LEECHES, LICE AND LAMPREYS Leeches, Lice and Lampreys

A Natural History of Skin and Gill Parasites of Fishes

by Graham C. Kearn School of Biological Sciences, University of East Anglia, Norwich, United Kingdom A C.I.P. Catalogue record for this book is available from the Library of Congress.

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Cover photograph: The cymothoid isopod parasite Anilocra pomacentri attached in its typical position on the head of the Barrier Reef chromis (Chromis nitida). Reproduced with kind permission of Dr Robert Adlard, Queensland Museum, South Brisbane, Australia.

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Printed in the Netherlands. Frontispiece. A common sole (Solea solea) from the North Sea infested with the leech Hemibdella soleae. Photograph by Sheila Davies. I dedicate this book to my grandchildren, Megan and Thomas.

“………….whilst this planet has gone cycling on according to the fixed law of gravity, from so simple a beginning endless forms most beautiful and most wonderful have been, and are being evolved.”

Charles Darwin (1859). Concluding line from “The Origin of Species by means of Natural Selection”. TABLE OF CONTENTS ______

Preface xv

Acknowledgements xvii

Introduction 1

1 The hosts 2 1.1 Overview 2 1.2 The British Fish Fauna 2 1.3 The external features of fishes 5 1.4 Fish skin 8 1.5 Skin and gill mucus 11 1.6 Fish gills 12 1.6.1 The gills of teleosts 12 1.6.2 The gills of elasmobranchs 16 1.7 Resistance and repair 16

2 ‘Protozoans’ 22 2.1 Introduction 22 2.2 Epizoic ciliates 22 2.3 An ectoparasite – Ichthyobodo 27 2.3.1 Free-swimming stage 28 2.3.2 Parasitic stage 29 2.3.3 Pathological effects 30 2.4 A parasite of the epidermis – Ichthyophthirius 30 2.4.1 Infective stage 30 2.4.2 Parasitic stages 32 2.4.3 Escape from the host 34 2.4.4 Encysted stage 35 2.4.5 Pathological effects 36

3 Monogenean (flatworm) skin parasites – Entobdella 37 3.1 Introduction to monogeneans 37 3.2 The biology of Entobdella soleae 39 3.2.1 Attachment and locomotion 40 3.2.2 Food, feeding and egestion 43 3.2.3 Mating 46 3.2.4 Egg assembly 46 3.2.5 Life with little oxygen 47 3.2.6 The egg, hatching and host finding 48 3.2.7 The larva and host invasion 51 3.2.8 Post-invasion migration 52 x TABLE OF CONTENTS

3.2.9 Host to host transfer and migration of adults and juveniles 55 3.2.10 Why migrate to the lower surface? 57 3.3 Entobdella hippoglossi 58 3.4 Entobdela diadema 58 3.5 Host specificity and host switching 59

4 Other monogenean skin parasites 61 4.1 Introduction 61 4.2 Capsala martinieri 61 4.3 Acanthocotylids 62 4.4 Microbothriids 66 4.5 Udonellids 68 4.6 Gyrodactylids 70 4.6.1 Attachment 72 4.6.2 Feeding 73 4.6.3 Consequences of viviparity 74 4.6.4 Transmission to new hosts 75 4.6.5 Host specificity 77 4.6.6 Gyrodactylids in Britain 78 4.6.7 The threat of Gyrodactylus salaris 80

5 Monogenean gill parasites – monopisthocotyleans 82 5.1 Introduction 82 5.2 Unspecialised gill parasites 83 5.3 ‘Dactylogyroideans’ 83 5.3.1 The British fauna 83 5.3.2 Attachment 85 5.3.3 Partial endoparasitism – Amphibdella flavolineata 93 5.3.4 Locomotion 96 5.3.5 Copulatory apparatus 98 5.3.6 Ecology of ancyrocephalines from mullets 101

6 Monogenean gill parasites – polyopisthocotyleans 103 6.1 Introduction 103 6.2 British polyopisthocotyleans 103 6.3 Attachment 105 6.3.1 Hexabothriid suckers 107 6.3.2 Suctorial clamps of Diclidophora spp. 108 6.3.3 The open clamps of Cyclocotyla 111 6.3.4 Non-suctorial clamps 112 6.3.5 Anthocotyle merluccii from hake, Merluccius merluccius 113 6.4 Food and feeding 114 6.5 Symmetry versus asymmetry 116 6.5.1 Reasons for asymmetry in Axine 117 6.5.2 Are asymmetrical parasites sedentary? 119 6.5.3 Maintenance of symmetry 119 6.6 Eggs, hatching and host finding 121 TABLE OF CONTENTS xi

6.6.1 Convergent evolution of dogfish parasites 122 6.6.2 Rhythmical hatching in Discocotyle sagittata 123 6.6.3 Hatching response to shadows in Plectanocotyle gurnardi 123 6.6.4 Egg bundles and mechanical stimulation in Diclidophora luscae 124 6.6.5 Diapause (?) in Gastrocotyle trachuri 125 6.7 Route to the gills 126 6.8 Niche restriction and mating 127

7 Leeches 131 7.1 Introduction 131 7.2 The British fauna 132 7.2.1 Marine leeches 132 7.2.2 Freshwater leeches 135 7.3 Attachment 137 7.4 Locomotion 139 7.5 Host finding 140 7.6 Feeding 141 7.7 Mating 145 7.8 Cocoon assembly 147 7.9 Some observations on life cycles 149 7.9.1 Marine leeches 149 7.9.2 Freshwater leeches 150 7.10 Leeches as transmitters of diseases 152

8 Siphonostomatoid copepods: (1) Fish lice – caligids 154 8.1 Introduction to copepods 154 8.2 General features of caligids 155 8.3 The adult caligid 159 8.3.1 The role of the suctorial cephalothorax in attachment 159 8.3.2 Locomotion 160 8.3.3. Sensory capabilities 160 8.3.4 Camouflage 161 8.3.5 Feeding 161 8.3.6 Mating 164 8.3.7 Site preference 166 8.4 Fate of the eggs 167 8.5 Nauplius larvae 167 8.6 The copepodid 168 8.6.1 Host finding 168 8.6.2 Settlement and initial attachment to the host 169 8.7 Chalimus stages 170 8.8 The problem of moulting 171 8.9 Host specificity and speciation – Lepeophtheirus pectoralis 173 8.10 ‘Sea lice’ and salmonid fishes 174 8.10.1 Pathology and host susceptibility 176 8.10.2 Control 176 xii TABLE OF CONTENTS

9 Siphonostomatoid copepods: (2) pennellids 178 9.1 Lernaeocera 178 9.1.1 Invasion of the first fish host and larval development 180 9.1.2 Mating 182 9.1.3 Establishment and growth of the egg-laying female 184 9.1.4 Ectoparasite or endoparasite? 185 9.1.5 Taxonomic problems and British species 185 9.2 Eye-maggots – Lernaeenicus 186 9.2.1 Lernaeenicus in British waters 187 9.2.2 Life cycle 188 9.2.3 The question of pathogenicity 193

10 Siphonostomatoid copepods: (3) lernaeopodids 195 10.1 Introduction – changes in attachment 195 10.2 The salmon gill maggot 196 10.2.1 Occurrence and site of attachment 196 10.2.2 Feeding in the adult female 197 10.2.3 Hatching and invasion of the host 197 10.2.4 Development on the host 198 10.2.5 Mating 203 10.2.6 Relationship with the salmon life cycle 205 10.3 Other British lernaeopodids 205

11 Cyclopoid copepods – the anchor worm 208 11.1 Introduction 208 11.2 Life cycle 210 11.3 Pathology and resistance 213 11.4 The anchor worm in Britain 213

12 Poecilostomatoid copepods 214 12.1 Introduction 214 12.2 Ergasilids 214 12.2.1 British ergasilids 215 12.2.2 Development and attachment of the female 220 12.2.3 Food, feeding and colour 224 12.3 Bomolochids and taeniacanthids 226 12.4 The chondracanthids 228 12.4.1 The adult female 229 12.4.2 Where is the male? 230 12.4.3 The life cycle 232 12.4.4 A mesoparasitic chondracanthid – Lernentoma asellina 233 12.5 Philichthyids 234

13 The common fish louse – Argulus 237 13.1 Introduction 237 13.2 General morphology 238 13.3 British branchiurans 239 TABLE OF CONTENTS xiii

13.4 Attachment 241 13.5 Host finding 244 13.6 Food and feeding 249 13.7 Reproductive systems and mating 251 13.8 Eggs 257 13.9 Hatching and development 258 13.10 Interactions with other organisms 261 13.11 Relationships 263

14 A mesoparasitic barnacle – Anelasma 265

15 Isopods 274 15.1 Introduction 274 15.2 British isopod fish parasites 275 15.3 Cymothoids 277 15.3.1 General morphology 278 15.3.2 Sex change and mobility 279 15.3.3 Mating 281 15.3.4 Egg incubation and hatching 282 15.3.5 Infecting new hosts 283 15.3.6 Nature of the food 284 15.4 Gnathiids 284 15.4.1 Host invasion 285 15.4.2 Attachment to the fish 285 15.4.3 Mouthparts 286 15.4.4 Feeding and digestion 288 15.4.5 Transmission of microorganisms 290 15.4.6 Predation on gnathiid larvae 291 15.4.7 The free-living reproductive phase in Paragnathia formica 292

16 Unionacean molluscs (naiads) 296 16.1 Introduction 296 16.2 The adult unionacean 297 16.3 The life cycle 299 16.4 British unionaceans 300 16.5 The swan mussel – Anodonta cygnea 301 16.5.1 The glochidium 301 16.5.2 Host finding and establishment on the host 302 16.5.3 Host specificity and infection sites 304 16.5.4 The parasitic stage 307 16.6 The pearl mussel – Margaritifera margaritifera 308 16.6.1 The glochidium 310 16.6.2 Infection of the host 311 16.6.3 Survival in the host 312 16.6.4 Development of glochidia 313 16.6.5 Host specificity 313 16.6.6 Overview of the life cycle 313 xiv TABLE OF CONTENTS

16.6.7 Threats to the pearl mussel 314 16.7 Some special unionaceans 315 16.8 Acquired immunity to glochidia 316

17 Lampreys 318 17.1 Introduction 318 17.2 The river lamprey – Lampetra fluviatilis 320 17.2.1 The ammocoetes 320 17.2.2 Metamorphosis (transformation) 323 17.2.3 Attachment, feeding and breathing in the adult 324 17.2.4 Spawning 329 17.3 The sea lamprey – Petromyzon marinus 333 17.4 Flexibility of lamprey life cycles 334 17.4.1 Loch Lomond lampreys 334 17.4.2 Sea lampreys in North America 335 17.4.3 The brook lamprey – Lampetra planeri 336 17.5 Other fishes with parasitic tendencies 337

18 Conclusions 339 18.1 Crustacean dominance 339 18.2 Life cycles 339 18.3 Reproductive biology 340 18.4 Attachment and feeding 341 18.4.1 Hooks, harpoons and pincers 341 18.4.2 Suction 343 18.4.3 Glands 343 18.4.4 Mesoparasites 344 18.4.5 Diet 346 18.5 Pathogenesis and host defences 346 18.6 Host specificity and speciation 347 18.7 Morphology and molecules 348 18.8 Habitat selection and niche restriction 349 18.9 The future of the British parasite fauna 350

Appendix 1 Classified list of fishes with common and scientific names 353

Appendix 2 Classified list of genera of epizoic and parasitic invertebrates 361

Glossary 365

References 375

Index of scientific and common names 419

Subject Index 425 PREFACE ______

This book is about the lives of parasites found on the skin and gills of freshwater and marine fishes. Although many of these parasites are large enough to attract the attention of fishermen, aquarists or naturalists, their biology is well known only to a few professional parasitologists and the book is intended as a reference work for anyone with an interest in finding out more about the natural history of these fascinating, sometimes bizarre and often commercially important animals. The idea for this book has its origins in the “New Naturalist” series of volumes, published by Collins. These books are scientifically up-to-date accounts of British natural history topics, written in such a way that they appeal to professional biologists as well as to informed naturalists. In 1952, Miriam Rothschild and Theresa Clay published a volume in this series entitled “Fleas, Flukes and Cuckoos”. In this book the authors described the natural history of parasites of British birds and included an account of the virtually unknown feather lice or Mallophaga and a study of the special brood parasitism of the cuckoo. This book is no longer in print, but when it was published it was a new venture, representing a considerable departure from the topics covered by previous volumes in the series. A few years later, in 1959, Sir Alistair Hardy published another volume in the New Naturalist series, namely “The Open Sea, Fish and Fisheries”. In this book he clearly recognised the importance of parasites, as the following quotation from the book demonstrates:

“There must be few adult animals of the size of a small fish (or larger) which do not harbour at least two or three different kinds of parasite. When we consider this, and that every host may carry several of each kind, we begin to realise a fact of nature which at first seems to us most extraordinary: the number of animals we see living freely in the world……is actually far smaller than the number living tucked away in their insides.”

Hardy went on to focus for the first time on parasites of fishes, but he had space to deal with them only in a superficial way as part of a chapter devoted to parasitism in general. He summarised the problem as follows:

“The lives of parasites present as fascinating a field of study to the naturalist as any other; lack of space unfortunately, will only allow the briefest introduction to the subject in a book devoted to the whole of the open sea.”

Since that time there has been no comprehensive attempt to describe the biology of fish parasites, despite the fact that the parasite fauna of totally aquatic vertebrates like fishes is substantially different from the parasite fauna of terrestrial vertebrates like birds. xvi PREFACE

Encouraged by Hardy’s words and by my professional interest in fish parasites, the idea of a whole volume devoted to fish parasites began to take shape. This was fuelled by the relatively recent resurgence of interest in parasitism and parasites, with the increasing awareness of the numbers and diversity of parasitic organisms, the influence that they may have on communities and their potential as a force for evolutionary change. Having decided to write about fish parasites, I was faced with the problem that a book of acceptable size is too small to accommodate the great diversity of parasites, even when this diversity is restricted to parasites of a single major host group such as the birds or fishes. I did not wish to restrict the fish groups even further by limiting the study to either freshwater fishes or to marine fishes - this would inevitably exclude many parasites that are of special interest. I decided therefore to restrict the parasites rather than the hosts by focussing on those parasites that are most likely to be encountered by the aquarist, angler or naturalist. These are the external parasites or ectoparasites, living on the surfaces washed by water. Naturally this includes the gills as well as the skin. Many skin parasites extend their range onto the gills and many gill parasites are closely related to skin parasites. Larger ectoparasites on the skin are visible with the naked eye, and those on the gills may be seen if the gill cover or operculum is raised. Some ‘protozoan’ ectoparasites are too small to be seen, even with a hand lens, but they may be present in sufficiently large numbers to induce pathological changes that are visible externally. I have excluded all the endoparasites, that is those parasites dwelling inside the host’s body, such as tapeworms, roundworms and most ‘protozoans’, but brief mention has been made of a few that are transmitted by ectoparasites. The examples of fish parasites referred to in the book are mainly taken from the British fauna, thereby complementing the study of bird parasites by Rothschild and Clay. However, all the major groups of fish ectoparasites have representatives in the British fauna and many of the British examples, or their close relatives, have extensive geographical ranges in the northern hemisphere or beyond. Wherever appropriate I have made reference to interesting parasites not represented in the British fauna. Consequently, the non-British reader should feel comfortable and familiar with the subject matter of the book. For the British reader I have provided for each group of parasites a brief summary of the British fauna. In writing this book I have tried to produce a well-illustrated text that is up-to- date and sufficiently informative to satisfy the professional biologist, but, at the same time, comprehensible and interesting for the enquiring amateur. Wherever possible I have attempted to explain terms and concepts as they arise in the text. In addition, terms that are used frequently in the text are defined in a glossary. To set the scene, I have included an introductory chapter (Chapter 1) on the general biology of fishes. I have used the common names of fishes where appropriate in the text, but the corresponding scientific names of all the fishes are also indicated and the interrelationships and environmental preferences of the fishes mentioned in the book are given in Appendix 1. The generic names of the parasites and their relationships are presented in Appendix 2.

Graham Kearn Norwich July 2004 ACKNOWLEDGEMENTS ______

I am greatly indebted to many people for help and advice throughout the preparation of this book. I am particularly grateful to the following, who kindly took on the task of reading and reviewing drafts of selected chapters related to their own special interests, as well as helping in other ways: Eugene Burreson, Leslie Chisholm, Roger Lincoln, Peter Maitland, Nigel Merrett, Alan Pike, Ian Whittington, Rodney Wootten and Mark Young. Their advice was invaluable and any errors remaining in the text are entirely my responsibility. I am also grateful to Sheila Davies of the University of East Anglia for her photographic help, to Emma Roberts and other staff at the library of the Centre for Environment, Fisheries and Aquaculture Science, Lowestoft for patiently satisfying endless requests for papers, to Deirdre Sharp at the Library of the University of East Anglia for seeking permission for use of the many illustrations and to Paul Wright also of the University of East Anglia for advice on IT matters. Others who have helped are listed alphabetically as follows: Rob Adlard, David Aldridge, Geoffrey Boxshall, Angela Davies, Bo Fernholm, Bill Gaze, David Gibson, Eileen Harris, Peter Heuch, Tammy Horton, Bozena Koubková, Iveta Matejusová, Andy Shinn and Vaughan Southgate. Comments on my original proposal by anonymous referees also helped to shape the book. My wife Margaret provided useful criticism of the manuscript and invaluable encouragement during the long process of preparation. INTRODUCTION ______

Fishes, especially the teleosts or bony fishes, are the most abundant of the vertebrates and most aquatic habitats on the planet have been colonised by them. Their abundance and diversity are matched by their parasites1. Practically every tissue and organ in a fish’s body provides a substrate or niche for parasites. The skin and gills, those surfaces of fishes that are in contact with water, offer particularly favourable conditions for the establishment and survival of parasitic animals. Many parasites of fishes choose to attach themselves externally to these surfaces (ectoparasites), while others are partly exposed and partly embedded in host tissue (mesoparasites). External parasites of fishes do not have to cope with dehydration, as do the mainly arthropod ectoparasites of terrestrial and aerial vertebrates, and food is much more accessible in the form of living epithelial cells covering the skin and gill surfaces or the rich and superficial supply of blood flowing through the gills. It is these ectoparasites and mesoparasites, many of which are large enough to be visible to the naked eye, that concern us in this book. Many other parasites live inside the body of the host (endoparasites), where they are hidden from the observer, although they may betray their presence by the effects their activities have on the condition or behaviour of the host, or by the release externally of their offspring (eggs or larvae). Endoparasites reach their internal sites by penetration of the skin or the gill epithelium or by ingestion in food. Some endoparasites may be descended from parasites living on the skin and gills and therefore a thorough knowledge of the biology of external parasites of fishes is important if we are to understand how parasites evolve and progress. Given the wide distribution and abundance of fishes and the accessibility and vulnerability of their skin and gill surfaces, it is not surprising that interactions between invertebrates and fishes have been frequent in the past and that many of these associations have led to parasitism. The range of invertebrates with representatives that parasitise the external surfaces of fishes is broad and includes ‘protozoans’, flatworms, annelid worms, many kinds of crustaceans and molluscs (see Appendix 2). Even lampreys, which are agnathan (jawless) vertebrates (see Appendix 1), have become parasitic on some of their gnathostome (jawed) relatives. However, before considering the parasites we need information about the hosts, in particular an appreciation of the range of types of fishes and their habitats, the structure of their skin and gills and the nature of the defences that they are able to mobilise against parasites. These topics will be considered in Chapter 1.

1 In this book the term ‘parasite’ is restricted to unicellular or multicellular eukaryotic animals that derive benefit from a symbiotic relationship at the expense of their partner (the host).