Parasitology: An Integrated Approach PDF

JWST138-fm JWST138-Gunn February 21, 2012 16:59 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Parasitology JWST138-fm JWST138-Gunn February 21, 2012 16:59 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Parasitology An Integrated Approach Alan Gunn Liverpool John Moores University, Liverpool, UK Sarah J. Pitt University of Brighton, UK Brighton and Sussex University Hospitals NHS Trust, Brighton, UK A John Wiley & Sons, Ltd., Publication JWST138-fm JWST138-Gunn February 21, 2012 16:59 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC This edition ﬁrst published 2012 © 2012 by by John Wiley & Sons, Ltd Wiley-Blackwell is an imprint of John Wiley & Sons, formed by the merger of Wiley’s global Scientiﬁc, Technical and Medical business with Blackwell Publishing. Registered Ofﬁce John Wiley & Sons Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK Editorial Ofﬁces 9600 Garsington Road, Oxford, OX4 2DQ, UK The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK 111 River Street, Hoboken, NJ 07030-5774, USA For details of our global editorial ofﬁces, for customer services and for information about how to apply for permission to reuse the copyright material in this book please see our website at www.wiley.com/wiley-blackwell. The right of the author to be identiﬁed as the author of this work has been asserted in accordance with the UK Copyright, Designs and Patents Act 1988. 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, electronic, mechanical, photocopying, recording or otherwise, except as permitted by the UK Copyright, Designs and Patents Act 1988, without the prior permission of the publisher. Designations used by companies to distinguish their products are often claimed as trademarks. All brand names and product names used in this book are trade names, service marks, trademarks or registered trademarks of their respective owners. The publisher is not associated with any product or vendor mentioned in this book. This publication is designed to provide accurate and authoritative information in regard to the subject matter covered. It is sold on the understanding that the publisher is not engaged in rendering professional services. If professional advice or other expert assistance is required, the services of a competent professional should be sought. Library of Congress Cataloging-in-Publication Data Gunn, Alan. Parasitology : an integrated approach / Alan Gunn and Sarah J. Pitt. p. ; cm. Includes bibliographical references and index. ISBN 978-0-470-68424-5 (cloth) – ISBN 978-0-470-68423-8 (pbk.) I. Pitt, Sarah J. II. Title. [DNLM: 1. Host-Parasite Interactions. 2. Parasites–physiology. 3. Parasitic Diseases. QY 45] 616.9 6–dc23 2011043529 A catalogue record for this book is available from the British Library. Wiley also publishes its books in a variety of electronic formats. Some content that appears in print may not be available in electronic books. Set in 10.5/12.5pt Times by Aptara Inc., New Delhi, India First Impression 2012 JWST138-fm JWST138-Gunn February 21, 2012 16:59 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC None of us truly live alone JWST138-fm JWST138-Gunn February 10, 2012 9:40 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Contents Preface xiii 1 Animal associations 1 1.1 Introduction 1 1.2 Animal associations 1 1.2.1 Symbiosis 2 1.2.2 Commensalism 5 1.2.3 Phoresis 5 1.2.4 Mutualism 6 1.2.5 Parasitism 7 1.2.6 Intra-speciﬁc parasites 8 1.2.7 Parasitoids 9 1.2.8 The concept of harm 10 1.3 Parasite hosts 11 1.3.1 Protozoa and helminths as hosts 11 1.3.2 Classes of hosts for parasites 12 1.4 The co-evolution of parasites and their hosts 13 1.4.1 Evolutionary relationships between host and parasite 14 1.4.2 Parasites and the evolution of sexual reproduction 15 1.5 Parasitism as a ‘lifestyle’: advantages and limitations 16 1.5.1 Main advantages of a parasitic lifestyle 17 1.5.2 Main limitations of a parasitic life style 17 1.6 The economic cost of parasitic diseases 18 1.6.1 Economic consequences of parasitic diseases of humans 18 1.6.2 Economic consequences of parasitic diseases of domestic animals 19 1.6.3 Estimating the costs of morbidity due to disease 19 1.6.4 Economic consequences of parasitic diseases of wildlife 20 1.7 Why parasitic diseases remain a problem 21 1.8 Taxonomy 24 1.8.1 The binomen system 25 Questions 27 2 Parasitic protozoa, fungi and plants 28 2.1 Introduction 28 2.2 Parasitic protozoa 28 2.2.1 Kingdom Protista 28 JWST138-fm JWST138-Gunn February 10, 2012 9:40 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC viii CONTENTS 2.3 Phylum Rhizopoda 29 2.3.1 Genus Entamoeba 29 2.3.2 Other species of pathogenic amoebae 33 2.4 Phylum Metamonada 34 2.4.1 Order Diplomonadida 34 2.4.2 Order Trichomonadida 37 2.5 Phylum Apicomplexa 40 2.5.1 Genus Plasmodium 42 2.5.2 Plasmodium life cycle 43 2.5.3 Genus Theileria 45 2.5.4 Genus Babesia 46 2.6 Subclass Coccidiasina 50 2.6.1 Suborder Eimeriorina 50 2.6.2 Isospora group 51 2.6.3 Genus Cyclospora 52 2.6.4 Family Sarcocystidae 53 2.6.5 Genus Toxoplasma 54 2.6.6 Genus Neospora 58 2.6.7 Family Cryptosporidiidae 60 2.7 Phylum Kinetoplastida 62 2.7.1 Genus Leishmania 63 2.7.2 Leishmania life cycle 66 2.7.3 Genus Trypanosoma 70 2.8 Phylum Chlorophyta 81 2.8.1 Genus Prototheca 82 2.9 Kingdom fungi 83 2.9.1 Microsporidia 83 2.10 Kingdom plantae 85 Questions 85 3 Helminth parasites 86 3.1 Introduction: invertebrate taxonomy 86 3.2 Phylum Platyhelminthes 87 3.3 Class Trematoda 87 3.3.1 Family Fasciolidae 89 3.3.2 Family Cathaemasiidae: Genus Ribeiroia 93 3.3.3 Family Dicrocoeliidae 95 3.3.4 Family Opisthorchiformes 96 3.3.5 Family Paragonomidae 98 3.3.6 Family Schistosomatidae 99 3.4 Class Cestoda 103 3.4.1 Order Pseudophyllidea/Diphyllobothriidea 103 3.4.2 Order Cyclophyllidea 104 3.4.3 Family Taeniidae 105 3.4.4 Family Anoplocephalidae 110 3.5 Phylum Acanthocephala 112 3.6 Phylum Nematoda (Nemata) 114 3.6.1 Class Enoplea 117 3.6.2 Class Rhabdita 121 3.6.3 Family Onchocercidae 129 3.6.4 Family Dracunculidae 132 Questions 135 JWST138-fm JWST138-Gunn February 10, 2012 9:40 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC CONTENTS ix 4 Arthropod parasites 137 4.1 Introduction 137 4.2 Phylum Chelicerata 138 4.2.1 Family Demodicidae 139 4.2.2 Family Sarcoptidae 140 4.2.3 Family Psoroptidae 143 4.2.4 Suborder Ixodida 144 4.2.5 Family Argasidae 145 4.2.6 Family Ixodidae 146 4.2.7 Tick paralysis 147 4.3 Phylum Crustacea 148 4.3.1 Subclass Copepoda 148 4.3.2 Infra-Class Cirripedia 150 4.3.3 Subclass Branchiura 150 4.3.4 Subclass Pentastomida – tongue worms 151 4.4 Sub-phylum Hexapoda 153 4.4.1 Order Phthiraptera (lice) 155 4.4.2 Order Siphonaptera (ﬂeas) 159 4.4.3 Order Diptera (true ﬂies) 162 4.4.4 Suborder Nematocera 162 4.4.5 Suborder Brachycera 163 4.4.6 Family Calliphoridae 166 4.4.7 Genus Chrysomya 168 4.4.8 Genus Cochliomyia 168 4.4.9 Genus Auchmeromyia 169 4.4.10 Genus Cordylobia 170 4.4.11 Family Sarcophagidae 170 4.4.12 Family Oestridae 171 4.4.13 Subfamily Gasterophilinae 173 4.4.14 Subfamily Hypodermatinae 174 4.4.15 Subfamily Cuterebrinae 176 4.4.16 Family Streblidae 177 4.4.17 Family Nycteribiidae 178 Questions 178 5 Parasite transmission 180 5.1 Introduction 180 5.2 Contaminative transmission 181 5.3 Transmission associated with reproduction 184 5.3.1 Sexual transmission 184 5.3.2 Transmission within the gametes 187 5.3.3 Congenital transmission 188 5.4 Autoinfection 189 5.5 Nosocomial transmission 190 5.6 Active parasite transmission 191 5.7 Hosts and vectors 192 5.7.1 Paratenic hosts 192 5.7.2 Intermediate hosts 193 5.7.3 Vectors 194 5.8 Host factors 196 5.8.1 Host identiﬁcation 196 5.8.2 The inﬂuence of host behaviour on parasite transmission 197 JWST138-fm JWST138-Gunn February 10, 2012 9:40 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC x CONTENTS 5.9 Co-transmission and interactions between infectious agents 199 5.10 How religion can inﬂuence parasite transmission 202 5.11 The inﬂuence of war on parasite transmission 204 5.12 The inﬂuence of parasites on host behaviour 205 5.13 Environmental factors 207 5.13.1 Natural environmental variables 207 5.13.2 Pollution 207 5.13.3 Global warming 209 Questions 211 6 Immune reactions to parasitic infections 212 6.1 Introduction 212 6.2 Invertebrate immunity 213 6.3 Vertebrate immunity 215 6.3.1 Innate immunity 215 6.3.2 Adaptive immunity 218 6.3.3 Cell-mediated immunity 220 6.4 Innate immunity to parasitic infection 221 6.4.1 Physical factors 221 6.4.2 Chemical and microbial factors 222 6.4.3 The acute inﬂammatory response 223 6.4.4 Cell-mediated immunity 225 6.5 Adaptive immunity 226 6.5.1 Avoiding the host immune response 227 6.5.2 Depression of the immune system 232 6.6 Immunity to malaria 233 6.7 Schistosoma mansoni and Hepatitis C virus interactions 237 6.8 HIV-AIDS and parasitic disease 238 6.8.1 Parasites and the transmission of HIV 239 6.8.2 Parasite-HIV co-infections 240 6.8.3 Leishmania-HIV co-infections 240 6.8.4 Malaria–HIV co-infections 242 6.8.5 Toxoplasma–HIV co-infections 243 6.8.6 Microsporidia–HIV co-infections 243 Questions 243 7 Pathology 245 7.1 Introduction 245 7.2 Factors that inﬂuence pathogenesis 245 7.2.1 Host factors that inﬂuence pathogenesis 245 7.2.2 Parasite factors that inﬂuence pathogenesis 246 7.3 Mechanisms by which parasites induce pathology 247 7.3.1 Direct damage 248 7.3.2 Indirect damage 249 7.4 Types of pathology 250 7.4.1 Abortion and obstetric pathology 250 7.4.2 Anaemia 251 7.4.3 Anorexia 253 7.4.4 Apoptosis 253 7.4.5 Calciﬁcation 254 JWST138-fm JWST138-Gunn February 10, 2012 9:40 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC CONTENTS xi 7.4.6 Cancer 255 7.4.7 Castration 257 7.4.8 Delusional parasitosis 258 7.4.9 Diarrhoea 258 7.4.10 Elephantiasis 260 7.4.11 Fever 261 7.4.12 Granulation and ﬁbrosis 262 7.4.13 Hyperplasia 264 7.4.14 Hypertrophy 265 7.4.15 Inﬂammation and ulceration 265 7.4.16 Jaundice 267 7.4.17 Metaplasia 267 7.4.18 Pressure atrophy 267 7.4.19 Psychological disturbance 268 7.5 Damage to speciﬁc organs 269 7.5.1 The bladder 269 7.5.2 The brain 270 7.5.3 The digestive system 273 7.5.4 The genitalia 276 7.5.5 The kidney 277 7.5.6 The liver 279 7.5.7 The lungs 281 7.5.8 The skin 284 7.5.9 The spleen 288 7.6 Co-infections and pathogenesis 289 Questions 290 8 The useful parasite 292 8.1 Introduction: the goodness of parasites? 292 8.2 The importance of parasites for the maintenance of a healthy immune system 293 8.2.1 The hygiene hypothesis 293 8.2.2 Type 1 diabetes mellitus 294 8.2.3 Irritable bowel syndrome (IBS) 296 8.2.4 Inﬂammatory bowel disease 297 8.3 The use of parasites to treat medical conditions 297 8.3.1 Helminth therapy 298 8.3.2 Larval therapy 302 8.3.3 Leech therapy 304 8.3.4 Malaria therapy (malariotherapy) 305 8.4 Parasites as sources of novel pharmaceutically-active compounds 308 8.5 Parasites as biological control agents 309 8.5.1 Life cycle of the entomopathogenic nematodes Heterorhabditis and Steinernema 310 8.6 Parasites as forensic indicators 312 Questions 314 9 Identiﬁcation of protozoan and helminth parasites 316 9.1 Introduction 316 9.2 The importance of correct identiﬁcation 316 9.3 Properties of an ideal diagnostic test 318 9.4 Isolation of parasites 320 JWST138-fm JWST138-Gunn February 10, 2012 9:40 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC xii CONTENTS 9.5 Identiﬁcation from gross morphology 323 9.5.1 Morphological identiﬁcation of Entamoeba 325 9.5.2 Morphological identiﬁcation of Plasmodium and Babesia 326 9.5.3 Morphological identiﬁcation of Taenia tapeworms 327 9.5.4 Morphological identiﬁcation of ﬁlarial nematode infections 327 9.6 Biochemical techniques 329 9.7 Immunological techniques 329 9.8 Molecular techniques 331 9.9 Rapid diagnostic tests (RDTs) 334 9.9.1 Rapid diagnostic tests for malaria 335 9.9.2 Rapid diagnostic test for ﬁlariasis 337 9.10 MALDI-TOF MS 337 Questions 338 10 Parasite treatment and control 339 10.1 Introduction 339 10.2 Importance of understanding parasite life cycles for effective treatment and control 339 10.3 Treatment of parasitic diseases 341 10.3.1 The ideal antiparasitic drug 341 10.3.2 Pharmaceutical drugs 345 10.3.3 DNA/RNA technology 347 10.3.4 Molecular chaperones (heat shock proteins) 349 10.3.5 Nanotechnology 350 10.3.6 Quantum dots 352 10.3.7 Natural remedies 353 10.3.8 Homeopathy 355 10.4 Vaccines against parasitic diseases 356 10.4.1 Attenuated vaccines 358 10.4.2 Killed vaccines 359 10.4.3 Recombinant vaccines 359 10.4.4 Toxoid vaccines 360 10.4.5 DNA vaccines 361 10.4.6 Vaccine administration 362 10.5 Control of parasitic diseases 362 10.5.1 Eradication, elimination and control of parasitic diseases 362 10.5.2 Education 364 10.5.3 Environmental modiﬁcation and cultural control 365 10.5.4 Remote Sensing (RS) and GIS technology 368 10.5.5 Treating the individual or the population 369 10.5.6 Piggy-backing control programmes 370 10.5.7 Disruptions to control programmes 371 10.5.8 Role of governments, foundations, and aid organisations 371 Questions 373 References 375 Index 431 JWST138-Pre JWST138-Gunn February 10, 2012 9:42 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Preface Protozoan and helminth parasites are fascinating organisms and examples of their parasitism are found in a broad range of hosts, including plants, invertebrates and vertebrates. The interaction between a parasite and its host is complex and dynamic. Therefore we think that studying par- asitology is a useful tool for appreciating a range of concepts in biological sciences including growth and reproduction, biochemistry, immunology and pathology. Parasites do not live within their hosts in isolation. We feel that it is instructive to recognise how an individual organism might interact with other members of the same species, other species of protozoa and helminths and other classes of microorganism within a particular host. The ef- fects on the host of harbouring a particular species of parasite are inﬂuenced by a range of host factors, including genetic constitution, immune status, and behaviour. Also, for parasites of hu- mans in particular, consideration of social, religious, and cultural factors is often necessary. We have therefore called this book Parasitology: An Integrated Approach to emphasise how parasites inﬂuence, and are inﬂuenced by, a complex web of interacting factors. We have divided the book into conventional chapters but because we wish to show how topics are inter-related, the reader will ﬁnd certain subjects are picked up, put down, discussed in more detail elsewhere, and then returned to in a later chapter. This is also a good way of learning since it is better to take in bite-sized chunks of information and return to them frequently rather than attempting to grasp all aspects of a topic in a single sitting. We ﬁrst introduce the concept of parasitism and the terms used by parasitologists to describe parasite lifestyles (Chapter 1). We then provide three chapters (Chapters 2–4) in which we introduce some of the ‘key players’, explain their basic biology and how they interact with one another. We have not included many diagrams of parasite life cycles as there is an excellent online resource available at the DPDx – CDC Parasitology Diagnostic Web Site (http//:dpd.cdc.gov/dpdx). There follows a chapter on parasite transmission (Chapter 5) in which we consider, among other topics, not only how parasites exploit other animals as vectors and intermediate hosts but also how they manipulate their host’s behaviour to increase their chances of transmission. We provide separate chapters on immunology (Chapter 6) and pathology (Chapter 7) but in truth it is virtually impossible to separate these topics because they are so inter-dependent. Chapter 8 is designed as a counterbalance to the bad press that parasites receive. Parasites not only can be used for the treatment of medical conditions but also may (in small doses) actually be good for us. Before one can begin to study parasites, one needs to be able to ﬁnd them and count them. Even if the host is dead, this is not necessarily as simple as it sounds. Correct parasite diagnosis is essential before treatment can be given and to determine the necessity for or success of a control programme. We therefore devote Chapter 9 to parasite diagnosis that encompasses techniques ranging from straightforward light microscopy to advanced molecular biology. Finally, the book ends with Chapter 10 on treatment and control in which we again emphasise how these topics are informed by advances in medicine, genomics, and economics. JWST138-Pre JWST138-Gunn February 10, 2012 9:42 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC xiv PREFACE Figure 0.1 One can form a close relationship with a tapeworm! Source: © Serre, C. (1984) Stufﬁng. Methuen London Ltd, London, UK This book is designed mainly for undergraduate students of biological sciences, biomedical sciences, medicine and veterinary sciences who need to know about protozoan and helminth para- sites and understand how they affect their hosts. It would also be useful for postgraduate students who need background information about parasites to support their research and for members of any other professional group who need an insight into the subject for their work. In the spirit of integration, we have provided web-based support material via the publisher’s website. This includes the numerous photographs of parasites that we could not include in the book without increasing its size and cost. There are also more extensive questions based on each chapter, and a number of project ideas that do not require access to complex laboratory facilities or use laboratory animals such as mice, rats, and rabbits. Alan Gunn and Sarah J. Pitt, 2011 JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC (a) (b) Merozoite 0h 1–24 h Erythrocyte Bloodstream Liver 24–30 h 30–36 h 36–48 h (c) Knob Maurer’s PfEMP1 cleft PV Endoplasmic Vesicle-like 48 h reticulum structure Nucleus PVM Plate 1 Schizogony in Plasmodium falciparum. (a) = Mosquito injects sporozoites into the bloodstream and these then travel to the liver. The sporozoites invade the hepatocytes and undergo exoerythrocytic schizogony during which they produce merozoites. (b) = Merozoites leave the liver cells, enter the circulation and infect red blood cells. Within the red blood cells the merozoites undergo erythrocytic schizogony over a period of 48 hours. During the ﬁrst 24 hours the ring stage starts to grow; during 24–36 hours the parasite enters the trophozoite stage in which it grows and DNA replication takes place; between 36 and 48 hours the schizont is formed that culminates in the formation of merozoites and the death of the red blood cell. (c) = The parasites export proteins through the parasitophorous membrane (PVM) that re-model the cell membrane of infected red blood cells so that ‘knobs’ are formed. Exported proteins include Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1). Source: Goldberg and Cowman, 2010 JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Intracellular amastigote Phagolysosome Proliferation Uptake Lysis Re-invasion Macrophage Attachment Sandfly bite Sandfly bite Metacyclic promastigotes Amastigotes Procyclic Promastigotes Proliferation in the midgut Plate 2 Diagrammatic representation of the life cycle of Leishmania donovani. Source: Chappuis et al., 2007. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nature Reviews Microbiology 5, 873–882. JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 3 Forearm of patient suffering from a cutaneous infection of Prototheca cutis. Note the cellulitis-like in- ﬂammation and ulcer. Source: Satoh et al., 2010. (Prototheca cutis sp. Nov., a newly discovered pathogen of pro- tothecosis isolated from inﬂamed human skin. International Journal of Systematic and Evolutionary Microbiology 60, 1236–1240. Reproduced by permission of Society for General Microbiology) Plate 4 Adult schistosomes. The long slender female is carried in the gynaecophoric canal of the shorter, more stumpy-shaped male JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 5 Echinococcus granulosus: Adult worm. Adults of this species are small (this specimen is 5 mm in length) and usually consist of 3–4 segments (proglottids). Note the presence of a rostellum at the tip of the scolex. The rostellum is armed with two rows of hooks. Plate 6 Echinococcus granulosus: hydatid cysts in the liver of a donkey JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 7 Hydatid ‘sand’ from inside a hydatid cyst of Echinococcus granulosus showing developing protoscolices Plate 8 Encysted larva of Trichinella spiralis Plate 9 Adult sheep scab mite Psoroptes ovis showing the mouthparts. JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 10 Engorged hard tick (family Ixodidae). Note how the mouthparts can be seen from above. Plate 11 Mallophaga, biting louse. Note how the triangular-shaped head is wider than the thorax and the unmodiﬁed tarsi (‘feet’) JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 12 Anoplura, sucking louse, Pediculus humanus capitatis. Note how the head is narrower than the thorax. The tibia and tarsi have evolved to become claw-like and adapted for clinging onto hairs. This specimen is a male as evidenced by the sword-like aedeagus at the posterior of the abdomen. Plate 13 Cephalopharyngeal skeleton of the third instar larva of the blowﬂy Calliphora vomitoria. Note the curved mouth-hooks JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 14 Sheep blowﬂy strike caused by Wohlfahrtia magniﬁca. The sheep is a fat-tailed Awassi breed and the larvae have almost completely destroyed the tail. Note how deeply the larvae have burrowed into the ﬂesh Plate 15 Third instar larva Oestrus ovis within the turbinate bones of a sheep. Note how the shape of the larva ensures it is tightly wedged within the cavities JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 16 Hypoderma lineatum: warble (arrow) on the back of a cow Plate 17 Hypoderma lineatum: mature larva removed from the warble illustrated in Plate 16. Scale in mm JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 18 Crusted scabies is highly debilitating and infectious. This photograph illustrates the foot of a 51-year- old woman admitted to hospital suffering from pulmonary tuberculosis and acute respiratory failure. Scabies can become severe in patients whose immune system is compromised by illness. From http://dermatlas.med.jhmi.edu/ derm/indexDisplay.cfm?ImageID=-1428734691. (Copyright Vincent C.B. Lin. MD, Dermatlas; http://www. dermatlas.org) Plate 19 Coenurus of the tapeworm Taenia multiceps removed from the brain of a sheep. Note the large number of protoscolices budding from the germinal membrane JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 20 Burkitt’s tumour. This severely disﬁguring and fatal tumour is associated with co-infection with EBV (Epstein-Barr virus) and malaria. Source: Peters and Gilles, 1989 Plate 21 Woman feeding her piglet. In parts of the New Guinea highlands pigs play such an important role in culture that piglets may be fed in preference to children. Source: Peters and Gilles (1977) JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 22 Encapsulation response to a latex bead injected into the haemolymph of the ﬁnal instar larva of the moth Spodoptera exempta Plate 23 Hatched egg (‘nit’) of the head louse Pediculus humanus capititis JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 24 Fatal toxoplasmic brain abscess from a patient who had AIDS. Source: Kean et al., 1991 Plate 25 Light microscope section through a cysticercus of Taenia solium. Note that there is only one proto- scolex and budding does not occur Plate 26 Light microscope section through a cysticercus of Taenia solium. Note that the protoscolex is armed with hooks JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 27 Huge numbers of Ascaris lumbricoides passed by a young child following anthelmintic treatment. When such large numbers are present, they can block the gastrointestinal tract. Source: Peters and Gilles, 1989 Plate 28 Heel of a man suffering from a co-infection of chromoblastomycosis and cutaneous myiasis. The rear ends of some of the larvae of Chrysomya bezziana are arrowed. Source: Slesak et al., 2011 JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC Plate 29 After this man’s tongue was re-attached, leeches were applied to relieve congestion until the venous blood supply was re-established. Source: Kim, J.S. et al., 2007. (Reprinted from Journal of Plastic, Reconstructive and Aesthetic Surgery, 60, Kim, J.S. et al., 1152–1155, 2007, with permission from Elsevier) Plate 30 Cerebrospinal ﬂuid is required for some tests to determine whether trypanosomes have invaded the central nervous system. This is an unpleasant procedure for the patient and carries risks of causing nerve damage. Source: Peters and Gilles, 1989 JWST138-cp JWST138-Gunn January 15, 2012 11:29 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC (a) (b) Plate 31 Gravid proglottids of Taenia saginata (a) and Taenia solium (b) injected with ink to show the difference in the number of uterine branches. Source: Kean et al., 1991 Plate 32 The Middle Eastern country where this photograph was taken had regulations requiring sheep to be slaughtered at ofﬁcial slaughterhouses where the meat could be inspected and waste disposed of safely. However, numerous small unlicensed butchers could be found throughout the country JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 1 Animal associations 1.1 Introduction In this introductory chapter we will introduce the concept of parasitism as a lifestyle and ex- plain why it is such a difﬁcult term to deﬁne. We shall also introduce some of the terms that are commonly used by parasitologists. Like all branches of science, parasitology has a number of as- sociated specialist terms such as ‘intermediate host’, ‘deﬁnitive host’ and ‘zoonosis’ that need to be understood before it is possible to make sense of the literature. We will explain why the study of parasites is so important and why parasites are likely to remain a problem for many decades to come. We will end by introducing the study of taxonomy because this will help inform the chap- ters on speciﬁc groups of organisms as well as the chapters on diagnosis, treatment, and control. Taxonomy is nowadays something of a Cinderella subject among biologists but it cannot be ig- nored because scientists must agree on the names things are to be called if they are to communicate with one another. 1.2 Animal associations All animals are in constant interaction with other organisms. These interactions can be divided into two basic types: intra-speciﬁc interactions and inter-speciﬁc interactions. Intra-speciﬁc interactions are those that occur between organisms of the same species. They range between relatively loose associations such as those between members of a ﬂock of sheep, to highly complex interactions such as those seen in colonial invertebrates (e.g. Bryozoans and some of the Cnidaria (jellyﬁsh and sea anemones)). For example, the adult (medusa) stage of certain jellyﬁsh may appear to be a single organism but it is actually composed of colonies of genetically identical but polymorphic individuals. These colonies divide labour between themselves in a sim- ilar manner to that of organ systems within a non-colonial organism, for example, some colonies are specialised for reproduction while others are specialised for feeding. Inter-speciﬁc interactions are those that take place between different species of organism (Figure 1.1). As with intra-speciﬁc interactions, the degree of association can vary between be- ing extremely loose to highly complex. Odum (1959) classiﬁed these interactions on the basis of their effect on population growth using the codes ‘+’ = positive effect, ‘−’ = negative effect, and ‘0’ = no effect. This leads to six possible combinations (00, 0−, 0+, etc.) and these too can be broken down into further subdivisions (Toft et al., 1993). Some authors also include a considera- tion of the direction and extent of any physiological and biochemical interactions between the two Parasitology: An Integrated Approach, First Edition. Alan Gunn and Sarah J. Pitt. © 2012 John Wiley & Sons, Ltd. Published 2012 by John Wiley & Sons, Ltd. 1 JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 2 CH01 ANIMAL ASSOCIATIONS Figure 1.1 Different species will occasionally co-operate for mutual beneﬁt organisms. A wide range of terms have been suggested in an attempt to compartmentalise these interactions (e.g. phoresis, mutualism, predation) but these are merely convenient tags and they cannot be deﬁned absolutely. This is because the variety of organism interactions is extremely broad and even within a single interaction there are a host of variables such as the relative health of the two organisms that determine the consequences of the interaction for them both. It is there- fore not surprising that there is a multiplicity of deﬁnitions in the scientiﬁc literature and it is not unusual for two authors to arrive at two different terms for the same type of interaction between species. In this section, we will discuss symbiosis, commensalism, phoresis, mutualism and ﬁnally parasitism, with some examples of each. 1.2.1 Symbiosis The term symbiosis is usually translated as ‘living together’ and is derived from the Greek syn meaning ‘with’ and biosis meaning ‘life’. It was originally used in 1879 by Heinrich Anton de Barry to deﬁne a relationship of ‘any two organisms living in close association, commonly one living in or on the body of the other’. According to this original deﬁnition, symbiosis covers an extremely wide range of relationships. Some authors state that both organisms in a symbiotic relationship beneﬁt from the association (i.e. it is [++]) although this is clearly a much more restrictive deﬁnition and it is more appropriately referred to as mutualism. However, some authors state that symbiosis and mutualism are synonymous – this only adds to the confusion. For the purposes of this book we will keep to de Barry’s original deﬁnition. Symbionts Strictly speaking, a ‘symbiont’ is any organism involved in a symbiotic relationship. However, the vast majority of scientists tend to restrict the term to an organism that lives within JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 1.2 ANIMAL ASSOCIATIONS 3 or upon another organism and provides it with some form of beneﬁt – usually nutritional. The association is therefore referred to as a host: symbiont relationship and the majority of symbionts are microorganisms such as bacteria, algae or protozoa. Where the symbiont occurs within the body of its host, it is referred to as an endosymbiont, while those attached to the outside are re- ferred to as ectosymbionts. Two types of endosymbiont are recognised: primary endosymbionts (or ‘p-endosymbionts’) and secondary endosymbionts. Primary endosymbionts form obligate re- lationships with their host and are the product of many millions of years of co-evolution. They are usually contained within specialised cells and are transferred vertically from mother to offspring. As a consequence, they undergo co-speciation with their host and form very close host-speciﬁc relationships. By contrast, secondary endosymbionts are thought to be the product of more recent host: symbiont associations and, in the case of insects, the symbionts are contained within the haemolymph (blood) rather than specialised cells or organs. Secondary endosymbionts tend to be transmitted horizontally and therefore do not show the same close host: symbiont relationship. It is not known how endosymbionts begin their association with their hosts but some authors sug- gest that they arise from pathogens that attenuated over time. The suggestion that a parasite–host relationship tends to start off acrimoniously and then mellow with time was once widespread in the literature, but while this may sometimes occur, it is not a foregone conclusion. The importance of symbionts to blood-feeding organisms Although blood contains proteins, sugars and lipids as well as a variety of micronutrients and minerals, it lacks the complete range of substances most organisms require to sustain life and to reproduce. Consequently, many of the animals which derive most or all of their nutrition from feeding on blood (haematophagy) have evolved symbiotic relationships with a variety of bacteria that provide the missing substances, such as the B group of vitamins. The need for supplementary nutrients is particularly acute in blood-sucking lice (sub-order Anoplura) because they have lost the ability to lyse (break up) red blood cells and therefore many nutrients will remain locked within these cells. In many cases, the bacteria are held within special cells called mycetocytes that are grouped together to form an organ called a mycetome. Although these terms appear to indicate the involvement of fungi, they originate from a time when scientists did not distinguish between the presence of yeasts and bacteria within cells. Many scientists continue to use the term ‘mycetocyte’ regardless of the na- ture of the symbiont but others use the term ‘bacteriocyte’ where it is known that the cells harbour only bacteria. In blood-feeding leeches belonging to the order Rhynchobdellida (there is a popular misconception that all leeches feed on blood; many of them are actually predatory), mycetomes are found surrounding or connected to the oesophagus. Mycetomes are not found in all blood- feeding leeches and in the medicinal leech, Hirudo medicinalis, the symbiotic bacteria are found within the lumen of the gut (Graf et al., 2006). The bacteria present in Hirudo medicinalis have been identiﬁed as Aeromonas veronii (earlier work on leeches often refers to it as Aeromonas hydrophila), a species of bacteria that has been associated with a number of other blood-feeding organisms. Aeromonas veronii has also been reported as causing wound infections in humans and inducing septicaemia and gastroenteritis. (Graf, 1999). Leeches are extremely useful in modern medicine, particularly to aid wound drainage following plastic surgery, but one of the risks asso- ciated with their application is that the patient acquires an Aeromonas infection. These infections are often trivial but they can become serious and lead to the formation of an abscess or cellulitis (e.g. Snower et al., 1989). This is a difﬁcult problem to solve because the symbiotic bacteria are essential for the leeches. JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 4 CH01 ANIMAL ASSOCIATIONS Box 1.1 The role of symbionts in the life of tsetse ﬂies and their transmission of trypanosome parasites Tsetse ﬂies, like most other blood-feeding organisms, harbour bacterial symbionts that facilitate the breakdown of the blood meal and provide essential nutrients to the ﬂy. In the case of tsetse ﬂies, these are principally B group vitamins, vitamin H (Biotin), folic acid and pantothenic acid and in the absence of the symbionts, the adult female ﬂy is unable to reproduce. Tsetse ﬂies have at least three different symbionts that are found within certain gut epithelial cells and these are passed on from the female ﬂy to her larvae as they develop in her uterus. Of these symbionts, Sodalis glossinidius is thought to be the most important in inﬂuencing the establishment of try- panosomes in the tsetse ﬂy. Tsetse ﬂies have an effective immune system that protects them from invading micro-organisms. This includes the production of lectins that attach to and kill the in- vading organisms and toxic reactive oxygen species such as superoxide and hydrogen radicals (Macleod et al., 2007). However, Sodalis glossinidius releases N-acetylglucosamine which in- terferes with the activity of the lectins and scavenges reactive oxygen species, thereby allowing the trypanosomes to establish. It is possible that there are differences between strains of Sodalis glossinidius in the production of N-acetylglucosamine and this may be (to a greater or lesser extent) the reason why there are differences in the susceptibility of tsetse ﬂies to infection with trypanosomes. In nymphs and adult males of the human body louse, (Pediculus humanus; sub-order Anoplura) intracellular symbionts are found within a mycetome that is sometimes referred to as the ‘stom- ach disc’. This mycetome is located on the ventral side of the mid-gut but unlike the leeches mentioned above, there is no actual connection between the mycetome and the lumen of the gut (Sasaki-Fukatsu et al., 2006; Perotti et al., 2008). In adult female lice, the bacteria re-locate to the oviducts and the developing eggs. This is in keeping with the observation that primary endosym- bionts are transmitted within the eggs (i.e. transovarially) to the offspring. The bacteria associated with Pediculus humanus have been identiﬁed as belonging to the gamma (␥ ) proteobacteria and have been given the name Riesia pediculicola. Interestingly, molecular phylogenetic analysis is unable to distinguish between the symbiotic bacteria isolated from human head lice (Pediculus humanus capitis) and human body lice (Pediculus humanus humanus). This adds support to phy- logenetic analysis of the lice themselves (Light et al., 2008) that indicates that although head lice and body lice occupy different ecological niches and body lice tend to lay their eggs on clothing while head lice attach their eggs to hair shafts, they are two morphotypes of the same species rather than two separate species. One suggestion is that the body lice evolved from head lice relatively recently in human evolution following the common practice of wearing clothing. The association between Riesia and Pediculus is estimated to be between 12.95 and 25 million years old, which makes it one of the youngest host: primary endosymbiont relationships so far recorded (Allen et al., 2009). In common with other primary endosymbionts, Riesia has undergone a re- duction in genome complexity and lost genes: this is because it has come to rely on its host for the provision of many nutrients, protection from the environment and protection from predators. In addition, because its transmission is via the eggs of its host, each louse symbiont population is in JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 1.2 ANIMAL ASSOCIATIONS 5 reproductive isolation and unable to undergo recombination with other strains of Riesia in other lice. This has led to the suggestion that Riesia will lack the capacity to develop rapid resistance mechanisms to antibiotics, and because the Riesia is essential for the lice, killing the symbiont would result in host mortality (Perotti et al., 2008). 1.2.2 Commensalism The term ‘commensalism’ is derived from the Latin commensalis and means ‘at the same table together’. Most deﬁnitions indicate that one species beneﬁts from the association and the other is unharmed (0+). The concept of ‘harm’ within any deﬁnition leads to complications because it may be difﬁcult to measure and depends upon the circumstances. Similarly, a ‘beneﬁt’ may not be immediately apparent and it is possible that some of the associations that are commonly cited as commensal involve a degree of beneﬁt to both parties (++) albeit they may not beneﬁt to the same extent. A commensal association may be ‘facultative’, in which both species are able to live independently of one another, or ‘obligatory’, in which one of the associates must live in association with its partner. For example, in many of the warmer parts of the world, the cattle egret (Bulbulcus ibis) is often observed riding on the back of cattle and big game from which it swoops down periodically to capture lizards and insects that are disturbed as its ride moves through the undergrowth. The egret is perfectly capable of living apart from cattle but it beneﬁts from its mobile ‘vantage point-cum-beater’. The egrets are not thought to remove many ectoparasites from the cattle and they get their Arabic name Abu Qerdan ‘father of ticks’ from the large number of ticks associated with their nesting colonies. The cattle, therefore, appear to gain little from the relationship although it is likely that the egret acts as an early warning system of the approach of predators. African Cape Buffalo (Synceros caffer) have a good sense of smell but notoriously poor eyesight and are therefore vulnerable to predators approaching from downwind. The red-billed oxpecker (Buphagus erythrorhynchus) is sometimes said to have a similar commensal relationship with cattle but this is almost certainly not the case. Unlike cattle egrets, the red-billed oxpecker has an obligatory relationship with cattle and big game, and far from removing ticks, it feeds primarily on scabs and wound tissue pecked from their host. This can delay wound healing and thereby make the affected animal vulnerable to infections and infestations with blowﬂy larvae (Weeks, 2000). The amoeba, Entamoeba coli (not to be confused with the gastrointestinal bacterium Es- cherichia coli which is also abbreviated to E. coli) is a common commensal that lives within the human large intestine. Unlike its highly pathogenic cousin, Entamoeba histolytica, Entamoeba coli does not invade the gut mucosa or consume red blood cells and it feeds on bacteria and gut contents. Entamoeba coli is of little interest per se, but due to its morphological similarity to Entamoeba histolytica, it is important to be able to distinguish between the two species in faecal samples. 1.2.3 Phoresis This association is usually described as one in which one species provides shelter, support or transport for another organism of a different species. This interaction may be temporary or JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 6 CH01 ANIMAL ASSOCIATIONS permanent. For example, apart from the ﬁrst instar, the larvae and pupae of the blackﬂy Simulium neavei attach themselves to the outer surface of freshwater crabs. The larvae feed by ﬁltering out phytoplankton and detritus from the water and the crabs act as a suitable ﬁrm yet mobile sub- strate on which to attach. An appreciation of this association is important because adult Simulium neavei are important vectors of the Onchorcera volvulus – the nematode that causes the disease ‘river blindness’ (see Chapter 3). 1.2.4 Mutualism Mutualistic (from Latin, mutuus meaning ‘reciprocal’) relationships are those in which both species beneﬁt from the association in terms of their growth and survival (++). Some authors further restrict the deﬁnition to one in which neither of the partners in the association is capable of living on their own, while others are less prescriptive. The association between Wolbachia bacteria and the ﬁlarial nematode, Onchocerca volvulus, is clearly mutualistic. The bacteria are conﬁned to the cells of the reproductive tissues and hypodermis of the female worms. The Wolbachia pro- vide metabolites which are demonstrably essential to the worms. If the bacteria are removed, for example, by exposure to the antibiotic tetracycline, the worms are unable to establish themselves in their host and grow and, in the case of adult worms, the female is rendered infertile (Taylor and Hoerauf, 1999). The bacteria are therefore a potential target for the chemotherapy of ﬁlarial nematode infections. Whether or not the relationship between the Cnidarian Hydra viridis and its algal partner Chlorella should be considered mutualistic depends upon the strictness of one’s deﬁnition. Hy- dra viridis are capable of growing and reproducing in the absence of their algal partner but there is some debate in the literature whether the strains/species of Chlorella associated with Hydra viridis can survive independently. The algae live within vacuoles in the endodermal cells of the Hydra and thereby impart the Hydra’s characteristic green coloration. Whether this provides cam- ouﬂage that is any way beneﬁcial is not known. When the Hydra reproduces by budding, its algal partner is passed on to the offspring; the algae are not essential to the budding process but Hydra viridis seldom undergoes sexual reproduction if the algae are absent. Experiments in which the algae are removed from the Hydra by exposure to high light intensities (Habetha et al., 2003) indi- cate that the nature of the relationship varies depending upon the environmental conditions. Like other Hydra species, Hydra viridis obtains its food by capturing prey on tentacles that are armed with nematocysts, while the alga carries out photosynthesis and releases the sugars maltose and glucose-6-phosphate that can potentially be used by Hydra viridis. If there is suitable illumination and plenty of prey for the Hydra, the growth of Hydra viridis with and without algae is similar. This indicates that the sugars released by the algae have little importance for the Hydra. If, how- ever, there is illumination but no food for the Hydra, then those Hydra lacking algae die after a few weeks, while those containing algae reduce in size but are able to survive for at least three months and will feed again if presented with food. Therefore, if Hydra viridis is starved, then the symbiotic algae play an important role in its survival. By contrast, if Hydra viridis are kept in the dark but with plenty of prey available, those lacking algae grow much better than those containing them. Furthermore, the algal population declines by about 60% although they are not lost entirely and the Hydra viridis remain pale green. This indicates that under these conditions, the algae must be receiving nutrients from the Hydra to such an extent that the nature of the relationship has changed from mutualism to one akin to parasitism. JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 1.2 ANIMAL ASSOCIATIONS 7 1.2.5 Parasitism Parasitism is a surprisingly difﬁcult term to deﬁne and there are numerous explanations in the literature. For the purposes of this book, the following deﬁnition has been used: ‘Parasitism is a close relationship in which one organism, the parasite, is dependent on another organism, the host, feeding at its expense during the whole or part of its life (− +).’ It is frequently a highly speciﬁc relationship that always involves a degree of metabolic dependence of the parasite upon its host and often, though not always, results in measurable harm to the host. The association is usually prolonged and although it may ultimately result in the death of the host, this is not usually the case. It is therefore distinct from predation in which a predator usually kills and consumes its prey within a short period of time. However, owing to the complexities of animal relationships, there are always ‘grey areas’ in which any deﬁnition starts to become unstuck. This is particularly apparent in the case of blood-feeding. Mosquitoes and tsetse ﬂies would not be considered parasites because they only feed for a few seconds or minutes before departing; in contrast, hookworms and crab lice would be considered parasitic, because they are permanently associated with their host. Blood- feeding leeches, however, are free-living organisms that remain attached to their host for several hours while taking a blood meal; some authors consider them to be parasites while others deﬁne their feeding as a type of predation. Box 1.2 From welcome guest to villain: the derivation of the term ‘parasite’ The word ‘parasite’ is derived from the Greek ‘para’ meaning ‘beside’ and ‘sitos’ meaning ‘food’. In Ancient Greece, the term ‘parasite’ had religious connotations and nothing to do with infectious organisms. According to a stone tablet in the temple of Heracles (Hercules) in Cynosarges, the priest was required to make monthly sacriﬁces in the presence of ‘parasites’ who were to be drawn from men of mixed descent. Refusal to act as a parasite would result in being charged with committing an offence. (Cynosarges was an area near to the city walls of Athens. In addition to the temple, there was also a gymnasium and it was where the Cynic philosophers gave classes.) Subsequently, the word was debased and came to mean someone who shared one’s food in return for providing amusement and ﬂattery. The ‘parasitus ridiculus’ was a popular character in Greek and early Roman comedies and they even had joke books to help them should they run out of witticisms. The greed of the parasite was a constant source of fun for dramatists and he was often given crude nicknames such as ‘little brush – because he swept the table clean’. Double entendres were as popular over 2000 years ago as they are today and the Latin for little brush ‘peniculus’ is also a diminutive for penis (Maltby, 1999). Some organisms are obligate parasites and at a particular stage in their life cycle they have to live as parasites of their host while others are facultative parasites and can develop as parasites or free-living organisms depending upon the circumstances they ﬁnd themselves in. For example, the larvae of the warble ﬂy Hypoderma bovis have to develop as parasites of cattle and are therefore obligate parasites. By contrast, the larvae of the blowﬂy Lucilia sericata are facultative parasites because they are able to develop as parasites should the eggs be laid upon a live sheep or as free-living detritivores if the eggs are laid on a dead sheep. JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 8 CH01 ANIMAL ASSOCIATIONS As mentioned above, some organisms, such as the human body louse Pediculus humanus, are parasitic at all stages of their life cycle, while others are only parasitic at one or more stages. For example, the blood ﬂuke Schistosoma haematobium is a parasite of humans during its adult stage and of snails during two of its larval stages but it also has two non-feeding free-living stages. The act of being a parasite is therefore ‘stage-speciﬁc’. Some estimates suggest that as many as 50% of all known species are parasites at some point in their life cycle. However, this estimate is subject to the caveat that there is some debate about what constitutes a species, especially among the prokaryotes. The number of species is also reﬂected in the interests of biologists in different groups of animals. For example, insects have been studied intensively for over 200 years and this is probably at least partly the reason why they are said to account for 72% of all known species. In one order alone, the ‘species-rich’ order Hymenoptera (bees, wasps), approximately 100,000 species are classed as parasitoids. By contrast, mites and nematodes have proved much less pop- ular and the diversity of their parasitic species is probably vastly underestimated. Nevertheless, parasitism is a remarkably common lifestyle and parasites (and their hosts) have been described from all the major groups of living organisms including the Archaea, Bacteria, Fungi, Plantae, Protozoa, invertebrates and vertebrates. There is some debate as to whether viruses should be con- sidered to be parasitic organisms. At one level, this would appear to be self-evident since viruses are incapable of maintaining themselves or reproducing except when within their host cell. How- ever, being composed of complex organic molecules and having the capacity to evolve is not necessarily synonymous with being a living entity, especially when those attributes are dependent upon existing within a host cell. The arguments against viruses being alive are discussed in detail by Moreira and López-Garcia (2009). In this book, we will mainly consider parasitic helminths (ﬂatworms and nematodes), arthropods and protozoa. The relationships between parasites in these groups and their hosts have been extensively studied and some of them have a major impact on our health and that of our domestic animals. 1.2.6 Intra-speciﬁc parasites Although most parasitic relationships involve two different species of animals, it is not unknown for intra-speciﬁc parasitism to take place. This is most often associated with adaptations to sexual reproduction in which the male attaches to the female and becomes dependent upon her for the provision of nutrients. For example, in certain deep-sea angler ﬁsh belonging to the suborder Ceratioidea, the larval ﬁsh develop in the upper 30 metres of sea water and then gradually descend to deeper regions as they metamorphose into adults. The adolescent males have a very different morphology to the females: they are much smaller, they have larger eyes and in some species they develop a large nasal organ that is presumably involved in their search for females. Furthermore, the males cease feeding and rely upon reserves laid down in their liver during the larval period to fuel their swimming. Upon ﬁnding a suitable female, the male grasps onto her using special tooth- like bones that develop at the tips of his jaws (his actual teeth degenerate during metamorphosis). Once he has attached, the male grows (although he remains much smaller than his consort) and his testes mature. His skin and blood vessels fuse with hers at the site of attachment and he remains attached for the rest of his life and draws all his nourishment from her. Some authors suggest that the male must ﬁnd a virgin female but although most females carry only a single male, there are records of females with three or more males attached to them. This is presumably an adaptation to life in the deep-sea regions in which the opportunity to locate suitable mates is limited. It does, JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 1.2 ANIMAL ASSOCIATIONS 9 however, beg the question of how sexual selection takes place because it is unusual in nature for a female to mate with just one male for life, especially if that male is the ﬁrst one to turn up. This type of relationship is not found in all ceratioid anglerﬁsh; in some species the males are facultative parasites rather than obligate ones as described in the above scenario, while in other species the males are free-living, capable of capturing their own food, and form only temporary attachments to females. Molecular evidence suggests that the development of the parasitic males is a variable phenomenon among anglerﬁsh and has evolved and subsequently become lost on several occasions (Shedlock et al., 2003; Pietsch, 2005). 1.2.7 Parasitoids The term parasitoid is restricted to certain parasitic insects whose hosts are almost exclusively other insects – although a few species attack certain crustacea, spiders, millipedes, centipedes and earthworms. Some parasites cause mortality and may even depend on the death of their host to effect transmission to the next stage of their life cycle, but host death is not inevitable. By contrast, parasitoids slowly consume their host’s tissues over a period of time so that the host remains alive until the parasitoid has completed its development. At this point the host dies either through the loss of vital tissues or through the parasitoid physically eating its way out of its host. Parasitoids are all parasitic during their larval stage and the adult insect is free-living and feeds on nectar, pollen or is predatory, depending upon the species. Parasitoids can develop as endoparasites within their host or as ectoparasites attached to the outside but with their mouthparts buried deep within the host’s body. The larva has only the one host in or on which it develops and those that are endoparasites tend to exhibit the most host speciﬁcity. This lifestyle is therefore distinct from those insects such as warble ﬂies (e.g. Hypoderma bovis) and bot ﬂies (e.g. Gasterophilus intestinalis) which exhibit a more ‘traditional’ parasitic way of life that does not inevitably result in the death of the host. Many of the order Hymenoptera (bees, ants, wasps) are parasitoids and it is also a common lifestyle among the Diptera (true ﬂies) but it is absent or very rare among the other orders. By contrast, most of the insect orders are hosts to parasitoids. Hyperparasitism is also common in which a parasitoid parasitises another species of parasitoid. Parasitoids are effective for the control of agricultural pests, particularly within closed environments such as greenhouses. However, they have had limited success as control agents for parasites, their vectors, or intermediate hosts. The parasitoid lifecycle typically begins with the adult female locating a suitable host and either injecting one or more eggs into the host or attaching them to the outer surface. Sometimes she also injects a toxin that temporarily or permanently disables her victim. The host is chosen on the basis of its stage of development which may be anywhere from the egg to the adult stage. Box 1.3 Parasitoid: virus interactions A number of endoparasitic wasps belonging to the families Icheumonidae and Braconidae have a fascinating relationship with certain polydnaviruses. The viruses replicate within the calyx cells of the wasps’ ovaries and are secreted into the oviducts. When a wasp injects her eggs into a suitable host, usually a caterpillar, the virus is transmitted as well. The viruses are unable to JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 10 CH01 ANIMAL ASSOCIATIONS replicate within the caterpillar but they can invade several cell types within which they integrate into the genome and cause the expression of substances that facilitate the establishment of the parasitoid. For example, one of the main immune responses that insects express in response to an invader is encapsulation (see Chapter 6). Encapsulation ﬁrst depends upon the invader be- ing recognised, and then a co-ordinated response occurs, during the course of which the invader is surrounded by amoeboid-like cells present in the haemolymph and then killed through the production of toxic chemicals and/or lack of oxygen, or the invader is physically isolated and therefore unable to damage the host. Wasp eggs that are implanted into suitable hosts without the virus are quickly encapsulated and killed. It is thought that the virus may cause the caterpil- lar to express protein tyrosine phosphatases and thereby interfere with the encapsulation process. Protein tyrosine phosphatases dephosphorylate the tyrosine residues of a number of regulatory proteins and are therefore closely involved in the regulation of signal transduction. Altering the levels of regulatory proteins makes it impossible for the host to develop an effective immune response and the parasitoid egg is able to develop unmolested. The viruses also have other ef- fects on the parasitoid’s host including preventing its further development once it reaches the stage at which the parasitoid is to emerge. The polydnaviruses therefore have a mutualist-like relationship with the parasitoid within which they replicate. They are vertically transmitted as an endogenous ‘provirus’ that is integrated into the wasp genome but has a pathogenic relationship with the parasitoid’s host, within which it is unable to replicate (Webb et al., 2006). Not all wasp parasitoids have relationships with viruses but they are still capable of causing similar disruption to the host immune response and host development through the injection of toxins. This has led some authors to suggest that the polydnaviruses found in the Ichneumonidae and Braconidae may have evolved from wasp genes. Many workers, however, think that the two wasp families, probably independently, evolved relationships with existing viruses (Dupas et al., 2008; Espagne et al., 2004). 1.2.8 The concept of harm The term ‘harm’ is often used when describing interactions between organisms but is particularly pertinent to the description of parasitism. Unfortunately, harm is a difﬁcult term to deﬁne and is not always easy to measure. For example, parasites are usually much smaller than their host and a single parasite may have such a minor impact that it cannot be measured in terms of its effect on the physiology and well-being of the host. By contrast, a large number of the same parasite could lead to serious illness or even death. Similarly, a low parasite burden may have little impact upon a healthy, well-nourished adult host but the same number of parasites infecting an unhealthy, starving young host may prove fatal. A common analogy is that a single glass of water will not harm you and may even do you good, but the rapid consumption of a thousand glasses of water would kill you. Does that mean that water is beneﬁcial or poisonous? Clearly, it can be both and, likewise, harm is dependent upon the context in which it is being considered. It is therefore not a good idea to make the ability to record measurable harm a prerequisite for the classiﬁcation of the relationship between two organisms. Indeed, it is now recognised that, in certain instances, low levels of parasitic infection may actually be beneﬁcial to the well-being of the host (Weinstock et al., 2004). Nevertheless, many parasites have the capacity to cause morbidity, that is, a diseased JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 1.3 PARASITE HOSTS 11 state, and some may cause mortality (death). The possible beneﬁcial consequences of low parasite burdens will be discussed in more detail in Chapter 8. The morbidity that parasite infections induce is often reﬂected in a reduction in the host’s ﬁt- ness as measured in terms of its growth or reproductive output. This is often attributed to the direct pathogenic effect of the parasite, such as through the loss of blood and the destruction of tissues or competition for resources (e.g. gut parasites feeding on nutrients in the intestine). However, in reality, the situation is far more complicated than this. Although a functional im- mune system is crucial to an organism being able to protect itself against pathogens, they are energetically costly and these costs often have to be traded off against other physiological pro- cesses. Ilmonen et al. (2000) demonstrated this by injecting one group of breeding female pied ﬂycatchers (Ficedula hypoleuca) with a diphtheria-tetanus vaccine and a control group with a saline solution. The vaccine was not pathogenic and did not induce an infection but it did cause the activation of the birds’ immune system. They found that the birds injected with the vaccine ex- hibited a lower feeding effort, invested less in self-maintenance and had a lower reproductive output, as determined by ﬂedgling quality and number. The authors therefore concluded that the energetic consequences of activating the immune system can be sufﬁcient to reduce the host’s breeding success. 1.3 Parasite hosts ‘Parasite host’ is the term used to deﬁne the organism on or in which the parasite attaches and from which it derives its nutrition. The host is usually not related taxonomically to the parasite although this is not always the case (see intra-speciﬁc parasites). Most parasites are highly host- speciﬁc and only infect one host species or a group of closely related species. This is due to the complex adaptations the parasite is required to evolve in order to identify, invade and survive within their host. For example, the nematode Ascaris suum is primarily a parasite of pigs while Ascaris lumbricoides is primarily a parasite of humans. A few parasite species, however, are able to exploit a wide range of hosts. For example, the protozoan parasite Toxoplasma gondii is ca- pable of infecting, growing and asexually reproducing in virtually all warm-blooded vertebrates although sexual reproduction only takes place within the small intestine of cats. 1.3.1 Protozoa and helminths as hosts Parasites can be infected by viruses although there is limited published information on how these affect their biology. Viruses have been identiﬁed in many parasitic protozoa, such as Entamoeba histolytica (Mattern et al., 1974) and Giardia lamblia (Wang and Wang, 1986), and it would be surprising if they were not common in helminth parasites. Parasites are also infected by prokary- otic (e.g. bacteria) and eukaryotic (e.g. fungi, and protozoa) parasites. Those parasites that infect other parasites are known as hyperparasites. For example, the microsporidian Nosema helmintho- rum is parasitic on the tapeworm Moniezia expansa that lives within the small intestine of sheep and goats (Canning and Gunn, 1984). The infective cysts of Nosema helminthorum must therefore ﬁrst be consumed by a sheep and then come into contact with and penetrate the tegument (tape- worms lack a gut of their own) of the tapeworm. Within the tapeworm, Nosema helminthorum re- produces and causes numerous raised opaque bleb-like patches but is not thought to be especially JWST138-c01 JWST138-Gunn January 13, 2012 19:14 Printer Name: Yet to Come P1: OTA/XYZ P2: ABC 12 CH01 ANIMAL ASSOCIATIONS pathogenic. Related microsporidia affect a range of other platyhelminth parasites (Canning, 1975) but there are remarkably few reports of them infecting parasitic nematodes (e.g. Kudo and Hether- ington, 1922). The discovery of microsproridia infecting the free-living nematode Caenorhabditis elegans (Hodgkin and Partridge, 2008; Troemel et al., 2008) has opened up the potential of devel- oping a laboratory model for studying both nematode immunity and the biology of microsporidia. This is because Caenorhabditis elegans is a commonly used model organism whose full genome has been sequenced. Microsporidia cause a number of pathogenic infections in humans and do- mestic animals and a simple laboratory model would prove extremely useful, for example, in the development of drug treatments. 1.3.2 Classes of hosts for parasites Hosts can be divided into classes, depending upon the role they play in the parasite’s life cycle. The ‘deﬁnitive’ (or ﬁnal) host is the one in, or on, which the parasite reaches maturity and undergoes sexual reproduction, while the ‘intermediate’ host is the one in which the paras

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