New Directions in Conservation Medicine

New Directions in Conservation Medicine Applied Cases of Ecological Health

Edited by A. Alonso Aguirre, Richard S. Ostfeld, and Peter Daszak

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CONTRIBUTORS

Roberto F. Aguilar, D.V.M. Veterinarian Cape Wildlife Center Humane Society of the United States Barnstable, Massachusetts

John Arnason, Ph.D. Professor Department of Biology University of Ottawa Ottawa, Ontario, Canada

A. Alonso Aguirre, D.V.M., M.S., Ph.D. Associate Professor Department of Environmental Science and Policy George Mason University Executive Director Smithsonian-Mason School of Conservation Front Royal, Virginia

Michael J. Balick, Ph.D. Vice President for Botanical Science Director and Philecology Curator Institute of Economic Botany The New York Botanical Garden Bronx, New York

Anne M. Alexander, M.A., Ph.D. Director of International Programs Department of Economics and Finance University of Wyoming Laramie, Wyoming

Rebecca Bartel, M.S., Ph.D. Terrestrial Ecologist Inventory and Monitoring Program National Wildlife Refuge System U.S. Fish and Wildlife Service Manteo, North Carolina

Emily Almberg, M.S. Department of Biology Pennsylvania State University University Park, Pennsylvania

Val R. Beasley, D.V.M., Ph.D., Dipl.A.B.V.T. Professor Emeritus of Veterinary, Wildlife, and Ecological Toxicology Department of Comparative Biosciences College of Veterinary Medicine University of Illinois at Urbana-Champaign, Urbana, Illinois

Sonia Altizer, Ph.D. Associate Professor Odum School of Ecology University of Georgia Athens, Georgia

Julieta Benítez-Malvido, M.S., Ph.D. Centro de Investigaciones en Ecosistemas Universidad Nacional Autónoma de México Morelia, Michoacán, Mexico

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Contributors Aaron Bernstein, M.P.H., M.D. Associate Director, Center for Health and the Global Environment Instructor in Medicine Harvard Medical School Physician in Medicine, Children’s Hospital Boston Boston, Massachusetts Jon Bielby, Ph.D. Postdoctoral Researcher Institute of Zoology Zoological Society of London London, Great Britain Leslie Bienen, D.V.M., M.F.A. Center for Large Landscape Conservation Bozeman, Montana Evan S Blumer, V.M.D., M.S. Principal OsoMono LTD Gahanna, Ohio and Retired Executive Director The Wilds Cumberland, Ohio

Cheryl J. Briggs, Ph.D. Professor Department of Ecology, Evolution and Marine Biology University of California, Santa Barbara Santa Barbara, California Ilana L. Brito, Ph.D. Postdoctoral Research Fellow Civil and Environmental Engineering Department Massachusetts Institute of Technology Cambridge, Massachusetts John S. Brownstein, Ph.D. Director and Assistant Professor Children’s Hospital Boston Harvard Medical School Harvard-MIT Division of Health Sciences and Technology Boston, Massachusetts Victor Cal Belize Indigenous Training Institute Punta Gorda, Belize

Tiffany L. Bogich, Ph.D. Postdoctoral Fellow Fogarty International Center National Institutes of Health Bethesda, Maryland

Roberto Carrasco-Hernández, M.S. Facultad de Medicina Veterinaria y Zootecnia Universidad Nacional Autónoma de México Mexico City, Mexico

Bob H. Bokma, D.V.M., M.P.V.M. Export Animal Products National Center for Import and Export Veterinary Services USDA Animal and Plant Health Inspection Service Riverdale, Maryland

Colin A. Chapman, Ph.D. Professor Canada Research Chair Fellow of the Royal Society Department of Anthropology McGill School of Environment McGill University Montreal, Québec, Canada

Christopher J. Brand, M.S., Ph.D. Branch Chief, Field and Laboratory Research U.S. Geological Survey National Wildlife Health Center Madison, Wisconsin

Edward E. Clark, Jr., B.A. President Wildlife Center of Virginia Waynesboro, Virginia

Edward B. Breitschwerdt, D.V.M. Professor of Internal Medicine College of Veterinary Medicine

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North Carolina State University Raleigh, North Carolina

Axel Cloeckaert, Ph.D. Institut National de la Recherche Agronomique Infectiologie Animale et Santé Publique Nouzilly, France

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Contributors Paul C. Cross, Ph.D. U.S. Geological Survey Northern Rocky Mountain Science Center Bozeman, Montana Patricia Curry, D.V.M. Ph.D. Candidate, Medical Sciences Department of Ecosystem and Public Health Faculty of Veterinary Medicine, University of Calgary Calgary, Alberta, Canada Peter Daszak, Ph.D. President EcoHealth Alliance New York, New York Joseph Le Doux Diffo, M.Sc. Ecology Team Leader Global Viral Forecasting Yaounde, Cameroon Cyrille F. Djoko, M.S. Regional Laboratory Director for Central Africa Global Viral Forecasting Yaounde, Cameroon Marion L. East, Ph.D. Research Scientist Evolutionary Ecology Research Group Leibniz Institute for Zoo and Wildlife Research Berlin, Germany Jonathan H. Epstein, D.V.M., M.P.H. Associate Vice President EcoHealth Alliance New York, New York Fernando Esponda, Ph.D. Computer Science Department Instituto Tecnológico Autónomo de Mexico Mexico City, Mexico Joseph N. Fair, M.P.H., Ph.D. Vice President, Executive Director – Government Services Global Viral Forecasting San Francisco, California Anne Fairbrother, D.V.M., M.S., Ph.D. Senior Managing Scientist EcoSciences Exponent Seattle, Washington

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Hume E. Field, B.V.Sc., M.S., Ph.D., M.A.C.V.S. Principal Scientist Queensland Centre for Emerging Infectious Diseases Department of Employment, Economic Development & Innovation Brisbane, Queensland, Australia Claudia Filoni, M.S., D.V.M., Ph.D. Professor Infectious Diseases and Microbiology Universidade Paulista Researcher and Member Instituto Brasileiro para Medicina da Conservação (TRÍADE) São Paulo, Brazil David C. Finnoff, Ph.D. Associate Professor Department of Economics and Finance University of Wyoming Laramie, Wyoming Spencer E. Fire, M.S., Ph.D. Biologist Marine Biotoxins Program NOAA National Ocean Service Center for Coastal Environmental Health and Biomolecular Research Charleston, South Carolina Matthew C. Fisher, Ph.D. Reader in Molecular Epidemiology Department of Infectious Disease Epidemiology Imperial College London St. Mary’s Campus London, Great Britain Patrick Foley, M.S., Ph.D. Department of Biological Sciences California State University Sacramento, California Janet E. Foley, D.V.M., Ph.D. Professor, Research Epidemiologist Department of Medicine and Epidemiology School of Veterinary Medicine University of California Davis, California

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Contributors Geoffrey Foster, C.Sci., F.I.B.M.S., Ph.D. Veterinary Centre Manager SAC C Veterinary Services Scottish Agricultural College Inverness, United Kingdom Sebastian Funk, Ph.D., Dipl. Phys. Postdoctoral Researcher Institute of Zoology Zoological Society of London London, Great Britain Trenton W. J. Garner, M.S., Ph.D. Senior Research Fellow Institute of Zoology Zoological Society of London London, Great Britain Claire Geoghegan, M.Res. Ph.D. Candidate and Researcher Mammal Research Institute Department of Zoology and Entomology University of Pretoria Pretoria, Guateng, South Africa E. Paul Gibbs, B.V.Sc., Ph.D., F.R.C.V.S. Associate Dean for Students and Instruction Professor of Virology College of Veterinary Medicine University of Florida Gainesville, Florida Jacques Godfroid, D.V.M., M.S., Ph.D. Professor, Head of the Section of Arctic Veterinary Medicine Norwegian School of Veterinary Science Tromsø, Norway Tony L. Goldberg, M.S., D.V.M., Ph.D. Professor of Epidemiology Department of Pathobiological Sciences School of Veterinary Medicine University of Wisconsin-Madison Madison, Wisconsin Andrés Gómez, Ph.D. Biodiversity Scientist Center for Biodiversity and Conservation American Museum of Natural History New York, New York

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Larry J. Gorenflo, Ph.D. Associate Professor Department of Landscape Architecture Stuckeman School of Architecture and Landscape Architecture University Park, Pennsylvania Christian Gortázar, D.V.M., Ph.D. Head, Wildlife Disease Department National Wildlife Research Institute IREC (CSIC-UCLM-JCCM) Ciudad Real, Spain K. Christiana Grim, D.V.M. Research Associate Center for Species Survival Smithsonian Conservation Biology Institute Front Royal, Virginia Timm Harder, Ph.D. Senior Scientist Friedrich Loeffler Institute Institute of Diagnostic Virology OIE and National Reference Library for Avian Influenza Insel Riems, Greifswalk, Germany Craig A. Harms, D.V.M., Ph.D., Dipl. A.C.Z.M. Associate Professor of Aquatic, Wildlife, and Zoo Medicine College of Veterinary Medicine Center for Marine Sciences and Technology North Carolina State University Morehead City, North Carolina Katherine Herrera, B.S. Research Assistant Institute of Economic Botany New York Botanical Garden Bronx, New York Heribert Hofer, D.Phil. Evolutionary Ecology Research Group Director Leibniz Institute for Zoo and Wildlife Research Berlin, Germany Pierre Horwitz, Ph.D. Associate Professor School of Natural Sciences Edith Cowan University Joondalup, Western Australia, Australia

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Contributors Parviez R. Hosseini, Ph.D. Senior Research Fellow EcoHealth Alliance New York, New York Sara E. Howard, B.A. Program Assistant EcoHealth Alliance New York, New York Peter J. Hudson, F.R.S. Willaman Professor of Biology Director of the Huck Institutes of Life Sciences Pennsylvania State University University Park, Pennsylvania Thierry Jauniaux, D.V.M., Ph.D. Assistant Professor Veterinary Pathology University of Liege Liege, Belgium David A. Jessup, D.V.M., M.P.V.M., Dipl. A.C.Z.M. Senior Wildlife Veterinarian, Retired Marine Wildlife Veterinary Care and Research Center California Department of Fish and Game Executive Manager Wildlife Disease Association Santa Cruz, California Damien O. Joly, Ph.D. Associate Director Wildlife Health Monitoring and Epidemiology Wildlife Conservation Society Nanaimo, British Columbia, Canada Menna Jones, Ph.D. Australian Research Council Future Fellow School of Zoology University of Tasmania Hobart, Tasmania, Australia Kate E. Jones, Ph.D. Senior Research Fellow Institute of Zoology Zoological Society of London London, Great Britain

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Rodrigo Silva Pinto Jorge, D.V.M., Ph.D. Environmental Analyst Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio/MMA) Researcher Instituto Brasileiro para Medicina da Conservação (TRÍADE) Brasilia, D.F., Brazil Laura H. Kahn, M.D., M.P.H., M.P.P. Research Scholar Program on Science and Global Security Woodrow Wilson School of Public and International Affairs Princeton University Princeton, New Jersey William B. Karesh, D.V.M. Executive Vice President for Health and Policy EcoHealth Alliance New York, New York Thomas J. Keefe, Ph.D. Professor, Biostatistics Department of Environmental and Radiological Health Sciences Colorado State University Fort Collins, Colorado Felicia Keesing, Ph.D. Associate Professor of Biology Bard College Annandale, New York Kevin Knight Department of Biology University of Ottawa Ottawa, Ontario, Canada Thijs Kuiken, D.V.M., Ph.D., Dipl. A.C.V.P. Professor of Comparative Pathology Department of Virology Erasmus University Medical Center Rotterdam, The Netherlands Susan Kutz, D.V.M., Ph.D. Associate Professor Department of Ecosystem and Public Health Faculty of Veterinary Medicine, University of Calgary Calgary, Alberta, Canada

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Contributors Wayne Law, Ph.D. Postdoctoral Research Associate Institute of Economic Botany New York Botanical Garden Bronx, New York

Ricardo G. Maggi, M.S., Ph.D. Research Assistant Professor College of Veterinary Medicine North Carolina State University Raleigh, North Carolina

Matthew LeBreton, B.Sc. Ecology Director Global Viral Forecasting Yaounde, Cameroon

Paulo Rogerio Mangini, D.V.M., M.S., Ph.D. Associate Researcher Instituto de Pesquisas Ecológicas (IPÊ) Researcher and Council of Directors Instituto Brasileiro para Medicina da Conservação (TRÍADE) Curitiba, Paraná, Brazil

Roberta A. Lee, M.D. Vice Chair Department of Integrative Medicine Co-Director Fellowship in Integrative Medicine Continuum Center for Health and Healing Beth Israel Medical Center New York, New York Jeffrey M. Levengood, Ph.D. Wildlife Toxicologist Department of Comparative Biosciences and Illinois Natural History Survey University of Illinois at Urbana-Champaign Urbana, Illinois Marc A. Levy, M.A. Deputy Director Center for International Earth Science Information Network Earth Institute Palisades, New York Elizabeth Loh, M.S. Research Scientist EcoHealth Alliance New York, New York Guillermo López, D.V.M., Ph.D. EGMASA-Consejería de Medio Ambiente de la Junta de Andalucia Córdoba, Spain Thomas E. Lovejoy, Ph.D. Professor Environmental Science and Policy George Mason University Fairfax, Virginia Biodiversity Chair The H. John Heinz III Center for Science, Economics and the Environment Washington, D.C.

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Daniel Martineau, D.V.M., M.S., Ph.D. Associate Professor Département de Pathologie et Microbiologie Faculté de Médecine Vétérinaire Université de Montréal St. Hyacinthe, Québec, Canada Fernando Martínez, D.V.M., M.Sc. Programa de Conservación Ex Situ del Lince Ibérico Centro de Cría en Cautividad El Acebuche Matalascañas, Huelva, Spain Maria Fernanda Vianna Marvulo, M.S., D.V.M., Ph.D. Professor of Veterinary Medicine and Public Health Universidade Federal Rural de Pernambuco (UFRPE) Researcher and Council of Directors Instituto Brasileiro para Medicina da Conservação (TRÍADE) Recife, Pernambuco, Brazil Jonna A. K. Mazet, D.V.M., M.P.V.M., Ph.D. Professor and Director Wildlife Health Center One Health Institute University of California Davis, California Hamish McCallum, Ph.D., D.I.C. Head Griffith School of Environment Griffith University Nathan, Queensland, Australia

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Contributors Dave L. McRuer, M.S., D.V.M., Dipl. A.C.V.P.M. Director of Veterinary Services Wildlife Center of Virginia Waynesboro, Virginia Melissa A. Miller, D.V.M., M.S., Ph.D. Senior Wildlife Veterinarian Marine Wildlife Veterinary Care and Research Center California Department of Fish and Game Santa Cruz, California Thomas P. Monath, M.D. Partner Pandemic and Biodefense Fund Kleiner Perkins Caufield & Byers Harvary, Massachusetts Edgardo Moreno, Ph.D. Professor of Cellular Biology Programa de Investigación en Enfermedades Tropicales Escuela de Medicina Veterinaria Universidad Nacional Heredia, Costa Rica Stephen S. Morse, Ph.D. Professor Department of Epidemiology Columbia University Mailman School of Public Health New York, New York Alessandra Nava, D.V.M., Ph.D. Senior Scientist EcoHealth Alliance Associate Researcher Biotropicos Institute São Paulo, Brazil Elizabeth S. Nichols, M.A., PhD. Visiting Scientist Center for Biodiversity and Conservation American Museum of Natural History New York, New York Ingebjørg Helena Nymo, D.V.M. Ph.D. Candidate Section of Arctic Veterinary Medicine Norwegian School of Veterinary Science Tromsø, Norway

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Kevin J. Olival, Ph.D. Senior Research Scientist EcoHealth Alliance New York, New York Glenn H. Olsen, D.V.M., Ph.D. Veterinary Medical Officer U.S. Geological Survey Patuxent Wildlife Research Center Laurel, Maryland Nancy Ortiz, M.P.H. Project Coordinator Global Viral Forecasting San Francisco, California Richard S. Ostfeld, Ph.D. Senior Scientist Cary Institute of Ecosystem Studies Millbrook, New York Sarah B. Paige, M.P.H., Ph.D. Research Associate/Program Manager Center for Community Health and Evaluation Group Health Research Institute Seattle, Washington Susan L. Perkins, Ph.D. Associate Curator and Professor Department of Invertebrate Zoology Sackler Institute for Comparative Genomics Richard Gilder Graduate School American Museum of Natural History New York, New York Todd J. Pesek, M.D. Associate Professor School of Health Sciences Director Center for Healing Across Cultures College of Sciences and Health Professions Cleveland State University Cleveland, Ohio Brian L. Pike, M.P.H., Ph.D. Director of Laboratory Sciences Global Viral Forecasting San Francisco, California

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Contributors Raina K. Plowright, B.V.Sc., M.S., Ph.D. David H. Smith Conservation Research Fellow Center for Infectious Disease Dynamics Pennsylvania State University University Park, Pennsylvania Julia B. Ponder, D.V.M. Executive Director The Raptor Center Assistant Clinical Professor College of Veterinary Medicine University of Minnesota St. Paul, Minnesota Wolfgang Preiser Prof. Dr. med. Dr. med. habil, D.T.M.&H., M.R.C.Path. Professor and Head: Division of Medical Virology Department of Pathology Faculty of Health Sciences Stellenbosch University and National Health Laboratory Service Tygerberg Tygerberg, South Africa Margo J. Pybus, Ph.D. Provincial Wildlife Disease Specialist Fish and Wildlife Division Edmonton, Alberta, Canada Barnett A. Rattner, Ph.D. Ecotoxicologist U.S. Geological Survey Patuxent Wildlife Research Center Beltsville Laboratory Beltsville, Maryland William C. Raynor, M.S. Director Micronesia Program The Nature Conservancy Kolonia, Pohnpei, Federated State of Micronesia Anne W. Rimoin, Ph.D. Associate Professor Department of Epidemiology UCLA School of Public Health Los Angeles, California

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Gail E. Rosen, M.S. Center for Infection and Immunity Mailman School of Public Health Columbia University New York, New York Melinda K. Rostal, M.P.H., D.V.M. Field Veterinarian EcoHealth Alliance New York, New York Karen E. Saylors, Ph.D. Director, Behavioral Sciences Global Viral Forecasting San Francisco, California Lisa M. Schloegel, B.A. Consulting Research Scientist EcoHealth Alliance New York, New York Jason F. Shogren, Ph.D. Department Chair Stroock Professor of Natural Resource Conservation and Management Department of Economics and Finance University of Wyoming Laramie, Wyoming Todd K. Shury, D.V.M. Wildlife Health Specialist Parks Canada Adjunct Professor Department of Veterinary Pathology Western College of Veterinary Medicine Saskatoon, Saskatchewan, Canada Jean Carlos Ramos Silva, M.S., D.V.M., Ph.D. Professor Veterinary Medicine and Public Health Universidade Federal Rural de Pernambuco (UFRPE) Researcher Instituto Brasileiro para Medicina da Conservação (TRÍADE) Recife, Pernambuco, Brazil

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Contributors Marcelo Renan de Deus Santos, D.V.M., M.S. President Instituto de Ensino Pesquisa e Preservação Ambiental Marcos Daniel Professor Vila Velha University Conservation Medicine Espíritu Santo, Brazil Jonathan M. Sleeman, M.A., Vet. M.B., Dipl. A.C.Z.M., Dipl. E.C.Z.M., M.R.C.V.S. Director U.S. Geological Survey National Wildlife Health Center Madison, Wisconsin Katherine F. Smith, Ph.D. Assistant Professor Department of Ecology and Evolutionary Biology Brown University Providence, Rhode Island Francisca Sohl The Conservation Society of Pohnpei Kolonia, Pohnpei, Micronesia Gerardo Suzán, Ph.D. Facultad de Medicina Veterinaria y Zootecnia Universidad Nacional Autónoma de México Mexico City, Mexico Gary M. Tabor, V.M.D., M.E.S. Director Center for Large Landscape Conservation Bozeman, Montana Ubald Tamoufe, M.S., M.P.H. Central Africa Regional Director Global Viral Forecasting Yaounde, Cameroon Morten Tryland, D.V.M., Ph.D. Professor Section of Arctic Veterinary Medicine Norwegian School of Veterinary Science Tromsø, Norway

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Frances M. Van Dolah, Ph.D. Research Biochemist Marine Biotoxins Program NOAA National Ocean Service Center for Coastal Environmental Health and Biomolecular Research Charleston, South Carolina Carlos Eduardo da Silva Verona, D.V.M., M.S., Ph.D. Professor and Postgraduation Coordinator Estácio de Sá University Vertebrate Zoology and Wildlife Management Researcher Instituto Brasileiro para Medicina da Conservação (TRÍADE) Rio de Janeiro, Brazil Lin-Fa Wang, Ph.D. CEO Science Leader CSIRO Livestock Industries Australian Animal Health Laboratory Geelong, Australia E. Scott Weber III, V.M.D., M.S. Associate Professor of Clinical Aquatic Animal Medicine UC Davis School of Veterinary Medicine VM: Medicine and Epidemiology Davis, California Adrian M. Whatmore, M.S., Ph.D. FAO/WHO Collaborating Centre for Brucellosis OIE Brucellosis Reference Centre Department of Bacteriology Veterinary Laboratories Agency Addlestone, Surrey, United Kingdom Bruce A. Wilcox, M.S., Ph.D. Director, Global Health Asia Program Adjunct Professor Faculty of Public Health Mahidol University Bangkok, Thailand Michelle M. Willette, D.V.M. Staff Veterinarian The Raptor Center College of Veterinary Medicine University of Minnesota St. Paul, Minnesota

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Contributors Nathan D. Wolfe, M.A., D.Sc. Founder & CEO Global Viral Forecasting Lorry Lokey Visiting Professor Program in Human Biology, Stanford University San Francisco, California Barbara A. Wolfe, D.V.M., Ph.D., Dipl. A.C.Z.M. Director Wildlife and Conservation Medicine The Wilds Cumberland, Ohio

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Scott D. Wright, Ph.D. Branch Chief, Disease Investigations U.S. Geological Survey National Wildlife Health Center Madison, Wisconsin Carlos Zambrana-Torrelio, M.S. Research Scientist EcoHealth Alliance New York, New York B. Zimmerman, M.S. President Wildlife Health International Fort Collins, Colorado

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