00-Collinge-Prelims.qxd 24/12/05 07:37 AM Page i Disease Ecology This page intentionally left blank Disease Ecology Community structure and pathogen dynamics edited by Sharon K. Collinge and Chris Ray University of Colorado, USA 1 3 Great Clarendon Street, Oxford OX2 6DP 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 With offices in 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 2006 The moral rights of the authors have been asserted Database right Oxford University Press (maker) First published 2006 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 Disease ecology / edited by Sharon K. Collinge and Chris Ray. p. cm. Includes bibliographical references. ISBN 0–19–856708–1 (alk. paper) — ISBN 0–19–856707–3 (alk. paper) 1. Communicable diseases—Environmental aspects. 2. Host-parasite relationships—Environmental aspects. 3. Communicable diseases in animals—Environmental aspects. I. Collinge, Sharon K. II. Ray, Chris. [DNLM: 1. Communicable Diseases—epidemiology. 2. Ecology. 3. Host-Parasite Relations. WA 110 D6113 2006] RA643.D57 2006 614.5—dc22 2005020774 Typeset by Newgen Imaging Systems (P) Ltd., Chennai, India Printed in Great Britain on acid-free paper by Antony Rowe, Chippenham, Wiltshire ISBN 0–19–856707–3 978–0–19–856707–3 ISBN 0–19–856708–1 (Pbk.) 978–0–19–856708–0 (Pbk.) 10987654321 To all the creatures that delight and inspire This page intentionally left blank Preface Our research on disease ecology began several We especially thank our prairie dog disease years ago when our collaborative research group research group for stimulating our thoughts and was awarded funding from the NSF/NIH joint engaging discussions regarding disease ecology, program, “Ecology of Infectious Diseases” to study including Jack Cully, Ken Gage, Whit Johnson, landscape change and disease dynamics in prairie Michael Kosoy, Andrew Martin, and Bai Ying, as well dogs. Many of the ideas and relationships that led as the graduate students in the group, Ellen Bean, to this book were generated through the annual PI Jory Brinkerhoff, David Conlin, Tammi Johnson, Ryan network meetings for this program. We have learned Jones, Kimberly Kosmenko, Amy Markeson, Sue volumes from the participants in this group and Rodriguez-Pastor, and Bala Thiagarajan. We would especially appreciate the support and vision of have made little progress without the enthusiastic Joshua Rosenthal (NIH Fogarty Center) and Sam work of numerous field assistants over the past Scheiner (NSF) in fostering collaborative interac- 3 years, and we sincerely thank them all. tions among a diverse group of scientists interested This book benefited greatly from careful review in ecology and infectious disease dynamics. and discussion of chapters by an informal “Disease The idea for this book arose at the 2002 meeting of ecology discussion group” at the University of the Ecological Society of America, where we were Colorado-Boulder, including Ellen Bean, Jory inspired by the growing number of presentations on Brinkerhoff, David Conlin, Ryan Jones, Matthew disease ecology. We followed up on this trend by Kern, Amy Markeson, Andrew Martin, Susan organizing a symposium explicitly focused on Perkins, and Jamie Voyles. We are grateful for their community ecology and epidemiology for the 2003 contributions and are happy to report that many of ESA meeting in Savannah. As two ecologists with the comments and insights made by this group found experience in population, community, and land- their way into the final versions of these chapters. scape ecology, we sought to gather the collective No serious project is completed without the expertise of ecologists working at the interface of understanding and endless patience of those people disease ecology and epidemiology. The symposium close to us. So a million thank-yous to Joan and Jeff in Savannah was highly successful (despite the for the emotional support, for being there with the delays incurred because participants had to catch a Chipotle burritos, and for putting up with the late ferry to reach our 8 a.m. symposium!) and we were nights and early mornings. encouraged by Ian Sherman’s enthusiasm for a Finally, we are sincerely grateful to Ian Sherman at related book project through Oxford University Press. Oxford for his continued patience, encouragement, We contacted additional contributors to add to the and support of this project, and to Kerstin Demata, breadth of topics covered, and began soliciting the Abbie Headon and Anita Petrie for expert answers chapters that you see in this volume. to our seemingly endless supply of questions. VII This page intentionally left blank Contents Contributors xi 1 Community epidemiology 1 Sharon K. Collinge and Chris Ray 2 Extending the principles of community ecology to address the epidemiology of host–pathogen systems 6 Robert D. Holt and Andrew P. Dobson 3 Community ecology meets epidemiology: the case of Lyme disease 28 Richard S. Ostfeld, Felicia Keesing, and Kathleen LoGiudice 4 Microbial community ecology of tick-borne human pathogens 41 Keith Clay, Clay Fuqua, Curt Lively, and Michael J. Wade 5 Disease dynamics in plant communities 58 Charles E. Mitchell and Alison G. Power 6 Host selection and its role in transmission of arboviral encephalitides 73 Robert S. Unnasch, Eddie W. Cupp, and Thomas R. Unnasch 7 Freshwater community interactions and malaria 90 Elisˇka Rejmánková, John Grieco, Nicole Achee, Penny Masuoka, Kevin Pope, Donald Roberts, and Richard M. Higashi 8 The community ecology of Vibrio cholerae 105 Kathryn L. Cottingham and Julia M. Butzler 9 Food webs and parasites in a salt marsh ecosystem 119 Kevin D. Lafferty, Ryan F. Hechinger, Jenny C. Shaw, Kathleen Whitney, and Armand M. Kuris 10 Shifting roles of abiotic and biotic regulation of a multi-host parasite following disturbance 135 Mary F. Poteet 11 Urbanization and disease in amphibians 153 David K. Skelly, Susan R. Bolden, Manja P. Holland, L. Kealoha Freidenburg, Nicole A. Freidenfelds, and Trent R. Malcolm IX x CONTENTS 12 Spatial-temporal dynamics of rabies in ecological communities 168 Leslie A. Real and James E. Childs 13 The emergence of Nipah and Hendra virus: pathogen dynamics across a wildlife-livestock-human continuum 186 Peter Daszak, R. K. Plowright, J. H. Epstein, J. Pulliam, S. Abdul Rahman, H. E. Field, A. Jamaluddin, S. H. Sharifah, C. S. Smith, K. J. Olival, S. Luby, K. Halpin, A. D. Hyatt, A. A. Cunningham, and the Henipavirus Ecology Research Group (HERG) 14 Potential effects of a keystone species on the dynamics of sylvatic plague 202 Chris Ray and Sharon K. Collinge Index 217 List of contributors Nicole Achee, Department of Preventive Medicine and Hume E. Field, Animal Research Institute, Biometrics, USUHS, 4301 Jones Bridge Rd., Bethesda, Dept. of Primary Industries, LMB 4, MD 20814, USA. E-mail: [email protected] Moorooka 4105, Brisbane, Queensland, Australia. Susan R. Bolden, School of Forestry & Environmental E-mail: [email protected] Studies, Yale University, New Haven, CT 06511, USA. L. Kealoha Freidenburg, School of Forestry & E-mail: [email protected] Environmental Studies, Yale University, Julia M. Butzler, Department of Biological Sciences, New Haven, CT 06511, USA. Dartmouth College, Hanover, NH 03755, USA. E-mail: [email protected] E-mail: [email protected] Nicole A. Freidenfelds, Department of Natural James E. Childs, Department of Epidemiology, Resources, University of New Hampshire, Durham, Yale School of Medicine, Yale University, New Haven, NH 03824, USA. E-mail: [email protected] CT 06510, USA. E-mail: [email protected] Clay Fuqua, Department of Biology, Indiana University, Keith Clay, Department of Biology, Bloomington, IN 47405, USA. Indiana University, Bloomington, IN 47405, USA. E-mail: [email protected] E-mail: [email protected] John Grieco, Department of Preventive Medicine and Sharon K. Collinge, Department of Ecology Biometrics, USUHS, 4301 Jones Bridge Rd., Bethesda, and Evolutionary Biology and Environmental Studies MD 20814, USA. E-mail: [email protected] Program, University of Colorado, Kim Halpin, CSIRO, Livestock Industries, Boulder, CO 80309-0334, USA. Australian Animal Health Laboratory, Private Bag 24, E-mail: [email protected] Geelong, Victoria 3220, Australia. Kathryn L. Cottingham, Department of Biological E-mail: [email protected] Sciences, Dartmouth College, Hanover, NH 03755, Ryan F. Hechinger, Department of Ecology, Evolution USA. E-mail: [email protected] and Marine Biology, University of California, Andrew A. Cunningham, Institute of Zoology, Santa Barbara, CA 93106, USA. Zoological Society of London, Regent’s Park, London E-mail: [email protected] NW1 4RY, U.K. E-mail: [email protected] Richard M. Higashi, Environmental Chemistry Group, Eddie W. Cupp, Department of Entomology and Crocker Nuclear Laboratory, University of California, Plant Pathology, Auburn University, Auburn, AL Davis, CA 95616, USA.