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A Study of the Pathobiology of Pomphorhynchus Laevis Muller•• in Freshwater Fish

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A Study of the Pathobiology of Pomphorhynchus Laevis Muller•• in Freshwater Fish A STUDY OF THE PATHOBIOLOGY OF POMPHORHYNCHUS LAEVIS MULLER•• IN FRESHWATER FISH by Stephen Terry Wanstall Thesis submitted in partial fulfilment for the degree of Doctor of Philosophy of the . Council for National Academic Awards DERBYSHIRE COLLEGE OF HIGHER EDUCATION JULY 1984 . ' A STUDY OF THE PATHOBIOLOGY OF Pomphorhynchus laevis MUller IN FRESHWATER FISH S.T. Wanstall ABSTRACT The relationship between adult P. laevis and its host was studied in terms of local and whole-body effects of infection. The study was confined to a naturally-infected population of the stone loach, Noemacheilus barbatulus L., from the river Severn and to experimentally-infected rainbow trout, Salmo gairdneri Richardson, maintained in the laboratory. The praesomal and metasomal integuments of P. laevis possessed surface layers that differed both structurally and chemically. Antigenic sites occurred throughout the integument and in some other tissues, suggesting that the antigens were excretory/s~cretory products. Incidence of infection and worm burden increased with the age of the stone loach; within the stone loach population, the parasites were overdispersed. In both hosts, the intestine posterior to the bile duct junction was the primary site of occurrence of P. laevis. The praesoma penetrated the gut wall and was invested by vascularised, collagenous inflammation tissue. The metasoma occupied the intestinal lumen abrading and compressing the mucosal epithelium. Heterophil granulocytes and fibroblasts char­ acterised the inflammatory response of the stone loach; neutrophils, eosinophilic granular cells and plasma cells were common in the trout. Neither host's 'inflammatory response seemed capable of rejecting P. laevis. Assessment of the nutritional status of infected hosts revealed a negative correlation between parasite burden and muscle protein concentration for spawning 2+ stone loach. Experimentally-infected trout may show a reduction in growth rate, particularly when subject to environmental stress. Although P. laevis can induce deleterious changes in an individual host, its overdispersed distribution in stone loach from the river Severn renders it unlikely that this parasite is a major pathogen of this population. 2 ACKNOWLEDGEMENTS I am very grateful to my supervisors, Dr P.W.J. Robotham and Dr J.S. Thomas for their invaluable help, advice and critical appraisals of this thesis; to Dr J.E. Harris for providing the rabbit anti-trout serum; to Derby~hire College of Higher Education and Plymouth Polytechnic for the provision of facilities and to staff in the School of Sciences for advice and assistance at various times. I would also like to thank Pat for the homogenising, Mrs S. Robotham for deciphering pencil scribblings and converting into typescript, and to J~ for listening. 3 CONTENTS PAGE ABSTRACT 2 ACKNOWLEDGEMENTS 3 GENERAL INTRODUCTION 7 CHAPTER 1. The integument of P. laevis, with particular reference to the praesomal integument. 12 Introduction 13 Section A : Structure and Composition 16 Materials and Method 17 Results 20 Discussion 41 Section B : Antigenic sites Materials and Method 51 Results 54 Discussion 57 2. The distribution and growth of P. laevis in stone loach and rainbow trout. 60 Introduction 61 Materials and Method 63 Results 65 Discussion 92 3. The pathology of P. laevis in the alimentary tracts of stone loach and rainbow trout. 101 4 Introduction 102 Materials and Method 104 Section A : Uninfected stone loach 107 Results 108 Discussion 119 Section B : Infected stone loach 125 Results 126 Discussion 137 Section C : Infected rainbow trout 146 Results 147 Discussion 155 General discussion 161 4. The effect of P. laevis on the energy reserves and growth of stone loach and rainbow trout 164 Introduction 165 Section A : Stone loach 167 Materials and Method 168 Results 171 Discussion 200 Section B : Rainbow trout 211 Materials and Method 212 Results 217 Discussion 228 5 CONCLUSION 232 APPENDIX A 236 APPENDIX B 238 References 245 .. 6 GENERAL INTRODUCTION Pomphorhynchus laevis (Ntlller) is a member of the phylum Acanthocephala, of order Palaeacanthocephala and family Pomphorhynchidae (Meyer, 1933; Chubb, 1982). Adults occur in freshwater fish throughout England, Wales and Ireland (Kennedy, 1974). The adult worm is divided into two main regions, the body (metasoma) and the attachment organ (praesoma). The praesoma consists of a long neck, expanded anteriorly to form the bulb, and terminating in a hooked proboscis (Meyer, 1933; Chubb, 1967), and forming the organ for attachment to the gut wall of the host. Muscles involved in eversion and movement of the proboscis are contained within the praesoma, together with the cerebral ganglion (Jones, 1982). The metasomal wall is very thick and is probably used for absorption of nutrients (Crompton, 1970). Within the body cavity of the metasoma are the gonads'and associated organs (Figure 1A and 1B). P. laevis, like other Acanthocephala, is dioecious. Female worms have a variable number of ovarian balls, contained within a ligament sac. A sorting mechanism, the uterine bell, ensures that only mature eggs (shelled acanthors) are passed into the uterus (Whitfield, 1968, 1970) and thence,into the host's intestine. The male possesses two testes, sex cement glands, Saefftigen's pouch and a muscular copulatory bursa (Chubb, 1965) (Figure 1B). 7 Figure 1 A Genitalia contained within the metasoma of a female P. laevis. B Genitalia contained within the metasoma of a male P. laevis. C The life cycle of P. laevis. A ~---ligament sac---~ B testis t---~o,var,an ., ball cement_-+ gland Saefftigen's pouch --~~ ,~~ __uterine bell bursal~~r­ apparatus IH----uterus acanthor h. ~f~ DEFINITIVE ~~ HOST .. ~~ (e.g. Barbus barbus) ('~..r.... ....... ingested WATER /"INTE-RME-oiATE--- ---7 /',' HOST , ,,' (Gammarus p'ulex) ~,,/ t'y'stacanth rtY~~ .~~~ acanthella 8 ~fuen an acanthor is eaten by the intermediate host, Gammarus pulex, a larva hatches and penetrates the gut wall, entering the haemocoel. The larva develops into an acanthella, which grows within the haemocoel of G. pulex, forming a cystacanth (Rumpus, 1973) (Figure 1C). The cystacanth stage is capable of infecting almost.any species of fish that consumes the intermediate host (Kennedy et aI, 1978). Upon ingestion by a fish, the proboscis of the cysta­ canth is everted and attaches the worm to the gut wall of the intestine. The bulb develops once the proboscis has penetrated the wall and serves as a secondary attachment organ; normally the worm can only be removed by breaking the neck region of the praesoma. Although P. laevis can be found in many species of freshwater fish,. only a few of which are regarded as ! suitable hosts (Hine and Kennedy, 1974a, 1974b; Rumpus, 1975; Kennedy et aI, 1978). Using the criterion of the presence of gravid females of P. laevis, the preferred hosts in the river Avon, Hampshire, are the chub, Leuciscus cephalus, and the barbel, Barbus barbus, whereas in Ireland it is the brown trout, Salmo trutta. Some other salmonids have also been suggested as suitable hosts (Kane, 1966; Pippy, 1969; Hine and Kennedy, 1974b; Kennedy et aI, 1978). Considerable damage may be done to the gut mucosa by the presence of P. laevis in the fish, particularly in multiple infections (Pippy, 1969; Hine and Kennedy, 1974b) 9 and occlusion of the gut by the bodies of the acantho­ cephalans may occur (Pippy, 1969). The praesoma often penetrates the entire gut wall, the bulb being visible on the external surface of the gut. An inflammatory response normally forms around the praesoma and a nodule of con­ nective tissue may develop around the exposed proboscis and bulb (Marochino, 1926; Wurmbach, 1937; Pippy, 1969; Hine and Kennedy, 1974b). Emaciated chub containing several hundreds of P. laevis have been reported from the river Mosel, Germany (Wurmbach, 1937) and the river Avon, Hampshire (Chubb, 1965). However, no deleterious effects on the condition of infected fish have been demonstrated to be caused by P. laevis and its status as a.pathogen is unclear (Hine and Kennedy, 1974b). The aim of the present study was to examine the relationship between adult P. laevis and its fish hosts in terms of the local and whole body effects of infection on the host. To this end, host-parasite relations were studied in both natural and laboratory infections. The rainbow trout, Salmo gairdneri Richardson, was chosen as the laboratory host for P. laevis owing to its suitability as a host when naturally infected (Kennedy et aI, 1978). Additionally, rainbow trout may be readily ,obtained from commercial hatcheries in groups of similar age and size. The stone loach, Noemacheilus barbatulus L., was selected as the host for the study of natural infections 10 because of the ready availability of these fish and their ~igh incidence of infection in the river Severn, near Shrewsbury. The study begins with an examination of the histology and histochemical properties of the parasites' integument, since this is the region of the'parasite in direct contact with the host. Immunological techniques were used in an attempt to identify the potential antigenic sites of the acanthocephalan. The distribution of the parasites in the host's alimentary canal was studied to assess which regions "..,ere most sui table for the growth and development of the parasite. Changes in gut morphology and histology caused by P. laevis were described and an assessment was made of the efficacy of the host's inflammatory response in eliminating the infection. Finally, the effect of P. laevis on the growth and condition of its host were examined. =vidence obtained from the study is the subject of a discussion in which tne status of P. laevis as a pathogen in stone loach and rainbow trout is assessed • . 11 CHAPTER ONE THE INTEGUMENT OF Pomphorhynchus laevis, WITH PARTICULAR REFERENCE TO THE PRAESOMAL INTEGUMENT 12 INTRODUCTION The metasomal integument of acanthocephala is con­ cerned with nutrient absorption (Crompton, 1970). Histological and histochemical studies have been made on the integument structure of P.
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