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Ecology of the Acanthocephala

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Ecology of the Acanthocephala This page intentionally left blank Ecology of the Acanthocephala Commonly known as spiny-headed worms, acanthocephalans have a characteristic eversible proboscis, which bears rows of recurved spines used for attachment to the intestine of their host. Acanthocephalans are endoparasitic and an extremely successful group found in almost all marine, freshwater and terrestrial systems, infecting a huge range of definitive (usually vertebrate) and intermediate (usually arthropod) hosts during their life cycles. This volume is concerned with the ecology (distribution and abundance) of the Acanthocephala, and through this approach aims to reveal the huge success of this group of parasites. The acanthocephalans have evolved differently from all other groups of parasites, and as such represent a distinct and alternative pathway of parasite evolution and hostÀparasite interactions. Written for parasitologists, ecologists and zoologists who are interested in learning about a different pathway of parasite evolution, this book is aimed at postgraduate and research scientists. C. R. KENNEDY is Emeritus Professor of Parasitology at the University of Exeter. Ecology of the Acanthocephala C. R. KENNEDY School of Biological Sciences, University of Exeter cambridge university press Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo Cambridge University Press The Edinburgh Building, Cambridge cb2 2ru, UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Information on this title: www.cambridg e.org /9780521850087 © Cambridge University Press 2006 This publication is in copyright. Subject to statutory exception and to the provision of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published in print format 2006 isbn-13 978-0-511-24525-1 eBook (EBL) isbn-10 0-511-24525-4 eBook (EBL) isbn-13 978-0-521-85008-7 hardback isbn-10 0-521-85008-8 hardback 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. Contents Preface pagevii 1 Introduction 1 1.1 Biodiversity and the Acanthocephala 1 1.2 An ecological approach to the Acanthocephala8 2 Life cycles and transmission 12 2.1 General strategy 12 2.2 The adult stage 14 2.3 Eggs 16 2.4 Intermediate hosts and cystacanths 18 2.5 Paratenic hosts 20 2.6 Post-cyclic transmission 24 2.7 Variation in life cycles 26 3 Biogeography and distribution 28 3.1 Phylogenetic influences 28 3.2 Biogeographical influences 32 3.3 Host features 43 4 Specificity 52 4.1 General strategy 52 4.2 Criteria for specificity 56 4.3 Spatial variations in specificity 63 4.4 Strain specificity 69 5 HostÀparasite interactions 75 5.1 Distribution of acanthocephalans within hosts 75 5.2 Relations in vertebrate hosts 81 5.3 Relations in invertebrate hosts 84 v vi Contents 5.4 Alterations in intermediate host behaviour 87 5.5 Significance of behavioural changes in hosts 99 6 Population dynamics 101 6.1 General considerations 101 6.2 Seasonality and short-term studies 104 6.3 Regulatory mechanisms 110 6.4 Long-term studies 116 6.5 Mathematical models 121 7 Community dynamics 125 7.1 General considerations 125 7.2 Richness and dominance of communities 127 7.3 Spatial and temporal variability 137 7.4 Niche dynamics 141 7.5 Interspecific interactions 146 8 Introductions and extinctions 158 8.1 Dispersal 158 8.2 Introductions and colonisation 165 8.3 Rarity 172 8.4 Extinctions 174 9 Relations to ecosystem changes 179 9.1 Biological tags 179 9.2 Acanthocephalans as indicators of pollution 183 9.3 Impact on ecosystems 192 10 Conclusions and overview 200 References 211 Index 241 Preface To do science is to search for repeated patterns, not simply to accumulate facts. The only rules of the scientific method are honest observations and accurate logic. To be great science it must also be guided by a judgement, almost an instinct, for what is worth studying. MacArthur (1972) We conclude that the complicated interplay between virulence and transmissibility of parasites leaves room for many coevolutionary paths to be followed, with many endpoints. Anderson & May (1982) The Acanthocephala are generally considered to be a small and rather insignificant group of parasites. They are a minor phylum of interest to specialists; as they rarely, and then accidentally, infect humans or cause significant disease or disorder to their farmed and domestic animals, they receive a cursory treatment even in most parasitology textbooks. Nevertheless, there have been some books devoted exclusively to them, principally Acanthocephala of Domestic and Wild Animals (Petrochenko, 1956, 1958), Vol. V of Systema Helminthum (Yamaguti, 1963), An Ecological Approach to Acanthocephalan Physiology (Crompton, 1970) and Biology of the Acanthocephala (Crompton & Nickol, 1985). The first two of these books are fundamentally systematic in their approach, whereas the latter two are far more biological. Crompton & Nickol’s (1985) book does contain some chapters on acanthocephalan ecology, but it was published 20 years ago, and more recent information on their ecology can only be found in the primary scientific literature. Much recent information is being presented at the International Acanthocephalan Workshops, but proceedings of these are not published. vii viii Preface Parasitology can be viewed as a special branch of ecology since it is concerned with the relationships between organisms and their environment. This present volume attempts to present a comprehen- sive account of the ecology of the Acanthocephala. By so doing, it aims to show how an ecological approach can open up a new perspective on the phylum such that acanthocephalans can now be seen as a common, widespread and very successful group of parasites. The pattern of their evolution has differed in many respects from those of all other groups of helminth parasites and so they present a distinctive and character- istic path of hostÀparasite co-evolution. Their impact on their hosts extends beyond host individuals onto populations and communities of free-living organisms and indeed into whole ecosystems. They are also proving to be very sensitive indicators of some forms of pollution. It is intended, therefore, that this book will be of interest to a wider readership, especially to freshwater and marine biologists and also to ecologists in general, as well as to parasitologists who may be excited by the prospect of recognising and studying a different pattern of parasite evolution. It is aimed primarily at postgraduates and researchers and it assumes at least an under- graduate knowledge of parasitology and ecology. It challenges some current ideas and paradigms on biodiversity, by showing what can be achieved in evolutionary terms by a group of organisms that comprises a small number of species and exhibits a high degree of morphological uniformity. It aims to provoke an interest in the group and to stimulate the reader. It also attempts to pluck the phylum from the obscurity of current textbooks and place it on a par with, for example, cestodes and nematodes as being a group worthy of study for its own sake. No book can be comprehensive in its coverage, and this one is no exception. I am solely responsible for the selection of examples, which have been chosen from a wide range of hosts and habitats around the world. Nearly all examples in figures and tables have appeared in published form previously and I must thank all the authors and publi- shers for permitting me to use them: the source of each is acknowl- edged fully in the legends to figures and captions to tables. While the author alone must be held responsible for presentation and any errors, no book can ever be completed without the help of many people. I would like particularly to thank Ward Cooper, the then Commissioning Editor at Cambridge University Press, for his advice and efforts on my behalf and also his successor Dominic Lewis for being available to answer my many queries and deal with problems. Many of the ideas presented here have been developed in discussion with friends and Preface ix colleagues over a long period of time; and although it is invidious to single out particular persons I would like to mention Al Bush, David Crompton, Bahram Dezfuli, Celia Holland, John Holmes, Brent Nickol and Phil Whitfield in particular who have all contributed, often unknowingly and unwittingly, to the development of my ideas. I owe them a great deal as colleagues and friends. Other ideas have emerged from discussions with my postgraduate students and postdoctoral fellows and to them, and especially to Rachel Bates and Alastair Lyndon, I express my thanks. Many other people have helped me in a variety of ways, by providing me with photocopies and advice, and I would particularly like to express my thanks to Omar Amin, Chris Arme, David Gibson, Eileen Harris, Robert Poulin, Jamie Stevens and Bernd Sures. Two other people deserve special thanks. The first of these is Ian Tribe, who, although a botanist, read through the manuscript for me and made many very valuable suggestions. Finally, and above all, I must thank my wife Pat. My interest in acanthocephalans was set alight by some of the questions raised in her thesis and now 30 years later I am still trying to explain and understand the significance of some of her findings. She was in large measure responsible for planting the idea of this book in my mind and in getting me to start on it despite my insistence that I would never write another book. She has supported me and encouraged me continually throughout the writing, through the creative times and through the inevitable frustrating times.
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