forests to the ’ makes future contribution of Canada associated risk due to natural and human ‐ global carbon cycle highly uncertain. Proceedings of the change. National Academy of Sciences of the United States of 105 , America 1555. – , 1551 REFERENCES MEA (Millennium Ecosystem Assessment) (2005). ‐ being: synthesis . Island Ecosystems and human well (2006). Areas Achard, F., Mollicone, D., Stibig, H. ‐ J., et al. Press, Washington, DC. of rapid forest Forest ‐ cover change in boreal Eurasia. ‐ Odling Smee, L. (2005). Dollars and sense. , , Nature 437 237 , Ecology and Management 334. – , 322 614 – 616. Achard, F. D., Eva, H. D., Mollicone, D., and Beuchle, R. Sekercioglu, C. H. (2006). Increasing awareness of avian (2008). The effect of climate anomalies and human , 21 , Trends in Ecology and Evolution ecological function. res in Russian boreal forests. fi ignition factor on wild 464 – 471. Philosophical Transactions of the Royal Society of ’ Canada Smith, W. and Lee, P., eds (2000). s forests at a London B , 363 2339. , 2331 – . World crossroads: an assessment in the year 2000 Bala, G., Caldeira, K., Wickett, M., (2007). Combined et al. Resources Institute, Washington, DC. cycle effects of large scale defores- ‐ climate and carbon ‐ Snyder, P. K., Delire, C., and Foley, J. A. (2004). Proceedings of the National Academy of Sciences tation. uence of different vegetation fl Evaluating the in – , 6550 104 , of the United States of America 6555. Climate Dynamics biomes on the global climate. , Bradshaw, C. J. A., Warkentin, I. G., and Sodhi, N. S. (2009). 302. , 279 – 23 Urgent preservation of boreal carbon stocks and biodi- et al. Soja, A. J., Tchebakova, N. M., French, N. H. F., 24 ,541 – 548. versity. Trends in Ecology and Evolution , induced boreal forest change: (2007). Climate ‐ Dirzo, R. and Raven, P. H. (2003). Global state of biodi- Predictions versus current observations. Global and versity and loss. Annual Review of Environment and Planetary Change , 56 , 274 – 296. 167 – 28 , Resources , 137 In addition, tundra areas will shrink as boreal destroyed in the last two centuries (Stein et al. forests spread north. – 2000). From 60 70% of all European wetlands have been destroyed outright (Ravenga et al. 2000). Many developing nations are now 4.3.5 Wetlands suffering similarly high levels of wetland loss, particularly as development in coastal zones ac- Although they do not fall into any single biome celerates. As discussed above, losses of mangrove type, wetlands have endured intense habitat de- forests, which are physiologically specialized for struction in many parts of the world. In the USA, the intertidal zone, are also very high. for instance, over half of all wetlands have been © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

97 Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 82 somewhat. Forest cover is now increasing in east- ern and western North America, Alaska, western and northern Europe, eastern China, and Japan (Matthews et al. 2000; MEA 2005, Figure 4.4). During the 1990s, for instance, forest cover rose 2 annually in the temperate by around 29 000 km and boreal zones, although roughly 40% of this increase comprised forest plantations of mostly non-native tree species (MEA 2005). Despite par- tial recovery of forest cover in some regions (Wright and Muller-Landau 2006), conversion rates for many ecosystems, such as tropical and subtropical forests and South American cerrado savanna-woodlands, remain very high. Because arable land is becoming scarce while agricultural demands for food and biofuel feed- stocks are still rising markedly (Koh and Ghazoul 2008), agriculture is becoming increasingly inten- si ed in much of the world. Within agricultural fi regions, a greater fraction of the available land is actually being cultivated, the intensity of cultiva- tion is increasing, and fallow periods are decreas- ing (MEA 2005). Cultivated systems (where over 30% of the landscape is in croplands, shifting fi ned-livestock production, or cultivation, con Figure 4.7 Boreal ecosystems, such as this alpine grassland in New freshwater aquaculture) covered 24% of the glob- Zealand, have suffered relatively little habitat loss but are particularly al land surface by the year 2000 (Figure 4.2). vulnerable to global warming. Photograph by W. F. Laurance. Thus, vast expanses of the earth have been al- tered by human activities. Old-growth forests have fi 4.4 Land-use intensi cation diminished greatly in extent in many regions, es- and abandonment pecially in the temperate zones; for instance, at Humans have transformed a large fraction of the least 94% of temperate broadleaf forests have ’ s land surface (Figure 4.2). Over the past Earth been disturbed by farming and logging (Primack three centuries, the global extent of cropland has 2006). Other ecosystems, such as coniferous forests, 2 , risen sharply, from around 2.7 to 15 million km are being rapidly converted from old-growth to mostly at the expense of forest habitats (Turner fi ed semi-natural production forests with a simpli 1990). Permanent pasturelands are even et al. stand structure and species composition. Forest 2 more extensive, reaching around 34 million km cover is increasing in parts of the temperate and by the mid-1990s (Wood et al. 2000). The rate of boreal zones, but the new forests are secondary land conversion has accelerated over time: for and differ from old-growth forests in species com- instance, more land was converted to cropland position, structure, and carbon storage. Yet other from 1950 to 1980 than from 1700 to 1850 (MEA ecosystems, particularly in the tropics, are being 2005). rapidly destroyed and degraded. For example, ma- Globally, the rate of conversion of natural ha- rine ecosystems have been heavily impacted by bitats has fi nally begun to slow, because land human activities (see Box 4.3). readily convertible to new arable use is now in The large-scale transformations of land increasingly short supply and because, in temper- cover described here consider only habitat loss ate and boreal regions, ecosystems are recovering .Ofthesurvivinghabitat,muchisbeing per se © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

98 1 HABITAT DESTRUCTION: DEATH BY A THOUSAND CUTS 83 Box 4.3 Human Impacts on marine ecosystems Benjamin S. Halpern, Carrie V. Kappel, Fiorenza Micheli, and Kimberly A. Selkoe salt marshes. Effects from climate change, such The oceans cover 71% of the planet. This as rising sea levels and temperatures and ocean vastness has led people to assume ocean cation, are observed with increasing acidi fi resources are inexhaustible, yet evidence to the frequency around the world. Global commerce, contrary has recently accumulated (see Box 4.3 aquaculture and the aquarium trade have Figure 1 and Plate 4). Populations of large fi sh, ‐ caused the introduction of thousands of non mammals, and sea turtles have collapsed due to native species, many of which become shing pressure, putting some species intense fi ecologically and economically destructive in shing gear such as fi at risk of extinction, and their new environment. These human caused ‐ sh but fi bottom trawls not only catch target stresses on ocean ecosystems are the most also destroy vast swaths of habitat (see Box 6.1). intense and widespread, but many other Pollution, sedimentation, and nutrient human activities impact the ocean where they fi enrichment have caused die ‐ offs of sh and are concentrated, such as shipping, “ corals, blooms of jelly fi sh and algae, and dead aquaculture, and oil and gas extraction, and ‐ zones depleted waters around the ” of oxygen many new uses such as wave and wind energy world. Coastal development has removed much farms are just emerging. of the world s mangroves, sea grass beds and ’ fi shing fl A few of the many human threats to marine ecosystems around the world. (A) The sea Box 4.3 Figure 1 oor before and after bottom trawl occurred [courtesy CSIRO (Australian Commonwealth Scienti fi c and Research Organization) Marine Research], (B) coastal development in Long Beach, California (courtesy California Coastal Records Project), (C) shrimp farms in coastal Ecuador remove coastal habitat (courtesy Google Eart h), ‐ and (D) commercial shipping and ports produce pollution and introduce non native species (courtesy public commons). synergisms among stressors that can amplify There are clear challenges in reducing the impacts. For example, excess nutrient input impacts of any single human activity on marine fi sh shing of herbivorous fi combined with over ecosystems. These challenges are particularly on coral reefs can lead to algal proliferation stark in areas where dozens of activities co ‐ and loss of coral with little chance of recovery, occur because each species and each ecosystem while each stressor alone may not lead to such may respond uniquely to each set of human an outcome. The majority of oceans are subject activities, and there may be hard predict ‐ to ‐ continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

99 Conservation Biology for All Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do 84 CONSERVATION BIOLOGY FOR ALL Box 4.3 (Continued) Table). The heaviest impacts occur in the North to at least three different overlapping human Sea and East and South China Seas, where stressors, with most coastal areas experiencing industry, dense human population, and a long over a dozen, especially near centers of history of ocean use come together. The least commerce like the ports of Los Angeles and impacted areas are small and scattered Singapore. throughout the globe, with the largest patches rst comprehensive map of the impacts of fi The at the poles and the Torres Strait north of 17 different types of human uses on the global Australia.Severalofthe countries whose seasare oceans provides information on where signi cantly impacted, including the United fi cumulative humanimpacts tomarineecosystems States and China, have huge territorial holdings, 2008; see Box 4.3 etal. are most intense (Halpern suggesting both a responsibility and an Figure 2 and Plate 5). The map shows that over cant difference in fi opportunity to make a signi 40% of the oceans are heavily impacted and less improving ocean health. than 4% are relatively pristine (see Box 4.3 High Impact (12.3–15.5) Very Low Impact (<2.4) Medium Impact (5.7–9.0) Very High Impact (>15.5) Low Impact (2.4–5.7) Medium High Impact (9.0–12.3) Global map of the cumulative human impact on marine ecosystems, based on 20 ecosystem types and 17 different human Box 4.3 Figure 2 activities. Grayscale colors correspond to overall condition of the ocean as indicated in the legend, with cumulative impact score cutoff values for each category of ocean condition indicated. continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

100 1 HABITAT DESTRUCTION: DEATH BY A THOUSAND CUTS 85 Box 4.3 (Continued) The amount of marine area within the Exclusive Economic Zone (EEZ) of countries that is heavily impacted. Countries are listed Box 4.3 Table s EEZ (including territorial waters) and includes a selection of countries chosen for illustrative ’ in order of total marine area within a country purposes. Global statistics are provided for comparison. Data are drawn from Halpern (2008). et al. Impact Category % of global ocean area Country Very Very ‐ Medium High High Low Low Medium High 100% 3.7% 24.5% 31.3% 38.2% 1.8% GLOBAL 0.5% Largest EEZs 62.1% 4.4% 0.7% 3.3% 2.0% 9.1% United States 21.5% 0.9% France 2.8% 0.2% 36.7% 40.1% 21.6% 0.4% 0.3% 26.3% 3.7% 26.4% 42.3% 2.5% Australia 1.0% 0.6% 0.3% Russia 2.1% 22.5% 30.8% 32.3% 13.5% 6.5% United Kingdom 1.9% 0.3% 25.2% 36.0% 29.0% 3.0% 3.0% 2.3% 32.0% 42.4% 1.7% Indonesia 2.1% 18.0% 1.0% Canada 5.5% 26.5% 22.8% 18.4% 25.8% 1.5% 76.2% Japan 3.2% 1.1% 0.0% 0.9% 9.7% 9.9% Brazil 0.5% 1.0% 3.1% 17.1% 32.4% 44.8% 2.1% 35.5% 0.3% Mexico 0.9% 1.2% 29.1% 32.7% 1.2% 7.3% 51.4% 6.8% 1.5% 0.1% 0.6% India 32.9% 5.7% 27.2% 20.1% 22.5% China 0.2% 0.0% 24.5% SMALLER EEZs 0.4% 43.7% 14.4% 4.4% Germany 0.02% 2.4% 34.6% 10.1% 0.0% 4.8% 58.4% 0.21% Iceland 0.4% 26.3% 2.2% 40.8% 6.6% 0.2% 0.0% 0.11% Ireland 50.3% 15.5% 64.5% 11.8% 4.7% Italy 0.15% 0.0% 3.5% 68.8% 0.0% 18.6% 1.5% Netherlands 0.04% 3.6% 7.7% 8.6% 6.7% 37.2% 2.5% Sri Lanka 0.15% 0.0% 45.0% 9.6% 3.4% 0.4% 21.9% 42.6% 0.08% Thailand 22.1% 35.7% 10.2% 5.4% Vietnam 0.18% 1.1% 21.0% 26.7% of marine ecosystems. Ultimately, it is now clear Complex but feasible management that marine resources are not inexhaustible approaches are needed to address the sector planning ‐ and that precautionary, multi cumulative impacts of human activities on the term of their use is needed to ensure long ‐ oceans. Comprehensive spatial planning of sustainability of marine ecosystems and the activities affecting marine ecosystems, or ocean crucial services they provide. zoning, has already been adopted and ’ implemented in Australia s Great Barrier Reef and parts of the North Sea, with the goal of minimizing the overlap and potential synergies of multiple stressors. Many countries, including REFERENCES the United States, are beginning to adopt Ecosystem ‐ Based Management (EBM) Halpern, B. S., Walbridge, S., Selkoe, K. A., et al. (2008). A approaches that explicitly address cumulative global map of human impact on marine ecosystems. impacts and seek to balance sustainable use of 319 , 948 – Science 952. , the oceans with conservation and restoration © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

101 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 86 CONSERVATION BIOLOGY FOR ALL degraded in various ways — Suggested reading such as by habitat fragmentation, increased edge effects, selective Sanderson, E. W., Jaiteh, M., Levy, M., Redford, K., Wan- · re fi logging, pollution, overhunting, altered nebo, A., and Woolmer, G. (2002). The human footprint regimes, and climate change. These forms of 904. and the last of the wild. BioScience , 52 ,891 – environmental degradation, as well as the impor- Sodhi, N.S., Koh, L P., Brook, B.W., and Ng, P. (2004). · tant environmental services these ecosystems pro- Southeast Asian biodiversity: an impending catastro- vide, are discussed in detail in subsequent phe. , 19 , 654 – Trends in Ecology and Evolution 660. chapters. MEA. (2005). Millennium Ecosystem Assessment. Ecosys- · . Island Press, Wa- tems and Human Well-Being: Synthesis shington, DC. Summary Laurance, W.F. and Peres, C. A., eds. (2006). Emerging · . University of Chicago Press, Threats to Tropical Forests Vast amounts of habitat destruction have already · Chicago. occurred. For instance, about half of all global forest cover has been lost, and forests have virtually van- ished in over 50 nations worldwide. Relevant websites Habitat destruction has been highly uneven · Mongabay: http://www.mongabay.com. among different ecosystems. From a geographic per- · Forest Protection Portal: http://www.forests.org. spective, islands, coastal areas, wetlands, regions · The Millennium Ecosystem Assessment synthesis re- with large or growing human populations, and · ports: http://www.MAweb.org. emerging agricultural frontiers are all sustaining rapid habitat loss. From a biome perspective, habitat loss has been · REFERENCES very high in Mediterranean forests, temperate for- est-steppe and woodland, temperate broadleaf for- Achard, F., Eva, H., Stibig, H., Mayaux, P., Gallego, J., Richards, T., and Malingreau, J.-P. (2002). Determination ests, and tropical coniferous forests. Other s humid tropical ’ of deforestation rates of the world ecosystems, particularly tropical rainforests, are Science 1002. , – , 999 forests. 297 now disappearing rapidly. Cincotta, R. P., Wisnewski, J., and Engelman, R. (2000). Habitat destruction in the temperate zone peaked · Nature , Human population in the biodiversity hotspots. th th in the 19 centuries. Although con- and early 20 – , 990 404 2. siderable habitat loss is occurring in some temperate (2004). Low- et al. Curran, L. M., Trigg, S., McDonald, A., ecosystems, overall forest cover is now increasing land forest loss in protected areas of Indonesian Borneo. from forest regeneration and plantation establish- , – , 1000 303 Science 1003. ment in some temperate regions.  rensen, M. K., Olwig, M. F. Danielsen, F., S et al. (2005). Primary (old-growth) habitats are rapidly dimin- The Asian Tunami: A protective role for coastal vegeta- · ishing across much of the earth. In their place, a Science , 310 , 643. tion. FAO (Food and Agriculture Organization Of The United variety of semi-natural or intensively managed eco- — Global forest resource assessment 2000 Nations) (2000). systems are being established. For example, al- . FAO, New York. main report though just two-tenths of the temperate coniferous Kauffman, J. B. and Pyke, D. A. (2001). Range ecology, global forests have disappeared, vast areas are being con- Encyclopedia of biodi- uences. In S. Levin, ed. fl livestock in verted from old-growth to timber-production for- versity 5 , pp. 33 – 52. Academic Press, San Diego, California. ed stand structure and ests, with a greatly simpli fi Klink, C. A. and Machado, R. B. (2005). Conservation of the species composition. Brazilian cerrado. Conservation Biology , 19 , 707 – 713. Boreal ecosystems have suffered relatively Koh, L. P. and Ghazoul, J. (2008). Biofuels, biodiversity, · limited reductions to date but are especially vulner- icts and nding op- and people: understanding the con fi fl able to global warming. Boreal forests could become portunities. – 2460. Biological Conservation , 141 , 2450 Koh, L. P. and Wilcove, D. S. (2008). Is oil palm agriculture increasingly vulnerable to destructive res if future fi ,60 – 64. 1 , Conservation Letters really destroying biodiversity. conditions become warmer or drier. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

102 1 87 HABITAT DESTRUCTION: DEATH BY A THOUSAND CUTS wetland ecosystems . World Resources Institute, Laurance, W. F. (1999). Re ections on the tropical defores- fl Washington, DC. – 117. tation crisis. , Biological Conservation 91 , 109 Sekercioglu C. H., Ehrlich, P. R., Daily, G. C., Aygen, D., Laurance, W. F. (2007). Forest destruction in tropical Asia. Goehring, D., and Sandi, R. (2002). Disappearance of 1550. – , 1544 93 , Current Science insectivorous birds from tropical forest fragments. Pro- Laurance, W. F., Albernaz, A., and Da Costa, C. (2001). Is ceedings of the National Academy of Sciences of the United deforestation accelerating in the Brazilian Amazon? En- States of America 99 , 28 – 11. , 305 vironmental Conservation , , 263 – 267. et al. (2002). Laurance, W. F., Lovejoy, T., Vasconcelos, H., Sodhi, N. S., Koh, L. P., Brook, B. W., and Ng, P. (2004). Ecosystem decay of Amazonian forest fragments: a 22- Southeast Asian biodiversity: an impending disaster. 16 , 605 year investigation. , 618. – Conservation Biology 660. – , 654 Trends in Ecology and Evolution 19 , MacKinnon, K. (2006). Megadiversity in crisis: politics, Precious Stein, B. A., Kutner, L. and Adams, J., eds (2000). policies, and governance in Indonesia s forests. In W. F. ’ . heritage: the status of biodiversity in the United States Laurance and C. A. Peres, eds Emerging threats to tropical Oxford University Press, New York. forests 305. University of Chicago Press, Chicago, – ,pp.291 Turner,B.L.,Clark,W.C.,Kates,R.,Richards,J.,MathewsJ., Illinois. and Meyer, W., eds (1990). The earth as transformed by human Matthews, E., Rohweder, M., Payne, R., and Murray, S. action: global and regional change in the biosphere over the past (2000). Pilot Analysis of Global Ecosystems: Forest Ecosys- . Cambridge University Press, Cambridge, UK. 300 years tems . World Resources Institute, Washington, DC. White, R. P., Murray, S., and Rohweder, M. (2000) Pilot Mayaux, P., Holmgren, P., Achard, F., Eva, H., Stibig, H.-J., analysis of global ecosystems: grassland ecosystems . World and Branthomme, A. (2005). Tropical forest cover change Resources Institute, Washington, DC. in the 1990s and options for future monitoring. Philosophical Whitmore, T. C. (1997). Tropical forest disturbance, Transactions of the Royal Society of London B , 360 , 373 384. – disappearance, and species loss. In Laurance, MEA (Millenium Ecosystem Assessment) (2005). Ecosys- W. F. and R. O. Bierregaard, eds Tropical forest Remnants: tems and human well-being: synthesis . Island Press, Wa- ecology, management, and conservation of fragmented shington, DC. communities – 12. University of Chicago Press, , pp. 3 Myers, N., Mittermeier, R., Mittermeier, C., Fonseca, G., Chicago, Illinois. and Kent, J. (2000). Biodiversity hotspots for conserva- Pilot analy- Wood, S., Sebastian, K., and Scherr, S. J. (2000). , , 853 – tion priorities. 403 858. Nature sis of global ecosystems: agroecosystems . World Resources Pimm, S. L. and Raven, P. (2000). Biodiversity: Extinction Institute, Washington, DC. Nature , 403 , 843 – 845. by numbers. WRI (World Resources Institute) (2003). World resources Primack, R. B. (2006). Essentials of conservation biology , 4th 2002 – 2004: decisions for the earth: balance, voice, and edn. Sinauer Associates, Sunderland, Massachusetts. power . World Resources Institute, Washington, DC. Ravenga, C., Brunner, J., Henninger, N., Kassem, K., and Wright, S. J. and Muller-Landau, H. C. (2006). The future of Payne, R. (2000). Pilot analysis of global ecosystems: 38 , 287 – 301. tropical forest species. Biotropica , © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

103 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CHAPTER 5 Habitat fragmentation and landscape change Andrew F. Bennett and Denis A. Saunders Broad-scale destruction and fragmentation of fragmentation for issues directly associated with ” native vegetation is a highly visible result the subdivision of vegetation and its ecological of human land-use throughout the world (Chap- consequences. ter 4). From the Atlantic Forests of South America This chapter begins by summarizing the con- to the tropical forests of Southeast Asia, and in ceptual approaches used to understand conserva- many other regions on Earth, much of the original tion in fragmented landscapes. We then examine vegetation now remains only as fragments the biophysical aspects of landscape change, and amidst expanses of land committed to feeding how such change affects species and commu- and housing human beings. Destruction and nities, posing two main questions: (i) what are fragmentation of habitats are major factors in of occurrence of patterns the implications for the the global decline of populations and species species and communities?; and (ii) how does (Chapter 10), the modi fi cation of native plant and processes landscape change affect fl that in uence animal communities and the alteration of ecosys- the distribution and viability of species and com- tem processes (Chapter 3). Dealing with these munities? The chapter concludes by identifying changes is among the greatest challenges facing the kinds of actions that will enhance the conser- “ the mission-orientated crisis discipline ” of conser- vation of biota in fragmented landscapes. vation biology (Soulé 1986; see Chapter 1). nition, is the Habitat fragmentation, by de fi ” breaking apart of continuous habitat, such as “ 5.1 Understanding the effects tropical forest or semi-arid shrubland, into dis- of landscape change tinct pieces. When this occurs, three interrelated 5.1.1 Conceptual approaches processes take place: a reduction in the total amount of the original vegetation (i.e. habitat The theory of island biogeography (MacArthur loss); subdivision of the remaining vegetation fl and Wilson 1967) had a seminal in uence in sti- into fragments, remnants or patches (i.e. habitat mulating ecological and conservation interest in fragmentation); and introduction of new forms of fragmented landscapes. This simple, elegant land-use to replace vegetation that is lost. These model highlighted the relationship between the three processes are closely intertwined such that s ’ number of species on an island and the island cult to separate the relative effect of it is often dif fi area and isolation. It predicted that species rich- each on the species or community of concern. ness on an island represents a dynamic balance Indeed, many studies have not distinguished be- between the rate of colonization of new species to tween these components, leading to concerns that the island and the rate of extinction of species ” “ is an ambiguous, or even habitat fragmentation already present. It was quickly perceived that meaningless, concept (Lindenmayer and Fischer habitat isolates, such as forest fragments, could “ 2006). Consequently, we use landscape change ” islands ” in a “ sea ” of de- “ also be considered as “ habitat to refer to these combined processes and veloped land and that this theory provided a 88 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

104 1 89 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE quantitative approach for studying their biota. live fences, and pastures with dispersed trees This stimulated many studies in which species each support diverse assemblages of birds, bats, richness in fragments was related to the area ies (Harvey fl dung beetles and butter 2006). et al. and isolation of the fragment, the primary factors To these species, the landscape represents a mo- in island biogeographic theory. saic of land uses of differing quality, rather than a The development of landscape ecology contrib- ” contrast between “ habitat . ” non-habitat “ and uted new ways of thinking about habitat Recognizing landscapes as mosaics emphasizes fragments and landscape change. The concept the need to appreciate all types of elements in of patches and connecting corridors set within the landscape. This perspective is particularly rel- a matrix (i.e. the background ecosystem or evant in regions where cultural habitats, derived land-use type) became an in fl uential paradigm from centuries of human land-use, have impor- (Forman and Godron 1986). It recognized the tant conservation values. importance of the spatial context of fragments. Different species have different ecological The environment surrounding fragments is great- attributes, such as their scale of movement, life- ed during landscape changes associated ly modi fi history stages, longevity, and what constitutes with fragmentation. Thus, in contrast to islands, uence how a species habitat. These each in fl “ per- fragments and their biota are strongly in uenced fl a landscape, as well as its ability to ” ceives by physical and biological processes in the wider ed landscape. Consequently, fi survive in a modi landscape, and the isolation of fragments de- the same landscape may be perceived by pends not only on their distance from a similar different taxa as having a different structure and habitat but also on their position in the landscape, different suitability, and quite differently from the types of surrounding land-uses and how they the way that humans describe the landscape. in uence the movements of organisms (Saunders fl ” species-centered “ A view of a landscape can be et al. 1991; Ricketts 2001). obtained by mapping contours of habitat suitabil- The in fl uence of physical processes and distur- 2004). ity for any given species (Fischer et al. bance regimes on fragments means that following habitat destruction and fragmentation, habitat 5.1.2 Fragment vs landscape perspective cation also occurs. Mcintyre and Hobbs fi modi Habitat fragmentation is a landscape-level pro- (1999) incorporated this complexity into a con- cess. Fragmented landscapes differ in the size ceptual model by outlining four stages along a trajectory of landscape change. These were: and shape of fragments and in their spatial con- (i) intact landscapes, in which most original veg- guration. Most studies ” habitat fragmentation “ fi etation remains with little or no modi fi cation; have been undertaken at the fragment level, with (ii) variegated landscapes, dominated by the orig- individual fragments as the unit of study. How- inal vegetation, but with marked gradients of ever, to draw inferences about the consequences of landscape change and habitat fragmentation, it habitat modi cation; (iii) fragmented landscapes, fi is necessary to compare “ whole landscapes ” in which fragments are a minor component in that differ in their patterns of fragmentation a landscape dominated by other land uses; and 10%) cover of < (iv) relict landscapes with little ( (McGarigal and Cushman 2002). Comparisons ed fi original vegetation, set within highly modi of landscapes are also important because: (i) land- surroundings. This framework emphasizes the scapes have properties that differ from those dynamics of landscape change. Different stages of fragments (Figure 5.1); (ii) many species along the trajectory pose different kinds of chal- move between and use multiple patches in the landscape; and (iii) conservation managers must lenges for conservation management. manage entire landscapes (not just individual fi Many species are not con ned solely to frag- fragments) and therefore require an understand- ments, but also occur in other land uses in mod- ed landscapes. In Nicaragua, for example, fi i ing of the desirable properties of whole land- riparian forests, secondary forests, forest fallows, scapes. Consequently, it is valuable to consider © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

105 Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: 90 CONSERVATION BIOLOGY FOR ALL many of these are intercorrelated, especially with a) b) the total amount of habitat remaining in the land- scape (Fahrig 2003). Several aspects of the spatial con guration of fragments that usefully distinguish fi between different landscapes include: (i) the degree of subdivision (i.e. number of fragments), (ii) the aggregation of habitat, and (iii) the complexity of fragment shapes (Figure 5.3). Some kinds of changes are not necessarily evi- dent from a time-series sequence. Landscape change is not random: rather, disproportionate Individual fragments Whole landscapes change occurs in certain areas. Clearing of vegeta- size compositional gradients tion is more common in fl atter areas at lower eleva- shape diversity of land-uses core area number of fragments tions and on the more-productive soils. Such areas vegetation type aggregation are likely to retain fewer, smaller fragments of orig- y isolation structural connectivit inal vegetation, whereas larger fragments are more Figure 5.1 Comparison of the types of attributes of a) individual likely to persist in areas less suitable for agricultural fragments and b) whole landscapes. orurbandevelopment,suchasonsteepslopes, poorer soils, or regularly inundated oodplains. fl This has important implications for conservation the consequences of landscape change at both the because sites associated with different soil types fragment and landscape levels. and elevations typically support different sets of species. Thus, fragments usually represent a biased sample of the former biota of a region. There also is 5.2 Biophysical aspects of landscape uence on landscape change fl a strong historical in change because many fragments, and the disturbance re- gimes they experience, are a legacy of past land 5.2.1 Change in landscape pattern settlement and land-use (Lunt and Spooner 2005). Landscape change is a dynamic process. A series of Land-use history can be an effective predictor of the “ ” at intervals through time (Figure 5.2) snapshots present distribution of fragments and ecosystem illustrates the pattern of change to the original condition within fragments. It is necessary to un- vegetation. Characteristic changes along a time derstand ecological processes and changes in the trajectory include: (i) a decline in the total area of past in order to manage for the future. fragments; (ii) a decrease in the size of many frag- ments (large tracts become scarce, small fragments 5.2.2 Changes to ecosystem processes predominate); (iii) increased isolation of fragments from similar habitat; and (iv) the shapes of frag- Removal of large tracts of native vegetation ments increasingly become dominated by straight changes physical processes, such as those relating edges compared with the curvilinear boundaries of fl uxes of wind and water to solar radiation and the natural features such as rivers. For small fragments (Saunders et al. 1991). The greatest impact on frag- and linear features such as fencerows, roadside ments occurs at their boundaries; small remnants vegetation, and riparian strips, the ratio of perime- and those with complex shapes experience the ter length to area is high, resulting in a large pro- “ strongest edge effects ” . For example, the micro- edge habitat. An increase in the “ portion of ” climate at a forest edge adjacent to cleared land overall proportion of edge habitat is a highly in fl u- differs from that of the forest interior in attributes ential consequence of habitat fragmentation. such as incident light, humidity, ground and air At the landscape level, a v ariety of indices have temperature, and wind speed. In turn, these phys- been developed to quantify spatial patterns, but ical changes affect biological processes such as © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

106 1 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE 91 Figure 5.2 Changes in the extent and pattern of native vegetation in the Kellerberrin area, Western Australia, from 1920 to 1984, illustrating the et al. (1993). process of habitat loss and fragmentation. Reprinted from Saunders litter decomposition and nutrient cycling, and the of disturbance-adapted butter fl ies and beetles structure and composition of vegetation. and elevated tree mortality extend 200 m or Changes to biophysical processes from land use more from the forest edge (Laurance 2008). In in the surrounding environment, such as the use of most situations, changes at edges are generally fertilizers on farmland, alterations to drainage pat- detrimental to conservation values because they fl terns and water ows, and the presence of exotic modify formerly intact habitats. However, in plants and animals, also have spill-over effects in some circumstances edges are deliberately man- fragments. Many native vegetation communities aged to achieve speci fi c outcomes. Manipula- are resistant to invasion by exotic plant species tion of edges is used to enhance the abundance unless they are disturbed. Grazing by domestic of game species such as deer, pheasants and stock and altered nutrient levels can facilitate the grouse (see Box 1.1). In England, open linear invasion of exotic species of plants, which mark- ” in woods may be actively managed to “ rides edly alters the vegetation in fragments (Hobbs and increase incident light and early successional habi- Yates 2003) and habitats for animals. tat for butter fl ies and other wildlife (Ferris-Kaan The intensity of edge effects in fragments and 1995). the distance over which they act varies between Changes to biophysical processes frequently processes and between ecosystems. In tropical have profound effects for entire landscapes. In forests in the Brazilian Amazon, for example, highly fragmented landscapes in which most changes in soil moisture content, vapor pressure fragments are small or have linear shapes, there fi cit, and the number of treefall gaps extend de may be little interior habitat that is buffered from about 50 m into the forest, whereas the invasion edge effects. Changes that occur to individual © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

107 . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: Conservation Biology for All 92 CONSERVATION BIOLOGY FOR ALL fragments accumulate across the landscape. 5.3 Effects of landscape change on species Changes to biophysical processes such as hydro- Species show many kinds of responses to habitat logical regimes can also affect entire landscapes. fragmentation: some are advantaged and in- In the Western Australian wheatbelt (Figure 5.2), crease in abundance, while others decline and massive loss of native vegetation has resulted in a become locally extinct (see Chapter 10). Under- rise in the level of groundwater, bringing stored standing these diverse patterns, and the processes salt (NaCl) to the surface where it accumulates underlying them, is an essential foundation for and reduces agricultural productivity and trans- conservation. Those managing fragmented forms native vegetation (Hobbs 1993). Box 5.1 Time lags and extinction debt in fragmented landscapes Andrew F. Bennett and Denis A. Saunders Habitat destruction and fragmentation result 7 in immediately visible and striking changes to 6 the pattern of habitat in the landscape. However, the effects of these changes on the 5 biota take many years to be expressed: there is a time ‐ lag in experiencing the full 4 ‐ consequences of such habitat changes. Long 3 lived organisms such as trees may persist for many decades before disappearing without Species richness 2 replacement; small local populations of animals 1 gradually decline before being lost; and ecological processes in fragments are sensitive 0 to long ‐ term changes in the surroundings. 1 100 10 1000 Conservation managers cannot assume that Area (ha) species currently present in fragmented Box 5.1 Figure A change in the species ‐ area relationship for landscapes will persist there. Many fragments mammals in rainforest fragments in Queensland, Australia, between and landscapes face impending extinctions, 1986 ( lled circles) and 2006 (open circles) illustrates a time lag in fi ‐ even though there may be no further change in the loss of species following fragmentation. Data from Laurance fragment size or the amount of habitat in the et al. (2008). landscape. We are still to pay the ‘ extinction declined further (see Box 5.1 Figure), with most debt ’ for the consequences of past actions. – 07, declines in the smaller fragments. By 2006 Identifying the duration of time ‐ lags and one species, the lemuroid ringtail possum forecasting the size of the extinction debt for ), was almost totally Hemibelideus lemuroides ( fi cult. The clearest fragmented landscapes is dif absent from fragments and regrowth forests insights come from long ‐ term studies that along streams and its abundance in these document changesincommunities. For example, habitats was only 0.02% of that in intact forest large nocturnal marsupials were surveyed in et al. (Laurance 2008). rainforest fragmentsin Queensland, Australia,in – 87 and again 20 years later in 2006 – 07 1986 et al. 2008). At the time of the fi rst (Laurance REFERENCES surveys, when fragments had been isolated for Laurance, W. F., Laurance, S. G., and Hilbert, D. W. (2008). 50 years, the fauna differed markedly from – 20 Long ‐ term dynamics of a fragmented that in extensive rainforest. Over the subsequent , rainforest mammal assemblage. Conservation Biology 20 years, even further changes occurred. 1164. – , 1154 22 Notably, the species richness in fragments had © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

108 1 93 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE required for a single individual or breeding unit, or for a self-sustaining population. Some species persist in fragmented landscapes by incorporating multiple fragments in their ter- ritory or daily foraging movements. In England, Strix aluco ) occupies territories of the tawny owl ( about 26 ha (hectares) in large deciduous woods, but individuals also persist in highly fragmented areas by including several small woods in their territory (Redpath 1995). There is a cost, however: individuals using multiple woods have lower breeding success and there is a higher turnover of territories between years. Species that require different kinds of habitats to meet regular needs (e.g. for foraging and breeding) can be greatly disadvantaged if these habitats become isolated. fi culty in Individuals may then experience dif moving between different parts of the landscape to obtain their required resources. Amphibians that move between a breeding pond and other habitat, such as overwintering sites in forest, are an example. Other attributes (in addition to fragment uence the occurrence of species in- fl size) that in clude the type and quality of habitat, fragment shape, land use adjacent to the fragment, and Variation in the spatial con guration of habitat in fi Figure 5.3 landscapes with similar cover of native vegetation: a) subdivision (many the extent to which the wider landscape isolates versus few patches); b) aggregated vs dispersed habitat; and c) compact populations. In the Iberian region of Spain, for vs complex shapes. All landscapes have 20% cover (shaded). example, the relative abundance of the Eurasian ) in large forest fragments is Meles meles badger ( landscapes need to know which species are most vulnerable to these processes. 1.0 0.9 0.8 0.7 5.3.1 Patterns of species occurrence 0.6 in fragmented landscapes 0.5 Many studies have described the occurrence of 0.4 species in fragments of different sizes, shapes, 0.3 composition, land-use and context in the land- Frequency of occurrence 0.2 scape. For species that primarily depend on 0.1 fragmented habitat, particularly animals, frag- 0.0 2–5 51–100 >100 21–50 6–10 11–20 ment size is a key in uence on the likelihood of fl occurrence (Figure 5.4). As fragment size de- Woodland area (ha) creases, the frequency of occurrence declines Frequency of occurrence of the common dormouse Figure 5.4 and the species may be absent from many ( ) in ancient semi natural woods in ‐ Muscardinus avellanarius small fragments. Such absences may be because ‐ Herefordshire, England, in relation to increasing size class of woods. Data from Bright (1994). et al. the fragment is smaller than the minimum area © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

109 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: 94 CONSERVATION BIOLOGY FOR ALL signi fl cantly in fi uenced by habitat quality and consequence of habitat fragmentation, but arise forest cover in the wider landscape (Virgos from land uses typically associated with subdivi- 2001). In areas with less than 20% forest cover, sion. Populations may decline due to deaths of uenced fl badger abundance in forests was most in individuals from the use of pesticides, insecti- by isolation (i.e. distance to a potential source cides or other chemicals; hunting by humans; 50% – 10 000 ha), whereas in areas with 20 > area harvesting and removal of plants; and construc- fl uenced by the qual- cover, badgers were most in tion of roads with ensuing road kills of animals. ity of habitat in the forest fragments. For example, in Amazonian forests, subsistence A key issue for conservation is the relative hunting by people compounds the effects of for- importance of habitat loss versus habitat frag- est fragmentation for large vertebrates such as the mentation (Fahrig 2003). That is, what is the rela- lowland tapir ( Tapir terrestris ) and white-lipped how much habitat remains in tive importance of ), and contributes to their Tayassu pecari peccary ( how fragmented it is? Studies the landscape versus local extinction (Peres 2001). of forest birds in landscapes in Canada and Aus- Commonly, populations are also affected by tralia suggest that habitat loss and habitat frag- factors such as logging, grazing by domestic signi both mentation are uences, cant in fi fl stock, or altered disturbance regimes that modify although habitat loss generally is a stronger in fl u- the quality of habitats and affect population ence for a greater proportion of species (Trczinski growth. For example, in Kibale National Park, an 1999; Radford and Bennett 2007). Important- et al. isolated forest in Uganda, logging has resulted in ly, species respond to landscape pattern in differ- long-term reduction in the density of groups of the ent ways. In southern Australia, the main Cercopithecus mitza )inheavily blue monkey ( Eopsaltria uence for the eastern yellow robin ( fl in logged areas: in contrast, populations of black ) was the total amount of wooded cover australis ) are higher in Colobus guereza and white colobus ( Col- in the landscape; for the grey shrike-thrush ( regrowth forests than in unlogged forest (Chap- luricincla harmonica ) it was wooded cover togeth- man 2000). Deterministic processes are partic- et al. fi guration (favoring aggregated er with its con fl uences on the status of plant ularly important in habitat); while for the musk lorikeet ( Glossopsitta species in fragments (Hobbs and Yates 2003). ) the in fl uential factor was not wooded concinna cover, but the con fi guration of habitat and diver- Isolation sity of vegetation types (Radford and Bennett Isolation of populations is a fundamental conse- 2007). quence of habitat fragmentation: it affects local populations by restricting immigration and emi- gration. Isolation is in fl uenced not only by the 5.3.2 Processes that affect species in fragmented distance between habitats but also by the effects landscapes ofhumanland-useontheabilityoforganismsto move (or for seeds and spores to be dispersed) The size of any population is determined by the through the landscape. Highways, railway lines, balance between four parameters: births, deaths, and water channels impose barriers to move- immigration, and emigration. Population size is ment, while extensive croplands or urban devel- increased by births and immigration of indivi- opment create hostile environments for many duals, while deaths and emigration of individuals organisms to move through. Species differ in reduce population size. In fragmented land- sensitivity to isolation depending on their type fl u- scapes, these population parameters are in of movement, scale of movement, whether they enced by several categories of processes. are nocturnal or diurnal, and their response to landscape change. Populations of one species Deterministic processes may be highly isolated, while in the same land- Many factors that affect populations in fragmen- scape individuals of another species can move ted landscapes are relatively predictable in their effect. These factors are not necessarily a direct freely. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

110 1 95 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE small initial population size. A decline in genetic Isolation affects several types of movements, diversity may make a population more vulnerable including: (i) regular movements of individuals to recessive lethal alleles or to changing environ- between parts of the landscape to obtain mental conditions. different requirements (food, shelter, breeding Fluctuations in the environment, such as varia- sites); (ii) seasonal or migratory movements of · tion in rainfall and food sources, which affect birth species at regional, continental or inter-continen- and death rates in populations. tal scales; and (iii) dispersal movements (immi- Small isolated populations are particularly vul- gration, emigration) between fragments, which · ood, fl nerable to catastrophic events such as fi re, may supplement population numbers, increase fi drought or hurricanes. A wild re, for example, the exchange of genes, or assist recolonization if may eliminate a small local population whereas in a local population has disappeared. In Western extensive habitats some individuals survive and Australia, dispersal movements of the blue- provide a source for recolonization. ) are breasted fairy-wren ( Malurus pulcherrimus affected by the isolation of fragments (Brooker and Brooker 2002). There is greater mortality of 5.3.3 Metapopulations and the conservation individuals during dispersal in poorly connected of subdivided populations areas than in well-connected areas, with this dif- ference in survival during dispersal being a key Small populations are vulnerable to local extinc- factor determining the persistence of the species tion, but a species has a greater likelihood of persistence where there are a number of local in local areas. populations interconnected by occasional move- For many organisms, detrimental effects of ments of individuals among them. Such a set isolation are reduced, at least in part, by habitat components that enhance connectivity in the me- “ of subdivided populations is often termed a landscape (Saunders and Hobbs 1991; Bennett ” (Hanski 1999). Two main kinds of tapopulation ” corridors “ 1999). These include continuous or metapopulation have been described (Figure 5.5). stepping stones ” of habitat that assist move- “ A mainland-island model is where a large main- 2003), or human land-uses et al. ments (Haddad land population (such as a conservation reserve) provides a source of emigrants that disperse (such as coffee-plantations, scattered trees in pas- to nearby small populations. The mainland pop- ture) that may be relatively benign environments ulation has a low likelihood of extinction, where- for many species (Daily et al. 2003). In tropical regions, one of the strongest in uences on the fl as the small populations become extinct relatively persistence of species in forest fragments is their frequently. Emigration from the mainland fi ed ability to live in, or move through, modi supplements the small populations, introduces habitats (Gascon 1999; Seker- et al. countryside ” “ new genetic material and allows recolonization 2002). et al. cioglu should local extinction occur. A second kind of metapopulation is where the set of interacting populations are relatively similar in size and all Stochastic processes have a likelihood of experiencing extinction (Fig- When populations become small and isolated, ure 5.5b). Although colonization and extinction they become vulnerable to a number of stochastic may occur regularly, the overall population per- (or chance) processes that may pose little threat to sists through time. larger populations. Stochastic processes include Hesperia comma The silver-spotted skipper ( ), a the following. rare butter fl y in the UK, appears to function as Stochastic variation in demographic parameters et al. a metapopulation (Hill 1996). In 1982, but- · such as birth rate, death rate and the sex ratio of ter fl ies occupied 48 of 69 patches of suitable offspring. grassland on the North Downs, Surrey. Over the Loss of genetic variation, which may occur due to next 9 years, 12 patches were colonized and seven · inbreeding, genetic drift, or a founder effect from a populations went extinct. Those more susceptible © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

111 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 96 Diagrammatic representation of two main types of metapopulation models: a) a mainland ‐ Figure 5.5 island metapopulation and b) metapopulation ‐ sized populations. Habitats occupied by a species are shaded, unoccupied habitat fragments are clear, and the arrows indicate typical with similar movements. Reprinted from Bennett (1999). to extinction were small isolated populations, 5.4 Effects of landscape change whereas the patches more likely to be colonized on communities were relatively large and close to other large 5.4.1 Patterns of community structure occupied patches. in fragmented landscapes The conservation management of patchily- distributed species is likely to be more effective by For many taxa ies, rodents, rep- fl birds, butter — taking a metapopulation approach than by focus- — tiles, vascular plants, and more species richness “ ing on individual populations. However, real in habitat fragments is positively correlated with ” populations differ from theoretical models. world fragment size. This is widely known as the Factors such as the quality of habitat patches and species-area relationship (Figure 5.6a). Thus, the nature of the land mosaic through which move- when habitats are fragmented into smaller pieces, ments occur are seldom considered in theoretical species are lost; and the likely extent of this loss models, which emphasize spatial attributes (patch can be predicted from the species-area relation- area, isolation). For example, in a metapopulation ship. Further, species richness in a fragment typi- of the Bay checkerspot butter Euphydryas editha y( fl cally is less than in an area of similar size within bayensis ) in California, USA, populations in topo- continuous habitat, evidence that the fragmenta- graphically heterogeneous fragments were less tion process itself is a cause of local extinction. likely to go extinct than those that were in topo- However, the species-area relationship does not graphically uniform ones. The heterogeneity reveal which particular species will be lost. provided some areas of suitable topoclimate each Three explanations given for the species-area year over a wide range of local climates (Ehrlich relationship (Connor and McCoy 1979) are that and Hanski 2004). small areas: (i) have a lower diversity of habitats; There also is much variation in the structure (ii) support smaller population sizes and therefore of subdivided populations depending on the fewer species can maintain viable populations; frequency of movements between them. At and (iii) represent a smaller sample of the original one end of a gradient is a dysfunctional meta- habitat and so by chance are likely to have fewer population where little or no movement oc- cult to species than a larger sample. While it is dif fi curs; while at the other extreme, movements distinguish between these mechanisms, the mes- aresofrequentthatitisessentiallyasingle sage is clear: when habitats are fragmented into patchy population. smaller pieces, species are lost. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

112 1 97 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE specialized ecological requirements are those 50 lost from communities in fragments. In several tropical regions, birds that follow trails of army 40 ants and feed on insects fl ushed by the ants in- clude specialized ant-following species and 30 others that forage opportunistically in this way. In rainforest in Kenya, comparisons of fl ocks of 20 ant-following birds between a main forest and Number of species forest fragments revealed marked differences 10 (Peters 2008). The species richness and num- et al. ber of individuals in ant-following fl ocks were 0 lower in fragments, and the composition of fl ocks 30 50 10 60 40 20 0 Area (ha) more variable in small fragments and degraded forest, than in the main forest. This was a conse- 60 quence of a strong decline in abundance of ve fi species of specialized ant-followers in fragments, 50 whereas the many opportunistic followers (51 species) were little affected by fragmentation 40 (Peters et al. 2008). The way in which fragments are managed is a 30 uence on the composi- particularly important in fl 20 tion of plant communities. In eastern Australia, Number of species for example, grassy woodlands dominated by 10 ) formerly covered white box ( Eucalyptus albens several million hectares, but now occur as small 0 0 60 10 20 30 50 40 fragments surrounded by cropland or agricultur- Tree cover (%) al pastures. The species richness of native under- story plants increases with fragment size, as Figure 5.6 Species ‐ area relationships for forest birds: a) in forest fragments of different sizes in eastern Victoria, Australia (data from Loyn expected, but tree clearing and grazing by domes- 2 1997); b) in 24 landscapes (each 100 km ) with differing extent of fl tic stock are also strong in uences (Prober and remnant wooded vegetation, in central Victoria, Australia (data from Thiele 1995). The history of stock grazing has the Radford 2005). The piecewise regression highlights a threshold et al. oristic composition in fl strongest in uence on the fl response of species richness to total extent of wooded cover. woodland fragments: grazed sites have a greater invasion by weeds and a more depauperate na- Factors other than area, such as the spatial and fl ora. tive temporal isolation of fragments, land management The composition of animal communities in fi cant predic- or habitat quality may also be signi fragments commonly shows systematic changes tors of the richness of communities in fragments. in relation to fragment size. Species-poor commu- In Tanzania, for example, the number of forest- nities in small fragments usually support a subset understory bird species in forest fragments (from of the species present in larger, richer fragments 0.1 to 30 ha in size) was strongly related to frag- (Table 5.1). That is, there is a relatively predict- ment size, as predicted by the species-area rela- able change in composition with species tionship (Newmark 1991). After taking fragment ” “ dropping out in an ordered sequence in succes- size into account, further variation in species rich- sively smaller fragments (Patterson and Atmar ness was explained by the isolation distance of 1986). Typically, rare and less common species each fragment from a large source area of forest. occur in larger fragments, whereas those present Species show differential vulnerability to in smaller fragments are mainly widespread and fragmentation. Frequently, species with more- nested subset “ ” common. This kind of pattern © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

113 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 98 Table 5.1 A diagrammatic example of a nested subset pattern of of communities. The loss of a species or a change J) within habitat fragments (1 – – distribution of species (A 9). in its abundance, particularly for species that in- teract with many others, can have a marked effect Species Fragments on ecological processes throughout fragmented 123456789 landscapes. A ++++ ++++ Changes to predator-prey relationships, for ex- B +++ ++++ ample, have been revealed by studies of the level of + + C +++++ nests in fragmented landscapes ’ predationonbirds D +++++ + ++++++ E (Wilcove 1985). An increase in the amount of forest ++ F edge, a direct consequence of fragmentation, in- +++ G creases the opportunity for generalist predators H ++ ed land-uses to associatedwithedgesormodi fi +++ I prey on birds that nest in forest fragments. In Swe- + J cial fi den, elevated levels of nest predation (on arti eggs in experimental nests) were recorded in agri- cultural land and at forest edges compared with has been widely observed: for example, in butter- the interior of forests (Andrén and Angelstam fl y communities in fragments of lowland rainfor- 1988). Approximately 45% of nests at the forest 2006). et al. est in Borneo (Benedick edge were preyed upon compared with less than At the landscape level, species richness has fre- > 200 m into the forest. At the 10% at distances quently been correlated with heterogeneity in the landscape scale, nest predation occurred at a great- landscape. This relationship is particularly rele- er rate in agricultural and fragmented forest land- vant in regions, such as Europe, where human scapes than in largely forested landscapes (Andrén land-use has contributed to cultural habitats that 1992). The relative abundance of different corvid complement fragmented natural or semi-natural species, the main nest predators, varied in relation habitats. In the Madrid region of Spain, the overall to landscape composition. The hooded crow richness of assemblages of birds, amphibians, rep- ) occurred in greatest abun- ( Corvus corone cornix 2 landscapes is tiles and butter fl ies in 100 km dance in heavily cleared landscapes and was pri- strongly correlated with the number of different marily responsible for the greater predation land-uses in the landscape (Atauri and De Lucio pressure recorded at forest edges. 2001). However, where the focus is on the com- Many mutualisms involve interactions be- munity associated with a particular habitat type tween plants and animals, such as occurs in the fl (e.g. rainforest butter ies) rather than the entire pollination of owering plants by invertebrates, fl uence assemblage of that taxon, the strongest in fl birds or mammals. A change in the occurrence or on richness is the total amount of habitat in the abundance of animal vectors, as a consequence of landscape. For example, the richness of woodland- fragmentation, can disrupt this process. For many dependent birds in fragmented landscapes in plant species, habitat fragmentation has a nega- southern Australia was most strongly in fl uenced tive effect on reproductive success, measured in by the total extent of wooded cover in each 100 terms of seed or fruit production, although the 2 landscape, with a marked threshold around km relative impact varies among species (Aguilar 10% cover below which species richness declined et al. 2006). Plants that are self-incompatible rapidly (Figure 5.6b) (Radford 2005). et al. (i.e. that depend on pollen transfer from another plant) are more susceptible to reduced reproduc- tive success than are self-compatible species. This 5.4.2 Processes that affect community structure difference is consistent with an expectation that pollination by animals will be less effective in Interactions between species, such as predation, small and isolated fragments. However, pollina- competition, parasitism, and an array of mutual- fl uence on the structure isms, have a profound in tors are a diverse group and they respond to © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

114 1 99 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE fragmentation in a variety of ways (Hobbs and smaller fragments, a likely consequence of the Yates 2003). smaller population sizes of species and the great- Changes in ecological processes in fragments er vulnerability of such fragments to external dis- and throughout fragmented landscapes are com- turbances. For example, based on a sequence of plex and poorly understood. Disrupted interac- surveys of understory birds in tropical forest frag- ow-on effects fl tions between species may have ments at Manaus, Brazil, an estimate of the time to many other species at other trophic levels. How- taken for fragments to lose half their species was ever, the kinds of changes to species interactions approximately 5 years for 1 ha fragments, 8 years and ecological processes vary between ecosystems for 10 ha fragments, and 12 years for a 100 ha and regions because they depend on the particular fragment (Ferraz 2003). et al. sets of species that occur. In parts of North Ameri- Ecological processes within fragments also ex- ca, nest parasitism by the brown-headed cowbird perience ongoing changes in the years after isola- ( Molothrus ater ) has a marked effect on bird com- tion because of altered species interactions and munities in fragments (Brittingham and Temple incremental responses to biophysical changes. 1983); while in eastern Australia, bird commu- One example comes from small fragments of nities in small fragments may be greatly affected tropical dry forest that were isolated by rising by aggressive competition from the noisy miner water in a large hydroelectric impoundment Manorina melanocephala ( 1997). Both of )(Grey et al. in Venezuela (Terborgh 2001). On small et al. these examples are idiosyncratic to their region. ( < – 12 ha) fragments, isola- 1 ha) and medium (8 fi They illustrate the dif culty of generalizing the tion resulted in a loss of large predators typical of effects of habitat fragmentation, and highlight the extensive forest. Seed predators (small rodents) importance of understanding the consequences of and herbivores (howler monkeys Alouatta senicu- landscape change in relation to the environment, lus Iguana iguana , iguanas , and leaf-cutter ants) context and biota of a particular region. became hyperabundant in these fragments, with cascading effects on the vegetation. Compared with extensive forest, fragments experienced re- duced recruitment of forest trees, changes in veg- 5.5 Temporal change in fragmented fi etation composition, and dramatically modi ed landscapes faunal communities, collectively termed an “ eco- Habitat loss and fragmentation do not occur in a (Terborgh 2001). et al. ” logical meltdown single event, but typically extend over many dec- ades. Incremental changes occur year by year as remaining habitats are destroyed, reduced in size, 5.6 Conservation in fragmented or further fragmented (Figure 5.2). Landscapes landscapes fi are also modi ed through time as the human Conservation of biota in fragmented landscapes population increases, associated settlements ex- is critical to the future success of biodiversity pand, and new forms of land use are introduced. conservation and to the well-being of humans. In addition to such changes in spatial pattern, National parks and dedicated conservation re- habitat fragmentation sets in motion ongoing serves are of great value, but on their own are changes within fragments and in the interactions ciently represen- too few, too small, and not suf fi between fragments and their surroundings. tative to conserve all species. The future status of When a fragment is rst isolated, species richness fi a large portion of Earth s biota depends on ’ does not immediately fall to a level commensu- how effectively plants and animals can be main- rate with its long-term carrying capacity; rather, a tained in fragmented landscapes dominated by termed gradual loss of species occurs over time — agricultural and urban land-uses. Further, the . That is, there is a time-lag in ” species relaxation “ persistence of many species of plants and animals experiencing the full effects of fragmentation in these landscapes is central to maintaining (see Box 5.1). The rate of change is most rapid in © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

115 Conservation Biology for All Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 100 Provide speci c habitat features required by par- fi ecosystem services that sustain food production, · ticular species (e.g. tree hollows, rock crevices, clean water, and a sustainable living environment ” specimen “ rainforest trees used by rainforest for humans. Outlined below are six kinds of ac- birds in agricultural countryside). tions necessary for a strategic approach to conser- vation in fragmented landscapes. 5.6.3 Manage across entire landscapes Managing individual fragments is rarely effective 5.6.1 Protect and expand the amount of habitat because even well managed habitats can be de- graded by land uses in the surrounding environ- Many indicators of conservation status, such as ment. Further, many species use resources from population sizes, species richness, and the occur- different parts of the landscape; and the pattern rence of rare species, are positively correlated and composition of land uses affect the capacity with the size of individual fragments or the total of species to move throughout the landscape. amount of habitat in the landscape. Consequent- Two broad kinds of actions relating to the wider ly, activities that protect and expand natural and landscape are required: semi-natural habitats are critical priorities in maintaining plant and animal assemblages (see fi c issues that have degrading im- Manage speci · also Chapter 11). These include measures that: pacts across the boundaries of fragments, such as pest plants or animals, soil erosion, sources of pollu- Prevent further destruction and fragmentation of · tion or nutrient addition, and human recreational habitats. pressure. Increase the size of existing fragments and the · Address issues that affect the physical environ- total amount of habitat in the landscape. · ment and composition of the land mosaic across Increase the area speci fi cally managed for conser- · broad scales, such as altered hydrological regimes vation. and the density of roads and other barriers. Give priority to protecting large fragments. · All fragments contribute to the overall amount 5.6.4 Increase landscape connectivity and pattern of habitat in a landscape; consequent- ly, incremental loss, even of small fragments, has Measures that enhance connectivity and create a wider impact. linked networks of habitat will bene fi t the conser- vation of biota in fragmented landscapes. Con- nectivity can be increased by providing speci c fi linkages, such as continuous corridors or step- 5.6.2 Enhance the quality of habitats ping stones, or by managing the entire mosaic to Measures that enhance the quality of existing allow movements of organisms. Actions that en- habitats and maintain or restore ecological pro- hance connectivity include: cial. Such management actions fi cesses are bene Protecting connecting features already present, c goals relevant fi must be directed toward speci · such as streamside vegetation, hedges and live to the ecosystems and biota of concern. These fences. include actions that: Filling gaps in links or restoring missing connec- · Control degrading processes, such as the inva- tions. · sion of exotic plants and animals. Maintaining stepping-stone habitats for mobile · Manage the extent and impact of harvesting nat- species (such as migratory species). · ural resources (e.g. timber, fi rewood, bushmeat). Retaining broad habitat links between conserva- · Maintain natural disturbance regimes and the tion reserves. · conditions suitable for regeneration and establish- Developing regional and continental networks of · ment of plants. habitat (see Boxes 5.2 and 5.3). © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

116 1 101 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE Box 5.2 Gondwana Link: a major landscape reconnection project Denis A. Saunders and Andrew F. Bennett The southwest region of Australia is one of In many locations throughout the world, ” hotspots “ s 34 biodiversity ’ the world .Itis conservation organizations and community particularly rich in endemic plant species. The groups are working together to protect and region has undergone massive changes over restore habitats as ecological links between the past 150 years as a result of development isolated areas. These actions are a ‐ otherwise for broadscale agricultural cropping and practical response to the threats posed by raising of livestock. Over 70% of the area of habitat destruction and fragmentation and are native vegetation has been removed. The undertaken at a range of scales, from local to remaining native vegetation consists of western ‐ continental. Gondwana Link, in south thousands of fragments, most of which are less Australia, is one such example of an ambitious than 100 ha. Many areas within the region plan to restore ecological connectivity and have less than 5 – 10% of their original enhance nature conservation across a large vegetation remaining. geographic region. continues west Western Australia. Shaded areas indicate remnant Box 5.2 Figure Diagrammatic representation of the Gondwana Link in south ‐ native vegetation. continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

117 Conservation Biology for All Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do 102 CONSERVATION BIOLOGY FOR ALL Box 5.2 (Continued) and Plate 6). It also involves protecting and This massive removal of native vegetation managing the fragments of native vegetation has led to a series of changes to ecological that they are reconnecting. processes, producing a wide range of problems The groups believe that by increasing that must be addressed. Without some form of connectivity and restoring key habitats they remedial action, over 6 million hectares of land will enable more mobile species that are (30% of the region ’ s cleared land) will become dependent on native vegetation to move safely salinized over the next 50 years, over 50% of between isolated populations. This should vegetation on nature reserves will be reduce the localized extinctions of species from destroyed, around 450 endemic species of plant isolated fragments of native vegetation that is will become extinct, over half of all bird species happening at present. Gondwana Link should from the region will be adversely affected, and also allow species to move as climatic no potable surface water will be available in conditions change over time. The revegetation the region because of water pollution by salt. should also have an impact on the hydrological Addressing the detrimental ecological regime by decreasing the amount of water consequences involves the revegetation, with entering the ground water, and reduce the deep rooted trees and shrubs, of up to 40% of ‐ quantity of sediment and pollution from cleared land in the region. Gondwana Link is an agriculture entering the river and estuarine ambitious conservation project involving systems. individuals, local, regional and national groups In addition to addressing environmental addressing these detrimental ecological issues the project is speeding up the consequences. The objective of Gondwana Link development of new cultural and economic is to restore ecological connectivity across ways for the region ’ s human population to south ‐ western Australia. The aim is to provide exist sustainably. ecological connections from the tall wet forests of the southwest corner of the state to the dry woodland in the arid interior. This will involve protecting and replanting native vegetation Relevant website that stretches over 1000 ” living link along a “ km from the wettest corner of Western • Gondwana Link: http://gondwanalink.org/ Australia into the arid zone (see Box 5.2 Figure index.html. Box 5.3 Rewilding Paul R. Ehrlich facilitating the recovery of strongly interactive Some conservation scientists believe that the species, including predators. Rewilding is the ultimate cure for habitat loss and ” goal of the “ Wildlands Network, an effort led fragmentation that is now spreading like by Michael Soulé and Dave Foreman (Foreman ecological smallpox over Earth is a radical form 2004). The plan is to re-connect relatively of restoration, called rewilding in North undisturbed, but isolated areas of North America. The objective of rewilding is to restore America, into extensive networks in which ‐ resilience and biodiversity by re connecting large mammals such as bears, mountain lions, severed habitats over large scales and by continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

118 1 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE 103 Box 5.3 (Continued) states more like those that prevailed before wolves, elk, and even horses and elephants industrial society accelerated the (which disappeared from North America only transformation of the continent. Similar 11 000 years ago) can roam free and resume rewilding projects on other continents are their important ecological roles in ecosystems now in the implementation stage as in the — where con fl ict with humans would be minimal. in Australia (see Box 5.2). Gondwana Link “ ” Rewilding would restore landscape linkages — The possible downsides to rewilding include employing devices from vegetated overpasses the spread of some diseases, invasive species, over highways to broad habitat corridors — fi and res and the social and economic fl ora allowing the free movement of fauna and consequences of increased livestock and accommodation to climate change. The depredation caused by large, keystone cooperation of government agencies and predators (as have accompanied wolf willing landowners would eventually create reintroduction programs) (Maehr et al. four continental scale wildways (formerly 2001). Careful thought also is needed about called MegaLinkages): thesizeoftheseWildways;tobesurethey Paci fi From southern Alaska c Wildway: are large enough for these species to again through the Coast Range of British Col- ” “ old homes persist in their . Nonetheless, it umbia, the Cascades, and the Sierra Ne- seems clear that such potential costs of vada to the high mountains of northern rewilding would be overwhelmed by the Baja California. ts that ecological and economic-cultural bene fi From Spine of the Continent Wildway: well designed and monitored reintroductions the Brooks Range of Alaska through the could provide. Rocky Mountains to the uplands of West- ern Mexico. Atlantic Wildway: From the Canadian REFERENCES AND SUGGESTED READING Maritime south, mostly through the Appalachians to Okefenokee and the (2006). Pleisto- et al. Donlan, J. C., Berger, J., Bock, C. E., Everglades. cene rewilding: an optimistic agenda for twenty- rst fi Arctic-Boreal Wildway: Northern North century conservation. American Naturalist , 168 , America from Alaska through the Canadi- – 681. 660 an arctic/subarctic to Labrador with an ex- Foreman, D. (2004). Rewilding North America: a vision tension into the Upper Great Lakes. st for conservation in the 21 . Island Press, Century Many critical ecological processes are Washington, DC. mediated by larger animals and plants, and Large Maehr, D. S., Noss, R. F., and Larkin, J. L., eds (2001). the recovery, dispersal, and migration of these mammal restoration: ecological and sociological chal- keystone and foundation species (species that lenges in the 21st centuary . Island Press, Washington, are critical in maintaining the structure of DC. communities disproportionately more than Soulé, M. E. and Terborgh, J. (1999). Continental conser- their relative abundance) is essential if nature vation: scienti fi c foundations of regional reserve net- is to adapt to stresses such a climate change works . Island Press, Washington, DC. and habitat loss caused by energy Soulé, M. E., Estes, J. A., Miller, B., and Honnold, D. L. development, sprawl, and the proliferation of (2005). Highly interactive species: conservation roads. Rewilding will help restore ecosystems policy, management, and ethics. BioScience , 55 , in the Wildways to structural and functional 176. – 168 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

119 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 104 profound in fl uence on fragments and their biota, 5.6.5 Plan for the long term particularly at fragment edges. Landscape change is ongoing. Over the long- Different species have different ecological attri- · term, incremental destruction and fragmenta- butes (such as scale of movement, life-history stages, tion of habitats have profound consequences fl what constitutes habitat) which in uence how a for conservation. Long-term planning is re- species perceives a landscape and its ability to sur- quired to sustain present conservation values fi vive in modi ed landscapes. and prevent foreclosure of future options. Differences in the vulnerability of species to land- · Actions include: scape change alter the structure of communities and modify interactions between species (e.g. pollina- Using current knowledge to forecast the likely · tion, parasitism). consequences if ongoing landscape change occurs. Changes within fragments, and between frag- Developing scenarios as a means to consider al- · · ments and their surroundings, involve time-lags be- ternative future options. fore the full consequences of landscape change are Developing a long-term vision, shared by the · experienced. wider community, of land use and conservation Conservation in fragmented landscapes can be goals for a particular region. · enhanced by: protecting and increasing the amount of habitat, improving habitat quality, increasing connectivity, managing disturbance processes in 5.6.6 Learn from conservation actions the wider landscape, planning for the long term, Effective conservation in fragmented landscapes and learning from conservation actions undertaken. demands that we learn from current management in order to improve future actions. Several issues include: Suggested reading Integrating management and research to more Land mosaics. The ecology of land- Forman, R. T. T. (1995). · effectively evaluate and re fi ne conservation mea- . Cambridge University Press, Cam- scapes and regions sures. bridge, UK. Monitoring the status of selected species Hobbs, R. J. and Yates, C. J. (2003). Turner Review No. 7. · Impacts of ecosystem fragmentation on plant popula- and ecological processes to evaluate the longer- Australian Journal tions: generalising the idiosyncratic. term outcomes and effectiveness of conservation , 471 51 of Botany , 488. – actions. Tropical Laurance, W. F. and Bierregard, R. O., eds (1997). forest remnants: ecology, management, and conservation of Summary fragmented communities . University of Chicago Press, Chicago, Illinois. Destruction and fragmentation of habitats are Lindenmayer, D. B. and Fischer, J. (2006). Habitat fragmen- · major factors in the global decline of species, the tation and landscape change. An ecological and conservation cation of native plant and animal commu- modi fi . CSIRO Publishing, Melbourne, Australia. synthesis nities and the alteration of ecosystem processes. Habitat destruction, habitat fragmentation (or · subdivision) and new forms of land use are closely Relevant websites intertwined in an overall process of landscape change. Sustainable forest partnerships: http://sfp.cas.psu. · Landscape change is not random: dispropor- edu/fragmentation/fragmentation.html. · tionate change typically occurs in fl atter areas, Smithsonian National Zoological Park, Migratory · at lower elevations and on more-productive soils. Bird Center: http://nationalzoo.si.edu/Conservation Altered physical processes (e.g. wind and water AndScience/ MigratoryBirds/Research/Forest_ · fl ows) and the impacts of human land-use have a Fragmentation/default.cfm. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

120 1 105 HABITAT FRAGMENTATION AND LANDSCAPE CHANGE United States Department of Agriculture, Forest ricultural landscapes of Costa Rica. Conservation Biology , · Service: http://nationalzoo.si.edu/Conservation – , 1814 17 1826. AndScience/MigratoryBirds/Research/Forest_ Ehrlich, P. and Hanski, I., eds (2004). On the wings of check- Fragmentation/default.cfm. erspots: A model system for population biology . Oxford Uni- versity Press, Oxford, UK. Mongabay: http://www.mongabay.com. · Fahrig, L. (2003). Effects of habitat fragmentation on biodi- , Annual Review of Ecology and Systematics 34 , 487 – versity. 515. Ferraz, G., Russell, G. J., Stouffer, P. C., Bierregaard, R. O., REFERENCES Pimm, S. L., and Lovejoy, T. E. (2003). Rates of species Aguilar, R., Ashworth, L., Galetto, L., and Aizen, M. A. Proceedings loss from Amazonian forest fragments. (2006). Plant reproductive susceptibility to habitat frag- of the National Academy of Sciences, United States of mentation: review and synthesis through a meta-analy- – 14073. 100 , America , 14069 – 980. sis. Ecology Letters , 9 , 968 Ferris-Kaan, R. (1995). Management of linear habitats for Andrén, H. (1992). Corvid density and nest predation in wildlife in British forests. In D. A. Saunders, J. L. Craig, relation to forest fragmentation: a landscape perspective. and E. M. Mattiske, eds Nature conservation 4: the role of , 794 73 , Ecology 804. – , pp. 67 77. Surrey Beatty and Sons, Chipping – networks Andrén, H. and Angelstam, P. (1988). Elevated predation Norton, Australia. rates as an edge effect in habitat islands: experimental Fischer, J., Lindenmayer, D. B., and Fazey, I. (2004). Ap- , 69 , 544 – evidence. 547. Ecology preciating ecological complexity: habitat contours as a Atauri, J. A. and De Lucio, J. V. (2001). The role of land- , conceptual landscape model. 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Harvey, C. A., Medina, A., Sanchez, D., 233. , Wildlife Research , 225 29 – tralian wheatbelt. terns of animal diversity in different forms of tree cover Chapman, C. A., Balcomb, S. R., Gillespie, T. R., Skorupa, , in agricultural landscapes. 16 , Ecological Applications J. P., and Struhsaker, T. T. (2000). Long-term effects of 1986 – 1999. logging on African primate communities: a 28 year com- Hill, J. K., Thomas, C. D., and Lewis, O. T. (1996). Effects of Conserva- parison from Kibale National Park, Uganda. Hesperia habitat patch size and isolation on dispersal by 14 , tion Biology 217. – , 207 fl comma butter ies: implications for metapopulation Connor, E. F. and Mccoy, E. D. (1979). The statistics and , 725 65 , 735. structure. Journal of Animal Ecology – biology of the species-area relationship. American Natu- Hobbs, R. J. (1993). 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121 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 106 CONSERVATION BIOLOGY FOR ALL Radford, J. Q. and Bennett, A. F. (2007). The relative impor- Australian populations: generalising the idiosyncratic. tance of landscape properties for woodland birds in – Journal of Botany 51 , 488. , 471 44 , Journal of Applied Ecology agricultural environments. , Laurance, W. F. (2008). Theory meets reality: how habitat – 737 747. fragmentation research has transcended island biogeo- Radford, J. Q., Bennett, A. F., and Cheers, G. J. (2005). – Biological Conservation , 141 , 1731 graphic theory. 1744. Landscape-level thresholds of habitat cover for wood- Lindenmayer, D. B. and Fischer, J. (2006). Habitat fragmen- land-dependent birds. , 124 , Biological Conservation tation and landscape change. An ecological and conservation – 317 337. synthesis . CSIRO Publishing, Melbourne, Australia. Redpath, S. M. (1995). Habitat fragmentation and the indi- Loyn, R. H. (1987). Effects of patch area and habitat on bird vidual: tawny owls in woodland patches. Strix aluco abundances, species numbers and tree health in fragmen- , , 652 – 661. Journal of Animal Ecology 64 ted Victorian forests. In D. A. Saunders, G. W. Arnold, A. Ricketts, T. H. (2001). The matrix matters: effective isola- Nature conserva- A. Burbidge, and A. J. M. Hopkins, eds The American Naturalist tion in fragmented landscapes. , tion: the role of remnants of native vegetation – ,pp.65 77. 158 ,87 – 99. Surrey Beatty and Sons, Chipping Norton, Australia. Nature conser- Saunders, D. A. and Hobbs, R. J., eds (1991). Lunt, I. D. and Spooner, P. G. (2005). Using historical vation 2: The role of corridors. Surrey Beatty & Sons, Chip- ecology to understand patterns of biodiversity in frag- ping Norton, New South Wales. mented agricultural landscapes. , Journal of Biogeography Saunders, D. A., Hobbs, R. J., and Arnold, G. W. (1993). The 32 , 1859 – 1873. Kellerberrin project on fragmented landscapes: a review of The theory of MacArthur, R. H. and Wilson, E. O. (1967). 64 ,185 current information. – , Biological Conservation 192. . Princeton University Press, Prince- island biogeography Saunders, D. A., Hobbs, R. J., and Margules, C. R. (1991). ton, New Jersey. Biological consequences of ecosystem fragmentation: a McGarigal, K. and Cushman, S. A. (2002). Comparative 32. 5 ,18 , Conservation Biology review. – evaluation of experimental approaches to the study of Sekercioglu, C. H., Ehrlich, P. R., Daily, G. C., Aygen, D., habitat fragmentation effects. Ecological Applications , 12 , Goehring, D., and Sandi, R. F. (2002). Disappearance of 335 345. – insectivorous birds from tropical forest fragments. Pro- McIntyre, S. and Hobbs, R. (1999). A framework for con- ceedings of the National Academy of Sciences of the United ceptualizing human effects on landscapes and its rele- 267. – States of America , 263 99 , Conservation vance to management and research models. real “ Soulé, M. E. (1986). Conservation biology and the – 1292. Biology , 13 , 1282 Conservation biology. The . In M. E. Soule, ed. ” world Newmark, W. D. (1991). Tropical forest fragmentation and – 12. Sinauer Associ- , pp. 1 science of scarcity and diversity the local extinction of understory birds in the Eastern ates, Sunderland, Massachusetts. Usambara Mountains, Tanzania. Conservation Biology , 5 , Terborgh, J., Lopez, L., Nunez V. P., (2001). Ecological et al. 67 – 78. Science 294 , meltdown in predator-free forest fragments. Patterson, B. D. and Atmar, W. (1986). Nested subsets and , the structure of insular mammalian faunas and archipe- 1923 1926. – 28 ,65 , – Biological Journal of the Linnean Society lagoes. 82. Trzcinski, M. K., Fahrig, L., and Merriam, G. (1999). Inde- Peres, C. A. (2001). Synergistic effects of subsistence hunt- pendent effects of forest cover and fragmentation on the ing and habitat fragmentation on Amazonian forest ver- distribution of forest breeding birds. Ecological Applica- tebrates. 15 , 1490 – 1505. , Conservation Biology – , , 586 9 593. tions Peters, M. K., Likare, S., and Kraemar, M. (2008). Effects of Virgos, E. (2001). Role of isolation and habitat quality in ocks of African habitat fragmentation and degradation on fl Meles shaping species abundance: a test with badgers ( 858. Ecological Applications – ,847 ant-following birds. , 18 L.) in a gradient of forest fragmentation. Journal of meles Biogeography , 28 , 381 – 389. Prober, S. M. and Thiele, K. R. (1995). Conservation of the Wilcove, D. S. (1985). Nest predation in forest tracts grassy white box woodlands: relative contributions of and the decline of migratory songbirds. 66 , Ecology , oristic composition and diver- fl size and disturbance to 1214. 1211 – , Australian Journal of Botany sity of remnants. 366. , 349 43 – © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

122 1 CHAPTER 6 Overexploitation Carlos A. Peres In an increasingly human-dominated world, habitat and the rates at which resources are har- where most of us seem oblivious to the liquida- ciency of exploitation by fi vested. Furthermore, ef ’ s natural resource capital (Chapters tion of Earth consumers and the highly variable intrinsic resil- 3 and 4), exploitation of biological populations ience to exploitation by resource populations may has become one of the most important threats have often evolved over long periods. Central to to the persistence of global biodiversity. Many these differences are species traits such as the regional economies, if not entire civilizations, population density (or stock size), the per capita have been built on free-for-all extractive indus- growth rate of the population, spatial diffusion tries, and history is littered with examples of from other less harvested populations, and the boom-and-bust economic cycles following the direction and degree to which this growth re- emergence, escalation and rapid collapse of un- sponds to harvesting through either positive or sustainable industries fuelled by raw renewable negative density dependence. For example, many resources. The economies of many modern long-lived and slow-growing organisms are par- nation-states still depend heavily on primary ex- ticularly vulnerable to the additive mortality re- fi sheries and logging, tractive industries, such as sulting from even the lightest offtake, especially if and this includes countries spanning nearly the these traits are combined with low dispersal rates entire spectrum of per capita Gross National that can inhibit population diffusion from adja- Product (GNP), such as Iceland and Cameroon. cent unharvested source areas, should these be Human exploitation of biological commodities available. These species are often threatened by involves resource extraction from the land, fresh- overhunting in many terrestrial ecosystems, un- water bodies or oceans, so that wild animals, sustainable logging in tropical forest regions, cac- plants or their products are used for a wide vari- in deserts, over ” rustling “ tus shing in marine fi ety of purposes ranging from food to fuel, shelter, and freshwater ecosystems, or many other forms ber, construction materials, household and gar- fi of unsustainable extraction. For example, over- den items, pets, medicines, and cosmetics. Over- hunting is the most serious threat to large verte- exploitation occurs when the harvest rate of any et al. brates in tropical forests (Cunningham 2009), given population exceeds its natural replacement and overexploitation, accidental mortality and rate, either through reproduction alone in closed persecution caused by humans threatens approx- populations or through both reproduction and fth (19%) of all tropical forest verte- fi imately one- immigration from other populations. Many spe- brate species for which the cause of decline has cies are relatively insensitive to harvesting, re- been documented [Figure 6.1; IUCN (Internation- maining abundant under relatively high rates of al Union for Conservation of Nature) 2007]. offtake, whereas others can be driven to local Overexploitation is the most important cause extinction by even the lightest levels of offtake. of freshwater turtle extinctions (IUCN 2007) and Fishing, hunting, grazing, and logging are classic fi the third-most important for freshwater sh ex- consumer-resource interactions and in natural tinctions, behind the effects of habitat loss and systems such interactions tend to come into equi- introduced species (Harrison and Stiassny 1999). librium with the intrinsic productivity of a given Thus, while population declines driven by habitat 107 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

123 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 108 Mammal Amphibian Bird Total 2000 4000 6000 0 12000 10000 8000 ecies p ical forest s p Number of tro Importance of threats to tropical forest terrestrial vertebrate species other than reptiles, which have not yet been assessed. Horizontal bars Figure 6.1 ed as vulnerable, fi indicate the total number of species occurring in tropical forests; dark grey bars represent the fraction of those species classi ices endangered, critically endangered or extinct in the wild according to the IUCN (2007) Red List of Threatened Species (www.iucnredlist.org). Dark sl in pie charts indicate the proportion of species for which harvesting, accidental mortality or persecution by humans is the primary cause of populati on declines. loss and degradation quite rightly receive a great then explore impacts of exploitation on both tar- deal of attention from conservation biologists get and non-target species, as well as cascading (MEA 2006), we must also contend with the spec- effects on the ecosystem. This leads to a re fl ection ‘ ’ half-empty ‘ or ’ empty ter of the forests, savan- at the end of this chapter of resource management nahs, wetlands, rivers, and seas, even if the considerations in the real-world, and the clashes physical habitat structure of a given ecosystem of culture between those concerned with either remains otherwise unaltered by other anthropo- the theoretical underpinnings or effective policy genic processes that degrade habitat quality (see solutions addressing the predicament of species Chapter 4). Overexploitation also threatens frogs: imperiled by overexploitation. with Indonesia the main exporter of frog legs for et al. markets in France and the US (Warkentin 2009). Up to one billion wild frogs are estimated 6.1 A brief history of exploitation to be harvested every year for human consump- Our rapacious appetite for both renewable and tion (Warkentin et al. 2009). non-renewable resources has grown exponential- I begin this chapter with a consideration of when early — ly from our humble beginnings why people exploit natural populations, includ- humans exerted an ecological footprint no larger ing the historical impacts of exploitation on wild — than that of other large omnivorous mammals plants and animals. This is followed by a review to currently one of the main driving forces in of effects of exploitation in terrestrial and aquatic reorganizing the structure of many ecosystems. biomes. Throughout the chapter, I focus on tropi- Humans have subsisted on wild plants and ani- cal forests and marine ecosystems because many mals since the earliest primordial times, and most plant and animal species in these realms have contemporary aboriginal societies remain pri- succumbed to some of the most severe and least marily extractive in their daily quest for food, understood overexploitation-related threats to fi medicines, ber and other biotic sources of raw population viability of contemporary times. I © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

124 1 109 OVEREXPLOITATION materials to produce a wide range of utilitarian and formed dense clusters along 3000 km of coast- and ornamental artifacts. Modern hunter-gath- rst fi al Atlantic forest. This species sustained the erers and semi-subsistence farmers in tropical trade cycle between the new Portuguese colony ecosystems, at varying stages of transition to an and European markets and was relentlessly agricultural economy, still exploit a large number nally became fi exploited from 1500 to 1875 when it of plant and animal populations. economically extinct (Dean 1996). Today, speci- fi nition, exploited species extant today By de fi mens of Pau-Brasil trees are largely con ned to have been able to co-exist with some background herbaria, arboreta and a few private collections. level of exploitation. However, paleontological The aftershock of modern human arrival is still evidence suggests that prehistoric peoples have being felt in many previously inaccessible tropical been driving prey populations to extinction long forest frontiers, such as those in parts of Amazo- before the emergence of recorded history. The nia, where greater numbers of hunters wielding late Paleolithic archaeology of big-game hunters fi rearms are emptying vast areas of its harvest- in several parts of the world shows the sequential sensitive megafauna (Peres and Lake 2003). collapse of their majestic lifestyle. Flint spear- In many modern societies, the exploitative heads manufactured by western European Cro- value of wildlife populations for either subsis- Magnons became gradually smaller as they tence or commercial purposes has been gradually shifted down to ever smaller kills, ranging in replaced by recreational values including both size from mammoths to rabbits (Martin 1984). consumptive and non-consumptive uses. In Human colonization into previously people-free 1990, over 20 million hunters in the United States islands and continents has often coincided with a eld in pursuit of fi spent over half a billion days a rapid wave of extinction events resulting from the nance vast fi wild game, and hunting licenses sudden arrival of novel consumers. Mass extinc- conservation areas in North America. In 2006, tion events of large-bodied vertebrates in Europe, ~87.5 million US residents spent ~US$122.3 bil- parts of Asia, North and South America, Mada- lion in wildlife-related recreational activities, in- gascar, and several archipelagos have all been cluding ~US$76.6 billion spent on shing and/or fi attributed to post-Pleistocene human overkill hunting by 33.9 million people (US Census Bu- (Martin and Wright 1967; Steadman 1995; McKin- reau 2006). Some 10% of this total is spent hunt- ney 1997; Alroy 2001). These are relatively well ing white-tailed deer alone (Conover 1997). corroborated in the (sub)fossil record but many Consumptive uses of wildlife habitat are there- more obscure target species extirpated by archaic nancing or justifying fi fore instrumental in either hunters will remain undetected. much of the conservation acreage available in the st century from game reserves in Africa, Aus- In more recent times, exploitation-induced ex- 21 tralia and North America to extractive reserves in tinction events have also been common as Europe- Amazonia, to the reindeer rangelands of Scandi- an settlers wielding superior technology greatly navia and the saiga steppes of Mongolia. expanded their territorial frontiers and introduced Strong cultural or social factors regulating re- market and sport hunting. One example is the source choice often affect which species are taken. decimation of the vast North American buffalo For example, while people prefer to hunt large- (bison; Bison bison ) herds. In the 1850s, tens of bodied mammals in tropical forests, feeding millions of these ungulates roamed the Great “ taboos and restrictions can switch on or off ” Plains in herds exceeding those ever known for depending on levels of game depletion (Ross s ’ any other megaherbivore, but by the century 1978) as predicted by foraging theory. This is close, the bison was all but extinct. Another exam- consistent with the process of de-tabooing species ple is the extirpation of monodominant stands of that were once tabooed, as the case of brocket Pau-Brasil legume trees ( Caesalpinia echinata ,Legu- deer among the Siona-Secoya (Hames and Vick- minosae-Mimosoidae) from eastern Brazil, a ers 1982). However, several studies suggest that source of red dye and hardwood that gave Brazil cultural factors breakdown and play a lesser role its name. These were once extremely abundant © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

125 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 110 when large-bodied game species become scarce, gaps and imparting much collateral damage due thereby forcing discriminate harvesters to be- to logging roads and skid trails (Grogan et al. come less selective (Jerozolimski and Peres 2003). 2008). Mahogany and other high-value tropical timber species worldwide share several traits that predispose them to commercial extirpation: excellent pliable wood of exceptional beauty; 6.2 Overexploitation in tropical forests natural distributions in forests experiencing 6.2.1 Timber extraction rapid conversion rates; low-density populations Tropical deforestation is driven primarily by (often < 1 tree/ha); and life histories generally frontier expansion of subsistence agriculture characterized as non-pioneer late secondary, with fast growth rates, abiotic seed dispersal, and large development programs involving re- and low-density seedlings requiring canopy dis- settlement, agriculture, and infrastructure turbance for optimal seedling regeneration (Chapter 4). However, animal and plant popula- in the understory (Swaine and Whitmore 1988; tion declines are typically pre-empted by hunt- et al. 2008). Sodhi ing and logging activity well before the coup de grâce of deforestation is delivered. It is estimated One of the major obstacles to implementing a that between 5 and 7 million hectares of tropical sustainable forestry sector in tropical countries is forests are logged annually, approximately fi nancial incentives for producers to the lack of limit offtakes to sustainable levels and invest in 68-79% of the area that was completely defor- regeneration. Economic logic often dictates that ested each year between 1990 and 2005 [FAO trees should be felled whenever their rate of vol- (Food and Agriculture Organization of the ume increment drops below the prevailing inter- United Nations) 2007]. Tropical forests account est rate (Pearce 1990). Postponing harvest beyond for ~25% of the global industrial wood produc- tion worth US$400 billion or ~2% of the global this point would incur an opportunity cost be- gross domestic product [WCFSD (World Com- cause pro ts from logging could be invested at a fi mission on Forests and Sustainable Develop- higher rate elsewhere. This partly explains why many slow-growing timber species from tropical ment) 1998]. Much of this logging activity forests and savannahs are harvested unsustain- opens up new frontiers to wildlife and non-tim- Dalbergia mel- ably (e.g. East African Blackwood ( ber resource exploitation, and catalyses the tran- ) in the Miombo woodlands of Tanzania; anoxylon sition into a landscape dominated by slash-and- Ball 2004). This is particularly the case where land burn and large-scale agriculture. Few studies have examined the impacts of se- tenure systems are unstable, and where there are lective logging on commercially valuable timber no disincentives against ‘ operations ’ hit-and-run species and comparisons among studies are lim- that mine the resource capital at one site and move on to undepleted areas elsewhere. This is ited because they often fail to employ comparable clearly shown in a mahogany study in Bolivia methods that are adequately reported. The best where the smallest trees felled are ~40 cm in case studies come from the most valuable timber diameter, well below the legal minimum size species that have already declined in much of (Gullison 1998). At this size, trees are increasing their natural ranges. For instance, the highly se- lective, but low intensity logging of broadleaf in volume at about 4% per year, whereas real mahogany ( Swietenia macrophylla ), the most valu- mahogany price increases have averaged at only able widely traded Neotropical timber tree, is 1%, so that a 40-cm mahogany tree increases in value at about 5% annually, slowing down as the driven by the extraordinarily high prices in inter- tree becomes larger. In contrast, real interest rates national markets, which makes it lucrative for in Bolivia and other tropical countries are often loggers to open-up even remote wilderness > 10%, creating a strong economic incentive to areas at high transportation costs. Mechanized liquidate all trees of any value regardless of re- extraction of mahogany and other prime timber species impacts the forest by creating canopy source ownership. Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

126 1 111 OVEREXPLOITATION 2 2 in in unhunted sites to only 89.2 kg/km kg/km 6.2.2 Tropical forest vertebrates heavily hunted sites (see Figure 6.2). In Kilum Ijim, Humans have been hunting wildlife in tropical Cameroon, most large mammals, including forests for over 100 000 years, but the extent of elephants, buffalo, bushbuck, chimpanzees, leo- consumption has greatly increased over the last pards, and lions, have been lost as a result of hunt- few decades. Tropical forest species are hunted ing (Maisels 2001). In Vietnam, 12 large et al. for local consumption or sales in distant markets vertebrate species have become virtually extinct as food, trophies, medicines and pets. Exploitation over the last fi ve decades primarily due to hunting of wild meat by forest dwellers has increased due (Bennett and Rao 2002). Pangolins and several to changes in hunting technology, scarcity of alter- other forest vertebrate species are facing regional- native protein, larger numbers of consumers, and scale extinction throughout their range across greater access infrastructure. Recent estimates of southern Asia [Corlett 2007, TRAFFIC (The Wild- the annual wild meat harvest are 23 500 tons in life Trade Monitoring Network) 2008], largely as Sarawak (Bennett 2002), up to 164 692 tons in the a result of trade, and over half of all Asian freshwa- Brazilian Amazon (Peres 2000), and up to 3.4 mil- ter turtle species are considered Endangered due lion tons in Central Africa (Fa and Peres 2001). to over-harvesting (IUCN 2007). Hunting rates are already unsustainably high In sum, game harvest studies throughout the across vast tracts of tropical forests, averaging six- tropics have shown that most unregulated, com- fold the maximum sustainable harvest in Central mercial hunting for wild meat is unsustainable Africa (Fa et al. 2001). Consumption is both by rural (Robinson and Bennett 2000; Nasi et al. 2008), and urban communities, who are often at the end and that even subsistence hunting driven by of long supply chains that extend into many re- local demand can severely threaten many medi- mote areas (Milner-Gulland et al. 2003). The rapid um to large-bodied vertebrate populations, with acceleration in tropical forest defaunation due to potentially far-reaching consequences to other unsustainable hunting initially occurred in Asia species. However, persistent harvesting of (Corlett 2007), is now sweeping through Africa, multi-species prey assemblages can often lead to and is likely to move into the remotest parts of post-depletion equilibrium conditions in which the neotropics (Peres and Lake 2003), re fl ecting slow-breeding, vulnerable taxa are eliminated human demographics in different continents. and gradually replaced by fast-breeding robust Hunting for either subsistence or commerce can taxa that are resilient to typical offtakes. For ex- profoundly affect the structure of tropical forest ample, hunting in West African forests could now vertebrate assemblages, as revealed by both vil- ned as sustainable from the viewpoint of be de fi fi les (Jerozolimski and Peres lage-based kill-pro urban bushmeat markets in which primarily ro- 2005) and wildlife surveys in hunted 2003; Fa et al. dents and small antelopes are currently traded, and unhunted forests. This can be seen in the resid- following a series of historical extinctions of vul- ual game abundance at forest sites subjected to nerable prey such as primates and large ungu- varying degrees of hunting pressure, where over- 2005). et al. lates (Cowlishaw hunting often results in faunal biomass collapses, mainly through declines and local extinctions of large-bodied species (Bodmer 1995; Peres 2000). 6.2.3 Non-timber forest products rst system- fi Peres and Palacios (2007) provide the Non-timber forest products (NTFPs) are atic estimates of the impact of hunting on the abun- biological resources other than timber which are dances of a comprehensive set of 30 reptile, bird, extracted from either natural or managed forests and mammal species across 101 forest sites scat- (Peters 1994). Examples of exploited plant pro- tered widely throughout the Amazon Basin and ducts include fruits, nuts, oil seeds, latex, resins, Guianan Shield. Considering the 12 most harvest- gums, medicinal plants, spices, dyes, ornamental sensitive species, mean aggregate population bio- fi rewood, plants, and raw materials such as mass was reduced almost eleven-fold from 979.8 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

127 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 112 Saguinus mystax Saguinus fuscicollis Cacajao spp. Callicebus moloch Cebuella pygmaea Pithecia spp. Saimiri spp. Penelope spp. Odontophorus spp. Cebus albifrons Tinamus spp. Mazama americana Crypturellus spp. Callicebus torquatus Psophia spp. Pecari tajacu Myoprocta spp. Geochelone spp. Mazama gouazoupira Callithrix spp. Cebus apella Dasyprocta spp. Alouatta seniculus Chiropotes spp. Aburria pipile Mitu/Crax spp. Lagothrix spp. Tapirus terrestris Ateles spp. Tayassu pecari 150 100 50 –100 –50 0 Chan o p e in mean ulation densit from non-hunted to hunted areas (%) y p g 2 Changes in mean vertebrate population density (individuals/km Figure 6.2 ) between non ‐ hunted and hunted neotropical forest sites (n = 101), including 30 mammal, bird, and reptile species. Forest sites retained in the analysis had been exposed to different levels of hunting pressure but otherwise were of comparable productivity and habitat structure. Species exhibiting higher density in hunted sites (open bars) are either small ‐ bodied or ignored by hunters; species exhibiting the most severe population declines (shaded bars) were at least halved in abundance or driven to local extinction in hunted sites (data from Peres and Palacios 2007). Desmoncus climbing palms, bamboo and rattan. mortality level in the exploited population. Tra- The socio-economic importance of NTFP harvest ditional NTFP extractive practices are often to indigenous peoples cannot be underestimated. hailed as desirable, low-impact economic activ- Many ethnobotanical studies have catalogued the ities in tropical forests compared to alternative wide variety of useful plants (or plant parts) har- forms of land use involving structural distur- vested by different aboriginal groups throughout bance such as selective logging and shifting agri- the tropics. For example, the Waimiri-Atroari In- 1989). As such, NTFP et al. culture (Peters dians of central Amazonia make use of 79% of the exploitation is usually assumed to be sustainable tree species occurring in a single 1 ha terra rme fi and a promising compromise between biodiversi- forest plot (Milliken 1992), and 1748 of the et al. ty conservation and economic development under ~8000 angiosperm species in the Himalayan re- varying degrees of market integration. The implic- gion spanning eight Asian countries are used it assumption is that traditional methods of NTFP medicinally and many more for other purposes exploitation have little or no impact on forest eco- (Samant 1998). et al. systems and tend to be sustainable because they Exploitation of NTFPs often involves partial or have been practiced over many generations. How- entire removal of individuals from the popula- ever, virtually any form of NTFP exploitation in tion, but the extraction method and whether tropical forests has an ecological impact. The spa- vital parts are removed usually determine the tial extent and magnitude of this impact depends Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

128 1 113 OVEREXPLOITATION on the accessibility of the resource stock, the oris- fl for which the harvest by destructive practices tic composition of the forest, the nature and inten- involves a lethal injury to whole reproductive sity of harvesting, and the particular species or individuals. What then is the impact of NTFP plant part under exploitation. extraction on the dynamics of natural popula- Yet few studies have quantitatively assessed tions? How does the impact vary with the life the demographic viability of plant populations history of plants and animals harvested? Are cur- sourcing NTFPs. One exception are Brazil nuts rent extraction rates truly sustainable? These are , Lecythidaceae) which com- Bertholletia excelsa ( key questions in terms of the demographic sus- prise the most important wild seed extractive tainability of different NTFP offtakes, which will industry supporting millions of Amazonian for- ultimately depend on the ability of the resource est dwellers for either subsistence or income. This population to recruit new seedlings either contin- rmly established in export fi wild seed crop is uously or in sporadic pulses while being sub- markets, has a history of ~200 years of commer- jected to a repeated history of exploitation. cial exploitation, and comprises one of the most Unguarded enthusiasm for the role of NTFP valuable non-timber extractive industries in trop- exploitation in rural development partly stems ical forests anywhere. Yet the persistent collection from unrealistic economic studies reporting high of B. excelsa seeds has severely undermined the market values. For example, Peters et al. (1989) patterns of seedling recruitment of Brazil nut reported that the net-value of fruit and latex ex- trees. This has drastically affected the age struc- traction in the Peruvian Amazon was US$6330/ ture of many natural populations to the point ha. This is in sharp contrast with a Mesoamerican where persistently overexploited stands have study that quanti fi ed the local value of foods, succumbed to a process of senescence and demo- construction materials, and medicines extracted graphic collapse, threatening this cornerstone from the forest by 32 indigenous Indian house- of the Amazonian extractive economy (Peres holds (Godoy et al. 2000). The combined value of 2003). et al. consumption and sale of forest goods ranged 1  1  yr , at the lower A boom in the use of homeopathic remedies from US$18 to US$24 ha end of previous estimates (US$49 - US$1 089 sustained by over-collecting therapeutic and aro- 1  1  yr ). NTFP extraction thus cannot be seen ha matic plants is threatening at least 150 species of as a panacea for rural development and in many fl European wild owers and plants and driving studies the potential value of NTFPs is exagger- fi c 1998). many populations to extinction (Traf ated by unrealistic assumptions of high discount Commercial exploitation of the Pau-Rosa or rose- rates, unlimited market demands, availability of wood tree ( Aniba rosaeodora , Lauraceae), which transportation facilities and absence of product contains linalol, a key ingredient in luxury per- substitution. fumes, involves a one-off destructive harvesting technique that almost invariably kills the tree. This species has consequently been extirpated from virtually its entire range in Brazilian Ama- 6.3 Overexploitation in aquatic ® and zonia (Mitja and Lescure 2000). Channel 5 ecosystems other perfumes made with Pau-Rosa fragrance Marine biodiversity loss, largely through over- gained wide market demand decades ago, but fi shing, is increasingly impairing the capacity of the number of processing plants in Brazil fell the world ’ s oceans to provide food, maintain from 103 in 1966 to fewer than 20 in 1986, due water quality, and recover from perturbations to the dwindling resource base. Yet French per- sheries provide fi (Worm et al. 2006). Yet marine fume connoisseurs have been reluctant to accept employment and income for 0.2 billion people replacing the natural Pau-Rosa fragrance with around the world, and fi shing is the mainstay of synthetic substitutes, and the last remaining po- the economy of many coastal regions; 41 million pulations of Pau-Rosa remain threatened. The shers or fi sh farmers in 2004, people worked as fi same could be argued for a number of NTFPs © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

129 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 114 operating 1.3 million decked vessels and 2.7 mil- 60 lion open boats (FAO 2007). An estimated 14 50 million metric tons of fuel was consumed by the sh-catching sector at a cost equivalent to US$22 fi 40 billion, or ~25% of the total revenue of the sector. In 2004, reported catches from marine and inland 30 fi capture sheries were 85.8 million and 9.2 million tons, respectively, which was worth US$84.9 bil- 20 rst sale. Freshwater catches taken every lion at fi Fully exploited 10 year for food have declined recently but on aver- Underexploited to moderately exploited Percentage of stocks assessed Overexploited, depleted or recovering age 500 000 tons are taken from the Mekong river 0 in South-East Asia; 210 000 tons are taken from 1975 2005 1980 2000 1995 1985 1990 fi sh the Zaire river in Africa; and 210 000 tons of Year are taken from the Amazon river in South Ameri- Figure 6.3 sh stocks fi Global trends in the status of world marine ca. Seafood consumption is still high and rising in monitored by FAO from 1974 to 2006 (data from FAO 2007). the First World and has doubled in China within the last decade. Fish contributes to, or exceeds quarter of the stocks were either underexploited 50% of the total animal protein consumption in or moderately exploited and could perhaps pro- many countries and regions, such as Bangladesh, duce more (Figure 6.3). Cambodia, Congo, Indonesia, Japan or the Brazi- )isa Sardinella brasiliensis The Brazilian sardine ( lian Amazon. Overall, sh provides more than fi shery. fi classic case of an overexploited marine 2.8 billion people with ~20% or more of their In the 1970s hey-day of this industry, 200 000 average per capita intake of animal protein. The tons were captured in southeast Brazil alone oscillation of good and bad years in marine fi sh- every year, but landings suddenly plummeted to eries can also modulate the protein demand from 20 000 tons by 2001. Despite new < shing regula- fi et al. terrestrial wildlife populations (Brashares tions introduced following its collapse, it is un- 2004). The share of fi sh in total world animal clear whether southern Atlantic sardine stocks protein supply amounted to 16% in 2001 (FAO have shown any sign of recovery. With the possi- landing statistics tend to 2004). These ‘ of ’ fi cial ble exception of herring and related species that severely underestimate catches and total values shed with highly fi mature early in life and are due to the enormous unrecorded contribution of selective equipment, many gadids (e.g. cod, had- sheries consumed locally. fi subsistence fi shes) have dock) and other non-clupeids (e.g. fl at s oceans are vast (see Box ’ Although the world experienced little, if any, recovery in as much as 15 4.3), most seascapes are relatively low-productiv- 99% reductions in reproductive – years after 45 ity, and 80% of the global catch comes from only biomass (Hutchings 2000). Worse still, an analysis ~20% of the area. Approximately 68% of the sh species con- of 147 populations of 39 wild fi c and north- ’ s catch comes from the Paci fi world cluded that historically overexploited species, east Atlantic. At current harvest rates, most of the such as North Sea herring, became more prone sheries world- fi economically important marine to extreme year-on-year variation in numbers, wide have either collapsed or are expected to rendering them vulnerable to economic or demo- collapse. Current impacts of overexploitation 2008). graphic extinction (Minto et al. and its consequences are no longer locally nested, Marine sheries are an underperforming glob- fi since 52% of marine stocks monitored by the FAO yields could be much greater if they — al asset in 2005 were fully exploited at their maximum were properly managed. The difference between sustainable level and 24% were overexploited or the potential and actual net economic bene ts fi depleted, such that their current biomass is much fi sheries is in the order of US$50 from marine lower than the level that would maximize their — billion per year equivalent to over half the sustained yield (FAO 2007). The remaining one- © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

130 1 115 OVEREXPLOITATION value of the global seafood trade (World Bank populations), but these were only reported after 2008). The cumulative economic loss to the global a median 53-year lag following their real-time economy over the last three decades is estimated disappearance. Some 80% of all extinctions were to be approximately US$2 trillion, and in many only discovered through historical comparisons; fi shing operations are buoyed up by countries e.g. the near-extinction of large skates on both fi subsidies, so that the global shery economy to sides of the Atlantic was only brought to the fi cit. the point of landing is already in de s attention several decades after the de- ’ world Commercial fi shing activities disproportion- clines have occurred. ately threaten large-bodied marine and fresh- et al. water species (Olden 2007). This results in fi shermen shing down the food chain, targeting fi 6.4 Cascading effects of overexploitation fi ever-smaller pelagic sh as they can no longer on ecosystems capture top predatory sh. This is symptomatic fi All extractive systems in which the overharvested of the now widely known process of ‘ fi shing resource is one or more biological populations, (see Box 6.1). Such se- ’ down marine food webs can lead to pervasive trophic cascades and other quential size-graded exploitation systems also unintended ecosystem-level consequences to take place in multi-species assemblages hunted non-target species. Most hunting, fi shing, and in tropical forests (Jerozolimski and Peres et al collecting activities affect not only the primary 2003). In the seas, overexploitation threatens the target species, but also species that are taken ac- cant populations persistence of ecologically signi fi cidentally or opportunistically. Furthermore, ex- of many large marine vertebrates, including ploitation often causes physical damage to the sharks, tunas and sea turtles. Regional scale po- fi environment, and has rami cations for other spe- pulations of large sharks worldwide have de- cies through cascading interactions and changes clined by 90% or more, and rapid declines in food webs. of > 75% of the coastal and oceanic Northwest In addition, overexploitation may severely Atlantic populations of scalloped hammerhead, erode the ecological role of resource populations white, and thresher sharks have occurred in the in natural communities. In other words, over- et al. past 15 years (Baum 2003; Myers and Worm exploited populations need not be entirely extir- 2003; Myers et al. 2007). Much of this activity is pated before they become ecologically extinct. In fl igate and often driven by the surging global pro ” half-empty “ communities that are (Redford and demand for shark fi ns. For example, in 1997 line- Feinsinger 2001), populations may be reduced to shermen captured 186 000 sharks in southern fi ciently low numbers so that, although still fi suf Brazil alone, of which 83% were killed and dis- present in the community, they no longer interact carded in open waters following the removal of fi cantly with other species (Estes 1989). et al. signi the most lucrative body parts (C.M. Vooren, pers. Communities with reduced levels of species in- comm.). Of the large-bodied coastal species af- teractions may become pale shadows of their for- fected by this trade, several have virtually disap- fi mer selves. Although dif cult to measure, severe peared from shallow waters (e.g. greynurse declines in large vertebrate populations may re- fi sharks, Carcharias taurus ). Of cial fi gures show sult in multi-trophic cascades that may profound- that 131 tons of shark ns, corresponding to US fi ly alter the structure of marine ecosystems such $2.4 million, were exported from Brazil to Asia in as kelp forests, coral reefs and estuaries (Jackson 2007. 2001), and analogous processes may occur in et al. Finally, we know rather little about ongoing many terrestrial ecosystems. Plant reproduction extinction processes caused by harvesting. For oras can be severely affected in endemic island fl example, from a compilation of 133 local, regional ying foxes (pteropo- by population declines in fl fi sh populations, and global extinctions of marine did fruit bats) that serve as strong mutualists as (2003) uncovered that exploitation Dulvy et al. 1991). pollinators and seed dispersers (Cox et al. was the main cause of extinctions (55% of all © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

131 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 116 In some Paci c archipelagos, several species may fi represent one of the most powerful mechanisms become functionally extinct, ceasing to effectively of functional and compositional impoverishment disperse large seeds long before becoming rare of remaining areas of tropical forests (Cochrane (McConkey and Drake 2006). A key agenda for 2003), and arguably the most important climate- future research will involve understanding the mediated phase shift in the structure of tropical non-linearities between functional responses to ecosystems (see also Chapters 8 and 9). the numeric abundance of strong interactors re- duced by exploitation pressure and the quality of 6.4.2 Hunting and plant community dynamics ecological services that depleted populations can Although the direct impacts of defaunation perform. For example, what is the critical density of any given exploited population below which it driven by overhunting can be predicted to some can no longer ful ll its community-wide ecologi- fi degree, higher-order indirect effects on commu- cal role? nity structure remain poorly understood since In this section I concentrate on poorly known Redford ’ s (1992) seminal paper and may have interaction cascades in tropical forest and marine profound, long-term consequences for the persis- tence of other taxa, and the structure, productivi- environments, and discuss a few examples of ty and resilience of terrestrial ecosystems how apparently innocuous extractive activities et al. (Cunningham 2009). Severe population de- targeted to one or a few species can drastically affect the structure and functioning of these ter- ’ clines or extirpation of the world s megafauna restrial and aquatic ecosystems. may result in dramatic changes to ecosystems, some of which have already been empirically demonstrated, while others have yet to be docu- 6.4.1 Tropical forest disturbance mented or remain inexact. Timber extraction in tropical forests is widely Large vertebrates often have a profound im- variable in terms of species selectivity, but even pact on food webs and community dynamics highly selective logging can trigger major ecolog- through mobile-linkage mutualisms, seed preda- ical changes in the understory light environment, tion, and seedling and sapling herbivory. Plant forest microclimate, and dynamics of plant regen- communities in tropical forests depleted of their eration. Even reduced-impact logging (RIL) op- megafauna may experience pollination bottle- erations can generate enough forest disturbance, necks, reduced seed dispersal, monodominance through elevated canopy gap fracture, to greatly of seedling cohorts, altered patterns of seedling augment forest understory desiccation, dry fuel recruitment, other shifts in the relative abundance loads, and fuel continuity, thereby breaching the of species, and various forms of functional com- forest fl ammability threshold in seasonally-dry pensation (Cordeiro and Howe 2003; Peres and forests (Holdsworth and Uhl 1997; Nepstad et al. Roosmalen 2003; Wang et al. 2007; Terborgh et al. 1999; Chapter 9). During severe dry seasons, 2008; Chapter 3). On the other hand, the net ef- often aggravated by increasingly frequent conti- fects of large mammal defaunation depends on nental-scale climatic events, extensive ground how the balance of interactions are affected by res initiated by either natural or anthropogenic fi population declines in both mutualists (e.g. high- sources of ignition can result in a dramatically quality seed dispersers) and herbivores (e.g. seed reduced biomass and biodiversity value of previ- fi predators) (Wright 2003). For example, signi - ously unburnt tropical forests (Barlow and Peres cant changes in population densities in wild 2004, 2008). Despite these undesirable effects, Suidae pigs ( ) and several other ungulates and large-scale commercial logging that is unsustain- rodents, which are active seed predators, may able at either the population or ecosystem level have a major effect on seed and seedling survival continues unchecked in many tropical forest fron- and forest regeneration (Curran and Webb 2000). et al. 2004; Asner tiers (Curran et al. 2005). Yet oras are most dependent on fl Tropical forest surface res aggravated by logging disturbance fi large-vertebrate dispersers, with as many as © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

132 1 117 OVEREXPLOITATION 97% of all tree, woody liana and epiphyte species diet, and seed handling outcomes (Peres and Dol- bearing fruits and seeds that are morphologically man 2000). adapted to endozoochorous (passing through the Large vertebrates targeted by hunters often gut of an animal) dispersal (Peres and Roosmalen have a disproportionate impact on community 2003). Successful seedling recruitment in many ecosystem engineers ” “ structure and operate as owering plants depends on seed dispersal ser- fl et al. 1994; Wright and Jones 2006), either (Jones vices provided by large-bodied frugivores (Howe performing a key landscaping role in terms of and Smallwood 1982), while virtually all seeds structural habitat disturbance, or as mega-herbi- s canopy succumb falling underneath the parent ’ vores that maintain the structure and relative — to density-dependent mortality caused by fun- abundance of plant communities. For example, gal attack, other pathogens, and vertebrate and elephants exert a major role in modifying vegeta- invertebrate seed predators (see review in Carson tion structure and composition as herbivores, et al. 2008). seed dispersers, and agents of mortality for A growing number of phytodemographic stud- many small trees (Cristoffer and Peres 2003). ies have examined the effects of large-vertebrate Two similar forests with or without elephants removal. Studies examining seedling recruitment show different succession and regeneration path- under different levels of hunting pressure (or dis- ways, as shown by long-term studies in Uganda perser abundance) reveal very different out- (Sheil and Salim 2004). Overharvesting of several comes. At the community level, seedling density other species holding a keystone landscaping role in overhunted forests can be indistinguishable, can lead to pervasive changes in the structure and greater, or less than that in the undisturbed function of ecosystems. For example, the decima- forests (Dirzo and Miranda 1991; Chapman and tion of North American beaver populations by Onderdonk 1998; Wright et al. 2000), but the con- pelt hunters following the arrival of Europeans sequences of increased hunting pressure to plant profoundly altered the hydrology, channel geo- regeneration depends on the patterns of deple- morphology, biogeochemical pathways and com- tion across different prey species. In persistently munity productivity of riparian habitats (Naiman hunted Amazonian forests, where large-bodied et al. 1986). primates are driven to local extinction or severely Mammal overhunting triggers at least two ad- reduced in numbers (Peres and Palacios 2007), ditional potential cascades: the secondary extir- the probability of effective dispersal of large- pation of dependent taxa and the subsequent seeded endozoochorous plants can decline by decline of ecological processes mediated by asso- over 60% compared to non-hunted forests ciated species. For instance, overhunting can se- (Peres and Roosmalen 2003). Consequently, verely disrupt key ecosystem processes including plant species with seeds dispersed by vulnerable nutrient recycling and secondary seed dispersal game species are less abundant where hunters exerted by relatively intact assemblages of dung are active, whereas species with seeds dis- beetles (Coleoptera: Scarabaeinae) and other co- persed by abiotic means or by small frugivores prophagous invertebrates that depend on large ignored by hunters are more abundant in the mammals for adult and larval food resources seedling and sapling layers (Nuñez-Iturri (Nichols et al. 2009). et al. 2007; Terborgh and Howe 2007; Wright 2008). However, the importance of dispers- et al. 6.4.3 Marine cascades al-limitation in the absence of large frugivores depends on the degree to which their seed dis- Apart from short-term demographic effects such as the direct depletion of target species, there is persal services are redundant to any given growing evidence that fi shing also contributes to plant species (Peres and Roosmalen 2003). Fur- important genetic changes in exploited popula- thermore, local extinction events in large-bodied species are rarely compensated by smaller species tions. If part of the phenotypic variation of target in terms of their population density, biomass, species is due to genetic differences among © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

133 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 118 individuals then selective shing will cause ge- fi sulting in signi fi cant bycatch mortality of many netic changes in life-history traits such as ages fi sh, reptile, bird and mammal popu- vulnerable and sizes at maturity (Law 2000). The genetic lations, thereby comprising a key management effects of fi shing are increasingly seen as a long- 2000). For issue for most fl fi eets (Hall et al. shing term management issue, but this is not yet man- example, over 200 000 loggerhead ( Caretta caretta ) aged proactively as short-term regulations tend Dermochelys coria- and 50 000 leatherback turtles ( to merely focus on controlling mortality. Howev- ) were taken as pelagic longline bycatch in cea er, the damage caused by over fi shing extends 2000, likely contributing to the 80 – 95% declines well beyond the main target species with pro- fi for Paci c loggerhead and leatherback popula- found effects on: (i) low-productivity species in 2004). tions over two decades (Lewison et al. mixed fi sheries; (ii) non-target species; (iii) food fi While shing pressure on target species relates webs; and (iv) the structure of oceanic habitats. shing pressure on bycatch fi to target abundance, species is likely insensitive to bycatch abundance Low-productivity species in mixed sheries fi (Crowder and Murawski 1998), and may there- Many multi-species sheries are relatively unse- fi “ extinctions. Bycatches ” fore result in piggyback lective and take a wide range of species that vary have been the focus of considerable societal con- in their capacity to withstand elevated mortality. cern, often expressed in relation to the welfare of fi This is particularly true in mixed trawl sheries individual animals and the status of their popula- where sustainable mortality rates for a produc- tions. Public concerns over unacceptable levels of tive primary target species are often unsustain- mortality of large marine vertebrates (e.g. sea able for species that are less productive, such as turtles, seabirds, marine mammals, sharks) have skates and rays, thereby leading to widespread therefore led to regional bans on a number depletion and, in some cases, regional extinction shing methods and gears, including long fi of processes. Conservation measures to protect un- drift-nets. fi sheries are always productive species in mixed Food webs shers targeting more produc- fi controversial since fi Over shing can create trophic cascades in marine ce yield in fi tive species will rarely wish to sacri communities that can cause signi fi cant declines in order to spare less productive species. species richness, and wholesale changes in coast- cant reductions Bycatches fi al food webs resulting from signi shing fi in consumer populations due to over Most seafood is captured by indiscriminate meth- 2001). Predators have a fundamen- et al. (Jackson ods (e.g. gillnetting, trawl netting) that haul in tal top-down role in the structure and function of large numbers of incidental captures (termed by- biological communities, and many large marine catches) of undesirable species, which numerical- > predators have declined by 90% of their base- ly may correspond to 25 – 65% of the total catch. 1998; Myers et al. line population levels (Pauly These non-target pelagic species can become en- and Worm 2003; see Box 6.1). Fishing affects fi tangled or hooked by the same shing gear, re- fi sheries Box 6.1 The state of Daniel Pauly (Pauly 2002). IUU catches include, for et al. Industrial, or large-scale and artisanal, or small- example, the fi sh discarded by shrimp trawlers fi sheries, generate, at the onset of scale marine st (usually 90% of their actual catch), the catch of the 21 century, combined annual catches of eets operating under ags high sea industrial fl fl – 140 million tons, with an ex-vessel value of 120 of convenience, and the individually small catch about US$100 billion. This is much higher than by millions of artisanal fi shers (including fi 90 million – cially reported landings (80 of women and children) in developing countries, tons), which do not account for illegal, which turns out to be very high in the unreported and undocumented (IUU) catches continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

134 1 119 OVEREXPLOITATION Box 6.1 (Continued) aggregate, but still goes unreported by receive annually as government subsidies, national governments and international eets a fl oat that have fl which now act to keep agencies. no fi sh to exploit (Sumaila et al. 2008). In This global catch, which, depending on the addition to representing a giant waste of source, is either stagnating or slowly declining, is economic resources, these overcapitalized the culmination of the three-pronged expansion eets have a huge, but long shing ‐ neglected fi fl sheries which occurred following the Second fi of targeted ‐ impact on their target species, on non World War: (i) an offshore/depth expansion, ‐ species caught as by catch, and on the marine resulting from the depletion of shallow-water, ecosystems in which all species are embedded. inshore stocks (Morato 2006); (ii) a et al. Also, these fl eets emit large amounts of carbon geographic expansion, as the fl eets of dioxide; for example trawlers nowadays often industrialized countries around the North burn several tons of diesel fuel for every ton of Atlantic and in East Asia, faced with depleted fi sh landed (and of which 80% is water), and stocks in their home waters, shifted their fi ciency declines over time because of their ef operations toward lower latitudes, and thence sh stocks (Tyedmers et al. 2005). declining fi to the southern hemisphere (Pauly et al. 2002); Besides threatening the food security of and (iii) a taxonomic expansion, i.e. capturing numerous developing countries, for example in and marketing previously spurned species of West Africa, these trends endanger marine sh and invertebrates to replace the fi smaller biodiversity, and especially the continued diminishing supply of traditionally targeted, existence of the large, long ‐ lived species that larger sh species (Pauly et al. fi 1998; see have sustained fi sheries for centuries (Worm Box 6.1 Figure). et al. 2006). In the course of these expansions, fi shing Thegoodnewsisthatweknowinprinciplehow effort grew enormously, especially that of toavoidtheovercapitalizationof fi sheriesandthe fl industrial eets, which are, overall, 3 – 4 times collapse of their underlying stocks. This would larger than required. This is, among other involve, besides an abolition of capacity ‐ – 34 billion they things, a result of the US$30 free fuel, loan enhancing subsidies (e.g. tax ‐ guarantees for boat purchases (Sumaila et al. 2008), the creation of networks of large marine protected areas, and the reduction of fi shing effort in the remaining exploited areas, mainly throughthecreationofdedicatedaccessprivilege (e.g. for adjacent small scale fi sher communities), . ” sh such as to reduce the fi “ race for Also, the measures that will have to be taken to mitigate climate change offer the prospect of a reduction of global fl eet capacity (via a reduction of their greenhouse gas emissions). This may lead to more attention being paid to sheries, so far neglected, but fi scale small ‐ whose adjacency to the resources they exploit, and use of fuel ‐ ef fi cient, mostly passive gear, offers a real prospect for sustainability. Schematic representation of the process, now Box 6.1 Figure widely known as shing down marine food webs ‘ sheries fi , by which ’ fi rst target the large fi sh, then, as these disappear, move on to fi REFERENCES smaller species of fi sh and invertebrates, lower in the food web. In the process, the functioning of marine ecosystems is profoundly Morato, T., Watson, R., Pitcher, T. J., and Pauly, D. (2006). disrupted, a process aggravated by the destruction of the bottom Fish and Fisheries , ,24 – 34. 7 Fishing down the deep. fauna by trawling and dredging. continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

135 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 120 (Continued) Box 6.1 ICES Journal of pacity, and resource sustainability. Pauly, D., Christensen, V., Dalsgaard, J., Froese, R., and , 832 Marine Science , 65 – 840. Torres, F. C. Jr. (1998). Fishing down marine food webs. Tyedmers, P., Watson, R., and Pauly, D. (2005). Fueling Science , 860 279 , 863. – fi shing fl eets. AMBIO: a Journal of the Human global Pauly, D., Christensen, V., Guénette, S., et al. (2002). – 638. Environment 34 , 635 , , , Nature sheries. 418 Towards sustainability in world fi (2006). et al. Worm, B., Barbier, E. B., Beaumont, N., 689 695. – Impacts of biodiversity loss on ocean ecosystem services. Sumaila, U. R., Teh, L., Watson, R., Tyedmers, P., and Science 314 – , 790. , 787 Pauly, D. (2008). Fuel price increase, subsidies, overca- predator-prey interactions in the shed commu- fi 6.5 Managing overexploitation nity and interactions between fi sh and other spe- This chapter has repeatedly illustrated examples cies, including predators of conservation interest of population declines induced by overexploita- such as seabirds and mammals. For example, tion even in the face of the laudable goals of fi sheries can compete for the prey base of seabirds implementing conservation measures in the real- and mammals. Fisheries also produce discards world. This section will conclude with some com- cant energy subsidies es- that can provide signi fi ments about contrasts between theory and prac- pecially for scavenging seabirds, in some cases tice, and brie y explore some of the most severe fl sustaining hyper-abundant populations. Current problems and management solutions that can fi understanding of food web effects of over shing minimize the impact of harvesting on the integri- is often too poor to provide consistent and reli- ty of terrestrial and marine ecosystems. fi able scienti c advice. Unlike many temperate countries where regu- latory protocols preventing overexploitation Habitat structure have been developed through a long and repeat- Over shing is a major source of structural distur- fi ed history of trial and error based on ecological sh- bance in marine ecosystems. The very act of fi fi principles and hard-won eld biology, popula- ing, particularly with mobile bottom gear, tion management prescriptions in the tropics are destroys substrates, degrades habitat complexity, typically non-existent, unenforceable, and lack and ultimately results in the loss of biodiversity the personnel and scienti fi c foundation on (see Box 4.3). These structural effects are com- which they can be built. The concepts of game pounded by indirect effects on habitat that occur wardens, bag limits, no-take areas, hunting or through removal of ecological or ecosystem en- shing licenses, and duck stamps are completely fi gineers (Coleman and Williams 2002). Many fi sh- unfamiliar to the vast majority of tropical subsis- ing gears contact benthic habitats during shing fi tence hunters or fi shers (see Box 6.2). Yet these and habitats such as coral reefs are also affected resource users are typically among the poorest by changes in food webs. The patchiness of im- rungs in society and often rely heavily on wild pacts and the interactions between types of gears animal populations as a critical protein compo- and habitats are critical to understanding the sig- nent of their diet. In contrast, countries with a shing effects on habitats; different fi cance of ni fi strong tradition in fi sh and wildlife management gears have different impacts on the same habitat and carefully regulated harvesting policy in pri- and different habitats respond differently to the vate and public areas, may include sophisticated same gear. For some highly-structured habitats legislation encompassing bag limits on the age such as deep water corals, recovery time is so and sex of different target species, as well as re- slow that only no fi shing would be realistically shing seasons and fi strictions on hunting and sustainable (Roberts et al. 2006). © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

136 1 121 OVEREXPLOITATION Box 6.2 Managing the exploitation of wildlife in tropical forests Douglas W. Yu Offtake restrictions are, however, less useful Hunting threatens the persistence of tropical in settings where governance is poor, such that wildlife, their ecological functions, such as seed ‐ nes are rarely expected and incursions into no fi dispersal, and the political will to maintain take areas go unpunished, or where subsistence use forests in the face of alternative land ‐ hunting is the norm, such as over much of the options. However, game species are important Amazon Basin (Peres 2000). In the latter case, sources of protein and income for millions of markets for wild meat are small or nonexistent, forest dwellers and traders of wildlife (Peres and human populations are widely distributed, 2000; Bulte and van Kooten 2001; Milner ‐ exacerbating the already ‐ dif fi cult problem of Gulland 2003; Bennett et al. et al. 2007; this monitoring hunting effort in tropical forests chapter). (Peres and Terborgh 1995; Peres and Lake 2003; Policy responses to the overexploitation of Ling and Milner ‐ Gulland 2006). Moreover, the wildlife can be placed into two classes: (i) largest classes of Amazonian protected areas side restrictions on offtake, to increase ‐ demand are indigenous and sustainable development side ‐ the cost of hunting, and (ii) the supply 2006; Peres and et al. reserves (Nepstad provisioning of substitutes, to decrease the Nascimento 2006), within which inhabitants bene fi t of hunting (Bulte and Damania 2005; hunt legally. Crookes and Milner ‐ Gulland 2006). Restrictions take areas, such as on offtake vary from no ‐ Such considerations are part of the parks, to various partial limits, such as reducing motivation for introducing demand ‐ side the density of hunters via private property remedies, such as alternative sources of protein. rights, and establishing quotas and bans on The logic is that local substitutes (e.g. fi sh from fi c species, seasons, or hunting gear, like speci aquaculture) should decrease demand for wild shotguns (Bennett et al. 2007). Where there are excess labor devoted ‐ meat and allow the now commercial markets for wildlife, restrictions can to hunting to be reallocated to competing also be applied down the supply chain in the activities, such as agriculture or leisure. form of market fi et al. nes or taxes (Clayton However, the nature of the substitute and 2005). Finally, some et al. 1997; Damania the structure of the market matter greatly. If wildlife products are exported for use as side remedy instead takes the ‐ the demand medicines or decoration and can be subjected form of increasing the opportunity cost of to trade bans under the aegis of the Convention hunting by, for example, raising the on International Trade in Endangered Species pro fi tability of agriculture, it is possible that 2007; Van et al. (CITES) (Stiles 2004; Bulte total hunting effort will ultimately increase, Kooten 2008). since income is fungible and can be spent on Bioeconomic modeling (Ling and Milner ‐ wild meat (Damania et al. 2005). Higher Gulland 2006) of a game market in Ghana consumer demand also raises market prices and nes on has suggested that imposing large fi can trigger shifts to more effective but more the commercial sale of wild meat should expensive hunting techniques, like guns (Bulte be suf fi cient to recover wildlife populations, 2005). More and Horan 2002; Damania et al. even in the absence of forest patrols generally, efforts to provide alternative 2005). Fines reduce expected (Damania et al. fi economic activities are likely to be inef cient ts from sales, so hunters should shift pro fi conservation ‘ and amount to little more than from fi rearms to cheaper but less effective by distraction ’ (Ferraro 2001; Ferraro and snares and consume more wildlife at home. Simpson 2002). The resulting loss of cash income should In many settings, the ultimate consumers are encourage households to reallocate labor not the hunters, and demand ‐ side remedies toward other sources of cash, such as could take the form of educational programs agriculture. aimed at changing consumer preferences or, continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

137 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Box 6.2 (Continued) It should also be possible to employ positive alternatively, of wildlife farms (e.g. crocodilian incentives in the form of payments for ranches) that are meant to compete with and ecological services (Ferraro 2001; Ferraro and depress the price of wild ‐ caught terrestrial Simpson 2002; Ferraro and Kiss 2002). For vertebrates. The latter strategy could, however, example, in principle, the state might pay local lead to perverse outcomes if the relevant communities in return for abundant wildlife as market is dominated by only a few suppliers, measured in regular censuses. In practice, who have the power to maintain high prices by however, the high stochasticity of such a restricting supply to market (Wilkie 2005; et al. monitoring mechanism, and the problem of Bulte and Damania 2005; Damania and Bulte free riders within communities, might make this 2007). Then, the introduction of a farmed mechanism unworkable. Alternatively, in the substitute can, in principle, induce intense case of landscapes that still contain vast areas of cutting competition, which would ‐ price high animal abundance, such as in many parks increase consumer demand and lead to more that host small human populations, a strategy hunting and lower wildlife stocks. Also, farmed that takes advantage of the fact that central ‐ substitutes can undermine efforts to stigmatize place subsistence hunters are distance limited is the consumption of wildlife products, ‐ appropriate (Ling and Milner Gulland 2008; increasing overall demand. Given these caveats, Levi et al. 2009). The geographic distribution of the strategy of providing substitutes for wildlife settlements is then an easily monitored proxy might best be focused on cases where the for the spatial distribution of hunting effort. As substitute is different from and clearly superior a result, economic incentives to promote to the wildlife product, as is the case for Viagra settlement sedentarism, which can range from versus aphrodisiacs derived from animal parts direct payments to the provision of public (von Hippel and von Hippel 2002). services such as schools, would also limit the Ultimately, given the large numbers of rural spread of hunting across a landscape. dwellers, the likely persistence of wildlife markets of all kinds, and the great uncertainties that remain embedded in our understanding of REFERENCES the ecology and economics of wildlife exploitation, any comprehensive strategy to (2007). Bennett, E., Blencowe, E., Brandon, K., et al. prevent hunting from driving wildlife Hunting for consensus: Reconciling bushmeat harvest, populations extinct must include no take areas ‐ conservation, and development policy in west and cen- — (Bennett et al. 2007) the bigger the better. 21 887. tral Africa. Conservation Biology , 884 , – ‐ The success of no take areas will in turn depend Bulte, E. H. and Damania, R. (2005). An economic assess- on designing appropriate enforcement Conservation ment of wildlife farming and conservation. measures for different contexts, from national 19 Biology , 1233. – , 1222 parks to indigenous reserves and working Bulte, E. H. and Horan, R. D. (2002). Does human popula- based management forests to community ‐ tion growth increase wildlife harvesting? An economic (Keane et al. 2008). assessment. , 66 , Journal of Wildlife Management A potential approach is to use the economic – 574 580. theory of contracts and asymmetric Bulte, E. H. and van Kooten, G. C. (2001). State interven- information (Ferraro 2001, 2008; Damania and tion to protect endangered species: why history and bad Hatch 2005) to design a menu of incentives and Conservation Biology luck matter. 1803. – , 1799 15 , punishments that deters hunting in designated Bulte, E. H., Damania, R., and Van Kooten, G. C. (2007). no take areas, given that hunting is a hidden ‐ The effects of one ‐ off ivory sales on elephant mortality. action. In the above bioeconomic model in , 613 71 – 618. Journal of Wildlife Management , Ghana (Damania 2005), hidden hunting et al. Clayton, L., Keeling, M., and Milner ‐ Gulland, E. J. (1997). effort is revealed in part by sales in markets, Bringing home the bacon: a spatial model of wild pig which can be monitored, and the imposition of hunting in Sulawesi, Indonesia. Ecological Application , ne causes changes in the behavior fi a punishing , 642 652. – 7 of households that result ultimately in higher Crookes, D. J. and Milner ‐ Gulland, E. J. (2006). Wildlife and game populations. economic policies affecting the bushmeat trade: a continues Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

138 1 123 OVEREXPLOITATION (Continued) Box 6.2 ‐ Gulland, E. (2008). When does spatial Ling, S. and Milner framework for analysis. South African Journal of Wildlife Journal structure matter in models of wildlife harvesting? Research – 165. , 159 36 , ,63 45 – of Applied Ecology , 71. Damania, R. and Bulte, E. H. (2007). The economics of Gulland, E., Bennett, E. & and the SCB 2002 Annual ‐ Milner wildlife farming and endangered species conservation. Meeting Wild Meat Group (2003). Wild meat: the bigger 472. – , 461 62 , Ecological Economics , 351 picture. 357. Trends in Ecology and Evolution , 18 – Damania, R. and Hatch, J. (2005). Protecting Eden: markets et al. (2006). Nepstad, D., Schwartzman, S., Bamberger, B., 351. , Ecological Economics or government? , 339 – 53 fi Inhibition of Amazon deforestation and re by parks and Gulland, E. J., and Crookes, D.J. Damania, R., Milner ‐ indigenous lands. Conservation Biology , 20 ,65 – 73. (2005). A bioeconomic analysis of bushmeat hunting. Peres, C. A. (2000). Effects of subsistence hunting on Proceedings of Royal Society of London B , 272 , 259 – 266. vertebrate community structure in Amazonian forests. Ferraro, P. J. (2001). Global habitat protection: limitation of Conservation Biology 253. – , 240 , 14 development interventions and a role for conservation Peres, C. A. and Lake, I. R. (2003). Extent of nontimber performance payments. 15 , Conservation Biology , resource extraction in tropical forests: accessibility to 990 1000. – game vertebrates by hunters in the Amazon basin. Ferraro, P. J. (2008). Asymmetric information and contract , 521 17 , 535. Conservation Biology – design for payments for environmental services. Ecolog- Peres, C. A. and Nascimento, H. S. (2006). Impact of game ical Economics 821. – , 810 65 , hunting by the Kayapo of south ‐ eastern Amazonia: im- Ferraro, P. J. and Kiss, A. (2002). Direct payments to con- plications for wildlife conservation in tropical forest in- Science , 298 , 1718 serve biodiversity. 1719. – digenous reserves. Biodiversity and Conservation , Ferraro, P. J. and Simpson, R. D. (2002). The cost ‐ effec- 15 , 2627 – 2653. 78 Land Economics , tiveness of conservation payments. , Peres, C. A. and Terborgh, J. W. (1995). Amazonian nature 339 – 353. reserves: an analysis of the defensibility status of existing ‐ Keane, A., Jones, J. P. G., Edwards Jones, G., and conservation units and design criteria for the future. Gulland, E. (2008). The sleeping policeman: Milner ‐ 9 – ,34 , Conservation Biology 46. understanding issues of enforcement and Stiles, D. (2004). The ivory trade and elephant conserva- , Animal Conservation compliance in conservation. , 309 31 – 321. , Environmental Conservation tion. 11 – ,75 82. von Hippel, F. and von Hippel, W. (2002). Sex drugs and Levi, T., Shepard, G. H., Jr., Ohl Schacherer, J., Peres, C. A., ‐ animal parts: will Viagra save threatened species? term sustain- and Yu, D.W. (2009). Modeling the long ‐ , 277 , 281. Environmental Conservation – 29 ability of indigenous hunting in Manu National Park, Van Kooten, G. C. (2008). Protecting the African elephant: ‐ Peru: Landscape scale management implications for A dynamic bioeconomic model of ivory trade. Biological 46 , 804 – 814. Amazonia. Journal of Applied Ecology , Conservation Ling, S. and Milner Gulland, E. J. (2006). Assessment of the ‐ , 141 , 2012 – 2022. Wilkie, D. S., Starkey, M., Abernethy, K. sustainability of bushmeat hunting based on dynamic (2005). Role et al. 20 , Conservation Biology , bioeconomic models. of prices and wealth in consumer demand for bushmeat 19 – ,1 1294 , Conservation Biology in Gabon, Central Africa. 1299. 7. – capture technology. Despite the economic value hunters sustainably harvest over 700 000 wild of wildlife (Peres 2000; Chardonnet 2002; et al. ) every Odocoileus virginianus white-tailed deer ( Table 6.1), terrestrial and aquatic wildlife in year, whereas Costa Rica can hardly sustain an ’ ‘ invisible many tropical countries comprise an annual harvest of a few thousand without push- commodity and local offtakes often proceed un- ing the same cervid species, albeit in a different restrained until the sudden perception that the food environment, to local extinction (D. Janzen, ected fl resource stock is fully depleted. This is re pers. comm.). in the contrast between carefully regulated and An additional widespread challenge in manag- unregulated systems where large numbers of ing any diffuse set of resources is presented when hunters may operate. For example, Minnesota resources (or the landscape or seascape which © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

139 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 124 Total estimated value of the legal wildlife trade worldwide in Table 6.1 they occupy) have no clear ownership. This is 2005 (data from Roe 2008). ‘ tragedy of the com- widely referred to as the mons ’ (Hardin 1968) in which open-access exploi- Estimated value tation systems lead to much greater rates of (US$ millon) Commodity exploitation than are safe for the long-term sur- Live animals vival of the population. This is dreadful for both Primates 94 the resource and the consumers, because each Cage birds 47 user is capturing fewer units of the resource 6 Birds of prey Reptiles (incl. snakes and turtles) 38 than they could if they had fewer competitors. Ornamental fi 319 sh Governments often respond by providing per- Animal products for clothing verse subsidies that deceptively reduce costs, or ornaments hence catalyzing a negative spiral leading to fur- 5000 Mammal furs and fur products ther overexploitation (Repetto and Gillis 1988). 338 Reptile skins The capital invested in many extractive industries Ornamental corals and shells 112 80 Natural pearls sheries and logging opera- fi such as commercial Animal products for food tions cannot be easily reinvested, so that exploi- sh) fi (excl. ters have few options but to continue harvesting Game meat 773 the depleted resource base. Understandably, this Frog legs 50 leads to resistance against restrictions on exploi- 75 Edible snails tation rates, thereby further exacerbating the pro- Plant products blems of declining populations. In fact, Medicinal plants 1300 Ornamental plants 13 000 exploitation can have a one-way ratchet effect, Fisheries food products (excl. 81 500 with governments propping up overexploitation aquaculture) when populations are low, and supporting in- 190 000 Timber vestment in the activity when yields are high. Total $292.73 bill Laws against the international wildlife and timber trade have often failed to prevent supplies sourced from natural populations from reaching For example, giant blue fi n tuna ( Thunnus thyn- their destination, accounting for an estimated US nus ), which are captured illegally by commercial $292.73 billion global market, most of it ac- and recreational shers assisted by high-tech fi counted for by native timber and wild sheries fi gear, may be the most valuable animal on the (see Table 6.1). Global movement of animals for planet, with a single 444-pound blue fi n tuna the pet trade alone has been estimated at ~350 sold wholesale in Japan a few years ago for US million live animals, worth ~US$20 billion per $173 600! In fact, a ban on harvesting of some fi c 2008). At least 4561 extant year (Roe 2008; Traf highly valuable species has merely spawned bird species are used by humans, mainly as pets ve fi a thriving illegal trade. After trade in all > 3337 species traded in- and for food, including species of rhino was banned, the black rhino be- ternationally (Butchart 2008). Some 15 to 20 mil- came extinct in at least 18 African countries lion wild-caught ornamental fi sh are exported [CITES (Convention on International Trade in alive every year through Manaus alone, a large Endangered Species) 2008]. The long-term suc- city in the central Amazon (Andrews 1990). cess of often controversial bans on wildlife trade Regulating illegal overharvesting of exorbitant- depends on three factors. First, prohibition on such as elephant — priced resource populations trade must be accompanied by a reduction in ivory, rhino horn, tiger bone or mahogany demand for the banned products. Trade in cat — presents an additional, and often insur- trees and seal skins was crushed largely because ethi- mountable, challenge because the rewards ac- cal consumer campaigns destroyed demand at crued to violators often easily outweigh the the same time as trade bans cut the legal supply. enforceable penalties or the risks of being caught. Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

140 1 125 OVEREXPLOITATION Second, bans may curb legal trade, which often (MPAs) that can be permanently or temporarily provides an economic incentive to maintain wild- closed-off to maximize game and sh yields. Pro- fi life or their habitat. Some would therefore argue tection afforded by these spatial restrictions allows they undermine conservation efforts and may populations to increase through longer lifespans even create incentives to eliminate them. The and higher reproductive success. Recovery of ani- American bison was doomed partly because its mal biomass inside no-take areas increases harvest rangelands became more valuable for rearing cat- levels in surrounding landscapes (or seascapes), tle (Anderson and Hill 2004). Third, international and as stocks build up, juveniles and adults can trade agreements must be supported by govern- eventually spill over into adjacent areas (e.g. Ro- ments and citizens in habitat-countries, rather berts 2001). However, the theoretical and et al. than only conscious consumers in wealthy na- empirical underpinnings of marine reserves have tions. But even well-meaning management pre- advanced well beyond their terrestrial counter- scriptions involving wildlife trade can be parts. Several typical life history traits of marine completely misguided bringing once highly species such as planktonic larval dispersal are abundant target species to the brink of extinction. lacking in terrestrial game species, which differ 1 mil- The 97% decline of saiga antelopes (from > widely in the degree to which surplus animals < lion to 30 000) in the steppes of Russia and can colonize adjacent unharvested areas. Howev- Kazakhstan over a 10-year period has been partly er, many wild meat hunters may rely heavily on attributed to conservationists actively promoting spillovers from no-take areas. A theoretical analy- exports of saiga ( Saiga tatarica ) horn to the Chi- sis of tapir hunting in Peruvian Amazonia showed 2 could sustain typi- nese traditional medicine market as a substitute that a source area of 9300 km 2 sink, if dispersal callevelsofhuntingina1700km for the horn of endangered rhinos. In October was directed towards that sink (Bodmer 2000). The 2002, saiga antelopes were fi nally placed on the degree to which source-sink population dynamics Red List of critically endangered species follow- can inform real-world management problems re- et al. ing this population crash (Milner-Gulland mains at best an inexact science. In tropical forests, 2001). In sum, rather few happy stories can be for example, we still lack basic data on the dispers- told of illegal wildlife commerce resulting in the al rate of most gamebird and large mammal spe- successful recovery of harvested wild popula- cies. Key management questions thus include the tions. However, these tend to operate through a potential and realized dispersal rate of target spe- stick-and-carrot approach at more than one link- ‘ ’ cies mediated by changes in density, the magni- age of the chain, controlling offtakes at the source, tude of the spillover effect outside no-take areas, the distribution and transport by intermediate how large these areas must be and still maintain fi traders, and/or nally the consumer demand at accessible hunted areas, and what landscape con- the end-point of trade networks. In fact, success- fi guration of no-take and hunted areas would ful management of any exploitation system will work best. It is also critical to ensure that no-take include enforceable measures ranging from de- fi areas are suf ciently large to maintain viable po- mand-side disincentives to supply-side incen- pulations in the face of overharvesting and habitat tives (see Box 6.2), with the optimal balance loss or degradation in surrounding areas (Peres between penalties on bad behavior or rewards et al. 2001; Claudet 2008). In addition to obvious on good behavior being highly context-speci fi c. differences in life-history between organisms in fi culties of managing many semi- Faced with dif marine and terrestrial systems, applying marine subsistence exploitation systems, such as small- management concepts to forest reserves may be scale sheries and bushmeat hunting, conserva- fi problematic due to differences in the local socio- tion biologists are increasingly calling for more political context in which no-take areas need to be realistic control measures that manipulate the accepted, demarcated and implemented (see large-scale spatial structure of the harvest. One Chapter 11). In particular, we need a better under- such method includes no-take areas, such as wild- standing of the opportunity costs in terms of life sanctuaries and marine protected areas © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

141 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 126 income and livelihoods lost from community rates of offtake, whereas others can be driven to activities, such as bushmeat hunting and timber local extinction by even the lightest levels of offtake. extraction, from designating no-take areas. This chapter reviews the effects of overexploi- · Finally, conservation biologists and policy-ma- tation in terrestrial as well as aquatic biomes. kers who bemoan our general state of data scarcity Options to manage resource exploitation are ddlers while Rome burns. Although areakinto fi also discussed. ne-tuning data are still needed on the life- fi more history characteristics and population dynamics of exploited populations, we already have a reason- Relevant websites ably good idea of what control measures need to be implemented in many exploitation systems. /www.bushmeat. Bushmeat Crisis Task Force: http:/ · Whether qualitative or quantitative restrictions org/portal/server.pt. are designed by resource managers seeking yield /www. Bioko Biodiversity Protection Program: http:/ · quotas based on economic optima or more preser- bioko.org/conservation/hunting.asp. Wildlife Conservation Society: http:/ /www.wcs.org/ vationist views supporting more radical reduc- · globalconservation/Africa/bushmeat. tions in biomass extraction, control measures will usually involve reductions in harvest capacity and mortality in exploited areas, or more and larger no- take areas (Pauly et al. 2002). Eradication of per- REFERENCES verse subsidies to unsustainable extractive indus- tries would often be a win-win option leading to Alroy, J. (2001). A multispecies overkill simulation of the stock recovery and happier days for resource users. , , Science late Pleistocene megafaunal mass extinction. 292 Co-management agreements with local commu- 1893-1896. The Not So Wild, Wild Anderson, T. L. and Hill, P. J. (2004). nities based on sensible principles can also work West: Property Rights on the Frontier . Stanford University provided we have the manpower and rural exten- Press, Stanford, CA. sion capacity to reach out to many source areas sh conservation. fi Andrews, C. (1990). The ornamental (Chapters 14 and 15). Ultimately, however, uncon- ,53 37 , Journal of Fish Biology 59. – trolled exploitation activities worldwide cannot be Asner, G. P., Knapp, D. E., Broadbent, E. N. (2005). et al. regulated unless we can count on political will and Science Selective Logging in the Brazilian Amazon. , 310 , enforcement of national legislation prescribing sus- 482. – 480 tainable management of natural resources, which Ball, S. M. J. (2004). Stocks and exploitation of East African are so often undermined by weak, absent, or cor- agship species for Tanzania ’ s Miombo fl blackwood: a rupt regulatory institutions. 7. – ,1 38 , woodlands. Oryx Barlow, J. and Peres, C. A. (2004). Ecological responses to res in central Amazonia: man- fi El Niño-induced surface agement implications for fl ammable tropical forests. , Philosophical Transactions of the Royal Society of London B Summary 380. – 359 , 367 Barlow, J. and Peres, C. A. (2008). Fire-mediated dieback Human exploitation of biological commodities · and compositional cascade in an Amazonian forest. Phil- involves resource extraction from the land, fresh- osophical Transactions of the Royal Society of London B , 363 , water bodies or oceans, so that wild animals, 1787 – 1794. plants or their products are used for a wide vari- et al. Baum, J. K., Myers, R. A., Kehler, D. G. (2003). Col- ety of purposes. lapse and conservation of shark populations in the Overexploitation occurs when the harvest rate Northwest Atlantic. Science , 299 , 389 – 392. · of any given population exceeds its natural re- Bennett, E. L. (2002). Is there a link between wild meat and placement rate. , 16 , 590 – 592 food security? Conservation Biology Many species are relatively insensitive to har- Hunting and wildlife trade Bennett, E. L. and Rao, M. (2002). · vesting, remaining abundant under relatively high in tropical and subtropical Asia: identifying gaps and © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

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143 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 128 Lewison, R. L., Freeman, S. A., and Crowder, L. B. (2004). fi sheries and aquaculture 2004 . FAO. (2004). The state of world sheries on threatened species: Quantifying the effects of fi Food and Agriculture Organization of the United the impact of pelagic longlines on loggerhead and leath- Nations, Rome. 231. – 7 , Ecology Letters erback sea turtles. , 221 ’ s Forests. Food and Agri- FAO. (2007). State of the World Maisels, F., Keming, E., Kemei, M., and Toh, C. (2001). The culture Organization of the United Nations, Italy, Rome. extirpation of large mammals and implications for mon- Godoy, R., Wilkie, D., Overman, H., et al. (2000). Valuation tane forest conservation: the case of the Kilum-Ijim For- of consumption and sale of forest goods from a Central – est, North-west Province, Cameroon. Oryx , 35 , 322 334. American rain forest. 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144 1 129 OVEREXPLOITATION Sustainable harvest of non-timber Peters, C. M. (1994). Montreal, and Center for International Forestry Research plant resources in tropical moist forest:an ecological (CIFOR), Bogor. Technical Series no. 33. . Biodiversity Support Program, Washington, primer ı (1999). ssimo, A., Alencar, A., et al. Nepstad, D. C., Ver DC. Large-scale impoverishment of Amazonian forests by Peters,C.M.,Gentry,A.H.,andMendelsohn,R.(1989). fi re. Nature 508. 398 , 505 – logging and , Nature , 339 , Valuation of an Amazonian rainforest. Nichols, E., Gardner, T. A., Peres, C. A., and Spector, 655 – 656. S. (2009). Co-declining mammals and dung beetles: an Redford, K. H. (1992). The empty forest. , 42 , BioScience impending ecological cascade. Oikos, 118 , 481 – 487. 412 – 422. Nuñez-Iturri, G., and Howe, H. F. (2007). Bushmeat and Redford, K. H. and P. Feinsinger. (2001). 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(2008). ing and habitat fragmentation on Amazonian forest ver- the contribution of wildlife trade management to sustainable tebrates. 1505. , 1490 – 15 , Conservation Biology livelihoods and the Millennium Development Goals . TRAF- Peres, C. A. and Dolman, P. (2000). Density compensation FIC International and WWF International. in neotropical primate communities: evidence from 56 Ross, E. B. (1978). Food taboos, diet, and hunting strategy: hunted and non-hunted Amazonian forests of varying the adaptation to animals in Amazon cultural ecology. 122 productivity. , Oecologia Current Anthropology , 19 ,1 – 36. , 175 – 189. Samant, S. S., Dhar, U., and Palni, L. M. S. (1998). Medicinal Peres, C. A. and Lake, I. R. (2003). Extent of nontimber plants of Indian Himalaya: diversity distribution potential resource extraction in tropical forests: accessibility to . G. B. Pant Institute of Himalayan Environment values Con- game vertebrates by hunters in the Amazon basin. and Development, Almora, India. 535. servation Biology 17 , 521 – , Sheil, D. and Salim, A. (2004). Forest trees, elephants, stem Peres, C. A. and van Roosmalen, M. (2003). Patterns of 521. – , 505 36 , Biotropica scars and persistence. primate frugivory in Amazonia and the Guianan shield: (2008). Corre- et al. Sodhi, N. S., Koh, L. P., Peh, K. S.-H., implications to the demography of large-seeded plants lates of extinction proneness in tropical angiosperms. in overhunted tropical forests. In D. Levey, W. Silva and Diversity and Distributions 14 10. – , ,1 Seed dispersal and frugivory: ecology, evolu- M. Galetti, eds c Steadman, D. A. (1995). Prehistoric extinctions of Paci fi – , pp. 407 423. CABI International, tion and conservation , Science islands birds: biodiversity meets zooarcheology. Oxford, UK. 1131. – , 1123 267 Peres C. A. and Palacios, E. (2007). Basin-wide effects of fi Swaine, M. D. and Whitmore, T. C. (1988). On the de ni- game harvest on vertebrate population densities in Am- tion of ecological species groups in tropical rain forests. azonian forests: implications for animal-mediated seed ,81 86. – Vegetatio , 75 – 315. , Biotropica , 304 39 dispersal. Terborgh, J., Nunez-Iturri, G., Pitman, N. C. A., et al. (2008). Peres, C. A., Baider, C., Zuidema, P. A., . (2003). Demo- et al Tree recruitment in an empty forest. , 89 , 1757 – Ecology graphic threats to the sustainability of Brazil nut 1768. , 2112 – 2114. Science , exploitation. 302 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

145 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 130 - fi The sunken billions: the economic justi World Bank. (2008). ’ s medicinal and aromatic plants: TRAFFIC. (1998). Europe cation for fi . Agriculture and Rural Develop- sheries reform . TRAFFIC International, their use, trade and conservation ment Department. The World Bank and Food and Cambridge, UK. Agriculture Organization, Washington, DC. s driving the wildlife trade? A review ’ What TRAFFIC. (2008). Worm, B., Barbier, E. B., Beaumont, N., et al. (2006). of expert opinion on economic and social drivers of the wildlife Impacts of biodiversity loss on ocean ecosystem services. trade and trade control efforts in Cambodia, Indonesia, Lao – , 787 314 Science , 790. PDR and Vietnam . World Bank, Washington, DC. Wright, J. P. and Jones, C. G. (2006). The concept of organ- US Census Bureau. (2006). 2006 National survey of fi shing, hunt- isms as ecosystem engineers ten years on: progress, lim- ing, and wildlife-associated recreation .U.S.Departmentofthe BioScience itations and challenges. 209. – , 203 56 , Interior, Fish and Wildlife Service, and U.S. Department of Wright, S. J. (2003). The myriad effects of hunting for Commerce, US Census Bureau, Shepherdston, WV. Perspectives in vertebrates and plants in tropical forests. Wang, B. C., Leong, M. T., Smith, T. B., and Sork, V. L. – Plant Ecology, Evolution and Systematics , 6 ,73 86. (2007). Hunting of mammals reduces seed removal and Wright, S. J., Zeballos, H., Dominguez, I., (2000). et al. Antrocaryon klainea- dispersal from the Afrotropical tree, Poachers alter mammal abundance, seed dispersal , – 347. (Anacardiaceae). num , 340 39 Biotropica and seed predation in a Neotropical forest. Conservation Warkentin, I. G., Bickford, D., Sodhi, N. S., and Bradshaw, Biology – 239. , 227 , 14 Conservation C. J. A. (2009). Eating frogs to extinction. Wright, S. J., Hernandez, A., and Condit, R. (2007). 23 , 1056 – 1059. , Biology The bushmeat harvest alters seedling banks by favoring Final Report on Forest Capital . World Com- WCFSD. (1998). lianas, large seeds and seeds dispersed by bats, birds mission of Forests and Sustainable Development., Cam- bridge University Press, Cambridge, UK. Biotropica 371. , 39 , 363 and wind. – Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

146 1 CHAPTER 7 Invasive species Daniel Simberloff Aninvasivespeciesisonethatarrives(oftenwith — especially islands (see Box 7.2) — intro- world human assistance) in a habitat it had not previ- duced species comprise a large proportion of all ously occupied, then establishes a population species. For instance, for the Hawaiian islands, and spreads autonomously. Species invasions almost half the plant species, 25% of insects, 40% are one of the main conservation threats today of birds, and most freshwater fi shes are intro- and have caused many species extinctions. The duced, while the analogous fi gures for Florida greatmajorityofsuchinvasionsarebyspecies are 27% of plant species, 8% of insects, 5% of introduced from elsewhere, although some na- birds, and 24% of freshwater shes. Not all intro- fi tive species have become invasive in newly occu- duced species become invasive, however. Many pied habitats (see Box 7.1). In some areas of the plant species imported as ornamentals persist in Box 7.1 Native invasives Daniel Simberloff with the introduction of European genotypes Although the great majority of invasive species th as a forage crop in the 19 are introduced, occasionally native plant century (Lavergne species have become invasive, spreading and Molofsky 2007). rapidly into previously unoccupied habitats. The second category of native invasives arises These invasions fall into two categories, both from human modi cation of the environment. fi rst, a native involving human activities. In the fi For instance, in western Europe, the grass species that is rather restricted in range and , previously a minor Elymus athericus habitat is supplemented with introductions component of high intertidal vegetation, from afar that have new genotypes, and the began spreading seaward because of increased new genotypes, or recombinants involving the nitrogen in both aerial deposition and runoff, new genotypes, become invasive. An example and it now occupies most of the intertidal in Phragmites in North America is common reed ( et al. many areas (Valéry 2004). The plant ), which was present for at least australis apparently uses the nitrogen to increase its thousands of years and is probably native, but tolerance or regulation of salt. In various which spread widely, became much more regions of the western United States, Douglas common, and began occupying more habitats Pseudotsuga menziesii ) and several other r( fi beginning in the mid ‐ nineteenth century. This tree species have invaded grasslands and invasion is wholly due to the introduction of fi shrublands as a result of re suppression, Old World genotypes at that time, probably in increased grazing by livestock, or both. Natural soil ballast (Saltonstall 2002). Similarly, reed fi re had precluded them, and when re was fi ), native to Phalaris arundinacea canarygrass ( suppressed, livestock served the same role North America but previously uncommon, (Simberloff 2008). By contrast, Virginia pine became highly invasive in wetland habitats Pinus virginiana ) in the eastern United States ( continues 131 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

147 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 132 Box 7.1 (Continued) emy of Sciences of the United States of America , 99 , res were invaded serpentine grasslands when fi 2449. – 2445 ‐ suppressed and long time grazing practices Simberloff, D. (2008). Invasion biologists and the biofuels were restricted (Thiet and Boerner 2007). Weed Science boom: Cassandras or colleagues? , 56 , 872. 867 – REFERENCES Thiet, R. K and Boerner, R. E. J. (2007). Spatial patterns Lavergne, S. and Molofsky, J. (2007). Increased genetic of ectomycorrhizal fungal inoculum in arbuscular my- variation and evolutionary potential drive the success of corrhizal barrens communities: implications for Proceedings of the National Academy an invasive grass. . 17 , , Mycorrhiza Pinus virginiana controlling invasion by , of Sciences of the United States of America , 104 507 – 517. 3883 3888. – Valéry, L., Bouchard, V., and Lefeuvre, J. ‐ C. (2004). Saltonstall, K. (2002). Cryptic invasion by a non native ‐ Impact of the invasive native species Elymus athericus , genotype of the common reed, Phragmites australis , Wetlands on carbon pools in a salt marsh. Proceedings of the National Acad- into North America. 276. – , 268 24 Box 7.2 Invasive species in New Zealand Daniel Simberloff changes nutrient cycling by mixing organic and Many islands have been particularly af fl icted by mineral layers of the soil. Of 120 introduced introduced species, even large islands such as bird species, 34 are established. To some extent those comprising New Zealand (Allen and Lee they probably compete with native birds and 2006). New Zealand had no native mammals, prey on native invertebrates, but their impact is except for three bat species but now has 30 poorly studied and certainly not nearly as introduced mammals. Among these, several severe as that of introduced mammals. are highly detrimental to local fauna and/or European brown trout ( Salmo trutta ) are fl ora. The Australian brushtail possum widely established and have caused the local Trichosurus vulpecula ; Box 7.2 Figure) now ( sh species. fi extirpation of a number of numbers in the millions and destroys Among the estimated 2200 established broadleaved native trees, eating bird eggs and introduced invertebrate species in chicks as well. Paci fi c and Norway rats are also devastating omnivores that particularly plague native birds. Introduced carnivores — the stoat ), weasel ( ), ferret M. nivalis ( Mustela erminea ( ) Erinaceus europaeus ), and hedgehog ( M. furo are all widespread and prey on various — combinations of native birds, insects, skinks, Sphenodon geckos, and an endemic reptile ( ). Many ungulates have been punctatus introduced, of which European red deer ( Cervus elaphus ) is most numerous. Trampling and grazing by ungulates has greatly damaged Sus native vegetation in some areas. Feral pigs ( scrofa ) are now widespread in forest and scrub habitats, and their rooting causes erosion, Box 7.2 Figure Brushtail possum. Photograph by Rod Morris. reduces populations of some plant species, and continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

148 1 INVASIVE SPECIES 133 Box 7.2 (Continued) plant species, and even these have been Vespula New Zealand, German wasps ( fi xers outcompeted by introduced nitrogen ‐ V. vulgaris ) and common wasps ( germanica ) such as gorse ( Ulex europaeus ), Scotch broom have probably had the most impact, especially ( Cytisus scoparius ), and tree lupine ( Lupinus by monopolizing the honeydew produced by ). As in other areas (see above), in arboreus native scale insects that had supported several parts of New Zealand these nitrogen ‐ xers fi Nestor native bird species, including the kaka ( have, by fertilizing the soil, favored certain ), the tui ( meridionalis Prosthemadera native species over others and have induced an Anthornis ), and the bellbird ( novaeseelandiae invasional meltdown by allowing other melanura ). introduced plant species to establish. About 2100 species of introduced plants are Given the enormous number of introduced now established in New Zealand, species invading New Zealand and the many outnumbering native species. Several tree sorts of impacts these have generated, it is not species introduced about a century ago are surprising that New Zealand enacted the rst fi now beginning to spread widely, the lag comprehensive national strategy to address the caused by the fact that trees have long life entire issue of biological invasions, the cycles. Most of the introduced plants in New Biosecurity Act of 1993. Zealand, including trees, invade largely or wholly when there is some sort of disturbance, clearing or forestry. However, such as land ‐ once established, introduced plants have in REFERENCE some instances prevented a return to the Biological invasions Allen, R. B. and Lee, W. G., eds (2006). original state after disturbance stopped. New . Springer, Berlin, Germany. in New Zealand Zealand also has relatively few nitrogen fi xing ‐ gardens with human assistance but cannot estab- 7.1 Invasive species impacts lishinlessmodi fi ed habitats. The fraction of in- 7.1.1 Ecosystem modi fi cation troduced species that establish and spread is a matter under active research, but for some organ- The greatest impacts of invasive species entail isms it can be high. For example, half of the modifying entire ecosystems, because such mod- sh,mammal,andbirdspeciesintro- fi freshwater i fi cations are likely to affect most of the originally duced from Europe to North America or vice- resident species. Most obviously, the physical versa have established populations, and of structure of the habitat can be changed. For in- these, more than half be came invasive (Jeschke stance, in Tierra del Fuego, introduction of a few and Strayer 2005). North American beavers ( )in Castor canadensis Invasive species can produce a bewildering 1946 has led to a population now over 50 000, array of impacts, and impacts often depend on and in many areas they have converted forests of context; the same introduced species can have southern beech ( spp.) to grass- and Nothofagus minimal effects on native species and ecosys- et al. sedge-dominated meadows (Lizarralde tems in one region but can be devastating 2004). In the Florida Everglades, introduced Aus- somewhere else. Further, the same species can tralian paperbark ( Melaleuca quinquenervia ) trees affect natives in several different ways simul- have effected the opposite change, from grass- taneously. However, a good way to begin to and sedge-dominated prairies to nearly mono- understand the scope of the threat posed by et al. c paperbark forests (Schmitz speci 1997). fi biological invasions is to classify the main In parts of Hawaii, Asian and American man- types of impacts. grove species have replaced beach communities © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

149 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 134 CONSERVATION BIOLOGY FOR ALL of herbs and small shrubs with tall mangrove Introduced species can change entire forests (Allen 1998). re regime (see fi ecosystems by changing the Introduced plant species can modify an entire Chapter 9). The invasion of the Florida Ever- ecosystem by overgrowing and shading out native glades by Australian paperbark trees, noted species. South American water hyacinth ( Eichhor- above, is largely due to the fact that paperbark ) now covers parts of Lake Victoria in nia crassipes catches res than fi re easily and produces hotter fi Africa (Matthews and Brand 2004a), many lakes the grasses and sedges it replaces. The opposite and rivers in the southeastern United States transformation, from forest to grassland, can (Schardt 1997), and various waterbodies in Asia also be effected by a changed fi re regime. In and Australia (Matthews and Brand 2004b), often Hawaii, African molassesgrass ( Melinis minuti- smothering native submersed vegetation. Vast ) and tropical American tufted beardgrass ora fl quantities of rotting water hyacinth, and conse- ) have replaced na- Schizachyrium condensatum ( quent drops in dissolved oxygen, can also affect tive-dominated woodland by virtue of increased many aquatic animal species. Similar overgrowth fi ’ Antonio and Vitou- re frequency and extent (D Caulerpa occurs in the Mediterranean Sea, where sek 1992). taxifolia (Figure 7.1), an alga from the tropical Introduced plants can change entire ecosys- c Ocean, replaces seagrass mea- southwest Paci fi tems by modifying water or nutrient regimes. At dows over thousands of hectares, greatly changing Eagle Borax Spring in California, Mediterranean the animal community (Meinesz 1999). salt cedars ( Tamarix spp.) dried up a large marsh ) Spartina anglica A new species of cordgrass ( et al. (McDaniel 2005), while in Israel, Australian arose in England in the late nineteenth century by eucalyptus trees were deliberately introduced to hybridization between a native cordgrass and an drain swamps (Calder 2002). By fertilizing nitro- introduced North American species. The new spe- xing plants gen-poor sites, introduced nitrogen- fi cies invaded tidal mud fl ats and, trapping much can favor other exotic species over natives. On the more sediment, increased elevation and converted geologically young, nitrogen-poor volcanic is- fl ats to badly drained, dense salt marshes with mud retree ( Morella faya ), a nitro- land of Hawaii, fi different animal species (Thompson 1991). The hy- fi xing shrub from the Azores, creates gen- brid species was later introduced to New Zealand conditions that favor other introduced species and the state of Washington with similar impacts. that previously could not thrive in the low-nutrient Caulerpa taxifolia . Photograph by Alex Meinesz. Figure 7.1 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

150 1 135 INVASIVE SPECIES soil and disfavor native plants that had evolved to 7.1.3 Aggression and its analogs tolerate such soil (Vitousek 1986). The red imported fi re ant ( Solenopsis invicta ) from Pathogens that eliminate a previously domi- southern South America has spread through the nant plant can impact an entire ecosystem. In southeastern United States and more recently has rst half of the twentieth century, Asian chest- the fi invaded California. It attacks other ant species it nut blight ( ) ripped Cryphonectria parasitica encounters, and in disturbed habitats (which through eastern North America, effectively elim- comprise much of the Southeast) this aggression ), a inating American chestnut ( Castanea dentata has caused great declines in populations of native tree that had been common from Georgia ant species (Tschinkel 2006). The Argentine ant through parts of Canada and comprised at least ), also native to South Ameri- Linepithema humile ( 30% of the canopy trees in many forests (William- ca, similarly depresses populations of native ant son 1996). This loss in turn led to substantial species in the United States by attacking them structural changes in the forest, and it probably (Holway and Suarez 2004). The Old World greatly affected nutrient cycling, because chest- Dreissena polymorpha ; Figure 7.2), zebra mussel ( nut wood, high in tannin, decomposes slowly, spreading throughout much of North America, while the leaves decompose very rapidly (Ellison threatens the very existence of a number of native et al. 2005). Chestnut was largely replaced by oaks freshwater bivalve species, primarily by settling spp.), which produce a recalcitrant litter. Quercus ( on them in great number and suturing their Because this invasion occurred so long ago, few valves together with byssal threads, so that they of its effects were studied at the time, but it is 1998). Al- et al. suffocate or starve (Ricciardi known that at least seven moth species host-spe- though plants do not attack, they have an analo- ci fi c to chestnut went extinct (Opler 1978). Such gous ability to inhibit other species, by producing pathogens are also threats to forest industries or sequestering chemicals. For example, the Afri- founded on introduced species as well as natives, Mesembryanthemum crys- can crystalline ice plant ( as witness the vast plantations in Chile of North ) sequesters salt, and when leaves fall and tallinum ) now Pinus radiata American Monterrey pine ( decompose, the salt remains in the soil, rendering threatened by recently arrived Phytophthora pini- it inhospitable to native plants in California that 2008). et al. (Durán folia cannot tolerate such high salt concentrations (Vivrette and Muller 1977). Diffuse knapweed ) from Eurasia and spotted Centaurea diffusa ( 7.1.2 Resource competition knapweed ( ) from Europe are both C. stoebe major invaders of rangelands in the American In Great Britain, the introduced North American West. One reason they dominate native range gray squirrel ( Sciurus carolinensis )foragesfor plants in the United States is that they produce nuts more ef fi ciently than the native red squirrel ), leading to the decline of the Sciurus vulgaris ( latter species (Williamson 1996). The same North American gray squirrel species has re- cently invaded the Piedmont in Italy and is spreading, leading to concern that the red squir- rel will also decline on the mainland of Europe as it has in Britain (Bertolino et al. 2008). The )fromSouth- house gecko ( Hemidactylus frenatus east Asia and parts of Africa has invaded many c islands, lowering insect populations that fi Paci serveasfoodfornativelizards,whosepopula- tions have declined in some areas (Petren and Zebra mussel. Photograph by Tony Ricciardi. Figure 7.2 Case 1996). © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

151 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 136 root exudates that are toxic to native plants (Call- nested on the ground and were highly susceptible away and Ridenour 2004). An invasive intro- to the invaders. Introduced rats, for example, duced plant can also dominate a native species have caused the extinction of at least 37 species by interfering with a necessary symbiont of the and subspecies of island birds throughout the native. For instance, many plants have estab- world (Atkinson 1985). The brown tree snake lished mutualistic relationships with arbuscular ( Boiga irregularis ; Figure 7.3), introduced to mycorrhizal fungi, in which the fungal hyphae Guam from New Guinea in cargo after World penetrate the cells of the plants ’ roots and aid War II, has caused the extinction or local extirpa- the plants to capture soil nutrients. Garlic mus- tion of nine of the twelve native forest bird spe- Alliaria petiolata ) from Europe, Asia, and tard ( cies on Guam and two of the eleven native lizard North Africa is a highly invasive species in the species (Lockwood et al. 2007). For these native ground cover of many North American wood- species, an arboreal habitat was no defense lands and fl oodplains. Root exudates of garlic against a tree-climbing predator. Another famous mustard, which does not have mycorrhizal as- introduced predator that has wreaked havoc with sociates, are toxic to arbuscular mycorrhizal native species is the Nile perch ( ), Lates niloticus fungi found in North American soils (Callaway deliberately introduced to Lake Victoria in the et al. 2008). shery would be estab- fi 1950s in the hope that a lished to provide food and jobs to local commu- nities (Pringle 2005). Lake Victoria is home of one 7.1.4 Predation of the great evolutionary species radiations, the shes. About half fi hundreds of species of cichlid One of the most dramatic and frequently seen of them are now extinct because of predation by impacts of introduced species is predation on the perch, and several others are maintained only native species. Probably the most famous cases 2007). by captive rearing (Lockwood et al. are of mammalian predators such as the ship rat Many predators have been deliberately intro- ( ), Paci R. norvegicus fi c ), Norway rat ( Rattus rattus of previously in- ” duced for “ biological control rat ( ), small Indian mongoose ( R. exulans Herpestes troduced species (see below), and a number of auropunctatus ), and stoat ( ) intro- Mustela erminea these have succeeded in keeping populations of duced to islands that formerly lacked such spe- the target species at greatly reduced levels. For cies. In many instances, native bird species, not instance, introduction of the Australian vedalia having evolved adaptations to such predators, Brown tree snake. Photograph by Gad Perry. Figure 7.3 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

152 1 INVASIVE SPECIES 137 ) in 1889 controlled ladybeetle ( Rodolia cardinalis American cassava mealybug ( Phenacoccus mani- ) Icerya purchasi Australian cottony-cushion scale ( hoti ), invading extensive cassava-growing parts on citrus in California (Caltagirone and Doutt of Africa, often destroys more than half the crop 1989). However, some predators introduced for yield (Norgaard 1988), while in the United biological control have attacked non-target spe- Diuraphis States, the Russian wheat aphid ( cies to the extent of causing extinctions. One of ) caused US$600 million damage in just noxia the worst such disasters was the introduction of fi three years (Of ce of Technology Assessment Euglandina rosea the rosy wolf snail ( ), native to 1993). In forests of the eastern United States, the fi Central America and Florida, to many Paci c European gypsy moth ( Lymantria dispar ) caused islands to control the previously introduced a similar amount of damage in only one year ). The predator giant African snail ( Achatina fulica (Of fi ce of Technology Assessment 1993). In high not only failed to control the targeted prey (which elevation forests of the southern Appalachian grows to be too large for the rosy wolf snail to Mountains, the Asian balsam woolly adelgid attack it) but caused the extinction of over 50 ( Adelges piceae ) has effectively eliminated the species of native land snails (Cowie 2002). The r tree (Rabenold fi previously dominant Fraser small Indian mongoose, implicated as the sole et al. 1998), while throughout the eastern United cause or a contributing cause in the extinction of States the hemlock woolly adelgid ( A. tsugae )is several island species of birds, mammals, and killing most hemlock trees, which often formed frogs, was deliberately introduced to all these distinct moist, cool habitats amidst other tree islands as a biological control agent for intro- species (Ellison et al. 2005). duced rats (Hays and Conant 2006). The mosqui- Plant-eating insects have been successful in sh ( to ) from Mexico and Central nis fi fi Gambusia af many biological control projects for terrestrial America has been introduced to Europe, Asia, s ’ and aquatic weeds. For instance, in Africa Africa, Australia, and many islands for mosquito Lake Victoria, a massive invasion of water hya- control. Its record on this score is mixed, and cinth was brought under control by introduction there is often evidence that it is no better than Neochetina eich- of two South American weevils, native predators at controlling mosquitoes. How- horniae (Matthews and Brand N. bruchi and ever, it preys on native invertebrates and small 2004a); these have also been introduced to attack shes and in Australia is implicated in extinction fi water hyacinth in tropical Asia (Matthews and of several fi sh species (Pyke 2008). Brand 2004b). The South American alligator- weed ea beetle ( fl Agasicles hygrophila ) has mini- mized the invasion of its South American host 7.1.5 Herbivory plant ( Alternanthera philoxeroides ) in Florida (Cen- ter et al. 1997) and contributed greatly to its fl ora of Introduced herbivores can devastate the control in slow-moving water bodies in Asia areas lacking similar native species, especially on ) introduced islands. Goats ( Capra aegagrus hircus (Matthews and Brand 2004b). A particularly fa- to the island of St. Helena in 1513 are believed to mous case was the introduction of the South 100 endemic  have eliminated at least half of American cactus moth ( Cactoblastis cactorum )to Australia, where it brought a massive invasion of plant species before botanists had a chance to prickly pear cactus ( Opuntia spp.) under control Or- record them (Cronk 1989). European rabbits ( rst fi et al. 2001). In probably the (Zimmermann yctolagus cuniculus ) introduced to islands world- successful weed biological control project, a Bra- wide have devastated many plant populations, zilian cochineal bug ( Dactylopius ceylonicus ) vir- often by bark-stripping and thus killing shrubs and seedling and sapling trees. Rabbits also often tually eliminated the smooth prickly pear cause extensive erosion once vegetation has been ( Opuntia vulgaris ) from India (Doutt 1964). In destroyed (Thompson and King 1994). Damage 1913, the same insect was introduced to South Africa and effectively eliminated the same plant to forests and crop plants by introduced herbi- (Doutt 1964). vores is often staggering. For instance, the South © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

153 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 138 CONSERVATION BIOLOGY FOR ALL However, occasionally, biological control intro- 7.1.6 Pathogens and parasites ductions of herbivorous insects have devastated Many introduced plant pathogens have modi fi ed non-target native species. The same cactus moth entire ecosystems by virtually eliminating domi- introduced to Australia was introduced to control nant plants. The chestnut blight was discussed pest prickly pear on the island of Nevis in the West above. A viral disease of ungulates, rinderpest, Indies. From there, it island-hopped through the introduced to southern Africa from Arabia or West Indies and reached Florida, then spread India in cattle in the 1890s, attacked many native further north and west. In Florida, it already ungulates, with mortality in some species reach- threatens the very existence of the native sema- ing 90%. The geographic range of some ungulate phore cactus ( O. corallicola ), and there is great species in Africa is still affected by rinderpest. concern that this invasion, should it reach the Because ungulates often play key roles in vegeta- American Southwest and Mexico, would not tion structure and dynamics, rinderpest impacts species but only threaten other native Opuntia affected entire ecosystems (Plowright 1982). also affect economically important markets for Of course, many introduced diseases have af- (Zimmermann ornamental and edible Opuntia fected particular native species or groups of them et al. Rhinocyllus con- 2001). The Eurasian weevil ( without modifying an entire ecosystem. For in- icus ), introduced to Canada and the United Plasmodium re- stance, avian malaria, caused by States to control introduced pest thistles, attacks , introduced with Asian birds lictum capristranoae et al. 1997), severalnativethistlesaswell(Louda and vectored by previously introduced mosqui- and this herbivory has led to the listing of the toes, contributed to the extinction of several na- native Suisun thistle ( var. Cirsium hygrophilum tive Hawaiian birds and helps restrict many of ) on the U.S. Endangered Species hygrophilum the remaining species to upper elevations, where List (US Department of the Interior 1997). In mosquitoes are absent or infrequent (Woodworth each of these cases of herbivorous biological et al. fi sh plague ( Aphano- 2005). In Europe, cray control agents threatening natives, the intro- ), introduced with the North Ameri- myces astaci ducedherbivorewasabletomaintainhighnum- Pacifastacus lenusculus ; fi can red signal cray sh ( bers on alternative host plants (such as the Figure 7.4 and Plate 7) and also vectored by targeted hosts), so decline of the native did not sh fi the subsequently introduced Lousiana cray cause herbivore populations to decline. sh ( Astacus astacus ). Photograph by David Holdich. fi sh (right) and a native European cray fi North American red signal cray Figure 7.4 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

154 1 INVASIVE SPECIES 139 ( Procambarus clarkii ), has devastated native Euro- Parasites and pathogens have also been used sh populations (Goodell 2000). pean cray fi et al. successfully in biological control projects against fi sh parasite Myxosoma cerebralis The European , introduced target hosts. For instance, the South shes, fi which causes whirling disease in salmonid American cassava mealybug in Africa, discussed Oncor- infected North American rainbow trout ( above, has been partly controlled by an introduced ) that had been previously intro- hynchus mykiss Epidinocarsis lopezi South American parasitic wasp, duced to Europe and were moved freely among (Norgaard 1988), while the European yellow clo- European sites after World War II. Subsequently, ver aphid ( Therioaphis trifolii ), a pest of both clover infected frozen rainbow trout were shipped to and alfalfa, is controlled in California by three North America, and the parasite somehow got Praon palitans, Trioxys introduced parasitic wasps, into a trout hatchery in Pennsylvania, from utilis ,and Aphelinus semi fl avus (Van Den Bosch which infected rainbow trout were shipped to 1964). The New World myxoma virus, intro- et al. many western states. In large areas of the West, duced to mainland Europe (where the European most rainbow trout contracted the disease and rabbit is native) and Great Britain and Australia sheries utterly collapsed (Bergersen and sport fi (where the rabbit is introduced), initially caused Anderson 1997). Introduced plant parasites can devastating mortality (over 90%). However, the greatly damage agriculture. For example, parasit- initially virulent viral strains evolved to be more ic witchweed ( Striga asiatica ) from Africa reached benign, while in Great Britain and Australia, the southeastern United States after World War rabbits evolved to be more resistant to the virus. II, probably arriving on military equipment. It Mortality has thus decreased in each successive icts great losses on crops that are grasses (in- in fl epidemic (Bartrip 2008). cluding corn) and has been the target of a lengthy, expensive eradication campaign (Eplee 2001). 7.1.7 Hybridization Introduction of vectors can also spread not only introduced pathogens (e.g. the mosquitoes vector- ciently closely fi If introduced species are suf ing avian malaria in Hawaii) but also native ones. related to native species, they may be able to Cyathocotyle For example, the native trematode mate and exchange genes with them, and a suf fi - cient amount of genetic exchange (introgression) bushiensis , an often deadly parasite of ducks, has can so change the genetic constitution of the na- reached new regions along the St. Lawrence River tive population that we consider the original spe- recently as its introduced intermediate host, the ), has in- Bithynia tentaculata Eurasian faucet snail ( cies to have disappeared a sort of genetic — vaded (Sauer et al. 2007). Introduced parasites or extinction. This process is especially to be feared pathogens and vectors can interact in complicated when the invading species so outnumbers the ways to devastate a native host species. Chinese native that a native individual is far more likely grass carp ( Ctenopharyngodon idella ) infected with to encounter the introduced species than a native as a prospective mate. The last gasp of a fi sh Bothriocephalus acheilognathi the Asian tapeworm native to Texas, , entailed Gambusia amistadensis were introduced to Arkansas in 1968 to control the species being hybridized to extinction introduced aquatic plants and spread to the Mis- sissippi River. There the tapeworm infected native through interbreeding with introduced mosquito fi shes, including a popular bait fi sh, the red shiner fi G. amistadensis sh (Hubbs and Jensen 1984), ). Fishermen or bait dealers then Notropis lutrensis ( fi while several shes currently on the United States carried infected red shiners to the Colorado River, Endangered Species List are threatened at least from which by 1984 they had reached a Utah partly by hybridization with introduced rainbow trout. The North American mallard ( Anas platyr- tributary, the Virgin River. In the Virgin River, hynchos ), widely introduced as a game bird, inter- n fi the tapeworm infected and killed many wound breeds extensively with many congeneric species ), a native minnow al- ( Plagopterus argentissimus ready threatened by dams and water diversion and threatens the very existence of the endemic projects (Moyle 1993). New Zealand grey duck ( A. superciliosa superciliosa ) © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

155 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 140 and the Hawaiian duck ( A. wyvilliana ), as well as, before the European mink males. The European perhaps, the yellowbilled duck ( A. undulata )and mink females subsequently abort the hybrid em- the Cape shoveller ( A. smithii )inAfrica(Rhymer bryos, so no genes can be exchanged between the and Simberloff 1996, Matthews and Brand 2004a). species, but these females cannot breed again European populations of the white-headed duck during the same season, a severe handicap to a )restrictedtoSpain,are ( Oxyura leucocephala small, threatened population (Maran and Hentto- threatened by hybridization and introgression nen 1995). with North American ruddy ducks ( O. jamaicensis ) et al. 2007). The latter had been (Muñoz-Fuentes 7.1.8 Chain reactions introduced years earlier to Great Britain simply as an ornamental; they subsequently crossed the Some impacts of introduced species on natives Channel, spread through France, and reached entail concatenated chains of various interactions: Spain. species A affecting species B, then species B af- Availability and increasing sophistication of fecting species C, species C affecting species D, molecular genetic techniques has led to the rec- and so forth. The spread of the Asian parasitic tapeworm from Arkansas ultimately to infect the ognition that hybridization and introgression fi )in Plagopterus argentissimus n minnow ( wound between introduced and native species is far Utah is an example. However, chains can be even more common than had been realized. Such hybridization can even lead to a new species. more complex, almost certainly unforeseeable. In the cordgrass ( Spartina ) case discussed An example involves the devastation of Europe- above, occasional hybrids were initially sterile, an rabbit populations in Britain by New World until a chromosomal mutation (doubling of myxoma virus, described above. Caterpillars of chromosome number) in one of them produced Maculina arion the native large blue butter fl y( )in Great Britain required development in under- a fertile new polyploid species, which became . ground nests of the native ant Myrmica sabuleti highly invasive (Thompson 1991). A similar case The ant avoids nesting in overgrown areas, which involves Oxford ragwort ( ), a Senecio squalidus hybrid of two species from Italy, introduced for centuries had not been problematic because of to the Oxford Botanical Garden ca. 1690. S. squa- grazing and cultivation. However, changing land escaped, fi lidus rst spread through Oxford, and use patterns and decreased grazing led to a situa- then during the Industrial Revolution through tion in which rabbits were the main species main- much of Great Britain along railroad lines, taining suitable habitat for the ant. When the virus devastated rabbit populations, ant popula- producing sterile hybrids with several native tions declined to the extent that the large blue Senecio . A chromosomal muta- British species of butter fl y was extirpated from Great Britain (Rat- tion (doubling of chromosome number) of a S. vulgaris hybrid between S. squalidus and cliffe 1979). In another striking chain reaction, (groundsel) produced the new polyploid species landlocked kokanee salmon ( Oncorhynchus S. cambrensis (Welsh groundsel) (Ashton and ), were introduced to Flathead Lake, Mon- nerka Abbott 1992). tana in 1916, replacing most native cutthroat It is possible for hybridization to threaten a ) and becoming the main sport O. clarki trout ( sh. The kokanee were so successful that they fi species even when no genetic exchange occurs. spread far from the lake, and their spawning Many populations of the European mink ( Mustela populations became so large that they attracted lutreola ) are gravely threatened by habitat de- M. vison ), widely struction. North America mink ( large populations of bald eagles ( Haliaeetus leuco- introduced in Europe to foster a potential fur- Ursus arctos horribilis ), cephalus ), grizzly bears ( bearing industry, have escaped and established and other predators. Between 1968 and 1975, many populations. In some sites, many female Mysis relicta ), native to large opossum shrimp ( European mink hybridize with male American deep lakes elsewhere in North America and in Sweden, were introduced to three lakes in the mink, which become sexually mature and active © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

156 1 INVASIVE SPECIES 141 upper portion of the Flathead catchment in order the introduced snail and the introduced trema- to increase production of kokanee; the shrimp tode combine to produce more mortality in ducks drifted downstream into Flathead Lake by 1981 than either would likely have accomplished and caused a sharp, drastic decline in populations alone. This is but one of myriad instances of melt- of cladocerans and copepods they preyed on. down. However, the kokanee also fed on these prey, Sometimes introduced animals either pollinate and kokanee populations fell rapidly, in turn introduced plants or disperse their seeds. For causing a precipitous decline in local bald eagle Ficus gs ( fi instance, spp.) introduced to Florida 1991; et al. and grizzly bear numbers (Spencer had until ca. 20 years ago remained where they Figure 7.5). were planted, the species unable to spread be- cause the host-speci g wasps that pollinate fi c fi the fi gs in their native ranges were absent, so 7.1.9 Invasional meltdown gs could not produce seeds. That situation the fi An increasing number of studies of invasion fi g- changed abruptly upon the arrival of the effects have pointed to a phenomenon called wasps of three of the fi g species, which now in which two or more ” invasional meltdown “ , has F. microcarpa produce seeds. One of them, introduced species interact in such a way that become an invasive weed, its seeds dispersed by the probability of survival and/or the impact of 1991). On the et al. birds and ants (Kauffman at least one of them is enhanced (Simberloff and island of La Réunion, the red-whiskered bulbul Von Holle 1999). In the above example of an ( Pycnonotus jocosus ), introduced from Asia via Bithynia tentaculata ), vec- introduced faucet snail ( Mauritius, disperses seeds of several invasive toring a native trematode parasite of ducks and introduced plants, including Rubus alceifolius, ’ s range, a re- thereby expanding the trematode Cordia interruptus , and Ligustrum robustrum , cent twist is the arrival of a European trematode which have become far more problematic since Bithynia ). Leyogonimus polyoon ( also vectors this et al. the arrival of the bulbul (Baret 2006). The species, which has turned out also to be lethal to ) was in- Asian common myna ( Acridotheres tristis ducks (Cole and Friend 1999). So in this instance, troduced to the Hawaiian islands as a biological phytop- McDonald Creek copepod lankton cladoceran kokanee opossum shrimp salmon Flathead Lake lake trout Shrimp stocking, salmon collapse, and eagle displacement. Reprinted from Spencer et al. (1991) © American Institute of Biological Figure 7.5 Sciences. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

157 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 142 control for pasture insects but has ended up dis- component of the vegetation in the vicinity of the Lan- persing one of the worst weeds, New World town of Darwin, but the water buffalo, opening tana camara , throughout the lowlands and even fl ood plains, created perfect germination up the into some native forests (Davis et al. 1993). Also in Mimosa sites of seedlings, and in many areas na- Hawaii, introduced pigs selectively eat and there- tive sedgelands became virtual monocultures of by disperse several invasive introduced plant . The mimosa in turn aided the water M. pigra species, and by rooting and defecating they also buffalo by protecting them from aerial hunters spread populations of several introduced inverte- (Simberloff and Von Holle 1999). brates, while themselves fattening up on intro- Aquatic plants and animals can also facilitate duced, protein-rich European earthworms one another. In North America, the introduced (Stone 1985). fi lters prodigious amounts of zebra mussel Habitat modi fi cation by introduced plants can water, and the resulting increase in water clarity lead to a meltdown process with expanded and/ favors certain plants, including the highly inva- or accelerated impacts. As noted above, the nitro- Myriophyllum spica- sive Eurasian watermilfoil ( Morella faya ( fi retree) from the Azores gen- fi xing ). The milfoil then aids the mussel by tum has invaded nitrogen-de fi cient volcanic regions providing a settling surface and facilitates the of the Hawaiian Islands. Because there are no movement of the mussel to new water bodies native nitrogen- retree is essential- fi xing plants, fi when fragments of the plant are inadvertently ly fertilizing large areas. Many introduced plants transported on boat propellers or in water (Sim- established elsewhere in Hawaii had been unable berloff and Von Holle 1999). cient to colonize these previously nutrient-de fi Some instances of invasional meltdown arise areas, but their invasion is now facilitated by the when one introduced species is later reunited fi retree (Vitousek 1986). In addition, activities of with a coevolved species through the subsequent fi retree fosters increased populations of intro- introduction of the latter. The fi g species and their duced earthworms, and the worms increase the fi pollinating g wasps in Florida are an example; fi rate of nitrogen burial from retree litter, thus the coevolved mutualism between the wasps and enhancing the effect of fi retree on the nitrogen fi g invasion. fi the gs is critical to the impact of the cycle (Aplet 1990). Finally, introduced pigs and However, meltdown need not be between coe- an introduced songbird (the Japanese white-eye, volved species. The water buffalo from Asia and ) disperse the seeds of the fi Zosterops japonicus re- from Central America could not Mimosa pigra tree (Stone and Taylor 1984, Woodward et al. have coevolved, nor could the Asian myna and 1990). In short, all these introduced species create in Hawaii. Lantana camara the New World a complex juggernaut of species whose joint interactions are leading to the replacement of 7.1.10 Multiple effects native vegetation. Large, congregating ungulates can interact Many introduced species have multiple direct with introduced plants, pathogens, and even and indirect effects on native species, harming other animals in dramatic cases of invasional some and favoring others at the same time. For meltdown. For instance, Eurasian hooved live- Neogobius melanosto- example, the round goby ( mus sh that arrived in ballast fi ), an Old World stock devastated native tussock grasses in North water, is widely recognized in the North Ameri- American prairie regions but favored Eurasian can Great Lakes as a harmful invader, feeding on turfgrasses that had coevolved with such animals and that now dominate large areas (Crosby 1986). native invertebrates and eggs and larvae of sev- In northeastern Australia, the Asian water buffalo fi shes. It also competes for food and eral native ), introduced as a beast of burden Bubalus bubalis ( space with other native fi sh species. However, the and for meat, damaged native plant communities round goby also feeds on the harmful zebra mus- and eroded stream banks. The Central American Dreissena bugen- sel and related quagga mussel ( sis ), although the impact on their populations is Mimosa pigra had been an innocuous minor shrub © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

158 1 INVASIVE SPECIES 143 not known. It also now is by far the main food has yet to be explained. In other instances, a source for the threatened endemic Lake Erie change in the physical or biotic environment can Nerodia sipedon insularum ), constitut- water snake ( account for a sudden explosion of a formerly ing over 92% of all prey consumed. Further, restricted introduced species. The spread of Bra- snakes that feed on the goby grow faster and zilian pepper in Florida after a century of harm- achieve large size, which may well decrease pre- less presence was caused by hydrological dation on the snake and increase population size draining farmland, various — changes ood con- fl (King et al. 2006). On balance, almost all observers trol projects, and lowering of the water table for would rather not have the round goby in this agricultural and human use. As described earlier, region, but it is well to bear in mind the complex- gs in south the sudden invasion by long-present fi ity of its impacts. Florida was spurred by the arrival of pollinating fi g wasps. In some instances, demography of a species dictates that it cannot build up population sizes rapidly even if the environment is suitable; 7.2 Lag times trees, for example, have long life cycles and many Introduced species may be innocuous in their do not begin reproducing for a decade or more. new homes for decades or even centuries before As genetic analysis has recently rapidly ex- abruptly increasing in numbers and range to gen- panded with the advent of various molecular erate major impacts. The case of the hybrid cord- tools, it appears that some, and perhaps many, grass , discussed above, is an Spartina anglica sudden expansions after a lag phase occur be- excellent example. The introduced progenitor, cause of the introduction of new genotypes to a S. alterni North American fl ora , had been present previously established but restricted population. in Great Britain at least since the early nineteenth The brown anole population in Florida was aug- century and had even hybridized with the native mented in the twentieth century by the arrival of S. maritima occasionally, but the hybrids were all individuals from different parts of the native sterile until one underwent a chromosomal mu- range, so that the population in Florida now has tation ca. 1891, producing a highly invasive weed far more genetic diversity than is found in any (Thompson 1991). Brazilian pepper ( Schinus tere- native population. It is possible that the rapid binthifolius ) had been present in Florida since the range expansion of this introduction results mid-nineteenth century as isolated individual from introductions to new sites combined with trees, but it became invasive only when it began the advent of new genotypes better adapted to to spread rapidly ca. 1940 (Ewel 1986). Giant reed the array of environmental conditions found in ) was Arundo donax ( rst introduced from the fi et al. Florida (Kolbe 2004). The northward range Mediterranean region to southern California in expansion of European green crab ( Carcinus mae- the early nineteenth century as a roo fi ng material ) along the Atlantic coast of North America nas and for erosion control, and it remained restricted was produced by the introduction of new, cold- in range and unproblematic until the mid-twenti- tolerant genotypes into the established popula- eth century, when it spread widely, becoming a tion (Roman 2006). fi re hazard, damaging wetlands, and changing An improved understanding of lag times is im- entire ecosystems (Dudley 2000). The Caribbean portant in understanding how best to manage ) Anolis sagrei rst appeared brown anole lizard ( fi biological invasions (Boggs 2006). It is not et al. in Florida in the nineteenth century, but it was feasible to attempt active management (see next restricted to extreme south Florida until the section) of all introduced species — there are sim- 1940s, when its range began an expansion that ply too many. Typically in each site we focus on accelerated in the 1970s, ultimately to cover most those that are already invasive or that we suspect 2004). of Florida (Kolbe et al. will become invasive from observations else- Many such invasion lags remain mysterious. where. However, if some currently innocuous es- For instance, the delay for giant reed in California tablished introduced species are simply biological © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

159 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 144 time bombs waiting to explode when the right For such lists to be effective, the risk analyses conditions prevail in the future, the existing ap- - fi have to be accurate enough, and the lists suf ce. proach clearly will not suf fi ciently large, that the great majority of species that would become invasive are actually identi- fi ed as such and placed on black lists or kept off white lists. There are grave concerns that neither 7.3 What to do about invasive species criterion is met. For instance, the black list of the Lacey Act is very short, and many animal species By far the best thing to do about invasive intro- that have a high probability of becoming invasive rst fi duced species is to keep them out in the if introduced are not on the list. The risk assess- place. If we fail to keep them out and they estab- ment tools, on the other hand, all yield some lish populations, the next possibility is to attempt percentage of false negatives — that is, species as- to fi nd them quickly and perhaps to eradicate sessed as unlikely to cause harm, therefore eligi- them. If they have already established and ble for a white list, when in fact they will become begun to spread widely, we may still try to eradi- harmful. Much active research (e.g. Kolar and cate them, or we can instead try to keep their Lodge 2002) is aimed at improving the accuracy populations at suf ciently low levels that they fi of risk analyses especially lowering the rate of — do not become problems. fl false negatives while not in ating the rate of false positives (species judged likely to become inva- sive when, in fact, they would not). 7.3.1 Keeping them out rst fi For inadvertent introductions, one must Introductions can be either planned (deliberate) identify pathways by which they occur (Ruiz or inadvertent, and preventing these two classes and Carlton 2003). For instance, many marine involves somewhat different procedures. In each organisms are inadvertently carried in ballast instance, prevention involves laws, risk analyses, water (this is probably how the zebra mussel and border control. For planned introductions, entered North America). Insects stow away on such as of ornamental plants or new sport sh fi ornamental plants or agricultural products. The or game species, the law would be either a white “ Anoplophora glabripen- Asian longhorned beetle ( black list, list, ” a or some combination of the ” “ ), a dangerous forest pest, hitchhiked to North nis two. A white list is a list of species approved for America in untreated wooden packing material introduction, presumably after some risk analysis from Asia, while snails have been transported in which consideration is given to the features of worldwide on paving stones and ceramics. The the species intended for introduction and the out- Aedes albopictus Asian tiger mosquito ( ) arrived in come in other regions where it has been intro- the United States in water transported in used duced. The most widely used risk analyses ed, fi tires. Once these pathways have been identi currently include versions of the Australian their use as conduits of introduction must be Weed Risk Assessment, which consists of a series restricted. For ballast water, for example, water of questions about species proposed for introduc- picked up as ballast in a port can be exchanged tion and an algorithm for combining the answers with water from the open ocean to lower the to those questions to give a score, for which there number of potential invaders being transported. is a threshold above which a species cannot be For insects and pathogens carried in wood, heat et al. admitted (Pheloung 1999). A black list is a and chemical treatment may be effective. For ag- list of species that cannot be admitted under any ricultural products, refrigeration, and/or fumiga- circumstances, and for which no further risk anal- tion are often used. The general problem is that ysis is needed. Examples of black lists include the each of these procedures entails a cost, and there United States Federal Noxious Weed list and a has historically been opposition to imposing such short list of animals forbidden for entry to the US costs on the grounds that they interfere with free under the Lacey Act. trade and make goods more expensive. Thus it © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

160 1 INVASIVE SPECIES 145 remains an uphill battle to devise and to imple- ular media and on the web, but they can yield ciently stringent that they fi ment regulations suf ts. For instance, the invasion of fi enormous bene constrict these pathways. the Asian longhorned beetle to the Chicago re- Whatever the regulations in place for both de- gion was discovered by a citizen gathering re- fi liberate and unplanned introductions, inspec- wood who recognized the beetle from news tions at ports of entry are where they come into reports and checked his identi fi cation on a state play, and here a variety of detection technologies agency website. This early warning and a quick, are available and improvements are expected. aggressive response by authorities led to success- Trained sniffer dogs are commonplace in ports ful regional extirpation of this insect after a ve- fi in many countries, and various sorts of machinery, year campaign. Similarly, the invasion in Califor- including increasingly accurate X-ray equipment, nia of the alga was discovered Caulerpa taxifolia are widely in use (Baskin 2002). Although technol- probably within a year of its occurrence by a ogies have improved to aid a port inspector to diver who had seen publicity about the impact identify a potential invader once it has been of this species in the Mediterranean. This discov- detected, in many nations these are not employed ery led to successful eradication after a four-year ed staff. fi because of expense or dearth of quali effort, and citizens have been alerted to watch for Also, improved detection and identi cation cap- fi this and other non-native algal species in both abilities are only half of the solution to barring the Mediterranean nations and California. introduction of new species either deliberately or Many introduced species have been successful- by accident (as for example, in dirt on shoes, or in ly eradicated, usually when they are found early untreated food). The other half consists of penalties but occasionally when they have already estab- suf fi ciently severe that people fear the conse- lished widespread populations. The keys to suc- quences if they are caught introducing species. cessful eradication have been as follows; Many nations nowadays have extensive publicity (i) Suf fi cient resources must be available to see at ports of entry, on planes and ships, and some- the project through to completion; the expense of times even in popular media, that combine educa- nding and removing the last few individuals fi tional material about the many harmful activities may exceed that of quickly ridding a site of the of invasive species and warnings about penalties majority of the population; (ii) Clear lines of au- for importing them. thority must exist so that an individual or agency can compel cooperation. Eradication is, by its nature, an all-or-none operation that can be sub- 7.3.2 Monitoring and eradication verted if a few individuals decide not to cooper- ate (for instance, by forbidding access to private The key to eradicating an introduced species be- property, or forbidding the use of a pesticide or fore it can spread widely is an early warning- herbicide); (iii) The biology of the target organism rapid response system, and early warning re- quires an ongoing monitoring program. Because must be studied well enough that a weak point in of the great expense of trained staff, few if any ed; and (iv) Should the fi its life cycle is identi nations adequately monitor consistently for all eradication succeed, there must be a reasonable prospect that reinvasion will not occur fairly sorts of invasions, although for speci c habitats fi quickly. fi (e.g. waters in ports) or speci c groups of species In cases where these criteria have been met, (e.g. fruit fl y pests of agriculture) intensive ongo- successful eradications are numerous. Many are ing monitoring exists in some areas. Probably the on islands, because they are often small and most cost-effective way to improve monitoring is to enlist the citizenry to be on the lookout for because reinvasion is less likely, at least for unusual plants or animals and to know what isolated islands. Rats have been eradicated agency to contact should they see something from many islands worldwide; the largest to 2 . Recently, large, longstanding date is 113 km (see Figure 7.6 and Plate 8). Such efforts entail populations of feral goats and pigs have been public education and wide dissemination in pop- © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

161 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 146 of Natural Resources. s aquatic invasive species. Poster courtesy of the Maryland Department ’ Maryland Figure 7.6 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

162 1 147 INVASIVE SPECIES 2 eradicated from Santiago Island (585 km )inthe effectively controlled by mechanical means Galapagos (Cruz et al. 2005). The giant African fi so long as suf — cutting and pulling roots — alone - snail has been successfully eradicated from sites cient labor is available (Matthews and Brand 2004a). in both Queensland and Florida (Simberloff Sometimes chemical control alone can keep a pest at 2003). Even plants with soil seed banks have low numbers. The Indian house crow ( Corvus splen- Cenchrus echi- been eradicated, such as sand bur ( ), is an aggressive pest in Africa, attacking na- dens natus ) from 400 ha Laysan Island (Flint and Re- tive birds, competing with them for food, preying hkemper 2002). When agriculture or public on local wildlife, stripping fruit trees, and even dive- health are issues, extensive and expensive eradi- bombing people and sometimes stealing food from cation campaigns have been undertaken and young children. It can be controlled by a poison, haveoftenbeensuccessful,crownedbytheglob- Starlicide, so long as the public does not object al eradication of smallpox. The African mosquito (Matthews and Brand 2004a). Many invasive plants ), vector of malaria, was era- ( Anopheles gambiae have been kept at acceptable levels by herbicides. dicated from a large area in northeastern Brazil For instance, in Florida, water hyacinth was drasti- (Davis and Garcia 1989), and various species cally reduced and subsequently managed by use of ies have been eradicated from many large fl of the herbicide 2,4-D, combined with some mechani- regions, especially in the tropics (Klassen 2005). cal removal (Schardt 1997). For lantana in South The pasture weed Kochia scoparia was eradicated Africa, a combination of mechanical and chemical from a large area of Western Australia (Randall control keeps populations minimized in some areas 2001), and the witchweed eradication campaign (Matthews and Brand 2004a). A South African pub- in the southeastern United States mentioned lic works program, Working for Water, has had above is nearing success. These successes sug- great success using physical, mechanical, and chem- gest that, if conservation is made a high enough ical methods to clear thousands of hectares of land priority, large-scale eradications purely for con- of introduced plants that use prodigious amounts of servation purposes may be very feasible. spp.) and several Prosopis water, such as mesquite ( A variety of methods have been used in these (Matthews and Brand 2004a). Sim- Acacia species of campaigns: males sterilized by X-rays for fruit- ilarly, in the Canadian province of Alberta, Norway ies, chemicals for fl and for rats, Anopheles gambiae rats have been kept at very low levels for many hunters and dogs for goats. Some campaigns that years by a combination of poisons and hunting by probably would have succeeded were stopped the provincial Alberta Rat Patrol (Bourne 2000). short of their goals not for want of technological However, long-term use of herbicides and pes- means but because of public objections to using ticides often leads to one or more problems. First is chemicals or to killing vertebrates. A notable ex- the evolution of resistance in the target species, so ample is the cessation, because of pressure from that increasing amounts of the chemical have to be animal-rights groups, of the well-planned cam- used even on a controlled population. This has paign to eradicate the gray squirrel before it happened recently with the use of the herbicide spreads in Italy (Bertolino and Genovese 2003). in Florida Hydrilla verticillata used to control Asian 2007), and it is a common phenomenon et al. (Puri in insect pests of agriculture. A second, related 7.3.3 Maintenance management problem is that chemicals are often costly, and they can be prohibitively expensive if used over If eradication is not an option, many available tech- large areas. Whereas the market value of an agri- nologies may limit populations of invasive species cultural product may be perceived as large enough so that damage is minimized. There are three main mechanical or physical control, chemical methods — to warrant such great expense, it may be dif cult fi control, and biological c ontrol. Sometimes these to convince a government agency that it is worth methods can be combined, especially mechanical controlling an introduced species affecting conser- vation values that are not easily quanti fi ed. Final- and chemical control. In South Africa, the invasive ly, chemicals often have non-target impacts, )canbe Australian rooikrans tree ( Acacia cyclops © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

163 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 148 including human health impacts. The decline of Summary raptor populations as DDT residues caused thin eggshells is a famous example (Lundholm 1997). Invasive species cause myriad sorts of conserva- • Many later-generation herbicides and pesticides tion problems, many of which are complicated, have few if any non-target impacts when used some of which are subtle, and some of which are properly, but expense may still be a major issue. not manifested until long after a species is intro- These problems with pesticides have led to duced. great interest in the use of classical biological con- The best way to avoid such problems is to prevent • deliberate introduction of a natural enemy trol — fi introductions in the nd fi rst place or, failing that, to (predator, parasite, or disease) of an introduced them quickly and eradicate them. fi re with pest. This is the philosophy of ghting fi However, many established introduced species • fi re. Although only a minority of well-planned can be managed by a variety of technologies so biological control projects actually end up that their populations remain restricted and their controlling the target pest, those that have suc- impacts are minimized. ceeded are often dramatically effective and con- ferred low-cost control in perpetuity. For instance, massive infestations of water hyacinth in the Sepik River catchment of New Guinea were well con- Suggested reading trolled by introduction of the two South American weevils that had been used for this purpose in . Island Baskin, Y. (2002). A plague of rats and rubbervines Press, Washington, DC. Neochetina eichhorniae N. bruchi and Lake Victoria, Invasion biology Davis, M. A. (2009). . Oxford University (Matthews and Brand 2004b). A recent success on Press, Oxford. the island of St. Helena is the control of a tropical The ecology of invasions by animals and Elton, C. E. (1958). ) that had Orthezia insignis American scale insect ( . Methuen, London (reprinted by University of plants threatened the existence of the endemic gumwood Chicago Press, 2000). tree ( Commidendrum robustum ). A predatory South Lockwood, J. L., Hoopes, M. F., and Marchetti, M. P. (2007). American lady beetle ( )now Hyperaspis pantherina . Blackwell, Malden, Massachusetts. Invasion ecology keeps the scale insect population at low densities Van der Weijden, W., Leewis, R., and Bol, P. (2007). 2001). Even when a biological control et al. (Booth KNNV Publishing, Utrecht, the Biological globalisation. agent successfully controls a target pest at one site, Netherlands. it may fail to do so elsewhere. The same two wee- vils that control water hyacinth in New Guinea and Lake Victoria had minimal effects on the hya- Relevant websites cinth in Florida, even though they did manage to establish populations (Schardt 1997). World Conservation Union Invasive Species Specialist • However, in addition to the fact that most Group: http://www.issg.org/index.html. biological control projects have not panned out, • National Invasive Species Council of the United States: ol agents have attacked several biological contr http://www.invasivespecies.gov. non-target species and even caused extinctions — • National Agriculture Library of the United States: the cases involving the cactus moth, rosy wolf snail, http://www.invasivespeciesinfo.gov. small Indian mongoose, mosquito sh, and thistle- fi aliens.org. European Commission: http://www.europe • ‐ eating weevil have been mentioned earlier. In gen- eral, problems of this sort have been associated with introduced biological control agents such as generalized predators that are not specialized to REFERENCES fi c target host. However, even species use the speci that are restricted to a single genus of host, such as Allen, J. A. (1998). Mangroves as alien species: the case of 7 , – 71. Global Ecology and Biogeography Letters Hawaii. ,61 thecactusmoth,cancreateproblems. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

164 1 149 INVASIVE SPECIES et al. (2008). Novel Callaway, R. M., Cipollini, D., Barto, K., Aplet, G. H. (1990). Alteration of earthworm community weapons: invasive plant suppresses fungal mutualisms in Hawaii. Oecologia , , Myrica faya 82 biomass by the alien , in America but not in its native Europe. 89 , Ecology 416. 411 – 1055. – 1043 Ashton, P. A. and Abbott, R. J. (1992). Multiple origins and Caltagirone L. E. and Doutt, R. L. (1989). The history of the genetic diversity in the newly arisen allopolyploid Vedalia beetle importation to California and its impact on , Heredity species, Senecio cambrensis Rosser (Compositae). Annual Review of the development of biological control. 32. 68 ,25 – Entomology 34 16. – ,1 , Atkinson I. A. E. (1985). The spread of commensal species Center, T. D., Frank, J. H., and Dray, F. A. Jr. (1997). to oceanic islands and their effects on island Rattus of Biological control. In D. Simberloff, D. C. Schmitz, and , Conservation of island birds avifaunas. 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165 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 150 Klassen, W. (2005). Area-wide integrated pest manage- s wildlands , pp. 53 ’ – California 58. University of California ment and the sterile insect technique. In V. A. Dyck, Press, Berkeley, California. J. Hendrichs and A. S. Robinson, eds Sterile insect tech- (2008). et al. Phy- Durán, A., Gryzenhout, M., Slippers, B., nique. Principles and practice in area-wide integrated sp. nov. associated with a serious nee- tophthora pinifolia , pp. 39 – 68. Springer, Dordrecht, the pest management in Chile. Pinus radiata dle disease of , 57 , Plant Pathology Netherlands. – 715 727. Kolar, C. S. and Lodge, D. M. (2002). Ecological predictions Ellison, A. M., Bank, M. S., Clinton, B. D., et al. (2005). Loss and risk assessment for alien fi shes in North America. of foundation species: consequences for the structure 1236. 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166 1 INVASIVE SPECIES 151 Finding Sauer, J. S., Cole, R. A., and Nissen, J. M. (2007). Of fi ce of Technology Assessment (US Congress). (1993). the exotic faucet snail (Bithynia tentaculata): Investigation Harmful non-indigenous species in the United States . OTA- of waterbird die-offs on the upper Mississippi River ce, Washington, DC. F-565. US Government Printing Of fi . US Geological Survey National Wildlife and Fish Refuge Opler, P. A. (1978). Insects of American chestnut: possible – 1065, US Geological Survey, Wa- Open-File Report 2007 importance and conservation concern. In J. McDonald, shington, DC. 85. West , pp. 83 The American chestnut symposium ed. – Schardt, J. D. (1997). Maintenance control. In D. Simberloff, Virginia University Press, Morgantown, West Virginia. D. C. Schmitz, and T. C. Brown, eds Strangers in paradise. Petren, K. and Case, T. J. (1996). 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Cock, eds Invasive alien species: A Proceedings of the Hawaii Volcanoes National Park al Park. , p. 174. toolkit of best prevention and management practices – Science Conference , 5 117. , 106 CAB International, Wallingford, UK. Thompson, H. V. and King, C. M., eds (1994). The European fl y. Ratcliffe, D. (1979). The end of the large blue butter rabbit. The history and ecology of a successful colonizer . New Oxford University Press, Oxford. Scientist 458. – , 457 8 , Thompson, J. D. (1991). The biology of an invasive plant: Rhymer, J. and Simberloff, D. (1996). Extinction by hybri- so successful? What makes , 41 , BioScience Spartina anglica Annual Review of Ecology and dization and introgression 401. – 393 Systematics , 27 – 109. ,83 fi Tschinkel, W. R. (2006). . Harvard University The re ants Ricciardi, A., Neves, R. J., and Rasmussen, J. B. (1998). Press, Cambridge, Massachusetts. Impending extinctions of North American freshwater US Department of the Interior (Fish and Wildlife Service). Dreis- mussels (Unionoida) following the zebra mussel ( (1997). Endangered and threatened wildlife and plants; , 67 ) invasion. sena polymorpha , Journal of Animal Ecology Determination of Endangered status for two tidal marsh – 619. 613 Cirsium hydrophilum plants — var. hydrophilum (Suisun Roman, J. (2006). Diluting the founder effect: cryptic inva- (Soft Bird mollis Thistle) and ssp. Cordylanthus mollis s- ’ sions expand a marine invader ’ s range. Proceedings of the Beak) from the San Francisco Bay area of California. 50 273 , 2453 – 2459. Royal Society of London B , – 61921. Federal Register , 62 , 61916 CFR Part 17. Invasive species. Ruiz, G. M. and Carlton, J. T., eds (2003). Van Den Bosch, R., Schlinger, E. I., Dietrick, E. J., Hall, J. C., . Island Press, Washing- Vectors and management strategies and Puttler, B. (1964). 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167 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 152 CONSERVATION BIOLOGY FOR ALL Woodward, S. A., Vitousek, P. M., Matson, K., Hughes, F., distribution, and phenology of imported parasites of Benvenuto, K., and Matson, P. (1990). Use of the exotic Therioaphis trifolii Ecolo- (Monell) in southern California. ’ i by native and exotic birds in Hawai Myrica faya tree gy 45 – , 621. , 602 Paci Volcanoes National Park. 93. – ,88 44 , c Science fi Vitousek, P. (1986). Biological invasions and ecosystem Woodworth, B. L., Atkinson, C. T., LaPointe, D. A., et al. properties: can species make a difference? In (2005). Host population persistence in the face of intro- H. A. Mooney and J. A. Drake, eds Ecology of biological duced vector-borne disease: Hawaii amakihi and avian – , pp. 163 invasions of North America and Hawaii 176. Proceedings of the National Academy of Sciences of malaria. Springer, New York. , the United States of America 102 1536. – , 1531 Vivrette, N. J. and Muller, C. H. (1977). Mechanism of Zimmermann, H. G., Moran, V. C., and Hoffmann, J. H. Invasion and Dominance of Coastal Grassland by Me- (2001). The renowned cactus moth, Cactoblastis cactorum , sembryanthemum crystallinum Ecological Monographs (Lepidoptera: Pyralidae): Its natural history and threat to 47 318. – , 301 fl oras in Mexico and the United States of native Opuntia Biological invasions Williamson, M. (1996). . Chapman and , 84 , 543 – 551. Florida Entomologist America. Hall, London, UK. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

168 1 CHAPTER 8 Climate change Thomas E. Lovejoy In 1896 Swedish physicist Arrhenius asked a is as – or more – sensitive to climate than any- new and important question, namely why is thing else society is concerned about. the temperature of the Earth so suitable for hu- The current levels of greenhouse gas concentra- mans and other forms of life? From that emerged tion have already led to an overall rise in global the concept of the greenhouse effect, namely that temperature of 0.75 degree Celsius (see Figure the concentrations of various atmospheric gases 8.1). In addition, because there is a lag between ), methane, nitrous [e.g. carbon dioxide (CO attaining a concentration level and the conse- 2 uorocarbons; also called green- fl oxide, chloro quent trapping of heat energy, the planet is slated house gasses] was such that some of the radiant for an additional 0.5 degree (for a total of 1.25 heat received from the sun is trapped, rendering degrees Celsius) even if greenhouse gas concen- the earth a considerably warmer planet than it trations were to cease to increase immediately. otherwise would be. Arrhenius even did a man- This chapter highlights the effects of human- ual calculation of the effect of doubling the pre- ’ induced climate change on Earth s physical environ- . His results are precisely industrial level of CO ments and biodiversity. Possible mitigation options 2 ’ scli- what the supercomputer models of Earth of this predicament are also brie y discussed. fl mate predict. We are well on the way toward concentration, having started at pre- that CO 2 industrial levels of 280 ppm (parts per million). 8.1 Effects on the physical environment , Current atmospheric levels are 390 ppm of CO 2 Already there are widespread changes in the and are increasing at a rate above the worst case physical environment, primarily involving the scenario of the Intergovernmental Panel for Cli- solid and liquid phases of water. Northern hemi- mate Change (IPCC) (Canadell et al. 2007). sphere lakes are freezing later in the autumn and Modern science is able to study past climate, so the ice is breaking up earlier in the spring. Gla- we now know that the last 10 000 years were a ciers are in retreat in most parts of the world, and period of unusual stability in the global climate. those on high peaks in the tropics like Mount This probably has been extremely bene fi cial to Kilimanjaro (Tanzania) are receding at a rate the human species for that period includes all that they will likely cease to exist in 15 years our recorded history as well as the origins of (UNEP 2007). The melt rate of Greenland glaciers agriculture and of human settlements. It is easy is increasing and the seismic activity they gener- to conclude that the entire human enterprise is ate is accelerating. based on a freak stretch of relatively unchanging Arctic sea ice is retreating at unprecedented climatic conditions. rates, as would be predicted by the increased A bit less obvious is the realization that ecosys- heat absorption capacity of dark open water as tems have adjusted to that stable climate also so compared to re fl ective ice. This represents a posi- fi ts society receives in they – as well as the bene tive feedback, namely the more dark water re- – ecosystem goods and services (see Chapter 3) ecting ice the more places what had been re fl are vulnerable to climate change as well. Indeed, heat is absorbed and the more the Earth warms. it is rapidly becoming clear that the natural world 153 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

169 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 154 CONSERVATION BIOLOGY FOR ALL 0.6 Annual mean 5-year mean 0.4 0.2 0.0 –0.2 Global land–ocean temperature anomaly (ºC) –0.4 1880 2000 1900 1940 1920 1980 1960 Year (2006) © National Academy et al. 80. Reprinted from Hansen – Global annual mean temperature anomaly relative to 1951 Figure 8.1 of Sciences, USA. The danger of positive feedbacks is that they Other possible examples of system change “ accelerate climate change and can lead to a run- would be methane release from thawing perma- away greenhouse effect ” . The fi rst summer with another dangerous positive – frost in the tundra an ice free Arctic Ocean once predicted for 2100 is rst signs of this have been fi feedback loop. The now possible in 2030, with some predictions sug- observed in Siberia and Alaska. These are all ve years. fi gesting as soon as in next part of how the Earth system functions. Although fi cant In addition, there is a statistically signi understanding of the Earth system is only prelim- increase in wild fi res in the American West be- inary it clearly includes thresholds and telecon- cause longer summers and earlier melt of the nections (changes in one part of the globe can snow pack have led to dryer environments and trigger changes in some far distant part). Increas- 2000). et al. higher fi re vulnerability (Flannigan ing climate change is taking the planet in that Argentina, the American southwest, and Austra- dangerous direction. lia in 2009 were experiencing unusual drought, Oceans are also threatened by acidi fi cation levels in the atmosphere. and parts of southern Australia had extraordi- caused by elevated CO 2 is absorbed by the fi cant part of that CO Asigni narily high temperatures and devastating fi res 2 oceans but some of it becomes carbonic acid. As a – in the summer of 2008 2009. In addition there is consequence the acidity of the oceans has increased the possible increase in the number of intense a number – 0.1 pH unit since pre-industrial times tropical cyclones like Katrina, although there is that sounds trivial but being on a logarithmic scale still some uncertainty on the matter. Another ad- is equivalent to 30% more acid. ditional system change was previewed in 2005 All these changes to the physical environment when Atlantic circulation changes triggered the have consequences for biodiversity. greatest drought in recorded history in the Ama- zon. The Hadley Center global climate model and other work predict similar but relatively perma- 8.2 Effects on biodiversity nent change at 2.5 degrees Centigrade with con- sequent Amazon dieback (mostly in the eastern Populations, species and ecosystems are respond- 2009). half of the basin) (Malhi et al. ing to these physical changes all over the planet. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

170 1 CLIMATE CHANGE 155 Many species are changing the timing of their life Temperature increase also will be greater in et al. 2003; Parmesan histories (phenology) (Root high latitudes and particularly in the northern 2006). Wherever there are good records in the hemisphere where there is more terrestrial sur- northern hemisphere many plant species are face. Climate change of course is not only about owering earlier in the spring as in central Eng- fl temperature it is also about precipitation. On land land (Miller-rushing and Primack 2008). Similar- the two most important physical parameters for ly, animal species are changing the timing in their organisms are temperature and precipitation. In life cycles, such as tree swallows ( Tachycineta bi- aquatic ecosystems the two most important are color ) nesting and laying their eggs earlier (Dunn temperature and pH. Drying trends are already and Winkler 1999). Some species are changing affecting Australia, the Argentine pampas, the their migration times and in North America, one American southwest and the prairie pothole hummingbird species has ceased to migrate (Par- region of the upper Midwest northward into mesan 2006). Canada. Prairie potholes are a critical landscape In addition, the geographical distribution of fl feature supporting the great central yway of some species is changing. In western North migratory birds in North America. America, the change both northward and up- For well known species such as the sugar s checkerspot butter ward in altitude of Edith ’ fl y maple ( Acer saccharum ), the environmental re- ) is well documented (Parme- ( Euphydryas editha quirements are fairly well known so it is possible san 2006). In Europe, many butter y species have fl to model how the geography of those require- moved northward as well, including the sooty ments is likely to change along with climate. In Heodes tityrus copper ( ), which now occurs and this case all the major climate models show that breeds in Estonia (Parmesan 1999). et al. at double pre-industrial levels of greenhouse There is considerable change among Arctic so char- – gases, the distribution of this species species because so many life histories are tied to acteristic of the northeastern United States that the ice which decreased dramatically both in area its contribution to fall foliage is the basis of a and thickness in 2007 and 2008. The polar bear signi will move north to – cant tourism industry fi ( Ursus maritimus ) is the best known by far with Canada. While the tourism and the appeal of stress/decline being observed in a number of the maple sugar and syrup are not signi cant ele- fi et al. 1999). Many bird spe- populations (Stirling ments of the northeast US economy, they are ), a Arctogadus glacialis cies feed on the Arctic cod ( signi fi cantwithrespecttoasenseofplace,and species that occurs near the edge and just under are partly why these states have taken a leader- the ice. Nesting seabirds like the black guillemot ship role on climate change. In the mid-Atlantic ( y from their nests on land to the fl ) Cepphus grylle )will Icterus galbula states, the Baltimore oriole ( edge of the ice to feed and return to feed their no longer occur in Baltimore due to climate- young. So as the distance to the edge of the ice driven range shift. increases, there is a point at which the trip is too In the northern oceans there are changes in rst the individual nest, then eventual- fi great and plankton (small organisms drifting along the ly the seabird colony fails. fi ocean currently) and sh distributions. The eel Species that occur at high altitudes will, as a Zostera marina grass ( ) communities of the great class, be very vulnerable to climate change simply North American estuary, the Chesapeake Bay, because as they move upslope to track their re- have a sensitive upper temperature limit. Accord- quired conditions, they ultimately will have no ingly, the southern boundary has been moving Ochotona further up to go. The American pika ( steadily northward year after year (http://www. ), a lagomorph species with a fascinating princeps chesapeakebay.net/climatechange.aspx). Simi- harvesting aspect to its natural history, is a prime larly, plankton populations have been moving example. It is comprised of roughly a dozen popu- northwards in response to water temperature in- lations in different parts of the Rocky Mountains crease (Dybas 2006). This trend, for example, has that we can anticipate will wink out one by one. resulted in low plankton densities around © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

171 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 156 Scotland, likely reducing the densities of plank- shrinks dramatically such that at 5 degrees Centi- fi ton-eating sh and bird species there (Dybas grade increase most are doomed to extinction 2006). (Shoo 2005). The Monteverde cloud forest et al. Changes have been observed not only in the in Costa Rica, an ecosystem type almost entirely Arctic and temperate regions but also in the tro- dependent on condensation from clouds for pics (see Box 8.1). There are more than 60 verte- moisture has been encountering more frequent s rainforests ’ brate species endemic to Australia dry days as the elevation at which clouds form including the grey-headed robin ( Heteromyias al- has risen. Nest predators like toucans are moving bispecularis ) and the ringtail possum ( Pseudo- up into the cloud forest from the dry tropical cheirus peregrinus ). With climate change the et al. forest below (Pounds 1999). The charismatic amount of suitable habitat available for them ) of Monteverde could Bufo periglenes golden toad ( Box 8.1 Lowland tropical biodiversity under global warming Navjot S. Sodhi and 51% will encounter the spatial gaps Global warming may drive species poleward between their current and projected ranges or towards higher elevations. However, how (Box 8.1 Figure). A number of these species tropical species, particularly those occupying will likely face both challenges. Authors lowlands, will respond to global warming cautioned that their local ‐ level data may remains poorly understood. Because the have underestimated regional elevation latitudinal gradient in temperature levels off ranges and must, in this regard, be to a plateau between the Tropic of Cancer considered as a worst case scenario. and the Tropic of Capricorn, latitudinal range However, it is also plausible that their results fi shifts are not likely for species con ned to represent a best case scenario, considering the tropics. This leaves upslope range shifts re, fi that other drivers such as habitat loss, as the primary escape route for tropical overharvesting and invasive species can species already living near their thermal synergistically drive species to decline and limit. One scenario is that tropical lowland et al. 2008). extinction (Brook biodiversity may decline with global species pool warming, because there is no ” “ to replace lowland species that migrate to 1.0 Biotic attrition (2008) et al. higher elevations. Colwell Range-shift gaps speculated on the effects of projected global Extinction 0.8 warming on lowland biotas by using relatively large datasets of plants and insects 0.6 from Costa Rica. Data on the distribution of 1902 species of epiphytes, understory rubiaceous plants, geometrid moths, and 0.4 ants were collected from a transect that traversed from sea level to 2900 m elevation. 0.2 Proportion of species Colwell et al. (2008) developed a graphic model of elevational range shifts in these 0.0 tes i y h p E p Moths Rubiaceae Ants species under climatic warming. Assuming ‐ 600 m upslope shifts with 3.2°C temperate Proportion of species projected to be affected by Box 8.1 Figure increase over the next century, they global warming. Data for the analysis were collected from a lowland elevational transect in Costa Rica. Proportion sums are greater than estimated that 53% of species will be one because a species may have more than one response. Reprinted lowland biotic attrition candidates for from Colwell et al . (2008). (decline or disappearance in the lowlands) continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

172 1 CLIMATE CHANGE 157 Box 8.1 (Continued) Most previous studies determining the REFERENCES effects of global warming on tropical Brook, B. W., Sodhi, N. S., and Bradshaw, C. J. A. (2008). species have focused on montane species, Synergies among extinction drivers under global reporting their elevation shifts or Trends in Ecology and Evolution change. , 23 , 453 – 460. et al. 1999). disappearances (e.g. Pounds Colwell, R. K., Brehm, G., Cardelús, C. L., Gilman, A. C., Colwell et al. ’ s (2008) fi ndings remind us and Longino, J. T. (2008). Global warming, elevational that lowland tropical biodiversity remains range shifts, and lowland biotic attrition in the wet equally vulnerable to the changing 322 , 261. – , 258 tropics. Science climate. Their study is yet another Pounds, J. A., Fogden, M. P. L., and Campbell, J. H. (1999). reminder that we need to urgently mitigate Biological response to climate change on a tropical the effects of human generated climate – 615. , 611 mountain. Nature , 398 changes. well be the fi rst documented terrestrial extinction years ago and become more frequent every year, caused by climate change (Figure 8.2; Pounds likely due to the elevation of sea temperature et al. 1999). The rapid extinction of large numbers (Hoegh-guldberg 1999). Coral reefs around the of amphibian species in which a chytrid fungus globe are threatened (Pandol fi et al. 2003). It is plays a major role may well be in synergy with hard to envision a reasonable future for tropical 1992; Collins and et al. climate change (Crump coral reefs and the diversity of marine life they Storfer 2003). support. In tropical oceans, coral reefs are quite temper- Species of coastal regions will encounter pro- ature sensitive. Only a slight increase in tempera- blems with sea level rise. Some will succeed in ture causes the basic partnership between a coral adapting and others probably will not. The rate of animal and an alga to break down. The coral cance: generally fi sea level rise will be of signi animal expels the alga triggering what are called speaking the more rapid the rise the more species bleaching events in which most of the color of the fi culty in adapting. Low lying will encounter dif communities is lost and productivity, biodiversi- island species constitute another class highly vul- ty and the ecosystems services of the reefs crash. nerable to climate change, principally because of Such occurrences were virtually unknown 40 sea level rise. Islands of course have major num- bers of endemic species such as the key deer Odocoileus virginianus clavium ( ) in the Florida Keys. Island species have been particularly vul- nerable to extinction because of limited popula- tions. Sea level rise caused by climate change will be the coup de grace for species of low lying islands. To change the basic chemistry of two thirds of the planet, i.e. ocean, is staggering to contemplate in itself. In addition, the implications for the tens of thousands of marine species that build shells and skeletons of calcium carbonate are very grave. They depend on the calcium carbonate equilibrium to mobilize the basic molecules of The golden toad. Photograph from the US Fish and Wildlife Figure 8.2 their shells and skeletons. This includes obvious Service. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

173 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 158 organisms like mollusks and vertebrates but also substantial extinction if they remain in their cur- tiny plankton like pteropods (tiny snails with rent condition. modi ed to fl ap like a wing to main- foot “ their ” fi A second difference is that we know from stud- tain them in the water column). At a certain point ies of past response to climate change that of increasing acidity the shells of such organisms biological communities do not move as a unit, but will go into solution while they are still alive. rather it is the individual species that move each at Effects have been seen already at the base of the its own rate and in its own direction. The conse- food chain in the North Atlantic and off of Alaska. quence is that ecosystems as we know them will Freshwater species will be affected as well. disassemble and the surviving species will assem- They all have characteristic temperature ranges gurations that largely fi ble into new ecosystem con that will be affected by climate change. Cold- defy the ability to foresee. Certainly that was the water species like trout and the many species of case as species moved in Europe after the last re- the food chains on which they depend will no treat of the glaciers (Hewitt and Nichols 2005). The longer be able to survive in many places where management challenge to respond to this is there- they occur today (Allan et al. 2005). fore hard to understand let alone plan to address. These kinds of changes are relatively minor We also know that in contrast to the climate ripples in the living world but are occurring vir- change models run on super computers that tually everywhere. Nature is on the move and change will be neither linear nor gradual. We this no longer is a matter of individual examples know there have been discontinuities in the phys- but is statistically robust. And this is with only ical climate system in the past. For example the 0.75 degrees Celsius increase in global tempera- global conveyor belt – the gigantic ocean current ture with at least that much and probably more in – that distributes heat around the globe has shut store by century ’ s end. The fi rst projection of down in the past. Equally disturbing, abrupt might what double pre-industrial levels of CO threshold change is already occurring in ecosys- 2 portend for the biota estimated extinction of tems. Bleaching in coral reef systems is clearly an 2004) et al. 35% of all species (Thomas – 18 a – example in the oceans (see above). range con fi rmed by the 2007 report of the Intergov- ernmental Panel on Climate Change (IPCC 2007). With more climate change, the impacts upon 8.3 Effects on biotic interactions and response of biological diversity will change Relationships between two species can depend qualitatively and become more complex and on relatively precise timing. Sometimes the harder to manage. Climate change of course is timing mechanism of one is based on day length nothing new in the history of life on Earth. Gla- and the other on temperature and has worked ciers came and went on a major scale in the well because of the relative climate stability. The northern and temperate latitudes in the last seabird nesting-Arctic Cod coupling is just such hundreds of thousands of years. Species were an example and under climate change leads to able to move and track their required climatic ” (see above). The Arctic hare ( Lepus “ decoupling conditions without much loss of biological diver- arcticus ), for example, changes from a white win- sity. The difference today is that the landscapes ter pelage that camou ages it in wintry white fl within which species would move in response to landscapes to a brownish pelage that blends into ed by fi climate change have been highly modi the vegetation after the snow and ice disappear. human activity through deforestation, agricultur- As spring thaw advances earlier with climate al conversion, wetland drainage and the like. change, Arctic hares become vulnerable to preda- Landscapes have been converted into obstacle tors as they are conspicuously white in no longer courses for dispersing organisms. Former Nation- wintry landscapes. al Zoo Director Michael Robinson stated that spe- Similarly, in terrestrial ecosystems threshold Philadelphia will be in the “ cies would move but change is occurring in coniferous forests in . Basically these landscapes will result in ” way © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

174 1 CLIMATE CHANGE 159 North America and Europe as climate change tips warming) should be the limit beyond which it is the balance in favor of native pine bark beetles. dangerous. This means limiting peak concentra- Milder winters allow more to overwinter and tion levels to as low a fi gure as possible and out of the atmosphere longer summers permit an additional generation seeking ways to draw CO 2 to return to a lower ppm as soon as possible. It is of beetles. The consequence is vast stretches of clear that the grave risk and urgency of climate forest in which 70% of the trees have been killed. change has not been recognized (Sterman 2008; fi re It is an enormous forest management and Solomon 2009). The IPCC (2007) synthesis et al. management problem, and being without itself is danger- report suggests 450 ppm of CO known precedent it is not clear how these ecosys- 2 ous. Remember, the earth is 0.75 degree warmer tems will respond. Yet more, there are the fi rst than pre-industrial times with another 0.5 already signs of system change, i.e., change on yet a in the pipeline. Yet at 0.75 ecosystem threshold greater scale. change is already occurring. The last time the Earth was two degrees Centi- grade warmer, sea level was four to six meters 8.4 Synergies with other biodiversity higher. The current changes in Arctic sea ice, the change drivers accelerating melting of the Greenland ice sheet, Climate change will also have synergistic effects together with major ecosystem disruption all sug- with other kinds of environmental problems such is the level above which gest that 350 ppm of CO 2 as invasive species (Chapter 7). The emerald ash ” . That is James Hansen ’ s conclusion it is not “ safe ), an Asian species, is Agrilus planipennis borer ( as a climate scientist. The insights emerging about causing major mortality of American ash trees biological diversity and ecosystems are conver- Fraxinus americana ) – ( from which baseball bats is at 390 gent with 350 ppm. Yet atmospheric CO 2 are manufactured – from the mid-west to Mid- ppm and climbing at rates beyond the worst case Atlantic States (http://www.emeraldashborer. projections. info/). The borer is over wintering in greater adaptation “ This means the agenda for ”– to numbers because of milder winters and has a s terminology ’ use the climate convention – is in- longer active boring season because of longer deed urgent. Conservation strategies need revi- summers. Another example will be the impact cation and the conservation sion and ampli fi of the introduced bird malaria vector mosquito biology of adaptation is a rapidly developing which causes mortality in most species of the eld. Restoring natural connections in the envi- fi endemic Hawaiian honeycreepers (see Figure ronment will facilitate the movement of organ- 12.4). Of the surviving honeycreeper species isms as they respond to changing climate (Box most of the vulnerable ones persist only above 8.2). Reducing other stresses on ecosystems re- the mosquito line – an altitude above which the – duces the probability of negative synergies with temperature is too low for the mosquitoes. With climate change. Downscaled climate projections climate change the mosquito line will move up to one square kilometer, for example, or similar and the area safe for honeycreepers diminishes will provide managers with useful data for (Pratt 2005). making needed decisions. While existing protected areas will no longer be lling their original purpose, e.g., Joshua trees fi ful 8.5 Mitigation ( Yucca brevifolia ) will no longer exist inside of the Joshua Tree National Park, they will have the All of this bears on probably the most critical environmental question of all time, namely at new value of being the safe havens from which , i.e., what point is climate change ” dangerous “ species can move and create the new biogeo- where should it be limited. For a long time con- graphic pattern. That together with the need for new protected areas for the new locations of im- servationists asserted that 450 ppm of CO 2 portant biodiversity plus the need for natural (roughly equivalent to 2 degrees Centigrade © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

175 . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 160 Box 8.2 Derivative threats to biodiversity from climate change Paul R. Ehrlich planet. Large areas of desert may be claimed Besides the obvious direct impacts on energy capturing devices. Wind by solar ‐ biodiversity, climate disruption will have many turbines are likely to dot landscapes and other effects. For instance, if climatologists are speed ‐ ‐ some near shore seascapes. New high correct, humanity is likely to be faced with a rail lines may be constructed, natural millennium or more of continuously changing ecosystems may be plowed under to plant patterns of precipitation that likely in itself will crops for conversion to biofuels (Box 13.3). et al. be devastating for biodiversity (Solomon This is already happening with deforestation 2009). But those changes will also require in the Amazon now accelerating in response humanity to continually reconstruct water ‐ to demand for biofuel crops. Expanding handling and food ‐ producing infrastructure farming operations are also destroying the around the globe. New dams, canals, and prairie pothole ecosystem of the northern pipelines will need to be built, often with plains of North America (http://www.abcbirds. devastating impacts on stream and river org/newsandreports/stories/080226_biofuels. ecosystems. Lakes behind new dams will ood fl html). That is critical habitat for many bird fl ows terrestrial habitats, and changing river populations, among other fauna, including will have impacts on estuaries and coral reefs, ducks much in demand by duck hunters who among the most productive of marine have in the past proven to be allies of environments. Reefs are especially sensitive to conservationists. the siltation that often accompanies major All of these changes will cause multitudes of upstream construction projects. populations, and likely many species, to fl ows means that new areas Changing water disappear, so that conservation biologists will be cleared for crop agriculture and should be consulted on each project, and subjected to grazing, as old areas become society should be made very aware as soon as unproductive. Roads and pipelines will icts between fl possible of the potential con doubtless need to be built to service new human and natural capital inherent in revision agricultural areas. What the net effects of of water, energy, and transport infrastructure. these shifts will mean is almost impossible to estimate, especially where old areas may be available for rewilding (Box 5.3). It is also likely that warming will open much of the Arctic to REFERENCES commerce, with an accompanying increase in ports, – the construction of infrastructure K., Knuttic R., and Friedlingsteind, ‐ Solomon, S., Plattner, G roads, towns, and so on. P. (2009). Irreversible climate change due to carbon Human society in response to growing Proceedings of the National Academy dioxide emissions. climatic problems will also begin to revise of Sciences of the United States of America , 106 , mobilizing infrastructure across the ‐ energy 1704 – 1709. connections between natural areas, clearly mean mitigation, but biology and conservation play a that more conservation is needed not less. cant role as well (Box 8.2). fi signi agenda ” mitigation “ to – Simultaneously, the Tropical deforestation (see Chapter 4) plays an use the convention ’ s term for limiting the growth important role in greenhouse gas emissions: liter- of greenhouse gas concentrations in the atmo- ally 20% of annual emissions come from the de- becomes a matter of huge global urgency sphere – struction of biomass, principally tropical because the greater the climate change the more deforestation and burning (IPCC 2007). In the dif fi cult is adaptation. Transforming the energy current rank order of emitting nations after base for human society is the dominant center of China and the United States are Indonesia and © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

176 1 CLIMATE CHANGE 161 Brazil because of their deforestation. There is now the planet more habitable for humans and all gathering effort to include Reductions in Emis- “ forms of life. sions from Deforestation and Degradation ” ¼ REDD) as part of the negotiations. Obviously ( ts in doing so in reduc- fi there are multiple bene Summary tion of emissions (and thus atmospheric concen- Massive releases of greenhouse gasses by hu- · fi tration levels), biodiversity bene ts and mans have altered the climate. ecosystem services (Chapter 3). There are techni- Rapid global warming is responsible for abiotic · cal problems in monitoring and measuring as changes such as receding of glaciers and increase in ”– leakage “ well as issues about when protection fi wild res. ects the deforestation to of one forest simply de fl Increased CO concentrations in the atmosphere 2 · – another but none of it seems intractable. fi have acidi ed the oceans. All greenhouse gas emissions involve the re- Populations, species, and ecosystems are re- · lease of solar energy trapped by photosynthesis sponding to these climatic conditions. whether ancient (fossil fuels) or present defores- Urgent actions are needed to reverse the climatic · tation and other ecosystem degradation. That changes. raises the important question of what role biology and biodiversity might play in removing some of accumulated in the atmosphere. Twice in the CO 2 Suggested reading the history of life on earth high levels of CO 2 concentrations had been reduced to levels on the Climate change Lovejoy, T. E. and Hannah, L., eds (2005). . Yale University Press, New Haven, CT. and biodiversity order of pre-industrial. The fi rst was associated with the origin of land plants and the second with the expansion of angiosperms (Beerling 2007). This suggests substantial potential if the bio- Relevant websites sphere is managed properly. Intergovernmental Panel on Climate Change: http:// • In the past three centuries, terrestrial ecosystems www.ipcc.ch/. have lost 200 billion tons of carbon and perhaps Nature reports on climate change: http://www.nature. • more depending on hard to estimate losses of soil com/climate/index.html. carbon. What is clear is that to the extent that United States Environmental Protection Agency: • terrestrial ecosystems can be restored, a substantial http://www.epa.gov/climatechange/. amount of carbon could be withdrawn from the atmosphere rather than lingering for a hundred to a thousand years. If that number is 160 billion tons REFERENCES of carbon, it probably equates to reducing atmo- spheric concentrations of it by 40 ppm. Allan, J. D., Palmer, M. E., and Poff, N. L. (2005). Climate change and freshwater ecosystem. In T. E. Lovejoy and This would be tantamount to planetary engi- L. Hannah, eds Climate change and biodiversity , pp. 274 – essentially a regreen- neering with ecosystems – 290. Yale University Press, New Haven, CT. ing of what Beerling (2007) terms the Emerald ’ The emerald planet: how plant s changed Beerling, D. (2007). Planet. All other planetary or geo-engineering . Oxford University Press, Oxford, UK. Earth ’ s history schemes have potential negative consequences, (2007). et al. Canadell, J. G., Quéré, C. L., Raupach, M. R., and only deal with temperature to the total ne- Contributions to accelerating atmospheric CO growth 2 glect of ocean acidi cation (Lovelock and Rapley fi ciency from economic activity, carbon intensity, and ef fi 2007; Shepherd et al. 2007). This takes the agenda of natural sinks. Proceedings of the National Academy of beyond forests to all terrestrial ecosystems, , 104 , 18866 – 18870. Sciences of the United States of America grasslands, wetlands, and even agro-ecosys- Collins, J. P. and Storfer, A. (2003). Global amphibian de- tems. Essentially it is conservation on a plane- cline: sorting the hypotheses. Diversity and Distributions , tary scale: managing the living planet to make 98. – ,89 9 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

177 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 162 Parmesan, C. (2006). Ecological and evolutionary Crump, M. L., Hensley, F. R., and Clark, K. L. (1992). responses to recent climate change. Annual Review of Apparent decline of the golden toad: underground or – , 637 , Ecology, Evolution and Systematics 37 669. 420. Copia , 1992 , 413 extinct? – et al. Parmesan, C., Ryrholm, N., Stefanescu, C., (1999). Dunn, P. O. and Winkler, D. W. (1999). Climatic change has y species Poleward shifts in geographic ranges of butter fl affected breeding date of tree swallows throughout – , , 579 associated with regional warming. 399 583. Nature North America. Proceedings of the Royal Society of London Pounds, J. A., Fodgen, M. P. L., and Campbell, J. H. (1999). – 2490. B , 266 , 2487 Biological response to climate change on a tropical Dybas, C. L. (2006). On collision course: ocean plankton – mountain. , 398 , 611 Nature 615. , BioScience and climate change. 56 , 642 – 646. Pratt, D. H. (2005). Hawaiian honeycreepers . Oxford Univer- Flannigan, M. D., Stocks, B. J., and Wotton, B. M. (2000). sity Press, Oxford, UK. res. Climate change and forest The Science of the Total fi Root, T. L, Price, J. T., Hall, K. R., et al. (2003). Fingerprints 262 229. – , 221 , Environment , Nature of global warming on wild animals and plants. Hansen, J., Sato, M., and Ruedy, R. (2006). Global temp- 60. – ,57 421 Proceedings of the National Academy of erature change. Shepherd, J., Iglesias-rodriguez, D., and Yool, A. (2007). – 14293. ,14288 Sciences of the United States of America , 103 Geo-engineering might cause, not cure, problems. Na- Hewitt, G. M. and Nichols, R. A. (2005). Genetic and evo- , 781. 449 ture , lutionary impacts of climate change. In T. E. Lovejoy Shoo, L. P., Williams, S. E., and Hero, J.-M. (2005). Climate , and L. Hannah, eds Climate change and biodiversity warming and the rainforest birds of the Australian wet pp. 176 – 192. Yale University Press, New Haven, CT. tropics: using abundance data as a sensitivity predictor Hoegh-Guldberg, O. (1999). Climate change, coral bleach- of change in total population. , 125 , Biological Conservation ing and the future of world Marine Freshwa- s coral reefs. ’ 335 – 343. 866. , ter Research – , 839 50 Solomon, S., Plattner, G.-S., Knutti, R., and Friedlingstein, impacts, adaptation and Climate Change 2007 IPCC. (2007). – P. (2009). Irrevesible climate change due to carbon dioxide vulnerability . Cambridge University Press, Cambridge, UK. Proceedings of the National Academy of Sciences of emissions. Lovelock, J. E. and Rapley, C. G. (2007). Ocean pipes could ,1704 1709. – 106 , the United States of America 449 Nature help the Earth to cure itself. , 403. , Sterman, J. D. (2008). Risk communication on climate: Malhi, Y., Aragão, L. E. O. C., Galbraith, D., et al. (2009). , 532 322 , Science mental models and mass balance. 533. – Exploring the likelihood and mechanism of a climate- Stirling, I., Lunn, N. J., and Iacozza, J. (1999). Long-term change-induced dieback of the Amazon rainforest. Pro- population trends in population ecology of polar bears ceedings of the National Academy of Sciences of the United in western Hudson Bay in relation to climate change. States of America , in press. 52 , 294 Arctic 306. – , Miller-Rushing, A. and Primack, R. B. (2008). Global warm- Thomas, C. D., Cameron, A., Green, R. E., et al. (2004). ’ owing times in Thoreau fl ing and s Concord: a commu- Extinction risk from climate change. Nature , – 89 , 332 nity perspective. Ecology 341. , 427 , fi et al. , J. M., Bradbury, R. H., Sala, E., Pandol 148. – 145 (2003). Global United Nations Environment Programme (UNEP). (2007). trajectory of the long-term decline in coral reef ecosys- Global outlook for ice & snow . UNEP, Nairobi, Kenya. , 955 – 958. tems. Science , 301 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

178 1 CHAPTER 9 Fire and biodiversity David M.J.S Bowman and Brett P. Murphy In a famous passage in the concluding chapter of ing tips buried beneath the surface soil (Figure 9.1). The Origin of Species, Darwin (1859, 1964) invites In this chapter we will show that the very same “ contemplate an entangled bank, the reader to evolutionary and ecological principles that Darwin clothed with many plants of many kinds, with espoused in that brilliant passage relate to land- birds singing on the bushes, with various insects scape re is enmeshed in the fi re. This is so because fi fl itting about, and with worms crawling through evolution and ecology of terrestrial life, including ect that these elaborately “ and re fl the damp earth ” our own species. This perspective is deeply chal- constructed forms, so different from each other, lenging to the classical view of the “ Balance of and dependent on each other in so complex a man- Nature that is still held by a broad cross-section ” ner, have all been produced by laws acting around of ecologists, naturalists and conservationists, most ” us. Likewise, let us consider a tropical savanna of who have trained or live in environments where fl ee- ablaze with hovering raptors catching insects fi landscape re is a rare event, and typically cata- ing the re-front, where fi ames sweep past tree fl strophic (Bond and Van Wilgen 1996; Bond and trunks arising from dry crackling grass. Within Archibald 2003). Only in the past decade have weeks the blackened savanna trees are covered in books been published outlining the general princi- green shoots emerging from thick bark, woody fi re ecology (Whelan 1995; Bond and Van ples of juveniles are resprouting from root stocks, and Wilgen 1996) and journals established to commu- herbivores are drawn to grass shooting from grow- fi ndings in nicate the latest re ecology and fi Figure 9.1 fi re that has occurred in the early dry season in Kakadu National Park, northern Australia. Note the A eucalypt savanna recovering from a owering fl palm and the strong resprouting response of juvenile woody plants on the still bare ground surface. Photograph by David Bowman. Livistona 163 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

179 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 164 wild re management (see http://www. fi recology. fi 9.2 Evolution and fi re in geological time net and http://www.iawfonline.org). There is evidence from the fossil record that wild fi res started to occur soon after vegetation established on the land surface (about 420 million re? fi 9.1 What is years ago) (Scott and Glasspool 2006). The long history of exposure of terrestrial life to re leads fi fi At the most basic level re can be considered a to the idea that fi re is an important evolutionary physiochemical process that rapidly releases ener- factor, and more controversially, that re and life fi gy via the oxidation of organic compounds, and have coevolved (Mutch 1970). While gaining “ . ” anti-photosynthesis can be loosely considered as some support from modeling (Bond and Midgley This physiochemical process if often summarized fi cult to prove because adapta- 1995), this is dif made up of the three key “ fi re triangle ” in a classic re cannot be unambiguously identi ed fi fi tions to factors to cause combustion: oxygen, fuel and igni- in the fossil record. For example, in many fi re- tions (Whelan 1995; Pyne 2007). Atmospheric oxy- prone environments, seeds are often contained in that controls window fi re “ ” gen levels create a woody fruits that only open after a re event, a fi activity because ignitions are constrained by atmo- feature known as serotiny. However, woody fruits spheric oxygen (Scott and Glasspool 2006). Fire may also be a defense against seed predators such cannot occur when levels fall below 13% of the as parrots, and seeds are released once mature, atmosphere at sea level, and under the current re (Bowman 2000). In most cases fi irrespective of oxygen levels (21%) fi re activity is limited by fuel it is impossible to know if fossilized woody fruits moisture, yet at 35% even moist fuels will are truly serotinous, thus woody fruit occurrence is burn. Because of substantial fl uctuations in atmo- re. Much fi not clear evidence of an adaptation to cantly fi re risk has changed signi fi spheric oxygen, fi care is required in the attribution of re adapta- through geological time. In the Permian Period tions. For example, microevolution can result in (between 290 and 250 million years ago) for exam- switching from possible fi re-adaptations, such as ple, oxygen levels were substantially higher than at the serotinous state. More problematic for under- present and even moist giant moss (lycopod) for- standing the evolution of ammability, Schwilk fl ests would have been periodically burnt (Scott and and Kerr (2002) have proposed a hypothesis they Glasspool 2006). However, fi re in the biosphere call ” genetic niche-hiking “ ammable traits fl that should not be considered merely a physicochemi- tof fi tness bene fi direct “ may spread without any cal process but rather a fundamental biogeochemi- ammable trait fl the ” . cal process. Fires instantaneously link biomass fl ammability Insights into the evolution of with the atmosphere by releasing heat, gases (nota- have been gained by tracking the emergence of bly water vapor), and the geosphere by releasing re-adapted lineages such as highly fi Eucalyptus. nutrients and making soils more erodible and thus Eucalypts are renowned for their extraordinarily changing the nutrient content of streams and rivers proli fi c vegetative recovery of burnt trunks via (hydrosphere). Fire is therefore quite unlike other epicormic buds (Figure 9.2). Recently, Burrows oods and cyclones, fl natural disturbances, such as (2002) has shown that eucalypt epicormics are given the complex web of interactions and numer- anatomically unique. Unlike other plant lineages, ous short and long-range feedbacks. Some ecolo- which have fully developed dormant buds on the res should be gists have suggested that landscape fi trunks, eucalypts, have strips of “ precursor cells ” “ biologically constructed ” considered as being , that span the cambium layer that, given the right and have drawn parallels with herbivory (Bond cues, develop rapidly into epicormic buds. The and Keeley 2005) or decomposition (Pyne 2007). advantage of this system is that should the trunk Such tight coupling between fi re and life bedevils be severely burnt the tree retains the capacity to simple attribution of cause and effect, and raises develop epicormic buds from cells protected in fascinating questions about the potential coevolu- the cambium. The molecular phylogeny of tion of fi re and life. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

180 1 165 FIRE AND BIODIVERSITY c epicormic sprouts on a recently burnt tall eucalypt forest in eastern Tasmania. Photograph by David Bowman. fi Proli Figure 9.2 eucalypts, dated using the fossil record, suggests Key aspects of the re regime include types of fi that this trait existed before the ” “ bloodwood fuels consumed (e.g. grass vs. canopies), spatial eucalypt clade split off from other eucalypts pattern (area burnt and shape), and consequences some 30 million years ago, given that it occurs (severity relative to impacts on the vegetation in both these lineages. Such an ancient feature to and/or soils) (Gill 1975; Bond and Keeley 2005). the lineage suggests that eucalypts had devel- res are often of low inten- fi For example, savanna fi oped a vegetative response to landscape re, sity and high frequency (often annual), while for- which appears to have become more common in res are often of low frequency (once every est fi the Australian environment associated with a dry few centuries) and very high intensity. Fire regimes climate and nutrient impoverished soils. This in- are part of the habitat template that organizes the terpretation is concordant with the fresh insights geographic distribution of biodiversity, and, in about the evolution of the Australian biota uence the spread of fl turn, species distributions in derived from numerous molecular phylogenies re. Some authors have even applied “ habitat suit- fi of quintessentially Australian plants and animals re is most ” ability modeling fi to predict where (Bowman and Yeates 2006). likely to occur at the global to local level. fl uenced by climate Fire activity is strongly in rs have developed empiri- variability. Fire manage cal relationships that combine climate data, such as 9.3 Pyrogeography cit, wind fi the intensity of antecedent moisture de Satellite sensors have revolutionized our under- speed, relative humidity, and air temperature, to re activity from landscape to global standing of fi calculate fi re danger (see http://www. fi renorth. scales. Global compilations of satellite data have org.au). Mathematical models combining such cli- re on fi demonstrated the occurrence of landscape mate data with fuel loads and topography have every vegetated continent, yet the incidence of re may behave fi been developed to predict how a fi re is not random across the globe (Justice et al. as it spreads across a landscape (Cary et al. 2006). 2003). Fire has predictable features regarding The spread of fi re is also strongly in fl uenced by how it spreads across landscapes and the fre- vegetation type (Figure 9.3). For example, grassy quency and season of occurrence. Such predict- environments carry fi re frequently because of the re regime ” ability has lead to the idea of the “ . fi rapid accumulation of fuel while rainforests burn © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

181 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 166 Landscape scale patterns of fi Figure 9.3 re spread in southwestern Tasmania. Fire spread is controlled by topography, vegetation, and the meteorological conditions that prevailed at the time of the fi ‐ random patterns of burnt and unburnt areas. Photograph by David Bowman. re creating strongly non infrequently because of microclimates that keep The study by Sibold et al. (2006) captures many fuels moist under all but drought conditions. Cli- of the above complexities in understanding fi re mate cycles such as the El Niño Southern Oscilla- extent and occurrence. They combined tree ring fl uence tion (ENSO) also strongly in re activity. For fi analyses and geographic information systems re activity typically increases in arid en- fi example, fl (GIS) techniques to identify the in uence of vege- vironments after a wet period because of the build- tation type and structure, elevation and aspect, up of fi ne fuels. Conversely, fi re activity increases uences on fl and regional climate in re activity in fi after a long drought period in moist forests. the Rocky Mountains National Park, Colorado, The satellite record has been extraordinarily ed the primary impor- fi USA. Their analysis identi useful in understanding fi re activity in highly tance of ENSO for fi re activity, yet this climatic re prone environments (see http://www. fi effect was modulated by landscape setting and cfa4wd.org/information/Forest_FDI.htm). Yet re fi vegetation type. Over the 400-year record, the limited time-depth of this record may mask activity was common in the dry, low elevation re events that occur fi the occurrence of infrequent re-prone lodgepole pine fi slopes that support re-prone vegetation such as the fi in long-lived ( Pinus contorta ) forests but at higher elevation boreal forests of Canada and Siberia. Under- there were large areas of long unburnt mesic standing the “ fi ” re regimes of long-lived forests Picea engelmannii r( fi spruce- ) forest. On the moist like those of the boreal zone demands historical western side of the mountain range were fewer, reconstruction such as dendrochronology (tree- but larger, fi res compared to the drier eastern ring analysis) to determine the timing of “ stand sides of the mountain range. This example which initiate a cohort of regen- replacing fi res ” fi re risk, shows that while climate is a driver of eration to replace the burnt forest. Statistical anal- re, climate and vegetation is the linkage between fi ysis of forest stand-age structures can be used to complex, frustrating simple attribution of cause “ fi re usage has a pro- and effect ” . Finally, human determine the inter- fi re intervals (Johnson and “ ” re activity, disturbing found effect on fi natural Gutsell 1994). Dendrochronology has also been re regimes. For example, tropical rainforests are fi re events by identify- used to date precisely past fi currently being transformed to pasture by burn- re scars) on the ing injuries to growth rings ( fi ing (see Box 9.1) yet in some environments, like trunks on long-lived trees (Swetnam 1993). Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

182 1 167 FIRE AND BIODIVERSITY the forests of the western USA, re managers have fi the question of whether the vegetation of the fi re prone effectively eliminated fi re from some fl cantly in fi Earth is signi uenced by landscape landscapes. re. The approach they took was via dynamic fi global vegetation models (DGVMs), which are computer simulations of vegetation based on physiological principles. The effect of landscape climate patterns – 9.4 Vegetation fi re on global vegetation patterns is implicit in decoupled by re fi DGVMs because they include “ fi re modules ” A classic view of plant geography is that vegeta- that introduce frequent disturbances to modeled tion and climate are closely coupled. Recently vegetation patterns and processes. Such modules Bond (2005) challenged this view by asking et al. are necessary in order to recreate actual Box 9.1 Fire and the destruction of tropical forests David M. J. S. Bowman and Brett P. Murphy Each year, extensive areas of tropical forest are Climate change Drought unintentionally burnt by anthropogenic fi res, and are severely degraded or destroyed as a Fragmentation Forest fire agrations result (see Chapter 4). Enormous con fl Increased amount of edge Increased desiccation can occur in response to drought events Increased tree mortality Increased fuel loads associated with ENSO, most notably the Forest degradation – res of 1997 1998, which burnt fi Indonesian Decreased canopy cover Increased desiccation around 8 million hectares of forest (Cochrane Increased grassy fuels 2003). Until recent decades, most tropical fi forests experienced res very infrequently, Deforestation Logging re return intervals in the order of with fi re centuries, although it is now clear that fi Box 9.1 Figure The synergistic effects of habitat fragmentation frequency has increased dramatically in the and degradation on the occurrence of tropical forest fi res. Adapted use past few decades. Current human land ‐ from Cochrane (2003). activities promote forest res by fragmenting fi and encourage grass growth. The waste (see Chapter 5) and degrading forests and biomass from logging operations can also providing ignition sources, which would dramatically elevate fuel loads. Similarly, otherwise be rare. These three factors can act fi re tend to be forests degraded by an initial synergistically to initiate a series of positive more susceptible to repeat res, further fi feedbacks that promote the massive tropical enhancing the feedback loop. forest fi res that have become common in The negative impacts of frequent, intense recent decades (see Box 9.1 Figure). Forest res on tropical forest biodiversity are likely to fi edges tend to be much more susceptible to fi re be enormous, given the existing threats posed than forest cores, because they tend to be more by the direct effects of deforestation (Chapter desiccated by wind and sun, have higher rates res fi 4) and overharvesting (Chapter 6). Intense of tree mortality and hence, woody fuel easily kill a large proportion of tropical forest accumulation and grassy fuel loads tend to be tree species, and repeated res can be fi re frequency tends to fi higher. The result is that especially detrimental to species regenerating increase with proximity to a forest edge, such vegetatively or from seed. Generally, repeated re fi that highly fragmented forests have high fi res lead to a loss of primary forest tree species, frequencies. Forests degraded by selective with these replaced by an impoverished set of logging are also at risk of re due to their fi pioneer species (Barlow and Peres 2008). The reduced canopy cover, which allows the forest re on forest animals are less well fi effects of to become desiccated and light to penetrate continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

183 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All 168 CONSERVATION BIOLOGY FOR ALL Box 9.1 (Continued) understood, although studies following the REFERENCES – 1998 Indonesian fi res suggest severe 1997 Barlow, J. and Peres, C. A. (2008). Fire ‐ mediated dieback impacts on many groups, especially those and compositional cascade in an Amazonian forest. ‐ trees and arthropod reliant on fruit Philosophical Transactions of the Royal Society of communities in leaf litter (Kinnaird and O ’ Brien London B 363 , , 1787 1794. – 1998). On Borneo, endangered orangutan Cochrane, M. A. (2003). Fire science for rainforests. Pongo pygmaeus ( ) populations suffered Nature , 421 , 913 – 919. declines of around 33% following the Kinnaird, M. F. and O Brien, T. G. (1998). Ecological effects ’ res (Rijksen and Meijaard 1999). fi 1998 – 1997 re on lowland rainforest in Sumatra. of wild fi Conservation In many tropical regions, climate change is 956. Biology , 12 ,954 – expected to exacerbate forest res. There is fi Rijksen, H. D. and Meijaard, E. (1999). Our vanishing rela- evidence that extreme weather events, such as tive: the status of wild orang ‐ utans at the close of the – the ENSO droughts that triggered the 1997 . Tropenbos Publications, Wagenin- twentieth century 1998 Indonesian fi res, and tropical storms, may gen, the Netherlands. become more frequent (Timmermann et al. Mann, M. E. and Emanuel, K. A. (2006). Atlantic hurricane 1999; Mann and Emanuel 2006). Additionally, trends linked to climate change. Eos, Transactions of the we can expect strong positive feedbacks 87 , , doi:10.1029/ American Geophysical Union re occurrence and climate fi between forest 2006EO240001. res result in change, because tropical forest fi Page, S. E., Siegert, F., Rieley, J. O., Boehm, H. D. V., Jaya, enormous additions of greenhouse gases to the A., and Limin, S. (2002). The amount of carbon released atmosphere, leading to even more rapid from peat and forest fi res in Indonesia during 1997. – climate change. For example, the 1997 1998 420 , Nature 65. – ,61 ‐ 2.6 Gt of carbon to Indonesian fi res released 0.8 Timmermann, A., Oberhuber, J., Bacher, A., Esch, 40% of the atmosphere, equivalent to 13 – M., Latif, M., and Roeckner, E. (1999). Increased global emissions due to burning fossil fuels, El Niño frequency in a climate model forced making a large contribution to the largest Nature , by future greenhouse warming. recorded annual increase in atmospheric CO 2 – 697. 398 , 694 2002). et al. concentration (Page vegetation patterns. Bond et al. (2005) found that and grasses can coexist in the long-term has long a world without fi re had very different vegetation puzzled savanna ecologists. Conventional ecolog- zones compared with the actual vegetation geog- ical theory of plant succession suggests that highly switched fi raphy. For example, when re was “ productive savannas are unstable and should off ” , dense ( 80%) tree cover increased from > gradually progress toward closed canopy forest. 27% to 56% of the vegetated Earth surface and While it seems that in less productive savannas, more than half (52%) of the current global distri- such as in low rainfall areas, tree biomass is indeed bution of tropical savannas were transformed to constrained by the limitation of resources, such as angiosperm-dominated forests. The core message water, recent research suggests that in more pro- fi re causes the “ of this analysis is that decou- ductive savannas, recurrent disturbance plays an of vegetation patterns from climate. ” pling – important role in maintaining a tree grass balance Arguably the most well known decoupling of et al. fl ammability (Sankaran 2005). Given the high vegetation and climate concerns the geographic fi of savannas, it seems that disturbance due to re is distribution of forest and savanna. Savannas are of particular importance. fi among the most re-prone biomes on Earth, and The most widely accepted explanation of how are characterized by varying mixtures of both tree res limit tree biomass in savannas as- frequent fi and grass biomass. The question of how both trees tree demographic-bottleneck “ sumes that a ” Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

184 1 169 FIRE AND BIODIVERSITY occurs. It is accepted that re frequency controls fi re trap plants to escape the , and increase in ” fi “ the recruitment of savanna trees, particularly the dominance (Sankaran 2004; Werner 2005). et al. growth of saplings into the tree layer. Unlike For example, extensive woody plant encroach- mature trees, saplings are too short in stature to ment has occurred in mesic grassland and savan- re-damage and unlike juveniles, if they fi avoid na in Queensland, Australia, and has been are damaged they cannot rapidly return to their re re- fi attributed to cattle grazing and changed previous size from root stocks (Hoffman and gimes (Crowley and Garnett 1998). This trend can Solbrig 2003). Thus saplings must have the abili- be reversed by reduced herbivory coupled with ty to tolerate recurrent disturbance until they sustained burning a methodology used by pas- — have suf cient reserves to escape through a dis- fi toralists to eliminate so called woody weeds ” “ into the ” turbance-free “ recruitment window from overgrazed savannas. Bond and Archibald canopy layer where they suffer less fi re damage. (2003) suggest that in southern African savannas re can stop savanna fi Recurrent disturbance by re frequen- fi there is a complex interplay between tree populations from attaining maximal tree cy and herbivory. Heavily grazed savannas biomass by creating bottlenecks in the transition support short grass , dominated by ” lawns “ re-sensitive sapling stage to the of the relatively fi species in the sub-family Chloridioideae, which 2004). In et al. re tolerant tree stage (Sankaran fi do not burn. These lawns support a diversity of the extreme case, a suf fi cient frequency of burn- large grazers including white rhino ( Ceratother- ing can result in the loss of all trees and the ium simum ), wildebeest ( Connochaetes spp.), impa- complete dominance of grass. Conversely, fi re la ( Phacochoerus ), warthog ( Aepyceros melampus protection can ultimately result in the recruit- Equus spp.) (Figure 9.4). ), and zebra ( africanus cient saplings to result in a closed fi ment of suf Under less intense grazing, these lawns can canopy forest. switch to supporting bunch grass, in the sub- Large herbivores may also interact with re fi family Andropogoneae, which support a less di- activity because high levels of grazing typically verse mammal assemblage adapted to gazing tall fi re frequency, and this can enable woody reduce grasses, such as African buffalo ( Syncerus caffer ). Figure 9.4 ’ in a humid savanna in Hluhluwe ‐ Umfolozi Park, South Africa. Bond and Archibald (2003) Zebra and wildebeest grazing on a ‘ lawn ammable by creating mosaics of lawns that increase the diversity of the fl suggest that intense grazing by African mammals may render savannas less fl ammable, tall grasses with a lower diversity of large fi large mammal assemblage. Large frequent res are thought to switch the savannas to more mammals. Photograph by David Bowman. See similar Figure 4.6. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

185 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 170 re. For example, the Tasmanian Abor- fi tinely use The high biomass of the bunch grasslands render igines always carried fi re with them, as it was an these systems highly ammable. Bond and Archi- fl indispensable tool to survive the cold wet environ- bald (2003) propose a model where frequent large ment (Bowman 1998). The expansion of humans res can result in a loss of lawns from a landscape fi throughout the world must have signi cantly fi with corresponding declines in mammal diversi- changed the pattern of landscape burning by either ty. The mechanism for this is that resprouting by fi re to forests to clear them or intentionally setting grasses following fi re causes a lowering in overall accidentally starting fi res. How prehistoric human grazing pressure across the landscape. Fully un- re usage changed landscape re activity and eco- fi fi derstanding the drivers of the expansion of system processes remains controversial and this woody vegetation into rangelands, including the issue has become entangled in a larger debate re and herbivory, remains a major eco- fi role of about the relative importance of humans vs. cli- logical challenge (see http://ag.arizonal.edu/re- mate change in driving the late Pleistocene mega- search/archer/research/biblio1.html). et al. faunal extinctions (Barnosky 2004; Burney and How savanna vegetation evolved is unclear. Flannery2005).CentraltothisdebateistheAborig- Some authors suggest that falling atmospheric car- ) concentrations may have stimu- inal colonization of Australia that occurred some bon dioxide (CO 2 lated the development of grasses that now 40 000 years ago. Some researchers believe that dominate tropical savannas (Bond et al. 2003). human colonization caused such substantial Tropical savanna grasses have the C4 photosyn- changes to re regimes and vegetation distribution fi thetic pathway that is highly productive in hot, patterns that the marsupial megafauna were concentrations wet climates, and under low CO driven to extinction. This idea has recently been 2 these grasses have a physiological advantage over supported by the analysis of stable carbon isotopes 13 C) in fossil eggshells of emus and the extinct woody vegetation that has the C3 photosynthetic d ( giant in the Lake Genyornis newtoni ightless bird fl pathway. The production of large quantities of Eyre Basin of central Australia. Miller et al. (2005a) ne and well-aerated fuels may have greatly fi interpreted these results as indicating that sus- re disad- increased the frequency of landscape fi tained Aboriginal landscape burning during colo- vantaging woody plants and promoting further nization in the late Pleistocene caused the grassland expansion. The development of mon- transformation of the central Australian landscape soon climates might have also been as important from a drought-adapted mosaic of trees, shrubs, a driver as low atmospheric concentrations of CO 2 (Keeley and Rundel 2003). The monsoon climate is and nutritious grasslands to the modern fi re- particularly fi re-prone because of the characteristic adapted desert scrub. Further, climate modeling alternation of wet and dry seasons. The wet season suggests that the switch from high to low leaf- allows rapid accumulation of grass fuels, while the area-index vegetation may explain the weak pene- dry season allows these fuels to dry out and be- tration of the Australian summer monsoon in the come highly fl ammable. Furthermore, the dry sea- present, relative to previous periods with similar son tends to be concluded by intense convective climates (known as “ interglacials ” et al. )(Miller storm activity that produces high densities of 2005b). lightning strikes (Bowman 2005). Yet despite the above evidence for catastrophic impacts following human colonization of Austra- lia, it is widely accepted that at the time of Euro- pean colonization Aboriginal re management fi re fi 9.5 Humans and their use of was skilful and maintained stable vegetation pat- Our ancestors evolved in tropical savannas and terns (Bowman 1998). For example, recent studies mas- this probably contributed to our own species ’ in the savannas of Arnhem Land, northern Aus- tery of re. Indeed, humans can be truly described fi fi re tralia, show that areas under Aboriginal as a re keystone species given our dependence on fi management are burnt in patches to increase kan- re; there is no known culture that does not rou- fi garoo densities (Figure 9.5; Murphy and Bowman Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

186 1 171 FIRE AND BIODIVERSITY 2007). Further, there is evidence that the cessation demands numerous studies, in order to detect of Aboriginal fi re management in the savannas local-scale effects and understand the underlying ammable grass has resulted in an increase in fl of their landscape burning practices (e.g. “ logic ” re activity fi biomass and associated high levels of Murphy and Bowman 2007). Also of prime im- fi re cycle “ – grass (see Box 9.2). consistent with a ” portance is study of the consequences of prehis- It is unrealistic to assume that there should only toric human colonization of islands such as New be one uniform ecological impact from indige- Zealand. In this case, there is clear evidence of nous fi re usage. Clearly working out how indige- dramatic loss of forest cover and replacement nous people have in uenced landscapes fl with grasslands (McGlone 2001). – re cycle fi Box 9.2 The grass David M. J. S. Bowman and Brett P. Murphy while other nutrients, such as phosphorus, are ’ Antonio and Vitousek (1992) described a D made more chemically mobile and thus fi re and invasive grasses feedback between susceptible to leaching. Thus, nutrient cycles that has the capacity to radically transform are disrupted, with a consequent decline in woodland ecosystems, a process they described overall stored nutrients for plants. This change re cycle grass – as the . The cycle begins with “ ” fi can further reinforce the grass re cycle fi – invasive grasses establishing in native because the ‐ loving grasses thrive on the fi re vegetation, increasing the abundance of temporary increase in the availability of fi aerated ‐ drying and well ‐ quick ne fuels that nutrients. promote frequent, intense res. While the fi An example of an emerging grass re cycle is fi – invasive grasses recover rapidly from these res fi provided by the tropical savannas of northern via regeneration from underground buds or Australia, where a number of African grasses seeds, woody plants tend to decrease in continue to be deliberately spread as improved abundance. In turn, this increases the pasture for cattle. Most notably, gamba grass abundance of the invasive grasses, further ) rapidly invades savanna Andropogon gayanus ( increasing fi re frequency and intensity. The loss vegetation, resulting in fuel loads more than of woody biomass can also result in drier ‐ invaded four times that observed in non microclimates, further adding momentum to et al. savannas (Rossiter 2003). Such fuel loads fi – re cycle. Eventually the grass fi – re the grass cycle can convert a diverse habitat with many res, resulting fi allow extremely intense savanna different species to grassland dominated by a in rapid reductions in tree biomass (see Box 9.2 few exotics. Figure). The conversion of a savanna woodland, The consequences of a grass – fi re cycle for with a diverse assemblage of native grasses, to ecosystem function can be enormous. The a grassland monoculture is likely to have increase in fi re frequency and intensity can enormous impacts on savanna biodiversity as result in massive losses of carbon, both directly, gamba grass becomes established over large via combustion of live and dead biomass, and tracts of northern Australia. Despite the widely indirectly, via the death of woody plants and acknowledged threat posed by gamba grass, it their subsequent decomposition or is still actively planted as a pasture species in combustion. For example, invasion of many areas. Preventing further spread of cheatgrass ( ) in the Great Bromus tectorum gamba grass must be a management priority, Basin of the United States and the given that, once established, reversing a grass fi re cycle has led to a – establishment of a grass fi re – cycle is extraordinarily dif fi cult. This is loss of 8 Mt of carbon to the atmosphere and is because woody juveniles have little chance of likely to result in a further 50 Mt loss in coming reaching maturity given the high frequency of decades (Bradley et al. res, fi 2006). During res and intense competition from fi intense nitrogen is also volatilized and lost in smoke, grasses. continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

187 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 172 Box 9.2 (Continued) REFERENCES Bradley, B. A., Houghtonw, R. A., Mustard, J. F., and Hamburg, S. P. (2006). Invasive grass reduces aboveground carbon stocks in shrublands Global Change Biology of the Western US. , 12 , – 1822. 1815 ’ D Antonio, C. M. and Vitousek, P. M. (1992). Biological invasions by exotic grasses, the grass/ fi re cycle, and global change. Annual Review of Ecology and System- ,63 atics , 23 – 87. Rossiter, N. A., Setter eld, S. A., Douglas, M. M., fi and Hutley, L. B. (2003). Testing the grass ‐ fi re cycle: alien grass invasion in the tropical savannas of northern Australia. Diversity and Distributions , Box 9.2 Figure An example of a grass ‐ fi re cycle becoming 9 – , 169 176. established in northern Australian savannas. African gamba grass is highly invasive and promotes enormously elevated fuel loads and high intensity fi res, resulting in a rapid decline in woody species. Photograph by Samantha Setter fi eld. Agricultural expansion is often enabled by acterized by an ensemble of positive feedbacks fi using re as a tool to clear forests, a pattern that res above the fi greatly increasing the risk of has occurred since the rise of civilization. Current- extremely low background rate (Cochrane et al. ly, this process is occurring most in the tropics. The 1999; Cochrane 2003; see Box 9.1). Recurrent burn- fi re-driven destruction of forests has been studied ing can therefore trigger a landscape-level trans- in close detail in the Amazon Basin, and is char- ammable formation of tropical rainforests into fl fi Figure 9.5 re is still practiced by indigenous people in many parts of northern and central Australia. Recent Traditional land management using ‐ scale mosaic of burnt patches of varying age, which is thought to fi re management results in a fi ne work in Arnhem Land suggests that skilful be critically important for maintaining populations of many small mammals and granivorous birds. Photograph by Brett Murphy. Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

188 1 173 FIRE AND BIODIVERSITY re fi light conditions (see Box 9.3). For example, scrub and savanna, exacerbated by the establish- is critically important for the regeneration of – “ ” fi re cycle grass (see Box 9.2). ment of a re-prone heath com- fi many plant species of the ’ s Mediterranean munities typical of the world climates (e.g. South African fynbos, southwest- 9.6 Fire and the maintenance ern Australian kwongan, Californian chaparral). of biodiversity Many species in these communities have deeply dormant seeds that only germinate following re-sensitive species 9.6.1 Fire-reliant and fi re, when normally limited resources, such as fi Many species in re-prone landscapes are not fi light and nutrients, are abundant. Many hard- re to complete fi re tolerant, but depend on fi only species Acacia seeded heath species, especially their life-cycles and to retain a competitive edge and other legumes, are stimulated to germinate in their environment. Such species typically by heat, while many others are stimulated by fi bene t from the conditions that prevail follow- chemicals in smoke (Bell et al. 1993; Brown re, such as increased resource availability fi ing a 1993). Other species in these communities typi- associated with the destruction of both living ower following a fl cally only fi re (e.g. Denham and dead biomass, nutrient-rich ash, and high and Whelan 2000). fi s giant ’ Box 9.3 Australia reweeds David M.J.S Bowman and Brett P. Murphy rainforest ” in Australia. These forests grow in “ Australian botanists have been remarkably a relatively high rainfall environment (>1100 unsuccessful in reaching agreement as to what mm per annum) with a limited summer constitutes an Australian rainforest (Bowman drought of less than three months duration. nitional problem lies fi 2000). The root of this de Elsewhere in Australia, such a climate in ” with the refusal to use the term “ rainforest would support rainforest if protected from the literal sense, which would involve including re. However, in southwestern Australia fi the tall eucalypt forests that occur in Australia ’ s there are no continuously regenerating high rainfall zones (see Box 9.3 Figure). This is and fi re intolerant rainforest species to despite the fact that the originator of the term, compete with karri, although geological German botanist Schimper, explicitly included and biogeographic evidence point to the eucalypts in his conception of rainforest. The existence of rainforest in the distant past. reason why eucalypt forests are excluded from The cause of this disappearance appears ” “ the term rainforest by Australians is that fi cation and the to be Tertiary aridi re disturbance to these forests require fi accompanying increased occurrence of regenerate, in contrast to true rainforests that re. For example, a pollen core landscape fi ‐ are comparatively sensitive. Typically, fi re from 200 km north of Perth shows that by fi res kill all individual infrequent very intense 2.5 million years ago the modern character c regeneration from eucalypts, allowing proli fi of the vegetation, including charcoal seed to occur, facilitated by the removal of the evidence of recurrent landscape fi res, canopy and creation of a nutrient rich bed of ‐ had established in this region, although fi re, regeneration from seed does ash. Without Nothofagus some rainforest pollen (such as aged stands of ‐ not occur, resulting in very even ) indicates that Phyllocladus and mature eucalypts. rainforest pockets persisted in the 90 m tall) karri ( Eucalyptus – The gigantic (50 landscape at this time (Dodson and ) forests of southwestern Australia diversicolor Ramrath 2001). underscore the complexity of the term continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

189 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 174 (Continued) Box 9.3 The gigantic size of karri and a regeneration limited reserves onto ashbeds, suggests re disturbance, fi strategy dependent upon convergent evolution with other, distantly including mass shedding of tiny seeds with related, eucalypts such as mountain ash E. regnans ( ) in southeastern Australian and E. grandis in northeastern and eastern Australia. Such convergence suggests that all have been exposed to similar natural selection pressures and have evolved to compete with rainforest species by using re as an agent of inter fi ‐ speci fi c competition (e.g. Bond and Midgley 1995). The extraordinary diversity of the genus Eucalyptus and convergent evolution of traits such as gigantism in different lineages in this clade, and similar patterns of diversi fi cation in numerous other taxonomic groups, leads to the inescapable conclusion that fi re had been an integral part of the Australian environment for millions of years before human colonization. Aborigines, therefore, learnt to live with an inherently fl ammable environment. REFERENCES Bowman, D. M. J. S. (2000). Australian rainforests: islands . Cambridge University Press, of green in a sea of re fi Cambridge, UK. an — Bond, W. J. and Midgley, J. J. (1995). Kill thy neighbor individualistic argument for the evolution of fl ammability. , 85. – ,79 73 Oikos tree in southern Tasmania. Box 9.3 Figure Giant Eucalyptus regnans Dodson, J. R. and Ramrath, A. (2001). An Upper Pliocene ‐ The life re to enable fi cycle of these trees depends upon infrequent Western ‐ lacustrine environmental record from south re a dense temperate seedling establishment. Without fi Nothofagus Australia preliminary results. — Palaeogeography rainforest develops because of the higher tolerance of rainforest seedlings to low light conditions. Photograph by David Bowman. 320. Palaeoclimatology Palaeoecology , 167 , 309 – re-prone landscapes, there may fi Even within ” “ fi re-bearing ” ), and slopes on the lee-side of ests be species and indeed whole communities that winds (Bowman 2000). Several factors lead to this re-sensitive. Typically these occur in parts are fi res burn more intensely up hill, es- fi association: fi re frequency or severity of the landscape where pecially if driven by wind; rocks tend to limit the is low, possibly due to topographic protection. amount of grassy fuel that can accumulate; deep For example, when fi re sensitive rainforest com- gorges are more humid, reducing the fl ammabili- munities occur within a ammable matrix of fl ty of fuels; and high soil moisture may lead to grassland and savanna, as throughout much of higher growth rates of the canopy trees, increas- the tropics, they are often associated with rocky ing their chances of reaching maturity, or a re- fi gallery for- “ gorges, incised gullies (often called res. resistant size, between fi © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

190 1 175 FIRE AND BIODIVERSITY Somewhat counter-intuitively, many re-sensi- fi tive species in re-prone landscapes are favored fi fi by moderate frequencies of low intensity res, res greatly fi especially if they are patchy. Such reduce fuel loads and thus the likelihood of fi res. In addition, because low in- large, intense tensity res are typically more patchy than high fi intensity res, they tend to leave populations of fi re-sensitive species undamaged providing a fi seed source for regeneration. Such an example is re-sensitive en- fi provided by the decline of the Athro- demic Tasmanian conifer King Billy pine ( taxis selaginoides ) following the cessation of Aboriginal landscape burning (Brown 1988; re-and- fi fi http://www.anbg.gov.au/ re ecology/ biodiversity.html). The relatively high frequency of low-intensity fi res under the Aboriginal regime ap- pearstohavelimitedtheoccurrenceofspatially res. Under the European extensive, high intensity fi Callitris Recently killed individuals of cypress pine ( Figure 9.6 intratopica fi re regime ), a conifer that is an obligate seeder. Changes in regime, no deliberate burning took place, so that re management fi following the breakdown of traditional Aboriginal res inevitably occurred, often started fi when wild have seen a population crash of this species throughout its range in by lightning, they were large, intense, and rapidly northern Australia. Photograph by David Bowman. destroyed vast tracts of King Billy pine. Over the last century, about 30% of the total coverage of King density, and stand structure signal departure from Billy pine has been lost. fi re regimes. historical A similar situation has resulted in the decline of ) in northern the cypress pine ( Callitris intratropica Australian savannas (Bowman and Panton 1993). 9.6.2 Fire and habitat complexity Cypress pine is a fi re-sensitive conifer found fi A complex re regime can create habitat com- across much of tropical Australia. Mature trees have thick bark and can survive mild but not plexity for wildlife by establishing mosaics of intense fi res, and if stems are killed it has very different patch size of regenerating vegetation limited vegetative recovery. Seedlings cannot sur- fi following res. Such habitat complexity provides res. Thus, it is aptly de- vive even the coolest fi a diversity of microclimates, resources, and shel- .Populationsof obligate seeder ” “ scribed as an ter from predators. It is widely believed that the catastrophic decline of mammal species in central fi res occurring cypress pine can survive mild Australia, where clearing of native vegetation for – every 2 8 years, but not frequent or more intense agriculture has not occurred, is a direct conse- res because of the delay in seedlings reaching fi res to fi maturity and the cumulative damage of ne-scale habi- fi quence of the homogenization of adults. Cessation of Aboriginal land management tat mosaics created by Aboriginal landscape has led to a decline of cypress pine in much of its burning. This interpretation has been supported former range, and it currently persists only in rain- fi ” by analysis of “ from historical aerial re scars forest margins and savanna micro-sites such as in photography and satellite imagery. For example, fi re Burrows and Christensen (1991) compared rocky crevasses or among boulders or drainage s Western Desert in scars present in Australia ’ re (Figure 9.6). lines that protect seedlings from fi 1953, when traditional Aboriginal people still oc- Fire sensitive species such as King Billy pine and cypress pine are powerful bio-indicators of altered cupied the region, with those present in 1986, fi re regimes because changes in their distribution, when the area had become depopulated of its © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

191 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 176 original inhabitants. In 1953, the study area t all. The quest for sustain- vation, one size can ’ t fi fi re scars with a mean area of 34 contained 372 able fi re regimes demands trialing approaches ha, while in 1986, the same area contained a sin- and monitoring outcomes while balancing biodi- fi re scar, covering an area of 32 000 ha. Clear- gle versity outcomes against other priorities such as ly, the present regime of large, intense and protection of life and property. This quest for infrequent fi res associated with lightning strikes continuous improvement in land management has obliterated the ne-grained mosaic of burnt fi “ has been formalized in a process known as adap- patches of varying ages that Aboriginal people tive management . This iterative process is most ” 2006). The et al. had once maintained (Burrows applicable when faced with high levels of uncer- cessation of Aboriginal landscape burning in cen- tainty, and involves continually monitoring and tral Australia has been linked to the range con- evaluating the outcomes of management actions, traction of some mammals such as the rufous and modifying subsequent actions accordingly. Lagorchestes hirsutus ) (Lundie-jen- hare-wallaby ( kins 1993). Recent research in northern Austra- s tropical savannas, where small mammals lia ’ re regimes 9.7 Climate change and fi and granivorous birds are in decline, also points There is mounting concern that the frequency and to the importance of unfavorable fi re regimes that intensity of wild res may increase in response to fi followed European colonization (Woinarski et al. global climate change (see Chapter 8), due to the 2001). A prime example is the decline of the par- greater incidence of extreme fi re weather. While ). This bird is par- Geophaps smithii tridge pigeon ( the effect is likely to vary substantially on a global fi ticularly vulnerable to changes in re regime scale, regions that are likely to experience sub- because it is feeds and nests on the ground and stantial increases in temperature and reductions has territories of less than 10 ha. Their preferred in rainfall are also likely to experience more habitat is a fi ne-grained mosaic of burnt and un- re weather. Indeed, such a trend is fi extreme burnt savanna, where it feeds on seeds on burnt already apparent in southeastern Australia ground but nests and roosts in unburnt areas (Lucas 2007) and the western United States et al. et al. (Fraser 2003). Aboriginal landscape burning et al. 2006). (Westerling fi ne-grained has been shown to produce such a In addition to the effects of climate change, an 2004). mosaic (Bowman et al. concentration is like- increase in atmospheric CO 2 ly to affect the abundance and composition of fuel 9.6.3 Managing re regimes for biodiversity fi loads, and hence the frequency and intensity of The contrasting requirements of different species concentration is likely to in- res. Elevated CO fi 2 re-prone landscapes and communities within fi crease plant productivity, especially that of spe- cies utilizing the C3 photosynthetic pathway fi culties faced by those manag- highlights the dif (mainly woody plants and temperate grasses), re regimes for biodiversity conservation. ing fi such that there have been suggestions that fuel fi re-reliant and fi re- How does one manage for et al. production will increase in the future (Ziska sensitive species at the same time? Lessons can concentration may 2005). Further, elevated CO clearly be learnt from traditional hunter-gatherer 2 lower the nitrogen content of foliage, slow- societies that extensively used, and in some cases ing decomposition and resulting in heavier fuel re as a land management tool. While it is still use, fi build up (Walker 1991). However, to state that an unlikely that the enormous complexity of tradi- concentration will increase fuel increase in CO fi tional re use can ever be fully encapsulated in 2 re frequency and intensity, is fi loads, and hence re regimes imposed by conservation managers, fi likely to be a gross over-generalization; the effects it is clear that spatial and temporal complexity of are in fact likely to vary substan- of elevated CO the regime must be maximized to ensure the max- 2 tially between biomes. For example, in tropical fi ts to biodiversity. Clearly, in the case imum bene savannas, it is likely that increases in CO fi of re regimes designed for biodiversity conser- 2 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

192 1 177 FIRE AND BIODIVERSITY concentration will strongly favor woody plants, extent of habitats; and (iv) rigorous evaluation of especially trees, at the expense of grasses and ts of management interventions. the costs and bene fi other herbaceous plants (Bond and Midgley “ thresholds of potential An important concept is fl 2000). A shift from highly ammable grassy which prede nes acceptable changes in fi ” concern fuels to fuels based on woody plants is likely to re regimes fi the landscape in response to different re frequency and intensity in savannas. reduce fi (Bond and Archibald 2003). Bradstock and Kenny Indeed, Bond and Archibald (2003) have argued (2003) provided an example of this approach for fi re fre- that managers should consider increasing fi assessing the effect of inter- re interval on species quencies to counteract the increase in growth diverse scherophyll vegetation in the Sydney re- rates of savanna trees that would result in higher gion of southeastern Australia. This vegetation tree “ tree densities due to a weakening of the supports a suite of species that are obligate seeders demographic bottle-neck . In contrast, in more ” re- fi whose survival is held in a delicate balance by arid biomes where fi re occurrence is strongly lim- frequency. Fire intervals that are shorter than the ited by antecedent rainfall (Allan and Southgate time required for maturation of plant species result 2002), an increase in productivity is indeed likely in local extinction because of the absence of seeds fi res can to increase the frequency with which while longer re intervals also ultimately result in fi occur with a corresponding decrease in woody regeneration failure because adults die and seed- cover. banks become exhausted. Bradstock and Kenny fi Climate change is set to make re management (2003) found that to sustain the biodiversity of even more complicated, given that climate sclerophyll vegetation, fi re intervals between 7 fi re risk, ecosys- change simultaneously changes and 30 years are required. Monitoring is required tem function, and the habitat template for most to ensure that the majority of the landscape does organisms, including invasive species. A recent “ thresholds of potential not move outside these . ” report by Dunlop and Brown (2008) discussing concern Fire management is set to remain a thorny issue the impact of climate change on nature reserves for conservation biologists given the need to devise in Australia succinctly summarizes the problem fi re regimes to achieve multiple outcomes that on conservation biologists now face. They write: the one hand protect life and property and on the “ The question is how should we respond to other maintain biodiversity and ecosystem ser- re regimes? Efforts to main- fi the changing vices. The accelerating pace of global environmen- tain historic fi ‘ re regimes through hazard ’ tal change, of which climate change is but one reduction burning and vigorous fi re sup- re fi component, makes the quest for sustainable pression may be resource intensive, of limit- management both more critical and more complex. ed success, and have a greater impact on re fi The current quest for ecologically sustainable biodiversity than natural changes in re- management can draw inspiration from indige- gimes. It might therefore be more effective nous societies that learnt to coexist with fi re to to allow change and manage the conse- create ecologically sustainable and biodiverse fi quences. The challenge is to nd a way to landscapes (also see Box 1.1). Modern solutions do this while ensuring some suitable habitat will undoubtedly be science based and use space- is available for sensitive species, and simul- age technologies such as satellites, global position- taneously managing the threat to urban ing systems, computer models and the web. ” areas, infrastructure, and public safety. Again this demands an adaptive management approach, the key ingredients of which include: (i) Summary clear stated objectives; (ii) comprehensive re fi The Earth has a long history of landscape fi re given: fi re activity across the mapping programs to track · (i) the evolution of terrestrial carbon based vegetation; landscape; (iii) monitoring the population of biodi- fi cient to (ii) levels of atmospheric oxygen that are suf versity indicator species and/or condition and © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

193 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 178 . University of Wa- Fire: a brief history Pyne, S. J. (2001). support the combustion of both living and dead or- · shington Press, Seattle. ganic material; and (iii) abundant and widespread ignitions from lightning, volcanoes and humans. There is a clear geographic pattern of fi re activity · across the planet re fl ecting the combined effects of Relevant websites climate, vegetation type and human activities. Most Online journal of the Association for Fire Ecology: re activity is concentrated in the tropical savanna fi · http:/ /www. fi recology.net. biome. International Journal of Wildland Fire, journal of the Fire activity shows distinct spatial and temporal · · / International Association of Wildland Fire: http:/ patterns that collectively can be grouped into “ fi re www.iawfonline.org. regimes . Species show preferences for different fi ” re North Australian Fire Information: http://www. fi re- regimes and an abrupt switch in re regime can fi · north.org.au. have a deleterious effect on species and in extreme Forest Fire Danger Meter: http:/ /www.cfa4wd.org/ · situations, entire ecosystems. A classic example of information/Forest_FDI.htm. this is the establishment of invasive grasses, which Proliferation of woody plants in grasslands and savan- · re frequency and intensity fi dramatically increase – nas /ag.arizonal.edu/research/ a bibliography: http:/ with a cascade of negative ecological consequences. archer/research/biblio1.html. Climate change presents a new level of complexity res affect biodiversity: http:/ How /www.anbg.gov. fi · · fi re management and biodiversity conservation for fi re-and-biodiversity.html. au/ re_ecology/ fi re risk due to climate fi because of abrupt changes in Kavli Institute of Theoretical Physics Miniconference: · change and simultaneous stress on species. Further, – 30, Pyrogeography and Climate Change (May 27 elevated atmospheric CO concentration may result /online.itp.ucsb.edu/online/pyrogeo_c08. 2008): http:/ 2 in changes in growth and fuel production due to ciency fi changes in growth patterns, water use ef and allocation of nutrients. Numerous research challenges remain in under- Acknowledgements · fi re including: standing the ecology and evolution of The Kavli Institute for Theoretical Physics Mini- ammability changes in response to nat- (i) whether fl conference: Pyrogeography and Climate Change meeting ural selection; (ii) how life-history traits of both /online.itp.ucsb.edu/online/pyrogeo_c08) helped us (http:/ re regimes; and plants and animals are shaped by fi organize our thinking. We thank the co-convener of that re in order to con- (iii) how to manage landscape fi meeting, Jennifer Balch, for commenting on this chapter. serve biodiversity. An Australian Research Council grant (DP0878177) sup- ported this work. Suggested reading Fire and Bond, W. J. and Van Wilgen, B. W. (1996). · REFERENCES . Chapman and Hall, London, UK. plants Bowman, D. M. J. S. (2000). Australian rainforests: islands Allan, G. E. and Southgate, R. I. (2002). Fire regimes in the · fi re . Cambridge University Press, of green in a land of spinifex landscapes of Australia. In R. A. Bradstock, J. E. Cambridge, UK. Williams, and M. A. Gill, eds Flammable Australia: the Fire Flannery, T. F. (1994). The future eaters: an ecological Regimes and Biodiversity of a Continent 176. Cam- – , pp. 145 · Reed Books, history of the Australasian lands and people. bridge University Press, Cambridge, UK. Chatswood, New South Wales, Australia. Barnosky, A. D., Koch, P. L., Feranec, R. S., Wing, S. L., and . Cambridge Uni- The ecology of Whelan, R. J. (1995). re fi Shabel, A. B. (2004). Assessing the causes of Late Pleisto- · versity Press, Melbourne, Australia. Science , 306 ,70 cene extinctions on the continents. 75. – Bell, D. T., Plummer, J. A., and Taylor, S. K. (1993). Seed Gill, A. M., Bradstock, R. A., and Williams, J. E. (2002). · germination ecology in southwestern Western Australia. Flammable Australia: the re regimes and biodiversity of a fi ,24 – 73. 59 , Botanical Review continent . Cambridge University Press, Cambridge, UK. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

194 1 179 FIRE AND BIODIVERSITY Burney, D. A. and Flannery, T. F. (2005). Fifty millennia of Bond, W. J. and Archibald, S. (2003). Confronting complex- Trends in catastrophic extinctions after human contact. fi re policy choices in South African savanna parks. ity: 401. Ecology and Evolution , 20 , 395 – – , 381 389. , 12 International Journal of Wildland Fire Burrows, G. E. (2002). Epicormic strand structure in Ango- herbi- ‘ Bond, W. J. and Keeley, J. E. (2005). Fire as a global im- — phora, Eucalyptus and Lophostemon (Myrtaceae) ammable ecosys- fl : the ecology and evolution of ’ vore re resistance and recovery. fi New plications for – , 387 20 , Trends in Ecology and Evolution 394. tems. 131. , Phytologist , 111 153 – Bond, W. J. and Midgley, J. J. (1995). Kill thy neighbor — an Burrows, N. D. and Christensen, P. E. S. (1991). A survey of individualistic argument for the evolution of fl ammabil- Aboriginal fi re patterns in the Western Desert of Austra- ity. 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195 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 180 Sankaran, M., Ratnam, J., and Hanan, N. P. (2004). Tree- Johnson, E. A. and Gutsell, S. L. (1994). Fire frequency grass coexistence in savannas revisited — insights from models, methods and interpretations. Advances in Ecolog- an examination of assumptions and mechanisms in- 287. – ical Research , 25 , 239 voked in existing models. Ecology Letters Justice, C. O., Smith, R., Gill, A. M., and Csiszar, I. (2003). A , 480 7 , 490. – fi re monitoring in Australia review of current space-based (2005). Sankaran, M., Hanan, N. P., Scholes, R. J., et al. and the GOFC/GOLD program for international coordi- Determinants of woody cover in African savannas. Na- International Journal of Wildland Fire nation. 258. , 12 ,247 – ture , , 846 – 438 849. Keeley, J. E. and Rundel, P. W. (2003). Evolution of CAM Schwilk, D. W. and Kerr, B. (2002). Genetic niche-hiking: an and C fl alternative explanation for the evolution of ammability. International carbon-concentrating mechanisms. 4 – 442. , 431 99 , Oikos , S55 – S77. 164 , Journal of Plant Sciences Scott, A. C. and Glasspool, I. J. (2006). The diversi fi cation of Lucas, C., Hennessey, K., Mills, G., and Bathols, J. (2007). Paleozoic re systems and uctuations in atmospheric fl fi Bush re weather in Southeast Australia: recent trends and fi oxygen concentration. Proceedings of the National Academy . Consultancy report projected climate change impacts – , 10861 103 , 10865. of Sciences United States of America prepared for the Climate Institute of Australia by the Sibold, J. S., Veblen, T. T., and Gonzalez, M. E. (2006). re CRC and Australian Bureau of Meteorology. Bush fi re regimes fi Spatial and temporal variation in historic Lundie-Jenkins, G. (1993). Ecology of the rufous hare- in subalpine forests across the Colorado Front Range in wallaby, Lagorchestes hirsutus Gould (Marsupialia: Journal Rocky Mountain National Park, Colorado, USA. Macropodidae), in the Tanami Desert, Northern Territo- , 631 – 33 , of Biogeography 647. , , Wildlife Research ry. I. Patterns of habitat use. 20 Swetnam, T. W. (1993). Fire history and climate change in 476. – 457 Giant Sequoia groves. 262 – , Science 889. , 885 McGlone, M. S. (2001). The origin of the indigenous grass- Walker, B. H. (1991). Ecological consequences of atmo- lands of southeastern South Island in relation to pre- spheric and climate change. Climatic Change , 18 , 301 316. – human woody ecosystems. New Zealand Journal of Ecolo- re Werner, P. A. (2005). Impact of feral water buffalo and fi – 25 gy , ,1 15. on growth and survival of mature savanna trees: an Miller, G. H., Fogel, M. L., Magee, J. W., Gagan, M. K., eld study in Kakadu National Park, fi experimental Clarke, J. S., and Johnson, B. J. (2005a). Ecosystem col- 30 – Austral Ecology , 625 647. northern Australia. , lapse in Pleistocene Australia and a human role in mega- Westerling, A. L., Hidalgo, H. G., Cayan, D. R., and Swet- Science , 309 , 287 – 290. faunal extinction. nam, T. W. (2006). Warming and earlier spring increase Miller, G. H., Mangan, J., Pollard, D., Thompson, S., Felzer, B., 943. , fi re activity. Science 313 , 940 – western US forest wild and Magee, J. (2005b). Sensitivity of the Australian Mon- Whelan, R. J. (1995). The ecology of fi re . Cambridge Univer- soon to insolation and vegetat ion: implications for human sity Press, Cambridge, UK. – Geology ,65 33 , impact on continental moisture balance. 68. Murphy, B. P. and Bowman, D. M. J. S. (2007). The interde- Woinarski, J. C. Z., Milne, D. J., and Wanganeen, G. (2001). re, grass, kangaroos and Australian Abor- fi pendence of Changes in mammal populations in relatively intact igines: a case study from central Arnhem Land, northern landscapes of Kakadu National Park, Northern Territo- , – 34 Journal of Biogeography Australia. 250. , 237 370. ry, Australia. Austral Ecology , 26 , 360 – — Mutch, R. W. (1970). Wildland fi res and ecosystems a Ziska, L. H., Reeves, J. B., and Blank, B. (2005). The impact , 1046 hypothesis. 1051. – , 51 Ecology of recent increases in atmospheric CO on biomass pro- 2 Pyne, S. J. (2007). Problems, paradoxes, paradigms: trian- Bromus duction and vegetative retention of Cheatgrass ( re research. fi International Journal of Wildland gulating tectorum ): implications for fi re disturbance. Global Change Fire , , 271 16 276. – 1332. – , 1325 11 , Biology © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

196 1 CHAPTER 10 Extinctions and the practice of preventing them Stuart L. Pimm and Clinton N. Jenkins In this chapter, we will outline why we consider the source of genes to protect crops from disease. species extinction to be the most important prob- Genetic uniformity can be catastrophic — the lem conservation science must address. Species famous example is the potato famine in Ireland extinction is irreversible, is progressing at a high in the 1840s. rate and is poised to accelerate. We outline the We simply do not know the genetic diversity of — how fast and global features of extinctions enough species for it to provide a practical measure where they occur. Such considerations should for mapping diversity at a large scale. There is, guide global allocation of conservation efforts; however, a rapidly increasing literature on studies they do to some extent, though the priorities of of the genetic diversity of what were once thought some global conservation organizations leave to be single species and are now known to be much to be desired. cantly alter our several. These studies can signi fi We conclude by asking how to go from these actions, pointing as they sometimes doto previous- insights to what tools might be used in a practical ly unrecognized species that need our attention. way. That requires a translation from scales of Martiny (Box 10.1) argues for the importance of 2 2 at to mere tens of km about 1 million km distinct populations within species, where the di- which most conservation actions take place. versity is measured simply geographically. She Brooks (Chapter 11) considers this topic in some , that the loss of local populations inter alia argues, detail, and we shall add only a few comments. means the loss of the ecosystem services species Again, the match between what conservation de- provide locally. She does not mention that, in the mands and common practice is not good. ’ it USA at least, “ Population segments, ” sthelaw. )or Puma concolor coryi such as the Florida panther ( )intheconti- Ursus arctos horribilis grizzly bears ( nental USA are protected under the Endangered 10.1 Why species extinctions have Species Act (see Chapter 12) as if they were full primacy species. Indeed, the distinction is likely not clear means three broad things (Norse ” Biodiversity “ ccommittees fi to the average citizen, but scienti and McManus 1980; Chapter 2): (i) there is diversity fi (National Research Council 1995) af s ’ rm Martiny within a species — usually genetic-based, but with- point and the public perception. Yes, it s important ’ in our own species, there is a large, but rapidly to have panthers in Florida, and grizzly bears in the shrinking cultural diversity (Pimm 2000); (ii) the continental USA, not just somewhere else. diversity of species themselves, and; (iii) the diver- That said, species extinction is irreversible in a sity of the different ecosystems they comprise. way that population extinction is not. Some species The genetic diversity within a species is hugely have been eliminated across much of their ranges important as an adaptation to local conditions. fl ourished — and later restored. And some of these Nowhere is this more obvious than in the differ- turkeys in the eastern USA, for example. Aldo Leo- ent varieties of crops, where those varieties are ’ sdictumapplies:the fi rst law of intelligent pold 181 © Oxford University Press 2010. All rights reserved. For permissions please email: academic.permissions[email protected]

197 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 182 Box 10.1 Population conservation Jennifer B. H. Martiny s three major crops ’ uniform strains of the world Although much of the focus of biodiversity (rice, wheat, and maize) are widely planted; conservation concentrates on species therefore, population diversity among wild crop extinctions, population diversity is a key relatives is a crucial source of genetic material to component of biodiversity. Imagine, for resist diseases and pests. instance, that no further species are allowed to Perhaps the most valuable bene fi tof go extinct but that every species is reduced to population diversity is the delivery of just a single population. The planet would be fi ecosystem services such as the puri cation of air uninhabitable for human beings, because many and water, detoxi fi cation and decomposition of the bene fi ts that biodiversity confers on of wastes, generation and maintenance of soil humanity are delivered through populations fertility, and the pollination of crops and rather than species. Furthermore, the focus on natural vegetation (see Chapter 3). These species extinctions obscures the extent of the services are typically provided by local biodiversity crisis, because population biodiversity; for a region to receive these extinction rates are orders of magnitude higher fi bene ts, populations that carry out the than species extinction rates. ecosystem services need to exist nearby. For When comparing species versus population instance, native bee populations deliver diversity, it is useful to de ne population fi valuable pollination services to agriculture but diversity as the number of populations in an elds within a few kilometers of the only to fi area. Delimiting the population units ’ natural habitats (Kremen etal. populations themselves is more dif fi cult. Historically, 2002; Ricketts 2004). etal. fi populations can be de ned both Estimates of population extinctions due to demographically (by abundance, distribution, and dynamics) and genetically (by the amount human activities, although uncertain, are much of genetic variation within versus between higher than species extinctions. Using a model fi intraspeci (2003) also etal. c groups). Luck of habitat loss that has previously been applied propose that populations be de ned for fi to species diversity, it is estimated that millions “ ‐ providing conservation purposes as service of populations are going extinct per year ” to link population diversity explicitly to units etal. 1997). This rate is three orders of (Hughes the ecosystem services that they provide. magnitude higher than that of species The bene fi ts of population diversity include all rm fi extinction. Studies on particular taxa con the reasons for saving species diversity and more these trends; population extinctions are etal. (Hughes 1998). In general, the greater the responsible for the range contractions of number of populations within a species, the extant species of mammals and amphibians more likely that a species will persist; thus, (Ceballos and Ehrlich 2002; Wake and population diversity is directly linked to species Freedenberg 2008). conservation. Natural ecosystems are composed of populations of various species; as such systems REFERENCES fi are disrupted or destroyed, the bene ts that Ceballos, G. and Ehrlich, P. R. (2002). Mammal population those ecosystems provide are diminished. These losses and the extinction crisis. 296 , Science 907. – ,904 bene fi ts include aesthetic values, such as the Hughes, J. B., Daily, G. C., and Ehrlich, P. R. (1997). Pop- fi rsthandexperienceofobservingabirdspecies , ulation diversity: Its extent and extinction. Science , 278 in the wild or hiking in an old growth forest. 689 – 692. ts that fi Similarly, many of the genetic bene Hughes, J. B., Daily, G. C., and Ehrlich, P. R. (1998). Pop- biodiversity confers to humanity, such as the ulation diversity and why it matters. In P. H. Raven, ed. discovery and improvement of pharmaceuticals 83. National Acade- , pp. 71 Nature and human society – and agricultural crops, are closely linked to my Press, Washington, DC. population diversity. For instance, genetically continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

198 1 183 EXTINCTIONS AND THE PRACTICE OF PREVENTING THEM (Continued) Box 10.1 Ricketts, T. H., Daily, G. C., Ehrlich, P. R., and Michener, C. D. Kremen, C., Williams, N. M., and Thorp, R. W. (2004). Economic value of tropical forest to coffee pro- (2002). Crop pollination from native bees at risk duction. Proceedings of the National Academy of Sciences fi from agricultural intensi Proceedings of cation. – 101 of the United States of America 12582. , , 12579 the National Academy of Sciences of the Wake, D. B. and Greenburg, V. T. (2008). Are we in the United States of America , 99 , midst of the sixth mass extinction? A view from the – 16812 16816. Proceedings of the National world of amphibians. Luck, G. W., Daily, G. C., and Ehrlich, P. R. (2003). Popu- , Academy of Sciences of the United States of America lation diversity and ecosystem services. Trends in Ecology – 105 11473. , 11466 18 , and Evolution – 336. , 331 group of species. So we ask fi rst: at what rate are tinkering is to keep every cog and wheel (Leopold birds becoming extinct? Then we ask: how similar 1993). So long as there is one population left, how- are other less well-known taxa? ever bleak the landscapes from which it is missing, To estimate the rate of extinctions, we calculate — there is hope. Species extinction really is forever the extinction rate as the number of extinctions per and, as we shall soon present, occurring at unprec- year per species or, to make the numbers more edented rates. reasonable, per million species-years MSY — There are also efforts to protect large-scale eco- 1995; Pimm and Brooks 2000). With (Pimm et al. systems for their intrinsic value. For example, in the exception of the past fi ve mass extinction North America, the Wildlands Project has as one of events, estimates from the fossil record suggest its objectives connecting largely mountainous re- that across many taxa, an approximate back- gions from Yellowstone National Park (roughly o N) to the northern Yukon territory (roughly ground rate is one extinction per million species- 42 o areas almost 3000 km away (Soulé and N) — 64 years, (1 E/MSY) (Pimm et al. 1995). This means we Terborgh 1999). A comparably heroic program in should observe one extinction in any sample where Africa is organized by the Peace Parks Foundation the sum of all the years over all the species under (Hanks 2003). It has already succeeded in connect- consideration is one million. If we consider a mil- ing some of the existing network of already large lion species, we should expect one extinction per national parks in southern Africa particularly year. Follow the fates of 10 000 bird species and we through transboundary agreements. These efforts should observe just one extinction per 100 years. proceed with little regard to whether they contain species at risk of extinction, but with the clear understanding that if one does maintain ecosys- 10.2.1 Pre-European extinctions tems at such scales then the species within them rst contact with modern On continents, the fi will do just fi ne. Indeed, for species that need very  humans likely occurred 15 000 years ago in the large areas tosurvive — wild dog and lion in Africa too far back to — Americas and earlier elsewhere such areas may hold the only hope for saving — allow quantitative estimates of impacts on birds. these species in the long-term. The colonization of oceanic islands happened much more recently. Europeans were not the fi rst trans-oceanic explorers. Many islands in the 10.2 How fast are species becoming Paci rst fi c and Indian Oceans received their fi extinct? human contact starting 5000 years ago and many only within the last two millennia (Stead- There are  10 000 species of birds and we know et al. 2009). man 1995; Gray their fate better than any other comparably sized © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

199 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 184 Counting the species known to have and esti- (2006) emphasize, the count of et al. As Pimm fi rst contact sug- mated to have succumbed to extinctions over a little more than 500 years has gests that between 70 and 90 endemic species an unstated assumption that science has followed were lost to human contact in the Hawaiian Is- the fates of the presently known species of bird all lands alone, from an original terrestrial avifauna over c description though fi all these years. Scienti et al. estimated to be 125 to 145 species (Pimm only began in the 1700s, increased through the 1994). Comparable numbers emerge from similar 1800s, and continues to the present. Linnaeus studies across the larger islands of the Polynesian described many species that survive to the pres- expansion (Pimm et al. 1994). One can also recre- ent and the Alagoas curassow ( ) that Mitu mitu ate the likely species composition of Paci fi c became extinct in the wild 220 years later. By  islands given what we know about how large ), contrast, the po ’ o uli ( Melamprosops phaeosoma an island must be to support a species of (say) described in 1974, survived a mere 31 years after pigeon and the geographical span of islands that its description. If one sums all the years that a pigeons are known to have colonized. Curnutt species has been known across all species, the and Pimm (2001) estimated that in addition to total is only about 1.6 million species-years and  200 terrestrial bird species taxonomists de- the the corresponding extinction rate is  85 E/MSY, scribed from the Paci c islands from complete fi per that is, slightly less than one bird extinction 1000 species fell to specimens, rst contact fi  year . This still underestimates the true extinction with the Polynesians. et al. rate for a variety of reasons (Pimm 2006). Species on other oceanic islands are likely to have suffered similar fates within the last 1500 st 10.2.3 Extinction estimates for the 21 century years. Madagascar lost 40% of its large mammals fi after rst human contact, for example (Simons Birdlife International (2006) lists 1210 bird species in various classes of risk of extinction, that com- c extinctions alone suggest one fi 1997). The Paci ” threatened, “ bined we call, for simplicity. The extinction every few years and extinctions else- critically endangered. ” most threatened class is “ where would increase that rate. An extinction every year is a hundred times higher than back- Birdlife International (2006) list 182 such species, ground (100 E/MSY) and, as we will soon including the 25 species thought likely to have show, broadly comparable to rates in the last few gone extinct but for conservation actions. For centuries. many of these species there are doubts about their continued existence. For all of these species, expert opinion expects them to become extinct with a few decades without effective conservation 10.2.2 Counting historical extinctions to protect them. Were they to expire over the next Birdlife International produces the consensus list 30 years, the extinction rate would be 5 species per of extinct birds (BirdLife International 2000) and a year or 500 E/MSY. If the nearly 1300 threatened regularly updated website (Birdlife International or data de cient species were to expire over the fi 2006). The data we now present come from Pimm next century, the average extinction rate would et al. (2006) and website downloads from that exceed 1300 E/MSY. This is an order of magni- year. In 2006, there were 154 extinct or presumed tude increase over extinctions-to-date. extinct species and 9975 bird species in total. The Such calculations suggest that species extinc-  31 E/MSY implied extinction rate is one — tion rates will now increase rapidly. Does this divides the 154 extinctions by 506 years times make sense, especially given our suggestion that 5 million species-years) on  the 9975 species ( the major process up to now, the extinction on the assumption that these are the bird extinctions islands, might slow because those species sensi- since the year 1500, when European exploration tive to human impacts have already perished? began in earnest. (They exclude species known Indeed, it does, precisely because of a rapid in- from fossils, thought to have gone before 1500.) crease in extinction on continents where there © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

200 1 EXTINCTIONS AND THE PRACTICE OF PREVENTING THEM 185 have been few recorded extinctions to date. To tion is one of the principal factors in their fully justify that, we must examine what we escaping detection so far. Second, they are also know about the global extinction process. First, certainly likely to be deemed threatened with ex- however, we consider whether these results for tinction since most new species, in addition to birds seem applicable to other taxa. being rare, live in tropical forests that are rapidly shrinking. We justify these two assumptions shortly. t know may 10.2.4 Other taxa: what we don ’ Suppose we take Dirzo and Raven s estimate at ’ make a very large difference face value. Then one would add the roughly 48 000 threatened species to the 100 000 as-yet un- Birds play an important part in this chapter be- known, but likely also threatened species, for a cause they are well-known and that allows a dee- per understanding of the processes of extinction total of 148 000 threatened species out of 400 000 than is possible with other taxa (e.g. Pimm et al. plants — or 37% of all plants. 1993). That said, birds constitute only roughly one With Peter Raven, we have been exploring s estimate is reasonable. ’ whether his and Dirzo thousandth of all species. (Technically, of eukary- It comes from what plant taxonomists think are ote species, that is excluding bacteria and viruses.) the numbers as-yet unknown. It is a best guess — Almost certainly, what we know for birds greatly and it proves hard to con fi rm. If it were roughly underestimates the numbers of extinctions of other correct, we ought to see a decline in the numbers taxa, both past and present, for a variety of reasons. On a percentage basis, a smaller fraction of because fewer — of species described each year birds are presently deemed threatened than mam- and fewer species are left undiscovered. ’ s Red- fi sh, and reptiles, according to IUCN mals, Consider birds again: Figure 10.1 shows the ”— “ the number of species de- discovery curve list (www.iucnredlist.org), or amphibians (Stuart scribed per year. It has an initial spike with Lin- et al. 2004). For North America, birds are the sec- naeus, then a severe drop (until Napoleone di ond least threatened of 18 well-known groups Buonaparte was fi nally eliminated as a threat to (The Nature Conservancy 1996). Birds may also world peace) and then a rapid expansion to about be intrinsically less vulnerable than other taxa because of their mobility, which often allows 1850. As one might expect, the numbers of new them to persist despite substantial habitat de- species then declined consistently, indicating that struction. Other explanations are anthropogenic. the supply of unknown species was drying up. That decline was not obvious, however, until a Because of the widespread and active interest good half of all the species had been described (as in birds, the recent rates of bird extinctions are far shown by the graph of the cumulative number of lower than we might expect had they not species described.) et al. received special protection (Pimm 2006; Interestingly, since 1950 there have been almost Butchart 2006). Millions are fond of birds, et al. which are major ecotourism attractions (Chapter 300 new bird species added and the numbers per 3). Many presently endangered species survive year have been more or less constant (Figure 10.1) entirely because of extraordinary and expensive Of these, about 10% were extinct when described, some found as only remains, others reassess- measures to protect them. ments of older taxonomy. Of the rest, 27% are The most serious concern is that while bird not endangered, 16% are near-threatened, 9% taxonomy is nearly complete, other taxa are far fi cient data to classify, but 48% are have insuf owering plants fl from being so well known. For threatened or already extinct. Simply, even for worldwide, 16% are deemed threatened among  300 000 already described taxonomically the well-studied birds, there is a steady trickle of (Walter and Gillett 1998). Dirzo and Raven new species each year and most are threatened. (2003) estimate that about 100 000 plant species Of course, we may never describe some bird spe- cies if their habitats are destroyed before scien- remain to be described. First, the majority of these tists fi nd them. will likely already be rare, since a local distribu- © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

201 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 186 plants being under-collected. They are a group for which international laws make their export dif fi cult, while their biology means they are fl ower when found and so must be often not in propagated. All this demands that we estimate numbers of missing taxa generally and, whenever possible, where they are likely to be. Ceballos and Ehrlich (2009) have recently ex- amined these issues for mammals, a group thought to be well-known. In fact, taxonomists described more than 400 mammal species since 1993 10% of the total. Most of these new  — species live in areas where habitats are being destroyed and over half have small geographical ranges. As we show below, the combination of these two powerful factors predicts the numbers of species on the verge of extinction. Number of bird species described per year and the Figure 10.1 10.3 Which species become extinct? et al . 2006. cumulative number of known bird species. Data from Pimm Of the bird extinctions discussed, more than 90% Now consider the implications for plants: plant have been on islands. Comparably large percen- taxonomy has rapidly increased the number of tages of extinctions of mammals, reptiles, land known species since about 1960, when modern snails, and fl owering plants have been on islands genetic techniques became available. For example, too. So, will the practice of preventing extinction  there are 30 000 species of orchids, but C. A. Luer simply be a matter of protecting insular forms? (http://openlibrary.org/a/OL631100A) and other “ The answer is an emphatic because the ” no taxonomists have described nearly 800 species from single most powerful predictor of past and likely Ecuador alone since 1995 — and there are likely future extinctions is the more general rarity ”— “ similar numbers from other species-rich tropical not island living itself. Island species are rare be- countries! There is no decline in the numbers of cause island life restricts their range. Continental new species — no peak in the discovery curve as very — species of an equivalent level of rarity there is for birds around 1850. may not have suf- — small geographical ranges Might Dirzo and Raven have seriously under- fered extinction yet, but they are disproportion- estimated the problem given that the half-way ately threatened with extinction. Quite against point for orchids might not yet have been reached? expectation, island species (and those that live in If orchids are typical, then there could be literally montane areas) are less likely to be threatened at 2 hundreds of thousands of species of as-yet un- (Figure 10.2). range sizes smaller than 100 000 km known plants. By analogy to birds, most have tiny Certainly, species on islands may be suscepti- geographical ranges, live in places that are under ble to introduced predators and other enemies, immediate threat of habitat loss, and are in immi- but they (and montane species) have an offsetting nal caveat for birds fi nent danger of extinction. The advantage. They tend to be much more abundant applies here, a fortiori. Many plants will never be locally than species with comparable range sizes described because human actions will destroy them living on continents. (and their habitats) before taxonomists fi nd them. Local rarity is a powerful predictor of threat in Well, Peter Raven (pers. comm., January 2009) its own right. While species with large ranges argues that orchids might not be typical of other tend to be locally common, there are obvious © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

202 1 187 EXTINCTIONS AND THE PRACTICE OF PREVENTING THEM 0.7 those populations that uctuate greatly from fl Lowland species Island species year-to-year (Pimm et al. 1988), likely brings po- 0.6 pulations to the very low numbers from which 0.5 they cannot recover. Given this importance of range size and local 0.4 abundance, we now turn to the geography of 0.3 species extinction. 0.2 Proportion of threatened species 0.1 10.4 Where are species becoming extinct? 0.0 10.4.1 The laws of biodiversity 100–1,000 1,001–10,000 10,001–100,000 100,001–1000,000 1,000,001–10,000,000 10,,000,001–100,000,000 to describe the ” laws “ There are at least seven e size g g raphical ran Geo geographical patterns of where species occur. By The proportion of bird species in the Americas that are Figure 10.2 “ law, ” we mean a general, widespread pattern, geographical range increases. threatened declines as the size of a species ’ that is, one found across many groups of species While more than 90% of all extinctions have been on islands, for ranges 2 and many regions of the world. Recall that Wal- less than 100 000 km likely to be , island species are presently less threatened with future extinction. Simpli ed from Manne fi et al . (1999). lace (1855) described the general patterns of evo- “ Sarawak Law ” paper. (He lution in his famous would uncover natural selection, as the mecha- — large carnivores, for example. Such exceptions nism behind those laws, a few years later, inde- species are at high risk. Manne and Pimm (2001) pendently of Darwin.) Wallace reviews the (2000) provide statistical analyses et al. and Purvis empirical patterns and then concludes: of birds and mammals, respectively, that expand ’ LAW 1. the following law may be deduced from on these issues. None of this is in any way Every species has come into these [preceding] facts: — surprising. Low total population size, whether existence coincident both in space and time with a pre- because of small range, local rarity or both, . existing closely allied species ’ exacerbated in fragmented populations and in 6000 1800 Mammals Non-passeringe birds 1600 Osscine birds 5000 Suboscine birds 1400 Amphibians 4000 1200 1000 3000 hibians p 800 Am 2000 600 Birds and mammals 400 1000 200 0 0 10000000 1000000 1000 100000 100 10000 2 ) Area (km 2 Cumulative numbers of species with increasing size of geographical range size (in km Figure 10.3 ) for amphibians (worldwide; right hand scale), and mammals and three groups of bird species (for North and South America; left hand scale). Note that area is plotted on a log scale. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

203 Conservation Biology for All Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do 188 CONSERVATION BIOLOGY FOR ALL 2 240 000 km other taxa range from  (mammals) There are other generalities, too. 2 (non-passerine birds). ranges are very small; few are to  LAW 2. Most species 570 000 km ’ LAW 3. Species with small ranges are locally scarce . very large . There is a well-established relationship across Figure 10.3 shows cumulative distributions of many geographical scales and groups of species range sizes for amphibians (worldwide) and for ’ range to its local abundance that links a species the mammals and three long-isolated lineages of (Brown 1984). The largest-scale study is that of birds in the Americas. The ranges are highly Manne and Pimm (2001) who used data on bird skewed. Certainly there are species with very species across South America (Parker 1996). et al. some greater than 10 million — large ranges 2 , for example. Range size is so strongly The latter use an informal, if familiar method to km skewed, however, that (for example) over half of “ common ” estimate local abundances. A species is all amphibian species have ranges smaller than ’ s if one is nearly guaranteed to see it in a day 2 . The comparable medians for the 6000 km  uncommon ” fi eldwork, then “ fairly common, ”“ SubOscine richness High : 85 Low : 1 SubOscine richness High : 215 Low : 1 Oscine richness High : 72 Low : 1 Oscine richness High : 142 Low : 1 Numbers of sub ‐ oscine and oscine passerine birds, showing all species (at left) and those with geographical ranges smaller than the median. Figure 10.4 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

204 1 EXTINCTIONS AND THE PRACTICE OF PREVENTING THEM 189 meaning it likely takes several down to ”— “ rare LAW 5. Species with small ranges are often geo- nd one even in the appropri- days of fi eldwork to fi ... graphically concentrated and ate habitat. Almost all bird species with ranges LAW 6 those concentrations are generally not ... 2 while ” common, are “ greater than 10 million km where the greatest numbers of species are found. nearly a third of species with ranges of less than 10 They are, however, often in the same general places 2 common. ” and very few are ” “ are “ rare 000 km in taxa with different origins. LAW 4. The number of species found in an area of Since the results on species extinction tell us given size varies greatly and according to some com- that the most vulnerable species are those with . mon factors small geographical ranges, we should explore Figure 10.4 shows the numbers of all species where such species occur. The simplest expecta- (left hand side) and of those species with smaller tion is that they will simply mirror the pattern of than the median geographic range (right hand all species. That is, where there are more species, side) for sub-oscine passerine birds (which there will be more large-ranged, medium-ranged, evolved in South America when it was geograph- and small-ranged species. Reality is strikingly ically isolated) and oscine passerines (which et al. 1994; Prendergast et al. different (Curnutt evolved elsewhere.) Several broad factors are ap- 1994)! parent, of which three seem essential (Pimm and Figure 10.4 shows that against the patterns for Brown 2004). all species, small-ranged species are geographi- cally concentrated, and not merely mirrored. Geological history Moreover, the concentrations of small-ranged The long geographical isolation of South America species are, generally, not where the greatest that ended roughly 3 million years ago allowed numbers of species are. Even more intriguing, as suboscine passerines to move into North America Figure 10.4 also shows, is that the concentrations across the newly formed Isthmus of Panama. The despite their are in similar places for the two taxa suboscines, nonetheless, have not extensively co- very different evolutionary origins . Maps of amphi- lonized North America and there are no small bians (Pimm and Jenkins 2005) and mammals ranged suboscines north of Mexico. (unpublished data) show these patterns to be general ones. At much coarser spatial resolution, Ecosystem type they mirror the patterns for plants (Myers et al. Forests hold more species than do drier or colder 2000). habitats, even when other things (latitude, for These similarities suggest common processes example) are taken into consideration. Thus, east- generate small-ranged species that are different ern North American deciduous forests hold more from species as a whole. species than the grasslands to their west, while Island effects the tropical forests of the Amazon and the south- — Likely it is that islands real ones surrounded east Atlantic coast of South America have more islands of high elevation ” montane “ by water and species than in the drier, cerrado habitats that habitat surrounded by lowlands — provide the separate them. isolation needed for species formation. Figure 10.4 shows that it is just such places where Geographical constraints small-ranged species are found. Extremes, such as high latitudes have fewer spe- so too — if less obvious — cies, but interestingly Glaciation history do peninsulas such as Baja California and Florida. This is not a complete explanation, for some et al. (2004) show there must be geo- Colwell mountains — obviously those in the western — graphical constraints by chance alone, there — do not generate unusual USA and Canada will be more species in the middle than at the numbers of small ranged species. Or perhaps extremes, given the observed distribution of geo- they once did and those species were removed graphical range sizes. by intermittent glaciation. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

205 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 190 Finally, there are simply anomalies: the Appa- lachian mountains of the eastern USA generate concentrations of small-ranged salamander spe- cies, but not birds or mammals. The mountains of western North America generate concentrations of small-ranged mammals but not birds. 10.4.2 Important consequences Several interesting consequences emerge. The species at greatest risk of extinction are con- · centrated geographically and, broadly, such species in different taxa are concentrated into the same places. As argued previously, similar processes may create similar patterns across different taxa. cance for it means fi This is of huge practical signi Threatened species that conservation efforts can be concentrated in High : 58 these special places. Moreover, priorities set for one taxonomic group may be sensible for some Low : 1 others, at least at this geographical scale. A second consequence of these laws is far more · problematical. Europe and North America have highly distorted selections of species. While most species have small ranges and are rare within them, these two continents have few species, very Figure 10.5 The number of species of birds threatened with extinction few species indeed with small ranges, and those in the Americas. ranges are not geographically concentrated. Any conservation priorities based on European and North American experiences are likely to be poor makes this region so unfortunately special is the choices when it comes to preventing extinctions, a exceptional high levels of habitat destruction. point to which we shall return. Myers approached these topics from a “ top down ” perspective, identifying 10 and later 25 areas with more than 1000 endemic plants 10.4.3 Myers ’ Hotspots et al. 2000). There are (Myers 1988, 1990; Myers important similarities in the map of these areas By design, we have taken a mechanistic approach (Figure 10.6) to the maps of Figure 10.4 (which to draw a conclusion that extinctions will concen- only consider the Americas.) Central America, trate where there are many species with small the Andes, the Caribbean, and the Atlantic — other things being equal . Other things ranges Coast forests of South America stand out in both are not equal of course and the other important maps. California and the cerrado of Brazil (drier, driver is human impact. inland forest) are important for plants, but not Figure 10.5 shows the distribution of threatened birds. species of birds in The Americas. The concentra- — and vital criterion Myers added the second tion is in the eastern coast of South America, a that these regions have less than 30% of their — place that certainly houses many species with idea is a ’ natural vegetation remaining. Myers small geographical ranges, but far from being very powerful one. It creates the number of “ the only place with such concentrations. What © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

206 1 191 EXTINCTIONS AND THE PRACTICE OF PREVENTING THEM fi ned by Myers . 2000 (in black). The map projection is by Buckminster Fuller (who called it Dymaxion). It has et al Figure 10.6 The 25 hotspots as de up and neither does the planet, of course. ” right way “ no small ranged species times habitat loss equals As for the land, oceanic inventories are likely ” extinction idea with another key and surprising very incomplete. For example, there are more insight. What surprises is that there are few ex- than 500 species of the lovely and medically im- amples of concentrations of small-ranged species . Of the 316 Conus portant genus of marine snail, that do not also meet the criterion of having lost c region, fi from the Indo-Paci Conus species of 70% of more of their natural habitat. The island of fi (1995) et al. Röckel nd that nearly 14% were New Guinea is an exception. Hotspots have dis- described in the 20 years before their publication. proportionate human impact measured in other There is no suggestion in the discovery curve that ways besides their habitat loss. Cincotta et al. the rate of description is declining. (2000) show that hotspots have generally higher rst step would be to ask whether the laws The fi human population densities and that almost all of we present apply to the oceans. We can do so using them have annual population growth rates that (2002) present geographi- et al. the data that Roberts ¼ 1.6% per annum) than the are higher (average cally on species of lobster, fi sh, molluscs, and corals. ¼ global average (1.3 per annum). Figure 10.7 shows the size of their geographical ranges, along with the comparable data for birds. Expressed as the cumulative percentages of species 10.4.4 Oceanic biodiversity with given range sizes, (not total numbers of species as Figure 10.3), the scaling relationships are remark- Concerns about the oceans are usually expressed ably similar. For all but corals, the data show that a in terms of over-exploitation of relatively wide- substantial fraction of marine species have very spread, large-bodied and so relatively rare species small geographical ranges. The spatial resolution Hydrodamalis sseacow( ’ such as Steller (Chapter 6) — about 1 degree latitude/ of these data is coarse — ) and various whale populations. That said, gigas 2 and likely overesti- —  10 000 km longitude or given what we know about extinctions on the land, mates actual ranges. Many of the species depend on wouldwelookforextinctionsintheoceans? whereelse © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

207 . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 192 100 Birds Lobsters Fishes Molluscs 80 Corals 60 40 20 Cumulative percentage of species 0 4 8 6 5 7 10 10 10 10 10 2 Ran e size (km ) g Figure 10.7 shes, molluscs, and corals) with birds for comparison (data from fi The cumulative number of species of marine organisms (lobsters, et al. 2002). Unlike Figure 10.3, these are scaled to 100% of the total number of species. Roberts coral reefs, for example, that cover only a small collide with unusually high human impacts. Given fraction of the area within the 1-degree latitude/ Conus species is incomplete, that the catalogue of longitude cell where a species might occur. that many have small geographical ranges, and The interesting generality here is that there are those occur in areas where reefs are being damaged, large fractions of marine species with very small it seems highly unlikely to us that as few as four geographical ranges — just as there are on land. 1%) are threatened with extinction < species ( Conus The exception are the corals, most of which ap- as IUCN suggest (www.iucnredlist.org). pear to occupy huge geographical ranges. Even fl here, this may be more a re ection of the state of coral taxonomy than of nature itself. 10.5 Future extinctions (2002) also show that the other laws et al. Roberts 10.5.1 Species threatened by habitat destruction apply. Species-rich places are geographically con- centrated in the oceans (Figure 10.8). They further The predominant cause of bird species endanger- show that as with the land, a small number of areas ment is habitat destruction (BirdLife International have high concentrations of species with small 2000). It is likely to be so for other taxa too. While ranges and they are often not those places with the large tracts of little changed habitat remain world- greatest number of species. Certainly, the islands ’ s natural ecosystems have wide, most of the planet between Asia and Australia have both many species been replaced or fragmented (Pimm 2001). Some and many species with small ranges. But concentra- ted from those changes, but fi species have bene tions of small range species also occur in the islands large numbers have not. The most important south of Japan, the Hawaiian Islands, and the Gulf changes are to forests, particularly tropical forests of California — areas not particularly rich in total ’ for these ecosystems house most of the world s (1998) do for reefs what et al. species. Finally, Bryant bird species (and likely other taxa as well). We and show that areas with — Myers did for the land now show that the numbers of extinctions pre- concentrations of small-ranged species are often dicted by a simple quantitative model match particularly heavily impacted by human actions. what we expect from the amount of forest lost. Were we to look for marine extinctions, it would We then extend these ideas to more recently defor- be where concentrations of small-ranged species ested areas to predict the numbers of species likely © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

208 1 EXTINCTIONS AND THE PRACTICE OF PREVENTING THEM 193 Species of Coral Reef Organisms 1251 – 1500 1001 – 1250 751 – 1000 501 – 750 251 – 500 1 – 250 et al . 2002). Species richness of coral reef organisms (data from Roberts Figure 10.8 to become extinct eventually. The observed num- Pimm and Askins (1995) considered why so bers of threatened species match those predictions, few species were lost, despite such extensive suggesting that we understand the mechanisms damage. They considered a predictive model of generating the predicted increase in extinction rate. how many species should be lost as a function of either through small range size or — Rarity the fraction of habitat lost. This model follows — does not itself cause extinction. local scarcity from the familiar species-area law that describes Rather, it is how human impacts collide with the number of species found on islands in relation such susceptibilities. As Myers reminds us, ex- to island area. There is an obvious extension to tinctions will concentrate where human actions that law that posits that as area is reduced (from ) then the original number of species S to A impact concentrations of small ranged species. A n o o in a characteristic way. will shrink to S Without such concentrations, human impacts n ) remaining /S LAW 7. The fraction of species (S will have relatively little effect. The eastern USA n o when human actions reduce the area of original habitat provides a case history. 0.25 to A . ) /A is (A A o n n o We call this a law because we now show it to hold across a variety of circumstances. 10.5.2 Eastern North America: high impact, First, Pimm and Askins noticed that while few few endemics, few extinctions forests were uncut, the deforestation was not si- multaneous. European colonists cleared forests Europeans settled Eastern North America in the along the eastern seaboard, then moved across early 1600s and moved inland from the mid- the Appalachians and then into the lake states. 1700s, settling the prairie states in the late 1800s. When settlers realized they could grow crops in Along the way, they cleared most of the decidu- the prairies, the eastern forests began to recover. ous forest at one time or another. Despite this At the low point, perhaps half of the forest re- massive deforestation, only four species of land mained. Applying the formula, the region should the Carolina parakeet — birds became extinct have retained 84% of its species and so lost 16%. ), passenger pigeon ( Conuropsis carolinensis Ecto- ( 26 species and that is  Now 16% of 160 species is pistes migratorius ), ivory-billed woodpecker ( Cam- clearly not the right answer. ’ s warbler pephilus principalis ), and Bachman Second, Pimm and Askins posed the obvious ( — Vermivora bachmanii ) out of a total of about thought-experiment: how many species should 160 forest species. © Oxford University Press 2010. All rights reserved. For permissions please email: acad[email protected]

209 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 194 CONSERVATION BIOLOGY FOR ALL have been lost if all the forest was cleared? The endemic bird species, original area, and the pres- answer is not 160, because most of those species ent area of remaining natural vegetation. This have ranges outside of eastern North America — provides a best-case scenario of what habitat some across the forests of Canada, others in the 1700 species  might remain. They predicted that western USA, some down into Mexico. They of birds should be lost eventually. Species can would survive elsewhere, even if all the forest obviously linger in small habitat fragments for fi ciently were cut. Indeed only 30 species have suf decades before they expire as evidenced by — small ranges to be endemic to the region and so at the rediscovery of species thought extinct for up risk if all the forest were lost. Applying the for- to a century. They suggest that bird extinctions mulae to these one predicts that there would be  among doomed species have a half-life of 50 — 4.8 species at risk surprisingly close to the right 1999b; Ferraz years (Brooks 2003). So et al. et al. answer, given that another eastern species, the 1250 — — perhaps three quarters of these species red-cockaded woodpecker ( ), is Picoides borealis will likely go extinct this century a number — threatened with extinction! very similar to the number Birdlife considers to Simply, that there were so few extinctions — be at risk. and so few species at risk is largely a conse- — 1000 E/ These estimates of extinction rates (  quence of there being so few species with small MSY) come from human actions to date. Two ex- ranges. So what happens when there are many trapolations are possible. The worst-case scenario species with small ranges? for the hotspots assumes that the only habitats that will remain intact will be the areas currently pro- tected. This increases the prediction of number of 10.5.3 Tropical areas with high impact, many extinctions to 2200 (Pimm and Raven 2000). The endemics, and many species at risk second adds in species from areas not already Case histories comparing how many species are extensively deforested. If present trends continue, threatened with extinction with how many are large remaining areas of tropical forest that house predicted to become extinct using Law 7 include many species (such as the Amazon, the Congo, and Fly basin of New Guinea) will have extinction birds in the Atlantic coast forest of Brazil (Brooks rates that exceed those in the hotspots by mid- and Balmford 1996), birds and mammals in insu- century. For example, the Amazon basin is often lar southeast Asia (Brooks et al. 1997; Brooks et al. ignored as a concentration of vulnerable species 1999a), plants, invertebrates, and vertebrates of because its 300 endemic bird species are found  Singapore (Brook et al. 2003), and birds, mam- 2 . At current rates of defores- mals, amphibians, reptiles, and plants across the 5 million km  across tation, most of the Amazon will be gone by 25 biodiversity that we now introduce. ” hotspots “ mid-century. There are plans for infrastructure These studies, by choice, look at areas where development that would accelerate that rate of there are many species with small geographical et al. 2001). If this were forest clearing (Laurance ranges, for the number of predicted extinctions to happen, then many of the Amazon sspecies ’ depends linearly on the number of such species. will become threatened or go extinct. But notice that Law 7 implies a highly non-linear relationship to the amount of habitat destruction. rst half of eastern North America fi s Losing the ’ 10.5.4 Unexpected causes of extinction forests resulted in a predicted loss of 16% of its There are various unexpected causes of extinction species. Losing the remaining half would have and they will add to the totals suggested from exterminated the remaining 84%! The studies habitat destruction. The accidental introduction the previous paragraph cites looked at areas of the brown tree snake ( Boiga irregularis) to with far more extensive habitat destruction than s birds in a couple ’ Guam eliminated the island eastern North America. et al. 2003). In the of decades (Savidge 1987; Wiles Pimm and Raven (2000) applied this recipe to oceans, increases in long-line fi sheries (Tuck et al. each of the 25 hotspots using the statistics on © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

210 1 195 EXTINCTIONS AND THE PRACTICE OF PREVENTING THEM 2003) are a relatively new and very serious threat certainly provide predictions of which species to three-quarters of the 21 albatross species (Bird- 2008), but the et al. are at most risk (Sekercioglu life International 2006). basic concerns are clear. If that fraction of species in mountains is typical of other taxa and other places, then a quarter of those species are at risk 10.5.5 Global change and extinction — a very substantial addition to species already threatened with extinction (Pimm 2008). cant factors in the fi Finally, one of the most signi extinction of species will undoubtedly be climate change (see Chapter 8), a factor not included in any of the estimates presented above. Thomas 10.6 How does all this help prevent (2004) estimate that climate change threatens et al. extinctions? 37% of species within the next 50 years de- – 15 Thus far, we have guided the reader to areas of pending on which climate scenario unfolds. Even 2 many orders of mag- — roughly one million km more species are at risk if one looks to climate nitude larger than the tens or at best hundreds of changes beyond 50 years. More detailed, regional 2 at which practical conservation actions un- km modeling exercises in Australia (Williams et al. fold. Brooks (Chapter 11) considers formal tools 2003) and South Africa (Erasmus 2002) et al. for setting more local conservation priorities. We have led to predictions of the extinction of many have rarely used such approaches in our work, species with narrowly-restricted ranges during though we understand the need for them. this or longer intervals. This chapter establishes a recipe for conserva- The critical question is whether these extinc- tion action that transcends scales. One can quite tions, which are predominantly of small-ranged literally zoom in on Figure 10.5 to nd out exactly fi species, are the same as those predicted from where the greatest concentrations of threatened habitat destruction or whether they are addition- species are and, moreover, plot their ranges on al (Pimm 2008). In many cases, they are certainly maps of remaining forest. Our experiences are the latter. shaped by two places where our operational For example, the Atlantic coast humid forests arm, www.savingspecies.org, has worked to of Brazil have the greatest numbers of bird spe- date: the Atlantic Coastal Forest of Brazil and cies at risk of extinction within the Americas the island of Madagascar. et al. (Manne 1999). The current threat comes We have told this story in detail elsewhere from the extensive clearing of lowland forest. (Harris 2005; Jenkins 2003; Pimm and Jen- et al. Upland forests have suffered less. Rio de Janeiro kins 2005; Jenkins and Pimm 2006). For the Amer- — State has retained relatively more of its forests icas, we start with the species map of Figure 10.5 < 23% survives compared to 10% for the region as (but much enlarged). This shows the very highest a whole. Less than 10% of the forest below 200 m concentration of threatened species to be in the remains though, whereas some 84% of the forest 2 . — State of Rio de Janeiro 40 000 km  an area of remains above 1300 m. It is precisely the species At that point, what compels us most strongly is in these upper elevations that are at risk from satellite imagery that shows what forest remains global warming, for they have no higher eleva- not ever more detail about where species are — tions into which to move when the climate and very little — found. There is not much forest warms. These upland, restricted-range species indeed of the lowland forest remains. And that will suffer the greatest risk from global warming, forest is in fragments. not the lowland species that are already at risk. Whatever conservation we do here is driven by Thus, the effects of direct habitat destruction and these facts. We do not worry about the issues of global warming are likely to be additive. capturing as many species in a given area (Pimm How large an additional threat is global warm- and Lawton 1998), and then write philosophical ing? For New World passerine birds, a quarter live papers about weighting species because of their 1000 m above sea-level. Detailed modeling can © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

211 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 196 CONSERVATION BIOLOGY FOR ALL Manne, L. L, Brooks, T. M., and Pimm S. L. (1999). Relative various ”— taxonomic distinctiveness, values “ risk of extinction of passerine birds on continents and for example. We do not fret about whether our , 258 – 261. 399 , islands. Nature priorities for birds match those for orchids for Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonseca, which we have only crude range information G. A. B., and Kent, J. (2000). Biodiversity hotspots for (Pimm 1996) or nematodes about which we 403 , conservation priorities. 858. – , 853 Nature know even less. What few remaining fragments Pimm S. L. (2001). The World According to Pimm: A Scientist remain will be the priorities for every taxon. Audits the Earth – Hill, New York, NY. . McGraw The practical solution is obvious too. The land Pimm, S. L. and Askins, R. (1995). Forest losses predict bird between isolated forests needs to be brought into extinctions in eastern North America. Proceedings of the protection and reforested. That is exactly what we National Academy of Sciences of the United States of America , have helped our Brazilian colleagues achieve – , 9343 92 9347. Pimm, S. L. and C. Jenkins. (2005). Sustaining the variety of (www.micoleao.org.br). Connecting isolated for- Scienti , Life. 73. fi c American – September ,66 est fragments by reforesting them in areas rich in small-ranged species is an effective and cheap way of preventing extinctions. We commend this solution to others. Relevant web sites /www.birdlife. BirdLife International, Data Zone: http:/ · Summary org/datazone. /www.globalamphi- Threatened amphibians: http:/ Extinctions are irreversible, unlike many other · · bians.org. environmental threats that we can reverse. The IUCN Red List: http:/ /www.iucnredlist.org. Current and recent rates of extinction are 100 · · Saving species: http:/ /savingspecies.org. times faster than the background rate, while future · rates may be 1000 times faster. Species most likely to face extinction are rare; rare · either because they have very small geographic ranges or have a low population density with a larger range. REFERENCES Small-ranged terrestrial vertebrate species tend to · . Threatened Birds of the World BirdLife International (2000). be concentrated in a few areas that often do not hold LynxEdicions and BirdLife International, Cambridge, UK. the greatest number of species. Similar patterns Birdlife web site (2006). http:/ /www.birdlife.org. apply to plants and many marine groups. Brook, B. W., Sodhi, N. S., and Ng, P. K. L. (2003). Cata- Extinctions occur most often when human impacts strophic extinctions follow deforestation in Singapore. · collide with the places having many rare species. – , 420 424 , Nature 423. While habitat loss is the leading cause of extinc- Brooks, T. and Balmford, A. (1996). Atlantic forest extinc- · tions, , 115. Nature , 380 tions, global warming is expected to cause extinc- Brooks, T. M., Pimm, S. L., and Collar, N. J. (1997). Defor- tions that are additive to those caused by habitat loss. estation predicts the number of threatened birds in insu- Conservation Biology 384. – , 382 11 , lar southeast Asia. Brooks, T. M., Pimm, S. L., Kapos V., and Ravilious Suggested reading C. (1999a). Threat from deforestation to montane and lowland birds and mammals in insular Southeast Asia. Brooks, T. M., Pimm, S. L., and Oyugi. J. O. (1999). Time 68 – , 1078. Journal of Animal Ecology , 1061 Lag between deforestation and bird extinction in tropical Brooks, T. M., Pimm, S. L., and Oyugi. J. O. (1999b). Time 13 , Conservation Biology forest fragments. 1150. – , 1140 lag between deforestation and bird extinction in tropical Ferraz, G., Russell, G. J., Stouffer, P C., Bierregaard, R. O., 1150. – Conservation Biology forest fragments. , 1140 , 13 Pimm, S. L., and Lovejoy, T. E. (2003). Rates of species Brown, J. H. (1984). On the relationship between abun- Proceedings of the loss from Amazonian forest fragments. dance and distribution of species. The American Natural- , National Academy of Sciences of the United States of America , 124 , 255 – 279. ist 14073. 100 , 14069 – © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

212 1 197 EXTINCTIONS AND THE PRACTICE OF PREVENTING THEM Janeiro. Chapter in Índice de Qualidade dos Municípios Bryant, D., Burke, L., McManus, J., and Spalding, M. (1998). Verde II. Fundação CIDE, 2003, Rio de Janeiro, Brazil. – s cator of the threats to the world ’ Reefs at risk: a map-based indi nindo Prioridades fi Jenkins, C. N. and Pimm S.L. (2006). De . Joint publication by World Resources Institute, coral reefs de Conservação em um Hotspot de Biodiversidade International Center for Livi ng Aquatic Resources Manage- ning conservation priorities in a global bio- fi Global (De ment, World Conservation Monitoring Centre, and United diversity hotspot). Chapter in Biologia da Conservação: Nations Environment Programme, Washington, DC. Essências. RiMa Editora, São Carlos, SP. Rocha, C.F.D.; Butchart S. H. M, Statters fi eld A, and Collar, N. (2006). H.G. Bergallo; M. Van Sluys & M.A.S. Alves. (Orgs.). Oryx How many bird extinctions have we prevented? , Laurance, W. F., Cochrane, M. A., Bergen, S., Fearnside, 278. – 40 , 266 Angelo, S., and P. M., Delamonica, P., Barber, C., D ’ Ceballos, G and Ehrlich, P. R. (2009). Discoveries of new Fernandes, T. (2001). The future of the Brazilian Ama- mammal species and their implications for conservation , 438 , Science zon. 291 439. – and ecosystem services. Proceedings of the National Academy Leopold, A. (1993). . Oxford University Press, Round River of Sciences of the United States of America 3846. – , 106 , 3841 Oxford, UK. Cincotta, R. P., Wisnewski, J., and Engelman, R. (2000). Manne, L. L. and Pimm, S. L. (2001). Beyond eight forms of Nature Human population in the biodiversity hotspots. rarity: which species are threatened and which will be , 990 – 404 992. , 221 – , Animal Conservation next? 230. 4 Colwell, R. K., Rahbek, C., and Gotelli, N. J. (2004). The mid- Manne, L. L, Brooks, T. M., and Pimm S. L. (1999). Relative domain effect and species richness patterns: what have risk of extinction of passerine birds on continents and we learned so far? The American Naturalist , 163 ,E1 – E23. islands. Nature , 399 , 258 – 261. Curnutt, J. and Pimm S. L. (2001). How many bird species Myers, N. (1988). Threatened biotas: hotspots ’ in tropical ‘ c before fi i and the Central Paci ’ in Hawai rst contact? In fi – 20. ,1 8 forests. , The Environmentalist J. M. Scott, S. Conant and C. van Riper III, eds Evolution, Myers, N. (1990). The biodiversity challenge: expanded ecology, conservation, and management of Hawaiian birds: a 10 , 243. hotspots analysis. , The Environmentalist 30. Studies in Avian Biology – , pp. 15 vanishing avifauna Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonseca, 22, Allen Press Inc., Lawrence, KS. G. A. B., and Kent, J. (2000). Biodiversity hotspots for Curnutt, J., Lockwood, J., Luh, H.-K., Nott, P., and Russell, 403 Nature 858. conservation priorities. , 853 – , Nature G. (1994). Hotspots and species diversity. , 326. 367 Science and the National Research Council (1995). Dirzo R. and Raven P. (2003). Global state of biodiversity Endangered Species Act . National Academy Press, Wa- loss. Annual Reviews in Environment and Resources , 28 , 137 – 167. shington, DC. Erasmus, B. F. N., van Jaarsveld, A. S., Chown, S. L., Norse, E. A. and McManus, R. E. (1980). Ecology and living Kshatriya, M., and Wessels, K. (2002). Vulnerability of Environmental quality resources: biological diversity. In Global South African animal taxa to climate change. 1980: the eleventh annual report of the Council on Environ- , Change Biology 8 , 679 – 693. mental Quality , pp. 31 80. Council on Environmental – Ferraz, G., Russell, G. J., Stouffer, P. C., Bierregaard, R. O., Quality, Washington, DC. Pimm, S. L., and Lovejoy, T. E. (2003). Rates of species Parker, T. A., III., Stotz, D. F., and Fitzpatrick, J. W. (1996). loss from Amazonian forest fragments. Proceedings of the Ecological and distributional databases for neotropical National Academy of Sciences of the United States of America , birds. In D. F. Stotz, T. A. Parker, J. W. Fitzpatrick and 100 , 14069 14073. – D. Moskovits, eds Neotropical birds: ecology and conserva- Gray, R.D., Drummond, A. J., and Greenhill, S. J. (2009). tion , pp.113-436. University of Chicago Press, Chicago, IL. Language phylogenies reveal expansion pulses and Pimm, S. L. (1996). Lessons from a kill. Biodiversity and Science pauses in Paci fi c Settlment. , 5 Conservation 1067. , 1059 – , – , 479 323 483. Oikos 90 6. – ,3 Pimm, S. L. (2000). Biodiversity is us. , Hanks, J. (2003). Transfrontier Conservation Areas (TFCAs) Pimm S. L. (2001). The World According to Pimm: A Scientist in Southern Africa: their role in conserving biodiversity, Audits the Earth . McGraw – Hill, New York, NY. socioeconomic development and promoting a culture of Pimm, S. L. (2008). Biodiversity: climate change or habitat 17 ,121 – 142. Journal of Sustainable Forestry , peace. Current Biology , 18 , which will kill more species? loss — Harris, G. M., Jenkins, C. N., and Pimm, S. L. (2005). 117 – 119. Conserva- Re fi ning biodiversity conservation priorities. Pimm, S. L. and Askins, R. (1995). Forest losses predict bird tion Biology , 1968. , 1957 – 19 extinctions in eastern North America. Proceedings of the Jenkins, C. N. (2003). Importância dos remanescentes de , National Academy of Sciences of the United States of America Mata Atlântica e dos corredores ecológicos para a pre- 92 – 9347. , 9343 servação e recuperação da avifauna do estado do Rio de © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

213 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 198 Savidge, J. A. (1987). Extinction of an island forest avifauna Pimm, S. L. and Brooks, T. M. (2000). The Sixth Extinction: Ecology by an introduced snake. , 68 , 660 – 668. Nature How large, how soon, and where? In P. Raven, ed. Sekercioglu, C. H., Schneider, S. H., Fay, J. P., and Loarie, and Human Society: the quest for a sustainable world , S. R. (2008). Climate change, elevational range shifts, and – pp. 46 62. National Academy Press, Washington, DC. – 150. , 22 , 140 Conservation Biology bird extinctions. Pimm, S. L. and Brown, J. H. (2004). Domains of diversity. Simons E. L. (1997). Lemurs: old and new. In S. M. Good- Science 304 , 831 – 833. , man and B. D. Patterson, eds Natural change and human Pimm, S. L. and C. Jenkins. (2005). Sustaining the variety of – impact in Madagascar 156. Smithsonian Institu- , pp. 142 – ,66 Life. Scienti 73. c American , September fi tion Press, Washington, DC. Pimm, S. L. and Lawton. J. H. (1998). Planning for biodi- Continental Soulé, M. E. and Terborgh, J., eds (1999). versity. Science 2069. , 279 , 2068 – Conservation: Scienti fi c Foundations of Regional Reserve Pimm, S. L. and Raven, P. (2000). Extinction by numbers. . Island Press, Washington, DC. Networks , 843 – Nature 403 845. Steadman D. W. (1995). Prehistoric extinctions of Paci fi c Pimm, S. L., Jones, H. L., and J. M. Diamond. (1988). On island birds: biodiversity meets zooarcheology. Science , The American Naturalist the risk of extinction. 132 , , 267 – 1131. , 1123 785. 757 – Stuart S. N., Chanson J. S., Cox N. A., et al. (2004). Status Pimm, S. L., Diamond, J., Reed, T. R., Russell, G. J., and and trends of amphibian declines and extinctions world- Verner, J. (1993). Times to extinction for small popula- wide. Science 306 , 1783 – 1786. tions of large birds. Proceedings of the National Academy of TNC Priorities for The Nature Conservancy (1996). , 10871 Sciences of the United States of America – 90 10875. , Conservation: 1996 Annual Report Card for U.S. Plant Pimm, S. L., Moulton M. P., and Justice J. (1994). Bird . The Nature Conservancy, Arlington, and Animal Species fi c. Philosophical Transac- extinctions in the central Paci VA. ,27 33. 344 , tions of the Royal Society B – (2004). et al. Thomas, C. D., Cameron, A., and Green, R. E., Pimm, S. L., Raven, P., Peterson, A., Sekercioglu, C. H., and Extinction risk from climate change. 427 Nature , 145 148. – Ehrlich P. R. (2006). Human impacts on the rates of Tuck G. N., Polacheck T., and Bulman C. M. (2003). Spatio- Proceedings recent, present, and future bird extinctions. shing effort in the Southern fi temporal trends of longline of the National Academy of Sciences of the United States of Biological Ocean and implications for seabird bycatch. America , 103 , 10941 – 10946. Conservation 114 27. – ,1 , Pimm, S. L., Russell, G. J., Gittleman, J. L., and Brooks T. M. Wallace, A. R. (1855). On the law which has regulated the , 347 Science , (1995). The future of biodiversity. 350. – 269 Annals and Magazine of Nat- introduction of new species. Prendergast, J. R., Quinn, R. M., Lawton, J. H., Eversham, ural History , September 1855. B. C., and Gibbons, D. W. (1994). Rare species, the coin- Walter K. S. and Gillett H. J., eds (1998). 1997 IUCN Red List cidence of diversity hotspots and conservation strate- of Threatened Plants 365 , Nature gies. 337. , 335 – . IUCN, Gland, Switzerland. Purvis, A., Gittleman, J. L., Cowlishaw, G., and Mace, Wiles G. J., Bart J., Beck R. E., and Aguon C. F. (2003). G. (2000). Predicting extinction risk in declining species. Impacts of the brown tree snake: patterns of decline Proceedings of the Royal Society of London B 267 , ,1947 s avifauna. Conservation ’ and species persistence in Guam – 1952. , 1350 – 1360. Biology , 17 (2002). Roberts C. M., McClean, C. J., Veron, J. E., et al. Williams, S. E., Bolitho, E. E., and Fox, S. (2003). Climate Marine biodiversity hotspots and conservation priorities change in Australian tropical rainforests: an impending for tropical reefs. Science 1284. – , 1280 295 Proceedings of the Royal Socie- environmental catastrophe Röckel, D., Korn, W., and Kohn A. J. (1995). Manual of the – 1892. , 1887 270 ., ty of London B , Vol 1. Springer-Verlage, New York, NY. Living Conidae © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

214 1 CHAPTER 11 Conservation planning and priorities Thomas Brooks Maybe the fi rst law of conservation science should and irreplaceability. It does not attempt to be which of course drives be that human population — comprehensive, but rather focuses on the bound- both threats to biodiversity and its conservation is — ary between theory and practice, where successful distributed unevenly around the world (Cincotta conservation implementation has been explicitly fi 2000). This parallels a better-known et al. rst law ’ planned from the discipline s conceptual frame- of biodiversity science, that biodiversity itself is also work of vulnerability and irreplaceability. In distributed unevenly (Gaston 2000; Chapter 2). other words, the work covered here has success- Were it not for these two patterns, conservation fully bridged the ” “ research – implementation gap would not need to be planned or prioritized. A (Knight 2008). The chapter is structured by et al. conservation investment in one place would have scale. Its rst half addresses global scale planning, fi the same effects as that in another. As it is, though, which has attracted a disproportionate share of the contribution of a given conservation investment “ hot- the literature since Myers ’ (1988) pioneering towards reducing biodiversity loss varies enor- treatise. The remainder of the chapter ” spots mously over space. This recognition has led to the tackles conservation planning and prioritization emergence of the sub-discipline of systematic con- on the ground (and in the water). This in turn is servation planning within conservation biology. organized according to three levels of increasing Systematic conservation planning now dates ecological and geographic organization: from spe- back a quarter-century to its earliest contributions cies, through sites, to seascapes and landscapes. (Kirkpatrick 1983). A seminal review by Margules and Pressey (2000) established a fi rm conceptual 11.1 Global biodiversity conservation framework for the sub-discipline, parameterized planning and priorities along axes derived from the two aforementioned — many people Most conservation is parochial laws. Variation in threats to biodiversity (and re- care most about what is in their own backyard sponses to these) can be measured as vulnerability (Hunter and Hutchinson 1994). As a result, (Pressey and Taffs 2001), or, put another way, the  maybe 90% of the US$6 billion global conserva- breadth of options available over time to conserve a tion budget originates in, and is spent in, econom- given biodiversity feature before it is lost. Mean- 1999). et al. ically wealthy countries (James while, the uneven distribu tion of biodiversity can Fortunately, this still leaves hundreds of millions 1994), be measured as irreplaceability (Pressey et al. exible conservation invest- fl of dollars of globally the extent of spatial options available for the conser- ment that can theoretically be channeled to wher- vation of a given biodiversity feature. An alternative ever would deliver the greatest bene t. The bulk fi the measure of irreplaceability is complementarity — of these resources are invested through multilat- degree to which the biodiversity value of a given eral agencies [in particular, the Global Environ- area adds to the value of an overall network of areas. ment Facility (GEF) (www.gefweb.org)], bilateral This chapter charts the history, state, and pro- donors, and non-governmental organizations. spects of conservation planning and prioritiza- Where should they be targeted? tion, framed through the lens of vulnerability 199 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

215 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 200 cation recognizes Wilson ’ s (2005) classi fi et al. fi 11.1.1 History and state of the eld four types of vulnerability measures: environ- Over the last two decades, nine major templates mental and spatial variables, land tenure, of global terrestrial conservation priorities have threatened species, and expert opinion. All ve fi been developed by conservation organizations, to of the global prioritization templates that guide their own efforts and attract further atten- incorporated vulnerability did so using the fi rst 2006). tion (Figure 11.1 and Plate 9; Brooks et al. cally habitat extent. fi of these measures, speci Brooks (2006) showed that all nine templates et al. Four of these utilized proportionate habitat loss, fi t into the vulnerability/irreplaceability frame- which is useful as a measure of vulnerability work, although in a variety of ways (Figure 11.2 because of the consistent relationship between and Plate 10). Speci fi cally, two of the templates the number of species in an area and the size of reac- “ prioritize regions of high vulnerability, as 2002). However, it is an et al. that area (Brooks , while three prioritized regions ” tive approaches fi imperfect metric, because it is dif cult to assess in . of low vulnerability, as proactive approaches “ ” xeric and aquatic systems, it ignores threats such The remaining four are silent regarding vulnera- as invasive species and hunting, and it is retro- bility. Meanwhile, six of the templates prioritize spective rather than predictive (Wilson et al. regions of high irreplaceability; the remain- “ frontier forests ” approach (Bryant 2005). The ing three do not incorporate irreplaceability. 1997) uses absolute forest cover as a et al. To understand these global priority-setting measure, although this is only dubiously re fl ec- approaches, it is important to examine the metrics tive of vulnerability (Innes and Er 2002). Beyond of vulnerability and irreplaceability that they habitat loss, one template also incorporates land use, and the spatial units among which they pri- tenure, as protected area coverage (Hoekstra et al. oritize. 2005), and two incorporate human population BH CE EBA G200 MC CPD FF HBWA LW Figure 11.1 . 2006): CE, crisis ecoregions (Hoekstra Maps of the nine global biodiversity conservation priority templates (reprinted from Brooks et al et al eld et al . 1998); CPD, centers of plant diversity fi . 2004); EBA, endemic bird areas (Statters et al . 2005); BH, biodiversity hotspots (Mittermeier (WWF and IUCN 1994 – 7); MC, megadiversity countries (Mittermeier et al . 1997); G200, global 200 ecoregions (Olson and Dinerstein 1998); HBWA, biodiversity wilderness areas (Mittermeier high ‐ . 2002a). et al . 1997); and LW, last of the wild (Sanderson et al . 2003); FF, frontier forests (Bryant et al With permission from AAAS (American Association for the Advancement of Science). © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

216 1 CONSERVATION PLANNING AND PRIORITIES 201 B A Proactive Reactive Proactive Reactive EBA, CPD BH HBWA MC, G200 FF CE Irreplaceability LW y Vulnerabilit Global biodiversity conservation priority templates placed within the conceptual framework of irreplaceability and vulnerability (reprinted Figure 11.2 et al . 2006). Template names follow the Figure 11.1 legend. (A) Purely reactive (prioritizing high vulnerability) and purely proactive from Brooks (prioritizing low vulnerability) approaches. (B) Approaches that do not incorporate vulnerability as a criterion (all prioritize high irreplacea bility). With permission from AAAS (American Association for the Advancement of Science). et al. et al. 2003; Sanderson density (Mittermeier ned a posteriori from the dis- fi one using regions de 2002a). tributions of restricted-range bird species (Statters- The most common measure of irreplaceability 1998), and the other seven using units like fi eld et al. is plant endemism, used by four of the templates, “ apriori ned fi ,de ” 2001). et al. (Olson ecoregions fth (Statters 1998) using bird with a fi fi eld et al. This latter approach brings ecological relevance, endemism. The logic behind this is that the more but also raises problems because ecoregions vary endemic species in a region, the more biodiversity in size, and because they themselves have no re- ’ s habitat is lost (although, strict- lost if the region peatable basis (Jepson and Whittaker 2002). The use ly, any location with even one endemic species is of equal area grid cells would circumvent these irreplaceable). Data limitations have restricted problems, but limitations on biodiversity data com- the plant endemism metrics to specialist opinion pilation so far have prevented their general use. estimates, and while this precludes replication or Encouragingly, some initial studies (Figure 11.3) formal calculation of irreplaceability (Brummitt et al. for terrestrial vertebrates (Rodrigues 2004b) and Lughadha 2003), subsequent tests have 2004) show et al. and, regionally, for plants (Küper found these estimates accurate (Krupnick and considerable correspondence with many of the Kress 2003). Olson and Dinerstein (1998) added et al. templates (da Fonseca 2000). taxonomic uniqueness, unusual phenomena, and ts of global fi What have been the costs and bene global rarity of major habitat types as measures of priority-setting? The costs can be estimated to lie in irreplaceability, although with little quanti ca- fi the low millions of dollars, mainly in the form of tion. Although species richness is popularly but fi staff time. The bene ts are hard to measure, but erroneously assumed to be important in prioriti- large. The most tractable metric, publication impact, 2005), none of the approaches et al. zation (Orme (2000), the benchmark paper reveals that Myers et al. relies on this. This is because species richness is on hotspots, was the single most cited paper in driven by common, widespread species, and so the ISI Essential Science Indicators category “ Envi- misses exactly those species most in need of con- for the decade preceding ” ronment/Ecology servation ( Jetz and Rahbek 2002). 2005. Much more important is the impact that One of the priority templates uses countries as its these prioritization templates have had on resource spatial unit (Mittermeier 1997). The remaining et al. allocation. Myers (2003) estimated that over the pre- eight utilize spatial units based on biogeography, ceding 15 years, the hotspots concept had focused © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

217 . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 202 . 2006). Global conservation setting (reprinted from Brooks ‐ data in global conservation priority Incorporating primary biodiversity Figure 11.3 et al prioritization templates h cation and specialist opinion, rather than primary biodiversity data. Such fi ave been based almost exclusively on bioregional classi rella of the IUCN Species Survival Commi ssion (IUCN 2007), and they allow pro gressive primary datasets have recently started to become available under the umb nement of templates. (A) Global gap analysis of coverage of 11 633 mammal, bird, turtle, and amphibian species ( testing and re fi 40% of terrestrial  vertebrates) in protected areas (Rodrigues neously by irreplaceability values of at degree grid cells characterized simulta ‐ . 2004a). It shows unprotected half et al least 0.9 on a scale of 0 1, and of the top 5% of values of an extinction risk indicator based on the presence of globally threatened species (Rodrigues – et al . 2004b). (B) Priorities for the conservation of 6269 African plant species (  2% of vascular plants) across a 1 ‐ degree grid (Küper . 2004). These are the 125 et al grid cells with the highest product of range size rarity (a surrogate for irreplaceability) of plant species distributions and mean human footprint (Sanderson ‐ et al . 2002a). Comparison of these two maps, and between them and Fig. 11.2, revea ls a striking similarity among conserva tion priorities for vertebrates an dthosefor plants, in Africa. First, it remains unclear the degree to which exible conservation US$750 million of globally fl ect prio- priorities set using data for one taxon re fl resources. Entire funding mechanisms have been rities for others, and, by extension, whether prio- fl ect global prioritization, such as established to re rities for well-known taxa like vertebrates and the US$150 million Critical Ecosystem Partnership plants re ect those for the poorly-known, mega- fl Fund (www.cepf.net) and the US$100 million Glob- diverse invertebrates, which comprise the bulk al Conservation Fund (web.conservation.org/xp/ of life on earth. Lamoreux (2006), for exam- et al. gef); and the ideas have been incorporated into the ple, found high congruence between conserva- Resource Allocation Framework of the Global Envi- tion priorities for terrestrial vertebrate species. ronment Facility, the largest conservation donor. et al. In contrast, Grenyer (2006) reported low congruence between conservation priorities for 11.1.2 Current challenges and future directions mammals, birds, and amphibians. However, this result was due to exclusion of unoccupied cells; Six major research fronts can be identi fi ed for the when this systematic bias is corrected, the same assessment of global biodiversity conservation data actually show remarkably high congruence 2006). et al. 2000; Brooks et al. priorities (Mace © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

218 1 CONSERVATION PLANNING AND PRIORITIES 203 25 Cross–taxon Environmental 20 15 10 Percentage of tests 5 0 –0.6 0.4 0 0.6 0.5 –0.5 –0.4 –0.3 –0.2 –0.1 0.3 0.2 0.1 1.0 0.9 0.8 0.7 SAI ) Species accumulation index ( Figure 11.4 Frequency distribution of values of a species accumulation index (SAI) of surrogate effectiveness for comparison between tests on terrestrial cross ‐ taxon and on environmental surrogates; the SAI has a maximum value of 1 (perfect surrogacy), and indicates random surrogacy when it has a value of 0, and surrogacy worse than random when it is negative (reprinted from Rodrigues and Brooks 2007). (Rodrigues 2007). More generally, a recent review North Sea) (see also Box 4.3). While much work found that positive (although rarely perfect) sur- remains in marine conservation prioritization, rogacy is the norm for conservation priorities and that for freshwater biodiversity has barely between different taxa; in contrast, environmental even begun, these early signs suggest that there surrogates rarely function better than random (Fig- may be some geographic similarity in conserva- ure 11.4 and Plate X; Rodrigues and Brooks 2007). tion priorities even between biomes. While surrogacy may be positive within Another open question is the extent to which biomes, none of the conservation prioritization conservation priorities represent not just current templates to date have considered freshwater or diversity but also evolutionary history. For marine biodiversity, and at face value one might et al. primates and carnivores globally, Sechrest expect that conservation priorities in aquatic sys- (2002) showed that biodiversity hotspots hold a tems would be very different from those on land disproportionate concentration of phylogenetic (Reid 1998). Remarkably, two major studies from diversity, with the ancient lineages of Madagascar the marine environment suggest that there may a key driver ofthisresult(Spathelf and Waite 2007). in fact be some congruence between conservation fi (2007) claimed to et al. By contrast, Forest nd that et al. priorities on land and those at sea. Roberts incorporating botanical evolutionary history for (2002), found that 80% of their coral hotspots, the plants of the Cape Floristic hotspot substantial- although restricted to shallow tropical reef sys- ly altered the locations of conservation priorities. tems, were adjacent to Myers et al. (2000) terres- et al. Using simulations, Rodrigues (2005) argued (2008) trial hotspots. More recently, Halpern et al. that phylogeny will only make a difference to con- measured and mapped the intensity of pressures servation prioritization under speci cconditions: fi on the ocean (regardless of marine biodiversity); where very deep lineages endemics are endemic to the pressure peaks on their combined map are species-poor regions. Addressing the question surprisingly close to biodiversity conservation globally across entire classes remains an important priorities on land (the main exception being the research priority. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

219 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 204 Even if existing conservation priorities capture 1998; Wilson et al. difference within regions (Ando evolutionary history well, this does not necessar- et al. 2000), et al. 2006), across countries (Balmford ily mean that they capture evolutionary process. et al. 2008). Further, and and globally (Carwardine Indeed, a heterodox view proposes that the encouragingly, it appears that incorporation of young, rapidly speciating terminal twigs of phy- costs may actually decrease the variation in con- logenetic trees should be the highest conservation servation priorities caused by consideration of although some work priorities (Erwin 1991) — different biodiversity datasets, at least at the glob- suggests that existing conservation priority re- al scale (Bode 2008). The development of a et al. gions are actually priorities for both ancient and fi ne-scale, spatial, global estimation of conserva- young lineages (Fjeldså and Lovett 1997). Others tion costs is therefore an important priority for argue that much speciation is driven from ecoton- global conservation prioritization. 1997) and that these et al. al environments (Smith are poorly represented in conservation prioritiza- 11.2 Conservation planning and priorities et al. 2001). The verdict is tion templates (Smith on the ground still out. The remaining research priorities for global For all of the progress of global biodiversity conser- conservation prioritization concern intersection vation priority-setting, planning at much fi ner with human values. Since the groundbreaking scales is necessary to allow implementation on the assessment of Costanza (1997), much work et al. ground or in the water (Mace et al. 2000; Whittaker has been devoted to the measurement of ecosys- et al. et al. 2006). Madagascar can and 2005; Brooks — tem service value although surprisingly little to exible conservation re- should attract globally fl prioritizing its conservation (but see Ceballos and sources because it is a biodiversity hotspot, for Ehrlich 2002). Kareiva and Marvier (2003) sug- example, but this does not inform the question of gested that existing global biodiversity conserva- where within the island these resources should be tion priorities are less important than other invested (see Box 12.1). Addressing this question regions for ecosystem service provision. Turner requires consideration of three levels of ecological (2007), by contrast, showed considerable et al. species, sites, and sea/landscapes — — organization congruence between biodiversity conservation addressed in turn here. priority and potential ecosystem service value, at least for the terrestrial realm. Moreover, that 11.2.1 Species level conservation planning there is correspondence of both conservation and priorities priorities and ecosystem service value with human population (Balmford 2001) and pov- et al. Many consider species the fundamental unit of erty (Balmford et al. 2003) suggests that biodiver- biodiversity (Wilson 1992). Conversely, avoiding sity conservation may be delivering ecosystem species extinction can be seen as the fundamental services where people need them most. goal of biodiversity conservation, because while Maybe the fi nal frontier of global priority- all of humanity s other impacts on the Earth can ’ setting is the incorporation of cost of conservation. be repaired, species extinction, Jurassic Park fan- This is important, because conservation costs per tting, fi tasies notwithstanding, is irreversible. It is unit area vary over seven orders of magnitude, then, that maybe the oldest, best-known, and but elusive, because they are hard to measure most widely used tool in the conservationist s ’ (Polasky 2008). Efforts over the last decade, how- toolbox informs conservation planning at the spe- ever, have begun to develop methods for estimat- cies level. This is the IUCN Red List of 1999, 2001; et al. ing conservation cost ( James Threatened Species (www.iucnredlist.org). Bruner et al. 2004). These have in turn allowed assessment of the impact of incorporating costs fi eld History and state of the into conservation prioritization — with initial in- The IUCN Red List now dates back nearly 50 years, with its fi rst volumes published in the dications suggesting that this makes a substantial © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

220 1 205 CONSERVATION PLANNING AND PRIORITIES When there is no reasonable doubt last individual has died Extinct (EX) When the species is known only to survive in cultivation, in Extinct in the wild (EW) captivity or as a naturalized population(s) outside the past range Critically Endangered (CR) When the species has beeb assessed against the criteria and is (Adequate data) (Threatened) thought to be facing high to extremely high risk of extinction in Endangered (EN) the wild Vulnerable (VU) When a species does not meet the criteria but is close to qualifying, (Evaluated) or likely to quality, for a threatened category in the near future Near Threatened (NT) Increasing extinction risk When a species does not meet listing under a higher category of Least Concern (LC) threat (for widespread and abundant taxa) When there is inadequate information to make a direct, or indirect Data Deficient (DD) assessment of the risk of extinction of a species based on its Unknown distribution and/or population status extinction risk When a species has not yet been evaluated against the criteria Not Evaluated (NE) Criterion Endangered Critically Endangered Vulnerable Qualifiers and notes a 70% ³ 90% ³ Over ten years/three generations in the past, where A1: reduction in population ³ 50% causes of the reduction are clearly reversible AND size understood AND ceased A2-4: reduction in population ³ 50% 0% ³ 30% ³8 a Over ten years/three generations in past, futute or size combination B1: small range (extent of 2 Plus two of (a) severe fragmentation and/or few locations 2 2 <20 000km <100km <5000km occurance) 5, £ (1, 10); (b) continuing decline; (c) extreme £ fluctuation 2 Plus two of (a) severe fragmentation and/or few locations 2 2 B2: small range (area of <10km <500km <2000km £ (1, £ 5, 10); (b) continuing decline; (c) extreme occupancy) fluctuation <10 000 <2500 Mature individuals. Continuing decline either: (1) over C: small and declining <250 specified rates and time periods; or (2) with (a) specified population population structure or (b) extreme fluctuation <1000 <250 D1: very small population Mature individuals <50 D2: very restricted N/A 2 N/A Capable of becoming Critically Endangered or even <20km area of population Extinct within a very short time frame occupancy or £ five locations Estimated extinction risk using quantitative models (e.g. 20% in 20 years/five ³ 10% in 100 years ³ ³ 50% in ten years/three E: quantitative analysis a a population viability analyses) generations generations a Whichever is lon er. g Figure 11.5 The IUCN Red List categories and criteria (reprinted from Rodrigues et al . 2006 © Elsevier). For more details see Rodrigues et al . (2006). 1960s (Fitter and Fitter 1987). Over the last two analyses have shown to be broadly equivalent decades it has undergone dramatic changes, 2008), and which between criteria (Brooke et al. moving from being a simple list of qualitative are robust to the incorporation of uncertainty threat assessments for hand-picked species to its (Akçakaya et al. 2000). current form of quantitative assessments across As of 2007, 41 415 species had been assessed entire taxa, supported by comprehensive ancil- against the IUCN Red List categories and criteria, et al. 2006). The lary documentation (Rodrigues yielding the result that 16 306 of these are globally heart of the IUCN Red List lies in assessment of threatened with a high risk of extinction in the fi cally in vulnerability at the species level, speci medium-term future (IUCN 2007). This includes estimation of extinction risk (Figure 11.5). Be- comprehensive assessments of all mammals cause the requirements for formal population vi- (Schipper 2008), birds (BirdLife International et al. 2000) are too severe to et al. ability analysis (Brook 2004), as well et al. 2004) and amphibians (Stuart allow application for most species, the IUCN Red as partially complete datasets for many other taxa List is structured through assessment of species (Baillie 2004). Global assessments are under- et al. status against threshold values for fi ve quantita- way for reptiles, freshwater species ( sh, mol- fi tive criteria (IUCN 2001). These place species into lusks, odonata, decapod crustaceans), marine broad categories of threat which retrospective sh, corals), and plants. fi species ( © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

221 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: 206 CONSERVATION BIOLOGY FOR ALL It is worth a short digression here concerning on thousands of species not yet assessed globally irreplaceability at the species level, where phylo- 2000). To this end, IUCN have et al. (Rodriguez genetic, rather than geographic, space provides developed guidelines for sub-global application the dimension over which irreplaceability can be of the Red List criteria (Gärdenfors 2001), but et al. et al. (2007) has measured. A recent study by Isaac much work is still needed to facilitate the data pioneered the consideration of this concept of fl ow between national and global levels. alongside the “ phylogenetic irreplaceability ” fi One speci c challenge worth high- fi c scienti IUCN Red List to derive species-by-species con- lighting here is the assessment of threats driven servation priorities. A particularly useful applica- by climate change. Climate change is now widely tion of this approach may prove to be in recognized as a serious threat to biodiversity conservation. prioritizing efforts in ex situ et al. 2004). However, it hard to apply (Thomas fi The bene ts of the IUCN Red List are numerous the Red List criteria against climate change et al. 2006), informing site conservation (Rodrigues threats, especially for species with short genera- 2008), environmental planning (Hoffmann et al. et al. 2006), because climate tion times (Akçakaya impact assessment (Meynell 2005), national policy change is rather slow-acting (relative to the time (De Grammont and Cuarón 2006), and inter- scale of the Red List criteria). Research is under- governmental conventions (Brooks and Kennedy way to address this limitation. 2004), as well as strengthening the conservation constituency through the workshops process. 11.2.2 Site level conservation planning Data from the assessments for mammals, birds, and priorities amphibians, and freshwater species to date sug- gest that aggregate costs for the IUCN Red List With 16 306 species known to be threatened with process average around US$200 per species, in- extinction, threat rates increasing by the year (Butchart 2004), and undoubtedly many et al. cluding staff time, data management, and, in par- thousands of threatened plants and invertebrates ticular, travel and workshops. This cost is expected yet to be assessed, the task of biodiversity conser- to decrease as the process moves into assessments of plant and invertebrate species, because these vation seems impossibly daunting. Fortunately, it taxa have many fewer specialists per species than is not necessary to conserve these thousands of do vertebrates (Gaston and May 1992). However, it species one at a time. Examination of those fi ts of the process will also is expected that the bene threatened species entries on the Red List for decrease for invertebrate taxa, because the propor- ed reveals that habitat fi which threats are classi destruction is the overwhelming driver, threaten- fi tion of data de ciency will likely rise compared to ing 90% of threatened species (Baillie et al. 2004).  the current levels for vertebrate groups (e.g. 23% The logical implication of this is that the corner- for amphibians: Stuart et al. 2004). However, a sampled Red List approach is being developed to stone of conservation action must be conserving allow inexpensive insight into the conservation — the habitats in which these species live estab- status of even the megadiverse invertebrate taxa lishing protected areas (Bruner 2001). This et al. (Baillie 2008). et al. imperative for protecting areas is not new, of it dates back to the roots of conservation — course — itself but analyses of the World Database on Current challenges and future directions Protected Areas show that there are now 104 The main challenge facing the IUCN Red List is 791 protected areas worldwide covering 12% of one of scienti fi c process: how to expand the Red s coverage in the face of constraints of taxo- ’ List ’ s land area (Chape et al. 2005). Despite the world ciency, lack of capac- fi nomic uncertainty, data de this, however, much biodiversity is still wholly et al. ity, and demand for training (Rodrigues unrepresented within protected areas (Rodrigues 2006). Some of the answer to this must lie in et al. 2004a). The Programme of Work on Pro- coordination of the IUCN Red List with national tected Areas of the Convention on Biological Di- versity (www.cbd.int/protected) therefore calls red listing processes, which have generated data © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

222 1 207 CONSERVATION PLANNING AND PRIORITIES for gap analysis to allow planning of “ compre- national gap analysis under the Convention on hensive, effectively managed, and ecologically ’ s Programme of Work on Biological Diversity representative ” protected area systems. How Protected Areas (e.g. Madagascar: Figure 11.6; can such planning best take place? Turkey: Box 11.1), and a comprehensive guidance manual published to support this work (Lan- fi eld History and state of the 2007). Furthermore, all of the et al. ghammer Broadly, approaches to planning protected area s international conservation organizations, ’ world systems can be classi ed into four groups. The fi and many national ones, have come together as ad hoc oldest is establishment, which often in- the Alliance for Zero Extinction (AZE), to identify creases protected area coverage with minimal and implement action for the very highest prio- value for biodiversity (Pressey and Tully 1994). et al. rities for site-level conservation (Ricketts The 1990s saw the advent of the rather more 2005, Figure 11.7 and Plate 12). successful consensus workshop approach, which The key biodiversity areas approach, in align- allowed for data sharing and stake-holder buy-in, ment with the conceptual framework for conser- and certainly represented a considerable advance vation planning (Margules and Pressey 2000), is approaches (Hannah over 1998). How- ad hoc et al. based on metrics of vulnerability and irreplace- ever, the lack of transparent data and criteria still 2007). Their vulnera- et al. ability (Langhammer limited the reliability of workshop-based site con- bility criterion is derived directly from the IUCN cation of sites regu- servation planning. Meanwhile, developments in Red List, through the identi fi larly holding threshold populations of one theory (Margules and Pressey 2000) and ad- or more threatened species. The irreplaceability vances in supporting software (e.g. Marxan; www.uq.edu.au/marxan), led to large scale ap- plications of wholly data-driven conservation planning, most notably in South Africa (Cowling 2003). However, the black-box nature of et al. these applications led to limited uptake in conser- vation practice, which some have called the re- “ 2008). et al. search ” implementation gap – (Knight To overcome these limitations, the trend in conservation planning for implementation on the ground is now towards combining data- driven with stakeholder-driven techniques (Knight 2007). This ap- et al. 2007; Bennun et al. proach actually has a long history in bird conser- important “ rst application of fi vation, with the ” bird areas dating back to the work of Osieck and Mörzer Bruyns (1981). This “ site-speci fi c syn- thesis ” (Collar 1993 – 4) of bird conservation data has gained momentum to the point where impor- fi tant bird area identi cation is now close to being complete worldwide (BirdLife International protected KBA 2004). Over the last decade, the approach has been extended to numerous other taxa (e.g. plants: Plantlife International 2004), and thence non-protected KBA key biodiversity areas ” ap- generalized into the “ et al. 2004). Several dozen countries proach (Eken have now completed key biodiversity area iden- Figure 11.6 Location and protection status of the Key Biodiversity Areas (KBAs) of Madagascar (reprinted from Langhammer et al . 2007). fi cation as part of their commitment towards ti © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

223 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All 208 CONSERVATION BIOLOGY FOR ALL criterion is based on regular occurrence at a site of stems from the fact that most applications of fi cant proportion of the global population a signi these approaches to date come from fragmented of a species. This is divided into sub-criteria to it often proves dif — habitats cult to identify sites fi recognize the various situations under which this fi cance in of global biodiversity conservation signi could occur, namely for restricted range species, regions that retain a wilderness character, for species with clumped distributions, congregatory instance, in the Amazon (Mittermeier et al. populations (species that concentrate during a 2003). Under such circumstances, the omission portion of their life cycle), source populations, errors attendant on use of occurrence data (be- and biome-restricted assemblages. The reliance cause of very low sampling density) combine on occurrence data undoubtedly causes omission fi with dif culty in delineating sites (because of errors (where species occur in unknown sites) overlapping or non-existent land tenure). These and hence the approach overestimates irreplace- problems can, and indeed must, be overcome by ability. These omission errors could in theory delineating very large key biodiversity areas, be reduced by use of modeling or extrapolation which is still a possibility in such environments techniques, but these instead yield dangerous (e.g. Peres 2005). commission errors, which could lead to extinction The second challenge facing site level conser- through a species wrongly considered to be safely vation planning is its extension to aquatic envir- represented (Rondinini 2006). Where such et al. onments. Human threats to both freshwater and fi t is in identifying techniques are of proven bene marine biodiversity are intense, but species as- research priorities (as opposed to conservation sessments in these biomes are in their infancy priorities) for targeted fi eld surveys (Raxworthy (see above), seriously hampering conservation et al. 2003). fi culties of low sampling density planning. Dif To facilitate implementation and gap analysis, and delineation are also challenging for conserva- key biodiversity areas are delineated based on ex- tion planning below the water, as in wilderness isting land management units, such as protected regions on land. Nevertheless, initial scoping sug- areas, indigenous or community lands, private gests that the application of the key biodiversity concessions or ranches, and military or other pub- areas approach will be desirable in both freshwa- lic holdings (Langhammer et al. 2007). Importantly, ter (Darwall and Vié 2005) and marine (Edgar this contrasts with subdivision of the entire land- et al. 2008a) environments, and proof-of-concept scape into, for example, grid cells, habitat types, or from the Eastern Tropical Paci c shows that it is fi watersheds. While grid cells have the advantage of feasible (Edgar et al. 2008b). analytical rigor, and habitats and watersheds de- The third research front for the key biodiversity liver ecological coherence, these spatial units are of et al. areas approach is prioritization (Langhammer minimal relevance to the stakeholders on whom — 2007) ed and deli- once sites have been identi fi conservation on the ground fundamentally de- neated as having global biodiversity conservation pends. Indeed, the entire key biodiversity areas cance, which should be assigned the most fi signi process is designed to build the constituency for urgent conservation action? This requires the mea- local conservation, while following global stan- surement not just of irreplaceability and species dards and criteria (Bennun et al. 2007). The costs vulnerability, but also of site vulnerability (Bennun and bene fi ts of site conservation planning ap- et al. 2005). This is because site vulnerability inter- proaches have yet to be fully evaluated, but some acts with irreplaceability: where irreplaceability is fi ts of early simulation work suggests that the bene high (e.g., in AZE sites), the most threatened sites incorporation of primary biodiversity data are are priorities, while where irreplaceability is lower, large (Balmford and Gaston 1999). the least vulnerable sites should be prioritized. This is particularly important in considering resilience Current challenges and future directions (i.e. low vulnerability) of sites in the face of climate Three important challenges can be discerned as change. As with global prioritization (see above), it rst facing site level conservation planning. The fi is also important to strive towards incorporating © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

224 1 Box 11.1 Conservation planning for Key Biodiversity Areas in Turkey _   z, Süreyya I lu, an, Özge Balk Güven Eken, Murat Ataol, Murat Bozdog sfendiyarog ı ç, and Y ı ld ı ray Lise l ı Dicle Tuba K ı We used the framework KBA criteria An impressive set of projects has already been developed by Eken etal. (2004) and assessed 10 carried out to map priority areas for 214 species occurring in Turkey against these conservation in Turkey. These include three inventories of Important Bird Areas (Ertan etal. criteria. Two thousand two hundred and forty ı l ı ç and Eken 1989; Magnin and Yarar 1997; K six species triggered one or more KBA criteria. These include 2036 plant species (out of 8897 in 2004), a marine turtle areas inventory (Yerli and Demirayak 1996), and an Important Plant Turkey; 23%), 71 freshwater fi sh (of 200; 36%), 2003). These Areas inventory (Özhatay etal. 36 bird (of 364; 10%), 32 reptile (of 120; 27%), 28 mammal (of 160; 18%), 25 butter y (of 345; projects, collectively, facilitated on ‐ the fl ‐ ground site conservation in Turkey and drew 7%), 11 amphibian (of 30; 37%), and 7 y (of 98; 7%) species. Then, we assessed fl dragon attention to gaps in the present protected all available population data against each KBA areas network. criterion and its threshold to select KBAs. We used the results of these projects as inputs ed 294 KBAs qualifying on one or fi We identi to identify the Key Biodiversity Areas (KBAs) of Turkey, using standard KBA criteria across eight more criteria at the global scale (Box 11.1 Figure and Plate 11). Two KBAs met the criteria for taxonomic groups: plants, dragon ies, fl butter sh, amphibians, reptiles, fi ies, freshwater fl seven taxon groups, while 11 sites met them for birds, and mammals. As a result of this study, an ve taxon groups. The greatest fi six and 18 for number of sites, 94, met the KBA criteria for two inventory of two volumes (1112 pages) was taxon groups, while 86 sites (29%) triggered the published in Turkish fully documenting the etal . 2006). country criteria for one taxon group only. ’ sKBAs(Eken Unprotected KBAs Protected KBAs 400 300 200 0 50 100 km fi The 294 KBAs (Key Biodiversity Areas) of global importance identi Box 11.1 Figure ed in Turkey. While 146 incorporate protected areas ’ (light), this protection still covers <5% of Turkey s land area. The remaining 148 sites (dark) are wholly unprotected. continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

225 . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: Conservation Biology for All (Continued) Box 11.1 have been lost entirely over the last decade, The greatest number of sites, 223, was and other sites have lost at least 75% of their selected based on the criteria for plants, area during the same period. followed by reptiles and birds with 108 and 106 Less than 5% of the surface area of Turkey ’ s sites selected respectively. For other groups, KBAs is legally protected, and so this should be smaller numbers of sites triggered the KBA expanded rapidly and strategically. Steppe criteria at the global scale: 95 KBAs were habitats, river valleys, and Mediterranean ies, 61 for fl selected for mammals, 66 for butter scrublands are particularly poorly covered by freshwater sh, and 29 each for amphibians fi the current network of protected areas. ies. The number of sites selected fl and dragon Wildlife Development Reserves, Ramsar Sites for plants is actually rather low, given the high and, in the future, Natura 2000 Sites, would number of plant species in Turkey which trigger likely be appropriate protected area categories the KBA criteria. This can be explained by the for this expansion. ‐ overlapping distributions of restricted range and threatened plants. The other taxon groups have relatively greater numbers of sites. For instance, the seven dragon fl y species triggered REFERENCES the KBA criteria for 29 sites. One exception is sh, which, like plants, have the freshwater fi et al. (2004). Key Eken, G., Bennun, L., Brooks, T. M., highly overlapping ranges. Bio- biodiversity areas as site conservation targets. Large scale surface irrigation, drainage, and 54 1118. – , 1110 , Science _   fi cant threats dam projects form the most signi Eken, G., Bozdog sfendiyarog an, M., I lu, S., K ı ı ç, D. T., and l   ’ s nature. Irrigation and drainage to Turkey ı ’ a nin önemli dog . Dog Lise, Y. (2006). a alanlar Türkiye  projects affect 74% of the KBAs and dams have Derneg i, Ankara, Turkey. an effect on at least 49%. Inef fi cient use of nin önemli ’ Türkiye ç,A.,andKasparek,M.(1989). ı l ı Ertan,A.,K   ̧ water, especially in agriculture, is the root alHayat iandInternational ı KorumaDerneg kus alanlar .Dog ı 3 cause of these threats. A total of 40 billion m Council for Bird Preservation, Istanbul, Turkey. ̧ ı ç, D. T. and Eken, G. (2004). Türkiye ’ nin önemli kus K ı alan- l of water is channeled annually to agriculture   i, Ankara, Turkey. ı .Dog 2004 güncellemesi aDerneg lar – (75%), industry (10%), and domestic use (15%), Magnin, G. and Yarar, M. (1997). Important bird areas in – but 50 90% of water used for agriculture is lost   . Dog Turkey al Hayat ı Koruma Derneg i, Istanbul, Turkey. during the transportation from dams to arable fi nin ’ Türkiye eld, A., and Atay, S. (2003). Özhatay, N., By land. As a result of these threats, wetlands and Türkiye, Istanbul, Turkey. ‐ ı önemli bitki alanlar . WWF associated grasslands are Turkey ’ s most Yerli, S. and Demirayak, F. (1996). Türkiye de denizkaplum- ’ threatened habitat types. At least ve wetland fi   ̧ ̧ bag ı s Marshes, mekaya Marshes, Hotam KBAs (Es . ve üreme kumsallar üzerine bir deg erlendirme alar ı ı    Sultan Marshes, Ereg li Plain, and Seyfe Lake) al Hayat i, Istanbul, Turkey. ı Koruma Derneg Dog cost of conservation. Given these complexities, the species level, and more than 20 at the site considerable promise may lie in adapting level. However, the recent growth of the fi eld of conservation planning software to the purpose of landscape ecology (Turner 2005) sounds a warning prioritizing among conservation actions across key that while species and site planning are essential biodiversity areas. for effective biodiversity conservation, they are not fi suf cient. Why not, and how, then, can conserva- tion plan beyond representation, for persistence? 11.2.3 Sea/landscape level conservation planning and priorities History and state of the eld fi The fi rst signs that conserving biodiversity in The conservation community has more than 40 isolated protected areas might not ensure years experience with conservation planning at © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

226 1 211 CONSERVATION PLANNING AND PRIORITIES Map of 595 sites of imminent species extinction (reprinted from Ricketts et al . 2005). Yellow sites are either fully protected or partially Figure 11.7 = 203 and 87, respectively), and red sites are completely unprotected or have unknown protection status n contained within declared protected areas ( ( n = 257 and 48, respectively). In areas of overlap, unprotected (red) sites are mapped above protected (yellow) sites to highlight the more urgent conservation priorities. persistence came from evidence of long-term ex- of large scale conservation corridors have been tinctions of mammal species from North Ameri- designed (Crooks and Sanjayan 2006), for exam- can national parks (Newmark 1987). Over the Yellowstone to Yukon “ ple, the (Raimer and ” following decade, similar patterns were uncov- Ford 2005) and Mesoamerican Biological Corri- ered across many taxa, unfolding over the time- dor (Kaiser 2001). There is no doubt that the scale of decades-to-centuries, for megadiverse ts biodiversity fi implementation of corridors bene tropical ecosystems in Latin America (e.g. Robin- 2002). However, the establish- et al. (Tewksbury 1999), and Asia et al. son 1999), Africa (e.g. Brooks ment of generic corridors has also been criticized, 2003). Large-scale experiments, et al. (e.g. Brook in that they divert conservation resources from most notably the Manaus Biological Dynamics of higher priorities in protected area establishment, Forest Fragments project, provide increasingly and, even worse, have the potential to increase et al. 2001). The re fi ned evidence (Bierregaard threats, such as facilitating the spread of disease, — mechanisms determining persistence or extinc- invasive, or commensal species (Simberloff et al. — in individual sites spans the full spectrum tion 1992). et al. from the genetic scale (Saccheri 1998; see Given these concerns, there has been a shift Chapters 2 and 16) through populations (Lens towards speci fi cation of the particular objectives 2002) and communities (Terborgh et al. et al. 2001), for any given corridor (Hobbs 1992). A promising to the level of ecosystem processes across entire avenue of enquiry here has been to examine the et al. 1991; see Chapter 5). landscapes (Saunders which require broad ” “ needs of landscape species fi The rst recommendations of how conserva- et al. 2002b). Boyd scale conservation (Sanderson tion planning might address persistence at land- (2008) have generalized this approach, re- et al. scape scales were generic design criteria for the viewing the scales of conservation required for all connectivity of protected areas (Diamond 1975). threatened terrestrial vertebrate species (Figure Conservation agencies were quick to pick up the 11.8 and Plate 13). They found that 20% (793) of concept, and over the last twenty years a number these threatened species required urgent broad © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

227 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 212 scale conservation action, with this result varying land. Boyd s (2008) results are consistent with ’ et al. fi cantly among taxa (Figure 11.9). They also signi this, with 74% of threatened marine tetrapods asked why each of these species required broad requiring broad scale conservation, and 38% in scale conservation. This yielded the surprising freshwater, and only 8% on land (Figure 11.9). fi nding that while only 43% of these 793 species This said, some recent work suggests that marine “ area-demanding ” and so required corri- were larval dispersal occurs over much narrower scales dors for movement, no less than 72% were de- et al. 1999) and so than previously assumed (Jones pendent on broad scale ecological processes there is no doubt that site level conservation will acting across the landscape (15% require both). remain of great importance in the water as well as In this light, recent work in South Africa to pio- et al. on land (Cowen 2006). neer techniques for incorporating ecosystem pro- A second research front for sea/landscape con- cesses into conservation planning is likely to be servation planning concerns dynamic threats. Re- particularly important (Rouget et al. 2003, 2006). cent work has demonstrated that changes in the nature and intensity of threats over time have Current challenges and future directions important consequences for the prioritization of As at the species and site levels, the incorporation conservation actions among sites (Turner and of broad scale targets into conservation planning Wilcove 2006). Such dynamism introduces partic- in aquatic systems lags behind the terrestrial envi- ular complications when considered at the land- ronment. Given the regimes of fl ows and currents scape scale, the implications of which are only inherent in rivers and oceans, the expectation is just beginning to be addressed (Pressey et al. that broad scale conservation will be even more 2007). Climate change is one such threat that important in freshwater (Bunn and Arthington will very likely require extensive landscape scale 2002) and in the sea (Roberts 1997) than it is on 2002), and may be even et al. response (Hannah A B CD 2008). Figure 11.8 Scale requirements for the conservation of globally threatened species in the short ‐ to medium term (reprinted from Boyd et al. (A, dark green) Species best conserved at a single site (e.g. ); (B, pale green) Species best conserved at a network of sites Eleutherodactylus corona ‐ tamarin (e.g. black lion ); (C, dark blue) Species best conserved at a network of sites complemented by broad Leontopithecus chrysopygus scale ‐ ); (D, pale blue) Species best conserved through broad scale conservation action Dermochelys cariacea ‐ conservation action (e.g. leatherback turtle (e.g. Indian vulture ). Photographs by S. B. Hedges (A), R.A. Mittermeier (B), O. Langrand (C), and A. Rahmani (D). Gyps indicus © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

228 1 CONSERVATION PLANNING AND PRIORITIES 213 Tortoises Amphibians and turtles Mammals Birds Terrestrial N=1030 N=1001 N=27 N=725 Freshwater N=82 N=92 N=12 N=969 Marine N=25 N=88 N=6 N=0 Figure 11.9 Percentages of globally threatened species requiring different scales of conservation in the short ‐ to medium term (reprinted from Boyd et al. 2008). Dark green = species best conserved at a single site; pale green = species best conserved at a network of sites; dark blue = species best conserved at a network of sites complemented by broad ‐ scale conservation action; pale blue = species best conserved through broad ‐ scale conservation action. The totals exclude species insuf ciently known to assess the appropriate scale required. Relative size of pies corresponds to the fi number of species in each taxon/biome combination. more serious in freshwater (Roessig 2004) et al. current explosive growth in markets for carbon and the ocean (Xenopoulos et al. 2005) (see Chap- as mechanisms for climate change mitigation will ter 8). likely make the restoration of forest landscapes Maybe the largest open research challenge for increasingly viable in the near future (Laurance sea/landscape conservation planning is to move 2008). Ultimately, planning should move from from maintaining current biodiversity towards simple restoration to designing landscapes that restoring biodiversity that has already been lost allow the sustainability of both biodiversity and (Hobbs and Norton 1996). Natural processes of countryside bio- “ human land uses, envisioned as succession provide models of how this can pro- ” (Daily geography et al. reconciliation “ 2001) or et al. ceed most effectively (Dobson 1997). How- ” (Rosenzweig 2003). ecology ever, restoration is much more expensive and much less likely to succeed than is preservation of biodiversity before impacts occur, and so ex- 11.3 Coda: the completion plicit planning towards the speci c biodiversity fi of conservation planning targeted to be restored is essential (Miller and The research frontiers outlined in this chapter are Hobbs 2007). Given these costs and challenges, formidable, but conservation planning is never- most efforts to date target very tightly con- theless a discipline with its completion in sight. It strained ecosystems that, as restoration proceeds, is not too far of a stretch to imagine a day where — are then managed at site scales wetlands are the top-down global prioritization and bottom-up best example (Zedler 2000). A few ambitious conservation planning come together. Such a vi- plans for landscape level restoration have already sion would encompass: been developed (Stokstad 2008). Moreover, the © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

229 . http://ukcatalogue.oup.com/product/9780199554249.do Sodhi and Ehrlich: Conservation Biology for All 214 CONSERVATION BIOLOGY FOR ALL The completion and continuous updating of that reactive priority regions are concentrated in the · IUCN Red List assessments of all vertebrate and tropical mountains and islands, and proactive prio- plant species, plus selected invertebrate groups. rities in the lowland tropical forests. fi cation of key biodiversity areas, Iterative identi Major remaining research fronts for global biodiver- · · based on these data, representing the full set of sites sity conservation prioriti zation include the examina- cance. of global biodiversity conservation signi fi tion of cross-taxon surroga cy, aquatic priorities, Measurement and mapping of the continuous phylogenetic history, evolutionary process, ecosystem · global surface of seascape and landscape scale eco- services, and costs of conservation. logical processes necessary to retain these species Maybe the most important tool for guiding con- · and sites into the future. servation on the ground is the IUCN Red List of Continuous measurement and mapping of the Threatened Species, which assesses the extinction · threats to these species, sites, and sea/landscapes, risk of 41 415 species against quantitative categories ts of conserving them. fi and of the costs and bene and criteria, and provides data on their distribu- Free, electronic, continuously updated access to tions, habitats, threats, and conservation responses. · these datasets, and to tools for their interpretation, The predominant threat to biodiversity is the de- · planning, and prioritization. struction of habitats (Chapter 4), and so the primary conservation response must be to protect these A particularly important characteristic of such places through safeguarding key biodiversity areas. a vision is its iterative nature. As knowledge of While protecting sites is essential for biodiversity · biodiversity increases, threats and costs change, conservation, persistence in the long term also re- and conservation is implemented successfully (or quires the conservation of those landscape and sea- not) it is crucial that mechanisms exist to capture scape level ecological processes that maintain these changing data, because changes to any one biodiversity. of these parameters will likely impinge on conser- vation planning across the board. Under such a vision, it would be possible, at any Suggested reading given point in time, to maximize the overall bene ts fi of a conservation investment at any scale, from Boyd, C., Brooks, T. M., Butchart, S. H. M., et al. (2008). · ex situ management of a particular species, through Scale and the conservation of threatened species. Con- gap analysis by a national protected areas agency, to servation Letters , ,37 – 43. 1 fl investment of globally exible resources by institu- Brooks, T. M., Mittermeier, R. A., da Fonseca, G. A. B., · et al. (2006). Global biodiversity conservation priorities. tions like the GEF. Given the pace of advance in – ,58 61. 313 Science , conservation planning over the last 20 years, it is Eken, G., Bennun, L., Brooks, T. M., (2004). Key et al. possible that such a vision is achievable within the · biodiversity areas as site conservation targets. BioSci- coming few decades. Its re alization will provide 54 , ence – 1118. , 1110 great hope for maintaining as much of the life with Margules, C. R. and Pressey, R. L. (2000). Systematic which we share our planet as possible. · conservation planning. , 243 405 – 253. , Nature Rodrigues, A. S. L., Pilgrim, J. D., Lamoreux, J. F., Hoff- · mann, M., and Brooks, T. M. (2006). The value of the Summary Trends in Ecology and IUCN Red List for conservation. 76. – ,71 21 , Evolution Conservation planning and prioritization are es- · sential, because both biodiversity and human popu- lation (and hence threats to biodiversity and costs Relevant websites fi and bene ts of conservation) are distributed highly unevenly. BirdLife International Datazone: http://www.birdlife. · Great attention has been invested into global bio- org/datazone. · diversity conservation prioritization on land over IUCN Red List of Threatened Species: http://www. · the last two decades, producing a broad consensus iucnredlist.org. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

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235 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CHAPTER 12 Endangered species management: the US experience David S. Wilcove To many people around the world, the conserva- the US has one of the oldest and strongest laws on tion of endangered species is synonymous with the books to protect endangered species, it pro- the conservation of biodiversity. Ecologists, of vides a useful case history. course, understand that biodiversity encom- My discussion is admittedly incomplete and, to passes far more than endangered species, but it some extent, idiosyncratic. Endangered species is nonetheless true that endangered species are programs, especially those that impose restric- among the most visible and easily understood tions on human activities, are invariably contro- symbols of the ongoing loss of biodiversity (see versial, and that controversy results in much Chapter 10). The protection of such species is a discussion and debate. The ESA, for example, popular and important part of efforts to sustain fi c has been the subject of many books, scienti ’ the earth s natural diversity (see Box 12.1). articles, and popular articles; it has been debated The process of conserving endangered species in the halls of Congress and in town halls across can be divided into three phases: (i) identi ca- fi the nation; and it has been litigated numerous tion determining which species are in danger — times in the courts. Complete coverage of all of determining and of extinction; (ii) protection — the issues associated with endangered species in implementing the short-term measures neces- the US or any other large country is simply not ’ slide to extinction; and sary to halt a species possible in a single book chapter. For that reason, (iii) recovery determining and implementing — I have chosen to review a subset of issues that are the longer-term measures necessary to rebuild likely to be of interest to both scientists and deci- the population of the species to the point at sion-makers in countries with active programs to which it is no longer in danger of extinction. conserve endangered species. Many countries today have laws or programs designed to protect endangered species, although cacy of these efforts varies widely. Most fi the ef cation 12.1 Identi fi follow the identi fi cation/protection/recovery 12.1.1 What to protect paradigm. One of the oldest and strongest laws Endangered Species Act is the United States ’ A fundamental question that quickly arises when (ESA), which was passed in 1973 and has served scientists and decision-makers discuss as a template for many other nations. In this endangered wildlife is what exactly should be chapter, I shall focus on the three phases of conserved (see Box 12.2). Protection efforts can endangered species management, emphasizing be directed at species, subspecies, or popula- the US experience. My reason for emphasizing tions, with important tradeoffs. If, for example, the US is not because I believe it has done a better protection is extended to subspecies and popula- job of protecting its endangered species than tions, the total number of plants and animals that other countries. Rather, I am most familiar with are deemed in need of protection is likely to conservation efforts in the US. Moreover, because increase dramatically, resulting in greater 220 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

236 1 221 ENDANGERED SPECIES MANAGEMENT: THE US EXPERIENCE Box 12.1 Rare and threatened species and conservation planning in Madagascar ClaireKremen, AlisonCameron, Tom Allnutt, and Andriamandimbisoa Raza fi mpahanana The fundamental challenge of reserve design is how to maximize biodiversity conservation given area constraints, competing land uses and that extinction risk is already high for many species, even without further habitat loss. Madagascar is ’ s highest priorities for one of the world et al. conservation (Brooks 2006) with endemism exceeding 90% for many plant and animal groups (Goodman and Benstead 2005). Recently, the President of Madagascar set the target for habitat protection at 10% of the land surface, representing a tripling of the region to be protected. This provided an unparalleled ’ s opportunity to protect Madagascar Box 12.1 Figure 1 Mantella cowanii , a critically endangered frog biodiversity. To aid the government in site of Madagascar. It is one of the species that was used by Kremen “ systematic conservation selection, we used a et al . (2008) to determine priority sites for protection in Madagascar. planning approach (Margules and Pressey 2000) ” Photograph by F. Andreone. to identify regions that would protect as many species as possible, especially geographically rare and threatened species, within that 10% target. above) against the actual protected areas, from We obtained occurrence data for 2315 2.9% area in 2002 to 6.3% area in 2006. endemic species of plants, lemurs, frogs, geckos, When individual taxonomic groups were fl ies and ants (see Box 12.1 Figure 1). We butter utilized to de fi ne priority regions (run i), the ‐ support utilized a spatial prioritization decision regions selected by Zonation provided superior tool (Zonation: Moilanen et al. 2005), and input protection for members of the taxon itself, but models of species distributions (for 829 species) relatively poor protection for species in other and point data for the remaining species (too groups. It was therefore more ef fi cient to rare to model, designated RTS for rare target utilize an analysis based on all taxonomic species). The Zonation algorithm preferentially groups together (run ii). Comparing this selects the best habitat for geographically rare analysis to the regions that had already been ‐ restricted) species. In addition, by (range set aside showed that, on an area by area basis, supplying weights based on past habitat loss, we cantly fi Zonation selected regions that signi instructed Zonation to favor species that had increased the inclusion of habitat for suffered large range loss within the past 50 years geographically rare and threatened species. In (threatened species). In this manner, our decision addition, we found that the trajectory for support tool picked regions that not only accumulating species and habitat areas from represented all of the species in our analysis, but cient to protect fi 2002 to 2006 would be insuf fi ed the habitats most important to also identi all species within the area target, but that geographically rare and/or threatened species. careful selection of the last 3.7% (Run iii) could We ran Zonation in three ways: (i) for each of greatly improve both representation of all the six taxonomic groups alone; (ii) for all groups species and the selection of habitat for the together; and (iii) for all groups together, after geographically rare and threatened species rst selecting existing protected areas, totaling fi (Kremen et al. 2008). 6.3% of the country. We then assessed how well Subsequently, this analysis was used along with the selected regions for each Zonation run other conservation inputs (Key Biodiversity protected rare and threatened species by Analyses, Important Bird Areas, and others; see determining what proportions of their habitats fi nal regions for Chapter 11) to justify the (for modeled species) or occurrence points (for protection totaling 6.4 million hectares (Box 12.1 RTS species) were included. We also compared Figure 2, black zones totaling just over 10%), and sselectionsbasedonalltaxa(runii ’ Zonation served to designate an additional 5.3 million continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

237 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: 222 CONSERVATION BIOLOGY FOR ALL Box 12.1 (Continued) hectares as important conservation regions mining activities. No new mining permits will ministerial decree limiting subject to an inter ‐ be issued in the highest priority zones (grey zones), and the remaining areas (light grey Antsiranana zones) will be subject to strict control (e.g. following Environmental Impact Assessment). N The rare target species, in particular, were WE ne these zones, in particular fi utilized to de S the 505 species currently known from only cant a single site. Furthermore, as a signi fi proportion of these priority zones contain Mahajanga existing mining permits (14% of the existing parks and highest priority areas), the Zonation result is an ideal tool for ‐ negotiating trade offs or swaps between mining and protected areas. Toamasina Antananarivo Antananarivo Antananarivo REFERENCES Brooks, T. M., Mittermeier, R. A., da Fonseca, G. A. B., (2006). Global biodiversity conservation priorities. et al. ,58 61. – 313 , Science Fianarantsoa Fianarantsoa Fianarantsoa Goodman, S. and Benstead, J. (2005). Updated estimates of biotic diversity and endemism for Madagascar. Oryx , 39 – 77. ,73 Kremen, C., Cameron, A., Moilanen, A., et al. Toliara (2008). Aligning conservation priorities across taxa Limit Region ‐ resolution planning tools. in Madagascar with high Existing and New Protected Areas , 226. – , 222 320 Science Priority Sites Sensitive Sites Margules, C.R. and Pressey, R. L. (2000). 0 50 50 100 150 Kilometers Nature Systematic conservation planning. , 253. , 243 405 – Moilanen, A., Franco, A. M. A., Early, R. I., et al. ‐ Box 12.1 Figure 2 This map portrays the Inter Ministry decree of ‐ use landscapes for (2005). Prioritizing multiple October 2008 delineating the new and existing protected areas ‐ conservation: methods for large multi species (black), the priority biodiversity areas where no new mining permits planning problems. Proceedings of the may be issued (grey) and the sensitive biodiversity sites (light grey), , 272 Royal Society of London B , which will be subject to environmental impact assessment prior to 1891. – 1885 permission of forestry or mining activities. See also Figure 11.6. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

238 1 ENDANGERED SPECIES MANAGEMENT: THE US EXPERIENCE 223 demands for funding and, potentially, more con- et al. 1997; essential to human welfare (Hughes fl icts with landowners, developers, and other Chapter 3). resource users. On the other hand, it has been A second consideration relates to geographic argued that populations should be the funda- scale. Should the frame of reference for deciding mental unit of biodiversity protection (see Box whether or not a species is endangered be the 10.1), since it is populations of plants and entire world (the species global status), a partic- ’ animals that provide the ecosystem services ular country (its national status), or a particular Box 12.2 Flagship species create Pride Peter Vaughan What makes a good Unlike the agship? fl governmental organization Rare: Rare is a non ‐ “ , indicator , ” concepts of “ keystone ” “ to conserve imperiled species whose mission is “ ” endangered , and ” species, which “ umbrella and ecosystems around the world by inspiring all have ecological or conservation implications, people to care about and protect nature ” (see fl agship species are chosen for their marketing ’ s program utilizes social Pride Chapter 15). Rare potential (Walpole and Leader marketing to educate and motivate people Williams 2002). ‐ who live in, or adjacent to, areas of high agship species are The key characteristics of fl biodiversity to adopt new behaviors that either (based on Karavanov 2008): protect, or are less damaging to, the local • Be charismatic or appealing to the target environment. audience; no slugs, worms, or mosquitoes! Social marketing: Many commercial Be local or endemic to symbolize the • ” their companies and/or marketers brand “ uniqueness of the conservation target area to ’ s products using symbols, such as Pillsbury foster a sense of local pride. ” doughboy bitten “ s ’ , or Apple Computer “ Be representative of the conservation target • apple. ” Similarly, Pride brands its social area by living in its habitat or ecosystem. marketing campaigns using species. “ fl agship ” Have no negative perceptions among local • While concepts such as ecosystem and people, such as being a crop pest, being biodiversity are central to Rare s overall ’ dangerous, or have existing cultural connota- conservation strategies, they are complex and tions that detract from or compete with the fail to evoke the emotional response that is s conservation messages. campaign ’ required to motivate behavior change among agship is to fl most people. The purpose of a How are fl agships chosen? Flagship species create a simple, instantly recognizable symbol are chosen through a lengthy process that that evokes a positive emotional response includes input from local stakeholders, among members of the target audience. As interviews with local experts, and results from Mohr (2008) states ‐ Mckenzie All persuasion “ surveys of the local human population. This depends upon capturing attention. Without agships have the process ensures that fl attention, persuasion is impossible. requisite characteristics outlined above. Communications can be made more effective Flagship species are agships used? fl How are by ensuring that they are vivid, personal and used in most of the marketing materials agship evokes feelings of concrete. ” A good fl produced during a Pride campaign, including trust, affection, and above all for Rare, a sense billboards, posters, puppet shows, songs, Pride in the local environment. Pride of place of videos, etc. such that they become ubiquitous is a powerful emotion that can motivate people agship species fl in the community. Although to change their behaviors and empower them ‐ human, they become symbolic are non to take environmental action. members of the local community, which continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

239 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 224 Box 12.2 (Continued) confers on them the credibility they need in order to be perceived as trustworthy sources of agship species serves as both fl information. The ” “ the face of the campaign and as a ” for the campaign ’ s messages. spokesperson “ opinion leadership role This activates the ” “ social diffusion networks that exist in all societies by stimulating interpersonal communication among members of the target audience, a key step in the behavior change process (Rogers 1995, Vaughan and Rogers 2000). fi rst ’ s fl agship species: Rare ’ s Among Rare 71 campaigns, 59% chose a bird, 16% chose a mammal, and 11% chose a reptile to be their agships species, but campaigns have also fl Pride campaign agship mascot representing the fl Box 12.2 Figure great hornbill in Laos. Photograph by R. Godfrey. sh, insects, crustaceans, amphibians, fi used and plants. About half of the chosen species were endemic to the country or region, but only about 8% have been listed as REFERENCES endangered or critically endangered by IUCN. Jenks, B., Vaughan, P. W., and Butler, P. J. (2010). The agship species play such a prominent Because fl Evolution of Rare Pride: Using Evaluation to Drive role in Pride campaigns, knowledge about Adaptive Management in a Biodiversity Conservation them can serve as markers for campaign Journal of Evaluation and Program Organization. exposure and impact. For example, during Planning Special Edition on Environmental Education the campaign in Laos (Vannalath Pride , in press. Evaluation s 2006), awareness among the campaign ’ ‐ Campaign design Karavanov, A. (2008). Including work target audience of the great hornbill . Rare Pride Leadership planning and monitoring ; Box 12.2 Figure) increased ( Buceros bicornis Development Program, Rare, Arlington, VA. from 61% to 100%; the percentage of Mckenzie ‐ Mohr, D. (2008). http://www.graduationpledge. respondents who know that the hornbill is in org/Downloads/CBSM.pdf (page 4) accessed December danger of extinction increased from 22% to 15, 2008. 77%; the percentage who knew that hunting Diffusion of innovations , 4th ed. The Rogers, E. M. (1995). or capturing the hornbill is prohibited Free Press, New York, NY. increased from 31% to 90%; and the Final Report, Rare Pride Campaign in Vannalath, S. (2006). cutting down the percentage that identi fi ed “ Nam Kading National Protected Area, Lao Peoples ” forest as one of the greatest threats to the Democratic Republic, Rare Diploma in Conservation Edu- hornbill increased from 17% to 65%. In . cation, University of Kent at Canterbury, United Kingdom addition to increasing knowledge, improving Wildlife Conservation Society and Rare, Arlington, VA. attitudes, and changing personal Vaughan, P. W. and Rogers, E. M. (2000). A staged model Pride campaigns have been credited behavior, of communication effects: Evidence from an entertain- with contributing to the creation of ment ‐ education radio drama in Tanzania. The Journal of protected areas, enactment of new laws and 227. Health Communication , 5 , 203 – regulations, and the preservation of Williams, N. (2002). Tourism ‐ Walpole, M. J. and Leader 2010). Central et al. endangered species (Jenks and fl agship species in conservation. Biodiversity and to all of these efforts has been the use of 547. – , 543 11 Conservation , agship species. fl © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

240 1 ENDANGERED SPECIES MANAGEMENT: THE US EXPERIENCE 225 state, county, or municipality (its local status)? c North- fi be some of the salmon runs in the Paci Aego- For example, the northern saw-whet owl ( west that have been added to the endangered ) is widely distributed across the lius acadicus species list in recent years. To qualify for listing, northern and western United States and in parts a given run must show signi cant genetic, demo- fi of Mexico. It is not in danger of extinction. But graphic, or behavioral differences from other runs within the US, the State of Maryland considers of the same species. the northern saw-whet owl to be an endangered One aspect of the ESA ’ s identi fi cation process species; Maryland is at the southeastern periph- merits special attention. The law explicitly states ery of the owl ’ s range and the bird is quite rare that the decision to add a plant or animal to the there. Conservationists continue to debate the endangered species list must be based solely on “ wisdom of expending scarce resources on the the basis of the best scienti fi c and commercial protection of peripheral or isolated populations (Endangered Species Act, Section 4(b) data ... ” of otherwise common species. Yet such popula- (1)(A)). In other words, whether or not a species is tions are often a source of pride to the citizens of a endangered is treated as a purely scienti fi c ques- given region, and they may contain unique alleles tion. Political considerations are not allowed to that contribute to the overall genetic diversity of interfere with the identi cation phase (although fi the species. in practice they sometimes do, leading to nasty A third consideration is whether to extend pro- legal battles). tection to all types of endangered organisms or to limit such efforts to particular groups, such as 12.1.2 Criteria for determining whether a species vertebrates or vascular plants. Proponents of ex- is endangered clusion argue that it is impossible to identify and protect all of the imperiled species in any large How does one know that a given species is in area (see below), and that by targeting a few, danger of extinction? Biologists typically look select groups, it should be possible to protect for data that indicate vulnerability: a small popu- the habitats of many other species. Although lation size, a declining population, ongoing losses some studies have supported this notion, others of habitat (see Chapter 4), etc. In some cases, those data are combined with models to yield have not. short and long-term projections of population Within the US, the ESA addresses these issues viability (see Chapter 16); in other cases, where in the following ways: it allows for the protection of species and subspecies of plants and animals not enough data exist to construct good models, (including invertebrate animals). In the case of the determination is based on expert opinion. vertebrates only, it also allows for the protection Needless to say, different experts weighing dif- of distinct population segments. In the early years ferent factors are likely to come to different con- of the ESA, the US Fish and Wildlife Service, the clusions as to which species are in trouble. Resources may be wasted on plants and animals agency charged with protecting imperiled wild- that are not really endangered, while other, life, allowed populations to be de fi ned on the gravely imperiled species go unprotected. The Ha- basis of political borders. Thus, bald eagles ( liaeetus leucocephalus ) in the coterminous 48 states need for a more transparent, standardized way (but not those living in Alaska or Canada) were to assess the status of species led the International added to the endangered list when their numbers Union for Conservation of Nature (IUCN) to plummeted due to pesticide poisoning. More re- develop a set of quantitative guidelines in 1994, cently, the Fish and Wildlife Service has turned now known as the Red List categories and cri- teria. These guidelines enable scientists to assign away from using political borders to delineate any plant or animal to one of six categories (Ex- vertebrate populations and has insisted that tinct, Extinct in the Wild, Critically Endangered, such populations be discrete ecological entities in order to be eligible for inclusion on the Endangered, Vulnerable, Near Threatened) based endangered list. An example of the latter would on factors such as range size, amount of occupied © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

241 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 226 habitat, population size, trends in population 12.2.1 What are the threats? size, or trends in the amount of habitat (www. Understanding the threats facing endangered iucnredlist.org/static/categories_crtiteria). The species is complicated due to four factors: original Red List categories and criteria were de- (i) threats may vary from taxon to taxon; the things signed to determine the global status of species, that imperil freshwater fi sh, for example, may not but conservation biologists subsequently have necessarily be the things that imperil terrestrial developed guidelines for applying those criteria mammals; (ii) threats may vary geographically, to individual nations, states, provinces, etc. depending on economics, technology, human de- ning The ESA, however, is notably vague in de fi mography, land-use patterns and social customs what constitutes a species at risk of extinction. in different areas; (iii) threats may change over It establishes two categories of risk, endangered time, again in response to technological, economic, and threatened, and de fi nes an endangered spe- social, or demographic factors; and (iv) for all but a any species which is in danger of extinc- “ cies as handful of groups (e.g. birds, mammals, amphi- tion throughout all or a signi fi cant portion of its bians), scientists simply do not know enough “ and a threatened species as ” any species range about most species to determine which ones are which is likely to become an endangered species imperiled and why they are imperiled. within the foreseeable future throughout all or a — For three groups birds, mammals, and am- signi fi cant portion of its range ” (Endangered Spe- phibians — the IUCN has determined the conser- cies Act, Sections 3(6) and 3(19)). In practice, most vation status of virtually all extant and recently plants and animals have not been added to the extinct species (Baillie et al. 2004). These data US endangered species list until they were close provide the best global overview of threats to to extinction. A study published in 1993 (Wilcove endangered species (Figure 12.1). With respect 1993) showed that the median total popula- et al. to birds and amphibians, habitat destruction is tion size of a vertebrate at time of listing was 1075 by far the most pervasive threat: over 86% of individuals; the median number of surviving po- fi birds and 88% of amphibians classi ed by IUCN pulations was two. For invertebrate animals, the as globally imperiled are threatened to some de- median total population size was less than 1000 gree by habitat destruction. Agriculture and log- individuals, and the number of surviving popu- ging are the most widespread forms of habitat lations was three. In the case of plants, the medi- destruction (see Chapter 4). Overexploitation an total population size was less than 120 for subsistence or commerce contributed to the individuals, and the number of surviving popu- endangerment of 30% of imperiled birds but only lations was four. One obvious consequence of 6% of amphibians (see Chapter 6). Alien species waiting until species are so rare before protecting were a factor in the decline of 30% of imperiled cult, fi them is that recovery becomes far more dif birds and 11% of amphibians (see Chapter 7). if not impossible, to achieve. Pollution affected 12% of imperiled birds and 4% of amphibians (see Box 13.1). Disease, which is often linked to pollution or habitat destruction, 12.2 Protection was a threat to 5% of birds and 17% of amphi- ed as bians. Surprisingly, few species were identi fi In order to develop an effective protection plan being threatened by human-caused climate for endangered species, one needs to know a change, perhaps because most threats are identi- minimum of two things: (i) What threats do the fi ed after the fact (see Chapter 8). However, species in question face?; and (ii) Where do those (2004) modeled the response of et al. Thomas species occur? Knowledge of the threats will de- localized species of various taxa to climate termine protection and recovery efforts, while change and concluded that 15 – 37% of them knowledge of the location and, in particular, the could be destined for extinction by 2050, making land ownership, will guide the choice of conser- climate change potentially a grave threat. vation strategy. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

242 1 ENDANGERED SPECIES MANAGEMENT: THE US EXPERIENCE 227 100 Birds Amphibians 80 60 40 20 Imperiled species affected by threat (%) 0 Alien species Habitat Disease Overexploition Pollution destruction Threats ’ Percentage of the world Figure 12.1 s imperiled birds (black bars) and amphibians (grey bars) threatened by different factors, based on global analyses performed by the IUCN/World Conservation Union. The total percentages for each group exceed 100% because many species are threatened by more than one factor. Data from Baille et al . (2004). A comprehensive status assessment of the 47% of imperiled vertebrates), pollution (46%), world ’ s mammals was published in 2008 (Schip- overexploitation (27%), and disease (11%) (Wil- et al. per 200; Figure 12.2). Unlike the analyses of 1998). In contrast, the most pervasive et al. cove birds and amphibians, the mammal assessment threat to imperiled vertebrates in China is over- did not separate imperiled from non-threatened exploitation, affecting 78% of species, followed by species in its breakdown of threats. Habitat de- habitat destruction (70%), pollution (20%), alien struction is the most widespread threat to mam- 1%) (Li and Wilcove < species (3%), and disease ( mals, affecting 37% of all extant and recently 2005; Figure 12.3). extinct species, followed by overexploitation Ecologists have long recognized that island (17%), invasive species (6%), pollution (4%), and ecosystems are more vulnerable to alien species diseases (2%). (The lower percentages compared than most continental ecosystems. In the Hawai- to birds and amphibians re fl ect the fact that the ian archipelago, for example, 98% of imperiled mammal assessment covered both imperiled and birds and 99% of imperiled plants are threatened non-threatened species). Accidental mortality, at least in part by alien species (Figure 12.4 and usually associated with bycatch in fi sheries, Plate 14). Comparable percentages for imperiled affects 5% of the world ’ s mammals; in the special birds and plants in the continental US are 48% case of marine mammals, it affects a staggering et al. and 30%, respectively (Wilcove 1998). et al. 83% of species (see Schipper 2008). These global analyses of threats mask some 12.2.2 Where do endangered species live? important regional differences that could in fl u- ence conservation decisions. For example, in the There is now a burgeoning literature that aspires US, the most pervasive threat to vertebrates is to identify key sites for endangered species, typi- habitat destruction, affecting over 92% of imper- cally by developing sophisticated algorithms that iled mammals, birds, reptiles, amphibians, and optimize the number of rare species protected per sh. This was followed by alien species (affecting fi 2007; see et al. acre or per dollar (see Dobson © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

243 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 228 CONSERVATION BIOLOGY FOR ALL 40 30 20 Species affected by threat (%) 10 0 Pollution Disease Accidental Invasive Over- Habitat destruction mortality species exploitation Threats . (2008). Note that this et al s mammals threatened by different factors, based on a global analysis by Schipper Percentage of the world Figure 12.2 ’ analysis covered both threatened and unthreatened species; as such, the data include threats to species that are not yet at risk of extinction, unlike Figure 12.1. 100 China United States 80 60 40 20 Imperiled species affected by threat (%) 0 Disease Habitat Alien species Pollution Over exploitation loss Threats Percentage of imperiled vertebrates in China and the USA threatened by different factors. Reprinted from Li and Wilcove (2005) Figure 12.3 © American Institute of Biological Sciences. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

244 1 ENDANGERED SPECIES MANAGEMENT: THE US EXPERIENCE 229 In the US, once a species has been added to the of fi cial list of threatened and endangered species “ listed species ” ), it is protected to (making it a varying degrees on both publicly-owned and pri- vately-owned lands. Federal agencies, for exam- ple, are prohibited from engaging in, authorizing, or funding any activities that may jeopardize the survival and recovery of a listed species, includ- ing activities that damage or destroy important habitats. Depending on circumstances, such activities can range from timber cutting in the national forests to the construction of federally- ), an endangered Hawaiian Palmeria dolei Akohekohe ( Figure 12.4 funded dams or the allocation of funds for the honeycreeper. Like many Hawaiian honeycreepers, it is endangered by a construction of interstate highways. Federal combination of habitat destruction and diseases transmitted by agencies are required to consult with the US introduced mosquitoes. Photograph by Jaan Lepson. Fish and Wildlife Service, the agency charged Chapter 11). In this section I shall focus on the with administering the ESA, prior to undertaking simpler issue of land ownership: does the species any activities that may harm listed species. This in question occur on publicly owned (federal or consultation requirement minimizes the risk that state government) land or private land? In the these other agencies will ignore the needs of im- US, at least, land ownership patterns are a periled species in the course of their day-to-day prime consideration in devising effective protec- operations. Typically, the US Fish and Wildlife tion and recovery strategies, given that approxi- Service will work with other government agen- mately 60% of land in the US is privately owned. cies to modify projects so they no longer pose a In the most authoritative assessment of land threat to listed species or, if such modi cations fi ownership and endangered species in the US, are impractical, to develop a mitigation plan that et al. Groves (2000) estimate that private lands compensates for any harm to a listed species. harbor populations of more than half of the Private citizens are prohibited from harming s imperiled species; if one focuses exclu- ’ nation listed animals. This includes direct harm, such sively on those imperiled species that have made as shooting or trapping, as well as indirect it onto the of cial federal list, that value rises to fi harm, such as habitat destruction. Listed plants, two-thirds. Approximately one-quarter of all on the other hand, are not afforded protection on documented populations of federally protected private lands unless the activity in question (e.g. endangered species occur on privately owned fi lling a wetland) requires a federal permit for fi land. This gure almost certainly underestimates some other reason. This distinction between ani- the degree to which private lands are important mals and plants dates back to English common to endangered species because many landowners law and does not have any ecological basis. are reluctant to allow biologists to come onto ’ s reach to the The decision to extend the ESA their property to look for rare plants and animals. activities of private citizens was revolutionary at the time, and it has been the source of consider- able controversy ever since. When the ESA origi- 12.2.3 Protection under the ESA nally was passed in 1973, the prohibition on harming a listed species was absolute. But this An effective law or program for endangered spe- cies must, at a minimum, be capable of protecting rigid requirement had an unfortunate conse- essential habitat, halting overexploitation, and quence: Landowners refused to discuss their slowing the spread of harmful alien species. In endangered-species issues with the US Fish and Wildlife Service because they knew the agency the US at least, it must also extend to both public ” “ could only say no, and the US Fish and Wildlife and private lands. © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

245 . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All Sodhi and Ehrlich: CONSERVATION BIOLOGY FOR ALL 230 danger of extinction and no longer requires extraor- Service turned a blind eye to the activities of dinary conservation measures. That process de- private landowners because it feared a political mands a careful balancing of science, economics, backlash if it slavishly enforced the law. Thus, and sociology (see Chapter 14). For example, scien- paradoxically, the law was too strong to protect ti c tools like population viability analysis can be fi endangered species effectively. In 1982, the US used to gure out how many populations must be fi ed the ESA so that private land- fi Congress modi protected, how large those populations should be, owners could obtain permits from the US Fish and how they must be distributed across the land- and Wildlife Service to engage in activities harm- scape in order to sustain the species in question ful to listed species provided the landowners de- (Chapter 16). Restoration ecology can be used to veloped a plan to minimize and mitigate the determine how to rehabilitate degraded habitats so impacts of those activities, to the maximum ex- “ as to increase the numbers and distributions of This change to the law, while ” tent practicable. endangered species (see Chapter 13). But securing controversial, probably averted a much greater the cooperation of landowners in the targeted areas weakening of the ESA down the road. or obtaining the necessary funding to implement For both federal agencies and private citizens the restoration plan requires careful consideration there is also an exemption process that permits of economics, politics, and social customs. All these important activities to go forward notwithstand- steps need to be integrated in order to recover an ing their impact on endangered species. It is re- endangered species. served for cases where the project in question In the US, the ESA requires that recovery plans cannot be modi fi ed or mitigated so as to avoid be developed for all listed species. Those plans jeopardizing the survival and recovery of a listed should, in theory, spell out the steps necessary to species. Because the exemption process is compli- ensure that a given species is no longer in danger cated, time-consuming, and politically charged, it of extinction as well as provide a budget has been very rarely used. Instead, the vast ma- for achieving that goal. One might assume that jority of con icts are resolved through consulta- fl recovery plans play a pivotal role in endangered tions with the US Fish and Wildlife Service and species management in the US but, in fact, they fi cations to the proposed projects. modi rarely do. Part of the problem is that the plans are Finally, it should be noted that while the ESA can not legally binding documents. Moreover, ac- prevent a landowner from undertaking activities et al. cording to several studies (Clark 2002; Hoek- that are harmful to a listed species (e.g. habitat et al. 2002), the plans often fail to make good stra destruction), it is doubtful that it can compel an use of available biological data for the purposes of fi individual to take af rmative steps to improve the developing quantitative recovery goals and out- well-being of a listed species, for example by re- lining recovery actions. In addition, many plans movinganinvasiveplantthatischokingoutthe lack adequate information on the threats facing habitat of an endangered bird. This is an important endangered species or fail to link recovery actions limitation of laws, such as the ESA, that focus on to speci c threats. And still others fail to set out a fi prohibiting harmful activities; they may not be ef- scienti fi cally sound monitoring protocol for fective at dealing with more passive threats, such as detecting changes in the status of species or asses- invasive species or diseases. I return to this issue in sing the impacts of recovery actions. In short, the my discussion of recovery programs (see below). recovery planning process has failed to deliver the sort of guidance needed to move species back from the brink of extinction. 12.3 Recovery 12.3.1 Recovery planning 12.3.2 The management challenge Recovery aims to secure the long-term future of the In theory, the goal of endangered species man- species, to rebuild its populations, restore its habi- agement is to undertake a series of steps that tat, or reduce the threats such that it no longer is in © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

246 1 231 ENDANGERED SPECIES MANAGEMENT: THE US EXPERIENCE eliminate the threats to the species in question will not survive without constant human inter- and result in healthy populations that no longer vention. require special protection or attention. And yet Third, more and more species are becoming sometimes termed these sorts of success stories — endangered by the spread of alien, invasive spe- ” because conservationists walk-away-species “ cies. In most cases, scientists have no way to elimi- will be few — are able to walk away from them nate or permanently control the invasive species. and far between. Instead, most endangered spe- Indeed, most attempts at biological control, such cies are likely to require intensive management as introducing a predator or pathogen of the harm- nite future. The rea- and protection for the inde fi ful alien, prove unsuccessful or, worse yet, end up sons are three-fold. harming other native species (Simberloff and First, the leading cause of species endangerment Stiling 1996). Consequently, the usual recourse is worldwide is habitat loss (Chapter 4). If, as a result to control invasive species by pulling them up, of this problem, species are reduced to living in poisoning them, hunting them, or trapping them. small, fragmented patches of habitat, they are likely Since these activities must be repeated whenever to remain at high risk of extinction until such time the population of the alien species rebounds, there as more suitable habitat is created via ecological is little prospect of declaring victory and “ walking restoration. In places where human demands for away. ” land are great (e.g. southern California), there may Wilcove and Chen (1998) estimate that 60% of be no practical way for conservation organizations the species protected or proposed for protection or government agencies to acquire land for restora- under the ESA are threatened to some degree by tion. Moreover, even if the land is available, it can re suppression. For virtually all fi alien species or take decades, even centuries, to restore certain of these species, ongoing management of their types of ecosystems, such as old-growth forests — habitats will be necessary to ensure their long- if those ecosystems can be restored to anything term survival. Wilcove and Chen (1998) further resembling their pre-industrial state [see Hobbs note that the longer the necessary management is and Harris (2001) for a discussion of key conceptual delayed, the greater the risk of extinction of rare issues in ecological restoration; also Box 5.3]. species and the greater the cost when the neces- Second, many species live in ecosystems that sary management is fi nally performed. For exam- are maintained by natural disturbances such as , an invasive woody plant, dominates Tamarix ple, fl res and fi oods. Examples of such ecosystems riparian areas in the Southwestern US unless it is include longleaf pine forests in the Southeastern controlled via herbicides and cutting. In places United States and riparian forests in the South- Tamarix where has been allowed to grow for western United States. As people dam rivers, many years, the cost of removal can be as high clear native vegetation to build homes and fi rst year, dropping as US$675 per acre in the farms, and settle those ecosystems, they disrupt below US$10 per acre in the second year. or eliminate the natural disturbances. The result Subsequent maintenance requires an expenditure is a growing roster of endangered species for of under US$10 per acre every two to three years. which overt habitat destruction is compounded We can think of endangered species management by the elimination of the natural disturbances as having two cost components: an accrued debt that were essential to maintaining the habitat. fl re ecting a deferred maintenance problem that res fi Given that people are unlikely to allow wild arises from inadequate management efforts in oods to reappear in places where these forces fl or ecting the the past and an annual payment re fl ” have been “ tamed, the only way to ensure the necessary upkeep of properly managed habitats. survival of disturbance-dependent species is to Scott et al. (2005) recommend that recovery be mimic the disturbances by using techniques viewed as a continuum of states. At one extreme re, controlled releases of fi such as prescribed are the species that can survive in the wild with water from dams, or direct manipulation of the essentially no active management once key vegetation. In short, a growing number of species threats have been eliminated or enough habitat © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

247 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do CONSERVATION BIOLOGY FOR ALL 232 has been protected. At the other extreme are spe- This woodpecker is restricted to mature, open cies that can persist in the wild, but only if people pine forests in the southeastern US. A combina- actively manage their habitats or control their tion of residential development and short- competitors, predators, etc. A simple recovered/ rotation forestry resulted in the elimination of not recovered dichotomy, as exists under the most of the old-growth pine forests in the South- ESA, does not re ect the complexity of contem- fl east and led the US Fish and Wildlife Service to porary conservation. place the woodpecker on the endangered list in 1970. This action ultimately resulted in protection of much of the woodpecker s remaining habitat. ’ However, reports began to trickle in of land- 12.4 Incentives and disincentives owners cutting down stands of young pine trees Policy tools to conserve endangered species can because they were afraid that red-cockaded be divided into two categories: incentives and woodpeckers would colonize their property if disincentives. An example of an incentive would the trees got much older. The landowners knew be a cash payment to a landowner for maintain- that once the woodpeckers arrived, their ability to ing the habitat of an endangered species. An ex- cut down the trees at a later date could be severe- ne or jail fi ample of a disincentive would be a ly restricted; they reasoned that cutting the trees sentence for harming an endangered species; now would ensure the woodpeckers never ar- this latter approach is the one taken by the ESA. rived. Similar fears prevented some landowners Conservationists have long debated the merits of from participating in recovery efforts for red- the two approaches. Theoretically, with unlimited cockaded woodpeckers and other endangered fi nancial resources, it should be possible to protect species. Why go out of one ’ s way to restore habi- and restore endangered species without incurring tat for endangered species if doing so could result much opposition. Landowners or resource users s property? ’ in restrictions on the use of one who stand to lose money or opportunities due to To remedy this situation, the federal govern- bought off ” restrictions on development could be “ “ safe ment implemented a program known as ’ sanappealing at whatever price they demand. It in 1995. Under this program, the govern- ” harbor scenario but also a deeply unrealistic one. Conser- ment assures landowners who engage in volun- vation programs are chronically under-funded. t endangered species that tary activities that bene fi Moreover, at least in the US, some of the regions they will not incur additional regulatory restric- of the country with the highest concentrations of tions as a result of their good deeds. In other imperiled species are also regions with some of the words, a landowner who restores a part of her highest real estate prices (e.g. San Francisco Bay fi property to bene and — t an endangered species et al. 1998), a congruence that would region; Ando agrees to maintain the restored habitat for a certain quickly break the budget of any incentives pro- period of time — will be given permission to undo gram. Fines and jail sentences are thus used to those improvements (i.e. develop the property) at deter developers from destroying the habitat of a later date, notwithstanding the fact that endangered golden-cheeked warblers ( Dendroica endangered species may now reside there. The ) in the US or poachers from killing chrysoparia reasoning is that without such assurances, the black rhinoceroses ( Diceros bicornis )inmanyAfri- landowner would never engage in the bene cial fi can countries. These types of laws, however, are action in the fi rst place. In some cases, government effective only if they are enforced, i.e., if violators agencies or private conservation organizations feel there is a non-trivial chance they will be caught have provided fi nancial assistance to landowners and punished. to cover some or all of the costs of habitat restora- Unfortunately, penalties sometime force peo- tion. To date, landowners have enrolled over 1.5 ple to engage in activities that are counterproduc- million hectares in the safe harbor program tive for conservation. Consider the case of ting a wide variety of fi (www.edf.org), bene ). Picoides borealis the red-cockaded woodpecker ( Bufo endangered species, from Houston toads ( © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

248 1 ENDANGERED SPECIES MANAGEMENT: THE US EXPERIENCE 233 houstonensis ) to northern aplomado falcons ( Falco contrast, fewer than 4% of invertebrate species femoralis septentrionalis ) to Utah prairie dogs ( Cy- have been assessed (Wilcove and Master 2005). ). nomys parvidens Among the species that have been assessed by Fee-hunting is another interesting and contro- experts, over 4800 are considered possibly ex- versial incentives program that has been used in tinct, critically imperiled, or imperiled; a strong parts of Africa to raise revenues and build local case can be made that all of them merit federal support for wildlife conservation. A limited num- protection under the ESA. Yet as of November ber of licenses to hunt game animals are sold, 2008, less than a third of these species had been with a portion of the revenues being returned to added to the federal endangered species list. the local communities on whose land the hunting Adding a species to the federal list is a time- occurs. The goal of such programs is to give these consuming and often controversial process. communities an economic incentive to conserve Moreover, the US Fish and Wildlife Service is wildlife, including animals such as lions ( Panthera chronically under-funded and under-staffed. leo ) Loxodonta africana ) and African elephants ( cult fi One can only imagine how much more dif that can be harmful to crops or dangerous to the situation must be in most of the developing people (Corn and Fletcher 1997). countries in the tropics, where the total number of Both disincentives and incentives play important species at risk is far greater, yet resources for roles in endangered species conservation. Disincen- conservation are far fewer. Hence, it does seem tives are most useful in the protection phase as a reasonable to conclude that a species-by-species means to discourage killing of endangered species approach to conservation inevitably will leave or further destruction of their habitats. Incentives many imperiled plants and animals unprotected are useful in the recovery phase as a means to and vulnerable to further losses. encourage landowners to restore habitats. Nonetheless, it would be dangerous to assume that endangered species conservation is a poor use of conservation resources. First, efforts to protect particular endangered species, especially 12.5 Limitations of endangered those with large territories or home ranges (e.g. species programs northern spotted owl, Strix occidentalis caurina ), Many conservation biologists believe that a focus often result in de facto protection for other on endangered species is misplaced. They argue endangered species that share the same ecosys- that the sheer number of species at risk makes a tem. By choosing the right species to focus on, species-by-species approach impractical or even ciency of fi conservationists can improve the ef futile. Thus, conservation efforts would be more their efforts. Second, many conservationists ef fi cient and successful if they were focused at the would argue that an essential goal of ecosystem level of whole ecosystems and landscapes, rather or landscape conservation should be to protect all than individual species. of the constituent species within that system, in- fi The US experience highlights the extreme dif - cluding the endangered ones. Moreover, certain culty of identifying and protecting even a fraction ecosystems, such as the Florida scrub or Hawai- ’ of a country s imperiled species, even when that ian rainforests, have such high concentrations of country is wealthy. To date, only about 15% of the endangered species that there is little practical known species in the US have been studied in difference between conservation programs suf cient detail to determine their conservation fi aimed at endangered species and those aimed at status (i.e. which species are in danger of extinc- the ecosystem as a whole. Finally, and perhaps gure is a tremendous fi tion). Embedded in this most importantly, endangered species have al- fl ecting a predictable variance between groups, re ways enjoyed tremendous support from the pub- bias in favor of vertebrates. Thus, the status of Grus lic. Species such as the whooping crane ( almost 100% of the mammals, birds, reptiles, americana ), giant panda ( Ailurapoda melanoleuca ), amphibians, and freshwater fi shes is known; in ), and Leontopithacus rosalia golden lion tamarin ( © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

249 Sodhi and Ehrlich: Conservation Biology for All . http://ukcatalogue.oup.com/product/9780199554249.do 234 CONSERVATION BIOLOGY FOR ALL A list of endangered species: http://www.iucnredlist. black rhinoceros have inspired millions of people · org/. around the world to care about biodiversity. While it may be impossible to identify and pro- tect each and every species that humanity has brought to the brink of extinction, there will al- REFERENCES ways be many that we care deeply about and Ando, A., Camm, J., Polasky, S., and Solow, A. (1998). cannot afford to lose. Species distributions, land values, and ef cient conser- fi , 2126 Science vation. 279 , – 2128. Baille, J. E. M., Hilton-Taylor, C., and Stuart, S. N., eds (2004). IUCN Red List of threatened species: a global Summary species assessment. IUCN, Gland, Switzerland. Endangered species conservation has three Clark, J. A., Hoekstra, J. M., Boersma, P. D., and Kareiva, P. · fi phases: identi cation, protection, and recovery. (2002). Improving U.S. Endangered Species Act recovery Protection can be directed toward species, sub- plans: key fi ndings and recommendations of the SCB · species, or populations. There are important eco- – ,1510 16 , Conservation Biology 1519. recovery plan project. Corn, M. L. and Fletcher, S. R. (1997). African elephant nomic and ecological trade-offs associated with issues: CITES and CAMPFIRE. Congressional Research protecting subspecies and populations. Service Report 97 752 ENR. Available online at http:// – Consistent, quantitative criteria for determining · digital.library.unt.edu/govdocs/crs/permalink/meta- the status of species have been developed by IUCN. crs-388:1 (accessed 9 November 2008). Protection of endangered species requires accu- · Dobson, A., Turner, W. R., and Wilcove, D. S. (2007). Con- rate knowledge of the threats to those species, the servation biology: unsolved problems and their policy location of existing populations, and land owner- Theoretical implications. In R. May and A. McLean, eds. ship patterns. ecology: principles and applications – , pp, 172 189. Third edi- Recovery of many endangered species will re- tion. Oxford University Press, Oxford, UK. · quire continual, active management of the habitat (2000). et al. Groves, C.R., Kutner, L. S., Stoms, D. M., or continual efforts to control populations of alien Owning up to our responsibilities. In B.A. Stein, L.S. Kutner, and J.S. Adams, eds Precious heritage: the status species. – , pp, 275 of biodiversity in the United States 300. Oxford Incentives may be needed to entice people to · University Press, Oxford, UK. participate in recovery programs. Hobbs, R. J. and Harris, J. A. (2001) Restoration ecology: s ecosystems in the new millennium. ’ repairing the earth Restoration Ecology 9 246. – , 239 , Hoekstra, J. M., Clark, J. A., Fagan, W. F., and Boersma, P. D. Suggested reading (2002). A comprehensive review of Endangered Species The en- Goble, D. D., Scott, J. M., and Davis, F. W. (2006). Ecological Applications , Act recovery plans. 640. – ,630 12 . Volume 1. Island Press, dangered species act at thirty Hughes, J. B., Daily, G. C., and Ehrlich, P. R. (1997). Population Washington, DC. 692. – ,689 278 , Science diversity: its extent and extinction. Wilcove, D. S. and Chen, L. Y. (1998). Management co- Li, Y. and Wilcove, D. S. (2005). Threats to vertebrate species Conservation Biology , 12 sts for endangered species. , ,147 in China and the United States. BioScience , 55 – 153. 1407. – 1405 (2008). The et al. Schipper, J., Chanson, J. S., Chiozza, F. et al. (1998). Wilcove, D. S., Rothstein, D., Dubow, J. A., status of the world s land and marine mammals: diver- ’ Quantifying threats to imperiled species in the Un- Science sity, threat, and knowledge. 322 , 225 – 230. , BioScience ited States. – , 607 48 , 615. et al. Scott, J. M., Goble, D. D., Wiens, J. A., (2005). Recovery of imperiled species under the Endangered Species Act: the need for a new approach. Frontiers in Ecology and the 3 , 383 Environment 389. , – Relevant websites Simberloff, D. and Stiling, P. (1996). Risks of species intro- US Fish and Wildlife Service, Endangered Species Pro- 78 , duced for biological control. Biological Conservation , · gram: http://www.fws.gov/endangered/. 192. – 185 © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

250 1 ENDANGERED SPECIES MANAGEMENT: THE US EXPERIENCE 235 Thomas, C.D., Cameron, A., Green, R. E., et al. (2004). Wilcove, D. S., McMillan, M., and Winston, K. C. (1993). , 145 148. 427 , Nature Extinction risk from climate change. – What exactly is an endangered species? An analysis of Wilcove, D. S. and Chen, L. Y. (1998). Management costs for Conservation the U.S. endangered species list: 1985 – 1991. – 1407. , ,1405 endangered species. Conservation Biology 12 – ,87 7 , 93. Biology Wilcove, D. S. and Master, L. L. (2005). How many (1998). et al. Wilcove, D. S., Rothstein, D., Dubow, J. A., endangered species are there in the United States? Quantifying threats to imperiled species in the United , 3 , 414 – Frontiers in Ecology and the Environment 420. 48 , 607 – 615. States. BioScience , © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

251 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CHAPTER 13 fi Conservation in human-modi ed landscapes Lian Pin Koh and Toby A. Gardner human impact (see Chapter 4) that can have neg- In the previous two chapters, we learn about the ative effects on biodiversity. This is especially so culties of prioritizing areas fi importance and dif because human beings have released toxic syn- for conservation (Chapter 11), and the manage- thetic organic chemicals, many of which are en- ment of endangered species in these habitats docrine disrupters (Box 13.1), that are now (Chapter 12). In this chapter, we discuss the chal- distributed from pole to pole. lenges of conserving biodiversity in degraded Although few data are available on changes to and modi fi ed landscapes with a focus on the the extent and condition of many habitats, re- tropical terrestrial biome, which is undergoing gions and ecosystems, what we do know is that, rapid deforestation and habitat degradation with few exceptions, changes that are currently (Chapter 4) and contains an untold diversity of underway are negative, anthropogenic in origin, rare and endemic species that are in urgent need ominously large and often accelerating (Balmford of conservation attention. We rst highlight the fi and Bond 2005). For example, the conversion of fi ed extent to which human activities have modi forests to agricultural land continues at a rate of natural ecosystems, and how these changes are approximately 13 million hectares per year, and fundamental in de fi ning ongoing conservation ed a full two- fi the last global assessment classi efforts around the world. We then outline oppor- ’ thirds of the world s forests as having been mod- tunities for conserving biodiversity within the fi i ed by human impacts (FAO 2006). dominant types of human land-use, including Some ecologists have gone so far as to consider logged forests, agroforestry systems, monocul- that the traditional concept of an intact ecosystem ture plantations, agricultural lands, urban areas, is obsolete, and instead propose a classi fi cation and regenerating land. We also highlight the system based on global patterns of human interac- highly dynamic nature of modi fi ed landscapes tion with ecosystems, demonstrating that much of and the need to recognize important human de- the world currently exists in the form of different ts that can be derived from con- velopment bene fi “ (Figure 13.1 and Plate 15; ” anthropogenic biomes servation action in these areas. Ellis and Ramankutty 2008). For many types of ecosystems, large areas of intact vegetation simply no longer exist, as is the case of the Atlantic forest cation fi 13.1 A history of human modi hotspot of Brazil which has been reduced, except wild nature “ and the concept of ” for a few conservation units, to a fragmented net- Efforts to improve human welfare have led to 100 ha), mainly work of very small remnants ( < landscapes and ecosystems worldwide being do- composed of secondary forest, and immersed in mesticated to enhance food supplies and reduce et al. 2009). agricultural or urban matrices (Ribeiro 2007). exposure to natural dangers (Kareiva et al. fi Even when we turn to areas that at rst appear As a consequence there are few places left on to be undisturbed by human impact, the bound- earth that have escaped some form of obvious pristine ” “ degraded ” can and aries between “ 236 Oxford University Press 2010. All rights reserved. For permissions please email: [email protected] ©

252 1 237 CONSERVATION IN HUMAN-MODIFIED LANDSCAPES Box 13.1 Endocrine disruption and biological diversity J. P. Myers the sudden and unprecedented arrival of Since the beginning of the Industrial hundreds, if not thousands, of chemicals capable Revolution, over 80 000 new chemicals have of disrupting hormone action and novel to body entered commerce and hence the biosphere. chemistry is a source of concern. These are compounds for which no organism Three key discoveries lie at the center of this has any evolutionary history and hence no – revolution in toxicology. First, hormones and opportunity to evolve over generations any contaminants that behave like hormones can – metabolic protections against potential harm. cause completely different effects at different Depending upon how they are used and upon levels of exposure. This is because the suite of their chemical characteristics, they have dispersed regulated by a hormone can ‐ or down ‐ genes up widely, many globally. For example, whales vary dramatically as the concentration of the feeding hundreds of feet beneath the surface of hormone varies. And at high levels, the the mid ‐ Atlantic accumulate brominated fl ame like contaminant) can ‐ hormone (or a hormone retardants from their prey. Bark of mature trees be overtly toxic, shutting down gene from virtually any forest in the world contains expression altogether. Hence all of the tests pesticides and industrial pollutants, even though that toxicologists have run that assume high they may be thousands of miles from the source. dose testing will catch low dose effects are Penguins in the Antarctic store persistent organic invalid. Compounds judged to be safe based on pollutants that have been carried to the Antarctic data from high dose testing may not be. Some, by atmospheric transport and stored for decades widely used in commerce, clearly are not. in glacial snow but that are now being liberated Second, changes in gene expression as an by global warming. Seemingly pristine cloud — organism is developing in the womb, as an egg, forest in Costa Rica is more contaminated by the as a larvae or a tadpole, etc — can have lifelong pesticides used on lowland banana plantations consequences, affecting virtually every system of than forest adjacent to the bananas, because the the body, including altering fertility, immune he lowland but are carried pesticides volatilize in t system function, neurological competency (and downwind and upward into the mountains, thus behavior), etc. Frogs in suburban Florida are where they condense because of lower less likely to be feminized than frogs in temperatures. disrupting ‐ agricultural Florida, where endocrine Decades of toxicological research focused on re used. Frogs exposed as agricultural chemicals a the effects of high exposures, which tadpoles to a mixture of pesticides die from unquestionably can be serious, indeed directly bacterial meningitis when adult, from a common lethal. Over the past 20 years, however, research bacteria easily resisted by control animals. has emerged revealing that this approach to cantly in their fi Third, individuals vary signi toxicology was blind to serious effects that stem capacity to metabolize these compounds and me contaminants to from the ability of so c variants of genes are resist their effects. Speci fi interfere with hormones, altering gene more, or less, effective at safely metabolizing a expression, even at extremely low doses. These contaminant and rendering it harmless. In endocrine disruption effects, deemed ‘ ’ have people, for example, there is at least a 40 ‐ forced toxicologists to rethink how they assess risk fold and have raised a wide array of questions about difference in capacity to metabolize how contaminants may be affecting the organophosphate pesticides. biosphere in unexpected ways, since hormones ... This is the stuff of Darwin heritable regulate a wide array of biological functions in differences among individuals that alter reover, the signaling both plants and animals. Mo reproductive success but it is happening to ... systems used by the endocrine system are highly people and biodiversity at a pace that may be conserved evolutionarily, operating in essentially unprecedented in the history of most, if not all fi sh and mammals despite 300 the same ways in species. Hundreds, if not more, of compounds million years of evolutionary separation. Hence capable of altering gene expression at low levels continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

253 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 238 Box 13.1 (Continued) In the most elegant experimental fi eld test to of exposure have been introduced into the date of population ‐ level effects of endocrine biosphere in fewer than 200 years. They alter disruptors, Kidd (2007) contaminated a et al. fertility, cognition, immune and cardiovascular lake in western Ontario with an active function, and more. The inescapable prediction, ingredient of birth control pills (17alpha ‐ clearly speculative but highly plausible, is that this ethynylestradiol), maintaining the past 200 years has been a period of remarkable, if contaminant ’ s concentration at 5 – 6 parts per not unprecedented speed in the molecular trillion for two years. This concentration is just evolution of life on earth. above levels typically found in sewage ef fl uent Documented effects extend to interactions and also in surface waters. The treatment led among species as well. For example, several initially to delayed sexual development of cacy of fi environmental estrogens decrease the ef fathead minnows in the lake. By the second bacteria and communication between Rhizobium year they observed that some males had eggs in their leguminaceous hosts, reducing nitrogen testis). And by the end of the their testes (ova ‐ fi xation. One widely used herbicide, atrazine, seventh year, long after the treatments were both increases the likelihood that ponds will halted, very few individuals were left. The trematode parasites, contain large numbers of population had crashed. There are many which cause limb deformities in frogs, it also sh testis in fresh water ‐ reports of ova fi ’ s immune defenses against undermines the frog populations from around the world. trematode infections. How large a role endocrine disruption plays in These emerging discoveries have come as biodiversity declines isn ’ surprises to traditional toxicology, because they t yet clear, because few raise questions about many chemicals in common conservation biologists have included these use that based on traditional approaches had mechanisms in the suite of hypotheses their been deemed safe. For conservation biologists, studies are designed to test. The solutions to they offer competing hypotheses to test against biodiversity declines caused by endocrine other interpretations. For example, is the disruption will contrast sharply with those from disappearance of the golden toad ( Bufo more conventional forces. No harvest zones and ) from Costa Rica a result of global periglenes arti fi cial reefs, for example, will prove futile if warming? Or have the pesticides now known to shell fi sh declines are caused by chemical cant concentrations in Costa fi be present in signi contamination. Hence in the search for tools to Rican cloud forests undermined their viability? maintain biodiversity, it is imperative that What is the role of contaminant ‐ reduced immune conservation biologists science widens to ’ ‐ system function in fungal caused deaths in frogs, incorporate these effects. clearly an important factor in amphibian extinctions? Is the chytrid fungus new? Or are frogs less able to withstand infestation? Was the Relevant website lake trout extinction in the Great Lakes the result • Synopses of new studies on endocrine disruption: fi ‐ of lampreys and over shing, or because dioxin http://tinyurl.com/a6puq7. sediment loads became so heavy that 100% of fry died? Have impairments by endocrine disrupters in the ability of young salmon to switch their osmoregulation from fresh water to salt water REFERENCE AND SUGGESTED READING when they reach the ocean in their fi rst Colborn, T., Dumanoski, D., and Myers, J. P. (1996). Our downstream migration contributed to salmon . Dutton, New York, NY. stolen future c coast? Are fi population declines along the Paci Cook, P. M., Robbins, J. A., Endicott, D. D., et al. (2003). declines in Chesapeake Bay oysters and crabs a ‐ mediated early life Effects of aryl hydrocarbon receptor result of invertebrate vulnerability to endocrine ‐ stage toxicity on Lake Trout populations in Lake Ontario disrupting contaminants? Is the relationship during the 20th century. Environmental Science and between coral and their symbiotic algae 37 – 3877. Technology , , 3864 disrupted by contaminatio n? Does this contribute et al. (2007). Accumu- Dally, G. L., Lei, Y. D., Teixeira, C., to coral bleaching? ‐ lation of current use pesticides in Neotropical montane continues © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

254 1 CONSERVATION IN HUMAN-MODIFIED LANDSCAPES 239 (Continued) Box 13.1 Proceedings of the National synthetic estrogen. Environmental Science and Technology , forests. , 41 Academy of Science of the United States of America , 1123. – 1118 , 8897 104 – 8901. ‐ Gore, A. C. (2007). Introduction to endocrine disrupting Welshons, W. V., Nagel, S. C., and vom Saal, F. S. (2006). chemicals. In A.C. Gore, ed. ‐ disrupting che- Endocrine Large effects from small exposures: III. Endocrine 8. – micals: From basic research to clinical practice , pp. 3 mechanisms mediating effects of bisphenol A at Humana Press, New Jersey. , 147 , Endocrinology levels of human exposure. Kidd, K. A., Blanch fi eld, P. J., Mills, K. H., et al. (2007). – S56 S69. sh population after exposure to a fi Collapse of a quickly become blurred on closer inspection. Ar- and urbanized centres (Heckenberger et al. 2003; chaeological and paleoecological studies over the 2004). Much of the lowland rainforests et al. Willis last two decades suggest that many contempo- of the Congo basin had similarly experienced ex- rary pristine habitats have in fact undergone tensive human habitation, forest clearance, and some form of human disturbance in the past agricultural activities between  3000 and  1600 (Figure 13.2 and Plate 16; Willis 2005; Willis et al. nds of stone years ago, as evidenced by extensive fi and Birks 2006; see Chapter 14). tools, oil palm nuts, charcoal horizons (subsoil For example, the Upper Xingu region of Brazil layers of charcoal), banana phytoliths (silica bodies comprises one of the largest contiguous tracts of found in plants preserved in sediments), and pot- tropical rainforest in the Amazon today. Emerging tery fragments (Mbida et al. 2000; White 2001). archaeological evidence suggests that parts of this Many further examples of extensive pre-European region had been densely populated with disturbance have been found in areas that conser-  pre-European human settlements (circa 1250 to pristine “ vationists today frequently describe as ” 1600 A.D.), and that extensive forests underwent  “ , including Southeast Asia, Papua New or intact ” large-scale transformation to agricultural areas 2004). Guinea and Central America (Willis et al. Dense settlements 11: Urban 12: Dense settlements Villages 21: Rice 22: Irrigated 23: Cropped & pastoral 24: Pastoral Forested 25: Rainfed 51: Populated 26: Rainfed mosaic 52: Remote Croplands 31: Residential irrigated Rangelands Wildlands 32: Residential rainfed 41: Residential 61: Wild forests 33: Populated irrigated 42: Populated 62: Sparse trees 34: Populated rainfed 43: Remote 63: Barren 35: Remote cover analysis reveals that that less than a quarter of the Earth Figure 13.1 s ice ‐ free land can still be considered Anthropogenic biomes. Global land ‐ ’ as wild. Biomes displayed on the map are organized into groups and are ranked according to human population density. Reprinted from Ellis and Ramankutty (2008). © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

255 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 240 Southern Thailand Prehistoric arboriculture and land management from 8000 years ago Central Amazonia Anthropogenic “terra preta” soils from 3500 years ago Gabon Iron–working furnaces from 961 B.C. Papua New Guinea Agriculture from 7000 years ago Upper Xingu River Region Intensive management of the landscape started 1250 to 1600 A.D. Lowland Congo Basin Stone tools, oil palm nuts, banana phytoliths, and pottery fragments from 3000 to 1600 years ago New Georgia “Virgin” rainforest is 150 years old ” fi tropical rainforest. Archaeological and paleoecological studies suggest that rainforests in “ Figure 13.2 cation of Evidence of human modi pristine the Amazon basin, the Congo basin, and Southeast Asia have regenerated from disturbance by prehistoric human settlements. Reprinted from Willis (2004) with permission from AAAS (American Association for the Advancement of Science). et al. In most of these cases, forest regeneration followed broader strategy to safeguard the future of the the abandonment of human settlements and agri- s biota. Gap analyses show that approxi- ’ world cultural activities resulting in the old-growth ’ s threatened spe- mately one quarter of the world stands that are regarded as pristine today. cies live outside protected areas (Rodrigues et al. 2004; Chapter 11), and that most of the world ’ s fi terrestrial ecoregions fall signi cantly short of the ed fi 13.2 Conservation in a human-modi 10% protection target proposed by the IUCN world et al. (Figure 13.3 and Plate 17; Schmitt 2009). Even where they exist, the integrity of protected How does all this evidence of historical and on- areas is often threatened by encroachment and fi cation of the natural world going human modi illegal extraction in areas that are undergoing relate to efforts to conserve biological diversity widespread deforestation (Pedlowski et al. 2005), today? There are at least two very profound im- and management of neighboring areas is vital to plications. ensuring their long-term viability (Wittemyer First, the sheer extent to which we have domi- et al. et al. 2008; Sodhi 2008). nated the biosphere (terrestrial, freshwater, and Second, evidence of historical recovery in areas marine) (Ehrlich and Ehrlich 2008) means that we that once hosted high levels of human activity have no choice but to integrate conservation ef- illustrates that while long-time scales are often forts with other human activities. It is broadly involved, the biotic impacts of many types of accepted that strictly protected areas provide a disturbance might not be completely irreversible. necessary yet grossly inadequate component of a © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

256 1 the Amazon, Southeast raphic realms. White areas indicate Australasia te biogeog Indo-Malay Not considered forested (Under 0.1% forest cover) Robinson Projection Afrotropic 50% – 100% Antarctic Palearctic ecoregions. The highest levels of protection can be seen in parts of Australia, 25% – 50% Basin in Central Africa and Northern Boreal forests. Black lines indica Neotropic Nearctic 10% – 25% (2009). et al. Oceania Under the 10% Target Percentage forest area protected: Distribution of the percentage of protected forest area within WWF Figure 13.3 Asia, and Alaska. Notable areas of low protection include the Congo no forest cover. Reprinted from Schmitt © Oxford University Press 2010. All rights reserved. For permissions please email: [email protected]

257 Sodhi and Ehrlich: . http://ukcatalogue.oup.com/product/9780199554249.do Conservation Biology for All CONSERVATION BIOLOGY FOR ALL 242 It is clear therefore, that partially modi ed land- fi 13.3 Selectively logged forests scapes are an important and valuable asset for As of 2005, approximately one third of the biodiversity conservation, and should not be a total of 1.3 billion hectares — s forests ’ world — overlooked by biologists and conservationists, were designated primarily for timber production - and abandoned to yet further levels of intensi fi (FAO 2006). In 2006, member nations of the Inter- cation. national Tropical Timber Organization (ITTO) ex- Against this backdrop of necessity and hope, it ported over 13 million cubic meters of tropical is self-evident that the future of much of the non-coniferous logs worth US$2.1 billion, making ’ s biodiversity depends on the effective world a substantial contribution to the economies of ed systems (Daily fi management of human-modi these nations (ITTO 2007). Logging activity on 2001; Lindenmayer and Franklin 2002; Bawa et al. this massive scale has resulted in huge areas of 2004). To face up to this challenge conservation forest being degraded following the selective re- biology needs to adopt a research perspective moval of high-value trees, and the collateral dam- that incorporates human activities as integral age associated with tree felling and extraction. components of ecosystems, and place a strong et al. (2005) estimated that in the Brazilian Asner emphasis on understanding the coupled social- Amazon between 1999 and 2002 the area of rain- ed lands (Palmer ecological dynamics of modi fi forest annually degraded by logging is approxi- et al. 2004; Sayer and Maginnis 2005). mately the same as that which is clear-felled for Ultimately conservation biologists need to agriculture (between 12 and 19 million hecatres). improve their understanding of how different Although all logging activity has a negative types of human land-use may confer different impact on the structure and composition of the fi bene ts for conservation. To what extent can forest, the severity of this impact depends on the modi fi ed land-uses support viable populations logging intensity, including the number of trees of native species, and help ensure the long-term removed per ha, length of the rotation time, and viability of isolated remnants of undisturbed veg- site management practices. The density of felled etation? Understanding which native species can trees varies among regions and management maintain viable populations in modi ed land- fi regimes from as few as one tree every several scapes, and under what management regimes, is has (e.g. mahogany, in Swietenia macrophylla one of the greatest challenges currently facing South America) to more than 15/ha in lowland conservation biologists (Fischer and Linden- dipterocarp forests of Southeast Asia (Fimbel et al. et al. mayer 2007; Sekercioglu , 2007; Sodhi 2008; 2001). In the last few decades Reduced Impact 2009a). While it is generally accept- et al. Chazdon Logging (RIL) techniques have been developed ed that the conversion of primary habitat for that involve careful planning and controlled har- intensive agriculture inevitably leads to dramatic vesting (e.g. preliminary inventories, road losses in biodiversity (Donald 2004; Sodhi planning, directional felling) to greatly minimize 2009), more information is certainly needed. et al. deleterious impacts (Fimbel et al. 2001; Putz et al. Conservation biologists are particularly uncertain 2008). of the extent to which more structur