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Melanie J. Hatcher and Alison M. Dunn
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Parasites in Ecological Communities
From Interactions to Ecosystems
Interactions between competitors, predators and their prey have traditionally
been viewed as the foundation of community structure. Parasites – long ignored
in community ecology – are now recognised as playing an important part in
influencing species interactions and consequently affecting ecosystem function.
Parasitism can interact with other ecological drivers, resulting in both detrimental and beneficial effects on biodiversity and ecosystem health. Species
interactions involving parasites are also key to understanding many biological
invasions and emerging infectious diseases. This book bridges the gap between
community ecology and epidemiology to create a wide-ranging examination of
how parasites and pathogens affect all aspects of ecological communities, enabling the new generation of ecologists to include parasites as a key consideration
in their studies.
This comprehensive guide to a newly emerging field is of relevance to
academics, practitioners and graduates in biodiversity, conservation and population management, and animal and human health.
melanie j. hatcher is Visiting Research Fellow, School of Biology, University of Bristol, UK, and Senior Research Fellow, Institute of Integrative and
Comparative Biology, University of Leeds, UK.
alison m. dunn is Reader in Evolutionary Ecology, Institute of Integrative
and Comparative Biology, Faculty of Biological Sciences, University of
Leeds, UK.
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Melanie J. Hatcher and Alison M. Dunn
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ecology, biodiversity and conservation
Series Editors
Michael Usher University of Stirling, and formerly Scottish Natural Heritage
Denis Saunders Formerly CSIRO Division of Sustainable Ecosystems, Canberra
Robert Peet University of North Carolina, Chapel Hill
Andrew Dobson Princeton University
Editorial Board
Paul Adam University of New South Wales, Australia
H. J. B. Birks University of Bergen, Norway
Lena Gustafsson Swedish University of Agricultural Science
Jeff McNeely International Union for the Conservation of Nature
R. T. Paine University of Washington
David Richardson University of Cape Town
Jeremy Wilson Royal Society for the Protection of Birds
The world’s biological diversity faces unprecedented threats. The urgent challenge facing
the concerned biologist is to understand ecological processes well enough to maintain
their functioning in the face of the pressures resulting from human population growth.
Those concerned with the conservation of biodiversity and with restoration also need
to be acquainted with the political, social, historical, economic and legal frameworks
within which ecological and conservation practice must be developed. The new
Ecology, Biodiversity and Conservation series will present balanced, comprehensive, up-todate and critical reviews of selected topics within the sciences of ecology and conservation
biology, both botanical and zoological, and both ‘pure’ and ‘applied’. It is aimed at
advanced final-year undergraduates, graduate students, researchers and university teachers, as well as ecologists and conservationists in industry, government and the voluntary
sectors. The series encompasses a wide range of approaches and scales (spatial, temporal
and taxonomic), including quantitative, theoretical, population, community, ecosystem,
landscape, historical, experimental, behavioural and evolutionary studies. The emphasis is on science related to the real world of plants and animals rather than on purely
theoretical abstractions and mathematical models. Books in this series will, wherever
possible, consider issues from a broad perspective. Some books will challenge existing
paradigms and present new ecological concepts, empirical or theoretical models and
testable hypotheses. Other books will explore new approaches and present syntheses on
topics of ecological importance.
Ecology and Control of Introduced Plants
Judith H. Myers and Dawn Bazely
Invertebrate Conservation and Agricultural Ecosystems
T. R. New
Risks and Decisions for Conservation and Environmental Management
Mark Burgman
Ecology of Populations
Esa Ranta, Per Lundberg and Veijo Kaitala
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Melanie J. Hatcher and Alison M. Dunn
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Nonequilibrium Ecology
Klaus Rohde
The Ecology of Phytoplankton
C. S. Reynolds
Systematic Conservation Planning
Chris Margules and Sahotra Sarkar
Large Scale Landscape Experiments: Lessons from Tumut
David B. Lindenmayer
Assessing the Conservation Value of Freshwaters: An International Perspective
Philip J. Boon and Catherine M. Pringle
Insect Species Conservation
T. R. New
Bird Conservation and Agriculture
Jeremy D. Wilson, Andrew D. Evans and Philip V. Grice
Cave Biology: Life in Darkness
Aldemaro Romero
Biodiversity in Environmental Assessment: Enhancing Ecosystem Services for Human Well-being
Roel Slootweg, Asha Rajvanshi, Vinod B. Mathur and Arend Kolhoff
Mapping Species Distributions: Spatial Inference and Prediction
Janet Franklin
Decline and Recovery of the Island Fox: A Case Study for Population Recovery
Timothy J. Coonan, Catherin A. Schwemm and David K. Garcelon
Ecosystem Functioning
Kurt Jax
Spatio-Temporal Heterogeneity: Concepts and Analyses
Pierre R. L. Dutilleul
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Melanie J. Hatcher and Alison M. Dunn
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Parasites in Ecological
Communities
From Interactions to Ecosystems
MELANIE J. HATCHER
University of Bristol, UK
ALISON M. DUNN
University of Leeds, UK
© in this web service Cambridge University Press
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Melanie J. Hatcher and Alison M. Dunn
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cambridge university press
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The Edinburgh Building, Cambridge CB2 8RU, UK
Published in the United States of America by Cambridge University Press, New York
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# M. J. Hatcher and A. M. Dunn 2011
This publication is in copyright. Subject to statutory exception
and to the provisions of relevant collective licensing agreements,
no reproduction of any part may take place without
the written permission of Cambridge University Press.
First published 2011
Printed in the United Kingdom at the University Press, Cambridge
A catalogue record for this publication is available from the British Library
Library of Congress Cataloguing-in-Publication data
Hatcher, Melanie J.
Parasites in ecological communities : from interactions to ecosystems / Melanie
J. Hatcher, Alison M. Dunn.
p. cm. – (Ecology, biodiversity and conservation)
ISBN 978-0-521-88970-4 (Hardback) – ISBN 978-0-521-71822-6 (Paperback)
1. Parasites–Ecology. 2. Parasites–Behavior. 3. Host-parasite relationships.
4. Parasitology. 5. Biotic communities. I. Dunn, Alison M. II. Title. III. Series.
QL757.H34 2011
577.80 57–dc22
2010050212
ISBN 978-0-521-88970-4 Hardback
ISBN 978-0-521-71822-6 Paperback
Cambridge University Press has no responsibility for the persistence or
accuracy of URLs for external or third-party internet websites referred to
in this publication, and does not guarantee that any content on such
websites is, or will remain, accurate or appropriate.
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Melanie J. Hatcher and Alison M. Dunn
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Contents
Acknowledgements
List of abbreviations
page xii
xiv
1 Introduction
1.1 Concepts from epidemiology
1.2 Concepts from community ecology
1.3 Parasites
1.4 Aims of this book
1
5
9
12
17
2 Parasites and competitors
2.1 Introduction
2.1.1 Parasitism in modules of competition
2.2 One-host–one-parasite systems
2.2.1 Population dynamics
2.2.2 Competitive release
2.3 Apparent competition
2.3.1 Baseline theory
2.3.2 Implications for biological control
2.3.3 Empirical evidence for apparent competition
2.4 Parasite-mediated competition
2.4.1 Specialist parasite-mediated competition
2.4.2 Shared parasite-mediated competition
2.5 Parasite-modified competition
2.6 Examples from conservation and management
2.6.1 Red squirrels, grey squirrels and poxvirus
2.6.2 Grey partridge, pheasants and nematodes
2.6.3 White-tailed deer, moose and brainworm
2.6.4 Red grouse, deer, mountain hare, sheep and
louping ill virus
20
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viii
2.7
2.8
Contents
Competition between parasites
2.7.1 Competition for resources
2.7.2 Apparent and host-mediated competition
2.7.3 Coinfections and trait-mediated indirect effects
Conclusions
72
77
78
81
86
3 Parasites and predators
3.1 Introduction
3.1.1 Overview of predation modules
3.2 Parasites of prey with specialist predators
3.2.1 Baseline theory
3.2.2 Empirical examples
3.3 Parasites of prey with generalist predators
3.3.1 Baseline theory
3.3.2 Empirical examples
3.3.3 Evolutionary dynamics and predation
3.4 Parasites of predators
3.4.1 Baseline theory
3.4.2 Empirical examples
3.5 Parasites of predators and prey
3.5.1 Patterns and evolution of manipulation and
trophic transmission
3.5.2 Theoretical impacts on populations and
communities
3.6 Applications: predator control and harvesting
3.6.1 Do predators keep the herds healthy?
3.6.2 Biological control
3.6.3 Harvesting infected populations
3.7 Conclusions
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4 Parasites and intraguild predation
4.1 Introduction
4.1.1 Parasitism and IGP
4.1.2 Predictions from basic IGP theory
4.2 Ecological significance of IGP
4.3 IGP as a unifying framework for competition and
predation
4.4 Parasites intrinsic to IGP
4.4.1 IGP in trophic transmission
4.4.2 Parasites and IGP in biological control
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Contents
4.4.3 Biological control scenarios with IGP
4.5 Parasites extrinsic to IGP
4.5.1 Parasite-modified IGP
4.5.2 The potential for parasitism to interact
with IGP
4.6 Models of parasitism extrinsic to IGP
4.7 IGP and the evolution of host–parasite relationships
4.8 Conclusions
ix
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5 Plant pathogens and parasitic plants
5.1 Introduction
5.1.1 Differences between animal and plant–parasite
systems
5.1.2 Parasites of plants
5.2 Soil-borne pathogens
5.2.1 The Janzen–Connell effect
5.2.2 Plant–soil feed back
5.2.3 Pathogen-modified and apparent competition
5.3 Plant defence strategies
5.3.1 Chemical signalling pathways
5.3.2 Multiple enemies: positive and negative
cross-talk
5.3.3 Signalling and manipulation
5.3.4 Above- and below-ground interactions
5.4 Parasitic plants
5.4.1 Dodder (Cuscuta)
5.4.2 Mistletoe (Santalales)
5.4.3 Broomrape (Orobanchaceae)
5.5 Endophtyes
5.5.1 Endophyte effects on communities
5.5.2 Endophyte interactions with plant parasites
and mutualists
5.6 Conclusions
176
176
6 Parasites and invasions
6.1 Introduction
6.2 Parasite introduction and acquisition
6.3 Loss of parasites by invaders: enemy release
6.3.1 Community studies of parasitism in invasive
versus indigenous species
224
224
226
229
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Melanie J. Hatcher and Alison M. Dunn
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x
Contents
6.4
6.5
6.6
6.3.2 Biogeographical studies of parasitism in the
native versus invasive range
6.3.3 Enemy release from vertically transmitted
parasites
Invasions and host–parasite co-evolution
6.4.1 Local adaptation
6.4.2 Evolution of increased competitive ability
6.4.3 Plant–soil feed back
The impact of parasitism on biological invasions
6.5.1 Parasite dilution by invading hosts
6.5.2 Invading hosts as infection reservoirs
6.5.3 Native hosts as infection reservoirs
6.5.4 Native–invader interactions mediated
by parasites
Conclusions
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244
244
245
246
248
248
249
256
259
263
7 Ecosystem parasitology
7.1 Introduction
7.2 Trophic cascades
7.2.1 Density-mediated trophic cascades
7.2.2 Trait-mediated trophic cascades
7.3 Parasite dynamics in multi-host communities
7.3.1 Baseline model: parasite establishment in
multiple host species
7.3.2 Reservoir versus dilution and host competence
7.3.3 Lyme disease risk, dilution and reservoir hosts
7.4 Biodiversity and disease
7.4.1 Determinants of disease spread
7.4.2 Transmission models and biodiversity
relationships
7.5 Parasites in the food web
7.5.1 Functional role and interaction strength
7.5.2 Parasitism and food web topology
7.5.3 Implications for community stability
7.6 Bioenergetic implications of parasitism
7.6.1 Parasite biomass
7.6.2 Parasite productivity
7.7 Ecosystem engineering
7.8 Ecosystem health
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Integrating population and community
approaches to the study of ecosystems
7.8.2 Are parasites indicators of healthy ecosystems?
7.9 Evolutionary considerations
7.10 Conclusions
xi
7.8.1
308
311
316
318
8 Emerging diseases in humans and wildlife
8.1 Introduction
8.1.1 Emerging approaches to the problem of EIDs
8.1.2 What are the problems caused by EIDs?
8.2 The process of disease emergence
8.2.1 Spillover
8.2.2 Persistence
8.2.3 Pandemic emergence
8.2.4 Heterogeneity in R0: superspreaders and
their effect on disease dynamics
8.3 The evolution of emergence
8.3.1 Virulence evolution of emerging diseases
8.4 Phylogenetic and temporal patterns of emergence
8.4.1 Which diseases emerge, and in which hosts?
8.4.2 Are EIDs increasing?
8.5 Environmental change and emergence
8.5.1 Land use changes
8.5.2 Trade and transport changes
8.5.3 Climate change and emerging diseases
8.6 Conservation and control
8.6.1 Monitoring
8.6.2 Contact reduction
8.6.3 Vaccination
8.7 Conclusions
320
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328
9 Where do we go from here?
386
References
Index
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Acknowledgements
The collaboration leading to this book was fostered in the smoky bars
and backstreets of Oxford in the 1980s, where the authors first met
whilst studying Zoology as undergraduates. In that respect, we would
like to thank Sir John Krebs for (just about) tolerating us.
The book has been fermenting for many years and we thank the
following for funding various research projects and studentships which
have contributed to the ideas and examples in the book: the Natural
Environment Research Council (particularly current grants NE/
D011000/1 and NE/G015201/1); the Royal Society; the Biotechnology and Biological Sciences Research Council; the Leverhulme Trust;
the European Science Foundation; Tarmac; the Yorkshire Dales
National Parks Authority; the Natural History Museum; the European
Union; and the Environment Agency.
For discussion on many of the ideas in this book, often over many
years, we thank the late Anne Keymer (who first sparked AMD’s interest
in parasites), Judith Smith, Jonathan Adams, John Lawton, Thierry
Rigaud, Pete Hudson, Andrew Read, Andy Dobson, Greg Hurst, Jack
Werren, Charles Godfray, Jaimie Dick and Chris Tofts; also, all the
fellow travellers at ecology, evolution and parasitology conferences with
whom we have had many stimulating and drunken conversations.
Various of AMD’s lab group members receive thanks for stimulating
conversations and dedicated research, with several of them also providing helpful comments on chapter drafts: Andy Kelly, Aurore Dubuffet,
Emily Imhoff, Neal Haddaway, Katie Arundell, Stephanie Peay, Paula
Rosewarne, Mandy Bunke, Calum MacNeil and Jolene Slothouber
Galbreath. We also thank Emily Imhoff for her lovely cartoon in
Chapter 6.
A number of colleagues made time in their busy schedules for critical
comment on individual chapters, which improved the work immensely.
We thank Paul Hatcher, Steve Sait, Bryan Shorrocks, Jaimie Dick, Bill
Kunin, Dan Tompkins, Robert Poulin, Simon Goodman, Rupert
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Acknowledgements
xiii
Quinnell and Chris Tofts. For advice and critical comment on the entire
work over its period of gestation, we thank Michael Usher, without
whose support this work would never have been produced. Thanks
are also due to Emma Walker, Megan Waddington and Dominic Lewis,
who have all shown patience and understanding over our plight as
novice book writers.
We thank the following publishers for kindly granting us permission
to re-use or modify figures for this book: the American Association for
the Advancement of Science; Cambridge University Press; Center for
Disease Control and Prevention; Chicago Press; Ecological Society of
America; Elsevier; National Academy of Sciences (USA); Nature Publishing Group; the Public Library of Science; the Royal Society; and
Wiley & Sons.
For untiring support, intellectual, emotional, practical and technical,
MJH especially wishes to thank Chris Tofts. For grandparenting services
beyond the call of duty she thanks Eileen and Maurice Tofts; for a room
with a view, Nicci Tofts; for advice and practical help in sustainable
resource management, Paul Hatcher; and for engendering an enquiring
mind, Erica and Michael Hatcher.
For their support and humour at times of crisis, AMD would like to
thank various friends and family, especially Moira and Robin Dunn for
support and help with fieldwork over the years (and no, Dad, we still
don’t know everything about those little shrimps) and to Claire Dunn,
David Watkin, Linda Bracey Aitchison and Claire Caddell for their
slightly bemused support of yet another late-night writing session.
Finally, we need to thank our own maddening and wonderful little
parasites, James and Jennifer Tofts, Ethan and Aidan Dunn. Without you
the book may have been sooner but less inspired. Without the book you
would have done less ballet and sports camp. You will thank us one day.
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Abbreviations
ABA
AMF
Bd
BYDVs
CDC
CDV
CPV
EICA
EID
EM
ERH
ET
FIV
FLV
FPLV
FPV
HA
HIV
IBMs
IG
IGP
ISR
JA
LIV
MSY
MVP
NA
PDV
PIVP
PSF
RHD
SA
SIV
abscisic acid
arbuscular mycorrhizal fungi
Batrachochytrium dendrobatidis
barley yellow dwarf viruses
Center for Disease Control
canine distemper virus
canine parvovirus
evolution of increased competitive ability
emerging infectious disease
ectomycorrhizal
enemy release hypothesis
ethylene
feline immunodeficiency virus
feline leukaemia virus
feline panleukopenia virus
feline parvovirus
haemaglutinin
human immunodeficiency virus
individual-based models
intraguild
intraguild predation
induced systemic resistance
jasmonic acid
louping ill virus
maximum sustainable yield
minimum viable population
neuraminidase
phocine distemper virus
parasite-induced vulnerability to predation
plant–soil feed back
rabbit haemorrhagic disease
salicylic acid
simian immunodeficiency virus
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List of abbreviations
SQPV
TMIEs
VOCs
WAIFW
WNV
xv
squirrel pox virus
trait-mediated indirect effects
volatile organic compounds
who acquires infection from whom
West Nile virus
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