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PARASITES of the MARINE Bivalveı University of Stirling

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PARASITES of the MARINE Bivalveı University of Stirling STUDIES ON SOME INTRACELLULAR PARASITES OF THE MARINE BIVALVEý TELLINA TENUM ( DA_ COSIA) Studies on a coccidian parasit6 oi the Jj-, ovary and a mycoplasma-like orSan. -,ir! with an associated virus in the diges-6- ive gland of the marine blva-l-ve, Tellina tenuis (da Costa) J. S. Buchanan B. Sc. (Wales) M. I. Biol. Unit Aquatic Pathob-1010f! of 2py University of Stirling November 1976 PUD-w"a mýUý,luý vt nýu-teý La Acknowledgemonts I gratefully acknowledge the supervision of this research project by Dr RJ Roberts of the Unit of Aquatic Pathobiology and the financial assistance provided by the Natural Environmental indebted Research Council. -I am to Mr IH Macrae and Mrs S Horne for assistance with the histological. preparation ofE specimens and collection of material in the field. I am further indebted to Mr T Forrest for technical assistance in the area of electron microscopy I thank especially Dr CR Madeley of the Regional Virus Laboratory, Glasgow, Dr M Whalley of the Animal Leukemia Research Unit and Dr E Follett of the Institute of Virologyý Glasgow University for their kind help and encouragement with -the virological aspects of this project. I qhould also like to thank Miss A Stirling of the Department of Agricult ture and Fishcries for SCOLJand, Mcirine. Resý:-, Civch Laboratory for pointing out the presence o.4 a parasite in the gonad of Tellina tenuis and Dr D Saward and Mr I Mackenzie also of DAFS, for giving so gencrously of their time in the collection of specimens from L. Ewe. I am f-urther indebted to Dr JG Duckett of the Scbool of Plant Biology, University Collego uf North Wales for reading 11--hemaauG-crJ_P/t_ and fur, hiu many hclpful suggestions and to Dr iG Moore, Mr JJP Clokie and Mr B Finlyson cf the Universities Marine Biological Station, M-511port, lor their encouragQire. nt and helpful advice. I furthcr aCknow_]_cdgc the helpf"I discussions axid cooperation provided by Dr BJ Hill and, Dr DJ Aldermann the 14Iii-Istry of .- of Agricultulc and 3 Fisheries, Fish Diseases Laboratory, Weymouthý a: id Dr F0 Perkins of the University of Maryland, U. S. A. I would also like to thank all other colleagues and friends from the University ol Stirling for their friendly cooperation and interest. My special thanks are due to Mrs A Rock for her expert typing of the manusc ript and finally5 grateful thanks to my wife and -three daughters for their sup-port, encouragement and inspiration. - -A B S-T--R. A CT STUDIES ON SOME INTRACELLULAR PARASITES OF THE MARINE BIVALVE TELLINA TENUIS (DA COSTA) This study is divided into four sections beginning with a consideration of the effects of anhitherto undescribed coccidian parasite of the ovary of this bivalve on the dynamics of a particular population from Kames Bay, Millport, Isle of Cumbrae, Scotland. The parasite was found to bring about complete or partial castration of female Tellina tenuis but had no effect on males. The general biology of Tellina-tenuis is reviewed and discussed in relation to observations that were carried out over one year on the age structure, growth, density, reproduction and degree of para, sitization of this bivalve. The population parameters were found to have changed little over the last fifty years. in There was not found to be any significant change the condition index that could be related to the destruction of the gonad by the parasite. This is the first description of a coccidian parasite of the ovaries of any marine mollusc. The second section describes the life cycle and developmental is stages of the coccidian parasite. The parasite believed in to be monoxenous with sporogony and anisogamY orcurring in the ovary of the host. Endogenous stages were observed the primary germ cells of the gonadal follicles. A diagnosis is presented based on the number of sprozoites per sporocys-t and sporocysts per oocyst. The name Mcrocys-tis tellinovum MerocyStis (sp. nov. ) is proposed for this coccidian. The gcnus belongs to the family Aggregatidac within the sub-order 5 Eimeriorina of the order Eucoccidiorida. An ultrastructural. study of both sexual and asexual stages is presented in support of this diagnosis. The third section of this study is an investigation of the observation that a large proportion of the Tellina tenuis examined histologically contained inclusion bodies within the secretory cells of the digestive gland. These inclusions were comprised of densc'masses of pleomorphic mycoplasma-like organisms. The first part of this section describes the morphology and ultrastructure of these organisms and the histopathological effects on the host digestive gland. A description of the normal digestive gland iss-given including observations of the cyclic changes in appearance that take place in response to the influence of tidal rhythms. This is believed to be the first descr. iption of a mycpplasma- like organism from a marine invertebrate. The fourth section is concerned with a series of experiments to determine the nature of a virus seen in association with the mycoplasma-like organism. The virus was isolated from the host'cells by density gradient centrifugation and its morphology was compared with a second virus isolated by Hill (1975) through the medium of a fish cell culture. It was found that these tt: o viruses were qjjj. te distinct from each other. Attempts were made to propagate both viruses in an established cell line from -the Atlantic salmon and the results are described and discussed. 6 TABLE . OF CONTENTS. page TITLE SHEET 1 ACKNOWLEDGMENTS 2&3 ABSTRACT 4&5 TABLE OF CONTENTS 6- 11 GENERAL INTRODUCTION 12 SECTION ONE: Observations on the distribution, growth and reproduction of a population of Tellina tenuis, at Kames Bay, Millport5 with particular reference to the effects of a coccidian parasite of the ovaries. 1.1 Introduction 13 1.2 Review of the Literature 13 - 21 a) Classification and distribution of the species b) Structure and adaptations 14 i) feeding anatomy external features iv) behaviour c) The Te"Llina community concept 16 d) The population ecology of Tellina and relatcd species 18 e) Parasitic castration in molluscs 20 1.3 Material's and Methods 22 - 25 a) Description of the habitat 22 b) Method of sampling 23 C) Sub-saippling 23 d) Processing of samples 211 0) Method of determining. condition 25 f) Method of determining age structure 25 g) Method of assessing growth rate 25 1.4 Observations an! Results 25 - 45 a) Age and growt-h rate estimates at different levels on t; ie beach 25 b) Parasitic/... 26 7 b) Parasitic castration 28 c) Reproduction 29 i) anatomy ii) maturation of the gametes iii) ratio of the sexes iv) spawning 44 d) Density of the population by e) The seasonal pattern of parasitization the coccidian 114 1.5 Discussion 45 - 511 145 a) Age structure and growth rate b) Reproduction and spawning 47 49 C) Density of the population 49 d) Parasitic castration ' e) Factors affecting failure oj settlement of spat 52 54 56 1.6 Summary and Conclusions - I 8 SECTION TWO: Studies on a coccidian parasite of the ovary of Tellina tenuis for which the name Merocystis tel. linovum (species nova) is proposed. page 2.1 IntrDduction 57 2.2 Revi, 2w of the Literature 58 2.3 Materials and Methods 61 2.4 Observations 63 80 a) The life cycle 63 b) Exogenous stages 65 C) Endogenous stages 65 d) Diagnosis 66 e) Distinctive features 67 i) relative size ii), variability of the oocyst wall iii) shape and shape index iv) colour V) cross infection experiments and host susceptibility f) Transmission and scanning electron microscopy of the sporozoite and the merozoite (infectiv e stages) 70 the pellicle the polar ring iii) the micro-tubules iv) the conoid V) rhoptries vi) micronemes vii) micropores Viii) crystalloid inclusions g) Transmission electron microscopy of the sexua l 76 stages D the microgamont and microgametogenesis ii) the macrogamont .- 2.5 Discussion and Conclusions 80 82 9 SECTION THREE: Light and electron microscopical observations of a mycoplasma-like organism infecting the secretory cells of the digestive gland of Tellina tenuis. pages 3.1 Introduction 84 3.2 Review of the Literature ' 84 - 70 a) The lamellibranchiate digestive gland 84 b) Cyclic changes in -the digestive gland 85 0' The morphology and ultrastructure of the Mycoplasmatales 86 3.3 Materials and Methods 90 a) Sampling sites b) Preparation of specimens for light inicroscopy c) Preparation of specimens for transmission electron microscopy 3.4 Observations and Results 90 a) The normal digestive gland in Tellina tenuis 90 cyclic changes secretory cells iii) absorptive cells b) Host-parasite interactions 93 i) light microscopy of the cytopatbic effect of the MLO ii) electron microscopy of infected cells C) The morphology and ultrastructural features of 914 the MLO i) the cell boundary ii) the capsular matrix iii) the cell contents iv) morphology V) replication 3.5 Discussion and Conclusions 97 a) Cycýical changes in the diges tive gland 97 b) Regeneratiori of the secretory cells 98 C) Artefacts and mycoplasma cell morpbologY 99 - and the effocts of MVT on the morpholcý, jy of-cells 99 d) The cell wall 100 e) The capsular matrix 100 f) The range of habitats 101 intracellular 102 104 g) an d h) Other parasites, - 10 SECTION FOUR: Studies on two viruses isolated from Tellina tenuis. page 4.1 in troduction 105 4.2 Re view of the literature 106 111 a) ' The Mycoplasmatales. viruses 106 b) Phage and L-forms of bacterýia, Rickettsiae and Chlamydiae 108 c) The viruses of marine invertebrates 109 ý. 3 Ma terials and methods a) Preparation of samples b) Preparation ' ol gradie -nts C) Centrifugation of gradients 112 d) Unloading the gradients 112 e) Preparation of grids for electron microscopy 113 .
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