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Studies on the Biology Of. Pladiorchis Elegans (Rudolphi, 1802), (Trematoda: Digenea) in Its Mammalian and Molluscan-Hosts

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Studies on the Biology Of. Pladiorchis Elegans (Rudolphi, 1802), (Trematoda: Digenea) in Its Mammalian and Molluscan-Hosts Studies on the biology of. Pladiorchis elegans (Rudolphi, 1802), (Trematoda: Digenea) in its mammalian and molluscan-hosts. Andrea M. Groan B. A. (Northeastern Boston Ma. ) Univ. f U. S. A. Submitted in. fulfillment of the requirements for the degree of Doctor of Philosophy. The University of Leeds Department of Pure and Applied Zoology January 1980. BEST COPY AVAILABLE Variable print quality To my Mother and-Father. ii ABSTRACT' The taxonomy of the genus Plaaiorchis Ltihe, 1899 is reviewed with particular reference to the species P. 'eleaans (Rud. 1802) and a list of Plagiorchia species previously recorded in'Britain is given. The life cycle was initially established using L se staEnalie, Chironomus sp. larvae and LACA mice; morphology, intraspecific vari- ation and host specificity-at all levels of the life cycle have been examined and described. Besides L. starnalis, L. paluatris is susceptible to infection with P. elepans while L. enrepra is refractory. Infections cause ex- tensive damage to the digestive gland of L., stapnalis although they do not curtail its life span. Immature and mature specimens of L. stnenalis were infected; the former vere. castrated and the latter con- tinued to reproduce. A. single mother sporocyst of P. ele s pro- duces approximately 650 daughter aporocyats from which develop several hundred thousand xiphidiocercariae. Upon release cercariae are negatively phototropic and negatively geotropic, with-light-and temperature affecting the rate of cercarial emmission. Cercariae encyst-in aquatic arthropods (Chironomus op., Asellus anuaticus and Gamnarus pulex) and precociously in the snail host. Adult P. elegans range in size from 1.04 to 3.89mm by 0.34 to 0.96mm. Both mammals (mice, rats, gerbils and hamsters) and birds (chicks, ducklings and pigeons) are susceptible to infection. Egg counts were performed to follow the course of the infection in mice and rats. Primary infections of LACA.mice are of short duration as a result of a host immune response. By means of surgical transplantation, the life span of P. elerens was increased from the expected 21 days to 63 days. Specimens recovered when the life cycle was completed using various combinations of intermediate and final hosts and those recovered from first and second challenge infections of LACA mice are compared statistically using canonical variate analysis. The only reliable anatomical criteria. for distinguishing species of Placiorchis are: 1. the relative sizes of the suckers and pharynx. 2. the presence or absence of a seminal receptacle, vas deferens and common genital atrium. 3. to a. limited extent egg size and host specificity. According to these criteria many previously described species are con- sidered to be synonymous with P. ele ans and its geographical range is iii extensive. ý: ý, iv ACKNOWLIDGFSMTS I would like. to thank Professor R. McNeil Alexander. and Professor Donald L. Lee for the use of the laboratory facilities while at the Department of Zoology. My thanks also to my supervisor, Dr. R. Wynne Owen, for his help and advice, particularly in the-preparation of this manuscript and for encouraging me to travel to Leeds and study a beast called Pladiorchis. I would like to extend my gratitude to Mr. S. Prudhoe of the British Museum for his help in deciphering the species of beast. For his able assistance with the statistical analy- sis technique I sincerely thank Dr. "Eeith Sadler. I should like to thank Dr. Arthur Chadwick for demonstrating the surgical transplanta- tion technique and Mr. Arthur Holliday for his assistance with the photography. For their help in caring and maintaining the laboratory animals I thank Mr. Stewart Pickeragill, M. Pauline Longthorne and Mr. John Oldroyd. And I offer a. very special thanks to my husband, Stuart Gelder, for his advice, encouragement and patience. Finally I an grateful to all who made my stay in England a very pleasant one. V CONTENTS i Title page .... .... .... .... to .... ...... .. .. .. ABSTRACT ii .... .. to .... .... .... .... .... .. .. .. ACKNOWLEDGEMENTS ii .... .... .... .... .... to .... .. .0 CONTENTS .... .... .... .... .... .... .... .. .. .. v INTRODUCTION 1 .... .... .... .... .... .... .... .. .. SECTION1. A review of the taxonomy of the genus Pla¢iorchis 3 Lühe, 1899. SECTION2. Establishment of the life cycle and morphology of 15 the larval stages. Introduction .... .... .... .... .... .. :::: : 16 Materials and Methods .... .... .... 40 .. Results 17 .... .... .... .... .... .... .... .. .. Establishment of the life cycle . .... .... .. .. .. 17 Morphology of the larval stages . .... .... .. .. .. 17 Egg 17 and micacidium .... .... .... .. of .. .. of 18 Mother and daughter sporocysta .... .... .. .. .. 19 Cercaria . .... ...... .... .... .. - .... .. .. Metacercaria 21 .... .... .... .... .... .. .. .. Discussion 22 .. .! .... 1 .... .... .. ".. .... .... .. Figures 27 .. *; * .... .... .... ........ ". .. .. SECTION3. The fintermediates: host .... .... .. .. .. 34 35 Introduction, .... ...... .... .... of .... .. .. .. Materials and Methods ...... .. is .... .... .. .. .. 35 Results 36 .... " .... .... .... .... .... .... .. .. specificity Host . .... .... .... .... .... .. .. 36 Exposure of Lymnaea ota¢alis to unknown number of .. 36 P. ele s eggs 10 P. Exposure of L. t is to 1p or 50 elePane .. 38 eggs Exposure of L. Perezra and L. palustris .... .. .. 39 Percentage hatch of P. eleQans eggs . .... .. .. .. 41 Length of life of embryonated eggs ........ .. .. 41 Fecundity of P. eleians mother aporocyst .... .. .. .. 42 Effects of parasitism upon the snail .... .... .. .. 42 L. 1s... Growth and survival of infected 9t .. .. 42 Pathology P. in L. is 44 of infections of ele ans sta . Effects 45 on reproduction in the snail host=. .... .. .. vi Infection immature of L. atsPnalls .. .. .... .... 45 Infection of mature L. stacnalis . of .. .... .. of 46 Discussion 47 .. is .. Of .... .... .. .. of .... .... Figures 56 .... of .. of .... .... .. .. .. .... .... ! Cercaria. letacercaria.. 65 SECTION 4. and .... .. .. .... .... Introduction 66 .... .... .... .... .. .. .. .... .... 66 Materials and Methods ...... .... .. of .. .. of of .. Results ..:. 67 .. 09.410 .... .... .... .... .. .. .... infe 67 Cercarial release= monomiracidial ctions . .... .. 69 Factors influencing cercarial release .. .. .... .... Temperature .... .... .... .. -.. .. .. .... .... 69 ]Photoperiodicity . .... .... .... is to .... .... 69 Cercarial behaviour and longevity ... .. .. .... .... 70 Metacercaria 71 ... ........ .... .. .. .. .... .... 72 Host specificity . .... .... ...: .. .. .... .... Amphibians 73 . .... .... .... .. .. .. .... .... Molluscs 73 .... .... .... .... .. .. .... .... .. Encyatment without host penetration .. .... .... 7l+ Attempts to induce .... 74 encyatment .... .. .. .... Discussion 75 .... .... .... .... .... .. .. .... .... Figuren 80 . .... .... .... .... .... .. .. .... .... 5. 84 SECTION Adult stage . q*.. .... .... .. .. .... .... Introduction .. 85 .... .. of .... .:.. .. .. .. of .... 86 Materials and Methode .... .... .... .. .. .... .... Results 88 .... .... .... .. ".. .... .. .. .. of .... Si 88 Anatomy of adult P. Ale . ...... .. .. .... .... 89 Morphological and anatomical variation due to age . .. LACA 89 mice .. .... .. ".. .... is is .. .. .... .... Laboratory 92- rate . .... .... .... .. .. .... .... 92 Effects of various hosts on morphology .. .... .... Definitive hosts 92 .... .... .... .. .. of .. " .... Second hoots 94 intermediate .... .. .. .. .. -.. .... First intermediate hosts . 94 .... .. .. .. .. of .. - Anatomical variation of P. eler-ans'. .. .. .... .... 95 Oral and ventral suckers .... .. .. .. .... .... 95 " Caeca ....... ............ .. .. .... .... 95 Gonads .... 96 .... .... .... .... .. .. .. .... Uterus .... ........:... .. .. .. ........ 96 Cirrus sac ... .... .... .... .. ...... 97 vii Vitellaria . .... .... .... .... .... .... .. 97 Final host specificity 98 .... of .., .... .... .... .. 98 Amphibians .... .... .... .. .".. .... .... .. " Birds II 99 . .... .. .... .... .... .... .... .... Mammals 99 .... .... .... .... .... .... .... .. Intestinal 101 length . .... .... .... .... ...... .. Egg 101 counts .... .... of .... .... .... .... .... 106 Discussion .... .... ..... .... .... .... .... .. Figures 115 . .... .... .... .... .... .... .... .... SECTION 6. Immunity 3.32 . .... .... .. to .... .... .... .. Introduction 133 . .... .... .... .... .... .... .... .. Materials and Methods go, of eel.... 134 Results 135 .... .... .... .... .... .... .... .... .. Duration of the primary infection ......... ...... 135 Egg-counts 135 .... .... .... .... .... .... .... .. Challenge infections 142 . .... .... .... .... .... .. High initial dose; low challenge dose ..... .... .. 1/+2 Low initial dose; low challenge dose ........ .... 143 Second challenge infections ....... .... .... .. 143 143 Age resistance . .... .".. .... .. is is .... .".. 147 Distribution . ...... .... .... .... .... .... .. 147 Primary infections ... .... .... .... .... .... 148 Challenge infections .... .... .... .... .... .. Discussion 149 .... .... .... Si .... .... .... .... .. Figures 152 .... .... .... .... .... .... .... .... .. 159 SECTION 7. Transplantation . .... .... is .... .... of .. Introduction 160 . .... .... .. is is .... .... .... .. Materials Methods 161 and . .... of .... .... .... .... .. 162 Results .... .... .... .... .... Si .... .... .... 162 Series I Preliminary experiment . .... .... .... .. 162 Series II Successive transplants
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