Advances in Parasitology Volume 20

Advances in

PARASITOLOGY

VOLUME 20

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Advances in

PARASITOLOGY Edited by

W. H. R. LUMSDEN (Senior Editor) University of Dundee, Department of Animal Services, Ninewells Hospital and Medical School, Dundee, Scotland

R. MULLER Commonwealth Institute of Parasitology, St. Albans, England

and

J. R. BAKER NERC Culture Centre of Algae andProtozoa, Institute of Terrestrial Ecology, Cambridge, England

VOLUME 20

1982

ACADEMIC PRESS A Subsidiary of Harcourt Brace Jovanovich, Publishers

London New York San Francisco Toronto Paris ,950 Paulo San Diego Sydney Tokyo

ACADEMIC PRESS INC. (LONDON) LTD 24/28 Oval Road, London NW17DX United States Edition published by ACADEMIC PRESS INC. 111 Fifth Avenue, New York, New York 10003

Copyright 0 1982 by ACADEMIC PRESS INC. (LONDON) LTD.

All Rights Reserved No part of this book may be reproduced in any form by photostat, microfilm, or any other means, without written permission from the publishers

British Library Cataloguing in Publication Data

Advances in uarasitology. -. VOl. 20 1. Veterinary parasitology-Periodicals 591.2’3 SF810.A3 ISBN 0-12-031720 LCCCN 62-22124

Typeset by Bath Typesetting Ltd., Bath and printed in Great Britain by John Wright & Sons (Printing) Ltd., at The Stonebridge Press, Bristol

CONTRIBUTORS TO VOLUME 20 JAMES C . CHUBB,Department of Zoology, University of Liverpool, Liverpool L69 3BX, England (p. 1) J. J. LAARMAN,Department of Parasitology, University of Amsterdam, Amsterdam, Netherlands (p. 293) WEDAD TADROS, Department of Parasitology, Institute of Tropical Hygiene, Amsterdam, Netherlands (p. 293)

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PUBLISHER’S ANNOUNCEMENT It is as much with regret as with gratitude that we announce the resignation from the senior editorship of this series of Professor Russell Lumsden. He promptly and readily took over the role on the sudden death of Professor Ben Dawes. He swiftly brought order to the confusion of completed, half completed and projected contributions inevitably left by the sudden departure of even so thorough an editor as Professor Dawes. He kept faith with early commitments, he recruited outstanding contributors to the series himself, he maintained its momentum, and he brought in to assist him the considerable talents of Drs Baker and Muller. We, his publishers, have found him always a delight to work with, constructive, helpful and responsive to our requirements. The series is indebted to him and we shall certainly miss him.

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PREFACE From its inception in 1963 by Professor Ben Dawes, Professor of Zoology in King’s College, University of London, the series Advances in Parasitology demonstrated its essential liveliness and relevance by faithfully appearing volume by volume in step with the progression of the years. When Professor Dawes died in 1976 he was actively preparing Volume 15. I was honoured at that time to be approached by Academic Press to take over the Editorship of this famous series so as to keep it in being. In accepting this responsibility I was fortunate to be able to enlist the support of the two very experienced scientists and editors, Drs J. R. Baker and R. L. Muller, to oversee, respectively, protozoology and helminthology, which composed most of the content of the series up to that time. These two medically and economically important subjects will necessarily continue to supply the main content of Advances in Parasitology, but we as an editorial team, although we are all “medical” parasitologists, have tried to regard the parasitic way of life as the unifying principle and so to enlarge the coverage and stimulation of the series by sokiting reviews on parasitic organisms other than protozoa and helminths, and on principles and processes fundamental to parasitism. The fruits of this policy have already begun to ripen and, leavening the purely protozoological and helminthological reviews, there are reviews of immunity to ticks (Willadsen) and of the role of tick salivary glands in feeding and disease transmission (Binnington and Kemp) in Volume 18 and on parasitic copepods (Kabata) in Volume 19. Other such reviews are in the pipeline. The present time, then, when Advances in Parasitology has survived the loss of its original founder and set itself on a propitious course for the future, seems an appropriate one for myself to relinquish the role of Senior Editor and leave Advances in Parasitology in the capable hands of Drs Baker and Muller, whose loyalty, enthusiasm, enterprise-and hard conscientious work -have been indispensable supports to me in ensuring the continuation of the series. W. H. R. LUMSDEN January 1982

Editors’ Note This volume departs slightly from the traditional annual publication mentioned by Professor Lumsden, but we felt that these two lengthy and important papers deserved publication as soon as possible; a precedent we propose to follow in future when necessary. R. M. and J. R. B.

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CONTENTS Contributors to Volume 20 Publisher’s Announcement Preface

............................................................... ...............................................................

v vii

.......................................................................................

ix

Seasonal Occurrence of Helrninths in Freshwater Fishes Part IV Adult Cestoda. Nematoda and Acanthocephala

.

JAMES C

. CHUBB

I . Introduction ........................................................................... 11 Classification ........................................................................... I11. Seasonal Studies ..................................................................... A. Class Cotyloda .................................................................. B . Class Eucestoda .................................................................. C . Class Nematoda. Subclass Adenophorea ................................. D . Class Nematoda. Subclass Secernentea .................................... E. Phylum Acanthocephala ...................................................... IV . Seasonal Studies in World Climatic Zones .................................... A . Tropical ... .................................................................. B . Subtropical ........................................................................ C . Mid-latitude ..................................................................... D. Polar ........... ............................................................... I?. Mountain ........................................................................ F. Species Studied in more than one Climate Zone ........................ V. General Conclusions .................................................................. A . Incidence and Intensity of Occurrence .................................... B . Principal and Auxiliary Hosts ................................................ C. Invasion of Fishes by Larvae ................................................ D . Growth and Maturation of the Helminths .............................. E. Abiotic Factors .................................................................. F. Biotic Factors .................................................................. G . Long-term Population Studies ............................................. H . An Hypothesis for Seasonal Occurrence ................................. I. Experimental Studies ......................................................... Acknowledgements .................................................................. References ..............................................................................

.

xi

1 3 3 3 70 102 105 158 199 199 202 204 221 221 223 231 231 233 234 241 249 252 253 254

255 256 259

xii

CONTENTS

Current Concepts on The Biology. Evolution and Taxonomy of Tissue Cyst-forming Eimeriid Coccidia

.

WEDAD TADROS

and

J

. J . LAARMAN

I . General Introduction ............................................................... I1. Toxoplasmosis and Toxoplasmid Coccidiosis ................................. A Introduction ..................................................................... B . The Source of Enteric Development of the Parasite in the Feline Host .............................................................................. C . The Developmental Cycle of Zsospora gondii in the Intestine of the Feline Final Host ............................................................... D . Sexual Differentiation ......................................................... E . Genetic Research ............................................................... F. Immunity of the Feline Final Host Against the Entero-Epithelial Cycle of Development of Z. gondii .......................................... G . Pathology of Toxoplasmid Coccidiosis in the Felid Host ........... H . The Survival, Sporulation and Dispersal of Oocysts .................. I. The Structure and Excystation of the Oocyst ........................... J . Host Cell Penetration ......................................................... K . Strain Virulence and Host Susceptibility ................................. L. Recent Studies on Toxoplasmosis in Farm Animals .................. M . Serological Diagnosis ......................................................... N . Immunity in the Intermediate Host ....................................... 0. Pathology of Human Toxoplasmosis ....................................... P. The Role of Cats in the Dissemination of Human Toxoplasmosis . I11. Zsospora datusi (Syn. Hammondia hammondi) ................................. IV . Besnoitiosis and Besnoitian Isosporiasis ....................................... A . General Aspects ........... ................................. B. Serology ........................................................................... C . Immunity . ..... ................................. D. Pathology ........................................................................ E . Transmission, Life Cycle and Epizootiology ........................... V. Other Isosporan Parasites with Extra-Intestinal Tissue Stages ............ VI. Sarcosporidiosis and Sarcocystis-induced Coccidiosis ........................ A . General Aspects ............................................................... B. Recent Knowledge on the Developmental Cycles of Sarcocystis ....................................... species.................................. C. Muscular Sarcosporidiosis in Pri es and Carnivores ............... D . Pathology of Sarcosporidiosis in the Intermediate Host ............ E . Pathology of Sarcocystis-induced Coccidiosis in the Final Host ... F. Serodiagnosis ..................................................................... References .............................................................................. Index ........................ .............................................

.

294 296 296 297 301 303 305 305 309 310 310 311 312 314 318 321 327 329 332 335 335 337 337 340 342 345 352 352 358 383 386 389 389 412 469

Seasonal Occurrence of Helminths in Freshwater Fishes Part IV. Adult Cestoda, Nematoda and Acanthocephala JAMES C. CHUBB

Department of Zoology, University of Liverpool, Liverpool L69 3BX, England 1 3 3 3 70 B. Class Eucestoda ... C. Class Nematoda, Subclass Adenophorea ...... ........... .... .. .... .. ..... .. . .. . ., 102 D. Class Nematoda, Subclass Secernentea ................ ... .. ... .. .... 105 E, Phylum Acanthocephala .. ........ ........... ..... ................ . .. ....... ..... . .. . . , 158 IV. Seasonal Studies in World Climatic Zones ..... ....... . .............. .. ....... ... .. . . . . 199 199 A. Tropical ...... 202 B. Subtropical ... 204 C. Mid-latitude 221 22 1 223 23 I 23 1 233 234 24 1 249 252 253 254 ............. 255 256 251

I. Introduction

............. .. ................. ..., 11. Classification .... ............. 111. Seasonal Studies.. ..................... ................................... .. ..........., ........, A. Class Cotyloda ...

I. INTRODUCTION

This fourth part of the review completes the series. The life cycles of virtually all the adult cestodes, nematodes and acanthocephalans are complex and require one or two intermediate hosts, of which the second in some instances is a fish (see Part 111 of review, Chubb, 1980), followed by the final development to sexual maturity and egg or larval release in the definitive fish host. Where relevant the information about the life cycle of each species is briefly summarized in Section 111. 1

2

JAMES C . CHUBB

None of the species described in this part of the review are potential health hazards to man, but many are actual or potential pathogens of fishes in both pond and artificial fish culture situations (see for instance Bauer et aZ., 1969, 1977; Needham and Wootten, 1978). With the increasing commercial interest in artificial rearing of freshwater fishes as food in, for example, Britain, there has been an increased need for the veterinary practitioner to be aware of the diseases and parasites of fishes, as made manifest by recent publications including Roberts and Shepherd (1974), Roberts (1975), Shepherd and Poupard (1975) and Shepherd (1978). What is rarely stressed, however, is the fact that almost all of the helminth parasites in these fishes undergo quite dramatic seasonal changes in presence, abundance and morphology during maturation, and in some species of nematodes, of migration through the tissues of their hosts. Treatment and elimination of many of these helminths in fish farming conditions will be most effective if related to a sound knowledge of the seasonal biology of the species involved. It is hoped, therefore, that the details provided in Section I11 of this and the other parts of the review (Chubb, 1977, 1979, 1980), will provide a preliminary guide to the literature for the veterinarian concerned with fish husbandry and management. The terms utilized follow the style of the first three parts of the review (Chubb, 1977, 1979, 1980). Incidence is used to indicate the percentage infection of the fish hosts and intensity of infection to show the numbers of parasites found in each host. Maturation stages are described where appropriate, and in Section VD (Table VII) it is again urged that a universal series of descriptive stages be adopted in order to synthesize observations made during both experimental studies and field investigations. The term invasion is used to describe the actual process of acquisition of the parasites by the host. Section I1 of the review notes the schemes of classification adopted. Section 111reports the seasonal studies of the cestode, nematode and acanthocephalan adults under species. Where a larval stage of a cestode or nematode species has already been discussed in Part 111of the review (Chubb, 1980), the relevant page numbers are given. In Section IV the seasonal information is related to the major climatic zones of the world. The general conclusions in Section V attempt to gather the data into meaningful headings, and thereby to facilitate our understanding. Where appropriate suggestions are made for further study which could assist in our appreciation of the complexities of the seasonal dynamics involved in the life cycles of the helminth species considered here. As in the previous parts an attempt has been made to abstract and review as much of the relevant literature as possible. The amount of information found was far larger than originally anticipated. It is hoped that an acceptably wide coverage has been achieved, and that too many generalities have not been lost owing to not seeing the wood for the trees.

HELMINTHS I N F R E S H W A T E R FISHES

3

11. CLASSIFICATION

Seasonal occurrence is reported in the sequence cestodes, nematodes and acanthocephalans. For the cestodes the classification of Wardle el al. (1974) is used. The arrangement of the nematodes follows that to be found in the series of keys to the nematode parasites of vertebrates which commenced publication in 1974 (see Anderson et al., 1974) and are still in progress. The classification of the Acanthocephala retains the orders of Van Cleave (1936), elevated to class status by Golvan (1958, through to 1962), but later returned to ordinal level by Golvan (1969). The arrangement of the families in the Order Eoacanthocephala follows Golvan (1959), but that for the Order Palaeacanthocephala uses the sequence to be found in Golvan (1969). The species and their seasonal biology are presented in alphabetical order under families. 111. SEASONAL STUDIES A.

CLASS COTYLODA

1. Order Amphilinidea (a) Family Amphilinidae Amphilina foliacea (Rudolphi, 1819) Dubinina (1974, 1976, 1978) has recently proposed that the Amphilinidea should be raised to the status of a class owing to the distinct morphological characters of this group, however here it is retained as an order. Dubinina (1974) has made a detailed study of the biology of A . foliacea in the Lower Volga Basin, U.S.S.R.The occurrence and length of the development appeared to depend on the species of Acipenser serving as host, although this was not evident in experimental infections. The intermediate hosts, seven species of gammarids, were infected by eating embryonated eggs. Janicki (1928) found mature parasites with eggs during the summer, and Salensky (1874) reported them during the winter. Kakacheva-Avramova (1977) noted a 16.7 % incidence in Acipenser ruthenus in the River Danube, Bulgaria in spring and summer. 2. Order Caryophyllidea

The arrangement of the families foilows Mackiewicz (1972). The larval stage in the oligochaete host was termed a caudate procercoid and the adult worms in the fish host progenetic procercoids by Mackiewicz (1972), but the terminology proposed by Freeman (1973) was, respectively, a caudate postplerocercoid and an acaudate adult. McCrae (1961) considered the caryophyllaeid life cycle to be of a fourth type distinct from the cyclophyllidean, pseudophyllidean (including Diphyllidea in this review) and proteocephalid types. The seasonal occurrence of the caryophyllaeids as a group was summarized by Mackiewicz (1972). Most of the studies he reviewed indicated that the

4

JAMES C . C H U B B

period of highest incidence was in late winter, or more commonly, early spring, and that the highest frequency of gravid stages was also in the spring when water temperatures rose and fishes were spawning. Mackiewicz (1972) noted exceptions to this generalization, Spartoides wardi and Hunterella nodulosa, where no seasonal fluctuations of mature worms had been seen (details provided later under species headings). Interspecific interactions between caryophyllaeids were also considered important in the dynamics of incidence and maturation cycles. Mackiewicz (1972) suggested that because multiple infections with caryophyllaeids were common, more information on niche width for each species, as well as on intraspecific and interspecific interactions in the fish hosts was needed. The incidences were seen as the result of the interactions of such complex factors as availability and kind of infected intermediate hosts, variations in host feeding habits, environmental changes, e.g. temperature, physiological variations in host resistance, host sex and the interspecific interactions of the parasites themselves. Mackiewicz (1972) suggested that while the caryophyllaeid population dynamics within the vertebrate body appeared to be governed by host reactions (immunity) stimulated by temperature, the general incidence picture seemed to be more a function of fish feeding habits, again influenced by temperature, rather than any other factor. Grimes and Miller (1976) found three different caryophyllaeid distributions in the one habitat: Penauchigetes sp. without a seasonal cycle; Biacetabulum meridianurn present all year, but with seasonal changes in incidence and maturation, and with intensity inhibited by the simultaneous presence of Monobothrium ulmeri; and M . ulmeri which was present during an eight month period, with seasonal incidence, mean intensity and maturation. However, Grimes and Miller (1976) stressed the fact that the distribution patterns they found at Lake Raleigh, North Carolina, U.S.A., should not be considered characteristic of the respective caryophyllaeid species, as each in another locality, or host species, or both might exhibit very different seasonal distributions. In the light of the above general comments, the variations of seasonal patterns at an intraspecific level will be more easily appreciated in each instance even if exact explanations cannot be given. (a) Family Caryophyllaeidae Archigetes species The taxonomic history of the genus Archigetes is fairly complicated and cannot be reviewed here. In this account the view of Calentine (1965a) is accepted where the genera Archigetes and Biacetabulum were distinguished on the basis of differences of definitive hosts, intermediate hosts, larval deveIopment and adult morphology. Archigetes brachyurus Mrhzek, 1908 This species has been placed in the subgenus Paraglaridacris of Glaridacris Cooper by Janiszewska (1964), however it is retained in the genus Archigetes here. Kennedy (1965b) provided a list of synonyms. Kulakovskaya (1962a, b) stated that the oligochaete intermediate hosts for A . brachywus (as Glaridacris

H E L M I N T H S I N F R E S H W A T E R FISHES

5

brachyurus) were Limnodriltis claparedeanus and L . hofmeisteri. Adult worms in fishes were considered to be very rare (Kulakovskaya, 1962a). Kupchinskaya (1972), using the name G . brachyurus, reported from the L'vov region, Ukraine,U.S.S.R. that in mature L. hofmeisteri only mature or close to mature A. brachyurus were found, whilst young larvae occurred in young hosts. Experiments showed that 53 % of 4 to 6 week old L. hoffmeisteri could be infected by eggs of A . brachytirus, but only 7 to 12% at 12 to 18 months of age. The seasonal dynamics of A . brachyurus are, therefore, closely tied to those of its oligochaete hosts. Marits and Vladimirov (1969), at the Dubossary Water Reservoir, Moldavia, U.S.S.R., found a 2.2% incidence of A. brachyurus (as G . brachyurus) in Vimba vimba vimba natio carinata in spring, but no worms were found summer or autumn. Archigetes limnodrili (Yamaguti, 1934) This species was described as Glaridacris limnodrili by Yamaguti (1934), and according to Kennedy (1965b), who proposed the combination Archigetes limnodrili, it includes Brachyurus gobii Szidat, 1938 and Glaridacris gobii a combination proposed by Yamaguti (1959). Kennedy (1965a) experimentally demonstrated that the life cycle could be completed in the oligochaete hosts, Limnodrilus species. The eggs embryonated in about 20 days at 14°C. Kennedy (1965a) recognized five stages of maturity in the oligochaetes: Stage I cercomer not formed ; Stage 11, cercomer formed, genital rudiments forming; Stage 111, bothria present, with full complement of reproductive organs ; Stage IV, adult, commencement of egg production; and Stage V, adult, eggs occupying greater part of the body. At 14°C the growth of the parasite occurred fairly steadily, Stage I was reached in about 30 days, Stage I1 in 40 days, Stage 111 in 75 days and Stage V in about 140 days post-infection. In natural conditions, at the Shropshire Union Canal, Backford, Cheshire and the River Thames, England, Kennedy (1965a) found no pattern of seasonal incidence in the oligochaetes. With respect to seasonal maturation, Stages I and I1 occurred in most months of the year, and the adults, Stages IV and V, in the canal from March to September and in the River Thames in July. In an experimental population of oligochaetes Stages I and I1 also occurred all months, and adults January to October. Young oligochaetes were readily infected and adult A . limnodrili were found in adult Limnodrilus species. Examination of fishes from the Shropshire Union Canal, March to August, failed to reveal any adult worms in their intestines. However, in other localities adults have been found, on occasion, in fishes: in Japan in July and December in Misgurnus fossilis and Pseudogobius esocinus (Yamaguti, 1934) and in Germany in May in Gobio jhviatilis (Szidat, 1938). It seems likely that the period of survival of A . limnodrili in fishes is brief, owing to the rarity of fish records, and the fact that the Limnodrilus species are the usual hosts, allowing completion of the life cycle without the necessity for a fish phase. Archigetes iowensis Calentine, 1962 The account by Calentine and Ulmer (1961a) of an unnamed caryophyllaeid cestode from near Iowa Falls, Iowa, U S A . , refers to A . iowensis

6

JAMES C . C H U B B

which was described by Calentine (1962). Naturally infected Limnodrilus hoffmeisteri were found in every monthly collection from the Iowa River; however, natural infections of Cyprinus carpio were limited to May, the spawning period of the fish (Calentine, 1962). Further information was provided by Calentine (1964). In C . carpio collected from March through to November, A . iowensis were recovered April to June only. Incidence was highest in June (77-82 %), but intensity peaked in May. Gravid worms first appeared in late April, reached a maximum in late May, and by early July A. iowensis had gone from the fishes. No immature Archigetes iowensis were ever found in Cyprinus carpio. The eggs embryonated in 14 days and remained viable for 80 days at room temperatures. In natural populations of the oligochaete host Limnodrilus hofmeisteri, around a 2.1 % incidence was found, peaking at 5.4% in October. Calentine (1964) found that L. hofmeisteri infected with one or two procercoids could live for up to two years, but if more than four parasites were present the host usually died by 100 days. Calentine (1964) attempted to experimentally infect Cyprinus carpio with Archigetes iowensis, but achieved positive results only in May, at the same time as the natural fish infections occurred. Laboratory reared procercoids 119 days old fed to C . carpio in August gave negative results. Sexually mature Cyprinus carpio had a greater incidence and intensity of occurrence of Archigetes iowensis than did immature fishes, but there was no difference in infection between male and female fishes (Calentine, 1964). The seasonal incidence of the Archigetes iowensis was explained by Calentine (1964) in the following way. Cyprinus carpio in the Iowa River first acquired invasions in early spring when they commenced feeding. At ice break, on 23 March 1963, Calentine found that the C. carpio had no food nor A . iowensis in their intestines, but about two weeks later, in both 1962 and 1963, nearly 50% of these fishes were infected, and most also had intestines full of food. The termination of the period of infection, late June, was ascribed by Calentine (1964) to possible changes in the resistance of the C.carpio to cestode invasion. This concept was supported by the presence of an undescribed species of Monobothrium in one area of the Iowa River from 6 April to 20 May 1962. Up to 95% of the C. carpio were infected in April, but no gravid stages were ever found in C. carpio, nor in any other fish species in that area of the river. Since the Monobothrium were not found in other fishes, Calentine (1964) suggested that its presence in C. carpio appeared to be as a result of low resistance on the part of these fishes, rather than being caused by a lack of host specificity on the part of the parasite. The presence of A. iowensis was thought to be a result of this same low host resistance. The finding of malformed individuals, with scolex misshapen or lacking, and with a conspicuously swollen body, in fishes at certain times of the year, in late June, and once in late autumn, was considered to lend further support to the concept of lowered host resistance. Calentine (1964) suggested that the lowered resistance might originate from overwintering of the C . carpio with decreased feeding, and with spawning as a contributing factor.

7

HELMINTHS I N FRESHWATER FISHES

Recently Williams (1979~)reported Archigetes iowensis from Red Cedar River, Wisconsin, U.S.A. In this instance none of more than 450 Cyprinus carpi0 were infected by the worms either at Red Cedar River or elsewhere in Wisconsin. In oligochaetes the occurrence varied from 41 % in May 1978 to 3 % in July 1978. Archigetes sieboldi Leuckart, 1878 Szidat (1937)proposed a new combination, Biacetabulum sieboldi, as a result of finding four A . sieboldi in Tinca tinca in Germany. However, as noted earlier, Calentine (1965a) was able to separate Biacetabulum from Archigetes species on a number of differences. Kennedy (1965b) included Archigetes appendiczdatus as a synonym of A . sieboldi, after examining a growth series of A. sieboldi. WiSniewski (1930) produced a monographic study of the biology of the genus Archigetes. In Archigetes sieboldi the life cycle can be completed in the oligochaete host (WiSniewski, 1930; Kulakovskaya, 1964a; Calentine and De Long, 1966).The eggs were infective to oligochaetes after 40 days (Wiiniewski, 1930) or 16 days (Calentine and De Long, 1966). The procercoids matured in 60-70 days and produced eggs by 100-1 10 days (Wiiniewski, 1930). Calentine and De Long (1966) obtained similar results, procercoid development 80-100 days, eggs about day 120, and a maximum survival time in Limnodrilus hofmeisteri of 144 days. In Wisconsin, U.S.A., Calentine and De Long (1966) found gravid procercoids in L . hoffmeisteri solely in spring (late April through June), at other seasons only immature and mature stages were present. Kulakovskaya (1964a) found that in the western Ukraine, U.S.S.R., two generations of A . sieboldi (as Biacetabulum appendicuZatum) could mature in the oligochaetes each year, one about May, and the other about September-October (see Fig. 1).

v

VI

vii

Vlll

IX

x

XI

XI1

I

II

111

IV

v

VI

VII

FIG.1 . A chart to show the seasonal life cycle and development of the cestode Archigetes sieboldi. Stages 1 and 6 represent the egg in water, 2 and 7 the oncosphere in the egg, 3 and 8 the immature procercoids in oligochaetes, 4 and 9 immature A.sieboldi in the body cavities of oligochaetes, 5 and 10 mature individuals in the body cavities of oligochaetes, and 10a a mature A. sieboldi in the intestine of a fish. The life cycle can be completed without the necessity for a fish host, and fishes are normally infected only about April to June. Months are in roman figures. (From Kulakovskaya (1964a), Fig. 3, p. 181.)

8

JAMES C. CHUBB

In natural conditions infections have been found in fishes in Germany (Szidat, 1937), Sweden (Nybelin, 1962), western Ukraine, U.S.S.R. (Kulakovskaya, 1962a, b, 1964a), Wisconsin, U.S.A. (Calentine and De Long, 1966), Bulgaria (Kakacheva-Avramova, 1973), Poland (J. Wierzbicka, 1978) and L e h , Spain (Alvarez Pellitero et al., 1978b). In general the season of occurrence in the fishes was spring and early summer, for instance in Abramis brama and Tincu tincu from April to the beginning of June (Kulakovskaya, 1962a), in Cyprinus carpi0 in April-May (Calentine and De Long, 1966), and in Blicca bjoerkna in April (J. Wierzbicka, 1978); however KakachevaAvramova (1973) reported a specimen from Gobio gobio in the autumn. Alvarez Pellitero et al. (1978b) observed a well-defined annual cycle, although A . sieboldi were not found in some months. WiSniewski (1930), Nybelin (1 962) and Calentine and De Long (1 966) failed to experimentally infect fishes but Kulakovskaya (1962a) succeeded using a Tincu tinca. Nybelin (1962) in his experimental studies with fishes found that the survival times of the A . sieboldi in the fishes were between 6 to 24 hours at 20°C. Young worms died in less than three hours post-infection, mature worms (his Stage IV, sex organs clear, but not fully developed) survived about 6 to 12 hours, whereas A . sieboldi with eggs were still moving at 12 hours, but two of three showed signs of damage at 24 hours. It is evident, therefore, that A . sieboldi has only a temporary survival in the fish intestine, a situation contrasting strongly with that of A . iowensis which normally needs a fish host (Calentine and De Long, 1966). Biacetabulum biloculoides Mackiewicz and McCrae, 1965 Immature and mature specimens of B. biloculoides were found in small pit-like structures which appeared as small, soft cysts on the serosal surface of the intestine of Catostomus commersoni. In New York, U.S.A., gravid worms were found during July, August, October and November, the only months collections were made (Mackiewicz and McCrae, 1965). Biacetabulwn carpiodi Mackiewicz, 1969 Williams and Ulmer (1 970) collected Carpiodes cyprinus in various habitats in Wisconsin, Iowa (mainly) and Nebraska, U.S.A. Where C. cyprinus was sampled through the year B. curpiodi was present in spring and early summer but was absent after July. Biacetabulum infrequens Hunter, 1927 Gravid B. infrequens were found only in summer, but details of their pattern of occurrence were not determined, in Moxostoma erythrurum and M. anisurum from the Iowa River, Iowa, U.S.A. (Calentine, 1965a). The eggs obtained from M . erythrurum were undeveloped when shed. At 18-22°C embryonation needed 14-15 days, whilst the eggs remained invasive at least 215 days if held at 5-10°C. Tubifex tubifex and T. templetoni were infected. At 18-22°C procercoid development took about 51 days, but the infected tubificids were short lived, only up to about 67 days (Calentine, 1965a). B. infrequens occurred solely in immature tubificids, and parasitized host individuals did not become sexually mature.

HELMINTHS I N FRESHWATER FISHES

9

Biacetabulum macrocephalum McCrae, 1962 This species was reported by name only in McCrae (1961) and a description published by McCrae (1962). Calentine and Fredrickson (1965), in Catostomus commersoni at the Iowa River, Iowa, U.S.A., found that three fishes examined in November and January each harboured one immature B. macrocephalum. However of 83 C. commersoni dissected in April and May, none were infected. In June to August gravid adults occurred, but only in C. commersoni, and in nature eggs were shed from late June through August. Calentine (1965a) reported that the eggs deposited from C. commersoni were undeveloped. Embryonation occurred in 14 days at 18-22"C, but then no further development took place until the eggs were eaten by the intermediate hosts, Tubifex templetoni and T. tubijex. The eggs remained invasive for 230 days at 5-1OoC, but not for 300 days. Young tubificids were readily infected. Procercoid development took about 62 days at 18-22"C, and most tubificids containing procercoids died by day 120, although some lived up to day 177 post infection (Calentine, 1965a). Calentine and Fredrickson (1965) showed by experiment that 62 day old procercoids in October were invasive to C. commersoni, so that it seemed that fishes in nature could acquire infections by late autumn. The periodicity in the fishes was probably contributed to by the length of larval development in the tubificids, however Calentine and Fredrickson (1965) also suggested that the presence of Glaridacris catostomi in C. commersoni perhaps prevented B. macrocephalum from becoming established, since the B. macrocephalum were generally absent from fishes during those months when G.catostomi were present. The tubificid phase of development of Biacetabulum macrocephalum was also studied by Buchwald and Ulmer (1964). In particular, they examined the effect of temperature stress on the development of the procercoids. Maximum growth of procercoids occurred at 22°C. Survival was greater at 6°C (I 10 days) than at 22°C (70 days) or 33°C (35 days). Procercoids formed at 6 and 33°C were of similar size, but smaller than those formed at 22°C. At 22°C the development of the cercomer, scolex and genital rudiments were apparent 24 days post infection. At 6°C procercoids had not attained full development even after 110 days, whilst at 33°C procercoids showed no evidence of cercomer development nor scolex differentiation (Buchwald and Ulmer, 1964). Biacetabulum meridianum Hunter, 1929 Self and Timmons (1955) found inconclusive evidence that Carpiodes carpio at Lake Texoma, Oklahoma, U.S.A., were more heavily infected by Biacetabulum meridianum in the spring months. Grimes and Miller (1973, 1976) at Lake Raleigh, North Carolina, U.S.A., were able to give a detailed account of the occurrence of this species in Erimyzon oblongus. Incidence of B. meridianum was seasonally periodic, although some worms were present all year. After a gradual rise, incidence peaked in May and remained steady through the summer months. No seasonal trend in mean intensity of infection was seen, but there were two unusually high peaks of immature worms in October 1971 and July 1972. The July 1972 peak was well represented in all

10

JAMES C . CHUBB

fishes and corresponded to a decisive drop in the intensity of occurrence of Monobothrium ulmeri in E. oblongus. Grimes and Miller (1976) were of the opinion that heavy worm burdens of M . ulmeri present in the spring may have been unfavourable to the establishment of B. meridianum. The Biacetabzhm meridianum were divided into three maturity groups : immature, mature but no eggs in uterus, and gravid. Seven length classes of worms were also established. The first two length classes contained only immature worms, and individuals less than 2.5 mm in length were probably recent invasions. Worms in these first length classes were present throughout the year. The third length class was the transition point from immature to gravid, since it included B. meridianum of all maturity groups. Gravid worms were restricted to the late spring and summer. After April there was an increase in the number of gravid worms and some growth into the higher length classes. However, except in May, gravid worms never represented a significant proportion of the population (Grimes and Miller, 1976). The restricted period of maturation of Biacetabulum meridianum may have resulted from increased water temperatures, or changes in the host hormonal balance, or both (Grimes and Miller, 1976). There was no relationship of presence of B. meridianum with host sex. Grimes and Miller (1976) assumed that the procercoids were available for invasion of E. oblongus throughout the year, recruitment was continuous, and parasites were lost if the stimulus for growth and maturation was not present. Caryophyllaeus brachycollis Janiszewska, 1953 The intermediate hosts for Caryophyllaeus brachycollis in the Ukraine, U.S.S.R. were Limnodrilus hoflnnzeisteri and Tubifex tubifex (Kulakovskaya, 1962b). Kakacheva-Avramova (1973) found C. brachycollis spring to autumn in Leuciscus cephalus and Vimba vimba tenella in the Central and Eastern Balkan Mountains, Bulgaria. Caryophyllaeus fimbriceps Annenkova-Khlopina, 1919 Some confusion of identity between Caryophyllaeus fimbriceps and C. laticeps has occurred, at least in the U.S.S.R. Thus, according to Bauer (1959a) the records of C. laticeps by Kanaev (1956) were probably of C.Jimbriceps. Dubinina (1949) found a maximal infection of Caryophyllaeus jimbriceps in Cyprinus carpio in the Volga Delta, U.S.S.R., when these fishes fed voracicusly after the winter. In winter the parasites died owing to starvation caused by a cessation of feeding by C. carpi0 (Dubinina, 1950). Ivasik (1952) reported Caryophyllaeusfimbriceps as a pathogen of Cyprinus carpio in fish ponds in the Ukraine, U.S.S.R. O+ fishes died in June owing to about 30 to 40 worms per fish, and one year old C. carpio in April and early May with 70 to 100 parasites per fish. C.$mbriceps was present in the C. carpio in fish farms through all seasons (Ivasik, 1953). Kanaev (1956), in the Kalinin and Moscow regions of the U.S.S.R. found a peak infection of C.$mbriceps in June, with a gradual decline and loss of worms through to the following May. Bauer (1957), in fish ponds in the Leningrad, Velikie and Novogorod districts, U.S.S.R., found that fingerling Cyprinus carpio were invaded in

H E L M I N T H S I N FRESHWATER FISHES

11

autumn and through the winter, especially when water temperatures were relatively high. For instance, if the fishes took food at 4"C, a mass invasion of worms could occur, but if the water temperature was below 2"C, then the C. carpio were not invaded by Caryophyllaeus jimbriceps until the spring (Bauer, 1959a). Bauer (1959a) and Bauer et al. (1969) summarized the life cycle of C.$mbriceps as: an egg stage which could survive for up to three months in water; intermediate hosts Psammoryctes albicola and Tubifex tubifex (see Kulakovskaya, 1962b); with procercoids invasive after six months development, but may live up to two years in the oligochaete and grow to 18 mm long with fully formed genitalia. The adult worms in the fishes lived 2-3 months. The annual cycle had a marked seasonal aspect, with the oligochaetes being invaded in summer, but although invasive procercoids occurred all year, many became established in the fishes in spring owing to the feeding patterns of the fish hosts. Thus epizootics were common in two year old pond C. carpio in May and June because they consumed large numbers of tubificids at that time (Bauer et al., 1969). Epizootics occur in other months as well, if conditions are appropriate, so that Ivasik (1952) noted that C. carpio fry suffered a massive mortality in the last part of July owing to C. jimbriceps. Unseasonable low water temperatures caused the fishes to feed on the benthic invertebrates, including oljgochaetes, rather than pIankton, their usual food at this time, so that heavy invasions by procercoids of C.Jimbriceps resulted. Kanaev (1956) claimed an age dependent immunity of Cyprinus carpio to invasion by Caryophyllaeus fimbriceps. Bauer (1959a) noted that this claim required experimental verification. It is likely that the decline in infection in older fishes could be related to changed diet. Kulakovskaya et al. (1965) found that under fish farming conditions in the Ukraine, U.S.S.R., the occurrence of C.$mbriceps in C. carpio was determined by the species composition and number of tubificids, their level of infection by procercoids and the extent that they were utilized as food by the fishes. Komarova (1964) noted Caryophyllaeus jimbriceps in Abramis brama in March at the Dnepr Delta, U.S.S.R., but not in February or April-August or October. A . brama was presumably an auxiliary host of C. fimbriceps (see Bauer, 1959a). Caryophyllaeus laticeps (Pallas, 178I) There is a considerable literature available for this species. Zschokke (1884) reported Caryophyllaeus laticeps from Leuciscus cephalus in Lake LCman, Switzerland, in January, June and August. Sramek (1901) at Pod& brady, Czechoslovakia, found it in eight species of Cyprinidae FebruaryJune, November and December, immature and mature worms occurred throughout. Ruszkowski (1926) noted it in habitats near Warsaw, Poland, in four species of cyprinids during February, May, October and November. Scheuring (1929) stated that the life cycle was completed in one year. The seasonal incidence pattern was ascribed by Scheuring (1929) to reduced feeding of the host fishes owing to the seasonal drop in water temperature. Sekutowicz (1932, 1934) showed that the intermediate hosts for C. laticeps

12

JAMES C . C H U B B

were Tubifex barbatus and Tubifex tubifex (see also Kulakovskaya, 1962b). The life cycle was described by Sekutowicz (1934). The oncosphere was fully developed after 14 days, and embryonated eggs could be kept alive in water at laboratory temperatures for three months. The development in the tubificids was elucidated. The procercoids became invasive at a state of development similar to Diphyllobothrium and Triaenophorus species, but if not eaten by a fish at this time the larvae continued to develop in the tubificids until the genitalia were formed; however these became functional only in the intestine of the fish host. Wunder (1939) in carp ponds in Germany (now Poland) found that the Cyprinus carpio were not infected from September to March; the highest incidences were April (44%) and May (54%) falling through June (26 %), July (9 %) and August (1 %). The infection during this period April-August was attributed to the fishes eating tubificids, the intermediate hosts. A similar peak incidence in spring was seen by Dogie1 and Bykhovskii (1939) in the Volga Delta area of the Caspian Sea, U.S.S.R. In four species of cyprinid fishes they observed that C. laticeps overall was most abundant in the first half of the summer. Incidences were: Tumak, May-July 29%, August-October 2.2 %, and at Sara Island, May-July 40 %, August-October 8.7 %. An annual cycle of occurrence was postulated. The following studies are briefly summarized, details of host species are given in Table I: Dubinina (1949), Volga Delta, U.S.S.R., present spring, summer, winter, highest incidence spring; Dubinina (1 950) C. laticeps died during winter owing to cessation of host feeding, degenerate worms found; Bogdanova (1958), River Volga, U.S.S.R., present February-March, May and July-August, highest incidence May ; Bogdanova (1959) intensity of infection increased in winter; Kosareva (1959), Volga-Don canal, U.S.S.R. more common May-June (spring) than August-September ; Kozicka (1959) Lake Druino, Poland, found spring to autumn, incidence highest spring; Izyumova (1958, 1958a, b, 1960), Rybinsk Reservoir, U.S.S.R., occurred in four cyprinid species, in Abramis brama present all year, high summer, but by the end of winter cestode numbers considerably reduced; KaiiC (1970), Lake Skadar, Yugoslavia, in Cyprinus carpio young worms present DecemberApril, maximum March, mature worms increasing January through March, peak April, declining May to disappear July; Komarova (1 964), Dnepr Delta, U.S.S.R., maximum incidence A . brama April and May, present all months in this host, but mostly May in auxiliary hosts Blicca bjoerkna, Rutilus rutilus heckeli and Vimba vimba vimba natio carinata: Lyubarskaya (1965, 1970), Kuybyshev Reservoir, U.S.S.R., A . brama strong infection spring, but gone in autumn; Marits and Vladimirov (1969), Dubossary Water Reservoir, Moldavia, U.S.S.R., Vimba vimba vimba natio carinata, highest incidence summer; Marits and Tomnatik (1971) also Dubossary Water Reservoir, A . brama highest incidence in summer; Kakacheva-Avramova (1977), River Danube, Bulgaria, present spring-autumn ; Alvarez Pellitero et al. (1978b), Duero and Sil Basins, Le6n, Spain, annual one generation cycle in cyprinids, but not found some months; and Wierzbicka (1978), Lake Dabie, Poland, commonest A . brama, present all year, slightly higher incidences in spring, whereas in B. bjoerkna, incidence low most samples, but

HELMINTHS I N FRESHWATER FISHES

23

high May 1970, 1971 and June 1970. From the above data, it can be seen that the pattern of incidence varied somewhat according to host and habitat, although there was a trend towards spring as the time of maximum incidence. Abramis brama appeared to be the preferred principal host, with maximal occurrences, and often with some C. laticeps year round, whereas other cyprinid hosts had lower occurrences, often seasonally limited, tending to maximal occurrence in spring. The remaining studies are discussed in more detail, because they show the variety of the seasonal biology in Curyophyllueus laticeps. Mishra (1966) studied the development of the genitalia of C. laticeps in Rutilus rutilus at the Shropshire Union Canal, Backford, England. He recognized three stages: I genitalia not developed; I1 genitalia developed, no eggs present; and 111 eggs in uterus. Incidence varied between 2-10% through the year, zero incidence was found in March, October and December, 1-2% in January, February, May-August, 8 % in September and November and the maximum 10% in April. Mean intensity per infected host was 1-6 during most months, but high (27) in April. The seasonal genital development pattern was clear, June and July all Stage I, August, September and November, progressive movement from Stage I to 11, January, February and April, all Stage 11, and May all Stage 111. Davies (1967) at the River Lugg, Herefordshire examined three species of fishes Leuciscus cephalus, L. leuciscus and R. rutilus. Incidence was low, 3-23%, but maximal for L. cephalus in June and L . leuciscus and R. rutilus in July. Intensity was also low 1 4 , with a peak of nine in R. rutilus in July. Davies (1967) used five stages of maturation: Stage I no genitalia; Stage I1 genitalia appearing; Stage I11 genitalia fully developed, no eggs; Stage IV eggs first present; and Stage V many eggs in uterus. Over the three host fishes, the maturation pattern was (expressed as percent of population of worms for respective host and month) : L. cephalus February Stage 111 50%, IV 50%, March Stage 111 loo%, June Stage 11, 9%, I11 9%, IV 18 % and V 64 %, and July, August and October Stage V 100 %; L. leuciscus April Stage I1 25 %, Stage 111 25 %, Stage IV 50 %, June Stage IV 100 %, July Stage IV 8 %, Stage V 92 %, October Stage I11 68 %, Stage V 32 %, and December Stage I11 100%; R. rutilus March present, no maturity data, April Stage I1 l#%, may Stage V 100%, June Stage 33 %, Stage V 67 %, July Stage I 74%, Stage I1 9 %, Stage I11 3 %, Stage V 14%, and December Stage V 100%. Over the three host species gravid worms (Stage V) were found in the River Lugg March, May-August, October and December, and in L. cephalus during five, L. leuciscus during two and R. rutilus during four of these months. At the River Avon, Hampshire, England, Kennedy (1968, 1969a, 1972c) observed the dynamics of Caryophyllaeus laticeps in Leuciscus leuciscus. In August to November, except for one worm in October, no C . laticeps were found. Incidence rose December, rapidly January (23-1 %), February (56 %) and March (59-2%) to a peak (60 %) in May. It declined in June (22.2 %) and no worms were present by August. Intensity went up with incidence, and was maximal in February. Kennedy (1968) used worm Iength to show monthly pattern of changes in the population, but gravid worms were present January

14

J A M E S C. C H U B B

to July, peak March-May. The dynamics were December-January recruitment high, February-May recruitment continued, but incidence and intensity steady, hence gain and loss of worms approximately equal March to May, and May to June recruitment declined, population lost. Kennedy (1968) noted that many C. Eaticeps had a short life span so that few survived a long time to increase in length. Length and maturity were interrelated, but not exactly. The explanation for the pattern of occurrence of C. laticeps in the River Avon suggested by Kennedy (1968,1969a, l971,1972a, c) will be considered below. At the River Glomma, Norway, Halvorsen (1972) found that Caryophyllaeus laticeps in Abramis brama was present from May to August, through which period the fishes were active. Gravid worms increased from 0% in May to 100% by August. The worms were recruited spring and summer, produced eggs and died. When the A . brama withdrew to their winter quarters they did not feed so were not invaded at this time. Anderson (1974a) studied the dynamics of a population of C. laticeps in a gravel pit near Dagenham, Essex, England. Four stages of maturity were separated : Stage I, immature with primordial germinal cell mass present, but gonads and associated structures not distinct; Stage 11, maturing worms with gonads and associated structures becoming distinct but vitellaria not developed ; Stage 111, mature with distinct gonads and associated structures and fully developed vitellaria; Stage IV, gravid worms with eggs present in the uterus. In summary C. laticeps was present all months, new arrivals were found each month, herefore invasion occurred throughout the year. At a water temperature of 12°C the worms took about I month to reach maturity in the fish host. Incidence was zero in O+ fishes, and heaviest in fishes 5+ years of age. Intensity of occurrence was maximal (mean number per fish, 5+ A . brama) in July. Gravid worms were present all months; when expressed as a percentage of the population in each month, occurrence was minimal (25%) in November and February, 50% or less October to May, and 71.2% in June, 80 % in July and 100 % in August and September. Water temperature ranged from 3°C in February up to 22°C in July. The factors involved in the dynamics at this locality will be considered below. In Lake Malaren, Sweden, Milbrink (1975) also surveyed the occurrence of Caryophyllaeus laticeps in Abramis brama. An identical cycle was found eachyear during the four years of study. Two peaks of infection were manifest, one in spring and one in the autumn, whilst the summer level was low. The ice cover in Lake MBlaren was from mid-December to mid-April, and the spring maximum commenced when the water temperature was still below 5°C. Overall, the worms were most numerous during the coldest half of the year. Reinsone (1955) at Lake Kals, Latvia, U.S.S.R., showed that high infections of Curyophyllaeus laticeps were present in winter in Abramis brama in this lake which contained hot water springs, so that the fishes continued to feed. Strizhak (1971) at the Ivan’kovsky Reservoir, U.S.S.R.,also in A. brama, compared the occurrence of C. laticeps in two bays, one heated by effluent from a power station, and the other unheated. In this instance, throughout

HELMINTHS I N FRESHWATER FISHES

15

the year the numbers of parasites were highest in the unheated bay, but the C. Iaticeps matured in the heated bay two to three months earlier. For example in February-March, the percentage of the population mature in the unheated bay was 0.7%, whereas it was 24.2% at that time in the heated bay. Whatever the season the rate of growth and maturation of the worms was higher in the heated bay, but the incidence and intensity of infection lower. The invertebrate intermediate hosts for Caryophyllaeus laticeps have been studied in a seasonal context by Kennedy (1969b, 1972a) and Milbrink (1975). Kennedy (1969b) found invasive larvae in Psammoryctes barbatus during all months except August, and they were most abundant October to July. However, the tubificids were found in the intestine contents of only three of 444 L. leuciscus examined over a year, so that no correlation with host feeding was possible (Kennedy, 1969a). The digestion of ingested tubificids in the intestinal bulb of the L. leuciscus was shown by experiment to be so rapid that they were only recognizable with certainty after three hours by using a high powered microscope. The invasion of the P. barbatus by ingestion of the eggs of C. Iaticeps was thought to occur July or August, but it was impossible to differentiate infected P. barbatus until October (Kennedy, 1972a). The P, barbatus had one generation per annum, and produced cocoons March to June. Milbrink (1975) found four species of intermediate hosts, Potamothrix hammoniensis, P. hemcheri, P. vejdovskyi and P. bedoti. The presence of small parasites in the intestinal bulbs of the A . bramae suggested that invasion occurred all year. Milbrink (1975) calculated that, assuming a 0.1 % infection by procercoids, about 190 000 to 250 000 tubificids must have been eaten by a fish to give an intensity of infection of 50C. laticeps, which was common in Lake Malaren. As can be seen from the preceding paragraphs a variety of patterns of occurrence are apparent for Caryophyllaeus laticeps. In order to understand this variety it is necessary to know something of the mechanisms of control. In the first instance it should be noted that potentially invasive larvae were available year round (Kennedy, 1969b; Milbrink, 1975). Kennedy (1971) studied the effect of water temperature on the establishment and survival of C. laticeps in Leuciscus idus. At 12°C and lower there was an initial loss post-invasion, but the survivors persisted for up to one month. However, a t 18°C the cestodes were killed and rejected after three days, and transplants to fresh hosts after two days indicated that the factors responsible for death of these worms became effective within this period. Neither inhibition of host peristalsis nor starvation influenced the cestode survival. Kennedy (1971) considered that circulating antibodies could not be involved owing to the speed of the response, and the experimental fishes were farm-reared with no previous experience of infections of C. laticeps. The results indicated that establishment and survival in L. idus were related to temperature, with a critical level around 13°C. It was not temperature per se that caused death of the cestodes, as the larvae survived in tubificids at 18°C. Single worm invasions eliminated the possibility of crowding as a factor. In the transplant experiments dead C. laticeps were recovered from the rectum of the fishes,

16

JAMES C. CHUBB

suggesting that the worms were killed rather than merely eliminated from the host intestine (Kennedy, 1971). Kennedy and Walker (1969) attempted to show an immune reaction against C. laticeps in Leuciscus leuciscus but failed to demonstrate circulating antibodies, although the speed of parasite rejection increased and the period of establishment decreased with a rise of temperature, which was consistent with an antibody system of resistance in fishes. The temperature dependent rejection response was clearly shown, but Kennedy and Walker (1969) could not demonstrate the exact mechanism of operation of the system. Harris (1973) later failed to demonstrate the production of skin-sensitizing antibody to antigenic extracts of C. laticeps by homologous passive cutaneous anaphylaxis or by heterologous PCA reaction in guinea-pigs. Anderson (I974a) also found that the mortality rate of Caryophyllaeus laticeps in Abramis brama increased markedly during the mid-summer months, and this was not a density dependent response. The temperature dependent host response system suggested by Kennedy (1969b) was invoked to explain the increased mortality. Milbrink (1975) also explained the spring and autumn peaks of infection in Lake Malaren using the same system. The lowered incidence in December-February was related to reduced feeding activity of A . brama and the slower rate of digestion at low temperatures. The spring peak incidence corresponded to a resumption of feeding, and whilst water temperatures were still low, an increased survival of the worms. The scarcity of C. laticeps during the summer months of high water temperature was attributed to the effect of the temperature controlled host response system. The feeding activity of the A . brama continued at a high level until the end of November. As water temperatures fell, so the host response was reduced and the autumn peak of incidence was established, these worms being progressively lost during the following winter (Milbrink, 1975). The population dynamics of Caryophyllaeus laticeps in Abramis brama at a gravel pit near Dagenham, Essex, were analysed in great detail by Anderson (1974a, b, 1976a, b). Seasonal incidence was related to the feeding of the fishes on tubificids and the temperature-dependent host response discussed above was suggested to explain the seasonal changes in the mortality of adult C. laticeps. A deterministic recruitment-mortality model was proposed containing non-homogenous recruitment and rates of mortality which described the life of an adult parasite population in a single fish (Anderson, 1974a). In a later paper Anderson (1976a) examined the ecological factors which generated seasonal fluctuations in even greater detail. The following are the main points relevant here: the populations of adult C. laticeps within the fish definitive host appeared to be controlled to a large extent by density independent factors. Water temperature seemed to be the dominant physical factor, which directly influenced the rate of mortality of adult worms, and which also in conjunction with day length, affected the feeding behaviour of the fishes and thus indirectly the recruitment rate of larval parasites (Anderson, 1976a). Density independent factors are primarily

H E L M I N T H S I N F R E S H W A T E R FISHES

17

physical in character and thus of a climatic nature (Anderson, 197613). Anderson (1976a) stressed that when considering the entire life cycle of C. laticeps, which involved five distinct parasite and host populations, each with separate niches in.the habitat, it was apparent that a large number of biological and physical parameters determined the dynamics of the system (see Fig. 2, from Anderson, 1976a).

Immigration

I & I

Adult parasite population

Death

B i r t h of eggs

*

Immigration

r Aquatic habitat Parasite egg populJtion

Emigration

FIG.2. A diagrammatic flow chart of the populations and population processes involved in the life cycle of the cestode Curyophyllueus luticeps. (From Anderson (1976a), Fig. 2, P. 284.)

The larval parasites, for example, gained entry to the definitive host as a result of the predatory activities of the Abramis brama and thus the dynamics of the predator-prey interaction, between definitive and intermediate hosts, would directly influence the flow of parasites through the life cycle. Changes in the sizes of invertebrate populations within the habitat were likely to determine the stability of this interaction since food preferences of cyprinid fishes have been shown to vary in response to prey densities. This type of host behavioural change could play an important role in determining the seasonal feeding activity of A . brama (Anderson, 1976a). A further point to be considered was the effect of time lags on the rate of flow of parasites through the life cycle system of Caryophyllaeus laticeps. These lags were primarily owing to developmental processes: for example, a

18

JAMES C. CHUBB

delay often occurred between the time of release of an egg from the adult parasite and the point when this egg was sufficiently developed to infect an intermediate host. The length of time lag might be controlled by environmental factors such as temperature, since an increase in this physical parameter was often associated with an increase in the rate of development of larval parasites (Anderson, 1976a). The life cycle of Caryophyllaeus laticeps contained many developmental time lags in the egg, larval and adult stages. These delays allowed a specific population, such as the adult parasites, to become temporarily extinct without resulting in the termination of the cycle. This type of situation would arise if the fish host ceased to feed on tubificid oligochaetes, owing perhaps to an abundance of an alternative and more desirable food source. Since the reservoir of infected intermediate hosts remained, however, the adult parasites would reappear when the fishes resumed feeding on tubificids. The length of this period of non-feeding would obviously be critical, as would be the timelag in development to the invasive state. If the non-feeding period was longer than the time taken to become invasive plus the maximum life span of this invasive stage, then the parasite might become extinct in a given habitat (Anderson, 1976a). Caryophyllaeus laticeps was well insulated against sudden changes in host habits since the larval parasites took approximately four months to become invasive in the intermediate host and could then survive for periods greater than one year. The eggs of C . laticeps were also thought to have long developmental and invasive periods, although no precise information was available. The stability of host-parasite systems, both to alterations in host behaviour and environmental conditions, was most probably greatly enhanced by these time lags in development and the long invasive periods of the eggs and larval parasites (Anderson, 1976a). Periodicity in the maturation of the adult parasite would also play an important role in the population dynamics of Caryophyllaeus laticeps. The proportion of mature parasites which produced eggs varied seasonally, the largest proportion arose in the summer months ; the warm water temperatures probably acted as a stimulus to reproductive development and hence egg production (Anderson, 1974a). The peak production period coincided with a decrease in the size of the adult parasite population which was moving towards a minimum value in autumn. This process might serve as a regulatory mechanism, controlling population size by preventing too large a proportion of the intermediate host population becoming infected as a result of the saturation of the habitat with parasite eggs (Anderson, 1976a). An additional factor influencing the population dynamics of Caryophyllaeus laticeps was related to the age structure of the fish population. The various age groups of the fish population had markedly different feeding habits. The age distributions of natural populations of Abramis brama were highly skewed, fewer fish occurred in the older age classes and thus differences in host feeding behaviour would have a marked effect on the numerical size of the totaI parasite population (Anderson, 1976a).

H E L M I N T H S I N F R E S H W A T E R FISHES

19

A feature of helminth parasite populations was the overdispersed nature of the distribution of adult parasites within the host population. In the instance of Caryophyllaeus laticeps, this observed pattern was mainly owing to heterogeneity between fishes in the number of larval parasites gaining entry to the host. This type of process, as demonstrated by Anderson’s (1976a) theoretical simulation studies, resulted in frequent local extinctions of parasite populations within individual fishes. These events were most apparent when the overall population size was at a minimum, during the autumn and winter months. Chance fluctuations during these periods of the year might lead to the extinction of the parasites in localized host populations for short periods of time (Anderson, 1976a). According to Anderson (1976a) the mathematical model of the population dynamics of Caryophyllaeus laticeps within the fish provided a useful framework for : (a) examining various biological assumptions by the comparison of observed and expected results; (b) assessing the relative influences of the immigration and death parameters on the population dynamics of the adult parasite ; (c) investigating the processes which generated the observed distribution of parasite numbers within the host population; (d) predicting future behaviour of the system under altered environmental conditions such as changes in water temperature; and (e) estimating the importance of chance effects on the dynamics of individual parasite populations (Anderson, 1976a). The major points of the discussion section of the paper by Anderson (1976a) have been incIuded above because they illustrate the extreme importance of the interplay of these factors in determining the seasonal dynamics, not only of Caryophyllaeus Iaticeps, but also of all the other helminth parasites included in this review. CaryophyIIaeus species Kulakovskaya (1964a), covering both Caryophyllaeus jimbriceps and C. laticeps, summarized the life cycles in conditions of the western Ukraine, U.S.S.R. as shown in Fig. 3. Markevich (1963) noted that adult worms of Caryophyllaeus species perished in early winter in the Ukraine, U.S.S.R., after having laid large quantities of eggs. Glaridacris catostomi Cooper, 1920 Calentine (1965b) showed that the intermediate hosts for Glaridacris catostomi were, with rate of larval development in parentheses, Limnodrilus hofmeisteri (1-2 mm long larvae in 46 days), L. udekemianus (0.8, 1.1 mm, 43 days), Tubifex templetoni (0-9 mm, 63 days, 70 days to complete development) and T. tubifex (0.7 mm, 46 days). Infected annelids were rather short-lived and did not become sexually mature, although one of each species did survive to 144 days at which time the experiment was terminated. Calentine and Fredrickson (1965) found that the egg (oncosphere) viability was 90 days at room temperature, but at least 230 days, but less than 300 days, at 5-10°C. Natural infections of procercoids in oligochaetes reached a peak in autumn (10%). Immature G . catostomi were commonly present in Catostomus commersoni

20

JAMES C. C H U B B

r

VI

VII

Vlll

IX

x

XI

XI1

I

II

111

IV

v

VI

VII

Vlll

FIG.3. A chart to show the seasonal life cycle and development of the cestodes of the genus Curyophyllueus in the Ukraine, U.S.S.R. Stages 1 and 9 represent the egg in water, 2 the oncosphere in the egg, 3 the immature stages of the procercoids in oligochaetes, 4 and 5 the invasive procercoids in the body cavity of the oligochaetes, 6 an immature but adult Curyophyllueus in the intestine of a fish, and 7 a mature adult in the intestine of a fish. The timing of occurrence of adult Curyophyllueus species in fishes shows great variability from one locality to another, see p. 10 - 19 in text. (From Kulakovskaya (1964a), Fig. 2, p. 179.)

at this season. A distinct seasonal periodicity was found in C. commersoni at Iowa River, Iowa, U.S.A., by Calentine and Fredrickson (1965). Gravid worms occurred January, April through June (no collections FebruaryMarch). The maximum incidence of gravid adults in fishes apparently occurred winter or very early spring. Eggs were deposited up to June, but not thereafter. Immature cestodes were almost completely absent from fishes in late spring and summer, but reappeared in September (19 % incidence), were abundant in October (53%) and November (63%). Invasion of fishes was considered to occur between September and November. At summer temperatures embryonation of the eggs took about 19 days. Calentine and Fredrickson (1965) thought that the oncospheres were unlikely to survive later than October, hence most tubificids must have acquired infections prior to that month. The peak occurrence of procercoids in tubificids was in October, and in nature it was likely that few infected tubificids survived the winter. The periodicity of G. catostomi in the Iowa River was explained by Calentine and Fredrickson (1965) as owing to the failure of embryonated eggs to overwinter, together with the short life of the infected annelids and of the adult G . catostomi in the fish host. At Central New York State, U.S.A., Mackiewicz (1965b) collected GZaridacris catostomi in Catostomus commersoni during all months except March and September, but gravid worms occurred only in February, April and May. Lawrence (1970) at Pushaw Lake, Penobscot County, Maine, U.S.A., found that C. commersoni were also with peak infections January-April. Lawrence (1970) divided the seasons into: January to April, ice cover to ice break;

HELMINTHS I N FRESHWATER FISHES

21

May to August; and September to November. No sampling was possible during ice formation in December. Duncan’s multiple range test indicated that the period January (85 % incidence) to April (67 %) was significantly different from May (63 %) to August (0 %) and September (38 %) to November (68 %). Lawrence (1970) found data which suggested that invasive larvae of G. catostomi occurred all through winter, and were taken by C. commersoni all through the year, as shown by the fact that immature G. catostomi were seen in all months except May and August. However, there was a steady recruitment from September to November. G. catostomi and Isoglaridacris bulbocirrus were found as concurrent infections to a greater extent than could be attributed to chance alone (Lawrence, 1970). In Lake Michigan, U.S.A., Amin (1977) found Glaridacris catostomiin small numbers in Catostomus commersoni; however gravid individuals occurred January, March and April and no worms were seen in September, suggesting a seasonal pattern similar to those reported above. At Red Cedar River, Wisconsin, U.S.A., Williams (1979b) studied the occurrence of Glaridacris catostomi in Catostomus commersoni from July 1977 to July 1978. The worms were divided into three categories: immature, lacking one or more reproductive organs; mature, with all reproductive structures present; and gravid, possessing eggs. Overall there was a high incidence autumn, winter and spring, until May, to fall to the lowest level of occurrence in July. Immature worms increased in abundance from June through until November, to decrease thereafter to May. Mature G. catostomi were present approximately three months later than the immature ones, increasing from September to a maximum in March, to fall and disappear by June. Mature worms were not present during the summer months. Gravid cestodes were seen about one month later than the mature and four months later than the immature individuals. The gravid G . catostomi increased in numbers until May, to decline gradually through the summer to disappear September. An annual cycle was postulated by Williams (1979b), with recruitment June to December, maximal gravid worms late winter and spring, and a population decline to early summer (June). Gluridacris confusus Hunter, 1929 Self and Timmons (1955) found inconclusive evidence that infections of Curpiodes carpio in Lake Texoma, Oklahoma, U.S.A., were heavier during the spring months. Gluridacris laruei (Lamont, 1921) At Pushaw Lake, Penobscot County, Maine, U.S.A., Lawrence (1970) found that Catostomus commersoni had the greatest incidence and mean intensity of Glaridacris laruei January (95 %, 25) through April (loo%, 25), the ice cover to ice break period. However high incidences and mean intcnsitjes occurred in all other months (range May 88 % to July 70 %, 22 October to 5 September). No samples were collected in December during ice formation. Calentine (personal communication to Lawrence, 1970) had found that in Wisconsin, U.S.A., peak incidence of G. laruei was approximately July to November, suggesting that variations were to be expected in different regions.

22

JAMES C . CHUBB

Lawrence (1970) found a slight statistical significance in level of occurrence of G. laruei between male and female C. commersoni, but offered no explanation. Williams (1979b) at Red Cedar River, Wisconsin, U.S.A., also studied the occurrence of Glaridacris laruei in Catostomus commersoni. In this investigation the worms were divided into the following developmental categories : immature, lacking one or more reproductive organs; mature, with all reproductive organs present; gravid, containing eggs. Although G. laruei was found in the fishes in all months of the year, Williams (1979b) noted maximal incidences in May and August through to December. Immature worms were present from June to December, maximal September-October, mature from June increasing to September, to decline thereafter to December, with low levels through January to June, and gravid G. laruei occurred all months, but peaked in May, August and November and were in the host fishes in largest numbers from May to December. Calentine and Fredrickson (1965) had suggested that the presence of Glaridacris catostomi infections in Catostomus comrnersoni might prevent larvae of other species from becoming established. Williams (1 979b) indicated that if concurrent presence of G. catostomi in his study (see above for account of seasonal occurrence of G. catostomi) inhibited or prevented the establishment of G . laruei, it would be expected that few G. laruei would be found when the incidence and intensity of gravid G. catostomi was highest. Overall, Williams (1979b) considered that his data supported the contention, except that both intensities of G. catostomi and G. laruei were high in May. He suggested that perhaps as water temperatures increased, thus affecting C. commersoni in some way, the inhibiting mechanism, as suggested by Calentine and Fredrickson (1965), no longer functioned. He conjectured that possibly G. catostomi influenced the population of G. laruei but was itself influenced by an immune response produced by C. commersoni during warm water conditions. Glaridacris yogei Mackiewicz, 1976 Williams (1978) collected gravid adults of this species from Catostomus macrocheilus in Fern Ridge Reservoir, Oregon, U.S.A. Eggs were shed into distilled water and at 19-23°C procercoids developed in 38-70 days in Limnodrilus claparedeianus, L. hofmeisteri and Tubifex templetoni. At 55 days fully developed procercoids averaged 1-5mm in body length. Dero digitata took eggs, but procercoids were dead after 15 days. Natural infections of L. claparedeianus (0.8 % of 2046 oligochaetes) were collected in Fern Ridge Reservoir from September to December. No information is available for the occurrence of the adult G. vogei. Hunterella nodulosa Mackiewicz and McCrae, 1962 Calentine (1965b) showed experimentally that the larval development of Hunterella nodulosa in Limnodrilus hofmeisteri at laboratory temperatures was completed in about 46 days. Some of the infected annelids became sexually mature, a condition seldom observed in annelids infected with larvae of other caryophyllaeid species. Two of the infectedl. hofmeisterisurvived for 466days.

H E L M I N T H S IN F R E S H W A T E R F I S H E S

23

Mackiewicz and McCrae (1962) suggested that their data concerning Hunterella nodulosa in Catostomus cornmersoni from central New York State and Colorado, U.S.A., throughout the year indicated that a seasonal distribution was not exhibited. Calentine and Fredrickson (1965) at the Iowa River, Iowa, U.S.A., found gravid adult H . nodulosa in C . commersoni during every month collections were made (January, April-November). Natural infections of procercoids in annelids reached a peak in the autumn, and Calentine and Fredrickson (1965) maintained experimentally infected Limnodrilus hoflineisteri at room temperature for 15 months, at which time the experiment was terminated. They suggested that this capability of the annelids to carry the procercoids from one year to the next might account for the lack of seasonal periodicity of the adult cestodes in fishes. A detailed analysis of the occurrence of Hunterella nodulosa in Catostomus commersoni in Nose Creek, Bow River, Alberta, Canada, was made by Mudry and Arai (1973). No seasonal changes in incidence or intensity of infection were observed. However, seasonal changes in frequency distribution of the cestode size classes indicated a seasonal infection cycle. The H. nodulosa were measured and placed in 1 mm length classes. A comparison, for instance, of May with July, showed a highly significant difference in size groups of worms. The general pattern was: only large worms (greater than 3 mm long) were present in early spring, smaller H. nodulosa were recruited during May and June, while the large worms were lost by July. The small worms increased in size, and their recruitment continued at least until October. The pits in which the H. nodulosa occurred in the host intestine were considered by Mudry and Arai (1973) to be very stable structures into which worms were continuously recruited from year to year, as was indicated by the changes in size groups of cestodes collected. Abandoned or semi-repaired pits were never found. A relatively long life span of the H. nodulosa in the fish host was considered important in the lack of seasonal changes in incidence and intensity of infection (Mudry and Arai, 1973). No host-response to H. nodulosa was noted in C. commersoni. Isoglaridacris bulbocirrus Mackiewicz, 1965 This cestode was reported as an undescribed species in Calentine and Fredrickson (1965), but the description was published by Mackiewicz (1965a). Experimental and natural infections of procercoids of Isoglaridacris bulbocirrus were in Limnodrilus hoflnieisteri. Eggs were produced by the adult worms in Cutostomus commersoni during June to September. Embryonation of the eggs required 16 days and larval development about 42 days at laboratory temperatures. According to Calentine and Fredrickson (1965) it seemed that C. commersoni could acquire invasions by late autumn, although they recovered only two immature cestodes, even though 119 fishes were examined in October, November, January, April and May. However in June an incidence of 34 % occurred, rising to 46 % in July, then falling to lower levels in August (21 %) and September (22%). The absence of I. bulbocirrus from the fishes corresponded to the period when Glaridacris catostomi was present (Calentine and Fredrickson, 1965).

24

JAMES C . C H U B B

Lawrence (1970) at Pushaw Lake, Maine, U.S.A., also investigated Isoglaridacris bulbocirrus in Cutostomus commersoni. He divided the year into: January to April, ice cover to ice break; May to August; and September to November. The cestodes were most abundant in the January to April period, but present all months, with minimum incidence in July (20%). Maximum incidence (83%) and intensity (mean 13 per fish) were seen in April. Lawrence (1970) found I. bulbocirrus and Glariducris cutostomi together in the same host fishes to a greater extent than could be attributed to chance alone. Isoglariducris folius Fredrickson and Ulmer, 1965 Fredrickson and Ulmer (1965) examined Moxostomu erythrurum from April to December, but not during the winter period of ice cover. The highest incidences of Isoglariducris folius were in April (50%) and in autumn (September 42%, October 37%, November 73% and December 100%). Low incidences of infection were found during the summer months (May IS%, June 14%, July 17% and August 11 %). Experimental infections of potential annelid intermediate hosts were attempted but all failed. Isoglaridacris longus Fredrickson and Ulmer, 1965 This cestode was investigated from Moxostomu mucrolepidotum in the border area of Iowa and South Dakota, U.S.A., by Fredrickson and Ulmer (1965). The fishes were sampled April to December, but not January to March, the time of ice cover. Incidence was high April (83%), declined May (67%) through to a minimum in August (8%) to rise again September (23%), October (50 %) and November (28 %). Two fishes captured December were both infected. Immature worms were present in all months in which field samples were obtained. Gravid I . longus were first found late April, but also during May to July and September to November. The failure to find gravid cestodes in August was considered to be associated with the decline in worm numbers during the late summer months. At room temperatures fully developed oncospheres were obtained in 21 days, but older annelids could not be experimentally infected (Fredrickson and Ulmer, 1965). Isoglariducris wisconsinensis Williams, 1977 This species occurred in Hypentelium mgricuns and was studied at Red Cedar River, Wisconsin, U.S.A., from June 1977 to August 1978 by Williams (1979a). During this time water temperatures ranged from 0-5 to 24.6"C. Three stages of maturation were identified: immature, lacking one or more reproductive organs; mature. all these organs present; and gravid with eggs. Increased incidences were seen in spring and autumn, with decreased incidences in July and February. A pattern ofincreasing length of I. wisconsinensis was found until June, then decreasing to October. Few immature and mature cestodes were found, but gravid worms were obtained in all months. An annual cycle was postulated by Williams (1979a), with recruitment from spring continuing until the onset of winter. The low incidence during winter was related to decreased feeding levels of the H . nigricans; little or no food was found in their stomachs. The increased level of feeding in the spring could have accoiinted for the increased incidence at that time, however other factors,

H E L M I N T H S I N F R E S H W A T E R FISHES

25

host hormones at spawning time or rising water temperatures might also have been involved. The increased incidences spring and autumn occurred at water temperatures of around 12"C, with the low summer incidences at water temperatures 18°C and above. However the temperature dependent factor did not explain the increase of immature cestodes during summer according to Williams (1979a). The gravid isoglaridacris wisconsinensis seen during the winter by Williams (1979a) possessed numerous ova, but these lacked egg shells, suggesting that the lower water temperatures adversely influenced the worm reproduction. Monobothrium hunteri Mackiewicz, 1963 Mackiewicz(1963) reported incidences in Catostomus coinmersoni in central New York State, U.S.A., in October, December-February and AprilAugust, with gravid worms in February, July and August. More information was presented by Calentine and Fredrickson (1965) from the same host in the Iowa River, Iowa, U.S.A. Immature worms were not found in the fishes until late spring or early summer. Gravid worms occurred May to July, but were maximal in May. In nature eggs were probably deposited during June to August. Limnodrilus hofmeisteri served as the intermediate host (Calentine, 1965b; Calentine and Fredrickson, 1965). Embryonation needed 18 days and procercoid development around 50 days at laboratory temperatures. All the larvae were preserved by 75 days, hence the duration of life of the annelid infection by procercoids was not established (Calentine and Fredrickson, 1965). It was suggested that C. cominersoni could acquire invasions of M. hunteri by late autumn, although immature stages in the fishes were not recovered until late spring. However, in the annelid intermediate host in nature these procercoids were present in every month of the year, but were common only in the autumn. Approximately 9 % of all caryophyllaeid larvae recovered from L. hofmeisteri were M . hunteri. The high incidence of annelid infection compared with the low incidence of fish infection was somewhat surprising, but M . hunteri appeared to be absent from C. commersoni when Glaridacris catostomi was present (Calentine and Fredrickson, 1965). Monobothrium ingens Hunter, 1927 Calentine (1965b) determined that the intermediate host was Limnodrilus hojkeisteri; development at laboratory temperatures needed about 45 days. Monobothrium ulmeri Calentine and Mackiewicz, 1966 This species was studied by Grimes and Miller (1973, 1976) in Erimyzon obfongus a t Lake Raleigh, North Carolina, U.S.A. Seven length classes and three maturity groups, immature, mature but no eggs in uterus, and gravid were separated by Grimes and Miller (1976). A distinct seasonal periodicity in incidence and mean intensity, with an infection period of eight months, December to July, was found. Following a January low, incidence increased sharply to a peak in April and then declined. Mean intensities were relatively high and stable between February to June, with the intensity of immature worms heaviest in February and March. Gravid worms were first recovered in January, and then, with the exception of March, were found throughout the remainder of the infection period until July. Most gravid worms were longer

26

JAMES C . C H U B B

than 15 mm (Grimes and Miller, 1976). A seasonal relationship with host sex was postulated for Monobothrium ulmeri. Male fishes had higher mean intensities of infection February to May, but the female Erimyzon oblongus acquired a progressively higher intensity from March through May, and by June, 1972 had surpassed that of the males. Maturation was also related to host sex. Gravid worms in January and February 1972 were recovered from male fishes only, even though nearly twice as many female hosts were examined. In April gravid worms were first discovered in female fishes, and from April to July 368 gravid worms were found in females as compared with 305 from males. Grimes and Miller (1976) saw a relationship between the mean intensities and occurrence of gravid M . ulmeri and the growth of the secondary sexual characteristic of tubercles on the snout and fins of male E. oblongus, and the development of the testes and ovaries of the fishes during the winter and early spring. However, although a parallel sexual development of host and parasite occurred, the host sexual changes may not necessarily have had a causal influence on the parasites. Monobothrium wageneri Nybelin, 1922 Komarova (1957) recorded this species from Tincu tincu in the River Donets, U.S.S.R., in April 1952 and July 1953, but not in April 1953, July 1952, October 1952, 1953 nor December 1952, 1953. At Lake Druino, Poland, Kozicka (1959) noted the highest incidence and intensity in T. tinca in spring, but also found Monobothrium wageneri during summer and autumn. Penarchigetes species undetermined Grimes and Miller (1973, 1976) found this species in Erimyzon oblongus in Lake Raleigh, North Carolina, U.S.A. It was recovered in every month sampled, with a higher incidence during the warmer months, May through September, but a definite seasonal periodicity was not indicated. The mean intensity was low, again without distinct seasonal trend. Immature and gravid worms were found in all months sampled except July 1971. The monthly mean intensities for the three maturity groups, immature, mature with no eggs in the uterus, and gravid, were generally similar (Grimes and Miller, 1976).

(b) Family Lytocestidae Atractolytocestus huronensis Anthony, 1958 Anthony (1958) collected Cyprinus carpio from the summer of 1950 until the autumn of 1951 in the Geddes Lake area of the Huron River, Michigan, U.S.A. No evidence for seasonality of Atractolytocestus huronensis was provided. At room temperatures the eggs developed to give an embryo usually in 7 to 10 days. In refrigerated conditions no development occurred and the eggs died in 10 to 14 days. Jones and Mackiewicz (1969) at the Tennessee River, Tennessee, collected A . huronensis in autumn, winter and spring for chromosome studies. All the cestodes collected were young to mature, with no evidence of senescence. Caryophyllaeides fennica (Schneider, 1902) Small amounts of seasonal data for Caryophyllaeides fennica can be found

H E L M I N T H S IN F R E S H W A T E R FISHES

27

in the following papers; hosts and localities are listed in Table I: Cernova (1975), Izyumova (1959a, 1960), Kakacheva-Avramova (1973, 1977), Kashkovski (1967), Komarova (1964), Kozicka (1959) and Marits and Vladimirov (1969). In the British Isles, Chubb (1961) found Caryophyllaeides fennica in Rutilus rutilus at Llyn Tegid, Wales in all months of the year except January. The incidence varied irregularly between 9 to 45 % and the mean intensity per infected fish between 1.0 and 3.3. The smallest worm seen was 1.4 mm long relaxed. Young worms were present March, May, June, September and October. Genitalia appeared at a length of 3 to 4 mm, maturing worms, without eggs, measured 6 to 10 mm and eggs were present in all worms 10 to 25 mm in length. Gravid worms occurred in all months except January (no worms at all) and August. Mishra (1966) investigated R. rutilus at the Shropshire Union Canal, Cheshire, England. Here too an irregular incidence and intensity of occurrence of C. fennica was seen, without obvious pattern, although much lower overall in the canal (2-9 %) than Llyn Tegid (9-45 %). Worms with eggs were seen in all months when infections were present. Egg production commenced when worms reached about 10 mm (relaxed length), and a maximum length of 33 mm was noted in May. At the River Lugg, Herefordshire, England, Davies (1967) reported C.fennica in Leuciscus cephalus, L. leuciscus and R. rutilus. Incidence was low in all three host species, but in total, C.fennica was present all year, without regular seasonal patterns of occurrence. Five stages of maturation were separated: I, no genitalia present; 11, genitalia appearing ; 111, genitalia fully developed ; IV, egg production just commencing; and V, many eggs present. In all three hosts Stage V was commonest, although not present in January and March. Stage I1 worms were present each month from August to December in L. cephalus. Recruitment was postulated to occur especially during August to December, but Davies (1966) was unable to determine the life span of the worms in the fish hosts. Studies by Borgstrom and Halvorsen (1968) at Lake Bogstad in Norway showed that Caryophyllaeides fennica occurred in Rutilus rutilus in May, June, August and November, but no worms were found in January, February, April or July. C. fennica with eggs were found in June and August only. Borgstrom and Halvorsen (1968) suggested that the water temperatures in Lake Bogstad limited egg production to June to August, but worms might be present in R. rutilus all year. Malakhova (1961), in the colder conditions of Lake Konche, Karelia, U.S.S.R., also found C. fennica in R. rutilus at all seasons of the year. At Lake Skadar, Yugoslavia, KaiiC (1 970) reported Caryophyllaeides fennica in Rutilus rubilio as: immature, April to June, none other months; mature January, April to peak May, falling through June to July. None found August to December. A similar pattern was seen in Leuciscus cephalus albus. Alvarez Pellitero et al. (1978a) also noted a well-defined annual cycle of one generation per annum in cyprinids of the rivers in the Duero and Sil basins of north west Spain.

TABLEI Studies on seasonal occurrence of cestodes of the orders Amphilinidea and Caryophyllidea listed in the climate zones of the World (see map Fig. 1, Chubb, 1977). (The species are in alphabetical order.) Climate zones

Cestode species

Host species

1. Tropical la. RAINY (humid climate)

Locality

References

tropical forest Lytocestus lativitellarium

Clarias batrachus

Lytocestus parvulus

Clarias batrachus

paddy fields, Sungei Furtado and Tan Besar, Sabak Bernam, (1973) Malaysia paddy fields, Sungei Furtado and Tan Besar, Sabak Bernam, (1973) Malaysia tropical grassland

Lytocestus indicus

Clarias batrachus

Raipur, India

no seasonal studies

tropical highland

no seasonal studies

hot semi-desert

no seasonal studies

hot desert

1b. SAVANNA (humid climate)

lc. HIGHLAND (humid climate) Id. SEMI-DESERT (dry climate) le. DESERT (dry climate) 2. Sub-tropical 2a. MEDITERRANEAN Caryophyllaeides fennica

Rutilus rutilus Leuciscus cephalus albus Rutilus rutilus

Satpute and Agarwal (1974)

scrub, woodland, olive Lake Paleostomi, Cernova (1975) Georgia, USSR Lake Skadar, KaiiC (1970) Yugoslavia

Caryophyllaeus Iaticep.7

Cyprinus carpio

2b. HUMID Biacetabulum meridianum Carpiodes carpio Glaridacris confusus

3. Mid-latitude 3ai. HUMID WARM SUMMERS

Carpiodes carpio

Lake Skadar, Yugoslavia deciduous forest Lake Texoma, Oklahoma, USA Lake Texoma, Oklahoma, USA

temperate grassland, mixed forest River Danube, Acipenser ruthenus Amphilina foliacea Bulgaria Dubossary Water Archigetes brachyurus Vimba vimba vimba Reservoir, Moldavia, natio carinata USSR Archigetes sieboldi Gobio gobio Central and Eastern Balkan Mountains, Bulgaria Abramis brama Western Ukraine, Tinca tinca USSR Biacetabulum meridianum Erimyzon oblongus Lake Raleigh, North Carolina, USA Caryophyllaeides fennica Barbus meridionalispetenyi Central and Eastern Leuciscus cephalus Balkan mountains, Phoxinus phoxinus Vimba vimba tenella 8 species of Cyprinidae Vimba vimba vimba natio carinata

Kaiic (1970) Self and Timmons (1955) Self and Timmons (1955)

Kakacheva-Avramova (1977) Marits and Vladimirov (1969) Kakacheva-Avramova (1973) Kulakovskaya (1962a, b, 1964) Grimes and Miller (1973, 1976) Kakacheva-Avramova (1973)

River Danube, Bulgaria Kakacheva-Avramova (1977) Dubossary Reservoir, Marits and Vladimirov Moldavia, USSR (1969)

w

TABLEI (continued) Climate zones

Cestode species

Host species

Locality

References

3ai. (continued)

Caryophyllaeusbrachycollis Leuciscus cephalus Vimba vimba tenella Caryophyllaeusfimbriceps Cyprinus carpio Caryophyllaeus laticeps Abramis brama Abramis sapa Vimba vimba vimba natio carinata Abramis brama Vimba vimba vimba natio carinata Abramis brama Abramis brama Carassius carassius Cyprinus carpio Rutilus rutilus Cyprinus carpio Cyprinidae Cyprinidae, 8 species Cyprinus carpio Leuciscus cephalus Khawia sinensis

Cyprinus carpio

Central and Eastern Kakacheva-Avrarnova Balkan Mountains, (1973) Bulgaria Ivasik (1952, 1953) Fish ponds, Ukraine River Danube, Bulgaria Kakacheva-Avrarnova (1977) Dubossary Reservoir, Moldavia, USSR Dubossary Reservoir, Moldavia, USSR Lake Kals, Latvia, USSR near Warsaw, Poland

Marits and Tomnatik (1971) Marits and Vladirnirov (1969) Reinsone (1955)

Germany Poland Pod6brad y, Czechoslovakia Germany (now Poland) Lake Lkman (Geneva), Switzerland Western Ukraine, USSR

Scheuring (1929) Sekutowicz (1932, 1934) Srgrnek (1901)

Ruszkowski (1926)

Wunder (1939) Zschokke (1884) Kulakovskaya (1964a)

Cyprinus carpio Monobothrium ulmeri

Erimyzon oblongus

Penarchigetes sp.

Erimyzon oblongus

Archigetes iowensis

Cyprinus carpio

Archigetes sieboldi

Cyprinus carpio

A tractolytocestus huronensis

Cyprinus carpio

Biacetabulum carpiodi

Carpiodes cyprinus

Biacetabulum infrequens

Moxostoma anisurum Moxostoma erythrurum Catostomus commersoni

3aii. HUMID COOL SUMMERS

Biacetabulum macrocephalum Caryophyllaeides fennica

Rutilus rutilus Blicca bjoerkna

L'vov region, Ukraine, Kulakovskaya et al. USSR (1965) Grimes and Miller Lake Raleigh, North Carolina, USA (1973, 1976) Lake Raleigh, North Grimes and Miller Carolina, USA (1973, 1976) temperate grassland, mixed forest Calentine (1962, 1964) Iowa River, Iowa, USA Calentine and Ulmer (1961a) impounded waters, Calentine and De Long Kinnickinnic River, (1966) Wisconsin, USA Geddes Lake area, Anthony (1958) Huron River, Michigan, USA various Wisconsin, Iowa Williams and Ulmer (mostly) and Nebraska (1970) habitats, USA Iowa River, Iowa, Calentine (1965a) USA Iowa River, Iowa, Calentine (1965a) USA Calentine and Fredrickson (1965) Rybinsk Reservoir, Izyumova (1959a) USSR Rybinsk Reservoir, Izyumova (1960) USSR

w

TABLEI (continued) Climate zones

Cestode species

Host species

w

h,

Locality

References

3aii. (continued) Caryophyllaeus fimbriceps Cyprinus carpio Cyprirzus carpio Caryophyllaeus laticeps

Abramis brama Abramis brama Rutilus rutilus Abramis ballerus Blicca bjoerkna Abramis brama Abramis brama Abramis brama

Glaridacris catostomi

Catostomus commersoni Catostomus commersoni Catostomus commersoni

Glaridacris laruei

Catostornus commersoni

Fish ponds, Leningrad, Bauer (1957) Velikic and Novogorod " districts, USSR Kalinin and Moscow Kanaev (1956) districts, USSR River Volga, USSR Bogdanova (1958, 1959) Rybinsk Reservoir, Izyumova (1958, 1959b) USSR Rybinsk Reservoir, Izyumova (1959a, b) USSR Rybinsk Reservoir, Izyumova (1959b, 1960) USSR Kuybyshev Reservoir, Lyubarskaya (1965, USSR 1970) Lake Malaren, Sweden Milbrink (1975) Ivan'kovsky Reservoir, Strizhak (1971) USSR Lake Michigan, USA Amin (1977) Iowa River, Iowa, USA Calentine and Fredrickson (1965) Red Cedar River, Williams (1979b) Wisconsin, USA Williams (1979b) Red Cedar River, Wisconsin, USA

Hunterella nodulosa

Catostomus commersoni

Isoglaridacris bulbocirrus

Catostomus commersoni

Isoglaridacrisfolius

Moxostoma erythrurum

Isoglaridacris longus

Moxostoma macrolepidotum Hypentelium nigricans

Isoglaridacris Wisconsinensis Khawia iowensis Khawia sinensis

Cyprinus carpio Cyprinus carpio Cyprinus carpio

Monobothrium hunteri

Catostomus commersoni

Monobothrium wageneri Spartoides wardi

Tinca tinca Carpiodes carpiodes Carpiodes cyprinus Carpiodesforbesi Carpiodes velifer

Glaridacris catostomi

Catostomus commersoni

3aiii. EAST COAST

Catostomus commersoni Glaridacris laruei

Catostomus commersoni

Iowa River, Iowa, USA Calentine and Fredrickson (1965) Iowa River, Iowa, USA Calentine and Fredrickson (1965) borders Iowa and South Fredrickson and Ulmer Dakota, USA (1965) borders Iowa and South Fredrickson and Ulmer (1 965) Dakota, USA Red Cedar River, Williams (1979a) Wisconsin, USA Iowa River, Little Sioux Calentine and Ulmer River, Iowa, USA (1961b) Central regions, Musselius et al. USSR (1 963) Moscow region, USSR Sapozhnikov (1970, 1972) Iowa River, Iowa, USA Calentine and Fredrickson (1965) River Donets, USSR Komarova (1957) various localities, Williams and Ulmer (1 970) Iowa (mostly), Nebraska and Wisconsin, USA temperate grassland, mixed forest Pushaw Lake, Maine, Lawrence (1970) USA Central New York Mackiewicz (1965b) State, USA Pushaw Lake, Maine, Lawrence (1970) USA

w w

TABLE I (continued) Climate zones

Cestode species

Host species

w

Locality

References

Central New York State, USA Pushaw Lake, Maine, USA Gunma Prefecture, Japan Central New York State, USA temperate grasslands, deciduous forest River Sil basin, Spain

Mackiewicz and McCrae (1962) Lawrence (1970)

3aiii. (continued) Hunterella nodulosa

Catostomus commersoni

Isoglaridacris bulbocirrus

Catostomus commersoni

Khawia sinensis

Cyprinus carpi0

Monobothrium hunteri

Catostomus commersoni

Archigetes sieboldi

Cyprinidae especially Barbus barbus bocagei Albramis brama Phoxinus phoxinus Blicca bjoerkna Cyprinidae

3b. MARINE WEST COAST

Caryophyllaeidesfennica

Rutilus rutilus Rutilus rutilus Leuciscus cephalus Leuciscus leuciscus Rutilus rutilus Abramis brama Blicca bjoerkna

Varmland, Sweden Goteborg, Sweden Lake Dqbie, Poland River Sil basin, Spain

Nakajima and Egusa (1977f) Mackiewicz (1 963)

Alvarez Pellitero el al. (1978a, b) Nybelin (1962)

Wierzbicka, J. (1978) Alvarez Pellitero et al. (1978a, b) Bogstad Lake, Norway Borgstrom and Halvorsen (1968) Llyn Tegid, Wales Chubb (1961) River Lugg, Davies (1967) Herefordshire, England Lake Druzno, Poland Kozicka (1959)

Rutilus rutilus Caryophyllaeus laticeps

Cyprinidae Abramis brama Leuciscus cephalus Leuciscus leuciscus Rutilus rutilus Abramis brama Leuciscus leuciscus Abramis brama Blicca bjoerkna Tinca tinca Rutilus rutilus

Khawia species Monobothrium wageneri

Abramis brama Abramis ballerus Blicca bjoerkna Cyprinidae, especially Barbus barbus bocagei Tinca tinca

3 ~ SEMI-DESERT . Amphilina foliacea

Acipenser guldenstadti Acipenser ruthenus Acipenser stellatus Huso huso

Shropshire Union Canal, Cheshire, England River Sil basin, Spain gravel pit, near Dagenham, Essex, England River Lugg, Herefordshire, England River Glomma, Norway River Avon, Hampshire England Lake Druzno, Poland Shropshire Union Canal, Cheshire England Lake Dqbie, Poland River Sil basin, Spain Lake Druzno, Poland prairie and steppe Lower Volga Basin, USSR

Mishra (1966) Alvarez Pellitero et al. (1978a, b) Anderson (1974a, b, 1976a, b) Davies (1967) Halvorsen (1972) Kennedy (1968, 1969a, b, 1972a, c) Kozicka (1959) Mishra (1966) Wierzbicka (1978) Alvarez Pellitero et al. (1 978a, b) Kozicka (1959) Dubinina (1974) w

VI

TABLEI (continued) Climate zones

Cestode species

Host species

w

Q\

Locality

References

3c. (continued) Acipenser ruthenus Archigetes sieboldi Caryophyllaeidesfennica

Cyprinidae especially Barbus barbus bocagei Cyprinidae Rutilus rutilus

Abramis brama Blicca bjoerkna Rutilus rutilus heckeli Caryophyllaeusfimbriceps Abramis brama Cyprinus carpio Abramis brama Caryophyllaeus laticeps Cyprinidae Abramis brama Abramis ballerus Blicca bjoerkna Cyprinus carpio Abramis brama Abramis brama Blicca bjoerkna

River Volga, Saratov, USSR River Duero basin, Spain River Duero basin, Spain Iriklin Reservoir, USSR Dnepr Delta, USSR

Janicki (1928)

Volga Delta, USSR

Dubinina (1949, 1950)

Dnepr Delta, USSR River Duero basin, Spain Volga Delta, Caspian Sea, USSR

Komarova (1964) Alvarez Pellitero et al. (1978a, b) Dogie1 and Bykhovskii (1939)

Volga Delta, USSR Dnepr Delta, USSR

Dubinina (1949, 1950) Komarova (1964)

Alvarez Pellitero et al. (1978a, b) Alvarez Pellitero et al. (1978a, b) Kashkovski (1967) Komarova (1964)

Rutilus rutilus heckeli Vimba vimba vimba natio carinata Abramis brama Hunterella nodulosa

Catostomus commersoni Catostomus commersoni

Khawia species

Cyprinidae, especially Barbus barbus bocagei no seasonal studies

Caryophyllaeides fennica

Rutilus rutilus

3d. DESERT 3e. SUB-POLAR 4. Polar 4a. POLAR 4b. ICE-CAPS

no seasonal studies no suitable habitats for freshwater cestodes

5. Mountain Khawia armeniaca

Varicorhinus capoeta sevangi

Volga-Don Canal, USSR near Fort Collins, Colorado, USA Nose Creek, Bow River Alberta, Canada River Duero basin, Spain cool desert coniferous forest Lake Konche, Karelia, USSR

Kosareva (1959) Mackiewicz and McCrae (1962) Mudry and Arai (1973) Alvarez Pellitero et al. (1978a, b) Malakhova (1961)

tundra icefields and glaciers heath, rocks and scree Lake Swan, Armenia, USSR

Begoyan (1977)

38

JAMES C . CHUBB

Khawia armeniaca (Cholodkowsky, 1915) Khawia armeniaca occurred in Varicorhinus capoeta sevangi, a fish endemic to Lake Sevan, Armenia, U.S.S.R., during all months of the year (Begoyan, 1977). It was concluded that there was an annual cycle of development of K. armeniaca. The main invasion of the fishes by procercoids from oligochaetes was considered to occur spring, to give sexually mature K. armeniaca before autumn. A less significant invasion summer to winter, up to November and December, overwintered to provide sexually mature cestodes in May (Begoyan, 1977). Khawia iowensis Calentine and Ulmer, 1961 The information presented for this species of caryophyllaeid is from Cyprinus carpio in two localities (Calentine and Ulmer, 1961b). Collection data from the Iowa River, Iowa, U.S.A., tended to indicate that C. carpio acquired their heaviest infections in late summer (August) and early autumn (September). Gravid cestodes were recovered only occasionally from April through August in this habitat, with the majority gravid in late autumn. However, by contrast, at Little Sioux River, Iowa, U.S.A., gravid worms were found regularly in C. carpio during June to August, 1960 by Calentine and Ulmer (1961b), although in this location too, incidence and intensity of occurrence of K. iowensis increased markedly as the summer progressed. Eggs shed from gravid cestodes produced oncospheres by day 15 at room temperatures but did not hatch. Khawia japonensis (Yamaguti, 1934) Demshin (1978) studied the biology of Khawia japonensis in the intermediate host Limnodrilus udekemianus. At 18-26°C the oncosphere developed in the egg in 12 to 14 days. After ingestion by the oligochaete, the oncosphere emerged, penetrated the intestine wall to enter the body cavity at the caudal end of the oligochaete, thereafter to gradually move forward to reach the 9 to 15th anterior segments and attain full development by 55 to 60 days. The mature procercoids were 1.68 mm long. The adult worms are found in Cyprinus carpio in the Amur region of the U.S.S.R. According to Nakajima and Egusa (1977f) K. japonensis and K. sinensis are distinguished only by the size of their eggs. Khawia sinensis Hsu, 1935 Bauer et al. (1969) summarized the information for this important parasite of Cyprinus carpio. In the U.S.S.R. as a whole, a one year cycle occurred; oviposition from the adult worms was mainly in April and May, the procercoids developing in oligochaetes in 2 to 3 months during the spring and summer. Khawia sinensis overwintered either in the tubificid intermediate or the fish definitive hosts. Much of the above summary was derived from studies carried out in the western Ukraine, U.S.S.R. Kulakovskaya (1962b) showed that the oligochaete intermediate hosts were Limnodrilus ukedemianus, L. hoffmeisteri, Tubifex tubifex and Zlyodrilus hammoniensis. The oncosphere developed prior to but did not hatch until ingestion of the egg by the oligochaete, penetrated to the body cavity through the intestine wall and there at laboratory temperatures

HELMINTHS I N FRESHWATER FISHES

39

reached full development of the procercoid in 30 to 32 days. According to Kulakovskaya (1964a) the procercoids lived no longer than 2 to 3 months in the oligochaetes, and formed their reproductive organs in the fish hosts where they occurred for 5 to 6 months. Khawia sinensis was introduced into the Ukraine and successfully competed with Caryophyllaeus jimbriceps, the indigenous species, replacing it in Cyprinus carpio in certain regions. Kulakovskaya (1964b) considered that part of the explanation for this was the wider spectrum of intermediate hosts utilized by K. sinensis and its ability to overwinter in fishes. In fish farms in the L'vov Region, Ukraine, K. sinensis adults occurred mainly in May and June (Kulakovskaya et al., 1965). Also in the L'vov Region, Kupchinskaya (1969, 1972) showed that the infection of Tubificidae by caryophyllaeid procercoids occurred in fish farms in wintering and fattening ponds, as well as the water channels. Details were provided in Kupchinskaya (1969), but in summary, procercoids were present throughout the year. Invasion of Tubificidae by Khawia sinensis procercoids commenced in May, to peak in July and August. Young tubificids were more easily invaded than older worms (Kupchinskaya, 1972). In other parts of the U.S.S.R. some additional investigations have been carried out. In the Central regions, Musselius et al. (1 963) showed that rate of infection of Cyprinus carpio in fish farms increased up to June, but the incidence had fallen sharply by late August. In the Moscow district Sapozhnikov (1970) found that invasion of young-of-the-year C. carpio commenced July to August, with a maximal incidence achieved by October. However, in older fishes, 2 and 3 years plus, the highest incidences occurred in May and June. At the end of the summer a massive loss of the adult cestodes took place, although some were able to overwinter in the fish intestines. Further information was given by Sapozhnikov (1972). Ilyodrilus templetoni was reported as an additional intermediate host; 16.6% were infected, with an invasive potential of 40 %. In experimental infections of C. carpio in summer water conditions the K. sinensis were shown to reach maturity 15 days after establishment, and to be lost from the fish intestine 25 days later. However, K. sinensis overwintering in the C. carpio could remain in the fish intestine for 6+ to 74 months, but they showed marked indications of degeneration during the second part of the winter. Korting (1975a) reviewed the distribution of Khawia sinensis in Europe; seasonality of caryophyllaeids and other cestodes in fishes was indicated. Some notes on the seasonal occurrence of Khawia sinensis in Japan were provided by Nakajima and Egusa (1977f). At an irrigation pond farm in Gunma Prefecture, Cyprinus carpio six months old were examined monthly from November to May. The occurrences were: 3 November 12-1%, range 5-12 worms (water temperature 154°C); 20 November 5 2 % , 1-2 worms (10.5"C); 19 December 3*4%, 1 worm (1.2"C); thereafter no K. sinensis were found. In this instance it is clear that overwintering of the cestodes did not occur in young C. carpio. Khawia species undertermined Alvarez Pellitero et al. (1978a) noted a well-defined seasonal cycle of

40

JAMES C. C H U B B

incidence, intensity and maturation with one generation per annum in cyprinids, especially Burbus barbus bocagei in the River Duero and Sil basins, Spain. Lytocestus indicus (Moghe, 1925) The occurrence of Lytocestus indicus in Clarias batrachus in six water tanks at Raipur, India was studied over a two year period (Satpute and Agarwal, 1974). Incidence was high during February to August, with a peak in JuneJuly, and low during September to November in both years. Mostly immature worms were recovered from fishes examined during September to November. About 50 % of the cestodes were mature during December, 75 % from January to March, and most were mature (presumably gravid) during April to July. In the second August around 50% of the L. indicus were immature again. Lytocestus lativitellarittm Furtado and Tan, 1973 Furtado and Tan (1973) examined Clarias batrachus from paddyfields, Sungei Besar, Sabak Bernam, Malaysia. In this area the months JanuaryFebruary and July-August were drier, and the periods March to June and September to December wet seasons. The incidence of L. lativitellurium was low in the dominant dry season January-February, increased gradually from May to a maximum in August to November, the dominant wet period. The increase was thought by Furtado and Tan (1973) to perhaps be related to the wetter season, probably dependent on a change in the composition of the host diet. Lynsdale (1956) suggested that tubificids or entomostracans might be the intermediate hosts of Lytocestus species. Lytocestus parvulus Furtado, 1963 Also studied by Furtado and Tan (1973) from Clurias batrachus in paddyfields, Sungei Besar, Sabak Bernam, Malaysia. The overall incidence was similar to that of L. lutivitellarium noted above. (c) Family Capingentidae Spartoides wardi Hunter, 1929 Williams and Ulmer (1970) found Spartoides wardi in Carpiodes curpiodes, C. cyprinus, C .forbesi and C. velifer from a variety of habitats in Iowa (mostly), Nebraska and Wisconsin, U.S.A. The cestode appeared to lack a definite seasonal periodicity, having been present in collections throughout 1968. Immature, mature and gravid worms were usually present whenever samples were taken. (d) Caryophyllideans undetermined Fried et al. (1964) examined Catostomus commersoni from Bushkill Creek, Pennsylvania, U.S.A., and reported undetermined caryophyllideans in May and October to December. The worm burden appeared the same, spring and autumn. 3. Order Spathebothridea

(a) Family Cyathocephalidae Cyathocephalus truncatus (Pallas, 1781) The morphology of Cyathocephalus truncatus was studied in detail by

H E L M I N T H S I N F R E S H W A T E R FISHES

41

WiSniewski (1933b) and the life cycle by Wisniewski (1932a, b, 1933a). The eggs developed in the fish faeces, but not in pure water, to produce the oncospheres which were devoid of cilia, embryonic hooks or penetration glands. If swallowed by a species of gammarid, the embryonated eggs hatched and the oncospheres penetrated the body cavity, but only in young host individuals. Procercoids were formed containing fully developed gonads. On ingestion by a fish the mature cestodes established in the intestine, genetically representing the plerocercoid stage, and thus demonstrating the phenomenon of neoteny according to WiSniewski (1932a, 1933a). Freeman (1973) recommended the names “caudate adult” to correspond with the sexually mature procercoids in the gammarid, and “acaudate adult” for the stage in the fishes intestines. Most of the seasonal information for Cyathocephalus truncatus originates from Europe. Zschokke (1884) gave a few brief notes, but Wolf (1906) provided rather fuller but still incomplete seasonal information, which suggested that the infection was similar through the year. Vik (1954) in Salmo trutta and Salvelinus alpinus from the Anaya water system, Trmdelag, Norway, collected material from May to November, and noted no differences in incidence. At Hallingdalselva Vik (1958) saw no great changes in incidence in S. trutta during winter and spring. Some S. trutta were infected on 9 January at 8”C, eggs appeared in the faeces ten days later, and some C. truncatus remained in the fishes for 55 days. Although Senk (1952) had studied the occurrence of Cyathocephalus truncatus in Gammarus in the River Bosna, Yugoslavia, from source to mouth, and had found infected Gammarus in all months of the year, with incidences between 2-5 and 12.7%, it was Awachie (1963a, 1966a) who first combined a study of the seasonality of occurrence of the stages in both Gammarus pulex and Salmo trutta, at the Afon Terrig, Wales. In this stream water temperatures were minimal in January (2°C) and maximal in August (14.5”C). The incidence of larval C. truncatus in G.puZex was low, and the early stages (fruhprocercoidstadien) of WiSniewski (1933a) were not found. However the later forms (mittel- and reifeprocercoidstadien) occurred between September (0.08 %) and April (0.08 %), with a maximal incidence found in January (0.33 %). No infected G. pulex were found May to August. In S. trutta cestodes at all stages of development were found in the pyloric caeca. Incidence was high November to April (maximal February 52.4 %), to fall May to August, with none in September. Intensity tended to follow the trends of incidence. In October to November the C. truncatus were recently established and immature, but from March to July they contained eggs in the uteri. Awachie (1966a) concluded that there was a definite annual cycle in the Afon Terrig, with recruitment to the fishes in late autumn, maturation of the cestodes in late winter and early spring, and a disappearance of the worms by late summer. Water temperature was invoked by Awachie (1966a) to explain the cycle. Establishment in S. trutta occurred when the temperature fell below 9°C (October onward), and worms were lost, as shown by a sharp’drop in incidence and intensity of infection the following May, at which time the

42

JAMES C . C H U B B

water temperature rose above 10°C. At the nearby River Alyn, Wales, Rahim (1974) also found C. truncatus in S. trutta, from January (41 % incidence) to May (27 :d), to disappear after July (4 %). In the mountains of Norway, at Lake Melingen, VAgB and Lake Nedre Fipling, Vefsn, Halvorsen and Macdonald (1972) sampled S. trutta between June to October. The lakes were ice covered otherwise. In both lakes incidences were highest in June, and intensities in June or July, and lowest in August. In August the frequency of unattached adult C. truncatus was maximal, suggesting a loss of worms at that time. It may be speculated that the summer rise in water temperatures at these Norwegian lakes caused the loss of C. truncatus during August. Paggi et al. (1978) briefly reported seasonal patterns of occurrence of Cyathocephalus truncatus in Salmo trutta and three gammarid species, in the River Trino, L’Aquila, Italy. No details were provided in this preliminary publication. In the U.S.S.R. Malakhova (1961) at Lake Konche, Karelia, found highest incidences of Cyathocephalus truncatus in Lota Iota during the winter (17 %) and spring (16.2%), falling summer (9.6%) to autumn (4.8%), with a maximum intensity (mean 3.7, 1-1 1) in winter. The gammarid intermediates in the U.S.S.R. were listed by Bauer et al. (1 969) and included Pallasea quadrispinosa (Bauer and Nikol’skaya, 1952). In Lake Michigan, U.S.A., Amin (1978b) found that Pontoporeia afinis contained C. truncatus larvae, with 10 of 14 containing eggs in the uteri, and at least five had released eggs into the body cavity of the amphipods. DeGuisti and Budd (1959) in Lake Huron, Ontario, Canada, also reported P. afinis to be an intermediate host for C. truncatus, as it was too in Cold Lake, Alberta, Canada, where Leong (1975) examined the seasonal trends of occurrence of the adult cestodes in Coregonus clupeaformis. Unlike in Europe, Leong (1975) observed two peaks of abundance of Cyathocephalus truncatus, one in winter (maximum intensity January and February), and a second in summer (July in fishes aged VII and VIII). As Larkin (1948) had shown that Pontoporeia afinis young were born in winter and could survive for more than two years Leong (1975) suggested that the availability of this intermediate host did not seem to be a major factor in producing observed seasonal patterns in the fishes. He speculated that a reduction in resistance of the host fishes at low water temperatures might explain the winter peak abundance of C. truncatus in Coregonus clupeaformis. 4. Order Pseudophyllidea (a) Family Bothriocephalidae Bothriocephalzis achedognathi Yamaguti, 1934 Synonyms of this species are Bothriocephalus fluviatilis Yamaguti, 1952, B. gowkongensis Yeh, 1955, B. opsariichthydis Yamaguti, 1934 (=B. opsalichthydis) and B-phoxini Molnar, 1968. Yeh (1955) had separated B. gowkongensis from B. opsariichthydis owing to the fact that the eggs of the former were embryonated on release, whereas those of the latter were not, however Liao and Shih (1956) showed that the state of development of the eggs of

H E L M I N T H S I N F R E S H W A T E R FISHES

43

B. gowkongensis at release changed through the seasons. None-the-less, the name B. gowkongensis was most commonly used until about 1978. Korting (1975b) proposed that as B. opsariichthydis was considered a synonym of B. acheilognathi by Yeh (1955) and Yamaguti (1959), and if B. opsariichthydis and B. gowkongensis were also the same species, then the name B. acheilognathi should have priority. Molnhr (1977) demonstrated by experiment that B. phoxini and B. gowkongensis were indeed one species and supported the proposal of Korting (1975b) that B. acheilognathi should replace the name B. gowkongensis. Nakajima and Egusa (1974) use the name B. opsariichthydis for their cestodes from Japan. An account of the introduction of B. acheilognathi (as B. gowkongensis) from the River Amur and China, where it occurs naturally, into the Ukraine and other parts of the U.S.S.R., where it is now a potentially dangerous pathogen of cyprinid fishes, of frequent occurrence in fish farms, can be found in Bauer and Hoffman (1976). Subsequently B. acheilognathi has spread to many other countries, especially with acclimatized Ctenopharyngodon idella. A comprehensive study of the life cycle and seasonal dynamics of Bothriocephalus acheilognathi (as B. gowkongensis) was provided by Liao and Shih (1956) from Ctenopharyngodon idella in Kwangtung Province, China. In winter infections in 30 fish farm ponds in 1954 the incidence of infection varied from 20 % to 100 %, average 65 %. The highest intensity seen in a single fish was 467 worms. The eggs of B. acheilognathi when laid were partly segmented or fully embryonated, the proportions of each varied with season : November to February (water temperature 14-21°C) only 2 % embryonated; April to October (2429°C) up to 89% fully embryonated at release. The water temperature markedly influenced the rate of development of the eggs. At 28-30°C 77 % hatched in the first day after release, the remainder during the following five days. Below 25°C the hatching was more irregular. At 1415°C the incubation period ranged from 10 to 28 days. Little hatching occurred below 12°C and none above 37°C. Mesocyclops leuckarti, Thermocyclops taihokuensis and Ectocyclops phaleratus medius were readily infected on ingestion of the coracidia. Mature procercoids were obtained in about 21 days at 1@C, five days at 20°C and four days at 25 to 33°C. Longevity of the infected cyclopoids was a maximum of 49 days at 16.2"C (average water temperature December to January), 35 days at 20.5"C (March to April) and 1f to 18 days at 29-31°C (July to November) (Liao and Shih, 1956). The procercoids were ingested directly by the fishes on eating cyclopoids. Slow growth lasted for nine days, at which time proglottis formation started. A rapid growth then occurred from day 10 to 21, with consequent maturation, so that the first eggs were released between the 21st and 23rd day at 28-29°C (Liao and Shih, 1956). The growth of a population of B. acheilognathi within Ctenopharyrzgodon idella occurred in three phases; establishment, rapid growth, and a period of egg production. C. idella in their first year of life never acquired any immunity,

44

JAMES C . C H U B B

but were subject to reinfections. Large numbers of worms in a single fish inhibited growth and maturation of the cestodes, as well as that of the host. However, a high proportion of the adult worms were found in low intensities of infection and thus achieved maximum growth. When the C. idella reached a length of 100 mm and above the incidence of parasitization by B. acheilognathi declined, so that fishes beyond the one year age group were rarely infected. Accordingly, in C. idella the period between establishment and decline of the population of worms was about one year (Liao and Shih, 1956). In the U.S.S.R. Cyprinus carpio in fish farms are commonly infected by Bothriocephalus acheilognathi. Iskov (1966) provided some seasonal data, whilst Muzykhovskii (1969) has described the seasonal adaptation of this parasite to C. carpio in fish farming conditions. Ctenopharyngodon idella are also affected in the U.S.S.R., and Klenov (1972) found the highest incidence (97.4%) in O+ fishes in July and August. Incidence then fell, although the B. acheilognathi overwintered in the C. idella. In April and May the highest incidences in I+ and II+ fishes were 95 and 100%; incidences fell in July and August, to ascend again to a lesser peak in October (47 and 80 % respectively). Bauer et al. (1969) and Musselius (1973) present a summary of the developmental and other data pertaining to B. acheilognathi (as B. gowkongensis) in fish farms of the U.S.S.R. MolnAr (1968a, b) studied the occurrence of Bothriocephalus acheilognathi (as B. phoxini) in Phoxinusphoxinus in Teich T, Hungary. The water temperature was at 18°C all year and the worms were in the fish host during all months (Molnir, 1968b). However it was unusual to find a long strobila and gravid proglottids in winter. In January the worms normally comprized a scolex and one to ten proglottids. By March growth to a length of 20 to 40 mm had occurred and in April eggs were formed, to occur thereafter in worms 30 to 45 mm long until December. Daniyarov (1975) also investigated the occurrence of B. acheilognathi (as B. gowkongensis) in a spring in Tadzhikistan where the water was again a constant 18-20°C at every season of the year. Here, in Alburnoides bipunctatus eichwuldi, a summer incidence of 23 % had fallen to a zero incidence by autumn. Other seasonal notes about B. acheilognathi (as B. gowkongensis) in Europe can be found in Korting (1975a) and Kakacheva-Avramova (1977) (see Table 11). Korting (1975b) was able to complete the life cycle to young immature worms in Cyprinus carpio in two weeks. In Japan Nakajima and Egusa (1977a) found B. acheilognathi (as B. opsariichthydis) in six-month-old Cyprinus carpio. Some of these fishes were kept in a cage overwinter at 1.2 m depth and examined each month from November 1975 to May 1976. Water temperatures were 15°C in November, falling through NovemberJanuary to a minimum of 0.2T in February, rising to 20°C by May. Incidence was 20.7 % at the beginning of November, falling to 3.4 % by March. Eggs possessed an ability to hatch in November (lO-lS°C) and April and May (16-20°C) but were not present during the period December to March (0*2T-1Z0C). Nakajima and Egusa (1977a) concluded that the life cycle was contiiiued only by the overwintering worms, and not by the egg phase of

HELMINTHS I N FRESHWATER FISHES

45

the life cycle. Earlier, Nakajima and Egusa (1976) had shown experimentally that the embryos in the eggs died rapidly at 2 to 7°C. Experimental studies on Bothriocephalus acheilognathi (as B. gowkongensis) were carried out by Strazhnik and Davydov (1975). The life span at raised temperatures decreased with increasing temperature, in reverse relationship to the metabolism of the worms. Davydov (1978) experimented to determine the growth, development and fecundity of B. acheilognathi (as B. gowkongensis). He established a relationship between the body length and wet weight of the cestodes from hosts of different species and ages. It was established that the most important factors influencing the growth and fecundity of the worms were ambient temperature, the feeding regime, the age and intensity of infection of the host. Temperature was of prime importance to the growth rate and maturation of B. acheilognathi when parasitization was at a low level, whilst the amount of food was of prime importance when population densities were at a high level. In the Ukraine, Davydov (1978) found that the life cycle was completed in 14 to 2 months at 15-22”C, but in 6 to 8 months at low temperatures. In spring (May) immature worms of the new generation were present at the same time as mature worms in both Cyprinus carpio yearlings and two-yearold Ctenopharyngodon idella. By June the immature worms were in the majority but mature individuals of the old population were still present. In C. carpio underyearlings, only immature worms of the new generation occurred at this time. C. carpio were able to acquire invasions of B. acheilognathi from spring through to autumn. In the spring they matured in 30 to 40 days at a length of 30-40 mm. The autumn invasions, however, needed 200 to 300 days to mature at a length of 50-80 mm; thus the autumn generation lived longer than the spring-summer generations. If fishes containing cestodes were transferred from natural winter low temperature conditions to warm conditions in the laboratory they began to grow intensively. A weight of 53 12 mg at 5-7°C increased to 75 f 21 mg in three days at 14-16°C. Davydov (1978) also examined the fecundity of the cestodes. At lYC, from fed fishes, average egg production in 12 days was 17164 & 3120, whereas from an unfed fish it was only 2550 f 830 eggs in 12 days. The egg output was lowered as helminth population density increased: in 12 days one worm 80 mm, 60500; two worms 77 mm average length, 35400-41280; three worms 40 mm average length, 15987 f 1340 each; and five worms 32 mm average length, 4020 f 860 eggs each. B. acheilognathi were larger in fed fishes than in starved hosts; in the latter destrobilation or even total loss of the worms occurred. Bothriocephalus claviceps (Goeze, 1782) The life cycle of Bothriocephalus claviceps has been described by Jarecka (1959, 1963, 1964). At room temperatures the eggs hatched in 5 to 6 days and the coracidium lived 1 to 14 days. The principal copepod host was Macrocyclops albidus, a 100% invasion was obtained experimentally to give 5 to 25 procercoids (caudate bothrio-plerocercoids according to Freeman, 1973) within 12 days. Cyprinid fry were experimentally infected, but although some

TABLEI1 Studies on seasonal occurrence of cestodes of the orders Spathebothridea and Pseudophyllidea listed in the climate zones of the World (see m p Fig. 1, Chubb, 1977). The species are in alphabetical order. Climate zones

Cestode species

1. Tropical la. RAINY (humid climate) 1b. SAVANNA (humid climate) lc. HIGHLAND (humid climate) Id. SEMI-DESERT (dry climate) le. DESERT (dry climate) 2. Sub-tropical 2a. MEDITERRANEAN Bothriocephalus cluviceps

Host species no seasonal studies

tropical forest

no seasonal studies

tropical grassland

no seasonal studies

tropical highland

no seasonal studies

hot semi-desert

no seasonal studies

hot desert

Anguilla anguilla

Cyathocephalus truncatus Salmo trutta Triaenophorus meridionalis

Locality

Esox lucius

2b. HUMID

Bothriocephalus Ctenopharyngodon acheilognathi idella Bothriocephalus cuspidatus Micropterus salmoides

scrub, woodland, olive Lake Skadar, Yugoslavia River Trino, L'Aquila, Italy Lake Dzhapana, Georgia, USSR deciduous forest Kwangtung Province, China Par Pond, Savannah River Plant, Aiken, South Carolina, USA

References

Kazic (1970) Paggi et al. (1978) Cernova (1975) Liao and Shih (1956) Eure and Esch (1974)

P o\

3. Mid-latitude 3ai. HUMID WARM SUMMERS Bothriocephalus acheilognathi

Ctenopharyngodon idella Cyprinus carpio Cyprinus carpio Gymnocephalus schraetser Leuciscus idus Rutilus rutilus Cyprinus carpio Phoxinus phoxinus

temperate grassland, mixed forest Nivka fish farm, Ukraine, USSR River Danube, Bulgaria

Germany Teich (Pond) T, Hungary Bothriocephalus claviceps Anguilla anguilla River Danube, Bulgaria Anguilla anguilla PodEbrady, Bohemia, Czechoslovakia Lake Fort Smith, Bothriocephalus cuspidatus Lepomis gulosus Lepomis macvochirus Arkansas, USA Central and Eastern Bathybothrium Alburnus alburnus rectangulum Barbus barbus Balkan Mountains, Barbus meridionalispetenyi Bulgaria Barbus barbus Rivers Dniestr, Prout, Barbus meridionalispetenyi Stryi, Tissa, USSR Barbus barbus Podebrady, Bohemia, Czechoslovakia Cyathocephalus truncatus Coregonusfeva Lake Lbman (Geneva), Lota Iota Switzerland Salvelinus alpinus Switzerland Eubothrium crassum Salmo trutta (freshwater race)

Davydov (1978) Kakacheva-Avramova (1 977)

Korting (1975a, b) Molnfir (1968b) Kakacheva-Avramova (1977) Sramek (1901) Cloutman (1975) Kakacheva-Avramova (1973) Kulakovskaya (1959) Srfimek (1901) Zschokke (1884) Rosen (1919)

P 4

TABLEI1 (continued) Climate zones

Cestode species

Host species

P

Locality

References

3ai. (continued)

Eubothrium crassum (marine Atlantic race) Eubothrium rugosum Triaenophorus crassus

Salmo trutta Thymallus thjwallus Salmo salar

Lota lota Esox lucius Esox lucius Triaenophorus meridionalis Esox lucius Triaenophorus nodulosus

Esox lucius Esox lucius Esox lucius Esox lucius Esox lucius Esox lucius Esox l u c k

Esox lucius Esox lucius Esox lucius

Lake LCman (Geneva), Zschokke (1884) Switzerland Upper Rhine, Bgle, Zschokke (1891) Switzerland Uppsala, Sweden Nybelin (1922) Warsaw, Poland Michajlow (1932) Germany Scheuring (1929) River Danube, Kakacheva-Avramova Bulgaria (1977) Lipno Reservoir, River Ergens (1966) Vltava, Czechoslovakia Switzerland Fuhrmann (1926) River Danube, Kakacheva-Avramova Bulgaria (1977) Warsaw markets, Michajlow (1933) Poland Poland Michajlow (1951) Wigry Lakes, Poland Milicer (1938) Macha Lake fish pond Moravec (1979b) system, North Bohemia, Czechoslovakia Uppsala, Sweden Nybelin (1922) NeuchPtel, Rosen (1919) Switzerland Near Warsaw, Poland Ruszkowski (1926)

Esox lucius Esox lucius

Esox lucius 3aii. HUMID COOL SUMMERS Bothriocephalus acheilognathi

Ctenopharyngodonidella Cyprinus carpio

Bothriocephaluscuspidatus Perca flavescens Eubothrium crassum (marine Atlantic race) Eubothrium rugosum

Salmo safar

Eubothrium salvelini (American race)

Triaenophorus amurensis

Coregonus hoyi Salmo gairdneri Salmo trutta Salvelinus namaycush namaycush Salvelinus fontinalis Salvelinus namaycush Esox reicherti

Triaenophorus crassus

Esox lucius

Lota fota

Germany Podebrady, Bohemia, Czechoslovakia Lake Leman (Geneva), Switzerland temperate grassland, mixed forest Far-eastern fish farms, USSR Fish farms, Kurskou and Moscow Districts, USSR Yahara River lakes, Wisconsin, USA Baltic Sea

Scheuring (1929) SrBmek (1901)

Lake Vbrtsjarv, Estonia, USSR Lake Michigan, USA

Tell (1971)

Zschokke (1884)

Musselius (1973) Muzykovskii (1969) Pearse (1924) Zschokke (1891)

Amin (1977)

Lakes, Algonquin Park, MacLulich (1943) Ontario, Canada River Amur, USSR Kuperman (1967b, 197313) Lake Nipissing and Ekbaum (1937) Lake of the Woods, Ontario, Canada

?A

Climate zones

Cestode species

TABLEI1 (continued) Host species

3 Locality

References

3aii. (continued)

Esox Iucius

3aiii. EAST COAST

Lake Ladoga, Rybinsk Kuperman (1973) Reservoir, USSR Triaenophorus nodulosus Esox lucius River Volga, USSR Bogdanova (1958) Gymnocephalus cernua Rybinsk Reservoir, Izyumova (1959a) USSR Rybinsk Reservoir, Izyumova (1959b, Esox Iucius USSR 1960) Esox Iucius Lake Ladoga, Rybinsk Kuperman (1973) Reservoir, USSR River Oka, USSR Markova (1958) Esox Iucius Lake Dusia, Lithuania, Rautskis (1970b) Esox lucius USSR Lake Vtjrtsjarv, Tell (1971) Esox lucius Estonia, USSR Kuperman (1967b, 1973) River Amur, USSR Triaenophorus orientalis Esox reicherti temperate grassland, mixed forest Sanami District, Gunma Nakajima and Egusa Bothriocephalus Cyprinus carpio Prefecture, Japan (1977a) acheilognathi Oneida Lake, New Noble (1970) Bothriocephaluscuspidatus Perca flavescens York, USA Insular Newfoundland, Sandeman and Pippy Eubothrium salvelini Salmo gairdneri Canada (American race) Salmo salar (landlocked) (1967) Salmo trutta Salvelinusfontinah

3b. MARINE WEST COAST

Bothriocephalus claviceps Anguilla anguilla Cyathocephalustruncatus Salmo trutta Salmo trutta

Eubothrium crassum (freshwater race)

SaImo trutta Salvelinus alpinus Salrno gairdneri Salmo trutta Salmo trutta Salmo gairdneri Salmo trutta Salmo trutta Salmo trutta Salmo trutta Salmo trutta

Eubothrium crassum (marine Atlantic race) Eubothrium rugosum Eubothrium salvelini (freshwater European race)

Salmo gairdneri Salmo trutta Salmo trutta (migratory) Lota lota Salvelinus alpinus

temperate grassland, deciduous forest Llyn Tegid area, Wales Afon Terrig, Wales River Alyn, Afon Dyfrdwy, Afon Glyn, Wales anerya Water System Trerndelag, Norway Germany

Chubb (1961) Awachie (1963a, 1966a) Rahim (1974) Vik (1954, 1958) Wolf (1906)

Aderounmu (personal communication) Fish farm, Movangher, Arme and Ingham (1972) County Antrim, Ireland Ball (1957) Llyn Tegid, Wales Loch Leven, Scotland Campbell (1974) Rawson (1957) Lake Windermere, England Dunalastair Reservoir, Robertson (1953) Scotland Anoya Water System, Vik (1963) Trondelag, Norway Hanningfield Reservoir, Wootten (1972) Essex, England Fahy (1980) Off Irish Coast, Irish Sea Nybelin (1 922) Gothenburg, Sweden Annya Water System, Vik (1963) Trrandelag, Norway

Llyn Tegid, Wales

VI

TABLEI1 (continued) Climate zones

Cestode species

Host species

N

Locality

References

3b. (continued) Triaenophorus nodulosus

Esox lucius Esox lucius Esox lucius Esox lucius Esox lucius Esox lucius Esox Iucius Esox lucius Esox lucius

3 ~ .SEMI-DESERT Bothriocephalus acheilognathi

Cyprinus carpio Ctenopharyngodon ide!la

Bogstad Lake, near Oslo, Norway Llyn Tegid, Wales Loch Lomond, Scotland River Lugg, Herefordshire, England River Glomma, Norway Lake Druzno, Poland Shropshire Union Canal, Cheshire, England Gothenburg, Sweden Rostherne Mere, Cheshire, England prairie and steppe Vasilevsk fish farm, Kakhovsk Reservoir, USSR Mironov fish farm, Donetsk District, USSR

Borgstrom (1970) Chubb (1963a) Copland (1956, 1957) Davies (1967) Halvorsen (1972) Kozicka (1959) Mishra (1 966) Nybelin (1922) Rizvi (1964, 1968) Iskov (1966) Klenov (1 972)

Triaenophorus crassus (probably T. meridionalis) Triaenophorus meridionalis Triaenophorus nodulosus

Esox lucius

Dnepr Delta, USSR

Komarova (1964)

Esox hcius

Volga Delta, USSR

Kuperman (1973)

Esox lucius no seasonal studies

Cyathocephalus truncatus

Coregonus clupeaformis

Eubothrium rugosum

Lota Iota Perca fluviatilis Lota Iota maculosa Lota Iota

Komarova (1964) Dnepr Delta, USSR cool desert coniferous forest Cold Lake, Alberta, Leong (1975) Canada Lake Konche, Karelia, Malakhova (196 1) USSR Lake Winnipeg, Canada Kuitunen-Ekbaum (1933) Lake Konche, Karelia, Malakhova (1961) USSR Skogsfjordvatnet, Troms Kennedy (1978a) County, Norway

3d. DESERT 3e. SUB-POLAR

Eubothrium salvelini (freshwater European race) Triaenophorus crassus

SaIveIinus alpinus (non-migratory) Esox Iucius Esox Iucius Esox Iucius Esox lucius Esox lucius

Triaenophorus nodulosus

Esox lucius Esox Iucius

Lake Moose, Lake Winnipeg, Canada River Yenisei, Siberia, USSR Baptiste Lake, Alberta, Canada Lesser Slave Lake, Alberta, Canada Pasvikelva, North Norway River Yenisei, Siberia, USSR Lake Konche, Karelia, USSR

Ekbaum (1937) Kuperman (1973) Libin (1951) Miller (1943, 1952) Vik (1959) Kuperman (1973) Malakhova (1961)

wl w

TABLE I1 (continued) Climate zones

Cestode species

Host species

ul

Locality

References

3e. (continued) Esox Iucius Triaenophorus stizostedionis

Stizostedion vitreum

Triaenophorus crassus

Esox Iucius

Triaenophorus nodulosus

Esox Iucius

Lesser Slave Lake, Alberta, Canada Lesser Slave Lake, Alberta, Canada

Miller (1943) Miller (1945)

4. Polar

4a. POLAR

4b. ICE CAPS

no suitable habitats for freshwater cestodes

5. Mountain

Bothriocephalus acheilognathi

Alburnoides bipunctatus eichwaldi

Cyathocephalus truncatus

SaImo trutta

Eubothrium crassum (freshwater race)

Salmo trutta

Eubothrium salvelini (American race)

Oncorhynchus nerka Oncorhynchus nerka

tundra River Anadyr, Chukotka, USSR River Anadyr, Chukotka, USSR icefields and glaciers heath, rocks and scree Springs, Chilu-Chor Chashma, Tadzhikstan, USSR Lake Melingen, VBgB, Lake Nedre Fipling, Vefsn, Norway Lake Melingen, VBgB, Lake Nedre Fipling, Vefsn, Norway Babine Lake, British Columbia, Canada Babine Lake, British Columbia, Canada

Kuperman (1973) Kuperman (1973)

Daniyarov (1975) Halvorsen and Macdonald (1972) Halvorsen and Macdonald (1972) Boyce (1 974) Smith (1973)

HELMINTHS IN FRESHWATER FISHES

55

morphological changes were seen development did not occur. These larvae persisted in the cyprinids for 14 days. Young Anguilla anguilla, the natural definitive host of B. claviceps, were also experimentally infected. In these fishes,at three days post infection 10 to 15 larvae were present in the intestine, at seven days growth and strobilization had started in one of three larvae; growth of the others appeared to be arrested. At one month, two segmented cestodes were found, and in two months, two B. claviceps containing eggs were recovered. It is evident that only one intermediate host is necessary for completion of the life cycle. Srimek (1901) found mature Bothriocephalus claviceps in Anguilla anguilla in May (see Table I1 for locality). Chubb (1961) at LlynTegid, Wales, observed that this cestode was commonest in lake rather than stream eels. Samples were collected January, March, May to July and October only. The worms were gravid in all of these months except January. Incidence and intensity data showed no particular change with seasons. In Yugoslavia at Lake Skadar KaiiC (1970) reported immature B. claviceps in A. anguilla in May, October and November, and mature specimens in March, May, numbers rising a little to June, July and August, lower in September, none in October, but the November level was the same as that in June to August. KakachevaAvramova (1977) noted B. claviceps in A . anguilla in the River Danube, Bulgaria, in spring and summer. Bothriocephalus cuspidatus Cooper, 1917 Essex (1928) found eggs of Bothriocephalus cuspidatus in worms from Stizostedion vitreum at Ely, Minnesota, U.S.A., on 6 July. Development appeared to be completed after shedding of the eggs from the uterus, and hatching occurred in the laboratory on 13 July. First intermediate hosts experimentally infected were Cyclops brevispinosus, C. prasinus, C. leuckarti and C. serrulutus. Development was completed by the tenth day. Essex (1928) postulated that the fully developed larvae would be transferred from the copepods either via small fishes or direct to S . vitreum. He found all sizes of B. cuspidatus from 0-6 mm (twice length of procercoid) to sexually mature worms in S . vitreum. At the Yahara River lakes, Wisconsin, U.S.A., Pearse (1924) noted Bothriocephaluscuspidatus in PercaJEavescensin June to October, and January, but not in November or February to May. Van Cleave and Mueller (1934) found only a slight approach to sexual maturity in P.JEuvescensduring the summer months in Lake Oneida, New York, U.S.A., but Noble (1970) found three adults during late autumn (December) in the same host and habitat. Eure and Esch (1974) also observed the adult worms most commonly in Micropterus salmoides in winter, in unheated areas of Par Pond, Savannah River Plant, Aiken, South Carolina, U.S.A., Cloutman (1975) recorded B. cuspidatus in Lepomis gulosus in January and in L. macrochirus from January to June at Lake Fort Smith, Arkansas, U.S.A. Bothriocephalus species Markevich et al. (1976) commented that hot effluents from power plants had a marked effect on an ecosystem. The hot waters from the TripoI’ye

56

JAMES C . C H U B B

Power Plant on the Kanev Reservoir, U.S.S.R., increased the development of some planktonic (and benthic) invertebrates and thereby affected the abundance and seasonal dynamics of the parasites, including Bothriocephalus species. (b) Family Triaenophoridae Triaenophorus amurensis Kuperman, 1968 (For larval stages see Part 111 p. 3-4 of review). The development to maturity and the production of eggs in Triaenophorus amurensis occurs in Esox reicherti in the River Amur basin, U.S.S.R. over the winter months. The gravid worms were shed from their hosts at the end of May (Kuperman, 1967a, b, 1973). Triaenophorus crassus Forel, 1868 (For larval stages see Part I11 pp. 4-6 of review). Scheuring (1929), Michajlow (1932) and Ekbaum (1937) presented seasonal data concerning Triaenophorus crassus adults (see Table I1 for localities), but it was Miller (1943, 1952) who gave fuller details. In Lesser Slave Lake, Alberta, Canada, maximum incidence in Esox lucius occurred in spring and the minimum in early summer. During the first two weeks of June the E. Zucius were relatively free of worms, as the gravid generation had just been lost. In mid-June fresh infections of small immature worms were present. Immature worms were seen throughout the year, indicating that invasion of the E. lucius took place at all seasons, however in May they too appeared to pass out from the intestines of E. lucius together with the gravid cestodes. On recently acquired immature T . crassus the cauda was retained for a time. Growth of the worms in the fishes intestines commenced in SeptemberOctober, genital rudiments probably appeared in November but were well formed by December, the first eggs were seen in January, and the uteri were distended with eggs by February. Oncospheres could be seen in the eggs in March, and eggs were released from worms when they were placed in water during April. Dates of egg release have already been presented in Chubb, 1980, Part 111, but by 15 May most of the old T . crassus had been lost, although a few persisted until early June. Miller (1952) noted an interesting change in behaviour of the T. crassus in the host intestine: before egg release started the worms had their strobilae much tangled together and kinked, but once egg release was occurring the worms extended for their full lengths down the intestine. Kuperman (1973) found essentially the same development pattern in the U.S.S.R. as that described by Miller (1943, 1952). In the Rybinsk Reservoir the gravid worms left Esox Iucius by May to mid-June, but in the colder conditions in Siberia and Chukota gravid cestodes persisted in the intestines until the end of June or mid-July. Kuperman (1973) regarded this as further evidence of the importance of temperature in relation to the maturation of the worms and the formation of ripe eggs. Throughout its distributional range T . crassus appeared to have a single optimum temperature for embryonic development and synchronization of its egg-laying. In the U.S.S.R. this particular temperature was made manifest by the delayed onset of sexual

HELMINTHS I N FRESHWATER FISHES

57

maturity from west to east of the geographical range in that country. Vik (1959) collected some Triaenophorus crassus (as T. robustus) from Pasvikelva, North Norway on 27 September to 3 October 1951. He stated that some of the worms contained fully developed eggs. An experimental attempt was made by Libin (1951) to obtain Triaenophorus crassus eggs at all seasons by injecting pituitary extract into the host Esox lucius. He noted the coincident spawning of E, lucius and T . crassus in the latter part of April and early May in Canada, which could be attributed to either or both water temperature or host pituitary factors. Libin (1951) concluded that the injections into the E. lucius resulted in their tapeworms developing to a more mature condition than those found in control fishes. Some worms were advanced to the stage when they released their undeveloped eggs upon contact with the water. The nearer the dates of injection to the natural spawning period, the easier it was to advance both the sex organs of the E. Zucius and of their T. crassus. However, Libin (1951) also called attention to the fact that the higher temperature of the tank as compared to the lake waters also probably advanced spermatogenesis to a certain extent, nevertheless he considered that there was a definite causal relationship between maturation of the host gonads and the parasite, mediated by the hormones secreted by the pituitary gland of the E. lucius. Komarova (1964) reported Triaenophorus crassus from Esox lucius in the Dnepr Delta, U.S.S.R., with a high incidence (80-93%) during all months sampled. It should be noted, owing to their southern location, that these worms were probably Triaenophorus meridionalis. Triaenophorus meridionalis Kuperman, 1968 (For larval stages see Part I11 p. 6 of review). As in the other species of Triaenophorus, growth of the immature adults commenced in the autumn, sexual maturity occurred during the winter and the gravid cestodes left their hosts, Esox lucius, in May in the Volga Delta but at considerably higher water temperatures than for those which applied to Triaenophoruscrassus (Kuperman, 1973). Cernova (1975) a t Lake Dzhapana, Georgia, U.S.S.R., found the following incidences (and intensities, mean, range) in E. lucius in spring 60% (3.2, 1-10), with a fall to summer 13.3% (2.5, 1-4) rising thereafter autumn 23.1 % (1.7, 1-3) to winter 60% (2.3, 1-5). Kakacheva-Avramova (1977) noted the occurrence of T . meridionalis in E. lucius in the River Danube in spring. Triaenophorus nodulosus (Pallas, 1760) (For larval stages see Part 111pp. 6-12 of review). Triaenophorus nodulosus is a species which has received much attention from fish helminthologists. Zschokke (1 884) found worms in the intestine of Esox lucius in Lake Ltman, Switzerland, through all the year. Srhmek (1901) noted mature cestodes at Podzbrady, Czechoslovakia in April, but it was Rosen (1919) who provided fuller details of the biology from E. lucius in Lake NeuchBtel, Switzerland. Invasion of the fishes by T.,nodulosus occurred during summer, maturation was achieved by the end of February and these cestodes were lost at the end of June to be replaced by new invasions

58

JAMES C . CHUBB

during the ingestion of Percajuviatilis. Ripe eggs were seen at the end of February. Rosen (1919) also described the coracidium, obtained procercoids in experimentally infected Cyclops strenuus and C.fimbriatus, and observed the procercoid penetrate into the tissues of the intestine of P . Jluviatilis. Nybelin (1922), Scheuring (1923, 1929) and Michajlow (1933, 1951) all provided additional data about the biology of both adult and larval T. nodulosus. Michajlow (1951) found young T. nodulosus in the intestine of E. lucius at all times of the year. However, it was Miller (1943) collecting cestodes from E. lucius in Lesser Slave Lake, Alberta, Canada, who gave a rather more detailed account of the annual biology of the adult T. nodulosus. At Lesser Slave Lake, Miller (1943) observed the smallest worms in Esox Zucius in late May and early June. Growth commenced in the autumn, genital rudiments appeared December and eggs were seen in the uteri in February. Strobilae of gravid individuals commonly coiled together in a tight mass in the centre of the intestine lumen. As egg release approached the strobilae straightened and eventually stretched the full length of the intestine, sometimes protruding into the rectum. Miller (1943) saw that eggs with formed coracidia were first released in May, and the main egg laying period was the end of May and early June. Some Triaenophorus nodulosus were observed hanging out of the anus of the E. lucius, suggesting that they were voided into the water to release clouds of eggs. New invasions by plerocercoids were established by the last weeks of June (Miller, 1943). Markova (1958) at the River Oka, U.S.S.R., found a similar pattern of occurrence. Incidence was minimal in May (31.6%) and maximal in March (100 %). The main period of invasion of Esox lucius was considered to be June to August, but it occurred to a lesser extent at other times. Gravid worms were lost from March to May. However, Markova (1958) divided her cestodes into length groups, 4-17 mm, 17-50 mm, 50-100 mm and 100-180 mm and the patterns of distribution of the worms within these groups clearly demonstrated the presence of juvenile worms as 100% of the population in June and July, development commencing August to December, so that in December 90% of the worms were in the length group 100-180 mm. The loss of the gravid generation in May was also very evident, as in that month only 5 % of the T. nodtllosus were in the 4-17 mm length group, whilst the remainder of the worms were distributed through the three other length groups, whereas by June 100% of the worms were 4-17 mm in length once again. Concurrent with the increased lengths attained by the Triaenophorus nodulosus during the autumn and winter months, growth of the genitalia also occurs. In an attempt to quantify this growth Chubb (1963a) at Llyn Tegid, Wales, measured lengths (for length groups see Fig. 4) and in addition distinguished five stages of cestode maturity: Stage I consisted of worms with no genital development or strobilization. The worms retained the plerocercoid characters, with a fully formed scolex and an undivided body. Worms contained within this group were described as plerocerciform, but it was emphasized that this was not to imply that these worms possessed all the morphological and physiological attributes of the somatic plerocercoid.

59

H E L M I N T H S I N F R E S H W A T E R FISHES

E E

161 plus

-

81-160 41-80

I

04

5

I:J B

-a

21-40

0-20

'0

' N . ' D . ' J . ' F . ' M . ' A . ' M .

C

J.

JI.

Lo

L 3 ~

0

L

a

f

Stage

C

Stage IV

.-

.-"

v

-

5 Stage 111

u

Month

FIG.4. A histogram showing the annual pattern of changes in length and state of maturity of the adults of the cestode Triuenophorus nodulosus in the intestine of Esox lucius from Llyn Tegid, Wales. The ordinate shows five length groups, in mm, in the upper histogram, and the five stages of sexual maturity in the lower histogram. The abscissa in each instance shows the month. The data are expressed as percentages of the total numbers of worms found per month. (From Chubb (1963a), Fig. 2, p. 425.)

Stage I1 consisted of worms in which development of genitalia and strobilization had occurred, the genitalia being in all stages of development prior to the production of eggs, but no eggs were present in the uteri, or had been formed. Stage I11 consisted of worms in which egg production had occurred in some region of the strobila, the eggs were in the process of accumulation in the uteri. Living worms in this stage did not liberate eggs from the uteri when placed in cold tap water, although sectioned material revealed that the uterine passage opened to the exterior. Stage IV consisted of worms which when placed in cold tap water, liberated eggs from the uteri via the uterine pores. The worms in this group had a regular intact strobila, and there was no evidence to suggest that eggs had been discharged prior to the worms having been placed in water. This group and the next were easily distinguished, as Stage V worms always had some empty uteri, eggs having been liberated into the lumen of the Esox lucius intestine. Stage V consisted of worms which had started to liberate eggs whilst in the E. Zucius intestine, the worms being in all stages from starting to shed eggs, through all levels of decline and partial disintegration. The degree of fullness

60

J A M E S C. C H U B B

of the uteri varied along the length of the strobila, many proglottids were almost devoid of eggs. The posterior region of the strobila of these worms was irregular, partly degenerate, and usually narrower in width than the more medial regions of the strobila. Eggs which remained in the uteri were liberated on placing these worms in water (Chubb, 1963a). Chubb (1963a) stressed that as growth of the stobila in cestodes usually occurred from the region immediately posterior to the scolex, a gradient of development was found along the length of the strobila, the posterior proglottids were therefore, older and more mature than the more anterior proglottids, thus the stages defined would apply to rather limited posterior regions of the cestodes. Accordingly, the selection of the appropriate stage of maturation was based on the more posterior proglottids, although in the instance of Triaenophorus nodulosus, and of many other Pseudophyllidea, much of the strobila matured within a short period, especially after egg production had started. The information obtained by Chubb (1963a) is shown in Fig. 4, It may be seen that the Triaenophorus nodulosus in Esox lucius a t Llyn Tegid were all plerocerciform June to August (Stage I), growth of a few commenced in September, but genital development (Stage 11) did not occur until October, so that the first eggs (Stage 111) were found in December. Many of the worms were gravid by March (Stage IV), but peak egg liberation occurred in April and May (Stage V) and virtually all of the gravid worms were gone by the end of May. Chubb (1963a) was able to demonstrate that invasion of the Esox lucius by plerocercoids of Triaenophorus nodulosus from Percafluviatilis could occur at all times of the year, as the E. lucius were feeding during all the months. It was shown that although invasion of the E. lucius by plerocercoids occurred throughout the year, there was no increase in numbers of worms in the fishes intestines to a maximum at any period of the year, rather there was a more or less constant number of T. noddosus in E. IUcius of given length at all times of the year. It was postulated, therefore, that a dynamic equilibrium existed between gain of plerocercoids from P. fluviatilis taken as food and loss of worms from the E. lucius intestines at all times. Chubb et al. (1964) gave evidence that such a dynamic condition applied in both Cestoda and Acanthocephala in the intestines of freshwater fishes. Other studies in the British Isles (Copland, 1956, 1957; Rizvi, 1964, 1968; Mishra, 1966) showed similar dates and patterns of periodicity of occurrence of Triaenophorus nodulosus as those observed by Chubb (1963a). At Bogstad Lake, near Oslo, Norway Borgstrom (1970) observed the same pattern of occurrence as elsewhere. Perca jluviatilis containing plerocercoids were eaten by Esox lucius throughout the year, but most frequently June to September. Incidences of Triaenophorus nodulosus were high all year, 100% in March-April. Borgstrom (1970) recognized three stages of worm maturation, Stages I and I1 as Chubb (1963a, above) and Stage 111 including all worms with eggs. Stage I occurred all year, Stage I1 appeared from October, Stage I11 from December, increased until May, to be passed by the latter

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half of May and early June. At Bogstad Lake this time corresponded with the spawning of E. Zucius. Intensity of infection was low and rather constant June to December, but increased during the winter months. Borgstrom (1970) speculated that this could be owing to decreased resistance of the host to cestode infections at low water temperatures. In the River Glomma, Norway, Halvorsen (1972) also recovered gravid worms in May and June, and plerocercoid-like adults during the summer months. In Czechoslovakia, Ergens (1966) also found Triuenophorus nodulosus in Esox Zucius at Lipno Reservoir, River Vltava, during all seasons of the year. Moravec (1979b) too, at MBcha Lake fish pond system, North Bohemia, Czechoslovakia, noted the above, and observed that worms with eggs were present October to April. Bauer (1959a) has summarized much of the information about Triaenophorus nodulosus up to that time both for the U.S.S.R. and elsewhere. Studies in the U.S.S.R. include general faunistic surveys containing seasonal data, for instance, Bogdanova (1958), Izyumova (1959a, b, 1960), Komarova (1964), MaIakhova (1961), Rautskis (1970b) and Tell (1971). Localities are listed in Table 11. The major study on T. nodulosus in the U.S.S.R. is that of Kuperman (1965, 1967a, 1973). His work is summarized, together with most of the earlier investigations by other workers, in Kuperman (1973). At the Rybinsk Reservoir Kuperman (1973) studied T. nodulosus in Esox Zucius from February 1965 to February 1967. The worms were divided into length groups 1-80 mm, 81-160 mm, 161-240 mm and 241-280 mm or longer. Five stages of development were separated, using a modified Chubb (1963a) scheme: Stage I young worms, similar to plerocercoids, gonads completely absent. Stage I1 strobila, beginning at the posterior end, showed gonadial rudiments and the formation of cirrus, vas deferens, oviduct and uterus. Stage I11 strobila showed completely developed gonadial complex in most proglottids, but there were no eggs in the uterus. Stage IV worms contained a mass of eggs in the uterus and the eggs were readily deposited when the worms were transferred to water. Stage V worms with eggs, showing degeneration of strobila. These worms were in process of leaving the host intestine, which often showed clumps of strobilae. It will be noted that Stages I and I1 are identical in the Chubb (1963a) and Kuperman (1973) schemes, Kuperman Stage I11 would fall at the end of Stage 11 of the Chubb scheme, Chubb Stages 111 and IV would be placed together in Kuperman’s Stage IV, and finally, Stages V of both schemes are identical. In the Rybinsk Reservoir Kuperman (1973) found Triuenophorus nodulosus in the intestines of Esox Zucius all year. From the second half of June to September all worms were young (Stage I), 10 to 90 mm long. At the end of September gonadial rudiments appeared in worms 90 to 104 mm long, and during October through December growth was rapid to reach completion in the first half of January; the maximum length at the end of this time was 255 mm. Earliest eggs were seen in the uteri during the first week’in January, and these eggs were laid and developed normally if the worms were trans-

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ferred to water. In February and March the number of sexually mature worms increased rapidly, but there was also an increase in the diversity of maturation such that the same population contained individuals at different stages of development. The main deposition of eggs occurred at the end of April, particularly during May and in early June. At this time worms were leaving the host (Stage V) to break up in the water and release eggs. The last sexually mature worms were seen at the Rybinsk Reservoir on 16-19 June. During May some increase in newly invaded worms was seen, and in June these became more numerous than the gravid worms of the old generation (Kuperman, 1973). It was noted at the Rybinsk Reservoir that although invasion by plerocercoids from Percafluviatilis took place all year, there were seasonal changes in extent to which this occurred. Kuperman (1973) found the main invasion period to be autumn and winter, and he also stated that the infections built up during the winter months as there was no loss of sexually mature worms until April. In all of the investigations reported above it will have been noted that growth and sexual differentiation of the Triaenophorus nodulosus occurred at a time of falling water temperatures. Eggs first appeared in Llyn Tegid, Wales (Chubb, 1963a) and Lake Bogstad, Norway (Borgstrom, 1970), in December, in Rybinsk Reservoir, U.S.S.R., in early January, and in February jn Lake Neuchltel, Switzerland (Rosen, 1919), and Lesser Slave Lake, Alberta, Canada (Miller, 1943). As Triaenophorus species in the Volga Delta, U.S.S.R., were already packed with eggs as early as November, Kuperman (1973) suggested that the onset of sexual maturity occurred earlier in southern as compared with northern waters. Although the growth and differentiation of Triaenophorus nodulosus coincided with falling water temperatures, as indicated above, these processes are also concurrent with increasing development of the gonads of the host, Esox lucius. Halvorsen (1972) favoured the view that the sexual development of T. nodulosus was dependent on the hormone level of the fish host. Although Libin (1951) carried out experiments with Triaenophorus crassus (see above) to attempt to clarify this relationship between maturation of the cestodes, host hormones and water temperature, his results are equivocal, so that no final conclusion can be reached. As in so many biological phenomena, it may be the synergistic effect of both falling temperatures and host hormones which influence the cestode maturation. It is evident that rising water temperatures in spring coincide with the loss of gravid Triaenophorus nodulosus from the intestines of Esox lucius. Kuperman (1973) noted that most worms left E. lucius in Lake Ladoga, U.S.S.R., in May and June, but that in the colder conditions of Siberia and Chukotka worms persisted until the end of June and the middle of July respectively. However, even here temperature may not be the single determining factor, as a host immune response similar to that postulated by Kennedy (1968, 1969b) for the system Caryophyllaeus laticeps-Leuciscus leuciscus may apply. Kuperman and Shul’man (1972) attempted to resolve the influence of

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temperature on the development of both Triuenophorus nodulosus and T. crassus in Esox lucius by experiment. They concluded that the peak of cestode growth and the maturation of sex organs was related to a lowering of temperature in the autumn, and they showed that the shedding of the strobilae from the intestine was stimulated by increased temperatures. At 13-18°C the cestodes left the intestine in two to three days, and at 7-9°C after 25 or more days. They concluded that the shedding of worms was not dependent on their maturity, but on the water temperature. Nevertheless, these experiments could not exclude either the host hormonal or immune system influences on the parasites, so that although they show the relationship with temperature very clearly, the causal factor could still be temperature, host hormones or a host immune response, or a combination of these factors. Some evidence which may exclude the host hormonal factor as an influence on the expulsion of gravid worms was provided by Engelbrecht (1963). In freshwaters the loss of Triaenophorus nodulosus coincided with the Esox lucius spawning time, thus he concluded the ultimate development of the worms and their passing was decisively determined by the spawning period of the host. By contrast, in coastal brackish water conditions, the main time for loss of the worms was May to June, several weeks after the host fishes had finished spawning. In this latter instance, the slower warming of the larger water mass of the bays of the Baltic Sea may have determined the later expulsion of the worms. However, these observations do not differentiate the two factors temperature and host immune response. Pojmatiska (1976) and Pojmatiska et ul. (1978) have studied the effect of thermal pollution in lakes in the Konin region of Poland. Triaenophorus nodulosus was a thermophobic species, it prevailed in cooler lakes, but had almost completely disappeared in the heated waters. Triaenophorus orientalis Kuperman, 1968 (For larval stages see Part 111 p. 12 of review). The development to maturity of this species occurred in Esox reicherti in the River Amur basin, U.S.S.R., overwinter as in the other species of Triaenophorus (Kuperman, 1967b, 1973). The gravid worms were passed to the exterior at the end of May (Kuperman, 1973). Triaenophorus stizostedionis Miller, 1945 (For larval stages see Part I11 p. 12 of review). Miller (1945) found that at Lesser Slave Lake, Alberta, Canada, Stizostedion vitreum were infected by these cestodes a t all times of the year. As the gravid generation was lost about the first two weeks of June new invasions were commonly seen. Sexual development of the worms took place overwinter as with the other Triaenophorus species. Triaenophorus species Newton (1932) reported about the seasonality of the adult phase of Triaenophorustricuspidatus (=T. nodulosus) in Esox lucius in Western Canada. Ekbaum (1937) has pointed out that at least some of the cestodes must have been T . crassus. Figure 8 in Newton (1932) showed both T. noduulosus and

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T. crassus, so that it is evident that the two species were considered together. (c) Family Amphicotylidae Bathybothrium rectangulum (Bloch, 1778) Sramek (1901) at PodEbrady, Bohemia, Czechoslovakia, noted an immature worm 18 mm long in Barbus barbus in December, but Kulakovskaya (1959) has provided fuller information about its seasonal periodicity in B. barbus and B. meridionalis petenyi in the U.S.S.R. In the River Dniestr, by the second half of June, when the water was quite warm, scolices without strobila development appeared. At higher altitudes, in the River Stryi (Dniestr watershed) where the water warmed more slowly, the scolices did not occur until the end of July, whilst in the River Tissa (Transcarpathians) not until 7 August. By late August or September growth had occurred so that the worms reached 10 mm, and an increase in length continued through the winter months. By the end of February and March the B. rectangulum were 45 to 50 mm or longer. At this time Kulakovskaya (1959) noted the appearance of genital rudiments, and the sexual organs developed during March to May. The gravid worms containing ripe eggs were seen : middle reaches, River Dniestr, 27 May; in mountains, River Prout, 26 June and River Stryi 12 and 15 July. In the mountains the lower water temperatures were considered to have delayed maturation. In May-June the gravid generation was lost, to be followed by invasion by plerocercoids in the second half of the summer, but sometimes even during the time when gravid worms were present. The intermediate host development cycle was unknown to Kulakovskaya (1959) and still requires investigation. Kakacheva-Avramova (1973) noted Bathybothrium rectangulum during spring through to autumn in the Central and Eastern Balkan Mountains, Bulgaria, but provided no details. Erlbothrium crassum (Bloch, 1779) In a consideration of this species it is important to separate a number of races as the details of their biology differ, Kennedy (1978b) proposed the following: 1. freshwater race in Salmo trutta fario Europe, Eurasia. Coextensive with distribution of S. trutta. Life cycle has copepod as only intermediate host, other fishes serve as paratenic hosts. 2. marine Atlantic race in Salmo salar, coextensive with this host on both sides of the Atlantic Ocean. Life cycle unknown, but may be marine, coastal. 3. marine Pacific race in Oncorhynchus species, coextensive with these fishes, both sides of the Pacific Ocean. Life cycle unknown. Freshwater race. Worms of this race of Eubothrium crassum occured in Salmo trutta (freshwater resident form) at all times of the year (for localities see Table 11): Zschokke (1884), Ball (1957), Wootten (1972), Campbell (1974) and Aderounmu (personal communication). However, the incidences could vary, depending on the seasonal movements of the fishes in relation to the sampling sites of the investigators (see for instance Ball, 1957). The life cycle was demonstrated by Rosen (1919). Cyclops strenuus and

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C.jrnbriatus were shown to serve as first intermediate hosts. When eaten by fishes the procercoid seldom penetrated through the fish intestinal walls into the viscera, but remained in the lumen of the intestines of PercaJluviatilis. Rosen (1919) observed that Sulmo trutta in general became invaded by ingestion of young P. fluviatilis in whose intestinal lumen the plerocercoids were present. Gravid adult E. crassurn were seen at the end of March or the beginning of April, and Rosen (1919) saw degenerating worms in August. More recently Wootten (1972), at Hanningfield Reservoir, Essex, England, has provided greater details for the infection of both Salmo gairdneri and S. trutta. Although infected fishes occurred in all months the maximum incidences and the greatest numbers of cestodes were found from June to November. However, there was no evidence of any seasonal pattern of maturation of the worms, so that gravid E. crassurn were noted in all months. There was no fixed length at which the cestodes became mature or gravid. Wootten (1972) showed that S. trutta stocked into the reservoir in March-April had acquired invasions of worms by June and continued to acquire further invasions throughout the rest of the summer. Mature and gravid E. crassum were seen in the stocked fishes from July, therefore it was concluded that the worms could produce eggs within two to three months of establishment at that time of the year, having attained a length of 200 to 300 mm (Wootten, 1972). From August it was observed that numbers of E. crassurn decreased, despite continued acquisition of new invasions, so that there must have been a greater loss of worms than establishment of newly acquired invasive larvae. Wootten (1972) also showed that either an immune response or an intraspecific crowding effect operated and influenced the numbers of worms in older fishes. Data suggested that individual worms were better able to reach maturity in light intensities of infection. The overall picture obtained by Campbell (1974) for infection of Salmo trutta in Loch Leven, Scotland, was similar to that described above. The largest number of plerocerciform juveniles of Eubothrium erassum was found July to September although they were present at other times. These larvae were observed in the intestine of Perca juviatilis during the summer (see also Rosen, 1919, above). Gravid worms were seen occasionally from April to October, and in April to June many of the cestodes were appreciably longer and wider than at other times. Weights of E, crassurn were determined each month and increased during spring and early summer, often to reach a maximurn in June or July. Kennedy and Burrough (1978) noted that at Malham Tarn, Yorkshire, England, S. trutta stocked in April had a 100% incidence of E. crassurn by July. Some additional data can be found in Robertson (1953) and Rawson (1957). Vik (1963) fishing through ice in the Anerya Water System, Trerndelag, Norway, in January and March 1953 found plerocerciform, immature and mature Eubothrium crassum in Salrno trutta. Again in this area, Perca JEuviatiliswere involved in the life cycle and Vik (1963) experimentally demonstrated that Gasterosteus aculeatus was able to serve as paratenic host. Small S. trutta, less than 200 mm in length, could acquire the invasion direct from

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Cyclops species, which were present in h ~ y ina large populations in spring and autumn. Arme and Ingham (1972) from Ireland and Halvorsen and Macdonald (1972) from Norway also provided some information concerning the seasonal biology of E. crassurn. Marine Atlantic race. Zschokke (1891) reported this race (as Bothriocephalus infundibuliforrnis)in the Upper Rhine, Bale, Switzerland, and the Baltic Sea in Salmo salar. In the Upper Rhine incidences were 100% in July and August, and worms were seen all months sampled. In the Baltic fishes, incidence was 100% almost all months February to November. Nybelin (1922) noted a Eubothrium, probably E. crassurn, in S. salar in Sweden in October. As the worms were young, up to 50 mm long, they were assumed to be a recent invasion. Dogie1 and Petrushevskii (1935) examined S . salar from the White Sea, U.S.S.R.,during August to October. In “autumn” fishes fresh from the sea 100 or more strobilate cestodes were present, but in individual S. salar which had remained in the river from the previous year only the scolices remained. At the River Exe, Devon, England, Kennedy (1969~) found infections in S. salar and migratory Salrno trutta which were returning from the sea to spawn. The cestodes in S . salar freshly run from the sea were generally mature and some contained eggs. A decline in intensity of infection was seen as the fishes moved upstream to spawn. Fahy (1980) has recently demonstrated the pattern of life of the marine Atlantic race of Eubothriurn crassurn in migratory Salrno trutta off the Irish Coast of the Irish Sea. Within weeks of entering the sea for the first time the post-smolts acquired heavy burdens of E. crassurn, which during subsequent migrations of the hosts into freshwaters were successively reduced and then augmented in numbers again on the fishes returning to the sea. Worms which survived the migrations of their hosts into freshwaters continued to increase in length. One year was considered sufficient for growth from plerocercoid to gravid worm, however growth continued for at least two years and possibly longer. Fahy (1980) found that the proportion of plerocerciform and immature worms increased dramatically as the summer progressed, at the time the postsmolt s. trutta were feeding actively at sea, before they returned to freshwaters within weeks of going to sea. In later years, these fishes (as both maiden unspawned individuals and previous spawners) fed over a different period and while some adult migratory S. trutta did feed at sea during the summer months, when they accumulated large burdens of E. crassurn, the majority of maiden and previous spawners tended to have ceased feeding in the sea by the early summer. Thus as the cestodes were lost during the return of their hosts to freshwaters there was not such a large number of plerocerciform worms from which growth of replacement adult worms could occur. Fahy (1980) found that no post-smolts contained gravid E. crassurn, whereas in maidens 45 % and in previous spawners 41 % of the worms were gravid. Marine Pacific race. The author has not found any seasonal studies relating to this form of E. crassurn. Kuperman (1978) has studied the life cycle of Eubothrium crassurn in Oncorhynchus keta, 0. tschawytscha and Salvelinus leucornaenis in the

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Kamchatka region of the U.S.S.R. Here the E. crassum ova were sensitive to changes in water salinity, adapted to a salinity of 5 to 20%,, however the adult worms did occur in the migratory salmonids which were the definitive hosts. It is not clear how these Kamchatka E. crassum fit into the three races scheme postulated by Kennedy (1978b). It may be necessary to define a Pacific freshwater race, or they may be identical to the European freshwater form. Eubothrium rugosum (Batsch, 1786) Nybelin (1 922) provided data concerning seasonal development in Lota lota from Gothenburg and Uppsala, Sweden. In summary, genital rudiments were seen in September in one cestode, but not in seven others examined September and October. No worms were found in November. One Eubothrium rugosum collected in January had formed genitalia, with eggs in uteri, whereas of five worms in February the sexual organs were present but not functional in one, and fully formed but without eggs in four. In April 16 worms all had eggs in the uteri, as did one in May. The specimens Nybelin (1922) examined were collected over several years, 1910 to 1918, not all in the same one. Subsequent reports have confirmed the pattern described above. KuitunenEkbaum (1933b) found fully mature specimens present in Lota lota maculosa in Lake Winnipeg, Canada, during the period March to June. A t Lake Konche, Karelia, U.S.S.R., Malakhova (1961) found incidences in L. lota during winter (5.2%) and spring (3.6%) only, and not during summer and autumn. Tell (1971), for Lake Vbrtsjarv, Estonia, U.S.S.R., reported that a low incidence at the end of June or beginning of July gradually increased through to the following spring, when at the end of April and beginning of May the incidence and intensity of infection was high, the worms of maximum size and gravid. At the end of May and beginning of June the gravid generation was lost from the L. lota. Eubothrium salvelini (Schrank, 1790) Kennedy (1 976) noted that in North America Eubothrium salvelini replaced E. crassum in freshwater habitats, and he postulated that three races existed, American, Asian and European. However, in a later paper Kennedy (1978b) proposed two races, which will be utilized here : 1. Freshwater European race in Salvelinus alpinus, with a freshwater life cycle having a copepod intermediate host. 2. An American race occurring in North America and Eastern Asia in species of Oncorhynchus, Salmo and Salvelinus as well as other genera of fishes. The biology was the same as the European race. Freshwater European race Vik (1963) sampled Salvelinus alpinus in the h.noya Water System, Trerndelag, Norway, mostly in the autumn, but the few fishes examined between June and September were also infected. Cyclops strenuus was infected experimentally and procercoids obtained in three weeks. Kennedy (1978a) studied the occurrence of E. salvelini in the same host in Skogsfjordvatnet, Troms County, North Norway, from May to September. Incidence remained

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relatively constant through these months (minimum 35.3 % July, maximum 42.1 % June), but mean intensity increased from 3-5 in May to 6-4 by September. Small plerocercjform worms were present each month, and were considered recently acquired, therefore it was deduced that invasion had occurred during the whole period of investigation, even under ice cover in May. Gravid cestodes were also present each month, consequently egg production also occurred throughout the term of the study. However, the proportion of gravid E. salvelini was maximal in June and July and lowest in September. The proportion of plerocerciform worms was greatest July and September, so that a seasonal periodicity in the acquisition of invasions and of maturation was suggested. Although both phenomena occurred all summer, maturation peaked in mid-summer and recruitment in late summer (Kennedy, 1978a). American race. In Algonquin Park, Ontario, Canada, MacLulich (1943) found Eubothrium salvelini in Salvelinus fontinalis and S . namaycush. Some fishes, taken just before ice break-up, had both immature and mature worms. Smith (1973) studied the occurrence in smolts of Oncorhynchus nerka in Babine Lake, British Columbia, Canada. Worm maturation was not studied in detail, but circa 23 May onward they were usually gravid. Intermittant measurements made over a 20 year period suggested that commonly about one third of the 0. nerka population became infected by mid-summer, and that this level of incidence persisted until the fishes migrated as smolts. Two periods of exceptionally low infection were seen, which suggested that the usually rather stable incidence level could become disrupted and lower levels could then persist for several consecutive years. Smith (1973) observed that the initial invasion of yearling Oncorhynchus nerka in Babine Lake occurred progressively from south to north. This was attributed to warming trends in the surface waters of the lake, which normally occurred latest in the North Arm region. Boyce (personal communication to Smith, 1973, but see Boyce, 1974, below) showed in laboratory studies that the warming of waters supporting copepods infected with Eubothrium salvelini speeded up the development of the procercoids to an invasive condition. Boyce (1974) using Babine Lake materials experimentally demonstrated the life cycle of Eubothrium salvelini. Eggs were discharged spontaneously from gravid cestodes and survived for up to 30 days at 5°C. No hatching occurred. Cyclops bicuspidatus, C. scutifer and C. vernalis became infected readily on ingestion o f eggs. In 20 days at 5°C little development beyond the oncosphere stage was seen, but at 10°C large procercoids with the cercomer formation in progress were obtained, whilst at 15°C development of the metacestode was almost complete in this time. At 10°Cthe initial phase of cercomer formation was achieved in 15 to 20 days, maximum development in 25 to 30 days and no further development occurred to day 43 post infection. The latter procercoids (caudate bothrio-plerocercoids according to Freeman, 1973) were the same size as the first invasions to be seen in fishes (acaudate bothrio-plerocercoids, Freeman, 1973). Boyce (1974) found 2 of 2000 Cyclops

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scutijier from Babine Lake naturally infected by procercoids of E. salvelini during May to July. In experimental invasions of Oncorhynchus nerka at 10°C Boyce (1974) noted the onset of segmentation of the established cestodes by 30 days, but the development of the E. salvelini was not followed beyond 43 days. In Babine Lake early invasions were seen about 23 May, and the earliest mature worms in these fishes by 19 October of the same year. One of the mature worms was shedding eggs. Thus adult worms were achieved in the natural summer water temperatures of Babine Lake in 5 months, but Boyce (1974) postulated that the majority of the eggs from gravid E. salvelini would be released the following spring, as water temperatures were too low in winter. Smith (1973) summarized the dynamics of infection of Oncorhynchus nerka in Babine Lake as follows. Several million smolts, many infected with gravid Eubothrium salvelini, passed through the greater length of the lake each spring. These smolts released eggs which seemed likely to provide the prime source of invasion for the next 0.nerka year class. If correct, these eggs which were coincident with the known seasonal abundance of cyclopoid copepods, together with the changing food preferences of young 0. nerka, suggested a sequence of invasion consistent with the timing and behaviour of young 0. nerka and which accounted for the midsummer strobilization seen in incidences of E. sulvelini in underyearling fishes. Cyclopoids were commonest early spring and declined to a seasonal low in July. In the North Arm of Babine Lake juvenile 0. nerka stopped eating copepods by mid-August, which minimized new invasions thereafter and produced a stable incidence of infection in the underyearling fishes in August to October. The south to northward movement of spring the following year, with its concurrent warming of the lake waters and migration of smolts of 0. nerka, would once again ensure stabilization of infection levels in the same sequence as the previous year. Smith (1973) considered that two other factors could have terminated new cestode invasions of fishes after midsummer. E. salvelini eggs released in spring could by summer have sunk to the lake bottom, or below the level of easy access to copepods, or could have died naturally. Secondly, of the two generations of copepods per annum in Babine Lake, the first in May-June had a life span of 3 to 4 months, and the second in September had a life span of 8 to 12 months. Individuals of the May-June generation might be too small to ingest the cestode eggs at that time, hence would remain uninvaded, whilst the September generation which survived until the following spring could serve as the main intermediate hosts in the life cycle of E. salvelini in Babine Lake (Smith, 1973). Sandeman and Pippy (1967), in Salvelinus fontinalis, Salmo gairdneri, S. salar (landlocked) and S. truttu in Insular Newfoundland also found a seasonal maturation of Eubothrium sulvelini. Spring and summer cestodes were gravid, whereas those recovered in late August, September and later were immature worms only. Recruitment was considered to occur during August, followed by maturation during the winter months and spring, and release of eggs and death of the spent worms by late summer.

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In Lake Michigan, U.S.A., Amin (1977) made a few observations of Eubothrium sulvelini in four species of salmonids. These revealed mature adults in March, May, August, October and November. Kuperman (1978) studied the life cycle of Eubothrium salvelini in the lakes of Kamchatka, U.S.S.R. The procercoids occurred in Cyclops scutifer, the plerocercoids (acaudate bothrio-plerocercoids) in the intestines of five species of small, or juvenile, fishes, and the principal definitive hosts were lacustrine Salmo mykiss and Sulvelinus ulpinus. B.

CLASS EUCESTODA

1. Order Proteocephalidea Zschokke (1 884), Kraemer (1892), Riggenbach (1 896) and other early workers mention seasonal patterns of maturation in the genus Proteocephalus [as Taenia in Zschokke (1 884), Zchthyotaenia in Kraemer (1882) and Riggenbach (1896)] but do not give details. La Rue (1914) conveniently summarized the early studies about the Order (as Family). More recently Freze (1965a, b, 1966) has surveyed the literature concerning the classification and biology of the Order. In summary, the life cycle involves a copepod intermediate host, in which the procercoid larvae develop (caudate culcitacetabuloplerocercoid I, according to Freeman, 1973, and often termed plerocercoid larvae). On ingestion by plankton-feeding fishes these larvae are usually called plerocercoids (culcitacetabula-plerocercoid 11, Freeman, 1973) and in many instances where requirements of definitive host specificity are met these plerocercoids will grow to sexual maturity at the appropriate season of the year. However, in some species of Proteocephalidea a reservoir fish host may occur in the life cycle, in which the plerocercoids persist in the intestine lumen, but without growth or maturation. On ingestion of the reservoir fishes by a definitive fish host development of the plerocercoids to ultimate maturity occurs (Freze, 1965a, 1965b). In a few species, for instance Proteocephalus ambloplitis (see p. 82), parenteric and enteric phases of development occur in the definitive fishes before sexual maturity of the cestode is achieved. Freze (1965b) has indicated that an annual pattern of development was usual, with the plerocercoid stage prevailing in the definitive host fishes, these developing to maturity giving a period of maximum occurrence of sexually mature cestodes in spring and summer, followed by a rapid decline in adult numbers towards autumn. Freze (1966) was of the opinion that ecological factors had a greater influence on incidence of proteocephalids in fishes rather than variations in the physiological condition of the alimentary tract of the host. Brooks (1978) has recently reviewed the evolutionary history of the Proteocephalidea. His supraspecific classification differs only slightly from previous schemes. (a) Family Proteocephalidae. The division of the genus Corallobothrium into three genera proposed by Freze (1965b) is not used in this review.

H E L M I N T H S I N F R E S H W A T E R FISHES

71

Corallobothriumjimbriatum Essex, 1927 Details of the life cycle of Corallobothrium jimbriatum were given by Essex (1 927). Procercoids were obtained in Cyclops serrulatus, C. bicuspidatus and C.prasinus by the twelfth day, and these larvae were fed to Notropis blennius where they were recovered from the intestine, coelom and musculature. Ictaluruspunctatus 5 to 8 cm long were found to harbour adult cestodes, and Essex (1927) suggested that the life cycle could be completed either direct by ingestion of infected Cyclops or indirectly by feeding on N . blennius. Freeman (1973) has proposed alternative names for the larval stages described by Essex (1927). The adults of C.fimbriatum appeared in late spring and early summer, to reach a maximum occurrence during June and July and disappeared entirely by the latter part of October or early November. However plerocercoids were present in the definitive fishes at all times of the year. Essex (1927) also quoted information collected by Mr R. E. Richardson from I.punctatus which showed that adults were present from June to September, but not October to May. Edwards et ul. (1977) also reported segmented adults only during the summer and immature forms during spring and autumn, whilst Gruninger et al. (1977) noted that no one season yielded a higher burden of worms per fish, but did not give details of maturity of these cestodes (hosts and localities see Table 111). Corallobothrium giganteum Essex, 1927 The genus Megathylacoides was proposed by Freze (1965b) to include four species of North American Corallobothrium, including C. giganteum. However, in this review the original genus Corallobothrium is retained. As in CorallobothriumJimbriatum Essex (1927) found adult worms appearing in early summer to reach a maximum in June and July and to disappear by early autumn, although the plerocercoids were present in the host intestines at all seasons. The two species occurred most commonly in Ictaluruspunctatus and the majority of the information given by Essex (1927) was collected from fishes obtained in Rock River, U.S.A. Edwards et al. (1977) from the Kentucky River drainage, Kentucky, U.S.A., also noted the same seasonal pattern of occurrence of adult worms. Corallobothrium minutium Fritts, 1959 Freze (1965b) erected the genus Corallotaenia to include Corallobothrium parvum Larsh, 1941, C. intermedium Fritts, 1959 and C. minutium Fritts, 1959, and he considered that the latter two species were synonymous and retained the name Corallotaenia intermedia. For the moment the name Corallobothrium minutium is retained, although Befus and Freeman (1973) used Corallotaenia minutia for their study of the species in lakes in Algonquin Park, Ontario, Canada. Ictalurus nebulosus were infected in almost all these lakes. At all times of the year plerocercoids and non-gravid worms were recovered from the intestines of the fishes, but gravid adults were found only during the summer, between 7 June and 20 August, in potentially reproductive fishes of length more than 100 mm. Incidence generally increased with host length. The growth of C. minutium in copepod intermediate hosts was studied. To facilitate understanding, Befus and Freeman (1973) separated two phases of larval development in copepods phase I, the growth period which began

4 h,

TABLE111 Studies on seasonal occurrence of cestodes of the order Proteocephalidea listed in the climate zones of the World (see map Fig. 1, Chubb, 1977). The species are in alphabetical order Climate zones

Cestode species

1. Tropical la. RAINY (humid climate) lb. SAVANNA (humid climate) lc. HIGHLAND (humid climate) Id. SEMI-DESERT (dry climate) le. DESERT (dry climate) 2. Sub-tropical 2a. MEDITERRANEAN Proteocephalus macrocephalus Proteocephalus tumidocollus

Host species

no seasonal studies

tropical forest

no seasonal studies

tropical grassland

no seasonal studies

tropical highland

no seasonal studies

hot semi-desert

no seasonal studies

hot desert

Anguilla anguilla Salmo gairdneri Salvelinus fontinalis

2b. HUMID Proteocephalus ambloplitis

Locality

Micropterus salmoides

Proteocephalusplecoglossi Plecoglossus altivelis

scrub, woodland, olive Lake Skadar, Yugoslavia Loma Linda and Mentone, California, USA deciduous forest Par Pond, Savannah River Plant, Aiken, South Carolina, USA Lake Biwa, Japan

References

KaiiC (1970) Wagner (1953, 1954)

Eure (1974, 1975, 1976a), Eure and Esch (1974) Kataoka and Monma (1934)

3. Mid-latitude 3ai. HUMID WARM SUMMERS

temperate grassland, mixed forest Corallobothrium Ictalurus punctatus Kentucky River jimbriatum drainage, Kentucky, USA Rock River, Mississippi mostly Ictalurus punctatus River, USA Ictalurus punctatus Eagle Mountain Lake, Texas, USA Corallobothrium giganteum Ictalurus punctatus Kentucky River drainage, Kentucky, USA mostly Ictalurus punctatus Rock River, Mississippi River, USA Corallobothrium Ictalurus punctatus Lake Carl Blackwell, jimbriatum Oklahoma, USA Corallobothrium giganteum (mixed infections) Corallobothrium species Ictalurus punctatus Kentucky River drainage, Kentucky, USA Proteocephalus cernua

Proteocephalus dubius

Gymnocephalus cernua Gymnocephalus schraetser Stizostedion volgense Gymnocephalus cernua Gymnocephalus cernua Perca fluviatilis

River Danube, Bulgaria

Edwards et al. (1977) Essex (1927) Gruninger et al. (1977) Edwards et al. (1977) Essex (1927) Spa11 and Summerfelt (1969) Edwards et af. (1977)

Kakacheva-Avramova (1 977)

Lake Balaton, Hungary Molnar (1966a) Lake Balaton, Hungary Ponyi et al. (1972) Lake Lkman (Geneva), Zschokke (1884) Switzerland

4 P

TABLE111 (continued)

Climate zones

Cestode species

Host species

Locality

References

3ai. (continued) Proteocephalus exiguus Proteocephalus fallax

Coregonus albula Coregonusfera Coregonusfera

Proteocephalusjilicollis

Gasterosteus aculeatus

Proteocephalus longicollis Coregonus albula Proteocephalus percae

Perca fluviatilis Lucioperca lucioperca Esox lucius Perca .fluviatilis

Esox lucius Perca fluviatilis Proteocephalus stizostethi Stizostedion vitreum vitreum Proteocephalus torulosus Alburnus alburnus Leuciscus idus Rutilus rutilus Perca fluviatilis Squalius lepusculus

Poland Lake Lucern, Switzerland Lake Lkman (Geneva), Switzerland Lake Czerniakow, Poland Lakes Lansk and Maruski, Poland Hel-Zatoka, Baltic Sea, Poland Lake Balaton, Hungary Macha Lake fish pond system, North Bohemia, Czechoslovakia Lake Kals, Latvia, USSR Lake Erie, Michigan, USA River Danube, Bulgaria Podgbrady, Czechoslovakia

Kuczkowski (1925) Kraemer (1892) Zschokke (1884) Kuczkowski (1925) Kozicka (1949) Markowski (1933) Molnar (1966a) Moravec (1979b)

Reinsone (1955) Conor (1953)

Kakacheva-Avramova (1977) Sramek (1901)

Leuciscus idus Alburnus alburnus Proteocephalus species

Coregonus fera Alosa finta Coregonus lavaretus Perca fluviatilis

Silurotaenia siluri

Silurus glanis

3aii. HUMID COOL SUMMERS Corallobothrium minutium Ictalurus nebulosus Corallobothrium parafimbriatum Proteocephalus ambiguus

Ictalurus nebulosus Pungitius pungitius

Proteocephalus ambloplitis Micropterus salmoides Micropterus dolomieui Proteocephalus buplanensis Semotilus atromaculatus Proteocephalus cernua

Gymnocephalus cernua

Proteocephalus esocis

Esox lucius Esox lucius

Germany Lake Lkman (Geneva), Switzerland Lake Lkman (Geneva), Switzerland Lake Maggiore, Italy

Wagner (1917) Zschokke (1884) Jarecka and Doby (1965) Grimaldi (1964)

Lake Galwe, Wilno Wierzbicka (1951) Region, Poland River Danube, Kakacheva-Avramova Bulgaria (1 977) temperate grassland, mixed forest Lakes, Algonquin Park, Befus and Freeman Ontario, Canada (1973) Lakes, Algonquin Park, Befus and Freeman Ontario, Canada (1973) Obersee, near Tallinn, Schneider (1902) Estonia, USSR Gull Lake, Michigan, Esch et al. (1975) USA Lake Opeongo, Ontario, Fischer and Freeman Canada (1969, 1973) Pike River, Wisconsin, Amin and Mackiewicz USA (1977) Rybinsk Reservoir, Izyumova (1959a) USSR Rybinsk Reservoir, Izyumova (1960) USSR Lake Dusia, Lithuania, Rautskis (1970b) USSR

4 VI

4

TABLE I11 (continued) Climate zones

Cestode species

Host species

o\

Locality

References

3aii. (continued) Proteocephalus exiguus Proteocephalus filicollis Proteocephalus fluviatilis Proteocephalus parallacticus Proteocephahspearsei

Proteocephalus percae (larvae in fishes) Proteocephalus percae

Coregonus clupeaformis Lake Michigan, USA Amin (1977) Bauer and Nikol’skaya Coregonus lavaretus baeri Lake Ladoga, USSR natio ladogae (1957) Gasterosteus aculeatus River Chernaya, near Banina and Isakov Pungitius pungitius River Neva, USSR (1972) Micropterus dolomieui Lake Opeongo, Ontario, Fischer (1968,1974) Canada Lake Opeongo, Ontario, Freeman (1961,1964) Salvelinus namaycush Canada (mainly) Lake Opeongo, Ontario, MacLulich (1943) Salvelinus namaycush Canada Perca flavescens Lake Opeongo, Ontario, Cannon (1973) Canada Lake Opeongo, Ontario, Fischer (1974) Micropterus dolomieui Canada Perca flavescens Yahara River Lakes, Pearse (1924) Perca flavescens Wisconsin, USA Perca flavescens Tedla and Fernando Bay of Quinte, Lake Ontario, Canada (1 969) Lucioperca lucioperca Rybinsk Reservoir, Izyumova (1958) USSR Esox lucius River Volga, USSR Bogdanova (1958) Lucioperca lucioperca Rybinsk Reservoir, Izyumova (1958) USSR Rybinsk Reservoir, Izyumova (1959a) Gymnocephalus cernua USSR

Perca fluviatilis

Lake Dusia, Lithuania, Rautskis (1970a)

Proteocephalus torulosus

Abramis ballerus

Proteocephalus pinguis

Esox reticulatus

Proteocephalus ambiguus

Pungitius pungitius

Proteocephalus cernua Proteocephalus filicollis

Gymnocephalus cernua Gasterosteus aculeatus

Rybinsk Reservoir, Izyumova (1960) USSR temperate grassland, mixed forest Barrett and China Hunter (1929) ponds, near Carmel, New York, USA temperate grasslands, deciduous forest Amsterdam, Willemse (1965, 1968) Netherlands Netherlands Willemse (1965, 1969) Pond, Baildon Moor, Chappell (1969a) Yorkshire, England Shoulder of Mutton Dartnall (1972) Pond, and Hadleigh Marsh, England Lochan, near Bellshill, Hopkins (1959) North Lanarkshire, Scotland. Edgbaston Reservoir, Meggitt (1914) Birmingham, England Bunnefjorden, south of Rradland (1979) Oslo, Norway Various habitats, Willemse (1965, 1967, Netherlands 1968) Various habitats, Willemse (1965, 1969) Netherlands

USSR

3aiii. EAST COAST

3b. MARINE WEST COAST

Gasterosteus aculeatus Gasterosteus aculeatus Gasterosteus aculeatus Gasterosteus aculeatus Gasterosteus aculeatus Proteocephalus macrocephalus

Anguilla anguilla

4 4

4 W

TABLEI11 (continued) Climate zones

Cestode species

Host species

Locality

References

3b. (continued) Proteocephalus neglectus

Salmo trutta Salmo trutta

Proteocephalus percae

Perca fluviatilis Perca fluviatilis Perca fluviatilis Perca fluviatilis Gymnocephalus cernua Perca fluviatilis Perca fluviatilis Esox lucius Perca fluviatilis Perca fluviatilis Perca fluviatilis

Proteocephalus primaverus

Salmo clarki

Proteocephalus tetrastomus

Osmerus eperlanus

Chirk Fish Hatchery, Clwyd, Wales River Alyn, Clwyd, Wales Lake Reryetjern, Norway River Glomma, Norway Serpentine, London England Shropshire Union Canal, Cheshire, England Lakes, outskirts of Berlin, Germany Rostherne Mere, Cheshire, England Lake Dargin, Poland Various habitats, Netherlands Hanningfield Reservoir, Essex, England Lakes near Stevenson, Washington State

Aderounmu (personal communication) Rahim (1974) Andersen (1978) Halvorsen (1972) Lee (1977) Mishra (1966) Priemer (1979) Rizvi (1964, 1968) Wierzbicki (1970, 1971) Willemse (1965, 1967, 1969) Wootten (1974) Neiland (1952)

USA Various habitats, Netherlands

Willemse (1965, 1967, 1969)

Proteocephalus torulosus

Leuciscus cephalus Leuciscus leuciscus Leuciscus leuciscus

Proteocephalus species

Abramis ballerus Coregonus lavaretus Coregonus lavaretus Salmo gairdneri Salmo trutta

3 ~ .SEMI-DESERT

3d. DESERT

Proteocephalus esocis Proteocephalus osculatus

Esox lucius Silurus glanis Silurus glanis

Proteocephalus percae Proteocephalus torulosus

Lucioperca lucioperca Abramis brama Blicca bjoerkna Pelecus cultratus Vimba vimba vimba natio carinata no seasonal studies

Davies (1967) River Lugg, Herefordshire, England River Avon, Kennedy and Hine Hampshire, England (1969), Kennedy (19724 Lake Dqbie, Poland Wierzbicka (1978) Llyn Tegid, Wales Ablett (personal communication) Llyn Tegid, Wales Farenden (personal communication) Fish farm, Movanagher, Arme and Ingham County Antrim, (1972) Ireland Lakes Ovre Heimdal Lien and Borgstrom and Horns, Southern (1973) Norway prairie and steppe Dnepr Delta, USSR Komarova (1964) Volga Delta, USSR Dubinina (1949, 1950) Mingechaur Reservoir, Mikailov (1963) Azerbaidan, USSR Volga Delta, USSR Dubinina (1949) Dnepr Delta, USSR Komarova (1964)

cool desert

CQ

0

TABLE111 (continued) Climate zones

Cestode species

Host species

3e. SUB-POLAR Proteocephaius exiguus

Coregonus clupeaformis Coregonus albula

Proteocephalus filicollis

Coregonus artedii

Proteocephalus percae

Perca fluviatilis Perca jluviatilis

Proteocephalus torulosus

Proteocephaius species

1. Polar 4a. POLAR 4b. ICE-CAPS

Perca jluviatilis Alburnus alburnus Leuciscus idus Leuciscus leuciscus Cyprinids Esox Iucius Rutilus rutilus

no seasonal studies no suitable habitats for freshwater cestodes

5. Mountain Proteocephalus species

Salmo trutta

Locality

References

coniferous forest Cold Lake, Alberta, Leong (1975) Canada Lakes Vendursk and Malakhova and Uros, Karelia, USSR Anikieva (1975) Cold Lake, Alberta, Leong (1975) Canada Lakes Kimas, Luv and Ieshko et al. (1976) Vendurskom, Karelia, USSR Lake Konche, Karelia, Malakhova (1961) USSR Malakhova et al. (1978) Karelia, USSR Ieshko et al. (1976) Lakes Kimas, Luv and Vendurskom, Karelia, USSR Malakhova et al. (1978) Karelia, USSR Lake Konche, Karelia, Malakhova (1 961) USSR tundra icefields and glaciers heath, rocks and scree Lake Melingen, VBg5 and Lake Nedre Fipling, Vefsn, Norway

Halvorsen and Macdonald (1972)

HELMINTHS I N FRESHWATER FISHES

81

when the larva reached the haemocoel of the copepod, and phase 11, the differentiation stage, which began with the appearance of the cercomer. Differentiation was completed when the cercomer was lost and the scolex retracted or invaginated into the mid-body. Fully differentiated plerocercoids were found only in Cyclops vernulis. Two plerocercoid phases plerocercoid I in copepods and plerocercoid I1 in fishes were differentiated. Parenteral plerocercoid I1 of C. minutium were common in the viscera of I. nebulosus. Preliminary experiments of feeding infected copepods to I. nebulosus showed that at least some plerocercoids entered the viscera, but Befus and Freeman (1973) were of the opinion that there was insufficient information to determine if the life cycle of C. minutium was similar to that of Proteocephalus ambloplitis (see p. 82), in which parenteral development in the definitive host was essential. Befus and Freeman (1973) suggested that C. minutium probably required more than one year to complete its life cycle. Corallobothrium parajimbriatum Befus and Freeman, 1973 Corallobothrium parajimbriatum were found in the upper intestines of Ictalurus nebulosus in lakes at Algonquin Park, Ontario, Canada, by Befus and Freeman (1973). Egg shedding adult cestodes occurred in fishes more than 100 mm long between 1 June and 1I September. Plerocercoids were seen in the intestines of the fishes throughout the year. In this species of cestode a parenteral plerocercoid phase was not necessary. In Billy Lake, where C. parajimbriatum was the only species of Corallobothrium present, parenteral plerocercoids were not seen. Experimental observations suggested that the plerocercoids ingested by I. nebulosus remained in the intestine, to grow and differentiate as plerocercoids, but to lose their end organs before adult development began. The life cycle might be completed in one summer, but probably needed more than one year for completion according to Befus and Freeman (1973). Corallobothrium parvum Larsh, 1941 As Corallotaenid parva in Freze (1965b), but here retained in the genus Corallobothrium. The annual pattern of occurrence is probably similar to C. minutium, as Larsh (1 941) experimentally demonstrated that plerocercoids occurred in both the intestine and body cavity of the tropical fish Glaridichthys talcatus. Corallobothrium species Spa11 and Summerfelt (1969) at Lake Carl Blackwell, Oklahoma, U.S.A., studied the combined occurrences of Corallobothrium jimbriutum and C. giganteum in Ictalurus punctutus together with a Proteocephalus species. Considerable and highly significant changes in incidence were seen (all fishes and ages) : summer 40 %, autumn 78.6 %, winter 89.7 % and spring 92.3 %. Incidence paralleled changes in extent of intensity, strobilization and maturation of the worms. Thus increased incidence during autumn and winter corresponded to an increase in average parasite load and also in size of each worm. Fragmentation of fully mature (gravid) worms was observed-throughout the late winter and spring, and at the same time a fall of occurrence indicated a loss of worms from the host. Non-segmented, immature worms

82

J A M E S C. C H U B B

occurred all year but were most common during the autumn months (Spa11 and Summerfelt, 1969). Edwards et al. (1977) noted an immature form of Corallobothrium species in Ictalurus punctatus from the Kentucky River drainage, Kentucky, U.S.A., which was capable of inhabiting the definitive host year round. Proteocephalus ambiguus (Dujardin, 1845) Schneider (1902) reported this species from Pungitius pungitius at Obersee, near Tallinn (as Reval), Estonia. Most of his mature material was collected in May and June. La Rue (1914) regarded P. ambiguus and P.filicollis as the same species, but Willenise (1968) has shown that the two are distinct. Willemse (1965) completed the life cycle in the laboratory using Cyclops strenuus as intermediate host, and additionally was able to transplant worms experimentally from one fish to another, suggesting that cannibalism could carry the infection from small to large P.pungitius. In the Netherlands no regular cycle of incidence, growth or genital development occurred (Willemse, 1965, 1968). Gravid worms were found in all months from March 1963 to February 1964. Proteocephalus ambloplitis (Leidy, 1887) In Proteocephalus ambloplitis two stages occur in the definitive host fishes, parenteric plerocercoids and enteric adults. A life cycle for P. ambloplitis was postulated by Cooper (1918) involving a sequence of egg, entomostracan, small fish with parenteric plerocercoids and a predatory definitive fish host containing the adult worms. Hunter (1927, 1928) and Hunter and Hunter (1929) experimentally infected Cyclops albidus, C. prasinus, C. serrulatus and C. viridis to obtain procercoids and infected fry of Micropterus dolomieui and M . salmoides to recover plerocercoid larvae in the viscera. Feeding of the fry to yearling M . salmoides resulted in the recovery of enteric plerocercoids. Bangham (1927a) also observed 50 to 80 mm Micropterus salmoides become infected by procercoids of P. ambloplitis from cyclopoid copepods during the summer. However, the studies of Fischer and Freeman (1969, 1973) have shown that the life cycle is rather more complex than that understood by the earlier workers. In outline, Fischer and Freeman (1969, 1973) showed that the life cycle was : egg containing oncosphere eaten by copepod, to give plerocercoid I (=procercoid, above; acaudate invaginated glandacetabulo-plerocercoid I according to Freeman, 1973). If the plerocercoid I in the copepod was ingested by a species of Micropterus or another genus of fishes further growth would be parenteral, to give an initial plerocercoid 11. In Lake Opeongo, Ontario, Canada, where the Fischer and Freeman (1969, 1973) studies were carried out only Micropterus dolomieui had some factor(s) which permitted the initial plerocercoid I1 to complete parenteral development to a middle plerocercoid 11, which was an essential stage. The middle plerocercoid I1 reached the intestine of the definitive host, M . dolomieui in Lake Opeongo, either by direct entry from parenteral sites in the same host, or following cannibalism. In the intestine the middle plerocercoid .I1 completed a terminal phase of development (plerocercoid I1 larvae were invaginated glandacetabulo-plerocercoid I1 according to Freeman, 1973). Growth

H E L M I N T H S IN F R E S H W A T E R FISHES

83

thereafter, at the appropriate season, resulted in the strobilate adult (Fischer and Freeman, 1973). Fischer and Freeman (1969) at Lake Opeongo found that all Micropterus dolomieui 76 mm long or more caught between April and October, 1963 to 1968 had parenteral plerocercoids. However the occurrence of adult worms in the intestine was markedly seasonal: incidence was maxima1 May (loo%), falling June (80%), July (5779, August (52%) to a minimum September (33 %). Egg shedding adults (average per host) occurred June ( O e O l ) , July (1.7, maximum), August (1.3) and September (about 1). The migration of parenteric plerocercoids to the intestine was seen to occur in spring (May, also June). M . dolomieui captured during summer and kept at 4°C for two months did not have intestinal P. ambloplitis when killed. In Lake Opeongo migrating plerocercoids were found in May (102 in 24 of 68 fishes) and June (2 fishes only) but none thereafter. However, all fishes had plerocercoids in the viscera through the summer (July-October). Thus, at Lake Opeongo the plerocercoid migration occurred only during the spring rise in water temperature, from 4°C or less (winter), to 7 to 12°C. The temperature threshold for migration was thought by Fischer and Freeman (1969) to be between 5.5 to 7"C, since only two days at 7°C produced a massive migration. It was concluded that host hormonal factors might enhance the effect of temperature on the migration of the plerocercoids, as in 10 of 15 M . dolomieui less than 150 mm long no plerocercoids migrated, i.e, in the most immature fishes. Fischer and Freeman (1973) showed experimentally that plerocercoids of Proteocephalus ambloplitis must complete development parenterally in Micropterus dolomieui ( M . salmoides also elsewhere, see below) before they could become terminal plerocercoids in the intestine, that although fishes other than M . dolomieui might not be (true) intermediate hosts, they were an essential link for movement of the larvae from copepods to M . dolomieui, and that when these parenteral plerocercoids from fishes other than M . dolomieui were eaten by this host, such plerocercoids re-entered the viscera of the M . dolomieui. Terminal plerocercoids were acquired by the definitive host only from parenteral plerocercoids from its own viscera entering the intestine lumen, or by ingesting suitable parenteral or terminal plerocercoids from other M . dolomieui. Fischer and Freeman (1973) were of the opinion that if M . dolomieui did not harbour terminal plerocercoids I1 in the intestine by early summer, after re-entry of middle plerocercoid I1 from its own parentera1 tissues, it was unlikely that such M . dolomieui would produce gravid P. ambloplitis that year. Esch and Huffines (1973) noted more extensive damage from plerocercoid migration of Proteocephalus amblopliris in Micropterus salmoides in Gull Lake, Michigan, U.S.A., during June to August, rather than in spring and autumn. Eure (1974, 1975, 1976a), Eure and Esch (1974) and Esch et al. (1975) have provided further data concerning the seasonal biology of Proteocephalus ambloplitis. Esch et al. (1975) examined the seasonal changes of the adult worms in Micropterus dolomieui from Gull Lake, Michigan, U.S.A. Water

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temperatures were 4°C (11 April), 17°C (24 May), 24°C (8 July, 24 August) and 21°C (6 October). During the period of investigation a 100 % incidence of parenteric plerocercoids was seen. At Gull Lake the rise in water temperature from 4 to 7°C occurred mid-April, but enteric plerocercoids were not seen in most fishes until 20 May. The first egg shedding P. ambloplitis were seen on 28 May, and after this date about half of the sexually mature M . dolomieui had gravid worms, although this number began to decline from late August. At Gull Lake the enteric cestodes occurred in substantial numbers at a water temperature of 14"C, or higher. By October infections of adult cestodes were about 25 %, and Esch et al. (1975) suggested that the M . dolomieui were free of enteric worms during winter. They considered the absence of P . ambloplitis from the intestine of the definitive host during winter a phenomenon of northern latitudes, as in South Carolina (see below) they were present in January. Esch et al. (1975), based on the comparison of their Gull Lake study, and the investigation of Eure (1974, reported from Eure, 1976a in this review) postulated that the P. ambloplitis-M. dolomieui systems in Gull Lake and Lake Opeongo (Fischer and Freeman, 1969, 1973 see above) either were variable owing to differential latitudinal distribution, or that breeding condition (more likely hormone state) of the host was important in stimulating parenteric plerocercoids to migrate, or that a combination of these hypotheses along with temperature were involved. Esch et al. (1975) offered evidence supporting hormonal involvement as : sexually immature M . dolomieui (less 200 mm) were without adult P.ambloplitis, even though all had parenteric plerocercoids, and, their data plus those of Fischer and Freeman (1969, 1973) supported the fact that recruitment of adult cestodes was a n event which occurred but once a year. Even though water temperatures in both lakes were high throughout summer, nonetheless all M. dolomieui had parenteric plerocercoids, and migration did not occur. Freeman (personal communication to Esch et a[., 1975) suggested that the stimulation for plerocercoid migration was not high water temperatures per se, but the rise in water temperature from 4 to 7°C or higher, and the maintenance of the fishes at that temperature for at least two days. Notwithstanding this idea, Esch et al. (1975) felt that other springtime events such as increasing photoperiod per day and an unique combination of gonadotrophic and gonadal hormones within the host could also be potential stimuli for initiation of the migration of the parenteric plerocercoids. A main objection to the Fischer and Freeman (1969) temperature hypothesis was the finding by Ewe (1 976a) of adult Proteocephalus ambloplitis in Micropterus salmoides at Par Pond, Savannah River Plant, Aiken, South Carolina, U.S.A., during the month of January (Esch et al., 1975). The seasonal peak of enteric adults in Par Pond was mid-winter, from December incidence increased through January, fell February, March to April, increased May, to fall June through August to nothing by September to November (Eure, 1976a). This peak did not coincide with a rise in water temperature from 4 to 7"C, since at Par Pond the average minimum water temperature in January was 11°C (minimum SOC), with a maximum of 27°C during July to

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September (Eure, 1976a). In Par Pond the migration of the parenteric plerocercoids was found to occur at a water temperature of ll.5"C. Eure (1976a) suggested that the migration might be induced by an abrupt change in water temperature from some constant level to a radically different level. If correct this alternative temperature hypothesis explained the difference between northern and southern latitudes. Provided that a water temperature of 7 to 12°C was critical for plerocercoid migration, then in northern latitudes the water temperatures would need to increase (from 4 to 7°C) and decrease in southern latitudes (from 26°C to 11°C). Thus critical temperatures would be reached in spring in northern latitudes but would be present during early winter in southern latitudes (Eure, 1976a). It should be noted that other factors are also likely to be involved, as in northern latitudes water temperatures fall from a summer high, through 12 to 7°C in the autumn, to a winter minimum of 4°C or thereabout. Nonetheless, there are no reports of autumn migrations of parenteric plerocercoids in these latitudes as far as the author is aware. Thus, as Esch et al. (1975) suggested, the observations do strongly suggest other interrelated factors may be necessary to provide the appropriate stimulus for parenteric plerocercoid migration. Some in vitro studies might elucidate the exact triggering mechanism. Larval Proteocephalus ambloplitis have been reported on a seasonal basis, in addition to the studies reported above, by Becker (1967), Spa11and Summerfelt (1969), McDaniel and Bailey (1974) and Cloutman (1975). Becker (1967) found that the larvae tended to concentrate in the liver of Salmo gairdneri appearing in spring-planted fishes during summer. The summer invasions were correlated with warm water temperatures in Shoecraft Lake, Washington State, U.S.A., as well as the reproduction of adult cestodes in bass. McDaniel and Bailey (1974), at three habitats in Oklahoma, U.S.A., noted that there appeared to be two peaks of larval occurrence in Lepomis species, spring and late summer, and they considered that these might reflect the zooplankton peak pulses of occurrence, in autumn and spring respectively. Cloutman (1975) at Lake Fort Smith, Arkansas, U.S.A., observed the plerocercoids in Lepomis gulosus and Micropderus salmoides during all months of the year. Hoffman (1967) has stated that the plerocercoids of Proteocephalus ambloplitis have been reported from the viscera of many species of North American fishes, but warned that these indentifications should be checked experimentally because the larval worms could have been other species of Proteocephalus, or perhaps Corallobothrium. Proteocephulus buplanensis Mayes, 1976 Amin and Mackiewicz (1977) found this species in Semotilus atromaculatus in the Pike River, Wisconsin, U.S.A. A seasonal cycle occurred, with light infections of young, small, worms in autumn and more frequent occurrences of large, mature, cestodes in spring. None of nine S. atromuculatus examined in summer were infested. Competitive exclusion between P. buplanensis and Acanthocephalus parksidei was seen. Proteocephalus cernua (Gmelin, 1790) Izyumova (1 959a) reported incidences (and intensities) in Gymnocephalus

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cernua at the Rybinsk Reservoir, U.S.S.R., as: winter 8.99% (2-5); spring 20.83% (2-24); summer 0%; and autumn 13.33% (1). However a more detailed seasonal study was performed by Molnar (1966a) in Lake Balaton, Hungary. An infection of G. cernua was present all year, although maximum intensities of infection were seen during the winter. In May and June the majority of the fishes were infected but with fewer worms than in winter: most G. cernua contained one or two egg laying worms in May and June. In July-August minimal numbers occurred. In August invasion of fishes ceased, owing to the intermediate hosts not being available. Invasion occurred during the winter. Adult Proteocephalus cernua produced eggs from spring until July, especially in older fishes, then the majority of the cestodes were lost. Some young G. cernua contained fully mature worms 10 to 30 mm long during October (MolnBr, 1966a). Willemse (1965) completed the life cycle in the laboratory using Cyclops strenuus as intermediate host. Experimental transplants, Gymnocephalus cernua to G. cernua, were very successful, indicating that cannibalism could transfer the infection from small to large hosts. Willemse (1965, 1969) examined fishes from the Netherlands during March to October only. Throughout this period incidence did not vary very much and ripe eggs were present from April to October. Ponyi et al. (1972) presented some further data from Lake Balaton, Hungary, finding an essentially similar pattern of occurrence in Gymnocephalus cernua between May and October as that observed earlier by Molnar (1966a). Kakacheva-Avramova (1977) reported this species of cestode during spring and summer in G. cernua, G. schraetser and Stizostedion volgense from the River Danube, Bulgaria. Proteocephalus dubius La Rue, 1911 Freze (1965b) doubted the validity of this species, which is very close to Proteocephalus percae. Zschokke (1884) reported these cestodes (as Taenia Jilicollis) from PercafEuviatilis in Lake LCman, Switzerland, in February and March. His reports of Taenia ocellata from P. fEuviatilisfrom the same habitat may also be this species. In winter Zschokke (1884) always found young individuals with segmentation little developed and without genitalia. The latter organs appeared at the end of March and maturity was achieved by July and August. Proteocephalus esocis (Schneider, 1905) A parasite of Esox lucius, Izyumova (1960) found the following incidences (and maximum intensities) at the Rybinsk Reservoir, U.S.S.R. : winter 6.6 % (3); spring 20% (13); summer 6.6% (3); and autumn 0%. At the Dnepr Delta, U.S.S.R., Komarova (1964) did not find it in E. lucius in February or October, but did in March (26.6 %, 3-26) and April-May (3.7 %, 2). Rautskis (1970b) at Lake Dusia, Lithuania, U.S.S.R., did not observe Proteocephalus esocis in January-March or June-July, but did in April-May (6.2 %, range 1, average 1) and October-November (53.3%, 1-12, 4.7).

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Proteocephulus exiguus La Rue, 1911 A parasite of coregonids according to Freze (1965b), who expanded the diagnosis of the species. However Freze and Kazakov (1969) thought it to represent a collective species requiring revision. Kuczkowski (1925) found this species (as Ichthyotaeniu longicollis) in Coregonusulbula in Poland. A mass infection recovered in December consisted of worms full of eggs. CycZops serrulatus and C. strenuus were successfully infected experimentally. At Lake Ladoga, U.S.S.R., Bauer and Nikol’skaya (1957) examined Coregonus luvaretus baeri natio ludogae from July to November. Incidences (and average intensities) of infection were : July 27 % (0.7); August 47% (4.5); September 40% (3-9); October 20% (2.8); and November 27% (0.7). In July young worms predominated, with adults in August. The increase in incidence July-August was attributed to feeding on Cyclops species, the intermediate hosts. Malakhova and Anikieva (1975) studied the biology of Proteocephulus exiguus in Coregonus ulbulu in Lakes Vendursk and Uros, Karelia, U.S.S.R., between 1964 and 1973. Incidences varied between 48.9 to 99% in Lake Vendursk and 68.6% to 99.4% in Lake Uros. The most intense infections were seen in years with hot summers which favoured reproduction of the intermediate hosts. However invasion of fishes occurred during all times of the year. Some cestodes were able to reach maturity during a summer, in four months. Malakhova and Anikieva (1975) recognized three stages of development of worms : Stage 1,young forms; Stage 11, vitellaria, testes, ovary and uterus developed, but without eggs; and Stage 111 mature worms, IIIa, ripening, IIIb, mature eggs, and IIIc, eggs shed. The occurrence pattern for each these stages in the summer of 1972 was [incidence percent (intensity mean, maximum)]. 21-28 June 1-7 July 27.01 % (16.6, 260) 29.42% (72.25, 1050) 15.8%(1.7, 26) 21.1 % (2.62, 28) 19.7 % (2.3, 21) 17.85%(1.48, 15) 18.7 % (2-0, 25) 5.83% (0.45, 10) 1.97%(0.1, 7) 1.79 % (0.12, 6 ) (From Table 2, p. 171, Malakhova and Anikieva, 1975).

Stage

I I1 IIIa IIIb IIIC

31 Aug.-1 Sept. 9.63 % (0.61, 10) 20.06% (0.72, 7) 12.25 % (0.72, 7) 21.0% (1.8, 15) 17.5% (0.83, 8)

It can be seen that maximum occurrences of juvenile P. exiguus were in June and July and of gravid adults August-September. However, only a small percentage of the cestodes achieved maturity overall. Malakhova and Anikieva (1975) related the peaks in plerocerciform and mature worm numbers to the air and water temperatures, the food supplies available to the fishes and their physiological condition. The intermediate host copepods in Karelia included Eudiuptomus gracilis, E. graciloides, Cyclops scutifer, C. colensis and C. lacustris but their role varied in different waters (Malakhova et al., 1978). Earlier Malakhova et al. (1972) had shown relationships between the fat coefficient, nutritional state and intensity of infection by P. exiguus in Lake Mun, Karelia.

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In Cold Lake, Alberta, Canada, Leong (1975) found that Proteocephalus exiguus was primarily in young Coregonus clupeaformis and mainly during summer. Abundance in year classes IV and V increased suddenly to a peak in May, and thereafter declined to December? with little or no infection in winter. Year classes VII and VIII had a similar pattern of infestation, except that the cestodes were present for a much shorter period, May to August, and at much lower intensities. Gravid worms were found late summer only. Leong (1975) considered that invasion of the C . clupeaformis occurred late winter-early spring, with maturation taking place through the summer months. The lack of infection in the coregonids during the winter was attributed to an absence of copepods containing invasive plerocercoids at that time (Leong, 1975). At Lake Michigan, U.S.A. Amin (1977) found four gravid Proteocephalus exiguus in Coregonus clupeaformis in March. Proteocephalusfallax La Rue, 191 1 Zschokke (1884) probably found Proteocephalus fallax (as Taeniz ocellata in part) in Coregonusfera in Lake Leman, Switzerland, in August. Kraemer (1892) (as Taenia jilicollis) reported that the greatest percentage of adult cestodes occurred in C .fera in Lake Lucern, Switzerland, in summer. Gravid worms were seen at the end of March, July and August. ProteocephalusJilicollis (Rudolphi, 1802) This common cestode of Gasterosteus aculeatus was investigated by Meggitt (1914) (as Ichthyotaenia filicollis) in Edgbaston Reservoir, Birmingham, England. Meggitt (1914) reported that in autumn almost every fish was infected with one or more of these parasites, 75% of which were adult. In winter the number of infected fishes was considerably smaller and adults were rare, while in spring the proportion of adults again increased. Adult specimens were found, however, all through the months September to June, but whilst their proportion to young forms was 75 % in September it was only 15% in March (Meggitt, 1914). Egg cultures were made mid-October to the end of January, but no development occurred, but some Cyclops varius were invaded by egg ingestion on 7 January. Attempts to invade G. aculeatus with procercoids from Cyclops failed (Meggitt, 1914). In Poland Kuczkowski (1925) (as Ichthyotaenia percae) noted sexually mature Proteocephalus filicollis in Gasterosteus aculeatus in late April. Cyclops strenuus were successfully invaded to give a procercoid in 16 days and a plerocercoid, in the same host, in 21 days. A very detailed study of the seasonal cycle of Proteocephalus filicollis was undertaken by Hopkins (1959) at a lochan near Bellshill, North Lanarkshire, Scotland. In this habitat there was a very pronounced annual cycle in the Gasterosteus aculeatus. The most advanced states commonly found were : plerocercoids (0.25-5 mm) July to November ; strobilate worms with genital primordia (5-8 mm) December to April; mature worms (10 mm) April and May; and gravid individuals (20 mm) June and July. From a consideration of the seasonal variation in incidence (see Fig. 5) Hopkins deduced that the parasite population in the fishes was in dynamic balance and that approxi-

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mately 1 % of the P.filicollis present in the G . aculeatus were lost daily. Hopkins (1959) stressed that this significant point in the host-parasite relationship had been overlooked. The incidence throughout the year was in dynamic balance between loss and gain. This is clearly shown in Fig. 5, in which it can be seen that the incidence did not just rise while fishes were eating infected copepods (July to September) and then remain static until the worms became gravid and were lost, but showed considerable changes long before the cestodes were mature. In fact, according to Hopkins (1959), in P.filicollis the loss of “spent” worms accounted for the death of an insignificant fraction of the total. Less than 1% of the worms to become established survived to become gravid (as shown by comparison of the product of incidence x intensity in August with that of May, when gravid worms first appeared) and, if certain calculations made by Hopkins (1959) were accepted, the survival figure was probably lower still, around 0.5%. In other words, Hopkins stressed, of every 200 P.Jilicollis to become attached in the G . muleatus intestine, only one reached full maturity; the other 199 died as a result of unknown causes. The interpretation and consequences of these findings will be considered further in Section V of this review.

FIG.5. The incidence of the cestode Proteocephalus jilicollis in the intestine of Gasterosteus aculeatus from a lochan (pond) near Bellshill, North Lanarkshire, Scotland between

November 1956 and September 1958. 0 incidence in the 1956-57 and 1958-59 year class 0 incidence in the 1957-58 year class of G. uculeafus (From Hopkins (1959), Fig. 1, p. 533.)

The clearly defined pattern of occurrence of Proteocephalus Jilicollis seen by Hopkins (1959) was not found by Chappell (1969a) at a pond on Baildon Moor, Yorkshire, England, although the individual stages of development showed a seasonal periodicity. Unsegmented plerocercoids were most abundant November to January, whilst early segmented plerocercoids were

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present all the time except September, but most common March, May and June. Adults without eggs were commonest May and August, and gravid adults in September 1966 and August 1967. Chappell (1969a) observed recruitment all year, with a winter peak, and all four developmental stages at all times during the survey period, except for segmented plerocercoids in September. The peak abundances did, however, fall into a logical succession through the year. In the Netherlands, by contrast, Willemse (1965, 1967, 1968) found a pattern of occurrence essentially similar to that of Hopkins (1959). In the autumn an invasion of the Gasterosteus aculeatus took place, but these juveniles remained small during the winter, to grow to maturity and produce eggs the following spring and summer. Willemse (1968) noted that this cycle corresponded perfectly with the migratory habits of these G. aculeatus. Less complete information concerning seasonality of Proteocephalus $licollis in Gasterosteus aculeatus can be found in Banina and Isakov (1972) and Dartnall (1972) (see Table I11 for localities). R d l a n d (1979) studied an anadromous population of trachurus type fully-plated Gasterosteus aculeatus. These fishes migrated to the sea in November and returned the following April. Gravid adults were present May to August only. Recruitment of plerocercoids commenced 19 June, and their percentage relative to gravid P.Jilicollis rose to 80% by 24 July and 100% by 14 August. Few of these young cestodes developed any segmentation before the last fishes left the spawning area for the sea in November, but proglottids were present on their return in April. Thus, the results of Hopkins (1959) (non-anadromous host population), WiIlemse (1965, 1967, 1968) (anadromous) and Rerdland (1979) (anadromous) are comparable, whereas those of Chappell(1969a) (non-anadromous) show a less pronounced, although similar, trend of development through the year. The life cycle of the cestode accommodates to the life style of both migratory and non-migratory host populations. Chappell (1969b) observed a partial spatial separation between Proteocephalus Jilicollis and Neoechinorhynchus rutili in concurrent infections in Gasterosteus aculeatus, thought to be an example of competitive exclusion. However, in this instance there was no effect on the seasonal occurrence of either species. Leong (1975) reported a species of Proteocephalus in Coregonus artedii as P.Jilicollis. Some doubt must be attached to this identification owing to the high specificity of P. jilicollis to Gasterosteus aculeatus elsewhere. In Cold Lake, Alberta, Canada abundance of the worms peaked in August, with minimum values during winter. Gravid worms were seen only in late summer. Proteocephalus Juviatilis Bangham, 1925 The seasonal occurrence of this species which matured only in Micropterus dolomieui has been examined by Fischer (1968, 1974). Samples were collected May to September or October, 1963 through 1967. Three stages of development, plerocercoids, segmented and early gravid Proteocephalus jluviatilis were present throughout the sampling period. Fully gravid, egg-shedding

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cestodes were not found until mid- to late June, but thereafter were present in some of the M . dolomieui until the last day of sampling each year (latest 15 October 1967). In most instances the egg shedding worms first appeared concurrent with a surface water temperature of 15"C, the temperature at which the fishes also commenced spawning activity. In Lake Opeongo, Ontario, Canada, Fischer (1968) found feeding fry of M . dolomieui by late June or early July, and in two warm summers, 1964 and 1967, egg-shedding P.fluviatilis were first noted in these fry on 17 and 29 August respectively. Fischer (1 968) studied the life cycle of Proteocephalusfluviatilis.The eggs did not survive for more than around two weeks at about 4"C, the bottom temperature of Lake Opeongo during winter. Viable eggs were considered to be present in the lake for about four months, from midJune to mid-October. In the copepod hosts (four species in Lake Opeongo) a plerocercoid I developed (an ? acaudate culcitacetabulo-plerocercoid I, according to Freeman, 1973). These plerocercoids were present in the lake by late June at the earliest. If eaten by M . dolomieui fry the plerocercoids commenced development, even to give gravid worms that summer if water temperatures were high (see above). However, in Lake Opeongo this was thought to be unusual, so that normally most fry would enter winter with worms varying from small plerocercoids to segmented, but not egg-shedding, adults. An obligatory period of growth, termed plerocercoid I1 (culcitacetabulo-plerocercoid 11, Freeman, 1973) occurred prior to the onset of segmentation. Large M . dolomieui, although infected by P. fluviatilis, did not eat copepods, and cannibalism was rare, hence Fischer (1968) postulated that transfer to them might occur via the agency of other small fish species taken as food by the M . dolomieui. The plerocercoids from the intestines of M . dolomieui were shown to survive in the intestine of sticklebacks for as long as six days. Proteocephalus longicollis (Zeder, 1800) Linstow (1891) (as Taenia longicollis)did not find adult cestodes during the winter, his description of the species being based on material collected in the summer. Kozicka (1949) examined Coregonus albula from Lakes Lansk and Maruski, Poland and found an 80% incidence during the summer. Cyclops species in the intestines of these fishes contained the plerocercoids of the cestodes. Proteocephalus macrocephalus (Creplin, 1825) The life cycle of this parasite of Anguilla anguilla has been described by Doby and Jarecka (1966). Jarecka (1960) found the larvae in Cyclops insignis in Lake Goldapiwo, Poland, in November. Willemse (1965) also completed the life cycle in the laboratory, and additionally carried out experimental transplants, fish to fish, very successfully. Willemse (1965, 1969) collected mature and gravid worms in all seasons, but plerocercoids only during the winter in the Netherlands. At Lake Skadar, Yugoslavia, KaiiC (1970) recorded mature Proteocephalus macrocephalus in A . anguilla January to July and November, and immature worms during all months, although maximally in May, August and December.

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Proteocephalus neglectus La Rue, 1911 Aderounmu (personal communication) found Proteocephalus neglectus in Salmo trutta from Chirk, Fish Hatchery, Clwyd, Wales, in March (4%), April (15 %), May (18 %), June (6 %), November (16 %) and December (15 %) 1966 and January (5%) 1967. Rahim (1974) examined S. trutta in the River Alyn, Clwyd, Wales, from June 1969 through to July 1970 but saw P. neglectus only in June (15.5 %) and July (4.5 %) 1970. In Czechoslovakia Kr5l (1977) noted that Salmo gaivdneri in a fishery which were treated with an anthelmintic to remove the adult tapeworms at the end of the growing season continued to acquire further invasions of Proteocephalus neglectus from the copepods during the winter until as late as the following spring. Proteocephalus osculatus (Goeze, 1782) Dubinina (1949) reported high incidences of Proteocephalus osculatus in summer (86.7 %), winter and spring (both 100%). Although heavily infected through the year, during the winter when the host fishes Silurus glanis hibernated in hollows at the bottom of the River Volga, U.S.S.R., the cestodes present were without strobilae. Growth and maturation of the worms occurred in spring, to be followed by egg production (Dubinina, 1950). In the Mingechaur Reservoir, Azerbaidan, U.S.S.R., Mikailov (1963) also observed an almost identical incidence and intensity of occurrence at all seasons. The same situation was also seen in the River Kure. Molnhr and Murai (1978) found proteocephalid scolices in the mesentery of the abdominal cavities of ten-week-old Cyprinus carpio fry. These were identified as either Proteocephalus osculatus or Ophiotaenia species and they suggested that the C. carpio were acting as paratenic hosts. Proteocephalus parallacticus MacLulich, 1943 MacLulich (1943), at Lake Opeongo, Ontario, Canada, did not find Proteocephalus parallacticus in Salvelinus namaycush during winter, except for the last fishes taken as the ice began to break up. The ratios of mature to immature worms recovered were: May 1 : 10-8, June 1 : 2.9 and July 1 :3.2. Freeman (1961, 1964) studied the biology of P. parallacticus in more detail, mainly in Lake Opeongo. S. namaycush were infected from ice-break through to November shortly before freeze-up. Ice-break occurred (body of lake ice-free) 1 May 1959,30 April 1960 and 10 May 1961. The earliest occurrences of gravid cestodes were 20 May 1959,5 June 1960 and 13 June 1961, although in this last year a hybrid S. namaycush x S.fontinalis had gravid worms on 25 May. The last dates of occurrence of gravid worms were 7 September 1959, 23 September 1960 (both also last date fishes examined) and 26 September 1961. A slight peak in numbers of gravid worms was seen in July and early August, but this was not statistically significant. At all times nearly every fish had some plerocercoids (plerocercoid IT, see below) and even in mid-summer some had only plerocercoids. Freeman (1964) found experimentally that at 16°C plerocercoids were formed in Cyclops bicuspidatus, C. vernalis, and probably C. scutifer. Normal growth was rare at 20°C and little growth occurred below 10°C. The copepod

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larvae were termed plerocercoid I (caudate culcitacetabulo-plerocercoid I in Freeman, 1973), and a second plerocercoid phase of growth, to plerocercoid I1 (culcitacetabulo-plerocercoid I1 in Freeman, 1973), was necessary in the intestine of Salvelinus namaycush for at least 30 to 40 days at an optimum of 12°C. Plerocercoid IT was morphologically identical to but about ten times larger than plerocercoid I. After a further 35 days, or less, segments developed and the plerocercoid I1 grew to a gravid adult. This growth was slow below 1O"C, optimal at 12°C and the maximum temperature for growth was 14°C. Invasion of fishes was either direct from copepods or via other fishes. Naturally infected copepods were first seen late-July (Freeman, 1964). Proteocephalus pearsei La Rue, 1919 Gravid Proteocephaluspearsei were found by Bangham (1925) in Lake Erie, Ohio, U.S.A., on 2 July. The intermediate hosts were shown to be Cyclops prasinus, Epischura lacustris and Eurycercus lamellatus (Bangham, 1925; 1927b). Pearse (1924) at the Yahara River Lakes, Wisconsin, U.S.A., found proteocephalids, mostly P. pearsei, in Perca flavescens during all months from June overwinter to May, except June, November and April. Fischthal (1953) was of the opinion that P. pearsei became sexually mature only in P.flavescens, and not in 16 other hosts reported at that time. Fischer (1974) at Lake Opeongo, Ontario, Canada, also found P. pearsei predominantly as a parasite of P. flavescens, although the cestode was present in Micropterus dolomieui fry during July and August. Fischer (1974) showed that the life cycle was strictly two-host, a copepod intermediate followed by the definitive host fish. At 18-23°C the plerocercoid I was developed in the copepod within three weeks. The plerocercoid could not survive the second passage through a fish stomach, hence invaded planktivorous M . dolomieui fry, but not large piscivorous M . dolomieui adults. Two studies have been carried out on seasonality of Proteocephalus pearsei in Percaflavescens. At the Bay of Quinte, Lake Ontario, Canada, an incidence of 50 % in July fell to 11 % by November, increased to 28 % in December, then declined gradually to 8 % in April. Intensity per infected fish was fairly constant about three, but was higher, about five in December and January (Tedla and Fernando, 1969). It is interesting that no worms found during the summer were segmented, but from September onwards worms with proglottids were more numerous, although no gravid worms were seen throughout the period of examination. Tedla and Fernando (1969) saw very small nonsegmented P. pearsei at all times of the year, which indicated that continuous invasion was occurring. Canon (1973) investigated the P. flovescens populations of Lake Opeongo (see Fischer, 1974 above). He found that the incidence fell from spring to summer of both years, and in 1968 incidence did not increase again until November, much later than in 1967. Cannon (1973) unfortunately made no comment about the condition of maturity of the P. pearsei. Proteocephalus percae (Miiller, 1780) Proteocephalus percae has been studied in a number of European countries, and in each instance, a well-marked pattern of seasonal maturation has been

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seen. The intermediate hosts were shown to be copepods: Wierzbicka (1956) found the larvae of the cestode as natural infections in Cyclops vicinus in Lake Dargin, Poland and Lake Galwe, Poland (now Lithuania, U.S.S.R.). Jarecka (1960) also recovered natural infestations in Eudiaptomus graciloides from Lake Goldapiwo (four in 10230) and Lake Mamry PMnocne, Poland (seven in 7638). In July the procercoids were growing, with cercomers and suckers in process of formation, whereas the larvae seen in August, October and November were fully-formed. An indication of the seasonal character of the life cycle was shown by the fact that the larval P. percae occurred only in the spring generation of E. graciloides (Jarecka, 1960). Izyumova (1958) at the Rybinsk Reservoir, U.S.S.R., recorded the larvae found in the intestines of Lucioperca lucioperca separately from the adults. The incidences of these larvae were: January-April 22.2 %, May-August 3.7 % and October to November 6.3 %. In 1933 Markowski reported adult Proteocephalus percae in PercnJluviatilis at Hel-Zatoka, Baltic Sea, Poland in April. Dubinina (1949), in Lucioperca Iucioperca at the Volga Delta, U.S.S.R., found an incidence of 20% in the spring of 1941. Bogdanova (1958) at the River Volga, U.S.S.R., also noted incidences, in Esox lucius, in February-March (I 3.2 %), May (I 3.2 %), but not jn August. E. lucius acquired the infection secondarily owing to the consumption of P. Jluviatilis (see Moravec, 1979b,below). However, Izyumova (1 958, 1959a) observed incidences in P. Juviatilis and Gymnocephalus cernua during all months of the year at the Rybinsk Reservoir. Incidences at all times of the year have also been described by Malakhova (1961), Molnhr (1966a) and Rautskis (1970a) (see Table 111 for hosts and localities). To understand the seasonal pattern of occurrence of Proteocephalus percae it is important to have data concerning the state of development of the worms in the intestines of the fishes. Various levels of information concerning maturation of the worms have been provided by Rizvi (1 964, 1968), Mishra (1966), Willemse (1967, 1969), Wierzbicki (1970), Halvorsen (1972), Wootten (1974), Ieshko et al. (1976), Lee (1977), Andersen (1978) and Priemer (1979). (See Table 111for hosts and localities.) In essentials, the same pattern of occurrence and maturation has been found by all these workers, apart from some changes in timing of the events which can be attributed to climatic variations. Accordingly, a summary of the annual pattern will be presented from Wootten (1974) who worked at Hanningfield Reservoir, Essex, England. In this locality Cyclops agilis, C. leuckarti and C . viridis were all able to serve as intermediate hosts. At 14°C development of the procercoid was completed in C. viridis in 3-4 weeks. Wootten (1974) recognized four stages of maturation of the cestodes in Perca Jluviatilis: Stage I, immature, unsegmented, no genitalia; Stage 11, segmented, maturing with genitalia developing; Stage 111, mature, genitalia developed; and Stage IV, gravid. Wootten (1974) first found Stage I worms in June, and until November they were the only stage to occur. The Stage I cestodes increased in mean length very rapidly through June to September, with little increase October and November. In November mean length was about 5 mm. Some maturation

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occurred in December to January, as Stage I1 and I11 worms developed, concurrent with a further increase in length (mean about 30 mm). By March to April the majority of the cestodes were mature (Stage HI),and in May were gravid (Stage IV) (see Fig. 6). The mean length of the gravid worms was about 75 mm. The gravid Proteocephalus percae were lost from the Percafluviatilis during May. Wootten (1974) noted that the initial period of growth of the cestodes in the fishes intestines corresponded to the plerocercoid I1 of Freeman (1964) and Fischer (1968) (see Proteocephalus parallacticus and P . fluviatilis respectively). Stage I immature &stodes stage I Moturlng &stodes %a*

8

m

Figures in brackets are number of Efrom each c a t w r y examined each month

Moture Cestodes

Stqe Ip Gmvid Cestodes

1968

' 1969

FIG.6. Monthly changes in the state of maturation of the cestode Proteocephalus percue in the intestine of Perca fluviatilis from Hanningfield Reservoir, Essex, England, March 1968 to January 1969. (From Wootten (1974), Fig. 5, p. 278.)

An increase of water temperature in an experimental tank containing Perca fluviatilis infected with undifferentiated (Stage I of Wootten, 1974) Proteocephalus percae was shown to result in rapid differentiation of the cestodes into mature worms with normal genitalia (Stage I11 of Wootten, 1974) by Willemse (1965, 1969). However, Wootten (1974) pointed out that in P. jZuviatiIis in Hanningfield Reservoir this transition from Stage I to Stage 111 worms commenced in December and January when water temperatures ranged from 2 to 7-5°C and were still falling, so that other factors in addition to temperature were involved. Thus maturation might be controlled by temperature (Willemse, 1965, 1969), physiological mechanisms of the host (Halvorsen, 1972) or endocrine levels of the host (Kennedy, 1969b). Wootten (1974) stated that at Hanningfield Reservoir the P . percae matured at the same time as the gonads of the P . fluviatilis became ripe and spawning of the fishes took place.

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High infections of Proteocephalus percae during winter in Esox lucius and Perca Jluviatilis in Lake Kals, Latvia, U.S.S.R., had been explained by Reinsone (1955) by the fact that the water temperatures in this habitat were kept high during winter owing to the presence of hot springs in the lake. Thus these fishes continued to feed and acquire invasions of worms during the winter. However, even in the colder conditions of Karelia, U.S.S.R., Malakhova (1961) found P.Jluviatilis to be infected overwinter (14.5 %, average 3-2, range 1-27 cestodes per host) at levels rather similar to those found by her during the autumn. Malakhova et al. (1978), in a preliminary note, stated that P. percae retained an annual cycle in P. Jluviatilis in the northern conditions of Karelia. Invasion of fishes took place during autumn and egg production by the cestodes during spring. In the northern, cooler, environment there was an increased period during which mature worms were present, with a shift to later in the year for recruitment of the next generation of cestodes. The late date of ice-break, the slow warming and the poorer food supplies for the fishes probably contributed to a reduced number of parasites in these northern waters (Malakhova et al., 1978). Wierzbicki (197 1) examined the distribution of Proteocephalus percae in littoral, shallow and deep water Perca fluviatilis in Lake Dargin, Poland. Highest infections occurred in the littoral zone. Jarecka (1960) had, however, found procercoids in copepods exclusively from the deep zones of lakes. Such an apparent discrepancy can perhaps be explained by either seasonal migrations of the P.Jluviatilis from shallow water in summer to deeper waters during the winter, or, by the problem of finding even small numbers of infected copepods in samples from natural waters. Moravec (1979b) has recently shown that the infections of Esox lucius by Proteocephalus percae in the MBcha Lake fish pond system, North Bohemia, Czechoslovakia, occurred November to April, with eggs in the uteri April only. In PercaJluviatilis at the same habitat the infections were found October to April, so that it was obvious that the findings in E. lucius followed its seasonal occurrence and maturation in the obligate host P. Jluviatilis. Proteocephalus pinguis La Rue, 1911 Hunter (1929) investigated the life cycle of this species in Lake Erie and near Carmel, New York State, U.S.A. An Esox reticulatus 115 mm long of the hatch of the current year contained an adult worm on 15 August, suggesting that the life cycle could occur within the one summer. Proteocephalus plecoglossi Yamaguti, 1934 Kataoka and Monma (1934) studied this species (as Proteocephalus neglectus). The fry of Plecoglossus altivelis hatched in the autumn at Lake Biwa, Japan, were infected by December of the same year. On 2 May ripe eggs were collected and infections of procercoids were obtained in Cyclops serrulatus. Proteocephalus primaverus Neiland, 1952 Neiland (1952) described this species from Salmo clarki in lakes near Stevenson, Washington State, U.S.A. In summer and autumn the S. clarki were not infected by larval cestodes, at which time the fishes were feeding on

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aerial and aquatic insects. In winter and early spring the S. clarki ate zooplankton, and larvae of Proteocephalus primaverus together with Diaptomus franciscanus were present in the stomachs. Overall a 90% incidence of the cestode was found by Neiland (1952). Eggs were incubated for 15 days at 15°C with D. franciscanus. Many of the copepods were then found to be infected with P. primaverus larvae, whereas control copepods were negative. Proteocephalus stizostethi Hunter and Bangham, 1933 The species was investigated in Stizostedion vitreum vitreum from Lake Erie, Michigan, U.S.A., by Connor (1953). Small immature specimens of Proteocephalus stizostethi were found on 18 September, worms with mature genitalia but no eggs from November to February, the uterine pouches were seen in March, eggs late April, early May and viable embryonated eggs were first noted on 30 June. Gravid cestodes disappeared from the fishes by August, as none were found from 3 August up to and including 13 September. Recruitment of the larvae to the fishes occurred from mid-September through until later in the winter, at which time Connor (1953) did not see any new invasions. No correlation between the numbers of P. stizostethi found in the fishes and season of the year was apparent. Proteocephalus tetrastomus (Rudolphi, 1810) Willemse (1965, 1967, 1969) found this species in Osmerus eperlanus at various habitats in the Netherlands. The cestodes were present in the intestines of the fishes all year, but with a lower level of incidence (25-40 %) during the summer months compared with the winter period (80-100 %). Intensity of infection was usually less than five worms per infected host during summer, but from five to several decads during the winter. Eggs of Proteocephalus tetrastomus fed to Cyclops strenuus developed to invasive larvae in about four weeks at 15°C. When eaten by Osmerus eperlanus young worms were obtained. Willemse (1965) found it easy to transfer worms from one fish to another experimentally, and inferred that cannibalism could carry infections from small to large 0. eperlanus. Recruitment to the host fishes commenced late summer or early autumn. During the winter months many worms were in the definitive hosts, but development into mature and gravid (ripe) cestodes commenced in spring. Eggs were found during the summer only: Willemse (1967, 1969) attributed the annual cycle to the effect of low winter water temperatures. Proteocephalus torulosus (Batsch, 1786) One early reference to seasonal occurrence of Proteocephalus torulosus (as Taenia torulosa, in part) may be found in Zschokke (1884). Kraemer (1892), a little later, produced a careful and detailed morphological and histological study. A further brief seasonal note, reporting immature and mature worms in March and April at Podgbrady, Bohemia, Czechoslovakia, in Perca jluviatilis (? Proteocephalus percae) and Squalius lepusculus was contained in Srhmek (1901). Subsequently Wagner (1917) in Germany stated that young, growing, but still not sexually mature worms (as Zchthyotaenia torulosa) occurred during the winter, whilst egg production of the adults took place from March-April until August. The procercoid stages were

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found infecting Diaptomus castor and Cyclops strenuus, in September and October, whilst the development through the plerocercoid stage occurred in the definitive host (Wagner, 1917). The next seasonal reports known to the author are more recent. Izyumova (1960) reported Proteocephalus torulosus from Abramis ballerus at the Rybinsk Reservoir, U.S.S.R., during summer (23*8%,1-19), but not winter, spring or autumn. At the Dnepr Delta, U.S.S.R., Komarova (1964) observed P. torulosus in Pelecus cultratus during all months in which fishes were examined, February (6.6 %, 1) March (46.6 %, 1-1 I), April-May (61.6 %, 1-31), JulyAugust (33-3%, 1-16) and October (SO%, 2-36). By contrast, much more irregular occurrences were seen in Abramis brama (May, 6.6%, 16), Blicca bjoerkna (April, 6.6%, 5 ) and Vimba vimba vimba natio carinata (March, 6.6% 2 and October 6.6%, 1). Presumably in the Dnepr Delta these latter fishes served only as auxiliary hosts. Davies (1967) at the River Lugg, Herefordshire, England observed ProteocephaIus torulosus in Leuciscus cephalus and Leuciscus leuciscus. In this instance, as well as recording incidence and intensity of occurrence the state of maturation was also carefully noted for each cestode. Five stages were distinguished: Stage I, plerocerciform, less than 10 mm in length, with no segmentation; Stage 11, plerocerciform, 11 to 30 mm in length, with no segmentation ;Stage 111, strobilization in progress, genital rudiments apparent; Stage IV, proglottids containing mature genitalia, but no eggs; and Stage V, proglottids with mature genitalia and eggs. Davies (1967) found the longest P. torulosus in L. leuciscus. Overall, the annual pattern of occurrence of these stages within the worm population was for high incidences (100%) of Stage I cestodes in L. cephalus during September, and both host fishes in October with 100% incidences of Stage I1 worms in November and December. In January, perhaps owing to a sampling deficiency, no worms were found in either host. From February to June a progressive maturation of the P. torulosus was observed: a 100% incidence of Stage I11 in L. leuciscus in February and March, but in April 6 % Stage I, 42 % Stage 11, 19% Stage I11 and 32 % Stage IV, whilst in June and July in this same host the figures were, respectively, Stage I 15%, 14%, Stage I1 5 % , OX, Stage 111 12%, 14%, Stage IV 17%, 0 % and Stage V 51 %, 71 %. In August no P. torulosus were seen in the definitive host fishes. The pattern in L. cephalus was essentially similar to that found in L. leuciscus, except that the cestodes were found only September to October and April to July. At the River Avon, Hampshire, England, Kennedy and Hine (1969) also studied the seasonality of Proteocephalus torulosus in Leuciscus leuciscus. Here too an obvious cycle was seen, with invasion commencing November and December and infection levels continuing to rise until the spring. Between May and June a steep fall in incidence and intensity of occurrence was seen and all the worms were gone by August. Recruitment continued until April, and an absence of small worms at that time was taken by Kennedy and Hine (1969) to indicate that these recruits must have grown fairly rapidly and so passed into the larger size classes. As seen by Davies (1967), gravid worms

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were never a large proportion of the parasite population until after March. The majority were gravid April and May and in June and July they destrobilated. Egg production occurred at water temperatures of 5.5 to 14.4"C, hence no critical temperature was apparent. Both Davies (1967) and Kennedy and Hine (1969) emphasised the population dynamics inherent in the pattern of occurrence of the Proteocephalus torulosus in the host fishes. Growth of the worms occurred even at low winter temperatures. Although water temperature appeared to be a causal factor for egg production, Kennedy and Hine (1969) disputed the direct effect of temperature on the maturation cycle of the tapeworm. They proposed the hypothesis that the seasonal changes in resistance of the Leuciscus leuciscus were in themselves directly dependent on temperature ; that in winter resistance was at its lowest thus permitting invasion, that rising temperatures in spring stimulated the parasite growth but increased host resistance to new invasions, and that at the higher water temperatures of summer host resistance had reached the point where new worms could not establish and all the old worms were eventually rejected. Kennedy (1972~)reiterated this view, having found a consistent pattern of occurrence for P. torufosus in L. leuciscus in the River Avon from March 1966 to February 1970. Small differences in timing were seen from year to year, as in 1967, when infections commenced earlier and terminated later than in other years. By contrast with the short break in occurrence of Proteocephalus torulosus (August) seen by Davies (1967), and the longer one (August and September) noted by Kennedy and Hine (1969) in their host fishes, Wierzbicka (1978) at Lake Dabie, Poland, found a high incidence (50-100%) in Abramis bdlerus during the whole period of her study (June 1969 to September 1971), except in June 1970, when it fell to zero. Young P . torulosus were seen in almost all samples, and mature cestodes mainly in spring and summer (Wierzbicka, 1978). In the colder conditions of Karelia, U.S.S.R., leshko et al. (1976) reported a clear annual cycle with autumn recruitment of Proteocephalus torulosus to the cyprinids (see Table I11 for species) and spring maturation. Sexually mature worms (their Stage 111) were seen May (maximum 20%) up to midAugust. An increased period of maturation, with a shift in the times of host infection and reduced numbers of worms, owing to later ice break-up, relatively slow warming of lake waters and poor food supplies for the fishes were thought to be involved (Ieshko et al., 1976; Malakhova el af., 1978). Kakacheva-Avramova (1977) noted Proteocephalus torulosus in cyprinids (see Table 111) in the River Danube, Bulgaria, during spring and summer. Proteocephalus tumidocollus Wagner, 1953 Studied by Wagner (1953, 1954) at Loma Linda and Mentone, California, U.S.A., in Salmo gairdneri and Salvelinus fontinalis. The intermediate hosts were Cyclops vernalis and Eucyclops agilis and others. At room temperatures the egg invasive potential was maintained for 13 days, but for more than one month at 0,1,5 and 10°C, 19 days at 20°C but only 8 days at 32°C. C. vernalis was infected with 100% success on many occasions. However, in a two-year-

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old culture of these copepods total resistance to invasion occurred. Larval growth in copepods was optimal at about 20"C, with rapid development during the first 20 days, but within one month of the initial egg ingestion the copepods died. Temperature influenced the larval development, it was inhibited at 1"C, and erratic at 26 to 32°C. If infected copepods were held at 1°C for 40 days and then warmed to 20°C normal growth resumed to give mature larvae at between 40 to 60 days. Wagner (1953, 1954) experimentally infected SaZmo gairdneri and maintained them at 12-18°C. One day post-infection the majority of the larvae were in the pyloric caeca region of the intestine. At the 1 lth day some were established in the pyloric caeca attached a t the blind tip. By 26 days the cestodes were 3 to 6 mm long. Between days 11 and 26 the length of the larvae increased 10 times, although no new structures were formed. In 33 days proglottis formation was apparent in worms 7-1 1 mm long, and some of the larger ones had testes and cirrus pouch development. The worms reached 25 to 44mm in length at 63 days, containing eggs in the uterine pouches, whilst by 106 days, at 70 to 400 mm, eggs were being expelled. The potential for transfer of worms established in small fishes to large fishes was demonstrated experimentally by Wagner (1954). Supra-infections were also made by feeding infected fishes with additional copepods containing invasive larvae 44 days after the first feeding. No establishment of the larvae from the second feeding occurred, and Wagner (1954) attributed this to some immunological factors. Proteocephalus species undetermined The precise determination of species of Proteocephalus can be difficult. Some species have been described only once, and even for widely distributed species there may be insufficient descriptive information to recognize variation between different hosts and geographical regions (Freze, 1965b). Accordingly, a number of forms are noted here which remain unidentified but for which some seasonal data have been collected. They are considered in alphabetical order of host species. Coregonus fera Lake Ltman (Geneva), Switzerland Doby and Jarecka (1964) described a species resembling Proteocephalus pollanicola and P. neglectus. Jarecka and Doby (1964) found abundant gravid aduIts in August. Eggs were released on placing the worms into water. Natural infections of Cyclops abyssorurn (1 of 150) were seen, and experimental development of larvae at laboratory temperatures took 15 days to completion in C. strenuus strenuus and C . abyssorum. Coregonus lavaretus and Alosa jinta Lake Maggiore, Italy. This species resembled Proteocephalus agonis and P. longicollis (Pecorini, 1959). The natural infections of four species of copepods in Lake Maggiore were investigated by Pecorini (1959). Cyclops strenuus were infected all year, minimally April, maximally July-August ; Eudiaptornus vulgaris all year except May, minimum April, peaks June to August and December to January; Mesocyclops Zeuckarti all year except December-January, maximum July to August; and Mixodiaptomus lacinatus, no infection April, low June and July,

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but higher February, May, August (maximal), October and November. Grimaldi (1964) found the adult worms from May, the incidence gradually attaining a maximum during June and July, then slowly decreasing through the late autumn and winter to a minimum in February. Infections were not found March and April. Coregonus lavaretus Llyn Tegid, Wales Chubb (1961) provided a description of this Proteocephalus species but did not attempt to name it. He suggested that possibly, owing to genetic variation and isolation of the populations of Proteocephalus in the British Isles and elsewhere, a different form of Proteocephalus might occur in each isolated population of Coregonus species. A seasonal cycle of maturation was apparent but not investigated. Farenden (personal communication) examined the incidence, intensity and maturation of the worms from October 1975 to March 1976. Four stages of maturity were separated: Stage I immature; Stage I1 with developing genitalia; Stage I11 mature, with eggs; and Stage IV gravid. The incidence (and average intensity) decreased from October 13.3 % (3), through November 12.0% (I.@, December 4.5% (1) and January 2.8% (I), no worms were found February, whereas in March a dramatic increase occurred 19.4% (10.6). These changes appeared unrelated to water temperature (at 16m depth 10-5"COctober, falling to 6 . 9 2 December, 6.0"C January, 6.5"C February, but 4.5"C in March). Gravid worms were seen in October (12) November and January (one each month) and March (34). In March the worm numbers for each stage of maturation were: Stage I 7, Stage I1 8, Stage 111 12 and Stage IV 34. The hosts spawned about January, coregonid eggs were found during that month, so that the decline in numbers might be related in some way to this event. However Ablett (personal communication) made a further study of the pattern of occurrence during the period October 1978 to March 1979. On this occasion incidence (and average intensity) were once again seen to decline through the overwinter period : October 83.3 % (9.04), November 56.6 % (7-94), December 56.6 % (5.47), January 33-3% (3.50), February 20% (2-16) and March 13.3% (3.00). In this instance owing to a very careful search for small plerocerciform worms (down to 0.5 mm in length) higher incidences and intensities of occurrence were reported. A rapid increase in worm length occurred in March, similar to that found by Farenden (personal communication, above), but in this second overwinter period of investigation no gravid worms were recovered. Esox lucius and Rutilus rutilus Lake Konche, Karelia, U.S.S.R. MaIakhova (1961) found the following incidences (average intensities, range): Esox lucius, autumn 1.56% (3, 3); winter 9 % (1-5, 1-2); spring 15.6% (2.83, 1-17); and summer 9.1 % (2.38, 1-9): Rutilus rutilus, autumn 1.1 % (3, 3); winter 0%; spring 1-1% (1, 1); and summer 0%. Perca JEuviatilis Lakes, Wilno Region, Poland (now Vilnius, Lithuania, U.S.S.R.) Wierzbicka (1951) reported that Perca JEuviatiZis in Galwe Lake, Wilno Region, Poland (now Vilnius Region, Lithuania, U.S.S.R.), were infected by a Proteocephalus species (? P. percae) in October and November, with mature worms at the end of May 1936. The material was not identified and later

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destroyed. Cyclops kolensis contained Proteocephalus larvae in October, November and January, an 11.16 % infection overall, but not in March, July, August and September. Cyclops vicinus were infected September (I 1.11%) and October (1.11 %), but not in January, March, July, August, or November. Salmo gairdneri Fish farm, Movanagher, County Antrim, Ireland In spring and summer of 1971Proteocephalus species with mature segments were found and in autumn gravid proglottids were present containing embryonated eggs (Arme and Ingham, 1972). Salmo trutta Norway Halvorsen and Macdonald (1 972) found a Proteocephalus species in this host in Lake Melingen, Vhgh (June 16.7%, not July to October) and Lake Nedre Fipling, Vefsn (June 19.2%, July 9.6% not August to October). The lakes were both ice-covered the remainder of the year. Borgstrom and Lien (1973) provided a description of a species of Proteocephalzrs from Lake Horns. It most resembled P.percae, but differed in some characters, and also was similar to the Proteocephalzls species found by Doby and Jarecka (1964) in Lake Lkman (see above). In one lake, Ovre Heimdalsvatn, in Southern Norway, the worms invaded the Salmo trutta in October and November, to achieve a stable incidence during the winter and spring, although the intensity of infection varied greatly. The worm population decreased to zero, or almost so, in August and September. The smallest worms were less than 1 mm, the largest 210 mm. Small worms occurred October to May. In a few, differentiation of genitalia was seen in mid-March, but the number maturing increased during spring, and by July all were gravid. In Ovre Heimdalsvatn the S. trutta were free of infection for August and September, whereas, by contrast in Hornsvatn the fishes were probably reinvaded by larvae of Proteocephalus species prior to the loss of the gravid worms (Lien and Borgstrom, 1973). Proteocephalus species juveniles undetermined Proteocephalus juveniles can occur in the intestines of a wide variety of fishes which are not the usual definitive host for the particular species. Some of these may ultimately reach their definitive host owing to predation of small fishes by larger fishes, but many are no doubt lost without further development. A number of authors have recorded seasonal information concerning these juveniles. They include Pearse (1924), Izyumova (1958, 1959a, 1960), KaiiC (1970), Leong (1975) and KaiiC et al. (1977). Proteocephalus cysts were reported on a seasonal basis by Pearse (1924) and Holl (1932). Silurotaenia siluri (Batsch, 1786) Kakacheva-Avramova (1977) noted this cestode in Silurus glanis from the River Danube, Bulgaria during the summer. C.

CLASS NEMATODA, SUBCLASS ADENOPHOREA

1. Order Enoplida (a) Family Capillariidae A revision of the taxonomy of the nematodes of the genus Cdpillaria from

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European freshwater fishes (Moravec, 1980) was received after the writing of this section was completed. However, Moravec’s conclusions have been added in the relevant place for each species considered here. Capillaria acerinae Thieme, 1961 The genus Hepatospina was proposed by Thieme (1961) for his species Capillaria acerinae which he had described in a previous paper in the same year. Khalil (personal communication) states that no other species had so far been assigned to this new genus. When proposing the new genus Thieme (1961) did not give any differential diagnosis or even state why Hepatospina was different from Capillaria. In this circumstance, the species is retained here in the genus Capillaria. According to Kutzer and Otte (1966) and Moravec (197 1 a, 1980) C. acerinae is a synonym of Capillaria petruschewskii (see below). Thieme (1961) provided some data concerning seasonal occurrence of Capillaria acerinae, but a fuller account was given in Thieme (1964). The nematode was found in the liver of Gymnocephalus cernua. Invasive first stage larvae could not be identified for certain but all others from second stage larvae to adult were studied. All nematodes in one host were at the same stage of development except for a few where second stage larvae and adults occurred. Thieme (1964) found first (?) and second stage larvae from May 1959 (start of the investigation) representing 53-8% of the worm population, falling thereafter through to August (7-1 %) after which they disappeared until more were seen January-February (79 %) and March-April 1960 (45-4%). Third and fourth stage larvae made up 35.9 % of the population in May, 42.8 % (maximum) in June 1959, declining subsequently to 16.6 % in September. They were not found October to December, but more appeared January (21 %) and February 1960 (50.8%). Adults were present May 1959 (10.3 % of population) and their percentage representation rose progressively from then until only adult C. acerinae were found in October. No nematodes at any stage of development were seen November or December 1959. Thus, invasion of the fishes appeared to have occurred from January onward, with development to adults through spring and summer so that only adults remained by October, to disappear thereafter. Oviposition occurred in the G. cernua liver, the eggs embryonated to contain first stage larvae and became encapsulated by the host tissues. Thieme (1964) attempted experiments using naturally infected liver containing embryonated eggs. These were digested from the host encapsulation tissues, but then were passed from the experimental fishes with their faeces. Thus Thieme (1964) was unable to determine the method of invasion of the fishes by C. acerinae. He concluded, however, that the eggs were released from the G. cernua livers after their death, by decay or digestion by predators. Thieme (1964) promised further investigations, but these have not been found in the literature by this reviewer. Capillaria brevispicula (Linstow, 1873) This species was reported in Abramis brama from the River Volga, .U.S.S.R., in February-March 1957 (6.6 %), but not found in the same host July-August 1956 or May 1957 (Bogdanova, 1958). Izyumova (1960) at the Rybinsk

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JAMES C . C H U B B

Reservoir, U.S.S.R., noted it in Blicca bjoerkna in summer (7%) but not in the other seasons. At the Dnepr Delta, U.S.S.R., Komarova (1964) examined Abramis brama February to October (excluding September) and observed Capillaria brevispicuh in April (20 %, 1-3) and May (6-6%, 1) only. Capillaria coregoni Shul’man-Al’bova, 1953 This species is a synonym of Capillaria salvelini (see below) according to Moravec (1980). In rivers in the Duero and Sil basins, Le6n, Spain, a well-defined seasonal cycle of incidence, intensity and maturation, with two generations per annum, was found (Corder0 de Campillo and Alvarez Pellitero, 1976a; Alvarez Pellitero et al., 1978a). The main period of invasion of the Salmo trutta was at the end of spring-early summer, with a second, smaller period of invasion during winter. Capillaria coregoni were present in the fishes all through the year, none the less, the seasonal pattern of the two generations was evident. Water temperature influenced the rate of development of the nematodes, maturation was most rapid during the spring and summer. Capillaria lewaschofi Heinze, 1933 Capillaria IewaschofJi is a synonym of C. brevispicula (see above) according to Moravec (1980). Komarova (1964) reported this nematode in Pelecus cultratus from the Dnepr Delta, U.S.S.R., in March (6.6 %, 3), April-May (5.5 %, 3) and JulyAugust (6.6%, 2). It was not found February or October. Capillaria petruschewskii (Shul’man, 1949) Originally described as Hepaticola petruschewskii by Shul’man (1 949) from the liver of Lepomis gibbosus captured in Lake Kagwl, U.S.S.R., Yamaguti (1961), however, included Hepaticola as a synonym of Capillaria. Shul’man (1949) observed invasion of the fishes in spring with development of the adults reaching completion towards the autumn. Kutzer and Otte (1966), in Austria, showed experimentally that the life cycle required an intermediate host. C. petruschewskii larvae were recovered in Eiseniella tetraedra collected from an area where the adult parasites were known to occur. These larvae developed to maturity within 6 months at 10°C when fed to Salmo gairdneri. Molnhr (1968b), at Teich T, Hungary, observed Capillaria petruschewkii in the livers of Phoxinus phoxinus during all months of the year, except October. The worms were readily apparent owing to morphological changes of the host liver. Many eggs were found in the liver parenchyma. No significant changes in numbers were seen through the seasons. At Lake Paleostomi, Georgia, U.S.S.R., Cernova (1975) found the worms in Rufilus rutilus in autumn 13-3% (range 85-155 per fish), but not the other seasons. In the River Danube, Bulgaria, Kakacheva-Avramova (1977) noted an infection of Lepomis gibbosus in spring. Capillaria salvelini Polyanskii, 1952 Awachie (1963a) found a Capillaria species in Salmo trutta in the Afon Terrig, Wales, in January, March, April, June and August, but not in the other months. These worms are now considered to be C. salvelini. Aderounmu

H E L M I N T H S I N F R E S H W A T E R FISHES

105

(personal communication) observed infections in the intestines of S . trutta from Chirk Fish Hatchery, Clwyd, Llyn Celyn and Llyn Tegid, Wales. Worms were present most months of the year in low incidences (3-21 %) from the wild fishes, but in higher incidences in the cultivated S. trutta (6-8%). Campbell (1974) at Loch Leven, Scotland, also found C. salvehi throughout the year, with no clear evidence of a seasonal pattern. Incidence in Loch Leven decreased during the period of his survey from 50% in 1967 to 15% in 1972. CdpilIaria species undetermined Malakhova (1961) observed an undetermined species of Capillaria in the intestines of Lota Zota at Lake Konche, Karelia, U.S.S.R., winter (1.3%, 2) and spring (1-8 %, l), but not summer or autumn. (b) FamiIy Cystoopsidae Cystoopsis acipenseris Wagner, 1867 Janicki and R a s h (1929) observed that growth in the amphipod intermediate hosts was accelerated by an increase in water temperature. The larvae were invasive after 22 days at 8"C, but 14 days at 20°C. According to Bauer (1959a) the life span of the worms in Aciyenser ruthetzus and other acipenserids was probably one year or longer. The worms occurred below the skin of the acipenserids in cysts and the eggs were released into the water by the rupture of the cyst wall to the exterior during the summer months. D. CLASS NEMATODA, SUBCLASS SECERNENTEA

1. Order Ascaridida

(a) Family Anisakidae Contracaecum aduncum (Rudolphi, i 802) (For larval stages see Part I11 p, 53 of review). The sexually mature individuals are found in the gut lumen of the host fishes. At Lake Skadar, Yugoslavia, KaiiC (1 970) observed Contracaecum species larvae in Alosa fallax nilotica during all months of the year. Juvenile C. aduncum in the gut of the same host were found April and May, and mature nematodes, in larger numbers, from April to June. Contracaecum bidentatum (Linstow, 1899) According to Izyumova (in Bykhovskaya-Pavlovskaya et al., 1962) this nematode is a parasite of Acipenseridae; reports of incidences from other families of fishes were probably erroneous. However, Bogdanova (1958) reported C. bidentatum from Esox lucius in the River Volga, U.S.S.R., in February-March and May but not August. Kakacheva-Avramova (1977) at the River Danube, Bulgaria, found low incidences (4.2 to 11.5%) in five species of fishes (see Table IV) in summer, whilst the incidence in Acipenser ruthenus was 46.7 %, with worms present spring through autumn. Assuming correct determination of the C . bidentatum, it would be interesting .to know whether these nematodes in non-acipenserid hosts had achieved sexual maturity (see Geller, 1957 below).

-

TABLEIV Studies on seasonal occurrence of nematodes listed in the climate zones of the World (see map Fig. 1, Chubb, 1977). The species are in alphabetical order. Climate zones

Nematode species

Host species

1. Tropical la. RAINY (humid climate)

Locality

References

tropical forest Procamallanus clarias

Clarias batrachus

Procamallanusparvulus

Clarias batrachus

lb. SAVANNA (humid climate) lc. HIGHLAND (humid climate) 1d. SEMI-DESERT (dry climate) le. DESERT (dry climate)

no seasonal studies

Furtado and Tan Paddy fields, Sungei Besar, Sabak Bernam, (1973) Malaysia Paddy fields, Sungei Furtado and Tan Besar, Sabak Bernam, (1973) Malaysia tropical grassland

no seasonal studies

tropical highland

no seasonal studies

hot semi-desert hot desert

Procamallanus laeviconchus

2. Sub-tropical 2a. MEDITERRANEAN Capillariapetruschewskii Contracaecum aduncum

Clarias anguillaris Clarias lazera Clarias lazera Rutilus rutilus Alosa fallax nilotica

River Nile, Egypt River Nile, Egypt

Iman (1971, quoted by Moravec, 1975) Moravec (1975)

scrub, woodland, olive Lake Paleostomi, Cernova (1975) Georgia, USSR Lake Skadar, KaiiC (1970) Yugoslavia

Goezia ascaroides

Anguilla anguilla

Philometra ovata

Gobio gobio Iepidolaemus Esox lucius

Raphidascaris acus

Anguilla anguilla Truttaedacnitis truttae

Salmo trutta

Camallanus oxycephalus

Gambusia afinis

Philometroides carassii

Carassius auratus

Spinitectus carolini

Gambusia afinis

2b. HUMID

Lepomis cyanellus Lepomis humilis Lepomis macrochirus Lepomis megalotis

3. Mid-latitude 3ai. HUMID WARM SUMMERS Camallanus lacustris

Esox lucius Gymnocephalus cernua Lucioperca lucioperca

Lake Skadar, Yugoslavia Lake Skadar, Yugoslavia Lake Dzhapana, Georgia, USSR Lake Skadar, Yugoslavia River Trino, L’Aquila, Italy deciduous forest San Marcos area, Texas, USA Ichikawa City, Chiba Prefecture, Japan San Marcos area, Texas, USA Little River, Buncombe Creek and Lake Texoma, Oklahoma, USA

KaiiC (1970)

KaiiC et al. (1977) Cernova (1975) KaiiC (1970) Paggi et al. (1978) Davis and Huffman (1978) Nakajima and Egusa (1977b, c) Davis and Huffman (1978) McDaniel and Bailey (1974)

temperate grassland, mixed forest Lipno Reservoir, Ergens (1966) River Vlatava, Czechoslovakia Lake Balaton, Hungary Molnar (1966a) +

c

0

TABLEIV (continued) Climate zones

Nematode species

Host species

00

Locality

References

3ai. (continued)

Esox lucius

Camallanus oxycephalus

Camallanus truncatus

Gasterosteus aculeatus Anguilla anguilla Esox lucius Perca jluviatilis Perca jluviatilis ( ?) Esox Iucius Lota lota Perca jluviatilis Salmo trutta Lepomis gulosus Lepomis macrochirus Micropterus salmoides Ictalurus punctatus Pomoxis annularis Morone chrysops Notropis hudsonius Notropis spilopterus Perca flavescens Gymnocephalus cernua Perca fluviatilis

MBcha Lake fish pond system, North Bohemia, Czechoslovakia near Warsaw, Poland PodEbrady, Czechoslovakia

Moravec (1979b)

Ruszkowski (1926) Sramek (1901)

Sweden Tornquist (1931) Lake Leman (Geneva), Zschokke (1884) Switzerland Lake Fort Smith, Arkansas. USA

Cloutman (1975)

Lake Carl Blackwell, Oklahoma, USA Lake Erie, USA

Spa11 and Summerfelt (1969) Stromberg (1973); Stromberg and Crites (1974a, 1975b)

Lake Balaton, Hungary Ponyi et al. (1972) River Svratka, Vojtkova (1959) Czechoslovakia

Capillaria petruschewskii

Lepomis gibbosus

River Danube, Bulgaria Teich T, Hungary Lake Kagwl, USSR River Danube, Bulgaria

Phoxinus phoxinus Lepomis gibbosus Contracaecum bidentatum Abramis brama Acipenser ruthenus Esox lucius Gymnocephalus schraetser Proterorhinus marmoratus Silurus glanis Dubossary Reservoir, Vimba vimba vimba Cucullanus dogieli Moldavia, USSR natio carinata Central and Eastern Cystidicoloides tenuissima Salmo trutta Balkan Mountains, Bulgaria River Bystfice, Salmo trutta Czechoslovakia Lake Carl Blackwell, Ictalurus punctatus Dichelyne (Dichelyne) Oklahoma, USA robustus MBcha Lake fish pond Esocinema bohemicum Esox lucius system, North Bohemia, Czechoslovakia PodEbrady, Paraquimperia tenerrima Anguilla anguilla Czechoslovakia Central and Eastern Gobio gobio Philometra abdominalis Balkan mountains, Bulgaria RokytnB River, Gobio gobio Moravia, Czechoslovakia

Kakacheva-Avramova (1977) MolnAr (1968b) Shul'man (1949) Kakacheva-Avramova (1977)

Marits and Vladimirov (1969) Kakacheva-Avramova (1973) Moravec (1971~) Spa11 and Summerfelt (1969) Moravec (1979b)

Sramek (1901) Kakacheva-Avramova (1973) Lelek (1964)

TABLE IV (continued) ~ _ _ _ _ ______

~

Climate zones

Nematode species

Host species

Locality

References

3ai. (continued) Cobio gobio

Phoxinus phoxinus Philometra fujimotoi Philometra kotlani

Ophiocephalus argus Aspius aspius

Philometra obturans

Esox lucius Esox lucius

Philometra ovata

Philometra rischta

Abramis brama Rutilus rutilus Leuciscus cephalus Abramis brama Alburnus alburnus

Philometra species

Enneachanthus gloriosus Ictalurus natalis

Magyarkut and Kemence Brooks, Borzsony Mountains, Hungary Rokytka Brook, Czechoslovakia near Seoul, Korea Lake Balaton, Rivers Tisza and Danube, Hungary Rivers Tisza and Danube, Hungary Macha Lake fish pond system, North Bohemia, Czechoslovakia Lake Balaton, Hungary

Molnar (1967)

Podbbrady, Czechoslovakia Dubossary Reservoir, Moldavia, USSR Lake Balaton and River Danube, Hungary Various habitats, North Carolina. USA

Srkrnek (1901)

Moravec (1977b) Furuyama (1934) Molnar (1969a) Molnar (1976) Moravec and Dykovh (1978); Moravec (1979b) Molnar (1966b)

Marits and Tomnatik (1971) Molnar (1966b) Holl (1932)

Lepomis gibbosus Lepomis gulosus Perca flavescens Philometroides cyprini

Cyprinus carpio Cyprinus carpio

Philometroides sanguinea Raphidascaris acus

Carassius auratus gibelio Carassius carassius Salmo trutta Esox lucius

Esox lucius Salmo gairdneri Salmo trutta Thymallus arcticus baicalensis Esox lucius Lota Iota Rhabdochona cascadilla Ictalurus punctatus Rhabdochona decaturensis Pomoxis annularis Rhabdochonadecaturensis Aplodinotusgrunniens Ictalurus punctatus Rhabdochona denudata Alburnus alburnus Alburnus bipunctatus Leuciscus cephalus

I=

Yahara River lakes, Wisconsin, USA L'vov Ternopol, Western Ukraine, USSR Ternopol, Western Ukraine, USSR Fish farms, Vinnitsa Region, USSR River Bystfice, Czechoslovakia Macha Lake fish pond system, North Bohemia, Czechoslovakia Podgbrady, Czechoslovakia Dobsina Dam, Czechoslovakia

Pearse (1924)

Lake Lkman (Geneva), Switzerland Lake Carl Blackwell, Oklahoma, USA Eagle Mountain Lake, Texas, USA Central and Eastern Balkan Mountains, Bulgaria

Zschokke (1884)

Ivasik et al. (1967a, 1967b, 1971) Vasil'kov (1964) Yashchuk (1971, 1975) Moravec (1970b) Moravec (1979b)

Sramek (1901) Zitfian (1973)

Spa11 and Summerfelt (1969) Gruninger et al. (1977) Kakacheva-Avramova (1973)

TABLE IV (continued)

Climate zones

Nematode species

Host species

Locality

References

3ai. (continued) Vimba vimba tenella Alburnus alburnus

R..~bdochonahellichi

Phoxinus phoxinus Alburnus alburnus Leuciscus cephalus Barbus barbus Barbus meridionalis petanyi Barbus barbus

Rhabdochona phoxini

Phoxinus phoxinus

Rhabdochona species undetermined Spinitectus carolini

Abramis saga Zingel streber Lepomis gulosus Lepomis macrochirus Micropterus salmoides Lepomis gibbosus Lepomis gulosus Ictalurus punctatus

Spinitectus gracilis

Pornoxis.annularis

River Danube, Bulgaria Teich T, Hungary Lake Leman (Geneva), Switzerland Central and Eastern Balkan Mountains, Bulgaria River Danube, Bulgaria Rokytka Brook, Czechoslovakia River Danube, Bulgaria Lake Fort Smith, Arkansas, USA

Kakacheva-Avramova (1 977) Molnar (1968b) Zschokke (1884)

Settling pond, near Durham, North Carolina, USA Lake Carl Blackwell, Oklahoma, USA Lake Carl Blackwell, Oklahoma, USA

Holl (1932)

Kakacheva-Avramova (1973) Kakacheva-Avramova (1977) Moravec (1 977a) Kakacheva- Avramova (1977) Cloutman (1975)

Spall and Summerfelt (1969) Spall and Summerfelt (1969)

Truttaedacnitis sphaerocephala Truttaedacnitis truttae

Acipenser guldenstadti

Camallanus lacustris

Lucioperca lucioperca Perca fluviatilis Gymnocephalus cernua

Lampetra lamottenii

3aii. HUMID COOL SUMMERS

Esox lucius Perca fluviatilis

Esox hcius Perca fluviatilis Camallanus truncatus

Esox lucius Lucioperca lucioperca Pelecus cultratus Perca fluviatilis Gymnocephalus cernua Lucioperca lucioperca

Esox lucius Capillaria brevispicula

Abramis brama

River Danube, Bulgaria Big Creek, Lake Erie, Canada temperate grassland, mixed forest Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR Lake Dusia, Lithuania, USSR Lake Dusia, Lithuania, USSR Lakes Galstas, Obelija and Shlavantas, Lithuania, USSR River Volga, USSR Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR River Volga, USSR

Kakacheva-Avramova (1 977)

Pybus et al. (1978a)

Izyumova (1958, 1959b) Izyumova (1959a) Izyumova (1960) Rautskis (1970a) Rautskis (1970b) Rautskis (1977) Bogdanova (1958) Izyumova (1958) Izyumova (1959a) Izyumova (1959b) Izyumova (1960) Bogdanova (1958)

I

w

c

TABLEIV (continued) Climate zones

Nematode species

Host species

P

Locality

References

3aii (continued) Rybinsk Reservoir, Izyumova (1960) USSR River Volga, USSR Bogdanova (1958) Contracaecum bidentatum Esox lucius River Volga, USSR Geller (1957) Acipenser ruthenus Bauer and Nikol’skaya Coregonus lavaretus baeri Lake Ladoga, USSR Cystidicola farionis (1957) natio ladogae Dichelyne (Cucullanellus) Perca flavescens Lake Michigan, USA Amin (1977) Lake Opeongo, Ontario, Cannon (1973) cotylophora Perca flavescens Canada Perca flavescens Yahara River lakes, Pearse (1924) Wisconsin, USA Philometra abdominalis Abrama brama River Volga, USSR Bogdanova (1958) Kuybyshev Reservoir, Lyubarskaya (1970) Abramis brama USSR Philometra cylindracea Perca flavescens Laurel Creek, Ontario, Molnar and Fernanado Canada (1975) Philometra obturans Rybinsk Reservoir, Izyumova (1960) Esox lucius USSR Lake Dusia, Lithuania, Rautskis (1970b) Esox lucius USSR Philometra ovata Rybinsk Reservoir, Izyumova (1958) Abrarnis brama USSR Rybinsk Reservoir, Izyumova (1960) Blicca bjoerkna USSR Philometra rischta Rybinsk Reservoir, Izyumova (1959a) Gymnocephalus cernua USSR Blicca bjoerkna

Philometroides cyprini

Cyprinus carpio Cyprinus carpio

Philometroides huronensis

Catostomus commersoni

Philometroides sanguinea

Carassius auratus gibelio

Raphidascaris acus

Gasterosteus aculeatus

Esox lucius Esox lucius Esox lucius Esox l u c k

Spinitectus gracilis

Esox lucius Lota lota Perca fluviatilis Perca jlavescens

Truttaedacnitis truttae

Lampetra lamottenii

Cystidicoloides tenuissima Dichelyne (Cucullanellus) bullocki

Salmo salar (juvenile)

3aiii. EAST COAST

Fundulus heteroclitus

Kalingrad, Minsk, Moscow districts, USSR Latvia, USSR Lake Huron, Ontario, Canada Lake Bol'shoe, Omsk Region, USSR River Chernaya, near River Neva, USSR River Volga, USSR Rybinsk Reservoir, USSR Oka River, USSR Lake Dusia, Lithuania, USSR Lake Vbrtsjarv, Estonia, USSR

Vasil'kov (1964, 1968a, b, 1976) Vismanis (1966, 1967, 1970) Uhazy (1977a, b, c, 1978) Lyubina (1970) Baninina and Isakov (1972) Bogdanova (1958) Izyumova (1960, 1964) Markova (1958) Rautskis (1970b) Tell (1971)

Lake Opeongo, Ontario, Cannon (1973) Canada Blue Springs Creek, near Pybus et al. (1978b) Lake Ontario, Canada temperate grassland, mixed forest Trout Brook, New Hare and Burt (1975) Brunswick, Canada Johnson Creek, Kuzia (1979) Durham, New Hampshire, USA

CL

F

wl

TABLE IV (continued) Climate zones

Nematode species

Host species

Locality

References

3aiii. (continued) Philometra species Morone saxatilis Philonema agubernaculum Salmo salar Salvelinus fontinalis Osmerus mordax Salmo salar

3b. MARINE WEST COAST Camallanus lacustris

Perca fluviatilis Perca fluviatilis Perca fluviatilis Perca fluviatilis Esox lucius

Camallanus truncatus

Perca fluviatilis Perca fluviatilis

Capillaria acerinae Capillaria coregoni

Gymnocephalus cernua Salma trutta

Capillaria salvelini

Salmo trutta

Chesapeake Bay, USA Maine, USA

Bier et al. (1974) Meyer (1960)

Rangeley Lakes, Maine, Vik (1964) USA temperate grasslands, deciduous forest Lake Rrayetjern, Andersen (1978) Norway Llyn Tegid, Wales Andrews (1977) Serpentine, London, Lee (1977) England Shropshire Union Canal, Mishra (1966) Cheshire, England Rostherne Mere, Rizvi (1968) Cheshire, England Lake Dargin, Poland Wierzbicki (1970) Lakes, outskirts of Priemer (1979) Berlin, Germany Germany Thieme (1961, 1964) River Sil basin, Spain Corder0 del Campillo and Alvarez Pellitero (1976a) ;Alvarez Pellitero et al. (1978a) Chirk Fish Hatchery, Aderounmu (personal Clwyd, Wales communication)

Salmo trutta

Llyn Celyn, Wales

Salmo trutta

Llyn Tegid, Wales

Salmo trutta Salmo trutta Salmo trutta

Afon Terrig, Wales Loch Leven, Scotland Llyn Tegid, Wales

Salmo trutta Salmo trutta Salmo trutta

Afon Terrig, Wales River Alyn, Wales River Sil basin, Spain Afon Terrig, Wales River Alyn, Wales Rivers Lupawa and Reda, Poland

Paraquimperia tenerrima Philometra ovata Philometra rischta Philometroides sanguinea

Salmo trutta Salmo trutta Salmo gairdneri Salmo trutta Thymallus thymallus Anguilla anguilla Abramis brama Abramis brama Carassius carassius

Philonema oncorhynchi

Oncorhynchus nerka

Raphidascaris acus

Perca fluviatilis Esox lucius Perca fluviatilis Salmo trutta

Cystidicola farionis

Cystidicoloides tenuissima

Llyn Tegid area, Wales Lake Dqbie, Poland Lake Dqbie, Poland Lakes Skrwilno and Track, Poland Sweltzer Creek, Cultus Lake, British Columbia, Canada Llyn Tegid, Wales Loch Leven, Scotland

Aderounmu (personal communication) Aderounmu (personal communication) Awachie (1963a) Campbell (1974) Aderounmu (personal communication) Awachie (1963a, 1973b) Rahim (1974) Alvarez Pellitero (1976b, 1976c), Corder0 del Campillo and Alvarez Pellitero et al. (1978a) Awachie (1963a, 1973b) Rahim (1974) Wierzbicki (1962) Chubb (1961) Wierzbicki (1978) Wierzbicki (1978) Wierzbicki (1960) Platzer and Adams (1967) Andrews (1977) Campbell (1974)

TABLEIV (continued) Climate zones

Nematode species

Host species

Locality

References

3b. (continued)

Rhabdochona denadata

Salmo trutta

River Sil basin, Spain

Esox lucius

River Lugg, Herefordshire, England River Sil basin, Spain

Rhabdochona gnedini

Cyprinids, usually Leuciscus cephalus cabeda Barbus barbus bocagei

Rhabdochona sulaki

Salmo trutta

Spinitectus gordoni

Salmo gairdneri Salmo trutta

Truttaedacnitis truttae

Anguilla anguilla Lampetra planeri

Cordero del Campillo and Alvarez Pellitero (1976a) ; Alvarez Pellitero (1978); Alvarez Pellitero et al. (1978a) Davies (1 967)

Alvarez Pellitero et al. (1978a); Pereira Bueno (1978) River Sil basin, Spain Alvarez Pellitero et al. (1978a) ;Pereira Bueno (1978) Leon Province, Spain Cordero del Campillo and Alvarez Pellitero (1976a) River Sil basin, Spain Cordero del Campillo and Alvarez Pellitero (1 976a, b) ; Alvarez Pellitero et al. (1978a) Llyn Tegid area, Wales Chubb (1961) River StensBn, Sweden Moravec and Malmqvist (1977)

Salmo trutta Salmo trutta 3 ~ SEMI-DESERT .

Camallanus lacustris Camallanus truncatus

Capillaria brevispicula Capillaria coregoni

Lucioperca lucioperca Silurus glanis Lucioperca Iucioperca Lucioperca lucioperca Esox lucius Lucioperca lucioperca Abramis brama Salmo trutta

Capillaria lewaschofi Pelecus cultratus Cystidicoloides tenuissima Salmo trutta

Philometra abdominalis Philometra nodulosa Philometra ovata

Lucioperca lucioperca Catastomus commersoni Abramis brama Abramis brama Cyprinids

Philometra rischta

Abramis brama Rutilus rutilus caspicus

River Alyn, Wales River Teify, Wales prairie and steppe Volga Delta, USSR

Rahim (1974) Thomas (1964)

Dnepr Delta, USSR Volga Delta, USSR Dnepr Delta, USSR

Komarova (1964) Dubinina (1949) Komarova (1964)

Dubinina (1949)

Komarova (1964) Cordero del Campillo and Alvarez Pellitero (1976a); Alvarez Pellitero et al. (1978a) Komarova (1964) Dnepr Delta, USSR Alvarez Pellitero (1976b, River Duero basin, 1976~);Cordero del Spain Campillo and Alvarez Pellitero (1976a) ; Alvarez Pellitero et al (1978a) Dnepr Delta, USSR Komarova (1964) Colorado, USA Dailey (1966) Volga Delta, USSR Dubinina (1949) Dnepr Delta, USSR Komarova (1964) Mingechaur Reservoir, Mikailov (1963) Azerbaidan, USSR Mingechaur Reservoir, Mikailov (1963) Azerbaidan, USSR

Dnepr Delta, USSR River Duero basin, Spain

e

t 4 0

TABLE IV (continued) Climate zones

Nematode species

Host species

Locality

References

3c. (continued) Philometra species undetermined Raphidascaris acus

Rutilus rutilus Salmo trutta

Lucioperca lucioperca Silurus glanis Esox lucius Lucioperca lucioperca Vimba vimba vimba natio carinata Esox lucius Perca fluviatilis Rhabdochona acuminata Barbus barbus Varicorhinuscapoeta Rhabdochona ? cascadilla Salmo trutta Rhababchona denudata

Iriklin Reservoir, USSR River Duero basin, Spain

Volga Delta, USSR

Corder0 del Campillo and Alvarez Pellitero (1976a) ; Alvarez Pellitero (1978); Alvarez Pellitero et al. (1978a) Dubinina (1949)

Dnepr Delta, USSR

Komarova (1964)

Krasnodar region, USSR Mingechaur Reservoir, Azerbaidan, USSR North Fork, South Platte River, Colorado, USA Cyprinids, usually River Duero basin, Spain Leuciscus cephalus cabeda Blicca bjoerkna Rutilus rutilus heckeli

Kashkovski (1967)

Dnepr Delta, USSR

Supryaga and Mozgovoi (1 974) Mikailov (1963) Voth et al. (1974) Alvarez Pellitero et al. (1978a); Pereira Bueno (1978) Komarova (1 964)

(Not indicated) Rhababchona gnedini

Barbus barbus bocagei

Rhababchona sulaki

Salmo trutta

Spinitectus gordoni

Salmo gairdneri Salmo trutta

Truttaedacnitis sphaerocephala

Acipenseridae

Raphidascaris acus

Esox lucius

3d. DESERT

3e. SUB-POLAR Camallanus lacustris

Osmerus eperlanus

Esox Iucius Lota Iota Perca fluviatilis Perca fluviatilis Capillaria species undetermined

Lota Iota

Mingechaur Reservoir, Mikailov (1963) Azerbaidan, USSR Alvarez Pellitero et al. River Duero basin, (1978a) ; Pereira Bueno Spain (1978) Leon Province, Spain Cordero del Campillo and Alvarez Pellitero (1976a) Cordero del Campillo River Duero basin, and Alvarez Pellitero Spain (I976a, b) ;Alvarez Pellitero et al. (1978a) Azov and Caspian Seas, Khromova (1975) lower reaches River Volga, USSR cool desert Engashev (1964b, 1966a, Amu Darya basin, USSR 1969) coniferous forest Lake Pyhajarvi, Finland Levander (1926) Lake Konche, Karelia, Malakhova (1961) USSR Lake Kuito, Karelia, Shul'man et al. (1974) USSR Lake Konche, Karelia, Malakhova (1961) USSR

c h) h)

TABLEIV (continued) ~~

Climate zones

~

Nematode species

Host species

Locality

References

3e. (continued) Cystidicola farionis

Coregonus clupeaformis Coregonus nasus

Haplonema hamulatum Philometra obturans

4. Polar 4a. POLAR 4b. ICE-CAPS 5. Mountain

Esox lucius Lota Iota Esox lucius

Philometra species undetermined Philonema sibirica

Rutilus rutilus

Raphidascaris acus

Esox lucius Lota Iota

Coregonus albula

no seasonal studies no suitable habitats for freshwater nematodes no seasonal studies

Cold Lake, Alberta, Canada Bothnian Bay, Baltic Sea Lake Konche, Karelia, USSR Lake Konche, Karelia, USSR Lake Konche, Karelia, USSR Lake Kuito, Karelia, USSR Lake Konche, Karelia, USSR tundra icefields and glaciers heath, rocks and scree

Leong (1975) Valtonen and Valtonen (1978) Malakhova (1961) Malakhova (1961) Malakhova (1961) Rumyantsev (1965) Malakhova (1961)

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Geller and Babich (1953) showed that embryonation of the eggs of Contracaecum bidentatum was considerably extended by a fall in temperature. At 20-22°C larvae developed in 6 to 8 days, whereas at 8-10°C they were not formed until 20 to 25 days. The eggs were laid in the intestine of Acipenser ruthenus at an 8-16 blastomere stage. Within the eggs in the water the larvae moulted once. The freshly emerged larvae were 0.25-0.3 mm long and could survive for 3 to 15 days depending on water temperature. The third and invasive larval stage occurred in invertebrate intermediate hosts, the fourth moult and development to maturity in A . ruthenus (Geller and Babich, 1953). Geller (1957) observed that in the River Volga, U.S.S.R., up to 94% of A . ruthenus were infected. Occurrences were at a peak in September and October, and were highest after a period with a warm autumn followed by an early spring. By contrast a cool autumn and a late spring abruptly decreased the incidence and intensity of occurrence. The C. bidentatum normally lived in the oesophagus and stomach of the A . ruthenus, but in starved or dying hosts the gravid females tended to emerge from the gill slits. If these, or other C. bidentatum passed from the acipenserids were eaten by small fishes the eggs retained their viability. Geller (1957) considered that this process might play an important role in the distribution of the eggs in the habitat. Goezia ascaroides (Goeze, 1782) According to Mozgovoi et al. (1971) Silurus glanis was the definitive host. They described the details of the life cycle. KaiiC (1970) reported immature Goezia ascaroides in Anguilla anguilla July, August (peak) and September and mature worms in October (peak), falling November, from Lake Skadar, Yugoslavia. Raphidascaris acus (Bloch, 1779) (For Larval stages see Part 111, p. 55 of review). There are many studies of Raphidascaris acus. Some of these contain little detailed information, so will not be discussed here. They include Zschokke (1884, as Ascaris a m and A. adiposa), Sr6mek (1901, as Ascaris crisfata), Dubinina (1949), Bogdanova (1958), Markova (1958), Izyumova (1960, 1964), Komarova (1964), Rautskis (1970b), Banina and Isakov (1972), Cernova (1975) and Andrews (1977). Hosts and localities are to be found in Table IV. The life cycle was studied by Thomas (1937, as Raphidascaris canadensis). At 2428°C the eggs embryonated within eight hours. After one moult in the egg, infection of minnows and Percaflavescens was achieved, to give larvae encapsulated in the mesenteries and livers of these fishes. The cycle was completed when the small fishes were eaten by Esox lucius. However, some more recent life cycle investigations have claimed the need for an invertebrate intermediate host, for instance Chironomus species, other chironomid genera, Tubificidae, Naididae etc. (see for example, Engashev, 1964a; Kosinova, 1965). Subsequently, Engashev (1965d) considered that an oligochaete was an obligatory intermediate host for Raphidascaris acus, and that the insect larvae were infected by eating oligochaetes. Cyprinid and

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other fishes in their turn became infected by larvae which became encapsulated in the tissues (Engashev, 1965e). Such larvae persisted in these fishes to provide a source of invasion for the predatory fishes at all times of the year (see Engashev, 1965c, 1966b and Part I11 of this review). Moravec (1970a) made further investigations, which showed that the invertebrates were reservoir hosts for R. acus, whereas appropriate fishes were in fact the intermediate hosts, thus confirming the view of Thomas (1937). In summary, according to Moravec (1970a) the life cycle of Raphidascuris ucus was: the adult worms occurred in the pyloric caeca and anterior portion of the intestine of predatory fishes and their eggs were released to the water along with the host faeces. The first stage larvae developed after several days, moulted within the egg capsule, to become a second stage invasive larva. At a water temperature of 22°C this development took five days. Some days thereafter larvae might emerge from their egg shells, and these, or the unhatched eggs containing the second stage larvae, might be eaten by either invertebrates or fishes. In invertebrates the larvae penetrated the body cavity where they could grow slightly, but did not moult for a second time. When these invertebrates were eaten by fishes, or accidentally, the eggs or free larvae of R. acus were ingested, the second stage larvae penetrated the wall of the fish intestines and entered the body cavity, mainly the liver, where the next moult occurred. At this point these third stage larvae became invasive to the definitive hosts, predatory fishes. The remaining two moults occurred in the intestines of the definitive host, where at summer water temperatures egg production commenced in about two months. A full discussion of all the life cycle literature can be found in Moravec (1970a). Since that date Supryaga and Mozgovoi (1974) have carried out further life cycle studies. In the predatory definitive host fishes either one or two generations of adult worms can occur each year. One generation was reported by Malakhova (1961) in Esox lucius and Lota lota at Lake Konche, Karelia, U.S.S.R., Davies (1967) in E. Iucius at the River Lugg, Herefordshire, England (gravid females July), KaiiC (1970) in Anguillu anguilla at Lake Skadar, Yugoslavia (peak June), Moravec (1970b) in Sulmo trutta at the River Bystfice, Czechoslovakia (egg release May and June, see Fig. 7), Tell (1971) in E. Zucius, L. Zofa and PercafEuviutilis at Lake Vbrtsjarv, Estqnia, U.S.S.R. (adults at maximum end of May and beginning of June), Zitiian (1973) in Sulmo gairdneri, S. trutta and Thymallus arcticus baicalensis at Dobsina Dam, Slovakia, Czechoslovakia (oviposition July and August), and Moravec (1979b) in E. lucius at the MBcha Lake fish pond system, North Bohemia, Czechoslovakia (gravid females May and beginning of June). Two generations each year were found by Engashev (1964b, 1966a, 1969) in Esox Iucius in lakes in the Amu Darya Basin, Uzbekistan, U.S.S.R. (main generation early spring, March-May, smaller one in autumn, August to October), Supryaga and Mozgovoi (1974) in E. lucius and P.Juviatilis in the Krasnodar Region, U.S.S.R. (first generation end of February to beginning of June, second end of August to October), and Corder0 del Campillo and Alvarez

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Pellitero (1976a), Alvarez Pellitero (1978) and Alvarez Pellitero et at. (1978a) in S. trutta in rivers in L e h , North West Spain (adult egg producing worms spring-summer, maximum numbers and autumn-winter, at lower numbers). The occurrence of either one or two generations will be determined by the water temperatures during the summer months which must be high enough for a sufficient period to allow the complete maturation of a n autumn generation of Raphidascaris acus, from egg in spring, through fish intermediate host and finally for growth to sexual maturity to take place in the fish definitive host.

L

I

h

-EE 40

5 30 E2 20 8

e

-

g 10

S

i IV

v

VI

VII Vlll

IX

x

XI

XI1

I

I1

111

IV

v

VI

VII

Month I

1967

1968

I

FIG.7. The range of lengths and maturation of the nematode Raphidascaris acus in the intestine of Salmo m r f a from the River Byst'iice, Czechoslovakia, April 1967 to July 1968. (From Moravec (1970b), Fig. 3, p. 321.) 1111 = adults absent = adults present

Engashev (1965a) showed that benthophagous fishes which fed on invertebrates containing Raphidascaris acus larvae were infected by larval stages more often and more intensively than were phytophagous or planktophagous fishes which were insignificantly infested or free from infection. The larvae were cumulative in Abramis brama, but dynamic seasonal changes were seen for the adults in Esox lucius. In both circumstances incidence and intensity increased with fish age and size (Engashev, 1965b). A mortality of Abramis brama caused by the larvae of R. acus in Lake Dvin-Velinsk, Pskov District, U.S.S.R., from ice break in the spring of 1969 until July of the same year was described by Bauer and Zmerzlaja (1973). Campbell (1974) at Loch Leven, Scotland, found maximum incidences and intensities of infection of PercafEuviatilis and SaImo trutta during the summer months. During his survey from 1967 to 1972 the overall incidence in the habitat declined.

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According to Pojmanska et al. (1978) who surveyed the effect of thermal pollution in lakes in the Konin region of Poland Raphidascaris acus prevailed in the cooler lakes and was therefore a thermophobe. (b) Family Cucullanidae. The species names are mainly those from Petter (1974). Cucullanus dogieli Krotas, 1959 Marits and Vladimirov (1969) recorded this species in Vimba vimba vimba natio carinata from Dubossary Reservoir, Moldavia, U.S.S.R., as follows (incidence, range): spring 0%; summer 5.0%, 1-17; and autumn 7.6%, 1-18. Dichelyne (Cucullanellus) bullocki Stromberg and Crites, 1972. Kuzia (1979) examined the seasonality of this species in Fundulus heteroclitus at Johnson Creek, Durham, New Hampshire, U.S.A. Third stage larvae were recruited into the fishes in summer, developed into fourth stage larvae by autumn, overwintered in the fishes to mature to adult worms the following late spring. The infective third stage larvae were reared in sea water from eggs recovered from gravid female nematodes. Dichelyne (Cucullanellus) cotylophora (Ward and Magath, 1916) Pearse (1924) observed this species (as Dacnitoides cotylophora) in Perca JYavescens in the Yahara River Lakes, Wisconsin, U.S.A., in June to October and January, but not in November or February to March. At Lake Opeongo, Ontario, Canada, Cannon (1973) recorded the highest incidences in P . JYavescens in mid-summer (June 1967, July 1968). Amin (1977) at Lake Michigan, U.S.A., noted one male and one female worm in November. Amin (1977) proposed revival of the genus Dacnitoides as a valid independent entity, of which D . cotylophora was the type species. Dichelyne (Dichelyne) robustus (Van Cleave and Mueller, 1932) Spa11 and Summerfelt (1969) at Lake Carl Blackwell, Oklahoma, U.S.A., found Dichelyne (Dichelyne) robustus during June, July and early August in both 1967 and 1968 in Ictalurur punctatus. Otherwise, one worm was seen in October 1967. They could not explain the disappearance of the worms after the summer. Truttaedacnitis sphaerocephala (Rudolphi, 1809) Khromova (1975) examined the life cycle of this parasite of acipenserid fishes (as Dacnitis sphaerocephalus caspicus) in the Azov and Caspian Seas and the lower reaches of the River Volga, U.S.S.R. The fishes were invaded by third stage larvae during the summer months. Attempts to infect the Acipenseridae by direct invasion with larvae failed, so it was concluded that an intermediate host was essential for the completion of the life cycle. Cucullanid type larvae were found in Nereis diversicolor in the Caspian Sea, and it was suggested by Khromova (1975) that these might be the intermediate hosts. Kakacheva-Avramova (1977) found Truttaedacnitis sphaerocephala (as Cucuiianussphaerocephala) in Acipenser giildenstadti from the River Danube, Bulgaria, in late summer. Truttaedacnitis truttae (Fabricius, 1794) Truttaedacnitis stelmioides is included here as a synonym of T . truttae

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following the study of the life cycle by Moravec (1979c, as Cucullanus (Truttaedacnitis) truttae). Moravec (1 976a) speculated concerning the role of Lampetra planeri in the life cycle of Truttaedacnitis truttae, suggesting that the adults named as Dacnitis stelmioides (=T. stelmioides) by Vessichelli (1910) were in fact progenetic forms of T. truttae. Moravec and Malmqvist (1 977) presented further evidence to support this view. However, Pybus et al. (1978a) considered T. stelmioides a distinct species. Pybus et al, (1978b) demonstrated the life cycle of T. stelmioides in Lampetra lamotteni in Canada. The eggs hatched on the stream bed in spring and early summer (late April, early May). Hatching was influenced by water temperature, at 13°C it required 18 to 20 days and at 22°C only 8 to 10 days. Development was not completed at 4 and 10°C. At 13°C the hatched larvae remained alive for up to 75 days. Living larvae were recovered from the intestines and cystic ducts of the liver of ammocoete and transformer L. lumotteni. Larval incidence was low in spring, but relatively high during summer, decreased significantly in autumn and was extremely low during winter. The mean length of the larvae increased with increasing length of the ammocoetes. Adult T. stelmioides were found in the intestine lumen of transformer and adult L. lamotteni. The larvae in the liver were in a state of arrested development which could persist for up to four years. During the transformation process these larvae re-entered the intestine of the host. L. lamotteni transformed early autumn, spawned the following spring and died thereafter. Accordingly, the egg release from the gravid T. stelmioides could occur from August to May. Pybus et al. (1978b) were of the opinion that transmission took place during late autumn and throughout the spring and early summer. Owing to the eggs ceasing development below 13°C they considered transmission during winter unlikely. Spawning adult L. lamotteni returned to the ammocoete beds in spring when the water temperature was above 15°C. Thus, Pybus et ai. (1978b) did not accept that T. stelmioides was a synonym of T. truttae, but thought it distinct, using L. lamotteni as both intermediate and definitive hosts. The life cycle of Truttaedacnitis truttae in Czechoslovakia was investigated by Moravec (1979~).Female T. truttae laid 2 to 5 eggs at 1-2 minute intervals. At 5°C development did not occur, but at 22-24°C hatching as second stage larvae occurred in 7 to 8 days, although some did not hatch for a further five days or more. The larvae lived six days at 22-24°C but 28 days at 13°C. Attempts to infect Salmo gairdneri with second stage larvae directly were unsuccessful. The development of the larvae in Lampetru planeri was not studied owing to lack of suitable fishes. Third stage larvae from L. planeri were fed to S. gairdneri. At first the larvae attached to the wall of the intestine in the region of the pyloric caeca or slightly below. At day 20 postinfection a third moult occurred to give fourth stage larvae which moved into the pyloric caeca. A fourth moult took place between days 30 to 40, and the juvenile T. truttue continued to grow, so that by day 89 gravid female nematodes were found. Thus, at 13 to 15°C the prepatent period was about three

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months. Moravec (1979~)suggested that ammocoete L. planeri acted as intermediate host only, the adult T. truttae developing in predatory fishes. If metamorphosis of the ammocoetes containing T. truttae larvae occurred, then the nematodes could achieve full development, and in this circumstance the adult L. planeri became definitive hosts. Accordingly, Moravec (1979~) disagreed with Pybus et al. (1978a) and thought T. stelmioides conspecific with T. truttae. Truttaedacnitis truttae was found in the intestine lumen of Anguilla anguilla in the Llyn Tegid area, Wales, by Chubb (1961). Female worms containing eggs were recovered January (28.6 % of nematode population), March (45 %), May (46 %), June (52 %), but no worms were found in July, and only one male in October. Samples of A. anguilla were not available for other months. Thomas (1964) observed T. truttae (as Dacnitis truttae) in Salmo trutta in the River Teify, Wales at all times of the year. By contrast Rahim (1974) noted this nematode in S . trutta from the River Alyn, Wales, only in January, March, May to July and not in the other months. Moravec and Malmqvist (1977) found T. truttae adults in adult Lampetraplaneri from the River Stensin, Sweden, in September and October 1975 and March and April 1976. These T. truttae were in the abdominal cavities of the L. planeri. Paggi et al. (1978) have studied occurrence of T. truttae in S. trutta from the River Trino, Italy, but did not provide details. (c) Family Quimperiidae Haplonema hamulatum Moulton, 1931 Arthur and Margolis (1975) included Zchthyobronema conoura (Linstow, 1885) senxu Gnedina and Savina, 1930 as a synonym of this species. Malakhova (1961) reported I. conuura from Lake Konche, Karelia, U.S.S.R., in Esox lucius (incidence, average intensity, range) autumn (0 %), winter (l8.2%, 1-75, 1-3), spring (24.7%, 4.84, 1-17) and summer (0%) and Lota Iota autumn (8%, 3.8, 1-9), winter (42.9%, 8.76, 1-62), spring (54%, 5.72, 1-99) and summer (14-4%, 1-67, 1-2). L. Iota was the usual definitive host, the infections in E. lucius were probably acquired secondarily by predation. Paraquimperia tenerrima (Linstow, 1878) According to Moravec (1971a) Filaria conoura Linstow, 1885 was a synonym of Paraquimperia tenerrima. SrAmek (1 901) reported F. conoura from Anguilla anguilla at PodEbrady, Czechoslovakia in May 1900, and in addition, from other fish species. However, Moravec (1971a) thought that Srhmek (1901) may have mistaken members of the genus Rhabdochona for P. tenerrima in these other fishes. Chubb (196 1) noted incidences of Paraguimperia tenerrima in Anguilla anguilla from the Llyn Tegid area as follows: January OX, March 3*6%, May 1-7%,June 2.5%, July 60% and October 17%. Samples of A . anguilla were not obtained during other months. Moravec (1974) collected eggs from gravid female Paraquimperia tenerrima which hatched in 5 to 6 days at 20-25°C. The free larvae moulted at 8 to 10 days, to give second stage individuals which died within six days. Some second stage larvae were fed to two Anguilla anguilla. One at examina-

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tion was uninfected, but the other on day 16 post-infection contained a larva, thought to be at the third stage. Moravec (1974) did not exclude the possibility of a direct life cycle, but suggested it likely that invertebrates or small fishes would serve as intermediate or transport hosts. 2. Order Spirurida Ivashkin (1961) has summarized the knowledge about the life cycles of the spirurid nematodes. (a) Family Camallanidae Camallanus lacustris (Zoega, 1776) Seasonal records of Camallanus lacustris originating from faunal studies are to be found in the following papers: Zschokke (1884, as Cucullanus elegans), Srhmek (1901, as C . elegans), Levander (1926, as C . elegans), Ruszkowski (1926, as C . elegans), Dubinina (1949), Izyumova (1958, 1959a, b, 1960, 1964), Komarova (1964), Ergens (1966), Rizvi (1968), Shul'man et al. (1974) and Lee (1977). Hosts and localities are provided in Table IV. These publications are not discussed further here. Kupriyanova (1954) studied the life cycle of Camallanus lacustris. Mesocyclops leuckarti, Acanthocyclops viridis and Cyclops strenuus served as intermediate hosts. At 19 to 21°C the first moult occurred in 1 to 2 days, the second in 5 to 6 days. Temperatures from 6 to 9°C slowed development, the first moult taking place in 2 to 3 days and the second in 15 days. The third stage larvae in the copepods were fed to fry of Abramis brama, Leuciscus idus and L. leuciscus. The larvae survived in the anterior intestine for 37 days. These fry were fed to Percajluviatilis. During the first 14 days postinfection a considerable increase in the size of the larvae occurred. By 20 to 25 days the buccal capsule became tridentate; this process was completed in a further 5 to 7 days. Sexual maturity was achieved more slowly than in Camallanus truncatus, but this time was not stated. Kupriyanova (1954) considered that the life cycle could be completed either with or without the transport fish hosts, which might also serve as reservoir hosts. Campana-Rouget (1961) also investigated the life cycle of Camallanus lacustris. First stage larvae from the female worms were fed mainly to Acanthocyclops viridis and Macrocyclops species. Two larval moults occurred in these copepods, and the third stage larvae developed no further until eaten by a fish. In Perca jluviatilis the fourth stage was reached rapidly. Other fishes served as transport hosts. Moravec (1969) added more detail. Free first stage larvae remained viable in water for 12 days at 22"C, but 80 days at 7°C. A range of copepod hosts was used, development was completed to a 3rd stage invasive larva in 11-12 days at 20 to 25°C. In P. jluviatilis the third moult occurred at 13 to 15 days, the last moult of the male worms on the 35th day, but of the female C . lacustris on the 67 to 69th day. The males were sexually functional by the 67 to 69th day, so that copulation with the females occurred. The first motile larvae were seen in the female worms by 91 days post-infection. Moravec (1969) pointed out a number of differences between his observations and those of Kupriyanova (1954.)

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The third stage invasive larvae in copepods were a rich orange colour according to Moravec (1969). Monchenko (1972) demonstrated that only the dark brown immobile larvae from copepods would establish in Rutilus rutilus fry. Moravec (1971d) examined the problem of host specificity, reservoir parasitism and secondary infections of Camallanus lacustris. He recognized three groups of hosts: predatory fishes, in which normal development occurred, including Percidae, Salmonidae, Gadidae, and probably also Siluridae and Esocidae. Perca jluviatilis was the typical host. Non-predatory Cyprinidae and Cobitidae retained the third stage larvae for 5 to 20 days post-infection, but no changes of the larvae took place, so that these fishes served only as reservoir hosts. In predatory Cyprinidae, Leuciscus cephalus, development did occur but more slowly than in the first group of predatory fishes. Secondary infections of fourth stage larvae and adult C. lacustris were shown experimentally to re-establish in predatory fishes. Moravec (1979b) however considered that the survival times of C. lacustris in Esox lucius, a secondary predatory host, were short owing to the fact that he found no female nematodes containing larvae. Invasive third stage larvae from copepods would not develop in the intestine of E. lucius. Tornquist (1931), in Sweden, reported that the seasonal pattern of occurrence of Camallanus lacustris was of invasion of host fishes during summer, growth and maturation during autumn and winter, and release of the larvae from the female worms during late spring and summer. Other authors have not found such a well-defined seasonal development. Thus, at Lake Konche, Karelia, U.S.S.R., Malakhova (1961) observed little change in incidence of infection in Perca jluviatilis through the seasons, whilst some other authors, for example Mishra (1966), Rautskis (1970a), Wierzbicki (1970) and Andrews (1977) have found more varied incidences in P. Jluviatilis through the year, nonetheless, without obvious seasonal pattern. Andersen (1978) at Lake Reryetjern, also in P. jluviatilis, did find incidences all year, but the highest were autumn and early winter, with a marked drop during the spring months, lowest in May-June. Mishra (1966) at the Shropshire Union Canal, Cheshire, England, found immature female C. lacustris in all months except May and December and females containing larvae in the uteri in all months except June. Wierzbicki (1970) at Lake Dargin, Poland, observed a nearly equal abundance of the developmental stages at all seasons of the year. Andrews (1977) at Llyn Tegid, Wales, noted third and fourth stage larvae in P.fluviatilis during all months but with a low incidence July to September, and highest incidences during February, October and December 1975 and February 1976. Females containing larvae were also present all months, although most abundant during July and September 1975. During the autumn and winter of 1975-76 their incidence declined steadily suggesting that seasonal differences in gain and loss of C. lacustris from the intestines of the fishes took place. Release of first stage larvae was considered to occur in most months at Llyn Tegid. Andersen (1978) also found all stages of development in a11 samples through the year, but gravid worms dominated the nematode population only during the summer and autumn months. Moravec (1979b)

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summarized the situation by suggesting that although new invasions of fishes occurred year round, the warm seasons, spring to autumn, were more favourable for the development of the worms than the winter. Rautskis (1 977) examined the seasonal dynamics of Camallanus lacustris in Perca fluviatilis in three lakes of different depths and thermal regimes, shallow Lake Obelija, and deep Lakes Galstas and Shlavantas, all in Lithuania, U.S.S.R. Highest incidences were seen in the shallow lake (91.6-100%), whereas by contrast lower incidences were found in one of the deep lakes, Lake Galstas (50-69.2%). In the other deep habitat, Lake Shlavantas extremely low incidences were seen-8.3 % in June-July only. Although Rautskis (1977) stated correctly that in the Lithuanian lakes he examined the infections of P . puviatilis were highest in the shallow one, more information is required before this conclusion can be generally applied. Molnir (1966a) studied the combined seasonal occurrence of Camallanus lacustris and C. truncatus in Gymnocephalus cernua and Lucioperca lucioperca from Lake Balaton, Hungary. Plankton feeding L. lucioperca fry acquired infections very early, and incidences reached 60 % by July. Perca fluviatilis at Llyn Tegid, Wales, also became infected during their first summer of life (Andrews, 1977). Camallanus oxycephalus Ward and Magath, 1916 Spall and Summerfelt (1969) examined the occurrence of Camallanus oxycephalus in Ictalurus punctatus and Pomoxis annularis at Lake Carl Blackwell, Oklahoma, U.S.A. Larval-bearing female worms were more posterior in the hosts intestines than either male or immature female nematodes. Some mature female worms were seen protruding from the fishes anus. Females outnumbered males, hence a differential or earlier mortality of males was suggested. An annual cycle was apparent. Although in P . annularis maturation of the nematodes was rarely completely uniform in any population or season, the majority of the mature females were found during the spring and early summer. C. oxycephalus recovered during autumn and winter were largely immature. Female worms were gradually seen to increase in size through the spring. The uteri filled with eggs during April, to hatch in utero during May. Female nematodes containing larvae remained throughout the summer, but their numbers became fewer after July. In I. punctatus C. oxycephalus was absent in June 1967 and May and June 1968 collections. Spall and Summerfelt (1969) did not find a significant relationship between incidence of C. oxycephalus and host sex, nor between shallow and deep sampling sites. Older I. punctatus were more heavily infected and became invaded by eating small fishes. A test of infection rate compared with season was found not to be statistically significant. The life cycle was studied by Stromberg (1973) and Stromberg and Crites (1974a). The first stage larvae occurred in the uterus of the female Camallanus oxycephalus. Free living first stage larvae infected Cyclops bicuspidatus and C. vernalis. Development was faster at higher temperatures: first moult three days post-infection at 25"C, five days at 20°C; second moult, six days at 25"C, but ten days at 20°C. The invasive third stage larvae remained coiled

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in the copepod haemocoel. Morone chrysops, Notropis hudsonius, N. spilopterus and PercaBavescens were infected. At 26°C the third moult occurred in these fishes 9 to 10 days after infection. The male C. oxycephalus underwent their final moult 17 to 18 days and the females on the 24th day postinfection. Small fishes served as reservoir hosts ; this was demonstrated using P . jluvescens. Natural reservoir hosts included Dorosoma cepedianum but development did not continue beyond the fourth stage larvae. Stromberg and Crites (1975b) demonstrated seasonal patterns of population structure, site selection, intensity, maturation and reproduction of tbe Camallanus oxycephalus in Morone chrysops in western Lake Erie, U.S.A. The water temperatures varied between 1°C in February to 23-24°C in July. C. oxycephalus was in fishes of all sizes, with no difference between sexes. The worm population was overdispersed. Adult worms were present during all months except July and August. During these months they were mostly third and fourth stage larvae. The fishes were invaded July-August, the worms lived about one year and the adults died during summer. In August the sex ratio of newly recruited males to females was 2: 1, by September it was 1 : 1, and it remained at this ratio until the following July. It changed briefly to 2: 1 before the old worms died. There was little change in incidence during the year. A marked decrease in intensity occurred between July and the following June. Intensity increased rapidly in July, the invasion period, but a loss of worms occurred by September, and a decrease continued thereafter through the year so that the mean number of reproducing females in June was 30-60 % less than the original number of immature female C. oxycephalus seen the previous August. In 1970-71 and 1971-72 Stromberg and Crites (1975b) observed that the generations were similar in timing and size. The 1972-73 generation was delayed. In November the mean worm burden of Camallanus oxycephalus was markedly lower than the 1970 and 1971 values. A density dependent regulatory mechanism was postulated. The new generation of Camallunus oxycephalus larvae in July were distributed along the entire intestinal tract. The one year old adults were in the rectum at this time, but were lost shortly after. In August as maturation commenced a posterior migration occurred so that two thirds of the worms occurred in the rectum. By October, and then until the death of the generation the following July, the nematodes remained in the rectum (Stromberg and Crites, 1975b). In April to May the growing female C. oxycephalus protuded from anal openings of their hosts. The seasonal growth, as expressed by mean body length compared with time, showed the following characteristics. The initial autumn growth of female worms was more rapid than that of the males, but the growth of the females was arrested over winter from November to May. A difference in mean body length of the males, November as compared with May, revealed that the males continued to grow during winter. However the females resumed rapid growth in April, which continued until their deaths in July, at which time the female C. oxycephalus were four to five times longer than the males (Stromberg and Crites, 1975b).

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Copulation was shown to occur in the autumn, as sperm cells were present in the uteri of the females in October and November. Fertilization of the ova occurred the following April when the ova were released into the uterus. Development thereafter was relatively synchronous, larvae were visible by mid-June, and most embryos had completed growth by late-June, so that the uteri were filled with active first stage larvae. Most of these larvae were released by prolapse of the uterus over a short period of time in late June to the end of July when the female nematodes protruded from the rectum of the host fish. The dispersal of the Camallanus oxycephalus larvae coincided with the annual cyclopoid copepod population peaks, so that Cyclops bicuspidatus and C. vernalis were a t their annual maximum density in June and July. However, annual seasonal differences did occur. Stromberg and Crites (1975b) noted that 1972 was a cold summer compared with 1971 and 1973. The C. oxycephalds dispersal periods compared with the availability of maximum copepod density were determined as: 1971 38 days, copepods available 19 days, potential effectiveness of transfer 50%; 1972 30 days, copepods available 1 1 days, effectiveness 36 % ; and 1973 29 days, copepods available 26 days, effectiveness 89 %. Thus, the actual period for contact between the released first stage larvae and the potential copepod intermediate hosts varied from year to year, and therefore would influence the effectiveness of invasion of the intermediate hosts and thus ultimately effect the size of the subsequent generation of adult C . oxycephalus. Stromberg and Crites (1975b) found that forage fishes such as Dorosoma cepedianum served as reservoir hosts for a few weeks, 5-23 August. Consequently, the period of invasion of the Morone chrysops by larvae of Camallanus oxycephalus was short. An obvious predator-prey preference was seen: large M. chrysops eating large D. cepedianum, and small M . chrysops eating small D. cepedianum. In the discussion of their observations about the biology of Camallanus oxycephalus, Stromberg and Crites (1975b) stressed the dynamics of the parasite population biology. In particular, they emphasised that the seasonal dispersal at a limited annual period when the copepod intermediate hosts were present maximized the probability of parasite-host contact and was an effective reproductive adaptation. The mechanisms were attributed to a delay in growth and maturation during winter, probably owing to either the host physiology or water temperature, followed by a rapid growth of the female worms in spring, not related to temperature alone. The growth occurred during the host spawning season, and therefore might be stimulated by rising host hormone levels. The rapid growth of the female nematodes allowed as a consequence a maximal production of larvae. These dynamics and growth patterns were determined by natural selection (Stromberg and Crites, 1975b). Other seasonal data concerning Camallanus oxycephalus have been given by Cloutman (1975) (see Table IV for hosts and locality). Crites (1976) suggested that he had found an alternative life cycle pathway. Fourth stage larvae of C. oxycephalus were found encapsulated in the mesenteries of the

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posterior intestine of two Aplodinotus grunniens from western Lake Erie, U.S.A. When fed to Micropterus dolomieui some of these larvae developed to maturity, suggesting an alternative manner of transmission to predacious fishes. At several habitats near San Marcos, Texas, U.S.A., Davis and Huffman (1978) noted that Gambusia afinis was used primarily as a paratenic host, but at least seven gravid worms were recovered June to November, therefore this fish species could also serve as definitive host. It would be interesting to have further details concerning the precise state of development of these “gravid” worms, to see if the life cycle pattern in more southern conditions compared with that in Lake Erie. Stromberg and Crites (1975a) have discussed long term increases in abundance of C. oxycephala in Lake Erie, U.S.A., between 1927 as compared with 1972. The importance of parasite-host contact frequency and its relationship to parasite population density and regulation is discussed. Camallanus sweeti Moorthy, 1937 Included in the genus Zeylanema by Yeh (1960), but Chabaud (1975) did not accept the validity of this genus. Moorthy (1938) found that 95% of Ophiocephalus gachua were infected by adult Camallanus sweeti in the Chitaldrug District, Mysore, India. Moorthy (1938) completed the life cycle experimentally using Mesocyclops leuckarti. Infected copepods were kept alive 52 days at 32-39°C but 70 days at 13-21°C. Natural infections of third stage larvae were found in Barbus puckelli, Barbus ticto, Lepidocephalichthys thermalis and Gambusia species. Moorthy (1938) observed only a low incidence of C. sweeti larvae in M . leuckarti, and deemed this curious, but postulated that it was possible that in Camallanus infestations there was a particular period of the year when infection of cyclops was at its maximum. Thus it was probable that only during this period one would succeed in getting many infested cyclops. In view of the scarcity of seasonal studies in tropical conditions, C. sweeti would seem to be ripe for further study. Camallanus truncatus (Rudolphi, 1814) Kupriyanova (1954) described the life cycle of Camallanus truncatus. The adult worms have been reported in fishes at all seasons of the year (Dubinina, 1949; Bogdanova, 1958; Izyumova, 1958, 1959a, b, 1960; Komarova, 1964; Ponyi et al., 1972; and Priemer, 1979: see Table IV for hosts and localities). However, Vojtkova (1959) and Izyumova (1964) in particular found maximum infections in autumn and winter, with a considerable decrease in spring and summer. A detailed analysis of the maturation of the adult worms in the definitive host fishes has not been attempted as far as the author is aware, but would be interesting, as in many localities C. lacustris and C. truncatus occur together in the same hosts. Camallanus species larvae Izyumova (1958, 1959a, 1960) recorded incidences of Camallanus larvae in fishes separately from incidences of adult worms. At the Rybinsk Reservoir, U.S.S.R., she found both C. lacustris and C. truncatus, so that these data are for both these species together. Overall larvae occurred at all seasons. In Lucioperca lucioperca maximum incidences were in the autumn,

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January-April 40.7 %, May-August 59.2 % and October-November 93.7 %, but in Perca fluviatilis minimal incidences were not at that time, JanuaryApril 19.2%, May-July 20 % and October-November 10 % (Izyumova, 1958), whilst in Gymnocephalus cernua maximal incidences were in winter 22.2%, as compared with spring 4.2%, summer 4.8% and autumn 0% (Izyumova, 1959a). These differences can be attributed to variation in feeding habits of the respective fishes. Camallanus species in aquarium fishes A number of species of Camallanus, including C. moraveci Petter, Cassone and France, 1974 (see Petter et al., 1974), C. cotti (Fujita, 1927) (see Stumpp, 1975) and C . fotedari Raina and Dhar, 1972 (see Campana-Rouget et al., 1976) have been reported in aquarium fishes either on importation or subsequently during their maintenance in aquaria. The life cycle of C. cotti was completed in aquarium conditions for two generations by Stumpp (1975) and Campana-Rouget et al. (1976) showed that the intermediate hosts for C.fotedari were Cyclops species. At 20-25°C the complete cycle was completed in nine weeks, to give adult males and females with eggs at the tenth week. Three successive generations were achieved in the aquarium conditions (Campana-Rouget et al., 1976). Species such as the aforenamed, easily kept in laboratory conditions, should serve as potentially useful models for experimental investigations of the factors influencing the population dynamics of these parasites, and perhaps as a result additionally contribute to our minimal knowledge of seasonal patterns of occurrence in tropical fishes. Procamallanus clarias Ali, 1956 Furtado and Tan (1973) reported Procamallanus clarias from Clarias batrachus in the paddy fields, Sungei Besar, Sabak Bernam, Malaysia with incidences (and average intensities per infected fish) of occurrence as follows : May 66.7% (4), June 81.3% (9,July 100% (20), August 100% (23), October 93.3% (14.3) and November 93.3% (10). In this area the seasons were governed by the monsoon rainfall, so that January to February was the dominant dry season, but July and August were also dry. The dominant wet season was September to December, but March to June were also wet. According to Furtado and Tan (1973) the occurrence of camallanids (see also Procamallanus parvulus, below) increased May to August and decreased October to November, thus indicating an association with the drier season. They concluded that the changes in infection were probably dependent on the variation in composition of the diet of the C. batrachus. ProcamaIIanus Iaeviconchus (Wedl, 1862) According to Iman (1971, quoted from Moravec, 1975) a considerable increase in incidence of Procamallanus laeviconchus in the definitive hosts Clarias anguillaris and C . lazera in the River Nile, Egypt, occurred at the end of the spring and in summer. Moravec (1975) experimentally demonstrated the life cycle. The nematodes were ovoviviparous, the first stage larvae were released in the uterus of the female worms. Mesocyclops leuckarti ingested these larvae, which penetrated to the haemocoel, and after two moults became invasive third stage larvae in six days at 23-24°C. Gambusia

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afinis served as a reservoir host, but no development occurred therein. Fourth stage larvae and adult P. Zaeviconchus were seen in naturally infected C. lazera. Moravec (1975) stated that, as demonstrated by earlier work (see Moorthy, 1938; Kupriyanova, 1954; Moravec, 1969), temperature was one of the most important factors which influenced the rate of development of the Camallanidae. During the hot summer months the period needed for the development of Procamallanus laeviconchus shortened, and the wealth of planktonic animals available at this time provided optimal living conditions for these nematodes. This was reflected in the considerable increase in the occurrence of P. Iaeviconchus in the definitive hosts at the end of the spring and in the summer as reported by Iman (1971, see above) and confirmed by Moravec (1 975). Procamallanus parvulus Furtado and Tan, 1973 Incidences of this species were observed by Furtado and Tan (1973) in paddy fields at Sungei Besar, Sabak Bernam, Malaysia, from Clarias batrachus as follows (average intensity per infected fish in parentheses) : May 26.7% (3), June 50% (4), July 81.8% (141, August 88.2% (15), October 60 % (7) and November 40 % (5). The pattern of occurrence was attributed by Furtado and Tan (1973) to an association with the dry season, the changes in infection probably dependent on the variation in composition of the diet of the host fishes (see also Procamallanus clarias, above).

(b) Family Anguillicolidae Esocinema bohemicum Moravec, 1977 A rare species located on the serosa of the swim bladder of Esox lucius. Moravec (1979b) noted it in the Micha Lake fish pond system, North Bohemia, Czechoslovakia, during two months of the year only: in January, one juvenile female and one gravid female and in May one male nematode. Skrjabillanus scardinii Molnir, 1965 Tikhomirova (1970) determined the life cycle of this nematode parasite of cyprinid fishes. Argulus coregoni and A . foliaceus served as intermediate hosts. She suggested that a seasonal cycle of development of the nematodes in the fishes, transfer of infection to and development in the Argulus species and transmission back to the fishes would be found. According to Moravec (1978~)Tikhomirova (1975) found the third stage invasive larvae of Molnaria erythrophthalmi (Molnir, 1966) in Argulus foliaceus. However Moravec (1978~)discovered fourth stage larvae in A . foliaceus in March and November in Czechoslovakia, and he suggested that, as in some other aquatic spirurids (e.g. Rhabdochona), the development of larvae in the intermediate host did not cease on reaching the third, invasive, stage but could attain at least the fourth larval stage. (c) Family Philometridae A key to the European philometrid nematodes can be found in Moravec (1978a). The North American species are listed in Hoffman (1967) and

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Margolis and Arthur (1979), whilst Ivashkin et al. (1971) described all the species to that date. Philometra abdominalis Nybelin, 1928 Faunal studies containing some information about the seasonal occurrence of Philometra abdominalis include those of Bogdanova (1958), Komarova (1964), Lyubarskaya (1970) and Kakacheva-Avramova (1973). However, according to Molnar (1967, 1969) full development of P. abdominalis was achieved only in a limited range of hosts (see below), not including some of those from which this nematode has been reported by Bogdanova (1958), Komarova (1964) and Lyubarskaya (1970) (see Table IV). Lelek (1964) collected more detailed information concerning the occurrence of Philometra abdominalis from Gobio gobio in the Rokytnii River, Moravia, Czechoslovakia, but it was Molnar (1967) who provided a fuller account of the seasonal pattern of development. G.gobio was the host in which the female P. abdominalis developed to full maturity (see below also). The life cycle took one year for completion. Molnhr (1967) found that the fishes became invaded by larvae in June and July (locality, see Table IV). In these months the larvae were first found in the abdominal cavities of the host fishes. During summer developing nematodes were present under the serosa of the swim bladder of the host and copulation occurred here. Developing female P. abdominalis were in the host abdominal cavity during August and September, but males and unfertilized females stayed throughout the year under the serosa of the swim bladder. The developing females in the abdominal cavity grew to 22-66 mm long by autumn and 60-72 mm in length by the following spring. At the beginning of May Molniir (1967) observed the first stages of development of the larvae, and by mid-May the uteri were filled with fully-developed larvae. At the end of June the female P. abdominalis left the host fishes actively via the anus. In the water the nematodes burst to release the larvae which survived 3 to 5 days. The intermediate hosts were Cj~clopsspecies (Molniir, 1967). Molniir (1967) found Philometra abdominalis in Hungary in Gobio gobio, as well as Barbus meridionalis, Leuciscus cephalus, L. leuciscus and Phoxinus phoxinus. He concluded (1969b) that fully-developed and developing abdominally localized female P. abdominalis were found in G . gobio and the majority of P. phoxinus, provided at least one male and one female occurred in the fish. In about 15% of L. cephalus and L . leuciscus full development also occurred. Males in the swim bladder serosa, or retarded females, were found in all hosts having only male or female worms, and in the majority (about 85 %) of the L. cephalus and L. leuciscus infected by P. abdominalis. Two developing females found in one L. cephalus abdominal cavity were encapsulated in a thick connective tissue capsule. Moravec (1977c) examined the biology of Philornetra abdominalis in the copepod hosts. The released first stage larvae lived in water for 25 days at 7"C, but only two days at 30-34°C. They moved about in the water, to be eaten by copepods. Thereafter, in the body cavity of the infected copepods two moults occurred, at 20-24°C on days 5 and 6 and days 7 and 9 respectively,

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to give third stage invasive larvae. A range of copepod species were easily infected in experimental conditions (Moravec, 1977~).At the Rokytka Brook, Czechoslovakia, Moravec (1 977b) studied the seasonal pattern of occurrence of the adult P . abdominalis in Phoxinus phoxinus. An obvious one year cycle of maturation was found. Female worms with first stage larvae in the uteri were present from the second half of June to the first half of September, depending on water temperatures of the previous year. Males and unfertilized females were present in the fishes all year. The maximum incidence of females with first stage larvae was in July and August. They were located in the fish abdominal cavities, amongst the testicular or ovarian tissues. The females migrated to the host anus, to push part of their body out into the water, where they burst to release the larvae. The release of the larvae coincided approximately with the time of sexual maturation of the P . phoxinus and also with the period of optimum presence of the zooplankton intermediate hosts. Moravec (1977b) noted that Acanthocyclops vernalis was probably the principal intermediate host (but see also above). The annual reinvasion of the P . phoxinus by P . abdominalis was July to September. Moravec (1977b) concluded, however, that the males and unfertilized females could survive for two years or more in the fishes, accounting for their presence at all times of the year, located mostly at the posterior part of the swim bladder of the P. phoxinus. Copulation occurred at that site, the fertilized females migrating to the abdominal cavity, where their rate of development was very rapid. From November onward eggs were seen in the uteri of some females, and by the following July-August the females contained the motile larvae. It will be noted that MoInhr (1967) in Hungary found gravid P . abdominalis during May and June, whereas in Czechoslovakia Moravec (1977b) found them in July and August, even until September. Moravec (1977b) attributed these differences to lower water temperatures in the Rokytka Brook, Czechoslovakia, as compared with those in the much warmer region of Hungary investigated by Molnhr (1967). Philometra cylindracea (Ward and Magath, 1917) The life cycle of Philometra cylindracea was examined by Molnhr and Fernando (1975) at Laurel Creek, Ontario, Canada. A one year cycle occurred. Mature female nematodes with well developed larvae occurred from the middle to the end of June. Thereafter, only dead females were seen. At 20°C the released larvae remained living in water for two days, but for seven days at 4°C. They were rapidly ingested by Cyclops species, to become invasive third stage larvae in 7-10 days at 20°C. Some Percaflavescens were infected on 26 June. One week later the fourth stage larvae were in the abdominal cavity and serosa and two weeks post-infection they were under the serous membrane, above or under the swim bladder. At two months following infection the female P . cylindracea were mostly free in the host abdominal cavity, although some remained in the swim bladder. The males occurred mostly under the serosa of the swim bladder, but also in the subperitoneal tissues of the abdominal wall, where they remained throughout the investigation. All developing female worms found by Molnhr and Fernando (1975)

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were in the abdominal cavity. In November they were 17-28 mm long, in April 26-32 mm and by May 46-65 mm in length. During this time they turned red in colour, and embryos developed in the eggs. The worms achieved full length, up to 97 mm, in June, at which time their uteri were filled with active larvae (Molnhr and Fernando, 1975).

Philometra fujimotoi Furuyama, 1932 This species was studied by Furuyama (1934) in Ophiocephalus argus from the vicinity of Keijo, Chosen, now Seoul, Korea. When collected in the early summer of 1928 the uteri of the female P. fujimotoi contained only fullydeveloped larvae. The adults were in the subcutaneous tissues of the fins. One male was found in the abdominal cavity of 0. argus. The fully-developed females burst on placing them into water. At an unstated temperature the larvae lived one to two weeks. A range of Cyclops species were infected, in which growth seemed to be completed in about one week. Some 0. argus were experimentally infected by Furuyama (1934). On 30 October some worms were found in the fin of one fish. In naturally occurring 0. argus small female P. fujimotoi were seen in the body cavity on 28 August, one male in the same site on 5 September. The latest time female worms were recovered from the body cavity of the fishes was 29 October. On 9 October a female with all the eggs at a 1-cell stage was noted in a fin. Overwinter, the female worms grew slowly in the fins, and the contained eggs stayed at the 1-cell stage. However, at laboratory temperatures (10-20°C) growth of the female worms was seen to be more rapid than in natural, colder, waters. In early spring division of the cells within the eggs commenced, so that by early summer the female worms were fully-developed. On 25 June the last worms were observed in the fins (Furuyama, 1934). Philometra kotlani Molnhr, 1969 Studied in the host fish, Aspius aspius, in Lake Balaton, the Rivers Tisza and Danube, Hungary by Molnhr (1969a, b). According to Molnhr (1969b) fully-developed or normally developing abdominal females were found in 12% of A . aspius. Abdominally located, developing, but slightly retarded females encapsulated in connective tissues were seen in 7.3% of A . aspius, and at the same site, dead encapsulated females (length 10-25 mm, April) were noted in 12.7% of this fish species. Males and females occurred under the swim bladder serosa of 24.4 % of the A . aspius, of which 9.7 % were living. Thus, full development occurred only in a minority of A . aspius (Molnhr, 1969b). A regular annual cycle of development was seen (Molnhr, 1969a). Mature females with their uteri filled with larvae were found only in May. CycZops species served as intermediate hosts. Aspius aspius were invaded during the summer, by eating smaller plankton-feeding fishes containing infected Cyclops. Migrations of the female worms from the swim bladder to the abdominal cavity were not seen; they probably occurred early autumn, or even earlier (Molnhr, 1969a). Young females were in the host abdominal cavity in early spring. At the beginning of April the eggs matured, so that

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by the end of that month young larvae were visible. The mature larvae hatched in utero in May. The male P. kotlani remained by the swim bladder throughout the year (Molnhr, 1969a). Philometra nodufosa Thomas, 1929 Dailey (1966, original not seen, quoted from Uhazy, 1977b) investigated this species in Catostomus commersoni from CoIorado, U S A . Seasonal variations were seen, with sustained high incidence and low intensity of infection. Philometra obturarzs (Prenant, 1886) This species was redescribed by Moravec (1978a). Izyurnova (1960), Malakhova (1961) and Rautskis (1970) have reported it on a seasonal basis from Esox lucius as part of faunistic studies (localities, see Table IV). Molnhr (1976) observed the biology of Phifometra obturans in Esox lucius from the Rivers Danube and Tisza, Hungary. Contrary to the distinct seasonal development seen in the other members of the genus, in this instance female nematodes with eggs and mature larvae were found in all seasons. Molnhr (1976) infected Cyclops strenuus and Acanthocyclops viridis easily, to obtain invasive third stage larvae at 21-24°C in 7 to 10 days. The infection was transmitted to E. lucius by way of Cyprinus carpio fed on infected copepods. One male P. obturans was subsequently recovered beneath the serosa of the swim bladder of one E, fucius, and in a second group of these fishes, one female was found in the swim bladder serosa and two under the host peritoneum (MolnBr, 1976). Moravec (1978b) demonstrated experimentally and described in detail the development of Philometra obturans. First stage larvae were shown to penetrate to and develop in the haemocoel of five species of cyclopoid copepods. At 20-22°C the first moult occurred at 5-7 days, the second in 9-11 days, to give the third stage larvae which was invasive to fishes. By contrast, at 10°C the first moult did not take place until 30-35 days post-infection. Moravec and Dykovd (1978) and Moravec (1979b) recovered gravid female worms in Esox lucius at the Mdcha Lake fish pond system, North Bohemia, Czechoslovakia, throughout the year, as had Molnar (1976, see above). The incidence of P. obturans was probably highest in the spring and beginning of summer and again October to December. Sub-gravid females, with eggs, were also present all year, but young females, without eggs, in May and August only. Perca jluviatilis and Scardinius erythrophthalmus served as reservoir hosts; the nematodes were present in the host vitreous bodies, 10.4% incidence, 1 to 7 larvae, irrespective of season. Moravec and Dykova (1978) considered the annual cycle to be: first stage larvae were released from gravid female P. obturans into the water year round. The time of survival of these larvae in the water and their rate of development in the copepod hosts was influenced by temperature (see Moravec, 1978b, above), low temperatures slowing or arresting development. Invasion of E. lucius was either direct via feeding on infected copepods, or indirect by way of the reservoir fish hosts. The invasive larvae penetrated from the gut to the abdominal cavity of the E. lucius. Copulation occurred and maturation commenced in the

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host body cavity ; the male P. obturans died post-copulation, the females migrated to the gill arteries to grow and produce the embryos. When gravid, the female nematodes pushed their anterior ends through the wall of a gill artery, to burst by the action of osmosis and release the larvae into the environment. An annual span of development of Philometra obturans was postulated by Moravec and Dykovh (1978), but without the well-marked generation pattern seen in other philometrids. The reservoir fish hosts were believed to minimize the development of clear-cut generations in P. obturans, whereas in the other Philometridae the copepod seasonal rhythms and absence of fish reservoir hosts maximized the evolution of generation patterns of occurrence. Philometra ovata (Zeder, 1803) An early seasonal reference to this species (as Zchthyonema ovatum) can be found in Srimek (1901), and further seasonal faunistic studies mentioning Philometra ovata include Dubinina (1949), Izyumova (1958, 1960), Mikailov (1963) and Komarova (1964) (for hosts and localities see Table IV). The life cycle was studied in detail by Molnhr (1966b) at Lake Balaton, Hungary, where the timing of the events in the cycle were highly regular and predictable, even to within days each year. A 100% incidence of adult female Philometra ovata 9 to 12 cm long containing larvae was found only during the last days of May and the first of June, and only in two years of age and older Abramis brama and Rutilus rutilus also infected by either Ligula intestinalis and/or Digramma interrupta. In ligulid-free A. brama more than one year old male and female P. ovata also had a 100% incidence during the whole year, but the number of worms was smaller than in ligulidinfected fishes (see later) and only the male nematodes attained the size of mature worms. Both the male and female P. ovata dwelt in the tissues of the swim bladder, so that the females did not migrate to the abdominal cavity of the host fishes, nor did they grow to 3 mm or more in length. Thus, in Lake Balaton Molnhr (1966b) found that P. ovata reached sexual maturity only in ligulid-infected fishes. The larvae of Philometra ovata were found to develop in various cyclopoid copepods by Molnhr (1966b). Vasil’kov (1976) has also obtained similar results. Thereafter in Lake Balaton Molnir (1966b) observed that the invasion of Abramis brama and Rutilus rutilus by juvenile P. ovata occurred in the second half of June. By July male and female worms were growing, but on the host swim-bladder only. In August the male P. ovata attained their ultimate size, so that copulation could occur, and from this month development of the female worms was different in ligulid-free as compared with ligulid-infected fishes. In hosts free of ligulids the female nematodes did not grow anymore, and remained, living, until June of the next year under the serosa covering the posterior sac of the swim bladder. However, in plerocercoid containing fishes some of the female worms continued to grow and started to migrate from the swim bladder to the abdominal cavity. Concurrently, egg primordia appeared in the uteri of these P. ovata. By September the females in the abdominal cavity were growing, to become

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light-red colour in October, but with no additional growth in November. Molnar (1966b) was unable to examine fishes from November until February. In March the female worms in the host abdominal cavities were red and active, with their uteri filled with roundish, unsegmented and thin-walled eggs. By April the eggs contained 8 to 32 blastomeres, at the beginning of May crescent-shaped larval primordia were visible in the eggs and by the latter half of May the uteri of the female worms were filled with great numbers of free first stage larvae. At the end of May and start of June the fully-matured female P . ovata left the body of the host fishes through the tissues surrounding the anus, to rupture in water and release the larvae which slowly sank. Molnir (1966b) observed that at the time of loss of the gravid worms there were male and female Philometra ovata present on the swim bladder of the host fishes in more or less equal numbers. Thereafter the number of male nematodes decreased. Fresh invasions occurred late June, and at this time some of the female nematodes retarded in their development during their first, previous, year in the host may continue development in this next annual cycle of development. It was mentioned earlier that in ligulid-infected Abramis brama and Rutilus rutilus Molnar (1966b) observed a 100% incidence of Philometra ovata. In these A . brama 20 to 300 fully-grown female worms occurred, about the same number of males, and usually some two or three retarded females, whereas in ligulid-infected R. rutilus only 1 to 14 adult female worms were found, and approximately the same number of males. In fishes free from ligulid plerocercoids, A . brama had a 100% incidence, with an intensity of infection of 2 to 30 undeveloped female and male P . ovata, whilst R. rutilus had a 67% incidence, with 1 to 10 undeveloped female or male worms. No infections at all occurred in any fishes less than one year old (Molnir, 1966b). Supplementary information was provided by Molnir (1969b): 2.5 % of R. rutilus not infested by Ligula plerocercoids contained fully developed female P. ovata; 67 % of ligulid-free R.rutilus from Lake Balaton and about 50 % of A . ballerus, A . brama and R. rutilus from Hungarian rivers were infected by retarded females and male nematodes. The synergistic effect of the ligulid plerocercoids in A . brama and R. rutilus (4.5 % occurrence in Lake Balaton) played an important role in the maintenance of the P . ovata in that habitat, with 50 to 300 worms per host. The precise manner of operation of the synergism was unknown, but Molnar (1969b) speculated that the plerocercoids might either improve the conditions for growth of, or reduce the host resistance to, the P. ovata. KaBiC et al. (1977) reported Philometra ovata from Gobio gobio lepidolaemus from Lake Skadar, Yugoslavia. It was common, 7.5 to 27 % of the fishes were infected from September through to January, with more than 500 larval nematodes in some fishes. In Lake D;Lbie, Poland Wierzbicka (1978) noted incidences of 50 to 100% in Abramis brama September 1970 to September 1971. Mature females were reported in the host body cavities in spring.

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According to Pojmanska et al. (1978) P. ovata showed a preference for thermally polluted lakes in the Konin region of Poland. Philometra rischta Skryabin, 1917 Reports of seasonal incidences of Philometra rischta include those of Izyumova (1959a), Mikailov (1963), Marits and Tomnatik (1971) and Wierzbicka (1978) (see Table IV for hosts and localities). The life cycle was examined in detail by Molnhr (1966b). In Hungary P. rischta was a parasite of numerous species of cyprinids, but especially Alburnus alburnus. At Lake Balaton and in the River Danube Molnhr (1966b) observed the fully grown females at the end of May, early June on the inner surface of the gill operculum. The males occurred during summer only, usually at most two individuals under the serosa of the posterior sac of the swim bladder, Molnhr (1969b) noted that the factors determining development of P. rischta were not easily ascertained as after fertilization the males and females left the swim bladder serosa. After September, except for one in the tail fin, no further males were seen (Molnhr, 1966b). Molnhr (1966b) reported that the invasion of the cyprinids of two or more years old by Philometra rischta occurred at the end of June. He first found the males on the swim bladder in early July, and by the middle of August the males and females had gone from that organ. Some young females were already on the inner surface of the gill operculum and other parts of the head by August. During the period to October the females continued to grow, but no fishes were examined from November to March. In April Molnhr (1966b) saw larger females, containing eggs which were not or just segmented. By early May segmentation had reached a morula condition, and between I0 to 20 May the larval primordia were visible. At the end of May the uteri were filled with active first stage larvae. The female P. rischta left the cyprinids at the end of May and early June, to burst and free the larvae. A 100 % invasion of young copepods was achieved experimentally, but only 1 in 3 of the adults. Species infected were Cyclops strenuus, Macrocyclops albidus and Acanthocyclops viridis (Molnhr, 1966b). In Abramis ballerus at Lake Dqbie, Poland, Wierzbicka (1978) observed mature females most frequently in the pectoral fins in spring, the next generation occurring at the same site by August and September. Philometra species undetermined Seasonal occurrences of unidentified philometrids are reported in Pearse (1924) (as Ichthyonema), HolI (1932), Malakhova (1961) and Kashkovski (1967) (hosts and localities see Table IV). Bier et al. (1974) provided details of the annual cycIe of development of Philometra species in Morone saxatilis in Chesapeake Bay, U.S.A. Young Philometra sp. were first seen in the host body cavities in July. Eggs were first observed late summer, cleavage commenced the following spring, to give the morula stage in April, active larvae in May and release of the fully-matured Philometra sp. from M. saxatilis through the body wall in June. M . saxatilis spawned in freshwaters; but remained in the brackish bay waters for the rest of the year.

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Philometroides species Vismanis (1978), in a note concerning the taxonomy of the genus in the U.S.S.R., listed Ph. cyprini, Ph. dogieli, Ph. lusiana and Ph. sanguinea. Nakajima (1976) compared the morphology of Ph. cyprini (Ishii, 1931) and Ph. lusiana (Vismanis, 1962) and considered that the latter was a synonym of the former. This view is held here. Philometroides carassii (Ishii, 1931) Philometroides carassii n. comb. was proposed for Filaria carassii Ishii, 1931 by Nakajima and Egusa (1977b). They redescribed the species and discussed the taxonomy, considering that Ph. carassii was not a synonym of Ph. sanguinea. Adult Ph. carassii were found in the caudal fin of Carassius auratus in early spring. The gravid females emerged slowly through the skin of the host fin, with their heads at the base or the posterior end of the caudal fin. The exposed parts of their bodies soon discoloured, straightened and hardened, but no larvae were released whilst their heads remained in the fin. When the worms were removed from the fishes and dropped into water they burst to release the first stage larvae after several minutes (Nakajima and Egusa, 1977~).The first stage larvae moved actively, extending and contracting. In water their survival times changed with temperature: four days at 2-5°C; seven days at 15°C; five days at 25°C; but only up to six hours at 37°C (Nakajima and Egusa, 1977d). The larvae were eaten actively by Cyclops strenuus, C. vicinus and Tropocyclops prasinus. Penetration to the haemocoel was completed within five hours. At 21-26°C most larvae were fully developed within one week, having reached an average length of 470 pm (Nakajima and Egusa, 1977e). Philometroides cyprini (Ishii, 1931) As noted above, Nakajima (1976) considered Ph. lusiana (Vismanis, 1962) a synonym of Ph. cyprini. Vasil‘kov (1964) studied this species (as Philometra lusii, see lvashkin el al., 1971 for historical review of taxonomy) in fish farms in the Kaliningrad, Minsk, Moscow and Ternopol districts of the U.S.S.R. Cyprinus carpio aged less than one year were not infected, otherwise incidences up to 88 % occurred through the year. Mature nematodes were found in spring, on the whole of the fish body surface, although concentrated in the gill region. Active larvae were released from the female worms in vitro. Vasil’kov (1968a) provided more details of the life cycle (as P. lusiana). Acanthocyclops vernalis, A . viridis, Cyclops strenuus, Eucyclops macruroides and Mesocyclops leuckarti were infected by first stage larvae. Two moults occurred in the copepods to provide invasive third stage larvae in 8 to 9 days. When fed to one-year-old C. carpio in 3 to 5 days the larvae were found in the intestine wall, by 14 to 17 days the third moult took place in the liver, the fourth stage larvae migrated to the swim bladder, where the fourth moult occurred on days 20 to 21 post-infection. About days 30 to 40 copulation occurred in the host swim bladder region, the female Ph. cyprini thereafter migrating towards the skin whereas the males remained in the swim.bladder. Vasil’kov (1968b) showed that from the end of August through to the spring the female worms were present in the scale pouches of C. carpio, progressively

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maturing, the larvae ultimately being shed in spring. Re-invasion of the C. carpio occurred in May-June in the north west of the U.S.S.R. Some further information can also be found in Vasil'kov (1976). In Latvia, U.S.S.R., Vismanis (1966, 1967) observed up to a 90% incidence of Philometroides cyprini (as Philometra lusiana) in Cyprinus carpio. The annual developmental cycle lasted one year as described above, invasion of fishes taking place in June. Vismanis (1970) provided additional data resulting from experimental studies in Latvia, including details of principal and auxiliary copepod intermediate hosts. In the Ukraine, U.S.S.R., Ivasik et al. (1967a, 1967b, 1971) provided more experimental information concerning development in the intermediate copepod hosts, in this instance Cyclops coronatus. Bauer et al. (1969) have summarized the life cycle, based chiefly on the work of Vismanis (1966, 1967), whilst Verbitskaya (1975) has described the distribution, diagnosis and prevention of infections of Ph. cyprini (as Ph. lusiana) in the U.S.S.R. Philometroides huronensis Uhazy, 1976 The biology of Philometroides huronensis has been considered in depth by Uhazy (1977a, b, c, 1978). The fish hosts, Catostornus commersoni, were collected from Lake Huron, Ontario, Canada. A summary of the annual life cycle is given in Fig. 8 (from Uhazy, 1977b). Fin

GRAVID FEMALES

Bareof f i n

I

peritoneum

1

SUEGRAVID

FEMALES

I I

FEMALES

I

around

I

MALES

4Ih S T A G E

s w i m bladder

1

CYCLOPS sp.

AQUATIC

I*'STAGE

Winter

Spring

3'dSlAGE

LARVAE

LARVAE

1

LARVAE

Summer

Fall

Winter

FIG.8. The annual life cycle of the nematode Philomefroides huronensis in the body of Curostomus commersoni (white suckers) from southern Lake Huron, Ontario, Canada. (From Uhazy (1977b), Fig. 13, p. 1440.)

Uhazy (1977a) obtained gravid worms from Catostomus commersoni in Lake Huron in May and June. The nematodes burst in well-aerated water, and the development of the larvae after invasion of Cyclops bicuspidatus thomasi at 10°C and C. vernalis at 20 and 22-23°C was followed. At 10°C the larvae reached the haemocoel in five hours, the first moult occurred 14 to 18

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days post-infection, and the second moult in 30 days. At the higher temperatures (20-23°C) the first moult took place in 6 to 9 days post-infection, the second in 14 to 20 days. Copepods with late second or third stage larvae were lethargic and easy to catch. The transmission to C. commersoni was also examined experimentally, at 3-4, 5-6 and 15-17°C. The details of these can be consulted in Uhazy (1977a). In Lake Huron differences in incidence and intensity of infection of Catostomus commersoni by Philometroides huronensis between years were not significant, nor did the intensity vary with host age. The developmental stages occurred in seasonal sequence. Fourth stage larvae were seen in the peritoneum around the swim bladder in July, September, November and December. Uninseminated and inseminated females occurred all year in the same tissues. Uninseminated females appeared in July (61 % of all females), to decline to 6 % by September. Concurrently, an increase in inseminated females was observed, and April to June the following year only inseminated females were recovered. Mature males were found all year in the peritoneum around the swim bladder. Immature males were not located. Subgravid females contained ova in various stages of development and were seen in the fins of the C . commersoni. They first appeared in the base of the fins in September, and had a maximum incidence in December. By April their numbers declined, concurrent with their becoming gravid. Gravid females occurred in the fins through April to June, but not in July or August. In May 42 % of the female worms contained first stage larvae, but 72 % in June. Uhazy (1977b) drew attention to the fact that release of the first stage larvae in Lake Huron was synchronous with the time of peak presence of Cyclops bicuspidatus thomasi, late May-June, thus dispersal of the parasite took place at the optimum time. Transmission back to the fishes was estimated to occur in June, as fourth stage larvae were common in the fishes by July, but probably transmission continued through the summer. Uhazy (1977b) was of the opinion that the growth and production of eggs by female Ph. huronensis was influenced by water temperatures, and was probably independent of host physiological changes associated with spawning. However the release of the nematode first stage larvae and transmission of the parasite did coincide with C. commersoni spawning (early May-early June) and copepods containing invasive larvae were present in Lake Huron when juvenile fishes were abundant. Seasonal lesions associated with the presence of Philometroides huronensis in Catostomus commersoni occurred during spring (April to June) and were described by Uhazy (1978). Philometroides sanguinea (Rudolphi, 1819) The life cycle of Philometroides sanguinea was described by Wierzbicki (1960) on the basis of observations made at Lakes Track and Skrwilno in Poland, together with some laboratory studies. The host fishes were Carassius curassius. In nature the full cycle required one year, but in the laboratory in warm conditions two cycles were completed in one year. In the lakes the female Philometroides sanguinea were present in the fishes

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all year, but their state of development changed according to season. The most juvenile stages occurred in the host body cavity May to October, those in May being very small. Young females were noted in the body cavity of fishes in September and October only if no male Ph. sanguinea were present, so that copulation could not take place. After fertilization the females left the body cavity of the host, to appear in the fins during autumn and winter in increasing numbers. Maturation occurred from February to May, during which time no increase in worm numbers was seen. At the end of May to June almost all the female nematodes left the fins of the C. carassius to rupture and release larvae into the lake waters. Males were present in the body cavity of the fishes throughout the year, although maximal in numbers during summer and autumn. In the laboratory Wierzbicki (1960) observed the female worms in the body cavity of the Carassius carassius for only three months. After six months, at water temperatures of 15 to 22"C, the female Philometroides sanguinea which had moved to the fins contained invasive first stage larvae, and the mature worms were more than 10 cm in length. Thus, in suitable warm water conditions two generations of adult worms could be achieved in 12 months. However, in Polish natural climatic circumstances growth and maturation of the Ph. sanguinea were inhibited during the winter by low water temperatures (Wierzbicki, 1960). The free-living first stage larvae survived for 9 days. Species of Cyclops, Mesocyclops and Macrocyclops were infected by Wierzbicki (1960). The Philometroides sanguinea in these copepods became invasive to fishes after 4 to 14 days post-infection, but could live in the intermediate hosts for up to two months. On invasion of the fishes during the summer the larvae went to the peritoneum near the kidney, swim bladder and gonads. Growth, differentiation and copulation took place in the area of the swim bladder, prior to the inseminated females moving to the fins of the fishes towards the autumn. Dead encapsulated males were seen during winter (Wierzbicki, 1960). Yashchuk (1970, 1971, 1974, 1975) studied the dynamics of infections of the copepod hosts of Philometroides sanguinea. At 10 to 12°C the first stage larvae remained living for 28 to 30 days, but at 18 to 19°C for only 15 to 17 days. In Acanthocyclops languidoides, A . nanus, Cyclops strenuus strenuus and Diaptomus gracilis development of the larvae to an invasive condition was slower at low temperatures: 26-27 days at 10°C; 19-21 days at 12-14°C; 15-16 days at 16°C; 10-11 days at 18-19°C; and 7-15 days post-infection at 20.5-21°C (Yashchuk 1970, 1971). One moult occurred in the fishes, postinvasion, and the female Ph. sanguinea required 11 to 12 months and the males 14 months to complete their development (Yashchuk, 1971). In the Vinnitsa region of the U.S.S.R. the incidence and intensity of infection of copepodswas highest in May and June, falling steadily until September when no infected copepods were found (Yashchuk, 1974). The invasive first stage larvae were released from the Carassius carassius from 25 May until 25 June. Young C. carassius fry hatched in May and June began to eat copepods at an age of 3 to 4 weeks, acquiring a 12 to 26% infection of Ph. sanguinea, but fry

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hatched later in June and July were less heavily infected (0-3%) (Yashchuk, 1975). Lyubina (1970) also recorded some information concerning seasonal occurrence of Philometroides sanguinea (see Table IV for hosts and locality). Vasil’kov (1976) also refers to seasonal variations of philometrid infections in fish farms of the U.S.S.R. Philonema agubernaculum Simon and Simon, 1936 Meyer (1960) reviewed the literature relevant to the genus Philonema. P. agubernaculum was common in Salmo salar and Salvelinus fontinalis during the summer of 1952 in Maine, U.S.A. Gravid female worms burst on contact with water to release many active larvae. Meyer (1960) suspected that the peak time of occurrence of the larvae coincided with the time of spawning of the host fishes, late September or early October. Four species of copepods were infected experimentally, but Meyer (1960) was unable to transmit the infections to fishes. Vik (1964) used a pepsin-hydrochloric acid digest technique on 450 Osmerus mordax from the Rangeley Lakes, Maine and recovered nine Philonema larvae. On feeding to hatchery S. fontinalis, at autopsy two months later two male and four female P . agubernaculum larvae were found. Vik (1964) suggested that the female P . agubernaculum expelled their larvae via puncture of the host fish skin, as tunnels were found in the flesh. However larvae might also be released with the spawn of S. salar, as Philonema larvae were found in this manner, even in April. According to Vik (1964) such a release mechanism could explain the presence of dead and empty female P. agubernaculum in the body cavity of S. salar. KO and Adams (1969) found that at 10°C the rate of larval development and the morphological stages of Philonema agubernaculum were similar to those of P . oncorhynchi. In Cyclops bicuspidatus the first moult occurred in 12 to 15 days, the second between 30 to 34 days post-infection. Bashirullah (1973) obtained an infection rate of 13.5% in Salmo gairdneri and at 8-10°C the fourth larval stage was achieved 58 days after infection. Chacko (1976), at the Palisades Reservoir, Idaho, U.S.A., obtained invasive third stage larvae in C . bicuspidatus at 18°C by day seven, and orally-invaded S. gairdneri contained sub-adults in the body cavity on day 128 and adults by 205 days post-infection. Philonema oncorhynchi Kuitunen-Ekbaum, 1933 Philonema oncorhynchi occurs in the body cavity of the host fishes. KuitunenEkbaum (1933a) observed that spawning Oncorhynchus nerka harboured female worms packed with larvae. The worms were expelled with the spawn. Platzer and Adams (1967) studied the life cycle experimentally. Gravid female worms were collected from spawning 0. nerka. The nematodes burst on contact with water to release the first stage larvae. At 8°C the larvae lived in water for 17 days. Cyclops bicuspidatus were infected at 8 and 12°C. Second stage larvae were obtained in 25 days at 8°C and 17 days at ITC, and third stage larvae in later samples in 70 days at 8°C and 17 days at 12°C. The invasive third stage larvae were transmitted to 0. nerka at 12”C, and recovered from the connective tissue and the tunica adventitia of the swim

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bladder and swim bladder duct 4 to 10 days after infection. Platzer and Adams (1967) observed that 0. nerka migrating from Cultus Lake, British Columbia, Canada, in April were all heavily infected with P. oncorhynchi. No larval development occurred for six months (fishes age 12-17 months), but rapid growth took place during the next 8-16 months (fishes age 18-34 months). Fourth stage larvae appeared during the 15th month, with subadult worms in the body cavity of the fishes by the 20th month of sampling. The long period of development was considered by Platzer and Adams (1967) to be an adaptation to low water temperatures and the maturation cycle of the host fishes. In Cultus Lake there was a four year cycle between hatching of 0. nerka eggs and the spawning of those fishes, and the life pattern of P. oncorhynchi appeared well-matched to that of its host. The female nematodes were fully-grown and gravid with active first stage larvae in utero when the host spawned. C. bicuspidatus were abundant in Cultus Lake throughout the year, and was a major food source for the 0. nerka. Invasion of the young fishes probably occurred mainly in January and February, and they migrated in April having accumulated large infections. Development of the P. oncorhynchi to subadult worms in the coelom was completed at the time the fishes were 32 months old and starting to return to freshwaters. Growth of the host and nematode gonads was concurrent, so that 0. nerka at the mouth of the Fraser River in September contained worms with eggs in the uteri, whilst at Cultus Lake in September morulae and some larvae were present. The November spawning fishes contained female P. oncorhynchi with the uteri packed with larvae, so that both host and parasite arrived at the spawning grounds in a gravid condition. Platzer and Adams (1967) put forward the hypothesis that the maturation of both host and parasite was dependent on the host hormones. The functional bursting of the gravid Philonema oncorhynchi was investigated by Lewis et al. (1974). Bursting occurred about one minute after the worms had passed into the spawning redds with the fish eggs. The nematodes from the male fishes were found to have seldom reached full maturity. Osmotic uptake was shown to be responsible for the production of the bursting pressure in P. oncorhynchi. KO and Adams (1969) provided further detail concerning the rate of larval development in CycZops bicuspidatus, which was directly proportional to temperature within the range 4 to 15"C, being almost doubled by a 5°C rise. In Cultus Lake, British Columbia, Oncorhynchus nerka spawned mid-November to mid-December. The fry were free-swimming May, and stayed in the lake for 1I+ months to 2 years, migrating to sea midApril, with a peak in the first week of May each year. In the lake water temperature conditions KO and Adams (1969) suggested that copepods invaded mid-November were probably invasive to fishes by mid-January, and might live until May. Accordingly, two year classes of 0. nerka were potentially exposed to invasion, those migrating seawards in April, and those remaining for a further 12 months to migrate the following year. Adams (1969) studied the route of the invasive third stage larvae of P. oncorhynchi through the tissues of 0. nerka. At 17 hours the larvae had penetrated the

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intestine near the pyloric caeca and migrated to the swim bladder through the coelom and to a lesser extent across the mesentery and associated tissues. Bashirullah (1973) also examined the development of P. oncorhynchi larvae in C. bicuspidatus and salmonid fishes. Development of the fourth stage larvae required 240 to 360 days at 8-10°C, a time similar to that seen by Platzer and Adams (1967, see above). Philonema sibirica (Bauer, 1946) Rumyantsev (1965) reported this species from Coregonus albula from Lake Kuito, Karelia, U.S.S.R., during the summers of 1962 and 1963. (d) Family Rhabdochonidae Rhabdochona acuminata (Molin, 1860) Mikailov (1963) noted this nematode in Barbus barbus and Varicorhinus capoeta in the Mingechaur Reservoir, Azerbaidan, U.S.S.R., during all the year. No details were given, other than that incidence and intensity of occurrence were almost the same all the time. Rhabdochona cascadilla Wigdor, 1918 Rhabdochona decaturensis (Gustafson, 1949) Spa11 and Summerfelt (1969) presented data for the two species combined from Ictalurus punctatus and Pomoxis annutaris sampled from Lake Carl Blackwell, Oklahoma, U.S.A. No significant seasonal changes were detected in either host. Voth et al. (1974) noted the presence of a Rhabdochona species, probably R. cascadilla, but they were uncertain, in Salmo trutta from the North Fork, South Platte River, Colorado, U.S.A. Infection levels were claimed to be inversely related to high water flow, so that highest incidences were found September to February and April at times of low water flow. Rhabdochona decaturensis was found in Aplodinotus grunniens and Ictalurus punctatus in Eagle Mountain Lake, Texas, U.S.A., by Gruninger et al. (1977). It was the only nematode in the habitat showing seasonality. Heaviest parasite loads were seen during the summer and autumn. Rhabdochona denudata (Dujardin, 1845) Zschokke (1884) observed this species from Lake LCman in Switzerland in Leuciscus cephalus (as Dispharagus denudatus) and Alburnus alburnus (as D.$lgormis, probably a synonym of Rhabdochona denudata according to Yamaguti, 1961). Gravid female nematodes were seen in March, June and July. Other rather brief comments or data concerning seasonal occurrences of R. denudata can be found in Mikailov (1963), Komarova (1964), Molnhr (1968b) and Kakacheva-Avramova (1973, 1977). Hosts and localities are given in Table IV. Alvarez Pellitero et al. (1978a) noted that in the Duero and Sil Basins, Le6n, Spain there was an annual cycle of incidence, intensity and maturation with one generation each year. Pereira Bueno (1978) gave rather more information concerning the Le6n observations. Incidence and intensity of occurrence in cyprinids, usually Leuciscus cephalus cabeda, occasionally Rutilus arcasi, was maximal autumn to winter, coinciding with the main recruitment period September to December, and minimal in summer.

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In late spring a new peak of occurrence might occur, following a decrease in March or April. Adult R. denudata, including egg-producing females, were present in the fishes through most months of the year, but were maximal in incidence in spring and early summer, although some persisted until autumn. The proportion of adults rose quickly in March to April. Thus, an annual cycle was apparent, the monthly changes in the age composition of the worms showing a seasonal maturation rhythm, at least in part influenced by temperature. Third stage larvae were found in Ephemeroptera nymphs in the gastroenteric contents of some of the cyprinids (Pereira Bueno, 1978). Shtein (1959a) studied the life cycle of Rhabdochona denudata in Lake Syam, Karelia, U.S.S.R. The larvae were found in 21.8% of Heptagenia species (intensity to 36) and 1.9 % of Ephemerella species (intensity to four). The highest infection of nymphs was found in exposed areas of the lake, with high oxygen levels and low water temperatures. Rhabdochona ergensi Moravec, 1968 Moravec (1 972) studied the development of Rhabdochona ergensi in the nymphs of the ephemeropteran Habroleptoides modesta at 13-1 5°C. The eggs contained the first stage larvae, which hatched in the intestine of the nymphs and penetrated through the intestine wall to the haemocoel. Here two moults occurred at days 13 and 16 post-infection, to become the invasive third stage larvae. Thereafter these invasive larvae were enclosed in thinwalled capsules in the tissues of the intermediate host, but growth continued and a further moult took place to give the fourth stage larvae. This latter moult could probably alternatively occur in the definitive fish host, Noemacheilus barbatulus. Moravec (1972) demonstrated that at 20°C on ingestion of the infected nymphs the R. ergensi established in the host intestine. The fourth moult in male nematodes occurred between days 6 to 20, in females between days 33 to 43. Adult male worms were seen from day 20 postinfection, females from day 33. At 18°C mature eggs were produced from day 43, at which time most female R. ergensi were mature. Rhabdochona gnedini Skryabin, 1946 Although details were not provided, Alvarez Pellitero et al. (1978a) and Pereira Bueno (1978) reported a well defined seasonal cycle of incidence, intensity and maturation in Barbus barbus bocagei in six rivers in Le6n Province, Spain. Pereira Bueno (1978) found maximal incidence and intensity of occurrence in autumn and winter, coinciding with the period of maximal recruitment November to March. Incidence was minimal during summer, but the proportion of adults in the population of Rhabdochona gnedini rose quickly March to April. The monthly changes in the age composition of the nematode population showed a seasonal maturation rhythm, at least in part influenced by water temperature. The intermediate hosts were ephemeropteran nymphs, early third stage larvae were found in some nymphs from the contents of the stomachs and intestines of the fishes. Rhabdochona hellichi (grimek, 1901) Kakacheva-Avramova (1973, 1977) noted this species in the Central'and

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Eastern Balkan Mountains and the River Danube, Bulgaria, in Barbus barbus and B. meridionalis petanyi in spring and summer. Rhabdochona phoxini Moravec, 1968 The biology of Rhabdochona phoxini has been studied in detail by Moravec (1976b, 1977a). The eggs contained fully formed first stage larvae at deposition from the adult worms. Ephemeropteran nymphs Habrophlebia fusca and H. lauta were infected at 13-15°C. Hatching occurred in the intestine, followed by penetration of the larvae to the body cavity where two moults took place, the first on days 12 to I6 and the second on days 20 to 36 postinfection. The resulting third stage larvae remained coiled within and became encapsulated by the host from 30 days after invasion onwards, although growth continued. The third moult, to give fourth stage larvae, could occur up to day 172 post-infection. Development within one nymph was not synchronous, commonly 2 to 15 larvae occurred per host. Infested imagines could fly normally. In Phoxinus phoxinus experimentally infected at 20"C, 5 of 20 fishes took the invasions. Third stage larvae moulted within three days, fourth by 22 to 38 days post-infection. Moravec (1976b) suggested that the female R.phoxini did not attain maturity and start to produce eggs until after 60 days post-infection. The seasonal dynamics in Phoxinus phoxinus were studied at the Rokytka Brook, Central Bohemia, Czechoslovakia, by Moravec (I 977a). As indicated above the intermediate hosts were ephemeropteran nymphs, in nature Ecdyonurus dispar, Ephemera danica, Habrophlebia fusca and ff. lauta. The invasive larvae occurred from April to October, encapsulated, with the highest incidence in E. danica, although the principal sources of invasion for the fishes were the other species which were commoner. The food of the P. phoxinus included nymphs and imagines of Ephemeroptera at all seasons. In December to February it was mainly larval and nymphal insects, whereas from March to November the food was more varied, including also aerial and terrestrial insects with plankton a frequent component in August. Incidence and intensity of occurrence of the Rhabdochona phoxini in the fishes were high all year, with both abiotic and biotic factors influencing the fluctuations. An annual maturation cycle was evident (see Fig. 9). The invasion of the fishes was most common during summer and autumn, less so winter and spring. Larvae predominated in the P,phoxinus in summer, immature adults towards autumn, and from January to April mainly adult R. phoxini were present. During oviposition from late-May to June or July the ripe females left the central region of the intestine and moved posteriorly. After egg-laying they passed from the host. It was quite exceptional to find females with mature eggs in months other than May to July (Moravec, 1977a). The periodicity of the life cycle of Rhabdochona phoxini was attributed by Moravec (1977a) to water temperature conditions in the habitat, the population dynamics of the intermediate hosts and the changes of occurrence of invasive larvae, and perhaps also of host resistance. In warmer .climatic conditions Moravec (1977a) postulated that two generations of nematodes per annum might occur and mature in the fishes.

153

HELMINTHS IN FRESHWATER FISHES

-,

01

10

100 80 -

6040 20

01 20 -

e2==

40 60

'

~

80

loo 60 40 20

0 20 40 60 40

20 0

20 40

60 40

20 0 20

40 1973

1974

FIG.9. Monthly changes in the samples of the nematode Rhabdochona phoxini in the intestine of Phuxinus phuxinus from the Rokytka Brook, Czechoslovakia in 1973 and 1974. The data are expressed as percentages of the total number of nematodes found per month: larvae unshaded, juvenile females or females with immature eggs hatched, males stippled, and females with mature eggs black. (From Moravec (1977a), Fig. 2, p. 103.)

Rhabdochona sulaki Saidov, 1953 Corder0 del Campillo and Alvarez Pellitero (1976a) noted Rhabdochona sulaki in Salmo trutta in the Province of L e h , Spain. 5'. trutta was probably an accidental host as R. sulaki is normally a parasite of cyprinids. One cycle of occurrence per annum was found, with maximal intensities of infection between March and August.

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Rhabdochona species undetermined Rhabdochona were mentioned by Kakacheva-Avramova (1977) from Abramis sapa and Zingel streber during spring and summer in the River Danube, Bulgaria. (e) Family Cystidicolidae Cystidicola farionis Fischer, 1798 The systematics of the species of Cystidicola were revised by KOand Anderson (1969) and Cysticola farionis and C. stigmatura (Leidy, 1886) were shown to be morphologically indistinguishable, but were tentatively regarded as distinct until more data on their biology were available. Subsequently Arthur et al. (1976) stated that there was no longer justification for retaining C. stigmatura as an independent species and considered it a synonym of C.farionis. Bauer and Nikol’skaya (1957) examined Coregonus lavaretus baeri natio Zadogae from Lake Ladoga, U.S.S.R., July to November and found incidences of Cystidicola farionis of 50 to 72%. Fishes three years of age and older were mainly infected owing to their feeding on the amphipod intermediate host Pontoporeia afinis (Bauer and Nikol’skaya, 1952, 1957). Other coregonid seasonal information has been presented by Leong (1975) and Valtonen and Valtonen (1978). In Cold Lake, Alberta, Canada, Leong (1975) (as C. stigmatura) found high incidences during all months of the year. Thus in four- and five-year-old Coregonus clupeaformis incidences varied from a minimum of 37.5% up to loo%, and average intensities from 3.3 to 23.2. Overall maximal values occurred during winter and minimal ones in late summer. The C.farionis matured in spring and summer. Larval C.farionis were found in the fishes all year, suggesting that the infected intermediate hosts, Gammarus lacustris, were available to and taken by the C. clupeaformis as food at all times. Although the total abundance reached maximum values during winter, the greatest numbers of adult nematodes occurred in spring and early summer, larvae developing in the G. lacustris through the warm water period of the summer to reinfect the fishes in the autumn. The winter peak abundance was suggested as attributable to a reduced resistance of the host fishes to infection owing to the low water temperatures. In Coregonus nasus in the Bothnian Bay, Baltic Sea, Valtonen and Valtonen (1978) found no seasonal rhythm for incidence of C.farionis, although again there was a trend for the worms to be at their lowest occurrence during August. Intensity was more even, both seasonally and between sampling sites. Awachie (1963a, 1973b) studied occurrence of Cystidicola farionis in the swim bladder of Saimo trutta from the Afon Terrig, Wales. A seasonal trend for the incidence and intensity of infection was indicated with greater numbers of nematodes occurring during the colder months of the year. Gammarus puiex was the intermediate host. Peak incidence (1805%) in the gammarids was seen in December and incidences were higher September (9-5%) to February (8.9 %), and lower March (7.5 %) to August (3.8 %), minimal July (3.3 %). Awachie (1973b) suggested that the invasion of the G . pulex occurred during autumn and winter, and overwintering juvenile gammarids

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carried the infection over to the summer. Rahim (1974) also found C.farionis in S. trutta from the River Alyn, Wales. In this instance maximal incidences were in March (24.1 %), April (2143%) and May (18.6%). At Llyn Tegid, Wales, Aderounmu (personal communication) found varied incidences each month through the year, from zero up to 24%, without any obvious regularity. Such absence of pattern could be attributed to changing populations and age groups of S. trutta at different times of the year, owing to the migratory habits of the host species. Cystidicoloides tenuissima (Zeder, 1800) The systematic status of this species has been discussed by Moravec (1967), Maggenti and Paxman (1971) and De and Moravec (1979). Wierzbicki (1962) noted the species (as Sterliadochona tenuissima) in salmonids in the Lupawa and Reda Rivers, Poland, in March and October. Awachie (1963a, 1973b) provided more data (as Metabronema truttae) concerning occurrence in the definitive host Salmo trutta in the Afon Terrig, Wales. Incidence was high (32.1 to 71.4%) and more or less even through the year; it was almost 100 % throughout at his sampling station 111. Intensity of occurrence was highest during June (average per infected fish 17.1), lowest in July (5*5), August (4.6) and November (4.2) and it varied between 6.4 and 9.5 in the other months. Unfortunately Awachie (1963a, 1973b) did not study the maturation of these worms. Choquette (1955) studied the life cycle of Cystidicoloides tenuissima (as Metabronema salvelini) in Canada, whilst Moravec (1971b, c) investigated it in Czechoslovakia. Moravec (1971b) fed eggs to the nymphs of Ephemera danica, Habrophlebia lauta and Habroleptoides modesta and obtained invasive third stage larvae in 24 to 38 days at 13 to 15°C. The larvae could survive in the ephemeropteran imagines. Salmo trutta and Thymallus thymallus were experimentally infected at 18°C. Adult male C. tenuissima were obtained 12 days post-infection. Female nematodes moulted for the last time 12 to 20 days post-infection, but eggs were not laid until much later, but the exact time was not established (Moravec, 1971b). De and Moravec (1979) carried out further experimental infections, in this instance using Salmo gairdneri, at 11 to 16°C. In experiment 1 a third moult occurred on days 10 and 19 (experiment 2, day 15, 3 day 5 ) , a male underwent a fourth moult on day 28 (experiment 2, female day 32), whilst on day 34 post-infection a female worm was still at the fourth larval stage. In Noemacheilus barbatulus development continued for only 19 days post-infection, to the fourth stage larval condition. Thus this fish was, according to De and Moravec (1979), a metaparatenic host, using the scheme of Odening (1976). The seasonal dynamics of Cystidicoloides tenuissima were investigated in depth in Salmo trutta from the River Bystfice, Czechoslovakia, by Moravec (1971~).Invasive larvae were found in nymphs of Ephemera sp. (14-28-75%, 1 4 per host) and Habroleptoides modesta (1-03-4.48%, 1-2 per host) from November until April. In the fishes during most months incidence was constantly high (loo%), the only marked decrease being in August (60%) and September (87.5%). Three marked decreases in mean intensity were

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observed, in August-September, concurrent with the decrease in incidence (above), November-December and the end of February-March. Two generations of C. tenuissima per annum were completed in the River Bystfice; females containing eggs capable of infecting intermediate hosts were present from May until July and again from September to October. The spring generation was the largest, the autumn one smaller. Moravec (1971~)suggested that the eggs containing first stage larvae passed into the river May to July, to fall into the detritus and be eaten by ephemeropteran nymphs. The invasive stage in these intermediate hosts was reached in about one month. During summer Ephemera sp. was the intermediate host, possibly also Habrophlebia lauta. After the gravid adult worms had left the S. trutta by the first half of July, only juvenile C. tenuissima remained. These developed quickly in the warm water temperatures of summer and the adult females produced eggs September-October. At this time large nymphs of Habroleptoides modesta were present, thus served as the main intermediate host. From the end of October the last autumn generation mature nematodes had gone, and once more only juveniles remained in the fishes; these developed slowly owing to the low water temperatures. In November-December the host stomachs contained juveniles, January-February young males and females without eggs, and in March-April, as water temperatures rose, females with immature eggs were seen. It was mentioned earlier that Moravec (1971~)found a fall in intensity of infection at three times of the year, August-September, November-December and the end of February-March. The November-December decrease was related to the loss of the autumn generation Cystidicoloides tenuissima and the spawning of the Salmo trutta in November to January, at which time these fishes reduced or suspended feeding. At the end of February-March the S. trutta again ceased feeding owing to spring floods in the river. In both instances on cessation of feeding the nematodes were gradually lost. Clearly, the pattern of fish feeding was very significant in the dynamics of the life cycle of C. tenuissima. Moravec (1917~)suggested that either one or two generations of Cystidicoloides tenuissima per annum would occur in a habitat, depending on the water temperatures in the particular habitat, the host feeding habits, availability of invasive larvae and changes in host physiological resistance. At low water temperatures the winter generation required eight months for development, whereas in high water temperatures the summer generation needed only two months. The fasting and seasonal changes in host diet seemed only to influence incidence and intensity of occurrence of the nematodes and not their rhythm of maturation. Subsequent to the study of Moravec (197Ic) Hare and Burt (1975) (as Sterliadochona tenuissima) reported two generations in juvenile Salmo salar at Trout Brook, New Brunswick, Canada with the majority of gravid worms in May, June and November, although some were present each' month. Alvarez Pellitero (1976b, 1976c), Corder0 del Campillo and Alvarez Pellitero (1976a) and Alvarez Pellitero et al. (1978a) observed a spring and autumn

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generation each year in Salmo trutta in rivers in Le6n Province, Spain. In warmer, lower reaches of the rivers the invasion of.the fishes was more rapid and earlier than in the cooler, upper reaches, thus demonstrating the direct influence of temperature on the maturation of the nematodes. In this area of Spain, Alvarez Pellitero (1976a) noted two generations per annum of the trematodes Crepidostomum farionis and C. metoecus in S. trutta. Other seasonal notes concerning Cystidicoloides tenuissima can be found in Rahim’(1974) (as Metabronema truttae) and Kakacheva-Avramova (1973). Hosts and habitats are given in Table IV. Spinitectus carolini Holl, 1928 Holl (1932) observed that the highest incidence of infection of Lepomis gibbosus at a settling pond, near Durham, North Carolina, U.S.A., was during winter, but the highest intensity of infection during spring. In Lepomis gulosus at the same habitat incidence was variable through the year, but intensity maximal in summer (August). At Lake Carl Blackwell, Oklahoma, U.S.A., Spa11 and Summerfelt (1969) found no significant differences in incidence between seasons in infections of Ictalurus punctatus. At Little River, Buncombe Creek and Lake Texoma, Oklahoma, U.S.A., McDaniel and Bailey (1974) observed Spinitectus carolini in Lepomis cyanellus, L. humilis, L. macrochirus and L. megalotis in considerable numbers. Occurrence was maximal in summer (July), but with a secondary peak during the winter. They suggested that a state of equilibrium between seasonal recruitment and the degeneration of established infections was soon reached. Cloutman (1975) at Lake Fort Smith, Arkansas, U.S.A., recorded the average number of S. carolini in each fish species through the year. Maximal intensities were in January in L. gulosus, in August in L. macrochirus and in April in Micropterus salmoides. In all these fishes some worms were present each month of the year, except M . salmoides in August. At several localities near San Marcos, Texas, U.S.A., Davis and Huffman (1978) found a significant seasonal distribution in Gambusia afinis with the mean date of occurrence as July, but they did not provide details. Spinitectusgordoni Cordero del Campillo and Alvarez Pellitero, 1976 Spinitectus gordoni was specific to Sulmo gairdneri and S. trutta in L e h , Spain, occurring in the oesophagus and stomach, with highest infections in September and October (Cordero del Campillo and Alvarez Pellitero, 1976b). Two generations of gravid adults were seen each year, one in March-April. During summer the larvae from this first infection matured with great rapidity so that by September-October there was a further generation of adults (Cordero del Campillo and Alvarez Pellitero, 1976a). Well defined patterns of incidence and intensity of occurrence were seen. S . gordoni was more frequent and abundant in male fishes (Alvarez Pellitero et a f . ,1978a). Spinitectus grucilis Ward and Magath, 1916 The life cycle of Spinitectus gracilis was demonstrated by Gustafson (1939) from material collected at Lake Decatur, Illinois, U.S.A., and experimentally in the laboratory. The nymphs of Ephemeroptera, species of Heplagena, Hexagena and Streptonoura, readily ingested the embryonated eggs. Twelve

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hours post-exposure numerous toothed first stage larvae were seen in the nymph intestines, with more advanced larvae in their body cavities by three days. Specific characteristics appeared within eight days. By the eleventh day the larvae were invasive to Lepomis cyanellus, so that after three days in the fishesyoung adults were recovered. Ivashkin (1 961) figured this life cycle. Spa11 and Summerfelt (1969) found no significant differences in incidence between seasons in Pomoxis annularis from Lake Carl Blackwell, Oklahoma, U.S.A. At Lake Opeongo, Ontario, Canada, Cannon (1973) did not observe any seasonality of occurrence in Percaflavescens, although the species did not show a similar sequence in both years. According to Cannon (1973) the lack of clear seasonality in Spinitectus gracilis suggested considerable overlap of recruitment and mortality and no clear relationship with consumption of the insect intermediate hosts. Spinitectus inermis (Zeder, 1800) Although no seasonal studies have been carried out on Spinitectus inermis owing to its rarity of occurrence in the stomach of Anguilla anguilla in Europe, Moravec (1979a) has suggested that it is possible that the infrequent occurrence was influenced partly by its seasonal dynamics. In the other European freshwater species, S. gordoni, the highest infections occurred in the definitive host Salmo gairdneri and S . trutta during September and October (Cordero del Campillo and Alvarez Pellitero, 1976b). The mature specimens collected by Moravec (1979a) as well as those found by Markowski (1933) were obtained in September. However, Cordero del Campillo and Alvarez Pellitero (1976a) and Alvarez Pellitero el al. (1978a) observed seasonal peaks of S. gordoni in both March-April and September-October. At Llyn Tegid, Wales, Chubb (1961) collected S. inermis in A . anguilla in May, at which time the females were packed with eggs. Thus, the hypothesis of Moravec (1979a) may still be correct, but with two generations per annuni rather than one.

(f)Undetermined spiruroid adults Holl(l932) at an artificial lake, Lakeview, North Carolina, U.S.A., found an undetermined intestinal spiruroid in Enneacanthus gloriosus which appeared to have two periodic cycles a year, with the highest percentage of incidence and average intensity of occurrence in spring and autumn. In the absence of details, it can be speculated that these peaks represented two generations of adults per annum. E. PHYLUM ACANTHOCEPHALA

The terminology for the larval stages of the Acanthocephala has been discussed by Van Cleave (1937, 1947) and more recently by Nicholas (1967). In the following pages the terms adopted are from Nicholas (1967). The egg is called a shelled acanthor. The acanthor is the invasive stage for the intermediate host. The acanthella stages are the growing phases in the intermediate host, and the cystacanth the final stage reached in the intermediate host which is then invasive to the definitive host.

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Critical studies of the seasonal distribution of Acanthocephala of fishes were initiated by Van Cleave (1916). He was able to relate seasonal patterns with the length of time required for larval development of the parasites, the migrations of the hosts to and from sources of invasion, changes in the feeding habits of the hosts through the year, and the extent of the periods of invasion and the longevity of the acanthocephalans in their definitive hosts. 1. Order Eoacanthocephala (a) Family Quadrigyridae Acanthogyrus (Acanthosentis) cholodkowskyi (Kostylew, 1928) Daniyarov (1975) observed this parasite (as Quadrigyrus cholodkowskyi) in Varicorhinus heratensis steindachneri in hot springs, water temperature 18-20°C all year, at Chilu-Chor Chashma, Tadzhikstan, U.S.S.R.Nonetheless, a 90% incidence was found during summer, compared with only a 30% incidence in autumn. It would be interesting to have more information concerning seasonal dynamics of parasites in conditions of year-round constant water temperatures. Acanthogyrus (Acanthosentis)indica (Tripathi, 1956) This species (as Acanthosentis indica) was reported by Pal (1963) in Hilsa ilisha, a migratory fish from the Hooghly Estuary, India, during a few months of the year only. Maximum intensity of occurrence was seen during November of both years of study and in March 1962. Pal (1963) was of the opinion that the complete absence of the parasite during the monsoon months of July and August was significant. A. indica was found mostly in the freshwater zone of the Estuary. Acanthogyrus (Acunthosentis) tilapiae (Baylis, 1947) Samples were collected from Tilapia zilli in lake and river habitats at Zaria, northern Nigeria, from January to December 1973 by Shotter (1974). In both environments the mean number of worms per fish was highest November to February, and lowest June and July, although the river fishes had lower infections overall than the lake T . zilli. The period of maximum infection coincided with the middle of the dry season, which extended from October to June, when the waters were coolest and shallowest. Shotter (1974) postulated that the increased densities of the intermediate hosts (not known) and the fishes could facilitate transmission of the larvae of the Acanthogyrus tilapiae host to host. Pallisentis (Farzandia)nagpurensis(Bhalerao, 1931) The life cycle was completed experimentally by George and Nadakal(l973) in Cyclops strenuus and Ophiocephalus striatus, although both hosts were also found naturally infected in ponds at Trivandrum, Kerala, India. The shelled acanthors remained viable for 35 to 50 days at room temperatures (not given). Hatching occurred on ingestion by the copepods, within 8 to 12 hours. The acanthors were in the haemocoel within 30 to 48 hours, and had reached the invasive cystacanth stage after 15 to 20 days. On ingestion by 0. striatus rapid growth of the juvenile acanthocephalans commenced so that after about

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50 days shelled acanthors were produced by the female worms. Encysted, cystacanths were found in the livers of Aplocheilus melastigma, Barbus sp. Macropodus cupanus and Ophiocephalus gachua which acted as transport hosts. Although George and Nadakal(l973) did not provide any field seasonal data, it would appear probable that some six or seven generations of worms could occur per annum, unless environmental constraints limited such a level of reproduction. (b), Family Neoechinorhynchidae Gracilisentisgracilisentis(Van Cleave, 1913) Gracilisentis gracilisentis is a parasite of the fish Dorosoma cepedianum. Van Cleave (1 9 13, 1916) (as Neoechinorhynchus gracilisentis) described the seasonal dynamics from the Illinois River, IIlinios, U.S.A. Presence of worms in the fishes was confined to autumn through spring, and practically every fish was infected. In October there was a high incidence of small, immature worms. By the latter part of November many acanthocephalans had reached sexual maturity, with hard-shelled embryos in the body cavity of the females. In April the incidence was less than half that of October, with decreased intensities of infection, and every parasite was sexually mature and of maximum size. Many D. cepedianum were examined June through August, but none were infected. Van Cleave (1916) deduced that invasion of fishes commenced early autumn probably September, and that oviposition occurred April, followed by the loss of the spent generation of worms from the definitive hosts. Jilek (1978a, b) recently confirmed the above pattern of occurrence at Crab Orchard Lake, Illinois, U.S.A. Immature adults appeared in Dorosoma cepedianum midSeptember, attained sexual maturity mid-December and the generation died and was totally lost in May. The intermediate host was unknown, but Jilek (1978b) speculated that it might be a species of Bosmina. Mortality of D. cepedianum during the winter months was attributed to the presence of heavy infections of Gracilisentis gracilisentis at this time (Jilek, 1979). Neoechinorhynchus cyzindratus (Van Cleave, I9 13) Early seasonal studies of Neoechinorhynchus cylindratus were made by Pearse (1924) and HoIl (1932) (hosts and localities see Table V), but as these were part of faunistic surveys details were not provided. Ward (1940) demonstrated the life cycle. In Columbian Park Lagoon, Lafayette, Indiana, U.S.A., 0.5 % of Cypria (Physacypria)globula were infected by N . cylindratus larvae. In July and August 1937 four of 800 ostracods were infected, in March-July 1938 none of 300, and in April 1939 one of 220. All Lepomispallidus examined contained cystacanths of N . cylindratus encysted in their livers. Ward (1940) fed Micropterus salmoides with L. pallidus containing encysted cystacanths on 25 September. On 1 October one M . salmoides contained 8 1 juvenile acanthocephalans. Another fish died on 27 November. It had been fed cystacanths twice, and contained 138 N . cylindratus. However, a M . salmoides.fed L. pallidus from November 1937 to March 1938contained parasites in the faeces at intervals, owing to the N . cylindratus failing to establish. In April sheIled

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acanthors appeared in the fish faeces, and a fish killed in June contained 40 acanthocephalans. Using shelled acanthors from gravid females Ward (1940) obtained an experimental invasion of 47 % of ostracods. She was of the opinion that three hosts were necessary in the life cycle, owing to M. salmoides being a piscivore, hence acquiring invasions from L. pallidus. At Little River and Buncombe Creek, Oklahoma, U.S.A., McDaniel and Bailey (1974) observed Neoechinorhynchuscylindratus adults and cystacanths in Lepomis cyanellus, L. humilis and L. megalotis. The adult acanthocephalans infected the greatest number of fishes during the winter, rapidly disappeared thereafter through to June, to have a secondary peak of occurrenceduring July. By September infection was increasing again, in a manner suggesting it would peak once more the following February. The N. cylindratus overwintered as adults, and were mature passing shelled acanthors in spring, prior to their death. Reinvasion commenced in the autumn. A very detailed analysis of the annual population changes of Neoechinorhynchus cylindratus in Micropterus salmoides at Par Pond, Savannah River Plant, Aiken, South Carolina, U.S.A., was made by Eure (1974, 1976b) and Eure and Esch (1974). Details are to be found in Eure (1976b). Water temperature and availability of infected intermediate hosts were most significant in explaining the seasonal periodicities. Six sampling stations were designated, five in unheated parts of the reservoir, the sixth in the heated area. Water temperatures were : unheated areas, mean minimum 10°C January, mean maximum 27°C July ; heated area, mean minimum above 20°C January, mean maximum 35°C September. Most of the M. salmoidesremained within the confines of a relatively narrow home range. Eure (1976b) found no significant variations between the unheated stations for the mean numbers of worms, but each of these differed significantly from the data collected in the heated area. A pronounced seasonal cycle of occurrence of Neoechinorhynchuscylindratus was seen in both unheated and heated areas of Par Pond (Eure, 1976b). Mean numbers were low during summer and autumn in both. Significant increases began October and November and the population density peaked in December. A decline in January was accounted for by sampling problems. A population rise was seen in February, but not up to the December peak level. The population density jn the heated area continued to increase in February and March, but declined in April and remained stable through May. In the unheated areas a constant population density was maintained February through April, with an abrupt decline in May. In summary, both heated and unheated areas showed similar seasonal cycling patterns, although with significant population density differences, with the highest density in the heated area. The recruitment and maturation pattern of the Neoechinorhynchus cylindratus in Micropterus salmoides also followed a seasonal sequence. Eure (1976b) recognized new invasions as worms of 2 mm in length or less, and female worms at three stages of development, with ovarian balls, with immature acanthors, and with shelled (mature) acanthors. Significant invasion of fishes began in August in the unheated area, but the population remained low. In the

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heated area recruitment commenced in September. During the autumn and winter intense recruitment continued, although it declined in December in both areas. In the unheated area invasion continued to February, but levelled off thereafter and fell sharply in both areas in spring. In January more than 80 % of the acanthocephalans were less than 2 mm long. In February most were less than 3 mm long; testes were present in the males, but the females contained no immature nor shelled acanthors. By spring more than 80% of the N. cylindratus were longer than 4 mm. The females were at all stages of development. The population densities declined during summer in both unheated and heated areas, and now almost all the female worms contained shelled acanthors, and most males had gone. By late summer all females were gravid and no males remained (Eure, 1976b). The life cycle of Neoechinorhynchus cylindratus at Par Pond involved seven species of ostracods as first intermediate and Lepomis macrochirus as second intermediate hosts. Eure (1976b) found that in the heated area the ostracods were commonest June to August, thereafter decreasing so that by November all species were scarce. In the unheated stations a similar pattern prevailed. All the ostracod species were infected by N . cylindratus larvae to some degree, but at different times of the year, which probably accounted for continued recruitment by the L . macrochirus through the year. The L . macrochirus spawned in spring, their fry hatched in summer and ostracods were an important item of their diet, although in the heated area few were consumed until August, but then many. The feeding of the host fishes, both intermediate and definitive, proved an important factor in explaining differences in population density of the Neoechinorhynchus cylindratus at the various seasons in the heated and unheated areas (Eure, 1976b). The pattern of recruitment was similar in both, but owing to more intensive feeding in the heated areas, a higher worm burden per host resulted. Some quite striking differences in prey between heated and unheated areas were seen, which were a function of the elevated water temperatures on the behaviour of the prey species. In the autumn Lepomis macrochirus formed 60 % of the food of Micropterus salrnoides in the heated area, but by comparison at this time only 15 % in the unheated areas. Hence the increased incidence and intensity of infection in the heated area. Water temperature also appeared to have an important role in the establishment of the Neoechinorhynchus cylindratus in the definitive host Micropterus salmoides. Recruitment occurred as temperatures fell, and not during the summer when water temperatures were high, so that mean worm burdens dropped during summer. Eure (1976b) considered that his observations supported the concept of a temperature dependent host rejection response similar to that postulated by Kennedy (1972b) for Pomphorhynchus laevis, and for some fish-cestoderelationships. Neoechinorhynchus rutili (Miiller, 1780) The following authors have contributed some seasonal data concerning Neoechinorhynchus rutili as part of faunal surveys, but these are not considered in detail here: Zschokke (1884), Dyk (1957), Izyumova (1958, 1960),

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Komarova (1964), Thomas (1964), Davies (1967,) Dartnall (1972), gitiian (1973) and Moravec (1979b). Hosts and localities are presented in TabIe V. It is important to stress that although acanthocephalans frequently appear to have a wide host specificity if judged by occurrence only, in fact in many of these fishes the worms apparently cannot mature (Chubb, 1968). In the instance of Neoechinorhynchusrutili Chappell(l969a) found infections in Gasterosteus aculeatusduringeach month he sampled, but he stressed that all the worms were immature. Moravec (1979b), in Esox lucius, and Valtonen (1979) in Coregonus nusus also reported the same situation. Clearly at least some species of fishes do not present either the necessary physiological conditions or stimuli for the successful reproduction of the parasites, even though their feeding habits render them liable to invasion. Steinstrasser (1936) followed the maturation cycle of Neoechinorhynchus rutili in Salmo gairdneri in stock ponds at a trout farm in Germany. On 16 November the first small worms were recovered. By the following 15 February the first ripe shelled acanthors were noted, and by 28 February all the females were fully ripe, and no males were seen. Steinstrasser (1936) suggested that invasion of the S. gairdneri commenced about the middle of November, and that the female worms required some three months to mature. Merritt and Pratt (1964) studied the life cycle by observing natural infections in Suttle Lake, Oregon, U.S.A., and investigating laboratory infections. The acanthors were released from their shell membranes in the intestine of the ostracod Cypria turneri. At 15°C development in the haemocoel required 48 to 57 days to give the cystacanth stage. These cystacanths were directly invasive to the salmonid definitive hosts, hence differing from N. cylindratus in this respect. In Suttle Lake almost all the salmonids (see Table V) were infected. Intensity varied somewhat with season, increasing gradually to an autumn peak. Walkey (1967) made a detailed study of the seasonal occurrence of Neoechinorhynchus rutili in Gasterosteus aculeatus at a pond at Monkton, County Durham, England. It is pertinent to point out that Walkey (1967) recovered gravid N. rutili from this host fish, whereas, as indicated above, Chappell (1969a) never did. Walkey (1967) recognized three stages of development of the parasite: immature, less than 2 mm long; mature, 2-3.5 mm long; and gravid, more than 3-5 mm in length, most with shelled acanthors. Continuous invasion of fishes was seen throughout the year. Two ostracods were determined to be the intermediate hosts, Cypriu ophthalmica and Candona cundida, and they formed a food item for the fishes every month of the year, although overall with seasonal peaks during summer and autumn, with minimal values in the spring. Walkey (1967) observed gravid worms over quite extensive periods each year, so much so that he suggested it might be assumed therefore that shelled acanthor production occurred throughout much of the year. Incidence of the worms exhibited no obvious seasonal cycle, but there was a marked tendency for an increase of infection through the life of the host, so that there was a 10% incidence in the smallest fishes up to 80% in the largest. Concurrently, intensity rose too. A marked cycle of maturation through the year

c

m

TABLEV

P

Studies on seasonal occurrence of acanthocephalanslisted in the climate zones of the World (see map Fig. 1, Chubb, 1977). The species are in alphabetical order. ~

Climate zones

Acanthocephalan species

Host species

Locality

References

1. Tropical

la. RAINY (humid climate) 1b. SAVANNA (humid climate)

no seasonal studies

tropical forest tropical grassland

Acanthogyrus Hilsa ilisha (Acanthsentis) indica Acanthogyrus Tilupia zilli (Acanthosentis) tilapiue Neoechinorhynchustopseyi Polynemus heptadactylus

Hooghly Estuary, Pa1 (1963) India Lake, Ahmadu Bello Shotter (1974) University and River Galma, Zaria, Nigeria Calcutta Market, India Podder (1937)

lc. HIGHLAND (humid climate)

no seasonal studies

tropical highland

1d. SEMI-DESERT (dry climate) le. DESERT (dry climate)

no seasonal studies

hot semi-desert

no seasonal studies

hot desert

Salmo trutta

scrub, woodland, olive River Tirino, L'Aquila, Paggi et al. (1978) Italy

2. Sub-tropical 2a. MEDITERRANEAN Dentitruncus truttae

Echinorhynchus truttae

Lake Skadar, Yugoslavia Lake Skadar, Yugoslavia Gobio gobio lepidolaemus Lake Skadar, Yugoslavia deciduous forest Par Pond, Savannah Micropterus salmoides River Plant, Aiken, South Carolina, USA Little River and Lepomis cyanellus Buncombe Creek, Lepomis humilis Oklahoma, USA Lepomis megalotis

Anguilla anguilla Cyprinus carpio Pomphorhynchus bosniacus Leuciscus cephalus albus

2b. HUMID

Neoechinorhynchus cylindratus

3. Mid-latitude 3ai. HUMID WARM SUMMERS Acanthocephalus anguillae Abramis ballerus Abramis brama Esox lucius Leuciscus idus Lota Iota Leuciscus cephalus Blicca bjoerkna Leuciscus idus Rutilus rutilus 18 species of fishes Acanthocephalus jacksoni

Carassius auratuf Cyprinus carpio

Kaiic (1970) KaiiC (1970) Kaiic et al. (1977) Eure (1974,1976b); Eure and Esch (1974) McDaniel and Bailey (1974)

temperate grassland, mixed forest River Dnepr, Ukraine, Andryuk (1974a) USSR

Central and Eastern Kakacheva-Avramova Balkan Mountains, (1973) Bulgaria River Danube, Bulgaria Kakacheva-Avramova (1977) near Warsaw, Poland Ruszkowski (1926) Srhmek (1901) PodEbrady, Czechoslovakia Jackson Cutoff, Muzzall and Rabalais Ohio, USA (1975a)

P-

a?

TABLEV (continued)

Climate zones

Acanthocephalan species

Host species

Locality

References

3ai. (continued)

Acanthocephalus lucii

Lepomis cyanellus Lepomis macrochirus Semotilus atromuculatus Cyprinus carpio

Fish farms, Western Ivasik (1953) Ukraine, USSR River Danube, Bulgaria Kakacheva-Avramova (1 977)

Abramis sapa Benthophylus stellatus Gymnocephalus schraetser Leuciscus cephalus Lota lota Proteorhinus marmoratus Rutilus rutilus Abramis brama Dubossary Reservoir, Moldavia, USSR Lake Balaton, Hungary Gymnocephalus cernua Esox lucius Macha Lake fish pond system, North Bohemia, Czechoslovakia Perca fluviatilis River Svratka, Czechoslovakia Lake Leman (Geneva), Cyprinus carpio Esox lucius Switzerland Lota lota Perca fluviatilis

Marits and Tomnatik (1971) Molnar (1966a) Moravec (1979b)

Vojtkova (1959)

Acanthocephalus tenuirostris Echinorhynchus salmonis Gracilisentis gracilisentis

Barbus meridionulis petenyi Leuciscus cephalus Abramis brama Leuciscus idus Dorosoma cepedianum Dorosoma cepedianum

Fessisentis friedi

Catostomus commersoni

Leptorhynchoides plagicephalus Neoechinorhynchus cylindratus

Acipenser ruthenus

Neoechinorhynchus rutili

Lepomis gulosus Lepomis macrochirus Micropterus salmoides Enneachanthus gloriosus Leuciscus idus orfus Salmo trutta Salvelinus fontinalis Esox lucius

Cyprinus carpio Phoxinus phoxinus

Central and Eastern Kakacheva-Avramova Balkan Mountains, (1973) Bulgaria River Danube, Bulgaria Kakacheva-Avramova (1977) Jilek (1978a, b, 1979) Crab Orchard Lake, Illinois, USA Illinois River, Illinois, Van Cleave (1913, 1916) USA Bushkill Creek, Fried et al. (1964) Pennsylvania, USA Kakacheva-Avramova River Danube, (1977) Bulgaria Cloutman (1975) Lake Fort Smith, Arkansas, USA Holl (1932) Artificial lake, Lakeview, North Carolina, USA Poprad and Strbskk Dyk (1957) lakes, Czechoslovakia Macha Lake fish pond Moravec (1979b) system, North Bohemia, Czechoslovakia Fish ponds, South TesarCik (1970, 1972) Bohemia, Czechoslovakia Dobsina Dam, Slovakia, %than (1973) Czechoslovakia

c

TABLEV (continued) ~

Climate zones

~~

~

Acanthocephalan species

~

Host species

Locality

References

3ai. (continued) Rutilus rutilus

Paulisentis missouriensis

Semotilus atromaculatus

Pomphorhynchus bosniacus Vimba vimba tenella Pomphorhynchus laevis

Barbus barbus Gobio gobio Leuciscus cephalus Phoxinus phoxinus Salmo trutta 37 species of fishes Vimba vimba vimba natio carinata Phoxinus phoxinus 7 species of fishes

Tanaorhamphus .longirostris

Dorosoma cepedianum Dorosoma cepedianum

3aii. HUMID COOL SUMMERS

Lake LCman (Geneva), Switzerland Five creeks, Johnson County, Missouri, USA Central and Eastern Balkan Mountains, Bulgaria Central and Eastern Balkan Mountains, Bulgaria

Zschokke (1884)

River Danube, Bulgaria Dubossary Reservoir, Moldavia, USSR Bach M, Hungary Lake LCman (Geneva), Switzerland Crab Orchard Lake, Illinois, USA Illinois River, Illinois USA temperate grassland, mixed forest

Kakacheva-Avramova (1977) Marits and Vladimirov (1969) Molnkr (1968b) Zschokke (1884)

Keppner (1974) Kakacheva-Avramova (1973) Kakacheva-Avramova (1973)

Jilek (1978b) Van Cleave (1913, 1916)

Acanthocephalus anguillae Abramis brama Esox lucius Abramis brama Perca fluviatilis Gymnocephalus cernua Blicca bjoerkna Esox lucius Abramis brama Acanthocephalus lucii

Abramis brama Blicca bjoerkna Esox lucius Leuciscus idus Lota Iota Perca fluviatilis Rutilus rutilus Gasterosteus aculeatus Lucioperca lucioperca Perca JIuviatilis Gymnocephalus cernua Esox Iucius

Gymnocephalus acerina Gymnocephalus cernua Lucioperca lucioperca Perca fluviatilis Esox lucius

River Volga, USSR

Bogdanova (1958)

Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR Kuybyshev Reservoir, USSR River Dnepr, USSR

Izyumova (1958)

River Chernaya, near River Neva, USSR Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR Rybinsk Reservoir, USSR River Dnepr, USSR

Banina and Isakov (1972) Izyumova (1958)

River Oka, USSR

Markova (1958)

Izyumova (1959a) Izyumova (1960) Lyubarskaya (1970) Andryuk (1974a)

Izyumova (1959a) Izyumova (1960) Komarova (1950)

c

4

TABLEV (continued)

Climate zones

Acanthocephalan species

Host species

0

Locality

References

3aii. (continued) Perca Jluviatilis Esox lucius Perca Jluviatilis Acanthocephalusparksidei Catostomus commersoni Lepomis cyanellus Semotilus atromaculatus Catostomus commersoni Cottus cognatus and 10 others Echinorhynchus salmonis Oncorhynchus tshawytscha 14 species but mostly Osmerus mordax Coregonus lavaretus baeri natio ladogae Perca Jlavescens Leptorhynchoides thecatus Perca flavescens Ambloplites rupestris Lepomis macrochirus Lepomis macrochirus x Lepomis gibbosus

Lake Dusia, Lithuania, USSR Lake Dusia, Lithuania, USSR Lakes Galstas, Obelija and Shlavantas, Lithuania, USSR Pike River, Wisconsin, USA

Rautskis (1970a)

Lake Michigan, USA

Amin (1977)

Lake Michigan, USA Lake Michigan, USA

Rautskis (1970b) Rautskis (1977) Amin (1 975)

Amin (1978a) Amin and Burrows (1977) Lake Ladoga, USSR Bauer and Nikol’skaya (1957) Bay of Quinte, Lake Tedla and Fernando Ontario, Canada (1969, 1970) Lake Opeongo, Ontario, Cannon (1973) Canada Lake Mendota, De Giusti (1949) Wisconsin, USA Gull Lake, Michigan, Esch et al. (1976) USA

Perca flavescens Neoechinorhynchus cylindratus Neoechinorhynchus rutili

Perca flavescens Abramis brama

Abramis ballerus Esox lucius Pomphorhynchus bulbocolli Lepomis macrochirus Lepomis macrochirus x Lepomis gibbosus Pomphorhynchus laevis Abramis brama 3aiii. EAST COAST"

Echinorhynchus lateralis

Neoechinorhynchus cylindratus Neoechinorhynchus saginatus Pomphorhynchus bulbocolli

Coregonus clupeaformis Salmo gairdneri Salmo salar (landlocked) Salmo trutta Salvelinusfontinalis Perca flavescens Semotilus corporalis Catostomus commersoni

3b. MAR N E VEST COAST

Acanthocephalus anguillae Leuciscus idus Rutilus rutilus

Yahara River lakes, Wisconsin, USA Yahara River lakes, Wisconsin, USA Rybinsk Reservoir, USSR Rybinsk Reservoir USSR Gull Lake, Michigan, USA

P a r s e (1924) P a r s e (1924) Izyumova (1958) Izyumova (1960) Esch et al. (1976)

River Volga, USSR Bogdanova (1958) temperate grassland, mixed forest Insular Newfoundland, Sandeman and Pippy Canada (1967)

Lake Oneida, New York, USA Oyster River, New Hampshire, USA Pushaw Lake, Maine, USA temperate grasslands, deciduous forest Lake 0yeren, Norway

Noble (1970) Muzzall and Bullock (1978) Lawrence (1970)

Oien (1976, 1979)

The abstract of Bullock (196%) refers to species in this climate zone, but owing to the fact that only general information was presented in the abstract the species are not listed individually.

I-

=!

TABLEV (continued) ~~~~

Climate zones

Acanthocephalan species

~~~

~~

Host species

~

Locality

References

3b. (continued) Acanthocephalus clavula

Acanthocephalus lucii

Perca fluviatilis

Llyn Tegid, Wales

Perca fluviatilis Anguilla anguilla Esox lucius Rutilus rutilus Thymallus thymallus Gasterosteus aculeatus

Llyn Tegid, Wales Llyn Tegid, Wales

Anguilla anguilla Coregonus lavaretus Cottus gobio Rutilus rutilus Perca fluviatilis Perca fluviatilis Perca fluviatilis Perca fluviatilis Anguilla anguilla Esox lucius Perca fluviatilis

Andrews (1977); Andrews and Rojanapaibul (1976) Brattey (1982) Chubb (1963b; 1964a)

Priddy Pool, Somerset, Pennycuick (1971b) England Llyn Tegid, Wales Rojanapaibul (1977); Andrews and Rojanapaibul (1976) Lake Reryetjern, Andersen (1978) Norway Princes Park Lake, Andrews (1977) Liverpool, England River Glomma, Halvorsen (1972) Norway Serpentine, London, Lee (1977) England Shropshire Union Canal, Mishra (1966) Cheshire, England

Rutilus rutilus Perca Jluviatilis

Echinorhynchus truttae

Esox lucius Perca Jluviatilis Rutilus rutilus Perca JEuviatilis Salmo trutta

Priemer (1979)

Lake Dargin, Poland Afon Terrig, Wales

Wienbicki (1970, 1971) Awachie (1963a, b, 1965, 1966b, 1972a) Awachie (1963a, 1973a) Campbell (1974) Corder0 del Campillo and Alvarez Pellitero (1976a) Davies (1967)

Cottus gobio Salmo trutta Salmo trutta

Afon Terrig, Wales Loch Leven, Scotland L.e6n, Spain

Thymallus thymallus

River Lugg, Herefordshire, England River Alyn, Wales Dunalastair Reservoir, Scotland River, Bergischenland, Germany Frongoch Lake, Wales Pond, Baildon Moor, Yorkshire, England Hadleigh Marsh, England River Lugg, Herefordshire, England

Salmo trutta Salmo trutta Salmo trutta Neoechinorhynchus rutili

Lakes, outskirts of Berlin, Germany Rostherne Mere, Cheshire, England

Phoxinus phoxinus Gasterosteus aculeatus Gasterosteus aculeatus Esox lucius Leuciscus cephalus Leuciscus leuciscus Rutilus rutilus Thymallus thymallus

Rizvi (1964, 1968)

Rahim (1974) Robertson (1953) Steinstrasser (1936) Bibby (1972) Chappell (1969a) Dartnall (1972) Davies (1967)

c

4 P

TABLEV (continued) Climate zones

Acanthocephalan species

Host species

Locality

References

3b. (continued) Rutilus rutilus Salmo clarki Salmo gairdneri Leuciscus idus Rutilus rutilus Salmo trutta Salmo gairdneri Salmo trutta Salmo trutta Gasterosteus aculeatus Pomphorhynchus laevis

Leuciscus cephalus Leuciscus leuciscus Thymallus thymallus Cottus gobio Thymallus thymallus

3c. SEMI-DESERT Acanthocephalus lucii Echinorhynchus truttae

Esox lucius Lucioperca lucioperca Pelecus cultratus Salmo trutta

River Glomma, Norway Halvorsen (1972) Silver Lake, Washington Mamer (1978) State, USA Lake 0yeren, Norway 0ien (1976, 1979) Dunalastair Reservoir, Scotland Trout farm, Germany

Robertson (1953) Steinstrasser (1936)

River Teify, Wales Thomas (1964) Pond, Monkton, County Walkey (1967) Durham, England Hine (1970); Hine and River Avon, Hampshire, England Kennedy (1974a, b); Kennedy (1972c) River Avon, Rumpus (1975) Hampshire, England Van Maren (1979a) River Ain, France prairie and steppe Dnepr Delta, USSR Komarova (1964) Lebn, Spain

Corder0 del Campillo and Alvarez Pellitero (1976a)

Neoechinorhynchus rutili Pomphorhynchus laevis 3d. DESERT 3e. SUB-POLAR Acanthocephalus lucii

Echinorhynchus salmonis

Neoechinorhynchus rutili

Blicca bjoerkna Esox lucius Rutilus rutilus heckeli Vimba vimba vimba natio carinata no seasonal studies Esox lucius Lota lota Perca fluviatilis Lota lota Coregonus artedii Coregonus clupeaformis Oncorhynchus kisutch and 7 others Coregonus nasus

Esox lucius Lota lota Perca fluviatilis Rutilus rutilus Coregonus nasus

Neoechinorhynchus tumidus Coregonids 4. Polar 4a. POLAR 4b. ICE-CAP§

no seasonal studies no suitable habitats for freshwater acanthocephalans

Dnepr Delta, USSR

Kornarova (1964)

Dnepr Delta, USSR

Komarova (1964)

cool desert coniferous forest Lake Konche, Karelia, Malakhova (1961) USSR Lake Kuito, Karelia, USSR Cold Lake, Alberta, Canada

Shul’man et al. (1974) Leong (1975); Holmes et al. (1977)

North East Bay of Valtonen (1981a, b) Bothnia, Finland Lake Konche, Karelia, Malakhova (1961) USSR North East Bay of Bothnia, Finland Lower reaches, River Yenisei, USSR tundra icefields and glaciers

Valtonen (1979) Bauer (1959a)

TABLEV (continued) Climate zones

Acanthocephalan species

5. Mountain Acanthogyrus (Acanthosentis) cholodkowskyi Echinorhynchus baeri Neoechinorhynchus rutili

Pomphorhynchus laevis

Host species

Locality

References

heath, rocks and scree Springs, Chilu-Chor Daniyarov (1 975) Chasma, Tadzhikstan, USSR Coregonus lavaretus ludoga Lake Sevan, Armenia, Vartanyan and Coregonus Iavaretus USSR Mkrtchyan (1 972) maraenoides Prosopium transmontanus Suttle Lake, Cascade Merritt and Pratt Oncorhynchus nerka nerka Range, Oregon, USA (1964) Salmo gairdneri Salmo trutta Coregonus lavaretus ludoga Lake Sevan, Armenia, Vartanyan and Coregonus lavaretus USSR Mkrtchyan (1972) maraenoides Varicorhinus heratensis steindachneri

HELMINTHS I N FRESHWATER FISHES

177

was seen, with a high percentage of immature N . rutili during summer, autumn and winter. From February to May the population of immature forms dropped to its minimum, corresponding to an increase in the presence of mature worms. Gravid N . rutili were recovered in greatest numbers (10-30 % of population) during spring and early summer, declining through to a minimum value in winter. In summary, Walkey (1967) suggested that the simplest interpretation of the various relationships described at Monkton was that while temperature variations initiated the seasonal maturation cycle, the overall size of the parasite population was largely determined by the availability of infected intermediate hosts. Irregularities in the seasonal occurrence of ostracods lead to irregular fluctuations in the N. rutili population, and such changes in population size masked any tendency towards a seasonal incidence cycle. TesarEik (1970,1972) examined the infection of Cyprinus carpi0 in fish ponds in South Bohemia, Czechoslovakia. Here invasion commenced in spring, with the young acanthocephalans localized in the first quarter of the intestine, and later in the summer the adult worms were found along the whole length of the intestine, with the majority in the centre region (TesarEik, 1972). Shelled acanthor production commenced on 4 March and continued through to 29 July (TesarCik, 1970). In other host fishes there was some variation in times of maximal incidence through the year. 0ien (1979) in Norway found invasion of Leuciscus idus to commence in September, and increase in winter and spring. Malakhova (1961) in Karelia, U.S.S.R., found maximal incidences and intensities in Lota Iota during winter and spring, but in RutiIus rutilus in spring and summer. Bibby (1972) in Phoxinus phoxinus at Frongoch Lake, Wales, observed maximal occurrence May through to October. In salmonids Mamer (1978) in Washington State, U.S.A., observed 100 % incidences in both Salmo clarki and S. gairdneri April 1975 to March 1976, but highest mean intensities were February and January respectively. In Scotland Robertson (1953) noted maximal infestations of Salmo trutta to be in May and June. No doubt these variations of timing depended on the particular feeding habits of the host fishes and the seasonal cycling of the relevant intermediate hosts in each locality. Neoechinorhynchus saginatus Van Cleave and Bangham, 1949 A brief mention of Neoechinorhynchus saginatus in a seasonal context was made by Bullock (1962a) but a detailed analysis was provided by Muzzall and Bullock (1978). In Oyster River, New Hampshire, U.S.A.,the definitive host was Semotilus corporalis, and gravid worms were found only in this fish species, and not in four others in which worms were recovered. No clear pattern of seasonal incidence or mean intensity of occurrence was observed. A year round continuous source of invasion of the fishes was noted, as subadults were present in all months sampled. Gravid females were also collected during all months except July and September, 1975, July 1976 and September 1977. Ice was present on the river from the second week in December to the first part of March. The water temperature range was 0 to 30°C. According to Muzzall and Bullock (1978) temperature did not appear to be a factor involved

178

J A M E S C. C H U B B

in the maturation of the worms, although no doubt the rate of maturation varied with temperature. Host hormones also appeared to have no influence on N . saginatus maturation, as gravid worms were seen in small sexually immature S . corporalis. The life cycle of Neoechinorhynchus saginatus was investigated by Uglem and Larson (1969). Natural infections of cystacanths were found in Cypridopsis vidua. At 25°C the shelled acanthors hatched I hour post-feeding to this ostracod. Invasive cystacanths were obtained in 16 days. After 46 days from establishment in the fish Semotilus atromaculatus Uglem and Larson (1969) saw that the N . saginatus were still small. Neoechinorhynchus topseyi Podder, 1937 Podder (1937) reported that the host fish, Polynemus heptadactylus, was sold at Calcutta Market, India, from February to August. Infection by Neoechinorhynchus topseyi was marked during May to July. Neoechinorhynchus tumidus Van Cleave and Bangham, I949 Bauer (1959a) reported this species in the intestines of coregonids in the lower reaches of the River Yenisei, U.S.S.R., all through the northern summer. At the end of June to early July (early summer) small, young, sexually immature parasites were found. Towards September (autumn) large Neoechinorhynchus tumidus were recovered, with the body cavity of the females filled with shelled acanthors. Neoechinorhynchus species undetermined Bullock (1962a) mentioned two undetermined species in a seasonal context. The enzymes necessary for a functional pentose phosphate pathway were found in a Neoechinorhynchus species by Saxon (1972). The enzyme specific activity peaks coincided with host temperature and in N. sp.6-phosphogluconate dehydrogenase there appeared to be a biochemical response to seasonal changes in the environmental temperature of the host. Octospinifer macilentis Van Cleave, 1919 Harms (1963, 1965) experimentally demonstrated the life cycle of Octospinifer macilentis. At 21°C the shelled acanthors hatched in 4 hours in the intestine of Cyclocypris serena. By 24 hours the tissues dorsal to the host gut were penetrated and four days post-infection the acanthors were in the haemocoel. Invasive cystacanths were present from day 30 post-infection. Catostomus commersoni were infected by force feeding at 15°C. Harms (1 965) estimated that mature males would be achieved in about 8 to 10 weeks, but that the females required somewhat longer, about 16 weeks. Harms (1965) noted that the ostracod hosts were refractory to invasion during June and July of two consecutive years. Further investigation is needed to reveal the significance of this fact. Octospinifer species undetermined Bullock (1962a) noted an undetermined species of this genus in a seasonal context from New Hampshire, U.S.A., in unspecified host fishes. No details were given. Paulisentis missouriensis Keppner, 1974 Paulisentis missouriensis was described from the fish Semotilus atromaculatus

H E L M I N T H S I N F R E S H W A T E R FISHES

179

at five creeks in Johnson County, Missouri, U.S.A. Keppner (1974) collected fishes from June 1971 through to November 1972, and individual hosts longer than 60 mm had an incidence of infection of 80 %duringthe entire period. Both immature and mature P. rnissouriensis were often found in the same fish host during the summer months. Shelled acanthors ingested by Cyclops vernalis hatched within 2 hours and penetrated the gut wall inside 4 hours of feeding. The acanthella was developed by the sixth day a t 20-23°C and was invasive to the definitive host by the fifteenth day post-infection. After one week from feeding to S . atromaculatus juvenile worms recovered from the intestine had doubled in size and were further developed. By the third week female worms contained ovarian balls, but not shelled acanthors, and males contained sperm in the seminal vesicles although the pouches of the vasa efferentia were not formed. Development beyond three weeks was not studied (Keppner, 1974). Tanaorhamphus longirostris (Van Cleave, 1913) Bullock and Samuel (1975) transferred this species from the Family Tenuisentidae to the Family Neoechinorhynchidae. Van Cleave (191 3, 1916) described a seasonal pattern of occurrence for Tanaorhamphus longirostris (as Neoechinorhynchus longirostris) in Dorosoma cepedianum from the Illinois River, Illinois, U.S.A. In summary Van Cleave (1916) found the fishes to be free of infection January to May, immature worms appeared June and July, and gravid females were observed August, November and December. Overall, the incidence of T. longirostris in D. cepedianum was low. Jilek (1978b)also found Tanaorhamphus longirostris in Dorosoma cepedianum at Crab Orchard Lake, Illinois, U.S.A. A peak incidence of 43 % was seen in July. Immature adults were noted in March only. Sexually mature worms appeared in the latter part of March, and then through the spring and summer until August. Interestingly, the timing of occurrence of T. longirostris differed between Crab Orchard Lake and the Illinois River. It may be speculated that slower warming of the river habitat induced the later times of occurrence. (c) Family Tenuisentidae Paratemisentis ambiguus (Van Cleave, 1921) Bullock and Samuel (1975) concluded as a result of the examination of many specimens that Tanaorhamphus ambiguus was not congeneric with T. longirostris: the latter species was additionally moved to the Family Neoechinorhynchidae. Thenew genusParatemisentis was proposed, with P. ambiguusas the type species. Bullock (1962a) briefly mentioned P. ambiguus (as Tanaorhamphus) in a seasonal context, but gave no specific details. Johnson (1975), in a brief abstract, also indicated that P. ambiguus was in process of investigation for seasonal incidence in estuarine amphipods at North Carolina, U.S.A., but no further details are known to the author. 2. Order Palaeacanthocephala (a> Family Illiosentidae Dentitruncus truttae Sinzar, 1955 Golvan (1969) could not separate Pseudorhadinorhynchus and Dentitruncus

180

JAMES C . CHUBB

on the basis of descriptions, and was unable therefore to come to a conclusion as to the validity of Dentitruncus. Manilla et al. (1976) redescribed D.truttae using specimens collected from Salmo trutta in the River Tirino, Italy, and emended the generic diagnosis and the characteristics separating Dentitruncus from Pseudorhadinorhynchus. Paggi et al. (1978) have studied the occurrence of D. truttae over a 12 month period in the River Tirino, but details were not provided.

(b) Family Lep t orhynchoididae Leptorhynchoides plagicephalus (Westrumb, 1821) Kakacheva-Avramova (1977) noted this species in Acipenser ruthenus from the River Danube, Bulgaria, in spring. Leptorhynchoides thecatus (Linton, 1891) Pearse (1924) observed Leptorhynchoides thecatus (as Echiizorhynchus) in the intestine lumen ofPercafiavescens from the Yahara River lakes, Wisconsin, U.S.A., during most of the summer months, April to September, but only once during autumn and winter (November). Visceral cysts containing encapsulated larvae were of frequent occurrence through the months, but maximal during April and May. The life cycle of L. thecatus was studied experimentally by De Giusti (1949). Shelled acanthors stored at 4°C remained invasive for nine months. The amphipod Hyalella azteca served as intermediate host. At 25°C the development of the cystacanth was achieved in 30 to 32 days. Immature encapsulated L. thecatus were found in a variety of fishes, and experimental infections showed that fully-developed cystacanths (30 days age plus at 20-25°C) from the amphipods on ingestion became established in the fish intestine. However, cystacanths 26, 27 and 28 days old penetrated the intestine wall and wereencapsulated in the viscera of the fishes. Lateacanthella stages less than 26 days old did not establish at all in the fish host. At lower temperatures, 13-1 5"C,the larvae in H . azteca had developed in three months only to the condition achieved in 8 to 10 days at 20-25"C7 and many of the larvae became walled-off and enclosed in a brown chitinous-like covering after ten days to two months, which soon caused their deaths. At 30°C no increase in the rate of development as compared with 20 to 25°C was seen, but a mortality of the H. azteca was evident. De Giusti (1949) observed that in the fish Ambloplites rupestris the Leptorhynchoides thecatus grew in body size and completed sexual maturation. The male worms were fully developed after four weeks, and it was deduced that copulation occurred between the third and fourth week post-infection at 20-25°C. The female worms contained shelled acanthors by the eighth week, and these were recovered from the host faeces. In Lake Mendota, Wisconsin, U.S.A., a natural periodicity of occurrence was seen. At the end of February worms were found only occasionally, but by May and June the fishes harboured great numbers of immature L. thecatus. Peak occurrence was during July to September, with the majority of worms adult. In October and November few immature acanthocephalans were seen. During December through to February the population in the fishes declined to the winter low level. De Giusti (1949)

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suggested that the species achieved overwintering as either shelled acanthors or larvae in the intermediate host Hyalella azteca. Small amounts of additional seasonal information concerning Leptorhynchoides thecatus can be found in Bullock (1962a), Cannon (1973) and Johnson (1975). The last researcher found larvae of L. thecatus in estuarine Gammarus daiberi, G .fasciatus and G . tigrinus in North Carolina, U.S.A. An interesting live-box tether experiment was carried out usingLepomismacrochirus at Gull Lake, Michigan, U.S.A., by Esch et al. (1976). During the eight week study, late-June to mid-August, L. thecatus were initially recruited slowly, during which time Pomphorhynchus bulbocolli were recruited at a higher rate (see p. 196), but as the P . bulbocolli rate declined, so the recruitment rate for L. thecatus increased. However, Esch et al. (1976) could find no evidence of competitive exclusion between the two species. (c) Family Fessisentidae Fessisentis friedi Nickol, 1972 According to Nickol(l972) Fessisentis vancleavei mentioned in a seasonal context by Bullock (1962a), and Fessisentis sp. of Fried et al. (1964), later determined as F. vancleavei by Fried and Koplin (1967), were in fact F. friedi. Fried et al. (1964) found that at Bushkill Creek, Pennsylvania, U.S.A., their species was absent from Catostomus commersoni in May, but present in 39-1% of these fishes from October through to December. Muzzall(l978) investigated the occurrence of F.friedi in the isopod Caecidotea communis at Old Reservoir, Durham, New Hampshire, U.S.A. Cystacanths were discovered during all months sampled in 1975, but most isopods were believed to have been invaded in late May to July, since the majority of acanthellae were recovered at this time. Muzzall(1978), quoting from another source, stated that Esox americanus in Old Reservoir had adult F. jiiedi in their intestines in February, March and May. He suggested that the seasonal occurrence of F. friedi in the isopods was related to the spawning habits of the E. americanus which harboured adults of F. friedi, owing to the close timing between the release of shelled acanthors into the environment, the appearance of a new generation of isopods and changes in the composition of the isopod population. (d) Family Echinorhynchidae The genera Metechinorhynchus and Pseudoechinorhynchus proposed by Petrochenko (1956) are not used in this account. If used at all, they are best retained as subgenera as proposed by Golvan (1 960-61), even though he later elevated them to generic status (Golvan, 1969). The type species for the genus Pseudoechinorhynchus,P . clavula (Dujardin, 1845)was transferred to the genus Acanthocephalus by Grabda-Kazubska and Chubb (1968) after comparison of new specimens and examination of Dujardin’s original drawings (see Acanthocephalus clavula p. 182). Acanthocephalus anguillae (Muller, 1780) Seasonal findings of Acanthocephalus anguillae were given by Srhmek (1901, as Echinorhynchus globulosus), Ruszkowski (1926), Bogdanova (1958), Izyumova (I958,1959a, 1960),Lyubarskaya (1970) and Kakacheva-Avramova

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(1973, 1977) as part of faunistic surveys (see Table V for hosts and localities). Mostly these show no clear pattern of occurrence, although Izyumova (1958) found in Perca Juviatilis at the Rybinsk Reservoir, U.S.S.R., that minimal incidences were during October-November (10 %), increasing January-April (19.2 %) to a maximum May-July (33.3 %). Oien (1976,1979) at Lake 0yeren, Norway, reported that A . anguillae was commonest and largest in Leuciscus idus as compared with Rutilus rutilus. Greater occurrence in L. idus was attributed to greater food consumption owing to the larger size of this host, The greater size of the acanthocephalans in L. idus was ascribed to this fish being a more suitable host than R. rutilus (Oien, 1976). Lake 0yeren froze over during winter and the summer water temperature reached 20°C. Nonetheless 0ien (1979) found a 100 % incidence of A. anguillae in L. idus in nearly all months, although the intensity was highest in summer. The A. anguillae were divided into length groups of 0-5, 6-10, 11-15, 16-20 and 21 mm plus. All length groups were present each month except November to February when no worms measured greater than 20 mm. Most worms measured 6 to 10 mm each month. Shtein (1959b) noted that Asellus aquaticus was the intermediate host of Acanthocephalus anguillae in Karelia, U.S.S.R. Andryuk (1974a) found a 5.5% incidence of cystacanths in Asellus aquaticus in the River Dnepr, U.S.S.R. Invasion of the fishes occurred in spring when they fed on the infected isopods. The A . aquaticus were invaded by ingestion of shelled acanthors in autumn. In experimental infections of A. aquaticus Andryuk (1974~) found that invasive larvae were developed in 15 days at an external temperature of 24°C. The acanthor stage required 2-3 days, pre-acanthella stages ten days and the acanthella 2-3 days at 24°C. At 19"C, by contrast, the complete development in A. aquaticus required 43 days (Andryuk, 1979). In the fish host Percottus glehni sexual maturity of the worms was achieved within 15 days, but the fertilized females did not commence release of shelled acanthors until 49 days post-infection (Andryuk, 1979). Acanthocephalus clavula (Dujardin, 1845) Grabda-Kazubska and Chubb (1968) showed that specimens from Llyn Tegid, Wales, corresponded to Dujardin's original drawings preserved at Rennes, France. However, certain features of the anatomy, seen in the specimens and illustrated in the drawings, placed the species into the genus Acanthocephalus, to give the new combination A . clavula for Echinorhynchus cZavula sensu Dujardin, 1845. Some Polish specimens, corresponding to E. clavula sensu Liihe, 1911 were considered a synonym of Echinorhynchus borealis Linstow, 1901 by Grabda-Kazubska and Ejsymont (1969) (see p. 189). Chubb (1963b, 1964a) (as Echinorhynchus clavula) studied Acanthocephalus clavula in Anguilla anguilla, Esox lucius, Rutilus rutilus and Thymallus thymallus from Llyn Tegid, Wales. The intermediate host was Asellus meridianus; this was later experimentally demonstrated by Rojanapaibul(l976, 1977). Chubb (1964a) believed that the pattern of incidence of the acanthocephalans was partly a reflection of the feeding habits of the particular host fish: T. thymallus ate the highest proportion of A. meridianus and had the highest percent

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incidence; A . anguilla also ate many isopods and also had a high overall incidence of the parasite. In E. lucius secondary establishment from prey fishes was postulated. Unfortunately, no data concerning the feeding of R. rutilus were collected. No clear seasonal periodicity of incidence or intensity of occurrence of the A. clavula was seen in the four species of fishes, nor was there any obvious seasonal maturation cycle. Female worms with shelled acanthors were obtained during all months, except February and December, attributed to a sampling deficiency of fishes. Success of maturation of the female worms overall was correlated with the concentration of the acanthocephalans in the host intestine facilitating copulation, and perhaps also indicating a physiological suitability of the host intestinal lumen for the development of the A. clavula. The overall percentages of the female worms found containing shelled acanthors were: A. anguilla 82.2%, E. lucius 50.0%, T. thymallus 22.9% and R. rutilus 5.5 %. A dynamic equilibrium of variable but continuous invasion of the fishes by cystacanths through the year, and an equally variable and continuous loss of mature worms, also at all seasons, was postulated (Chubb, 1964a). This view was stressed as a result of further observations concerning Acanthocephalus lucii and Echinorhynchus truttae (Chubb et al., 1964). Pennycuick (197 1a, b, c, d) (as Echinorhynchus clavula) studied the biology of Acanthocephalus clavula in Gasterosteus aculeatus from Priddy Pool, Somerset, England. Incidence was about 50% in October 1966 to February 1967, falling to about 5 % by August 1967, rising again to about 30% over October to December 1967, to fall once more to around 5% by April 1968. In G . aculeatus 55.7% of the female worms contained shelled acanthors. Pennycuick (197 1b) described the patterns of gain and loss of the populations of A . clavula in G . aculeafus. In summary, most acanthocephalans were acquired in autumn, although invasions continued overwinter, but a decrease in the worm populations occurred in the spring. Pennycuick (1971b) was of the opinion that the seasonal fluctuations at Priddy Pool could in general be related to the feeding activity of the G . aculeatus and the abundance and activity of the intermediate host. Rojanapaibul (1976, 1977) investigated the life cycle of Acanthocephalus clavula experimentally. The complete cycle required at least 132 days at 8-1 3°C. In Asellus meridianus acanthellae were first seen 49 days post-infection and cystacanths after 78 days. Cystacanths fed to Cottus gobio produced female A. clavula releasing shelled acanthors in 48 days. Low temperatures slowed growth and development in A . meridianus, and high temperatures stimulated growth: invasive cystacanths were produced in 20 weeks at YC, 16 weeks at 10°C and 7-8 weeks at 19°C (Rojanapaibul, 1977). Andrews and Rojanapaibul (1976) studied occurrence of Acanthocephalus clavula in Anguilla anguilla, Coregonus lavaret us, Cottus gobio, Percafluviatilis and Rutilus rutilus from Llyn Tegid, Wales. The pattern of infection in each of these fish hosts was mainly determined by the feeding habits of that host, whilst the success of the maturation of the parasites was influenced by the intensity of infection and the intestinal anatomy of the host. High intensity in short intestines favoured maximal reproductive success of the female worms,

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achieved in particular in A . anguilla and C. gobio. Rojanapaibul (1977) provided more detail for four of the host species. In C. lavaretus and R. rutilus invasion occurred mainly late summer through to late autumn, with maturation of female worms in C . lavaretus from February to June. Mature worms occurred all year in A. anguilla and C . gobio. Incidence and intensity of occurrence in C. lavaretus was high (50-92 % incidences) February to August, but lower (1440%) September to January. In R . rutilus maximal incidences were in May (44%) and June (57%), low levels (418%) were seen July t o December, increasing January (23 %) to April (31 "/o) and May-June. In C. gobio high occurrences were observed late autumn to late spring, but low beginning of summer to autumn. By contrast, in A . anguilla high incidences and intensities were present all year (Rojanapaibul, 1977). There was no doubt that A . anguilla was the host in which maximal shelled acanthor production by the female worms occurred. In P . jiuviatilis Andrews (1977) noted peaks of incidence in April (90 %) and May (83 %), and to a lesser extent, in September(23 %)to November (20 %). Shelled acanthor presence was maximal in May (45.8% females with shelled acanthors) and June (44 %), but shelled acanthor presence was recorded from February (12.5 %) to July (6.5 %) with a minor occurrence in October (7.7 %) and November (10.5 % females with shelled acanthors). Andrews (1977) was also able to relate these changes to the feeding of P . fluviatilis on Asellus meridianus, the intermediate host in Llyn Tegid. From March to May the stomachs of these fishes contained large numbers of A . meridianus, and again in August to November. The increase in gravid females of A . clavula was attributed to the greater chances of successful copulation and fertilization occurring at periods of high occurrence of the worms. Andrews (1977) emphasised the dynamics of gain and loss of worms from the intestines of P.JEuviatilisat all seasons. Brattey (1982), once again working at Llyn Tegid, Wales, with Perca jluviatilis, also found spring-summer peak occurrences of Acanthocephalus clavula, and, as before, these occurrences were related to host feeding on Asellus meridianus. Throughout the infection period there was a continuous loss of both immature and mature A . clavula from the intestines of P.fluvialilis. Gravid females were found only in May to July and very few appeared to survive long enough to attain full maturity. Brattey (1982) is currently attemptinga series of laboratory experiments to test some of the factors involved in the P. jluviatilis-A. clavula relationship. Acanthocephalusdirus (Van Cleave, 1931) Camp (1977), at an unstated habitat in the United States of America, studied seasonality of occurrence of Acanthocephalus dirus in the fish host Semotilus atromaculatus and the isopod intermediate host Asellus intermedius. The incidence of infection fluctuated seasonally in both host species, but details were not provided. Seidenberg (1973) examined the ecology of occurrence of A . dirus in A . intermediusat Mud Creek, Illinois,U.S.A. Invasion of the isopods commenced during summer, so that by the following March up to 60 % were infected, According to Bullock (personal communication to Amin, 1975) the Seidenberg (1973) material was probably A. parksidei (see p. 188).

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Acanthocephalusjacksoni Bullock, 1962 Bullock (1962b) reported mature Acanthocephalus jacksoni in 6 species of fishes in New Hampshire and eastern Massachusetts, U.S.A. In 1963 he stated that the immature A . jacksoni were located in the host intestine more anteriorly than the mature infections. The seasonal periodicity of this species of acanthocephalan was studied in five fish hosts and the intermediate host, Lirceus lineatus, at Jackson Cutoff, Ohio, U.S.A., by Muzzall and Rabalais (I975a, b). Cystacanths first appeared in L . lineatus in October, adult acanthocephalans in the fishes (see Table V for species) in November. Jackson Cutoff was frozen in January and February. Intensity of occurrence rose sharply during the spring months. Female A . jucksoni with ovarian ball stages were seen December through July, and shelled acanthors were present January to July. In July the population of adult acanthocephalans declined abruptly, so that no A . jucksoni were present in the fish intestines from August to October (Muzzall and Rabalais, 1975a). The above seasonal periodicity of Acanthocephalusjacksoni was related to a number of environmental and host factors by Muzzall and Rabalais (1975a). Lirceus lineatus was absent from the habitat from July to September, but mature adults appeared very suddenly in October. These isopods were thought to survive the dry season, July to September, at Jackson Cutoff in interstitial spaces in the substrate, although the fish hosts were present through these months. It was suggested that A. jacksoni survived July to October as shelled acanthors. L . lineatus were not infected by A . jacksoni May to September, and this was correlated with the lack of contact between the isopods and the shelled acanthors. The absence of infected fishes August to mid-November was related to the lack of infected isopods. The cystacanths were only seen in the isopods October through April, although the isopods continued to be present until the end of June. The absence of the cystacanths from April onward was difficult to explain, especially as A . jucksoni larvae could develop at 21°C in L. lineatus. Muzzall and Rabalais (1975a) found experimentally that A. jacksoni had a short period of life in the fish intestines. Lepomis cyanellus and L. macrochirus held invasions for only eight days, but copulation occurred during this time. Naturally infected fishes at ambient temperatures held the infections for 16 days. The female worms passed out whole, containing shelled acanthors, and could also be seen hanging from the anal apertureof some fishes. The release of the shelled acanthors was thought to occur by disintegration of the female worms after they were voided from the fishes (Muzzall and Rabalais, 1975a). Of the cystacanths in L . lineatus the male A. jacksoni probably contained functional sperm (see also A . lucii, Brattey, 1980) and the ovary of the female acanthocephalans was fragmented (Muzzall and Rabalais, 1975b), suggesting that copulation and maturation of the worms could commence as soon as they entered the intestine of the fishes. Acanthocephalus hcii (Miiller, 1776) A widely distributed species, through Europe to the basins of the Volga and the Gulf of Finland, occurring in numerous types of fishes (Golvan, 1969), thus it is hardly surprising to find many relevant seasonal references. The following are listed in Table V, but not discussed further here: Zschokke

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(1884) (as Echinorhynchus angustatus); Ivasik (1953); Markova (1958); Izyumova (1959a, 1960); Vojtkova (1959); Komarova (1964); Rizvi (1964, 1968); Molnir (1966a); Rautskis (1970a, b); Wierzbicki (1970); Marits and Tomnatik (1971); Banina and Isakov (1972); Halvorsen (1972); Shul'man et al. (1974); Andrews (1977); Kakacheva-Avramova (1977); Lee (1977); and Priemer (1979). Komarova (1950) studied Acanthocephalus lucii mostly in Perca Jluviatilis from the River Dnepr, U.S.S.R. A well-defined annual pattern was found. In October one acanthocephalan only was seen. In December to January the incidence rose sharply; the worm lengths were 4.5-103 mm, and they were sexually immature, with non-functional testes in the male worms. In MarchApril incidence and intensity increased, worm lengths were 5-13 mm, but they were still sexually immature. At the end of spring and summer the A . lucii were mature, the females filled with shelled acanthors; worm lengths, May 7-193 mm, and summer 8.3-21 mm. During June to August the occurrence of the acanthocephalans declined (from 40.9 % in June to 23.8 % in August; maximal incidence May 75 %). Komarova (1950) interpreted the annual cycle as: shelled acanthors released summer, adult A . lucii died; development of cystacanths in Asellus aquaticus by the end of summer and autumn; invasion of fishes from autumn onward, growth during winter and spring to give sexually mature worms in summer. However, such clear pattern of invasion, occurrence and maturation of Acanthocephalus lucii has not been reported elsewhere. At the Rybinsk Reservoir, U.S.S.R., Izyumova (1958) found high incidences in PercaJluviutilis year round, although there was a tendency for minimal occurrence in autumn and maximal in summer: October-November 40 %, January-April 61.5 % and May-July 66.6%. In northern conditions of Lake Konche, Karelia, U.S.S.R., Malakhova (1961) observed the following levels of occurrence (percent incidence, mean intensity and range) in P.fEuviatilis: autumn 47.7 %, 4.8, 1-15; winter 36.3%, 3-68, 1-12; spring 45-5%, 3, 1-18; and summer 62.2%, 6.46, 1-38. The high occurrences during summer can be attributed to increased intensity of feeding by the fishes. Maximal incidence in any month was 70 % in August, and minimal 27.3 % in February. Mishra (1966) at the Shropshire Union Canal, Cheshire, England, recorded the presence of A . lucii in P. Juviatilis during all months of the year. Minimal incidence was in September (23 %) rising to a peak in October (61 %), falling again December (20 %), but remaining high January (70 %), February (67 %), March (85 %), April (61 %), May (73 %) and June (67 %), falling July and August (36 % each) to September. The percentage of the female worms containing shelled acanthors was highest in June (70 %) and September (62 %), but shelled acanthors were present during all months except February, August and December. Including the other species of fishes examined by Mishra (1966), Anguilla anguilla, Esox lucius and Rutilus rutilus shelled acanthors of A . lucii were present year through, January 1965to January 1966.At Lake Rsyetjern, Norway, Andersen (1978) also observed A. Iucii in P . Jluviatilis all year. Highest incidences were summer and autumn when up to 65% of the fishes were infected. During

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winter and spring months there was a drop in incidence, lowest 15.4% in May-June, and there was also a tendency towards lower intensities of worms during the winter months. Immature worms were seen in all months, therefore invasions probably occurred year through. Gravid worms were present in all samples except December-January, but dominated the female population during the summer and early winter months. At MBcha Lake fish pond system, North Bohemia, Czechoslovakia, Moravec (19’79b) reported that Esox lucius acquired infections secondarily from Perca fluviatilis. An overall incidence of 63-5% was found, between 46 and 100% per month. Maximal infection occurred April-May, diminishing June to lowest July-August, increasing again during autumn. Mature female Acanthocephalus lucii containing shelled acanthors were present all months except December, but their proportion increased in spring, May-June, and again in autumn, September-October. Moravec (1979b) stressed that there were not two generations of A . lucii per annum in these E. lucius, but that both occurrence and maturation showed partial seasonal quantitative changes, these apparently being evoked by water temperatures and availability of intermediate hosts (via P . fruviatilis in the instance of E. lucius). A loss of gravid and dead worms was seen in June and July, so that a dynamicequilibrium similar to that noted by Chubb (1964a) for Acunthocephalus clavula and Kennedy (1 967) for Pomphorhynchus laevis was postulated. At the MBcha Lake system Moravec (1979b) observed that Asellus aquaticus was the intermediate host (10.8 % incidence in March), and A . lucii produced shelled acanthors also in Anguilla anguilla and P . jluviatilis. Asellus aquaticus was also the intermediate host of Acanthocephalus lucii in Poland (Styczynska, 1958), Karelia, U.S.S.R. (Shtein, 1959b), the River Dnepr, U.S.S.R. (Andryuk, 1974a, b), and the Forth and Clyde Canal, Glasgow, Scotland (Brattey, 1980), as well as those habitats noted earlier. Larvae were seen in 5.5 %of A . aquaticus in the River Dnepr, and their invasion occurred in autumn (Andryuk, 1974a). Development to cystacanths in the isopod required 72 days at 15-16°C and 60 days at 18°C (Andryuk, 1974b). Brattey (1980) found that at 22°C the cystacanths were invasive to fishes in 40 days. He observed a 1 :1 ratio male to female cystacanths in the A . aquaticus, with incidences of 4.8 % in September and 7.8 % in January. The female cystacanths had the ovary fragmented into ovarian balls, and active sperm was seen in the males. Experimental invasions of fishes revealed that the A . lucii could copulate in less than 24 hat 20°C. Statistically greater numbers of infected isopods were eaten by Perca Juviatilis during feeding experiments (Brattey, 1980). Chubb et al. (1964) reported that a male Acanthocephalus lucii and an ovarian ball stage female were recovered in a general lininological sample collected from the Grand Canal, County Dublin, Eire, thus demonstrating a loss of worms, even when immature, from their fish hosts in nature. Wierzbicki (1971) has investigated the effect of host depth and season on the occurrence of Acanthocephalus lucii in Perca fruviatilis from Lake Dargin, Poland. Maximal intensities of infection were found in shallow waters (7.5

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individuals per fish), as compared with littoral (2-4) and deep waters (2.1). Rautskis (1977), also examining P . Juviatilis, from three lakes with different thermal regimes in Lithuania, U.S.S.R., observed no significant seasonal differences in occurrence of A. lucii. Acanthocephalusparksidei Amin, 1974 The material identified as Acanthocephalus dirus by Seidenberg (1973) (see p. 184) was probably A . parksidei according to Bullock in a personal communication to Amin (1975). The seasonal biology of A . parksidei has been investigated in detail by Amin (1975). The parasites occurred in 11 species of fishes in the Pike River, Wisconsin, U.S.A., but seasonality was investigated only in Catostomus commersoni,Lepomis cyanellusand Sernotilusatromaculatus. The incidence and intensity of occurrence of A . parksidei was influenced mainly by the proportion of intermediate hosts in the diet of the fish species, which also varied seasonally, and with the size of the fish. A higher incidence was seen in large than small fishes of certain species. This was attributed to higher food volume consumption, changes in diet with host age and cumulative infections within a parasite generation. Host sex, concurrent infections and collection sites also influenced occurrence in some fishes. The seasonal pattern overall was of invasion from autumn through spring, with incidence and maturation peaking in spring, and mature worms virtually eliminated during summer. In C. commersoni the establishment of new invasions commenced late summer. New infections were characterized by distinct and relatively exclusive anterior localization of male worms, with the females sited more posteriorly. This pattern was not apparent in C. commersoni in spring. In September and October 72% of the female A. parksidei were at the ovarian ball stage; the remainder were packed with shelled acanthors, and some were believed by Amin (1975) to represent the previous generation. Continued maturation during winter produced a spring (May) population largely composed of females with shelled acanthors (80 %), about three-quarters of these being packed with shelled acanthors. Continued invasion was demonstrated by females with ovarian balls and the fact that mean intensity per host increased from 1-1 in September-October, to 13.55 in November and a peak of 95.59 in May. Dead worms were most frequent in the May collections. Male worms were more short lived than females (Amin, 1975). In Semotilus atromaculatus and Lepomis cyanellus the Acanthocephalus parksideigrew to a larger size, owing to these hosts providing a more favourable habitat. Maturation occurred earlier in S. atromaculatus, as shown by percent gravid females present per month. An overlap of “generations” was considered to occur in all hosts between July and October (Amin, 1975). However, the term generation is probably best avoided in this context, as there were clearly successive and continuous invasions and maturation of the A. parksidei, especially from October to May, but also through much of the year. In A . parksidei it has been noted above that the female worms were attached more posteriorly during autumn. With progressive maturation the females moved posteriorly to the hind-gut of Catostomus commersoni, L. cyanellus and S. atromaculntus, so that by spring the posterior position corresponded with the

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worm reproductive peak and the host breeding activity peak (Amin, 1975). Amin (1977) recovered females of Acanthocephalus parksidei at all stages of development from most of 12 hosts in Lake Michigan, U.S.A., during all months except June. The intermediate hosts of Acanthocephalus parksidei have been found to be Caecidotea intermedius (= Asellus militaris) (Amin and Burns, 1978) and Pontoporeia afJinis (Amin, 1978b). One generation per year of C . intermedius was evident in Pike River, breeding early spring, with a high frequency of juveniles 1-2 months later. The cystacanth developmental cycle was closely related to that of the isopod. Invasion of the isopods commenced in summer, following peak shelled acanthor production by female A . parksidei in fishes during spring. Cystacanths and the isopod hosts increased in size through autumn and winter to a maximum the following spring. One generation of A. parksidei in the intermediate host had a seasonally defined life span of a maximum of one year (Amin and Burns, 1978). Acanthocephalus tenuirostris (Akhmerov and Dobrovskaya-Akhmerova, 1941) Reported, as Paracanthocephalus tenuirostris, by Kakacheva-Avramova (1 973) in Barbus meridionalis petenyi and Leuciscus cephalus from the Central and Eastern Balkan Mountains, Bulgaria, during spring, summer and autumn. According to Petrochenko (1956) this acanthocephalan is a parasite of fishes in lakes of the Amur Basin, Rivers Lena and Ussuri, U.S.S.R. Acanthocephalus species undetermined Bullock (1962a) mentioned an unidentified Acanthocephalus species in a seasonal context from fishes in New Hampshire, U.S.A. Echinorhynchusbaeri (Kostylew, 1928) Vartanyan and Mkrtchyan (1972) observed this species (as Metechinorhynchus baeri) in Coregonus lavaretus ludoga and C. lavaretus maraenoides from Lake Sevan, Armenia, U.S.S.R. Incidences (and intensities, range, average) were: spring (May) 73.3% (3-17, 7.5); summer (June-July) 0 % ; autumn (October-November) 66-6% (5-75, 2.64) ; and winter (DecemberJanuary) 0 %. Echinorhynchus borealis Linstow, 1901 Grabda-Kazubska and Ejsymont (1969) showed that Echinorhynchus clavula sensu Liihe, 1911 (see p. 182) and E. cinctulusPorta, 1905were synonyms of E. borealis. They examined specimens from Poland, and also from Lake Ladoga (from Silurus glanis), the River Volga (from Lota Iota), the River Yenisei (from Perca fluviatilis), Taimyr Lake (from Thymallus arcticus) and Pert Lake (from Pallasea quadrispinosa), U.S.S.R. All were determined as E. borealis. However, acanthocephalans from the Far Eastern U.S.S.R. were thought to be Echinorhynchus parasiluri Fukui, 1929. Worms from the River Punkva, Czechoslovakia in Salmo trutta were also not E. borealis. The intermediate host of E. borealis in Poland was Gammarus pulex (Grabda, 1971). Van Maren (1979b) reported E. borealis from Lota Iota in the upper River Rhbne, France, and stressed that, owing to the nomenclatorial confusion between Echinorhynchus clavula sensu Dujardin, 1845 (now Acanthocephalus clavula, see p. 182) and Echinorhynchus clavula sensu Liihe, 1911 (now

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E. borealis) earlier literature data on the distribution and hosts of these parasites should be treated with caution. The following authors have presented seasonal data for acanthocephalan parasites which may in fact be E. borealis: Bogdanova (1958) as Pseudoechinorhynchus clavula, from Abramis brama, River Volga, U.S.S.R. ; Malakhova (1961) as Echinorhynchus clavula, from Lota Iota, Lake Konche, Karelia, U.S.S.R. ; Komarova (1964) as P. clavula from Esox lucius, Lucioperca lucioperca and Pelecus cultratus, Dnepr Delta, U.S.S.R.; Halvorsen (1972) as P . clavula from Lota Iota, River Glomma, Norway ;and Kakacheva-Avramova (1977)as P. clavula from six species of fishes, River Danube, Bulgaria. However, owing to the fact that these acanthocephalans require re-examination to confirm their identities, they are not discussed further nor tabulated in Table V. The same situation applies to intermediate host records for Pseudoechinorhynchus clavula. The identifications of Shtein (1959b), Yalinskaya (1967), Ivasik (1972) and Kurandina (1975) require confirmation that they really refer to E. borealis. Echinorhynchus laterah Leidy, 1851 Sandeman and Pippy (1967) observed Echiizorhynchus lateralis in Coregonus clupeaformis, Salmo gairdneri, S. salar (landlocked), S. trutta and Salvelinus fontinalis in Insular Newfoundland, Canada. Mature male and female acanthocephalans were found regularly at all times of the year, but the number of recently acquired worms increased in late-September. This peak of invasion was coincident with peak production of the amphipod intermediate host Hyalella azteca. Echinorhynchus salmonis Miiller, 1784 Bauer and Nikol’skaya (1957) reported an 81 % incidence in July and a 100% incidence August to November in Coregonus lavaretus baeri natio ladogae from Lake Ladoga, U.S.S.R. The fishes were mainly infected from their third year of life onward, owing to the fact that the amphipod intermediate hosts Pallasea quadrispinosa and Pontoporeia afinis dominated their diet from that age (Bauer and Nikol’skaya, 1952). High intensities of infection were common. Both male and young female Echinorhynchus salmonis were found July through November, so that Bauer and Nikol’skaya (1957) assumed invasion to occur continuously. The males and immature females were primarily attached in the pyloric caeca region of the intestine, but females with shelled acanthors predominated in the posterior part of the intestine. In Perca jlavescens at the Bay of Quinte, Lake Ontario, Canada, Tedla and Fernando (1969, 1970) examined occurrence of Echinorhynchus salmonis from May 1967 to February 1969 (see 1970 paper). A definitive cycle of both occurrence and maturation was seen. Incidence fell from 43.1 % in May 1967 to zero in August, and climbed from 7.1 % in September 1967 to 77.7% by March 1968,to decline again through the summer months to zero in September. A 2 % incidence in October 1968 had climbed to 80 % by February 1969, thus the pattern was repeated over two cycles. Intensity more or less followed incidence. In the autumn, at invasion, most worms were in the host upper

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intestine, but in May most were in the lower intestine. Production of shelled acanthors by the female E. safmonis was in spring and early summer, followed by progressive loss of the worms. By contrast to the marked seasonality of the biology of Echinorhynchus salmonis in Perca jlavescens, a year round occurrence and maturation was seen in Coregonus artedii and C. clupeaformis from Cold Lake, Alberta, Canada (Leong, 1975) (as Metechinorhynchus salmonis), in Osmerus mordax from Lake Michigan, U.S.A. (Amin and Burrows, 1977), and in Coregonus nasus from the Bay of Bothnia, Finland (Valtonen, 198la, b). Although in all these three instances some seasonal fluctuations of occurrence were seen, nonetheless, at no time did the levels reach anything near zero. Valtonen (1981a, b) was able to correlate the seasonal variations in occurrence with the migrations of the C. nasus from shallow waters, where the Pontoporeia afinis were less commonest, hence the invasion potential for the fishes by E. safmonis was greatest. An invasion period of at least six months was postulated (Valtonen, 1981a). Leong (1975) observed that in C. artedii there was no obvious seasonal pattern in the proportion of gravid females in the population; rather the percentage showed a general inverse relationship to the total number of E. salmonis in the same samples. The numbers of gravid females did not vary significantly between months. In C. clupeaformis neither the percent nor number of gravid females varied significantly between months. Amin and Burrows (1977) observed highest percentages of female worms with shelled acanthors during spring and summer in 0. mordax. Amin and Burrows (1977) and Valtonen (1981b) noted that the gravid E. safmonisoccupied aposterior station along the host intestine. Amin and Burrows (1977) summarized the situation as a dynamic one, with greater recruitment during cold months and greater maturation during warm months. The increased establishment of worms and decreased host feeding activity during the cold months was probably balanced by worm deaths and increased host feeding activity later during the warm period. Amin (1978a) was able to show that the maturation and posterior migration of Echinorhynchus safmonis in Oncorhynchus tshawytscha was coincident with host spawning. Worms in spawning 0. tshawytscha were significantly more mature and posteriorly placed than in non-spawning hosts, and with proportionally fewer males owing to their earlier elimination, as is characteristic of acanthocephalan populations in the latter part of their infection cycle. Thus Amin (1978a) suggested that E. salmonis maturation and migration might be affected by the sex hormones of the spawning hosts. This view was further supported by the fact that E. safmonis reached peak maturity in 0. tshawytscha during autumn, its spawning time (Amin, 1978a), but in PercaJEavescensin spring, its spawning period (see Tedla and Fernando, 1970). Accordingly, Amin (1978a) considered host breeding to be a significant factor influencing the timing of acanthocephalan mortality and recruitment and thereby their seasonal infection cycles. Hnath (1 969) demonstrated experimentally that Echinorhynchus salmonis could re-establish in the intestines of predatory fishes.

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The intermediate hosts of Echinorhynchus salmonis included Pontoporeia aflnis in both Asia (Shtein, 1959b)and North America (Amin, 1978b; Holmes et al., 1977). Seasonal and year to year variations were seen by Shtein (1959b) in Karelia, U.S.S.R. Holmes et al. (1977) used a deterministic mathematical model employing discrete generations to illustrate the flow rates of Echinorhynchus salmonis in ten species of salmonid and other fishes from Cold Lake, Alberta, Canada. Computer simulations of the model were utilized. They concluded that a suprapopulation (all the individuals of a single species in an ecosystem) of a parasite species could be regulated at the level of the host individual by a mechanism operating on infrapopulations (all the individuals in a single host individual) in only one of several of the host species. In the instance of E. salmonis it was shown that a mechanism operating by regulation at the level of the host individual, by an immune mechanism, or some other means, and operating solely on the infrapopulations in Coregonus clupeaformis, a principal definitive host, could regulate the suprapopulation of the parasite species. Such a system could regulate the parasite population by operation on infrapopulations in only one of the several species of hosts involved, provided that the combined flow through the other host species be inadequate to maintain the suprapopulation (Holmes et al., 1977). Echinorhynchus truttae Schrank, 1788 Much of the relevant information originates from the field and experimental studies of Awachie (1963a) which have been published in a series of papers (see below). Other seasonal data for the British Isles can be found in Robertson (1953), Davies (1967), Campbell (1974) and Rahim (1974); Germany, Steinstrasser (1936); Spain, Corder0 del Campillo and Alvarez Pellitero (1976a) ; and Yugoslavia, KatiC (1970) (see Table V for hosts and localities). Awachie (1963a, b) examined Salmo trutta, the definitive host, and Gammarus pulex, the amphipod intermediate host, from the Afon Terrig, Wales, a small stream, over the period November 1961 to January 1963. Concurrently, developmental and other experimental studies were undertaken in the laboratory. The life cycle from shelled acanthor, through the developmental stages to the cystacanth in the G. pulex, followed by invasion, establishment and production of the next generation of shelled acanthors in S. trutta required about 152 days at a mean laboratory temperature of 17°C (range 10-20°C) (Awachie, 1963b). The field studies (Awachie, 1965) showed no seasonal cycle in the incidence of Echinorhynchus truttae in Salmo trutta in the Afon Terrig. Although the stream was frozen in part during 1961-62 and again during the long, cold winter of 1962-63 for two months, since these periods were usually short, it seemed that the absence of long cold spells in most years might be a factor which influenced the uniformity of incidence. This incidence pattern was directly attributable to the fact that there were two main broods in the life cycle of Gammaruspulex in the Afon Terrig which overlapped, so that invasive shelled acanthors and cystacanths were found throughout the year. The percent incidence of cystacanths in G. pulex did change with season, however, with a

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lower incidence June to August (summer) ; this was coincident with the birth of young shrimps and the death of the older generation in which infection was greatest, as well as the fact that in the S. trutta a -higher proportion of the female E. truttae from June to August had immature shelled acanthors and earlier stages (Awachie, 1965). The intensity of infection in both hosts changed seasonally, and with an inverse relationship to each other. In Salmo trutta while the intensity was high in summer (June to September), and low from October to April, the reverse applied in Gammarus pulex. According to Awachie (1965) this rhythmical fluctuation was caused by trends in the composition of the population of Echinorhynchus truttae, seasonal cycles in the life of the G. pulex, and the seasonal changes in the food and feeding levels of the S. trutta. G. pulex was the only intermediate host in the Afon Terrig, and was an important food component for the S. trutta at all seasons. Although the incidence and intensity of infection of G . pulex was lower during the warmer months. over 50 % of the larvae were invasive cystacanths from June to August. This higher availability of cystacanths seemed to be reflected in the higher proportion of E. truttae without mature shelled acanthors present in the fishes from May to August. Thus the lower incidence and intensity of infection of G .pulex during summer was offset by greater feeding activity of the S. trutta with increased temperatures and day-lengths, leading to an increase in intensity of infection. The highest mean number of E. truttae (30.8) and highest percent of worms without mature shelled acanthors, representing recently acquired invasions, was recorded in June when the stream water temperature was ll.2"C. S. trutta activity is known to be maximal about 10-12°C. The fall in mean number of E. truttae in July might represent a midsummer fall in feeding activity of S . trutta, but could also be attributed to a predominance of aerial insects (55.4%) in the diet at that time (Awachie, 1965). Awachie (1965) related the sequences of the developmental stages of Echinorhynchus truttae in Salmo trutta with cyclical changes in Gammarus pulex. A generation of G. pulex was born in March, matured in July and reproduced in August and September. The second generation born in AugustSeptember overwintered as juveniles, matured about March and reproduced through to June. Female E. truttae in the intestines of S . trutta containing mature shelled acanthors reached a peak occurrence in April and December. Therefore the peak abundance of young G . pulex was coincident with the release of large numbers of shelled acanthors into the Afon Terrig, resulting in the maximum numbers of cystacanths in the maximum number of G.pulex in each generation, and ultimately, reinvasion of S. truttae and the continuation of the species of parasite. The changes in the stage of development of the E. truttae in one of the hosts flowed through the two host populations : for example, the greater occurrence of mature shelled acanthors in female acanthocephalans during the colder months induced the subsequent finding in the G. p u l a of a greater proportion of larvae at the spherical and earlier stages of development (Awachie, 1965).

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The stages of development of Echinorhynchus truttae in Gammarus pulex and Salmo trutta were described by Awachie (1966b) from his experimental studies. At room temperatures (range 10-20°C) shelled acanthors hatched in the intestine lumen of Gammaruspulex in 1-20 h, and penetrated the haemocoel via the intestine wall in 11-20 h. Development to the invasive cystacanth required a further 80 to 84 days. The life span of the cystacanth was then up to 74 months, determined by the life span of the G. pulex. Upon invasion of the S. trutta by cystacanths the female E. truttae were at the ovarian ball stage after seven days, acanthors were developing in the ovarian balls by 14 days, were released into the body cavity of the female worm by 21 days and some were mature shelled acanthors by 63 days, with most at this invasive condition during 84 to 91 days post-infection. Copulation occurred in the fish upper intestine during the first three days post-infection, and the male worms were passed from the S. trutta from days 45 to 82. Shelled acanthors were seen in the fish faeces from days 64 to 85. The first female worm was voided in the faeces on the 69th day, and they continued to be lost up to 98 days, none being found thereafter (Awachie, 1966b). Temperature greatly influenced the rate of growth in G.pulex. At a water temperature of 2 4 C , only spherical and earlier stages were seen after 136 days; by contrast these were formed after 20-24 days at room temperature (mean 17"C), which indicated that development was very slow at the lowest winter temperatures. Development in S. trutta was also retarded by low water temperatures. Crowding in the intestine of S. trutta facilitated copulation (Awachie, 1966b). Intraspecific crowding of Echinorhynchus truttae in both Gammarus pulex and Salmo trutta retarded growth of the acanthocephalans (Awachie, 1966b), but simultaneous and successive co-invasions of G . pulex by E. truttae and Polymorphus minutus, another acanthocephalan occurring in the Afon Terrig, were possible (Awachie, 1967). In S. trutta experimental primary heavy and superimposed invasions were carried out (Awachie, 1972a). These experiments revealed that E. truttae at summer water temperatures tended to be lost from the host intestine during the first few days post-invasion. Thus, in one fish at 9-12°C 21 worms were shed during the first two days, no more thereafter, so that at autopsy eight were established in the intestine. At 12-16°C 9 of 24 and 34 of 37 worms respectively were shed from two fish after the first three days. All the acanthocephalans thus voided were normal in form and size. At winter water temperatures, 4-9"C, the number of E. truttae passed within the first three days as well as the total number recovered with faeces before autopsy was very low, for instance, two S.trutta shed four and five worms respectively before autopsy at day 14, but these were lost much later than at the summer water temperatures. Awachie (1972a) concluded that establishment of E. truttae in the intestines of S. lrutta was temperature dependent. At higher summer water temperatures large numbers of worms were eliminated, and consequently, the numbers of E. truttae established was about the same in both heavy and low invasions. Markedly more E. truttae established at low water temperatures which, therefore, depressed this host rejection reaction. Superimposed invasions were little influenced by already existing infections, but

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both heavy and superimposed invasions effected an early extension of the linear distribution of E. truttae along the length of the intestine of the S. trutta. Heavy invasions had a beneficial effect in facilitating copulation, but would elicit strong host reaction at higher water temperatures. In nature of course recruitment was gradual over a long period (Awachie, 1972a). Starvation of S. lrutta with either natural or experimental infections for periods of 5 to 24 days did not lead to expulsion of established E. truttae (Awachie, 1972b). Cottus gobio in the Afon Terrig were also infected by Echinorhynchus truttae in January, March to May and July, but not November and December. No fishes were examined during the other months. Awachie (1973) considered that the worms could mature in C. gobio if male and female worms occurred together to enable copulation to take place, but low incidences and intensities of occurrence owing to ecological conditions in the Afon Terrig minimized this. Chubb et al. (1964) summarized and stressed the evidence for a dynamic equilibrium in the incidence of Acanthocephala in the intestines of the fish hosts. Much of this evidence originated from the experimental work of Awachie (1972a). The attachment of the E. truttae initially in the pyloric region of the intestine, and as they matured their movement to a more posterior region of the intestine, with gravid females in the rectal region was also emphasised. Spent male worms were lost from fishes, but also immature males and female worms at all stages of maturation. The regular phenomenon of worm movement within the host intestine lumen was considered to contribute to this loss. Hoffman (1954) observed that in the River Syre, Luxembourg, the incidence of Echinorhynchus truttae was maximal in those sections of the river where Gammarus pulex was commonest. Other studies on the seasonal dynamics of E. truttae in the intermediate host include: Parenti et al. (1965) Gammarus pungens pudanus, River Po, Italy; Yalinskaya (1967) G . balcanicus, G. kischinefensis, upper River Dnestr reservoirs, U.S.S.R. ; Ivasik (1972) G. balcanicus, rivers, Carpathian mountains, U.S.S.R. ; and Schiitze and Ankel (1976) G. pulex fossarum, small stream, Oberhessen, Germany. Echinorhynchus species undetermined Bullock (1962a) indicated that he had studied an undetermined species of Echinorhynchus in fishes from New Hampshire, U.S.A., during the period April to November, but gave no details. (e) Family Pomphorhynchidae Pomphorhynchus bosniacus KiSkaroIy and Cankovic, 1967 KaiiC (1970) gave some seasonal data for Pomphorhynchus bosniacus in Leuciscus cephulusalbus from Lake Skadar, Yugoslavia. The acanthocephalan was found February to October and December, with peak presence in August. KaiiC et al. (1977) also found P . bosniacus in Gobio gobio lepidolaemus from the same habitat, May to November, and in 6 % of these fishes. KakachevaAvramova (1973) noted P . bosniacus in Vimba vimba tenella from theCentral and Eastern Balkan Mountains, Bulgaria, in summer.

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Pomphorhynchus bulbocolli Linkins, 1919 Bullock (1962a) mentioned this species in a seasonal context from fishes of New Hampshire, U.S.A., but provided no detailed information. At Pushaw Lake, Penobscot County, Maine, U.S.A., Lawrence (1970) observed that incidence in Catostomus commersoni was high all year, with peak intensity during the summer months, which declined to a lower, fairly constant level from September to May. Live-box tether experiments using Lepomis macrochirus and L. macrochirus xL. gibbosus hybrids for an eight week period, late June to mid August were carried out by Esch et al. (1976) at Gull Lake, Michigan, U.S.A. The data collected indicated that Pomphorhynchus bulbocolli was recruited at a higher rate early in the period of investigation, but then the rate declined, whereas thereafter the rate of recruitment of Leptorhynchoides thecatus (see p. 181) increased. No evidence of competitive exclusion between the two species was seen. Pomphorhynchus laevis (Zoega in Muller, 1776) The following seasonal records concerning Pomphorhynchus laevis are listed in Table V, and are not discussed further here: Zschokke (1884) (as Echinorhynchus proteus), Bogdanova (19x9, Komarova (1964), Molnar (1968b), Marits and Vladimirov (I 969), Vartanyan and Mkrtchyan (1972), Kakacheva-Avramova (1973, 1977). Many details of the biology of Pomphorhynchus laevis have been provided by Kennedy (1972b, c, 1974) and his students, following a mass occurrence of the acanthocephalan in Leuciscus cephalus from the River Avon, Hampshire, England (Chubb, 1965). Hine (1970) observed that Gammarus pulex, the intermediate host in this habitat, contained all stages of larval development all year, and that P. laevis occurred in Leuciscus leuciscus all year, with no evidence of a seasonal incidence cycle. In the River Avon, P. laevis females grew to maturity and produced shelled acanthors regularly in Barbus barbus and Leuciscus cephalus, rarely in L. leuciscus and Salmo trutta, and not at all in twelve other species of fishes (see also Hine and Kennedy, 1974a; Kennedy et al., 1978). However in L. leuciscus a partial maturation cycle was present. Hine (1970) observed that the proportion of female worms containing ovarian balls which began to divide many times and break down to lose their shape and finally become indistinct from each other, so that the uterine contents were a homogenous collection of small bodies finally dividing to produce unshelled acanthors increased from March to reach a peak in April and May, declined slightly until August and then fell sharply to a low winter level. Cement caps, a result of copulation, were seen on the vulva of increased numbers of female P. laevis from April, to reach a peak in August. However Hine (1970) rarely found female P. Iaevis with shelled acanthors in L. leuciscus, so that this fish species cannot serve as a principal definitive host for P. laevis. Owing to the small number of L. cephaZus available for examination Hine (1970) was unable to be certain concerning the seasonal patterns present in this principal definitive host of P. laevis, but he thought it likely that incidence and intensity were high and steady throughout the year, with small numbers of immature female worms,

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large numbers maturing and much larger numbers of mature P . laevis, containing shelled acanthors ripe for release (see also Hine and Kennedy, 1974a). Kennedy (1972b) experimentally investigated the effects of temperature and other factors on the establishment and survival of Pomphorhynchus laevis in Carassius auratus. Of the factors studied, temperature alone influenced establishment, but not survival thereafter. Low temperature (6°C) gave maximal establishment, higher temperatures (12°C and 18°C) progressively reduced establishment, so that at 18°C it was reduced by about 30 % after one week. A continuous loss of P . laevis was seen through the course of the experiments, the rate of which was independent of worm numbers and temperature, but which increased when the host fishes were starved. Figure 10 shows a model proposed by Kennedy (1972b) to illustrate the flow paths and control mechanisms relevant to an endoparasite-host system such as that of P . laevis and its fish hosts. In field conditions Kennedy (1972b) postulated that reduced establishment of P . laevis during summer high water temperature conditions would be compensated by increased host feeding activity, so that the overall effect would be to even out seasonal variations and provide more or less steady establishment and recruitment into the worm population throughout the year. Diet Host A response

I Unestablished

1

01utput

r\

J

FIG.10. A model of a non-seasonal endoparasite-host system showing the flow paths and control mechanisms. The symbols +ve and -ve refer to correlations with temperature. (From Kennedy (1972b). Fig. 6, p. 292.)

Further discussion of the events in the annual calendar of Pomphorhynchus laevis was provided by Kennedy (1972~).The pattern of population change in the River Avon Gammaruspulex was a consequence of population cycles in the definitive host. Since P . laevis in its definitive host fishes produced shelled acanthors throughout the year, and the two generations of G . pulex each year overlapped, the amphipods were infected with all larval stages of the acanthocephalan at all times of the year. There was, however, a decrease in the incidence and intensity of infection of the amphipods during summer, .owing to an increase in the populations of young Gammarus at this time, and an increase in autumn, subsequent to the increase in numbers of mature female

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P. Iaevis in Leuciscus cephalus producing invasive shelled acanthors in summer (see Hine, 1970; Kennedy, 1972~). According to Kennedy (1972~)most parasites which became established in the definitive fish host appeared to survive to maturity and die naturally. The host reaction to the Pomphorhynchus laevis was primarily local at the point of attachment of the worm, although P. laevis was able to provoke antibody production (discussed further below). Neither response was able to eliminate the acanthocephalans from the intestine of the fishes. Cystacanths were ingested throughout the year, and the rate of recruitment must have been more or less equal to that of mortality in order to maintain the stable population. Kennedy (1972~)suggested that the major control of recruitment rate, and hence of the flow of parasites through the system (see Fig. lo), was the host diet, and only in so far as temperature or host condition influenced this did it affect the system. Kennedy (1974) subsequently examined the importance of mortality of Pomphorhynchus laevis in regulating population size of the acanthocephalan in Carassius auratus. He concluded that the parasite mortality did not function as a feedback control and so was relatively unimportant in regulating population size of this acanthocephalan. Both field and laboratory studies suggested that population size was largely determined by factors influencing recruitment. Hine and Kennedy (1974b) provided details of the population biology of Pomphorhynchus laevis in the River Avon. Much of the relevant data has been presented above, but they stressed the state of dynamic equilibrium and gain and loss of parasites which took place throughout the year, with the level of infection at any moment being determined primarily by the feeding behaviour of the host. They supported the hypothesis of Chubb (1964a) that temperature played a major part in determining the presence or absence of a well-defined periodicity of development and occurrence of fish acanthocephalans. The biology of Pomphorhynchus laevis in Cottus gobio from the River Avon was revealed by Rumpus (1975). In essence it conformed to the pattern found for the majority of fish species in the river. Only two gravid P . laevis were seen, in April and June, so that C. gobio was not a principal definitive host. Otherwise, the population structure was stable all year, owing to constant availability of cystacanths from Gammarus pufex. A drop in occurrence of P. laevis in the largest fishes was attributed by Rumpus (1975) to a change in their feeding away from G .pulex. Kennedy (1972~)and Kennedy and Rumpus (1977) observed that in the nine year period, 1966 to 1974, the population size of Pomphorhync~u~ Iaevis in the fishes of the River Avon had not changed to any great extent. It was noted above that antibody production in fishes was stimulated by Pomphorhynchus laevis. Harris (1970, 1972) showed that Leuciscus cephalus produced precipitating antibody in response to natural and experimental infections, although resistance was not manifest. Harris (1970) was of the opinion that it was unlikely that they gave any degree of resistance tp either current infections or further invasions by the acanthocephalans. The production of the precipitins was possibly stimulated by the great degree of pene-

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tration of the proboscis and proboscis bulb into the intestinal wall of the L. cephalus. The production of skin-sensitizing antibody by L. cephalus in response to antigenic extracts of P. laevis could not be demonstrated by either homologous or heterologous passive cutaneous anaphylaxis, the latter reaction using guinea-pigs (Harris, 1973). Van Maren (1979a) has recently reported on the biology of the larval stages of Pomphorhynchus Iaevis in Gummarusfossarum from the River Ain, France. The acanthellae and cystacanths were most abundant September (7 %) with a smaller peak in March (2%) and present in lower numbers (less than 1 % incidence) from April to August. Adult P. laevis were seen in Barbus barbus from the River Albarine and Thymallus thymaltus from the River Ain. The acanthocephalans were largest in B. barbus, and in T. thymallus hardly any female worms were mature. The numbers of P. laevis in T. thymallus were minimal during summer, but in spring and autumn more than 250 were counted in some fishes. These occurrences could be related to feeding on aerial insects during summer, and mostly G .fossarum during the autumn, at which time from 17 to 48 cystacanth larvae were found in the fish stomachs (Van Maren, 1979a). Pomphorhynchus rocci Cordonnier and Ward, 1967 A seasonal incidence of larval stages in Gammurus daiberi and G . tigrinus in estuarine conditions in North Carolina, U S A . , has been briefly reported by Johnson (1 975). STUDIES IN WORLD CLIMATIC ZONES IV. SEASONAL

The map showing the zones used in this review and the arguments for the division of the data about seasonal studies of helminth parasites into world climatic zones have already been given in Chubb (1977), with a further comment in Section IV of Chubb (1979). Tables 1-111 (Cestoda), Table IV (Nematoda) and Table V (Acanthocephala) list the studies on seasonal occurrence of adult helminths in the world climate zones. A.

TROPICAL (CLIMATE ZONE

1)

As seen also in the earlier parts of this review, there is a scarcity of information about seasonal patterns of occurrence of helminths of freshwater fishes in the tropical parts of the world. Stromberg and Crites (1974b) have suggested that the nematode Family Camallanidae was of highest diversity and degree of specialization in tropical areas. Their distribution pattern suggested that the family originated in the Old World tropics, spread to the New World tropics, and there underwent a radiation of species, the extent of which was still not fully known. Stromberg and Crites (1974b) considered that in tropical climates where water temperatures remained high all year, populations of copepods did not fluctuate to a

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large degree. They indicated that analysis of Moorthy’s (1938) data for Paracamallanus sweeti (here as Camallanus sweeti, see Section IV A 1) in India suggested that this species was reproducing more or less continuously since the population was apparently in a state of constant turnover. No estimate was possible on the length of time for one generation, although this information was available for Camallanus lacustris (see Moravec, 1969 and p. 129). Continuously reproducing camallanids were limited in their production of young only by the capacity of their reproductive organs. Large numbers of young necessary to ensure completion of the life cycle might be produced continuously in the ovary, to develop within the uterus and be released; such a process might continue for the entire reproductive life of the female. According to Stromberg and Crites (1974b) the continuous abundance of copepods in tropical climates would allow the camallanid cycling to go on constantly, with a high likelihood that some larvae would complete their growth to maturity. Supporting evidence for this view is provided by the studies of Camallanus cotti, C. fotedari and C. moraveci in tropical aquarium fishes (see p. 135), where a complete life cycle can be completed in about ten weeks, and where up to three successive generations have been obtained experimentally in constant aquarium conditions (Campana-Rouget et a]., 1976). 1. Rainy (Climate zone la)

Some information is available for six species, Lytocestus lativitellarium,

L.parvulus (Cestoda), Camallanus sweeti, Procamallanus clarias, P. parvulus (Nematoda) and Pallisentis nagpurensis (Acanthocephala). An indication of some seasonality of occurrence was noted for L. lativitellarium, L. parvulus, P. clarias and P. parvulus, perhaps related to changes in abundance of the intermediate hosts, or of their occurrence in the diet of the host fishes (Furtado and Tan, 1973), although apart from L. lativitellarium which was not found in May, the other three species were present at fairly high levels of incidence and intensity dlrring the period of investigation, May to November. Both C. sweeti and P.nagpurensis potentially could occur and reproduce at all times of the year, but actual seasonal observations to confirm this fact were not carried out by the respective authors, Moorthy (1938) and George and Nadakal (I 973). 2. Savanna (Climate zone lb)

Three species have been investigated in this climate zone, Lytocestus indicus (Cestoda), Acanthogyrus indica and A. tilapiae (Acanthocephala). With L. indicus Satpute and Agarwal (1974) observed some indications of seasonality of incidence and maturation. Mostly mature cestodes were seen from April to July. Pal (1 963) found a complete absence of A . indica from the fish Hilsa ilisha during the monsoon months July and August, but this could have been a reflection of the fact that these hosts were migratory, and therefore other factors could be operative. However, Shotter (1974) noted that in both

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20 1

lake and river Tilapia zillii at Zaria, Northern Nigeria, highest incidences of A . tilapiae occurred November to February, and the lowest in June and July. The maximum infections coincided with the middle of the dry season, October to June, when the waters of both lake and river were at their coolest and shallowest. Shotter (1974) suggested that these conditions increased the proximity of the intermediate hosts (unknown) and the T. zillii, thereby favouring heavier infections. Podder (1937) reported that the fish Polynemus heptadactylus was sold in Calcutta market, India from February to August. Neoechinorhynchus topseyi (Acanthocephala) infected these fishes particularly during May to July. 3.

Highland (Climate zone 1c)

Bothriocephalus (Clestobothrium) kivuensis Baer and Fain, 1958 (Cestoda) was reported by Baer and Fain, 1960 from Barbus altianalis altianalis from Lake Kivu, Congo (now Zaire), in November. Eggs from the gravid worms hatched at 20-25°C and copepods were infected, but the larvae from the copepods would not invade Tilapia species or Carassius auratus. In temperate climate zones some other species of Bothriocephalus (see for instance, 3. claviceps p. 55) can occur and reproduce at all seasons, but unfortunately no actual evidence for this has so far been collected for the genus from tropical climate zones (see below Section IV A 5, Bothriocephalus aegyptiacus). 4.

Semi-desert (Climate zone Id)

No seasonal studies of adult cestodes, nematodes or acanthocephalans are known to the author from this climate zone. 5.

Desert (Climate zone 1e)

RySavf and Moravec (1 975) described Bothriocephalus aegyptiacus from Barbus bynni from the River Nile, Egypt. In cestodes collected March and May eggs were present, so that they studied the life cycle, obtaining procercoids in Mesocyclops leuckarti in 8-10 days post-infection at 22-24°C. Unfortunately no seasonal information is available. However, Moravec (1975) also studied the life cycle of the nematode Procamallanus laeviconchus from Clarias lazera originating from the River Nile. In this instance he quoted Iman (1971, original not seen) as having found a considerable increase in incidence of P. laeviconchus in the definitive host fishes at the end of spring and summer. In conclusion, it may be suggested that although in theory high water temperatures year round in tropical conditions might allow continuous reproduction of fish helminths in practice the small amount of seasonal data so far collected indicates that, notwithstanding the possibility of constant reproduction, some changes in occurrence of these parasites do occur, so that it is likely that factors other than water temperature are involved. Clearly, there are great opportunities for critical and extensive seasonal investigations of fish helminths in the tropics.

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JAMES C . C H U B B B. SUBTROPICAL (CLIMATE ZONE

I.

2)

Mediterranean (Climate zone 2a)

Information for this climate zone is available for seven species of cestodes, six of nematodes and three of acanthocephalans. KaiiC (1970) and KaiiC et al. (1977) have provided information about the following species from Lake Skadar, Yugoslavia: Bothriocephalus claviceps, Caryophyllaeides fennica, Caryophyllaeus laticeps, Proteocephalus macrocephalus, Proteocephalus species juveniles, Contracaecum aduncum, Goezia ascaroides, Philometra ovata, Raphidascaris acus, Echinorhynchus truttae and Pomphorhynchus bosniacus. In most instances the patterns of occurrence were essentially similar to those for the same species in mid-latitude climate zones. The following examples are given: the cestode B. claviceps in Anguilla anguilla showed no evidence of a clear pattern of seasonality of maturation, although incidence was maximal in summer. The lack of a clear pattern o f seasonality conforms with observations elsewhere (see p. 55). By contast C. laticeps showed a clear pattern: immature worms were present November to January and March-April. Adult C. laticeps increased from January, peaked April, declined May to July to disappear thereafter. Such a pattern was similar to that seen for this cestode in some host fishes and habitats in niid-latitude climate zones (see for instance, Kennedy, 1968, p. 13). Some of the nematodes provided clear indications of seasonal maturation : C. aduncum juvenile April-May, mature April-May, gone June, but larvae were present all year; G. ascaroides, immature July, August (peak) and September, mature peaking October, falling November; and R. acus, larvae in cyprinids all months, juveniles in the intestine lumen of A . anguilla December to April, disappearing concurrently with the appearancc of mature worms January, March to July, peaking June. One generation per annum of R. acus apparently occurred (see p. 124). The acanthocephalan E. truttae was present in A . anguilla December to June, but not July to November. This contrasts strongly with its continuous high incidence in Salmo trutta in climate zone 3b (see Awachie, 1965, pp. 192, and Section IV C 4). Cernova (1975) observed Caryophyllaeides fennica and Capillaria petrusclzewskiiin Rutilus rutilus from Lake Paleostomi, and Raphidascaris acus from Lake Dzhapana, Georgia, U.S.S.R., but low occurrences preclude any useful contrast with data from mid-latitude climate zones. However, Triaenophorus meridionalis in Esox lucius in Lake Dzhapana showed the usual distinct maturation pattern seen in this genus of cestodes (see pp. 56-63). Paggi et al. (1978) have given preliminary notice that they have studied seasonal occurrence of Cyathocephalus truncatus, Truttaedacnitis truttae and Dentitruncus truttae in Salmo trutta from the River Tirino, L’Aquila, Italy, which falls within this climate zone. However, full details have not been seen at the time of writing this review. Much experimental information concerning the cestode Proteocephalus turnidocolluswas provided by Wagner (1 953, 1954) from studies carried out in California, U.S.A. Unfortunately, no comparative studies have been carried out on this species in any other climate zone.

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2. Humid (Climate zone 2b) Varying levels of data for nine species of helminths, six cestodes, two nematodes and one acanthocephalan, are pertinent to climate zone 2b. For two of these species, Biacetabulum meridianum and Glaridacris conjiusus there was inconclusive evidence that infections were heavier during the spring months (Self and Timmons, 1965). Eure and Esch (1974) reported that adults of Bothriocephalus cuspidatus in South Carolina, U.S.A., were most common in winter, in unheated areas of Par Pond, but unfortunately (see p. 55) there is little information from other climate zones with which to contrast this observation. McDaniel and Bailey (1974) and Davis and Huffman (1978) both reported that the nematode Spinitectus carolini was of maximal occurrence in fishes during summer in this climate zone. According to McDaniel and Bailey (1974) a secondary peak of presence occurred in the winter. Mature adults began to appear in early spring. Once again, there are few data for comparison from other climate zones. Precise evidence for seasonal changes in the biology of the cestodes Bothriocephalus acheilognathi and Proteocephalus ambloplitis, the nematode Philometroides carassii and the acanthocephalan Neoechinorhynchus cylindratus have been provided by studies in this climate zone. Although B. acheilognathi produced eggs in Kwangtung Province, China, all year, the percentage embryonated on release was low November to February, and high April to October (Liao and Shih, 1956, see p. 43). Esch et ul. (1975) and Eure (1976a) presented details concerning P . umbIoplitis at Par Pond, Savannah River Plant, South Carolina, U.S.A. Details of their studies have already been given (see pp. 83-84), and they areof especial interest because of the comparison of observations between this climate zone, and that of zone 3aii. In this zone the seasonal peak of enteric adults was from mid-winter onwards. At Par Pond the appearance of the adult P. ambloplitis coincided with a decrease in water temperature, whilst the appearances of adult tapeworms in Michigan and Ontario were coincident with increases in water temperatures (Eure, 1976a; Esch et al., 1975; Fischer and Freeman, 1969). Philometroides carassii from Carassius auratm became gravid in Japan in early spring (Nakajima and Egusa, 1977c) and were transmitted to copepod intermediate hosts at that time (Nakajima and Egusa, 1977e). Neoechinorhynchus cylindratus was also investigated at Par Pond, South Carolina, U.S.A. Eure (1976b) in this instance stressed the differences in seasonal patterns between the thermally polluted reservoir and unheated areas. The comparison was considered in depth earlier (p. 161), but in summary, recruitment occurred primarily in autumn, maturation overwinter, with gravid worms in spring, followed by the loss of the gravid population. The main effect of the heated waters was to increase the intensity of infection of the fishes, owing to changes in the fish feeding behaviour (Eure, 1976b). Kataoka and Monma (1934) provided some information concerning Proteocephalus plecoglossi from the region of Japan falling within this climate zone. Invasion of fry of the host Plecoglossus altivelis commenced before December, and gravid worms were seen in May.

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c.

MID-LATITUDE(CLIMATE ZONE 3)

1. Humid warm summers (Climate zone 3ai)

This climate zone is one of the three (3ai, 3aii and 3b) in which the majority of seasonal investigations of adult cestodes, nematodes and acanthocephalans have been carried out. In climate zone 3ai the following numbers of species have been examined: Cestoda, 37; Nematoda, 31 ; and Acanthocephala, 17. Naturally, the levels of available information vary greatly between species. Each group will be discussed separately. Only small amounts of relevant data were available for nine of the species of cestodes studied in this climate zone : Amphilina foliacea (KakachevaAvramova, 1977), Bothriocephalus claviceps (Sramek, 1901; KakachevaAvramova, 1977), B. cuspidatus (Cloutman, 1975), Proteocephalus exiguus (Kuczkowski, 1925), P. .fallax (Kraemer, 1892), P. jilicollis (Kuczkowski, 1925), P. longicollis (Kozicka, 1949), P. torulosus (Zschokke, 1884; Srimek, 1901 ; Wagner, 1917; Kakacheva-Avramova, 1977) and Silurotaenia siluri (Kakacheva-Avramova, 1977). Accordingly, it is currently impossible to indicate their patterns of occurrence in the zone. Three species were present in their respective fish hosts all (or most) of the year, but growth and maturation data were not provided : Caryophyllaeides fennica (Marits and Vladimirov, 1969,Kakacheva-Avramova, 1973,1977,present spring, summer and autumn), Caryophyllaeus brachycollis (Kakacheva-Avramova, 1973, present spring, summer, autumn) and C. jimbriceps (Ivasik, 1953, present all year, maximal spring and summer). A small number of the cestode species in climate zone 3ai were found to be present in their fish hosts for limited periods of the year. Thus Archigetes brachyurus was seen in Vimba vimba vimba natio carinata in spring only (2.2 %) (Marits and Vladimirov, 1969). Kulakovskaya (1962a) agreed that it was very rare to find A. brachyurus in fishes. A. sieboldi was also recovered from fishes at limited times, mostly April to early June (Kulakovskaya, 1962a, b, 1964a), although Kakacheva-Avramova (1 973) noted one specimen during autumn. Khawia sinensis overwintered in fishes in the Ukraine, U.S.S.R. (Kulakovskaya, 1964b), but showed a distinct seasonal incidence in Cyprinus carpio, occurring mainly May and June (Kulakovskaya et al., 1965). In Erimyzon oblongus in North Carolina, U.S.A., Grimes and Miller (1973, 1976) observed that Monobothrium ulmeri was present from December to July, an infection period of eight months. During this time invasion, growth, maturation and egg production and ultimately senescence occurred. A similar sequence of events was seen by Grimaldi (1964) for a Proteocephalus species in Coregonus lavaretus in Lake Maggiore, Italy. Here invasion commenced in May, the cestode population attaining a maximum during summer, declining overwinter to nothing during March and April. The last three species merge towards the next and major category of cestodes found in this climate zone, those seen to be present in the host fishes throughout the year.

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Caryophyllaeus laticeps actually spans the overlap, in that in some situations it occurred in fishes for only part of the year, whereas in others, the majority in this climate zone, it was present all year. Thus Wunder (1939) found C. Iaticeps in Cyprinus carpi0 in fish ponds April to August only, with maximal intensities April to June, whereas Milbrink (1975) in Abramis brama from Lake Malaren, Sweden, observed continuous incidences over a four year period, although with peaks of infection in spring and autumn each year. Clearly circumstancesin each respective habitat or host can modify the seasonal patterns of occurrence. Within the cestode species found to be present in their definitive fish hosts throughout the year in climate zone 3ai two broad subdivisions can be recognized. In the first some of the individuals of the population contain eggs at all times of the year; in the second the reproductive activity of the population is limited to a particular period, usually spring or summer. The first category includes Biacetabulum biloculoides (Mackiewicz and McCrae, 1965, gravid worms found all months sampled), perhaps Cyathocephalus truncatus (WiSniewski, 1932a, 1933a), and Penarchigetes species (Grimes and Miller, 1973, 1976). The second subdivision covers Bathybothrium rectangulum (Kulakovskaya, 1959, gravid May to July, according to altitude), Biacetabulum rneridianum (Grimes and Miller, 1973, 1976, gravid late spring, summer), Bothriocephalus acheilognathi (MolnBr, 1968b, gravid April to December; Korting, 1975a, gravid worms most numerous April; and Davydov, 1978, gravid mainly spring and summer), CorallobothriumJimbriatum(Essex, 1927, gravid late spring and early summer; Spall and Summerfelt, 1969, late winter and spring; and Edwards et al., 1977, summer), C. giganteum (Essex, 1927, gravid late spring and early summer; Spall and Summerfelt, 1969, late winter and spring; and Edwards et al., 1977,summer), Eubothrium crassum, freshwater race (Zschokke, 1884, gravid February onward; Rosen, 1919, end of March t o August; and Nybelin, 1922, May and July), E. rugosum (Nybelin, 1922, gravid January, April-May), Proteocephalus cernua (Molnhr, 1966a, gravid spring to July, October), P . dubius (Zschokke, 1884, gravid July-August), P . percae (Molniir, 1966a, gravid spring to July), P . stizostethi (Connor, 1953, gravid late spring, early summer), Triaenophorus crassus (Michajlow, 1932, gravid May), T. meridionalis (Kuperman, 1965, gravid spring) and T. nodulosus (Rosen, 1919, gravid end February to end of June; Nybelin, 1922, FebruaryMay; Fuhrmann, 1926, end February to end of June; Scheuring, 1929, winter to June; Michajlow, 1933, 1951, mid-November to mid-May, or June; Engelbrecht, 1963, gravid proglottids lost, freshwaters March-April, brackish waters May-June; and Moravec, 1979b, worms with eggs present October to April). The seasonal patterns of occurrence of the nematode species investigated in climate zone 3ai can be divided into groups in a manner similar to the cestodes. Insufficient data are available for the following: Contracaecum bidentatum (Kakacheva-Avramova, 1977), Cucullanus dogieli (Marits and Vladimirov, 1969), Dichelyne robustus (Spall and Summerfelt, 1969),Esocinema bohernicum (Moravec, 1979b), Paraquimperia tenerrima (Moravec, 1974),

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Rhabdochona ergensi (Moravec, 1972), R . hellichi (Kakacheva-Avramova, 1973,1977), Rhabdochona species (Kakacheva-Avramova, 1977), SkrjabillQnus scardinii (Moravec, 197%) and Truttaedacnitis sphaerocephala (KakachevaAvramova, 1977). No maturation data were collected for Rhabdochona cascadilla and R. decaturensis (Spall and Summerfelt, 1969), R. denudata (Kakacheva-Avramova, 1973, 1977), Spinitectus carolini (Holl, 1932; Spa11 and Summerfelt, 1969; Cloutman, 1975)and S. gracilis (Spall and Summerfelt, 1969) although all these nematodes were present during all the year, or seasons sampled. However, Gruninger et al. (1977) observed the presence of R. decaturensis mainly during summer and autumn, contrary to the lack of significant seasonal changes seen by Spall and Summerfelt (1969). The remaining nematode species were present in the fish hosts all year. Reproduction of Camallanus lacustris was considered to be in late winter and spring by Tornquist (193l), but Moravec (1 979b) found invasion and reproduction year round, although the warmer seasons, spring to autumn, were more favourable for development of the parasite. Camallanus truncatus (see Molnhr, 1966a)and Capillariapetruschewskii (see MolnLr, 1968b)probably reproduced through the year too, with warmer conditions speedingthe rate of development. Molnilr (1976), Moravec and DykovL (1978) and Moravec (1979b) found larvae and females with eggs and mature larvae of Philometra obturans in Esox lucius during all the year. This contrasts strongly with the situation seen in the other species of Philometra and Philometroides from climate zone 3ai (see below), and was attributed to the reservoir hosts existing in the life cycle of P. obturans (Moravec and DykovL, 1978). Reproduction of the remaining species was seasonally limited :in Camallanus oxycephalus one generation per annum, mature in spring and early summer (Spall and Summerfelt, 1969), adults released larvae July-August (Stromberg and Crites, 1975b); in Cystidicoloides tenuissima two generations each year in this zone, a main spring one and a smaller autumn generation (Moravec, 1971~);one generation in each of the philometrid species, Philometra abdominalis, larvae released second half June to first half of September, dependingon water temperature (Moravec, 1977b); P. fujimotoi, larvae released early summer, to June (Furuyama, 1934); P. kotlani, larvae released exclusively May (Molnhr, 1969a); P. ovata, larvae released only during last days of May and first in June (Molnhr, 1966b); P . rischta, larvae released end of May, early June (Molnar, 1966b); Philometroides cyprini, larvae released spring (Vasil’kov, 1964); Ph. sanguinea, larvae released from 25 May to 25 June (Yashchuk, 1975);Raphidascaris acus, one generation per annum, adults producing eg s May and June (Moravec, 1970b, 1979b), ovipositing July and August (fitfian, 1973); Iihabdochona phoxini, eggs laid end of spring and start of summer (Moravec, 1977a); and Truttaedacnitis truttae, eggs hatch on stream bed late April and early May (Pybus et al., 1978b). The acanthocephalans also may be subdivided. Insufficient information to allow conclusions for this climate zone was available for Acanthocephalus tenuirostris (Kakacheva-Avramova, 1973), Echinorhynchus salmonis (Kakacheva-Avramova, 1977), Fessisentisfriedi (Fried et el., 1964),Leptorhynchoides

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207

plagicephalus (Kakacheva-Avramova, 1977), Pomphorhynchus bosniacus (Kakacheva-Avramova, 1973) and P . rocci (Johnson, 1975). Acanthocephalus dirus (Camp, 1977), Echinorhynchus truttae (Ivasik, 1972), Neoechinorhynchus cylindratus (Pearse, 1924; Cloutman, 1975) and Pomphorhynchus laevis (Zschokke, 1884;Molnhr, 1968b; Kakacheva-Avramova, 1973) were present in fishes all year, but detailed maturity data were not presented by the respective authors. More details were provided for the remaining species of acanthocephalans studied in climate zone 3ai. Acanthocephalus jacksoni appeared in the fishes from November until July, with shelled acanthors present January to July. No worms were seen in the definitive hosts August to October. A short survival time for the adult worms in the fishes was postulated (Muzzall and Rabalais, 1975a). In the instance of Gracilisentis gracilisentis the fishes were free from parasites June to August. Thus Van Cleave (1916) found that invasion commenced September onward, maturation overwinter, with gravid worms occurringApril-May, whichwerelost shortly afterwards. Jilek (1978b) recorded a similar timing and sequence of events for G . gracilisentis in this climate zone. Tanaorhamphus longirostris also showed a periodicity of occurrence and maturation ; invasion was seen during summer (June and July), gravid worms in August, November and December, the fish host being free of infection late winter to early summer (Van Cleave, 1916). In this latter instance Jilek (1978b) found a rather different timing, even though both studies were in Illinois, U.S.A. : immature adults occurred in March only, with sexually mature T. Zongirostris from the later part of March through summer to August. No worms were seen thereafter until the following March. Variations in pattern of occurreqe of Neoechinorhynchus rutili within climate zone 3ai are also evident. Zitiian (1973) found high incidences (5045%) in each of his bimonthly samples of Phoxinusphoxinus, whereas TesarCik (1970,1972) observed that in fish ponds Cyprinus carpio were invaded in spring, with shelled acanthor release from 4 March to 29 July. It may be suggested that different patterns occur in natural as compared with artificial habitats. Acanthocephalus lucii was present year round in the fishes (Ivasik, 1953; Moravec, 1979b), although maximum infection in Esox Zucius was April-May and minimal July-August (Moravec, 1979b). Shelled acanthors were seen almost through the year (not December), although again peaks were evident May-June and September-October. Moravec (1979b) stressed that these peaks did not represent two generations : rather occurrence and maturation showed partial seasonal quantitative changes apparently evoked by variations in availability of intermediate hosts and water temperatures. A . anguillae was perhaps also present in fishes year through (Sramek, 1901), although Andryuk (1974a) suggested that invasion of fishes occurred in spring, with the intermediate hosts Asellus aquaticus becoming invaded in autumn. More information is needed here. Paulisentis missouriensis was collected by Keppner (1974) June 1971 to November 1972 and was present 1 to 28 worms per host through the entire study period. Immature and mature worms occurred together during summer.

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2. Humid cool summers (Climate zone 3aii) Some 45 species of cestodes, 16 of nematodes and 7 of acanthocephalans have been examined for various aspects of their seasonal biology in climate zone 3aii. In the light of the discussions in the previous parts of Section IV it is no surprise that a variety of different patterns of occurrence and maturation were evident. Insufficient information within this zone is available for the cestodes Bothriocephalus cuspidatus (Pearse, 1924; Essex, 1928), Caryophyllaeides fennica (Izyumova, 1959a, 1960), Cyathocephalus truncatus (Bauer, 1959a), Eubothrium salvelini (MacLuIich, 1943;Amin, 1977), Khawia iowensis (Calentine and Ulmer, 1961b), Monobothrium wageneri (Komarova, 1957), Proteocephalus ambiguus (Schneider, 1902), P. cernua (Izyumova, 1959a), P. exiguus (Bauer and Nikol'skaya, 1957; Amin, 1977), P. jilicollis (Banina and Isakov, 1972) and P. torulosus (Izyumova, 1960). The following were present in fish intestines all year, but maturation data were not given: Eubothrium crassum, marine Atlantic race (Zschokke, 1891), Isoglaridacris folius (Fredrickson and Ulmer, 1965), Proteocephalus esocis (Izyumova, 1960; Rautskis, 1970b), P. pearsei (Pearse, 1924; Tedla and Fernando, 1969; Cannon, 1973) and P. percae (Izyumova, 1958,1959a; Rautskis, 1970a). Cestodes of six caryophyllaeid species showed very limited periodicity of occurrence in their fish definitive hosts in zone 3aii. Thus, Archigetes iowensis was present in Cyprinus carpio April to Jube only, gravid worms late April, maximal late May (Calentine, 1964), A. sieboldi rare in fishes, one only (gravid) recovered April-May (Calentine and De Long, 1966), Biacetabulum carpiodi in Carpiodes cyprinus spring to July (Williams and Ulmer, 1970), B. infrequens in Moxostoma anisurum and M , erythrurum summer only as gravid worms (Calentine, 1965a),B. macrocephalum in Catostomus commersoni, immature individuals from late sping, gravid June to August only (Calentine and Fredrickson, 1965)and Monobothrium hunteri in C. commersoni, immature from late spring, gravid May to July (Calentine and Fredrickson, 1965). At other times these cestodes were present in the respective habitats either as eggs or in the oligochaete intermediate hosts. One other species, a proteocephalid Proteocephalus ambloplitis, also showed limited periodicity of occurrence in this climate zone. Fischer and Freeman (1969) observed adult worms in Micropterus dolomieui March to September only, with gravid worms shedding eggs June to September. Esch et al. (1975), at Gull Lake, Michigan, U.S.A., in climate zone 3aii, in addition found enteric P. ambloplitis in M . dolomieui from about mid-May until October, when sampling ceased. Gravid worms occurred from between 20-28 May until October, but from August their occurrence was declining. It was noted previously (p. 203, climate zone 2b) that in the warmer conditions of Par Pond the enteric adults were present earlier, from December to August (Eure, 1976a). The remaining species of cestodes scrutinized in climate zone 3aii were present in the intestines of their definitive hosts all year. Many of these were in a reproductive condition year through, although activity was enhanced during the spring and early summer months. This group included: Atracto-

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lytocestus huronensis (Anthony, 1958; Jones and Mackiewicz, 1969); Caryophyllaeus fimbriceps (Kanaev, 1956; Bauer, 1957, 1959a); C. laticeps (Bogdanova, 1958, 1959; Izyumova, 1958, 1959b), although Lyubarskaya (1965, 1970) did not find it during autumn and Strizhak (1971) made a similar observation in a thermally polluted bay in the Ivan’kovsky Reservoir (absent October) ; Glaridacris laruei, although having a definite seasonal maximal incidence (Williams, 1979b) was also present all months ; Hunterella nodulosa (Calentine and Fredrickson, 1965); Isoglaridacris wisconsinensis (Williams, 1979a); Khawia sinensis (Sapozhnikov, 1970, 1972); and Spartoides wardi (Williams and Ulmer, 1970). Some of the above species showed a distinct major cycle of growth to a gravid condition, notwithstanding the presence of gravid individuals all though the year. Nine species were found with more limited seasonal occurrence of gravid or egg-shedding worms :Bothriocephalus acheilognathi gravid spring to autumn (Bauer et al., 1969); Corallobothrium minutium egg-shedding 7 June to 20 August and C . parajimbriatum 1 June to 11 September (Befus and Freeman, 1973); Glaridacris catostomi gravid January to June and Zsoglaridacris bulbocirrus June to August (Calentine and Fredrickson, 1965); I. Iongus gravid late April to November (Fredrickson and Ulmer, 1965); Proteocephalus jluviatitis egg-shedding mid-to late June to 15 October (Fischer, 1968); and P.para1lacticus gravid 20 May to 26 September (Freeman, 1964). Finally, a few species showed a more limited seasonal release of eggs : Eubothrium rugosum May (Tell, 1971); Proteocephalus buplanensis spring (Amin and Mackiewicz, 1977); Triaenophorus amurensis April-May (Kuperman, 1967b, 1973);T. crassus eggs containing embryos May (Ekbaum, 1937) and May, early June (Kuperman, 1973); T . nodulosus end April, particularly May and in early June (Kuperman, 1973);and T . orientalis April-June (Kuperman, 1967b, 1973). Information for nematodes in climate zone 3aii is less complete than for the cestodes. Insufficient data for a clear assessment of their seasonal biology exists for the following: Capillaria brevispicula (Bogdanova, 1958; Izyumova, 1960), Contracaecum bidentatum (Geller, 1957 ; Bogdanova, 1958), Cystidicola farionis (Bauer and Nikol’skaya, 1957), Philometra abdominalis (Bogdanova, 1958; Lyubarskaya, 1970), P . obturans (Izyumova, 1960; Rautskis, 1970b), P . ovata (Izyumova, 1958, 1960), P . rischta (Izyumova, 1959a) and Philometroides sanguinea (Lyubina, 1970). Four species are known to occur in their fish hosts all through the year, but details of maturation patterns are lacking: CamalZanus lacustris (Izyumova, 1958, 1959a, b, 1960,1964; Rautskis, 1970a, b, 1977), C. truncatus(Izyumova, 1958,1959a, b, 1960,1964), Dichelyne cotylophora (Cannon, 1973) and Spinitectus gracilis (Cannon, 1973). Evidence for a year long occurrence with a clear developmental and reproductive pattern was demonstrated for four species: Philometra cylindracea annual cycle, invasive larvae released June (Molnar and Fernando, 1975); Philometroides cyprini annual cycle, invasive larvae released May-June (Vasil’kov 1964, 1968b; Vismanis, 1967, 1970), Ph. huronensis annual cycle, invasive larvae released May and June (Uhazy, 1977a, b); and Raphidascaris acus one generation each year, gravid worms end April to beginning of June (Tell, 1971).

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The acanthocephalans have been studied in more detail in this zone. Insufficient data are available for one species, Neoechinorhynchus rutili (Izyumova, 1958, 1960). Two species occurred year round, but details of maturation in the wild were not provided : Acanthocephalus anguillae (Izyumova, 1958) and Pomphorhynchus Zaevis (Bogdanova, 1958). Echinorhynchus salmonis was found with shelled acanthors present in female worms at all seasons (Amin and Burrows, 1977), although with enhanced maturation during the warmer summer months (Tedla and Fernando, 1970; Amin and Burrows, 1977; Amin, 1978a) and at the host spawning season (Amin, 1978a). Acanthocephalus lucii was shown to have a well-defined maturation pattern, with gravid worms at the end of spring and summer (Komarova, 1950; Andryuk, 1974a), although worms were present all year (Komarova, 1950; Izyumova, 1958, 1959a, 1960; Markova, 1958; Rautskis, 1970a, b, 1977). Such a maturation cycle was also seen in A . parksidei where the mature worms were virtually absent from the definitive host fishes during summer, although in Semotilus atromaculatus A. parksidei were seen with shelled acanthors in September to November (Amin, 1975). In Leptorhynchoides thecatus no seasonality of occurrence was seen by Cannon (1973) probably owing to the low incidences, but De Giusti (1949) observed maximal occurrence spring to September, with declining numbers to February, with few found in fishes at that time. Maturation was concentrated into summer through to November (De Giusti, 1949). It is relevant to note here that Esch et al. (1976) in their live-box tether experiments carried out in climate zone 3aii and which extended from late June to mid-August observed maximal recruitment later during the period of observation. 3. East coast (Climate zone 3aiii) Ten species of cestodes, four of nematodes and 12 of acanthocephalans have been examined in climate zone 3aiii. Incomplete seasonal data are available for Bothriocephalus cuspidatus (Noble, 1970), Monobothrium hunteri (Mackiewicz, 1963) and Proteocephalus pinguis (Hunter, 1929), Glaridacris catostomi was present in fishes during all months except August, with evidence of maximal occurrence January-April (Lawrence, 1970). Gravid G. catostomi were found in February, April and May by Mackiewicz (1965b). Glaridacris laruei and Isoglaridacris bulbocirrus were present all year, with significantly greater numbers January-April as in G . catostomi, but maturation data were not provided (Lawrence, 1970). No seasonal distribution of Hunterella nodulosa was exhibited by the material collected by Mackiewicz and McCrae (1962) in this zone and also in climate zone 3c. Nakajima and Egusa (1977f) examined Cyprinus carpi0 from November to May. Khawia sinensis was present in declining numbers during November to December, but absent thereafter. They also studied Bothriocephalus acheilognathi. This cestode overwintered, but the incidence dropped after November. Eggs would hatch in November, but were absent during December to March: however once eggs were produced and laid again in April and May these eggs would hatch.

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In this cestode Nakajima and Egusa (1977a) suggested that overwintering of the species in their area was achieved only by the adult worms in the fish intestines. The embryo in the eggs died rapidly if exposed to water temperatures of 2-7°C (Nakajima and Egusa, 1976). Finally, for the cestodes scrutinized within climate zone 3aiii, Sandeman and Pippy (1967) observed Eubothrium salvelini at all seasons, but maturity of the specimens showed a seasonal variation. Mature worms were taken during spring and early summer, immature ones in late August, September and later in the year. The nematode Cystidicoloides tenuissima exhibited little evidence of seasonal occurrence in this zone. Non-gravid females dominated each monthly sample, but with gravid females most abundant May, June and November although some were present each month (Hare and Burt, 1975). This pattern was similar to that seen in Czechoslovakia (Climate zone 3ai) by Moravec (1971~).Kuzia (1979) observed that Dichelyne bullockiweregravid late spring, with recruitment back into the definitive host population during summer. A one generation annual cycle was also evident for Philometra species in Morone saxatilis, where the adults released first stage larvae during June (Bier et al., 1974), and for Philonema agubernaculum where peak first stage larval maturity was suspected as being coincident with the host spawning time, late September, early October (Meyer, 1960). At first sight there appears to be a reasonable number of observations concerning Acanthocephala in climate zone 3aiii, but in fact many of the species were only briefly noted in an abstract which provided no specific detail (Bullock, 1962a). These included Acanthocephalus species undetermined, Echinorhynchus species undetermined, Fessisentis friedi, Leptorhynchoides thecatus, Neoechinorhynchus saginatus, two undetermined species of Neoechinorhynchus and one of Octospinifer,Paratenuisentis ambiguus andPomphorhynchus bulbocolli. Mention of N . cylindratus in a seasonal context within this climate zone was made by Noble (1970). Muzzall (1978) speculated that F. friedi maturation might be related to that of the fish host, Esox americanus, as this was associated closely with the timing of the release of shelled acanthors into the environment and the appearance of a new generation of the isopod intermediate hosts Caecidotea commupzis. Lawrence (1970) observed P. bulbocolli to be in fishes year round, with significant increases in numbers during summer, but he provided no maturation data. However both Echinorhynchus lateralis (Sandeman and Pippy, 1967) and N. saginatus (Muzzall and Bullock, 1978) were present in their host fishes all year, with mature males and females of E. 1ateraZis present regularly at all times, and gravid female N. saginatus also present in all months except July and September 1975, July 1976 and September 1977. 4.

Marine west coast (Climate zone 3b)

Some 20 species of cestodes, 18 of nematodes and 6 of acanthocephalans have been scrutinized in climate zone 3b. More information is needed for the following cestodes which have been

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observed at limited times of the year: Monobothrium wageneri spring to autumn, no maturation data (Kozicka, 1959);Proteocephalus cernua MarchJune, July and October, ripe eggs April to October (Willemse, 1965, 1969); P . neglectus March-June, November-January, no maturation data (Aderounmu, personal communication), and, June-July only, no maturity data (Rahim, 1974);P . primaverus absent summer and autumn, present autumn and winter no information concerning maturation (Neiland, 1952); and Proteocephalus species undetermined spring and summer mature, gravid autumn on SaImo gairdneri (Arme and Ingham, 1972). At the time of writing this review no details of the well-defined seasonal cycle for Khawia species noted in cyprinids in L e h , Spain (Alvarez Pellitero et al., 1978b) have been seen. One cestode Archigetes sieboldi has been observed in fishes in climate zone 3b in April only (Wierzbicka, 1978). Nybelin (1962) experimentally demonstrated that A. sieboldi had a very short survival time in fish intestines, not more than 12 hours in most instances. More seasonaljnformation from fishes has been promised (Alvarez Pellitero, 1978a), but A . sieboldi is probably primarily a parasite of oligochaetes (WiSniewski, 1930). Some of the cestodes studied in this zone showed different patterns of seasonal occurrence according to locality and host fishes. Thus, for Caryophyllaeides fennica in cyprinids, Alvarez Pellitero et al. (1978a) in Spain claimed a well defined annual cycle with one generation per annum, whereas, by contrast Chubb(1961), Mishra(1966)andDavies(1967)inEngland observed no clear pattern of incidence, but with worms containing eggs year round. At Bogstad Lake, Norway, Borgstrom and Halvorsen (1968) collected C . fennica May to November (no worms seen January, February, April and July), but eggs were seen in June and August only. The limited egg production in Norway was attributed to the water temperature conditions of the habitat (Borgstrom and Halvorsen, 1968). Similar examples can be found for Caryophyllaeus laticeps. Again in Spain Alvarez Pellitero et al. (1 978a, b) found an annual cycle with one generation, cestodes present in cyprinids, especially Leuciscus cephalus cabeda December to July, with gravid worms in spring. An essentially similar pattern was seen by Kennedy (1968) from the River Avon, England, in L. leuciscus. The C. laticeps were present December to June, with gravid individuals January to July, peaking March-May. However, Mishra (1966) from the Shropshire Union Canal, England, in Rutilus rutilus observed C . laticeps in all months, but with gravid worms limited to May, whereas Davies (1967) from the River Lugg, England, in L. cephalus, L. leuciscus and R. rutilus noted low incidences during most months except Janaury, September and November, with worms containing eggs during all months the cestodes were present, and Anderson (1974a) in Abramis brama from a gravel pit, Essex, England, recovered gravid C . laticeps during all months of the year, with lower percentages of the population gravid during the cooler months, November to February, as compared with the warmer months June to September. Finally, in A . brama from the River Glomma, Norway, Halvorsen (1972) saw C. laticeps May to August only, with the percentage of gravid worms increasing from zero in May to 100 % in August.

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Similar variations in pattern of annual cycle have been seen in climate zone 3b for Proteocephalus jilicollis in Gasterosteus aculeatus. The classical investigation of Hopkins (1959) carried out in North Lanarkshire, Scotland, showed a clear pattern (see Fig. 5), with gravid worms present in June and July only. Somewhat similar patterns were seen in the Netherlands (Willemse, 1965, 1967, 1968) and Bunnefjorden, Norway (Rardland, 1979), although with gravid worms present for longer periods, respectively May-September and May-August. As a complete contrast to these studies showing clear seasonal maturation, Chappell (1969a) recovered gravid P . JiZicolIis during all his bimonthly samples through the year, the percentage of the population gravid varying from 31 % (March) to 48 % (September); even in January 39 % of the P . jilicollis were gravid. The causal factors involved in these differences of maturation will be considered in Section V (see p. 241). The majority of the species of cestodes investigated in this climate zone showed a plan of late summer through winter recruitment, with growth to maturation in late winter to give gravid worms during spring and summer. In some instances a clear one or two month gap between generations was observed, when the fish hosts were free of infection. Such was apparent in Cyathocephalus truncatus (Awachie, 1963a, 1966a), Proteocephalus percae (Wierzbicki, 1971 ; Halvorsen, 1972; Andersen, 1978; Priemer, 1979), P. torulosus (Davies, 1967; Kennedy and Hine, 1969) and Proteocephalus species undetermined (Lien and Borgstrom, 1973). However, this gap can be bridged by new invasions of juvenile worms, as occurred on occasion in some of the aforementioned habitats, and normally in others for P. percae (Rizvi, 1964; Mishra, 1966; Wierzbicki, 1970; Wootten, 1974; Lee, 1977) and P . torulosus (Wierzbicka, 1978). Eubothrium rugosum was seen to develop overwinter and become gravid January and April-May, but no information was collected thereafter (Nybelin, 1922). Proteocephalus tetrastomus was present during all months with an annual cycle culminating in gravid worms in early summer (Willemse, 1965, 1967, 1969). Distinct times of maturation were not evident for Bothriocephalus claviceps (Chubb, 1961), Eubothriurn crassurn freshwater race (Wootten, 1972), Proteocephalus ambiguus (Willemse, 1965, 1968) and perhaps also P. macrocephalus (Willemse, 1969). In these instances recruitment may occur all year with progressive growth to maturity thereafter. In Triaenophorus nodulosus Chubb (1963a), Rizvi (1964) and Borgstrom (1970) found that plerocercoids were recruited into the intestines of Esox lucius at all times of the year. Nonetheless a well defined cycle of growth and maturation was seen (Chubb, 1963a, see Fig. 4; Rizvi, 1964; Borgstrom, 1970; Halvorsen, 1972). Chubb (1963a) thus showed that there was a dynamic balance between gain of plerocercoids from the intermediate host Perca fluviafilus taken as food and loss of adults from the intestines of E. lucius, the result being a more or less constant intensity of infection in E. lucius of given length year round. The maturation cycle proceeded notwithstanding the dynamics of invasion and rejection of T .nodulosus. Insufficient data have been collected for conclusions concerning the season-

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ality of the nematodes Camallanus truncatus (Priemer, 1979) and Paraquimperia tenerrima (Chubb, 1961) in climate zone 3b. Although present all year, no details of maturation were made available for Capillaria salvelini (Aderounmu, personal communication ; Awachie, 1963a; Campbell, 1974) and Cystidicola farionis (Aderounmu, personal communication; Awachie, 1963a, 1973b; Rahim, 1974), hence no conclusions are possible. Only one nematode in climate zone 3b is known to reproduce throughout all seasons. Camallanus lacustris was present all year and with all stages of maturation also occurring in five habitats distributed through the zone, in Britain (Mishra, 1966; Andrews, 1977; Lee, 1977), in Norway (Andersen, 1978) and in Poland (Wierzbicki, 1970). All the nematodes inhabiting the somatic tissues studied in climate zone 3b had one generation per annum. Capillaria acerinae, a parasite of the liver of Gymnocephalus cernua, was present in the fishes January to October, the percentage of adults in the population increasing from 3.8 % in March-April to 100% by October (Thieme, 1964). The transmission of Phifometra ovata and P. rischta occurred in spring (Wierzbicka, 1978) and of Philometroides sanguinea in June (Wierzbicki, 1960). Three species inhabiting the gut lumen of their respective hosts, Rhabdochona denudata, R. gnedini (Alvarez Pellitero et al., 1978a; Pereira Bueno, 1978) and R. sulaki (Cordero del Campillo and Alvarez Pellitero, 1976a) were claimed to have only one generation of adults per annum. Recruitment to the fishes was maximal for R. denudata during September-December, with maximal numbers of adults in spring and early summer, although some were present in most months of the year. R. gnedini had a maximum recruitment period of November to March, with a rapid development in the numbers of adults in March-April (Pereira Bueno, 1978). Two generations of adults each year, a major one in spring and a minor one during autumn were seen in four species of gut nematodes from climate zone 3b: Capillaria coregoni (Alvarez Pellitero et al., 1978a; Cordero del Campillo and Alvarez Pellitero, 1976a); Cystidicoloides tenuissima (Alvarez Pellitero, 1976b, c; Cordero del Campillo and Alvarez Pellitero, 1976a; Alvarez Pellitero et al., 1978a);Raphidascaris acus (Cordero del Campillo and Alvarez Pellitero, 1976a; Alvarez Pellitero, 1978 ;Alvarez Pellitero et al., 1978a); and Spinitectus gordoni (Cordero del Campillo and Aharez Pellitero, 1976a, b; Alvarez Pellitero et al., 1978a). It cannot be confirmed that two generations each year occurred throughout the zone, owing to the fact that studies of Cystidicoloides tenuissima and Raphidascaris acus from elsewhere within the zone have not provided details of maturation of the nematodes (C. tenuissima see Awachie, 1963a, 1973b; R. acus see Campbell, 1974; Andrews, 1977). Two instances of development of nematodes to maturity in relation to host sexual maturation are seen in zone 3b. Moravec and Malmqvist (1977) observed that Truttaedacnitis truttae fourth stage larvae in Lampetra planeri ammocoetes became adult in the abdominal cavities of these hosts as metamorphosis of the L. planeri took place. Of 70 L. planeri examined, 30% in September and October 1975 and March and April 1976 contained adult T. truttae. Moravec and Malmqvist ( I 977) suggested that the stimulus for

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maturation of the nematode larvae was provided by the host sex hormones produced by the transforming L. planeri. T. trutrae was present in all seasons from Salmo trutta, one of its usual definitive hosts, in zone 3b (Thomas, 1964), but unfortunately no details of maturation of the nematodes were provided. The length of life cycle of Philonema oncorhynchi was apparently synchronized to the length of life cycle of its definitive host Oncorhynchus nerka. At spawning of the 0. nerka the P. oncorhynchi females also burst releasing first stage larvae into the spawning redds. After development in Cyclops bicuspidatus invasion of young 0. nerka occurred; the larval development of the P. oncorhynchi was subsequently adapted in rate and timing to the development of the fishes, so that both worms and hosts achieved functional spawning condition concurrently (Platzer and Adams, 1967). The precise synchronization of host and nematode development was considered to be dependent on the hormone production of the fish (Platzer and Adams, 1967). All the species of acanthocephalans studied in climate zone 3b infected their hosts throughout the year. Acanthocephalus anguillae was present at almost 100% incidence in all months, although intensity of infection was maximal in summer. Invasion of fishes probably occurred at all seasons (0ien, 1976, 1979). As yet (August 1980) maturation data have not been seen by this reviewer. A year round occurrence of Acanthocephalus clavula, with shelled acanthars at all seasons, was seen by Chubb (1963b, 1964a) and Pennycuick (1971b), although the feeding habits of the respective host fishes greatly influenced incidence and intensity of occurrence (Chubb, 1964a ; Pennycuick, 1971b; Andrews and Rojanapaibul, 1976; Andrews, 1977; Rojanapaibul, 1977 ; Brattey, 1982). In some hosts, for instance Perca jluviatilis, shelled acanthor production was limited to a few months during summer (Brattey, 1982), whereas in others, for example, Anguilla anguilla, gravid females were found year round (Chubb, 1964a; Rojanapaibul, 1977). A dynamic equilibrium between invasion of the fishes by A . clavula and loss of the worms from the host intestines was suggested by Chubb et al. (1964). Invasive cystacanths of A. clavula were available in Asellus meridianus at all seasons (Rojanapaibul, 1977). A similar seasonal biology probably prevailed in climate zone 3b for Acanthocephalus lucii. Year round occurrence was reported by Rizvi (1964, 1968), Mishra (1966), Wierzbicki (1970, 1971), Lee (1977), Andersen (1978) and Priemer (1979), although in many instances with higher incidences and intensities of infection during spring and summer [see Rizvi, 1964; Mishra, 1966; Wierzbicki, 1970; and Andersen, 1978 (highest summer and autumn)]. However, in the River Glomma, Norway, Halvorsen (1972) observed infections of P. fluviatilis during June, September and October only, perhaps largely owing to the small numbers of fishes examined. Shelled acanthors were also present in some female A. Iucii most of the year [Mishra, 1966 (except February, August and November); Andersen, 1978 (highest summer and early winter, absent December and January)]. Again a dynamic balance between recruitment into and rejection of the A. lucii from the definitive host intestines almost certainly occurred (see Chubb et al., 1964).

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The study of Echinorhynchus truttae in a small stream by Awachie (1963a, 1965) revealed the close synergetic relationships between events in the life cycles of parasite, intermediate host Gammarus pulex and definitive host Salmo trutta. Within the apparently almost unchanging incidence of E. truttae in the S . trutta through the year, two major sequences of invasion and maturation of the acanthocephalans were taking place each year, resulting in maximal presence of shelled acanthors during April and December, even though females with shelIed acanthors were present during all months. These events in the fishes were correlated with and strongly influenced by the two main broods of G . pulex occurring in the stream each year (Awachie, 1963a, 1965). This study clearly demonstrated the advantages of working in a small and relatively easily sampled habitat with a parasite whose life cycle could be studied at all stages concurrently both in the field and the laboratory. The information for Neoechinorhynchus rutili provides two apparently contradictory patterns of occurrence. Steinstrasser (1936) in Germany (from a trout fish farm), Robertson (1953) in Scotland and 0ien (1979) in Norway observed a marked seasonal occurrence, with a period during which worms were not found in the fishes. Steinstrasser (1936) observed growth overwinter leading to maturity the following spring. Mien (1979) described invasion commencing in September, continuing with accumulation of the infections overwinter and spring. Growth occurred progressively from September until the following summer, at which time the N . rutili were mainly in his two longest length groups. The worms were all lost before the end of August having matured. As a contrast Thomas (1964), Bibby (1972) and Aderounmu (personal communication ; from a trout fish farm) in Wales, Walkey (1967) and Chappell(1969a) in England, Halvorsen (1972) in Norway and Mamer (1978) in Washington State, U.S.A., observed a year-through occurrence of N. rutili in the various fish hosts. Thomas (1964), Chappell (1969a) and Mamer (1978) noted maximal intensities during winter, Bibby (1972) during summer whilst WaIkey (1967) found wide fluctuations of incidence, but never below 18 %, during his first year of sampling. Chappell (1969a) never found any gravid N . rutili at any time, a fact difficult to interpret, Halvorsen (1 972) found the longest females during the period May to August, presumably maturing, whereas Walkey (1967) recovered immature, mature and gravid worms during virtually all months, although with peak shelled acanthor production during late spring and early summer. Walkey (1967) invoked two causal agents to explain his results. The overall size of the population in the fishes was determined by the availability of the infected intermediate hosts, ostracods; irregularities in the seasonal occurrence of the ostracods led to irregular fluctuations in the parasite population, such changes in population size masking any tendency towards a seasonal incidence cycle. The maturation cycle was initiated by water temperature, hence the warmer conditions of spring and summer facilitating maximal production of shelled acanthors. In conclusion then, the apparently contradictory patterns of occurrence for N. rutili in this climate zone in fact probably represent but different situations of availability of infected ostracod intermediate hosts, seasonal feeding of the

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host fishes on these and the influence of water temperature on the rate of development of the male and female N . rutili. Pomphorhynchus laevis also showed no seasonal incidence cycle in England in this climate zone; the population size was determined by availability of the infected intermediate host Gammarus pulex, definitive host diet and feeding intensity (Hine, 1970). Temperature influenced the rate of establishment in the fishes, higher water temperatures adversely influencing establishment, but not survival thereafter. However this effect was largely compensated for by increased host feeding at higher temperatures (Kennedy, 1972b). Higher water temperatures also facilitated maturation of P. laevis (Hine, 1970). Cystacanths were available year through, and no cycles of incidence or development in the G. pulex were seen (Hine and Kennedy, 1974b). Again, as in the other species of acanthocephalans studied in climate zone 3b, the populations of P. laevis in the fishes were in a state of dynamic equilibrium, where the level of infection at any one time was primarily determined by the feeding behaviour of the host fish species (Kennedy, 1972c; Hine and Kennedy, 1974b; Van Maren, 1979a). 5.

Semi-desert (Climate zone 3c)

The studies of Alvarez Pellitero (1976a, b, c, 1978), Alvarez Pellitero et al. (1978a, b), Cordero del Campillo and Alvarez Pellitero (1976a, b) and Pereira Bueno (1978) on seasonal occurrence of fish parasites in rivers of L e h , Spain fall around the boundary of climate zones 3b and 3c. For the purpose of Tables I to V the River Sil basin has been considered as falling within climate zone 3b, the River Duero basin within climate zone 3c. These studies have already been treated in Section IV C 4 and included the following species: Cestoda, Archigetes sieboldi, Caryophyllaeides fennica, Caryophyllaeus laticeps, Khawia species undetermined ; Nematoda, Capillaria coregoni, Cystidicoloides tenuissima, Raphidascaris acus, Rhabdochona denudata, R. gnedini, R. sulaki, Spinitectus gordoni; Acanthocephala, Echinorhynchus truttae. It is relevant to reiterate that full details were promised for A . sieboldi and Khawia species, but have not been seen by this reviewer; C. fennica, C. laticeps, R. denudata, R. gnedini and R. sulaki showed an occurrence pattern with one generation each year, and in contrast, C. coregoni, C . tenuissima, R. acus and S. gordoniexhibited a major spring and a minor autumn generation of adults each year. E. truttae was not discussed, as seasonal variation was merely noted and not detailed (Cordero del Campillo and Alvarez Pellitero, 1976a). If the above species are included the following numbers of species have been studied in climate zone 3c : Cestoda 16, Nematoda 18 and Acanthocephala 4. The degree of infection and prepatent period of the cestode Amphilina foliacea in acipenserid fishes in the Lower Volga, U.S.S.R., appeared to be determined by the particular species of Acipenser rather than depend on other factors, although such was not evident in experimental infections (Dubinina, 1974). Eggs of A.foliacea were present May to mid-September (Janicki, 1928). Markevich et al. (1976) considered that warm water effluents from power

218

JAMES C. CHUBB

stations in this climate zone might enhance the reproductive activities of genera such as Bothriocephalus, but provided no details. Only small amounts of information are available for CaryophylIaeides fennica, Proteocephalus esocis, P. percae, Triaenophorus crassus and T. nodulosus. Kashkovski (1967) observed C. fennica January to July and September in Rutilus rutilus, but not during the other months, however Komarova (1964) found it in May and June only in Abramis brama, April and May only in Blicca bjoerkna and April only in Rutilus rutilus heckeli. Proteocephalus esocis was recorded in Esox lucius March to May, not February and October (Komarova, 1964), P. percae spring only in Lucioperca lucioperca (Dubinina, 1949) and T. nodulosus in March, April-May and October in E. lucius (Komarova, 1964). T. crassus found by Komarova (1964) in all months sampled, February-May and October, may in fact have been the subsequently described species T,msridiona h (see p. 57). Some species of cestodes were present for limited seasons only. Thus Dubinina (1949) observed Caryophyllaeus jimbriceps spring only in Abramis brama and Cyprinus carpio and Komarova (1964) also in A . brama. Dubinina (1950) suggest that these worms died out during the winter owing to starvation caused by the host fishes ceasing feeding. Caryophyllaeus laticeps was also considered to occur in Caspian fishes primarily during the first half of summer, with fresh invasions occurring each spring (Dogie1 and Bykhovskii, 1939). Dubinina (1950) observed degenerating C. Iaticeps in A . brama during winter, and found (Dubinina, 1949) highest incidences in spring after the fish resumed feeding, whereas the cestode was uncommon in summer. Kosareva (1959) also found C. laticeps most commonly in A . brama in spring (May-June). Details of occurrence for a range of hosts were presented by Komarova (1964). In the principal definitive host A . brama high incidences and intensities were found in all months sampled, February to August and September. Maximal incidences and intensities were in April and May (93.3% each, 7-48 and 1-68 respectively), but February (86.6 %, 8-30) and JulylAugust (71.3 %, 12-46) were also high. By contrast in auxiliary host fishes occurrence was limited: Blicca bjoerkna February and May only, Rutilus rutilus heckeli May and October only and Vimba vimba vimba natio carinata AprilJMay and October only. Similar data apply for Proteocephalus torulosus: in Pelecus cultratus it was found all months sampled, whereas in A . brama it occurred May only, in B. bjoerkna April and in V . vimba vimba natio carinata March and October only (Komarova, 1964). These data show the importance of studying the range of hosts in which a parasite occurs in an area, as in each patterns of occurrence can differ quite markedly. Bothriocephalus acheiIognathi was present all year in fish farms in climate zone 3c (Iskov, 1966; Klenov, 1972), with highest incidences in Ctenopharyngodon idella O+ fishes in July and August. In 1 and 2+ fishes highest incidences were April-May, lowest July-August, with a second lesser peak in October. These data suggest two generations per annum, the small autumn peak originating from the completion of the life cycle during the summer months. Unfortunately details of maturation were not provided. Proteocephalus

+

HELMINTHS I N FRESHWATER FISHES

219

osculatus in Silurus glanis occurred year round, but during hibernation of the fishes in depressions at the river bottom only scolices were seen; in spring the strobilae developed and egg production commenced (Dubinina, 1949, 1950). Mikailov (1963) in the same host from the River Kure and the Mingechaur Reservoir observed almost constant incidences and intensities of occurrence ofP. osculatus all through the year. An essentially similar pattern of occurrence of Hunterella nodulosa was reported by Mudry and Arai (1973), but they provided detailed maturation information showing recruitment into the worm population in the fishes to commence during May and June and to continue at least until October; large gravid cestodes were present in early spring, but these were all lost by July. A similar pattern of occurrence of gravid worms in early spring was reported for Triaenophorus rneridionalis. In the Volga Delta, U.S.S.R., the cestodes left their hosts in May. This time was the same as for other species of Triaenophorus in Lake Ladoga (climate zone 3aii), but in the southern U.S.S.R. (this zone 3c) the water temperatures were considerably higher (Kuperman, 1973). Only small amounts of information are available for most of the nematode species scrutinized in climate zone 3c. Occasional findings of Capillaria brevispicula (April, May only), C. lewaschofi (March-May, July, August), Philometra abdominalis (October only) and Rhabdochona denudata (April, May only) by Komarova (1964), Philometra rischta and R. denudata (both springsummer) by Mikailov (1963) and Philometra species undetermined (March only) by Kashkovski (1967), all as part of larger seasonal faunistic studies, unfortunately do not provide any guide to our understanding of their seasonal dynamics in this zone. Camallanus lacustris (Dubinina, 1949), C. truncatus (Dubinina, 1949; Komarova, 1964), Philometra nodulosa (Dailey, 1966), P. ovata (Dubinina, 1949) and Rhabdochona acuminata (Mikailov, 1963) were present in their respective fish hosts all through the year, but details of maturation were not provided. The same situation applied for Raphidascaris acus (Dubinina, 1949; Komarova, 1964), but Supryaga and Mozgovoi (1974) observed two generations of adults per annum, one the end of February to the beginning of June and a second from the end of August to the beginning of October. This corresponds to the situation found in L e h , Spain for this species by Corder0 del Campillo and Alvarez Pellitero (1976a), Alvarez Pellitero (1978) and Alvarez Pellitero et al. (1978a). Khromova (1975) showed that invasion of Acipenseridae by Truttaedacnitis sphaerocephala occurred during summer in the Azov and Caspian Seas and the lower part of the River Volga, U.S.S.R. A11 seasonal acanthocephalan records from climate zone 3c known to the author originate from Komarova (1964) who found the following : Acanthocephalus lucii, February-May, October; Neoechinorhynchus rutili, February, April-August, October; and Pomphorhynchus laevis, April-May. 6. Desert (Climate zone 3d) The studies of Engashev (1964a, b, 1965a, b, c, d, e, 1966a, 1969) on the nematode Raphidascaris acus were made in this climate zone. Two generations

220

JAMES C. CHUBB

of adult worms were seen in Esox lucius from the Amu Darya Basin, U.S.S.R., each year, the main one in early spring (maximum incidences February, March) and a smaller one during autumn (September) (Engashev, 1964b). In Lakes Kok-su and Makpalkul’ in the same region the first ovipositions were, respectively, April-May and March-May, the second, August and August-October (Engashev, 1969). 7. Sub-polar (Climate zone 3e) Information is available for 13 species of Cestoda, 9 of Nematoda and 4 of Acanthocephala in this zone. Small amounts of data are to hand for Eubothrium crassum marine Atlantic race. Dogie1and Petrushevskii (1935) examined Salmo salar August to October. In fishes fresh from the sea 100 or more cestodes were found, but in fishes which had remained in the river from the previous year only scolices were seen in the pyloric caeca. Malakhova (1961) reported Proteocephalus species in the intestine of Esox lucius from Lake Konche, KareIia, U.S.S.R., at all seasons, with maximal occurrence in spring. Caryophyllaeides fennica was present in Rutilus rutilus all year in the same habitat, with a peak, but low incidence of 6-7 % in spring (Malakhova, 1961). Nu details of maturation were provided. Kennedy (1978a) observed a relatively constant incidence of Eubothrium salvelini year round in Salvelinus alpinus (non-migratory) in North Norway. Recruitment to the cestodepopulation occurred all year, and gravid worms were also found in all seasons, although with maximal numbers in June and July and minimal in September. All the remaining species of cestodes studied in climate zone 3e contained eggs at a limited period of the year. Thus mature or gravid worms were found : Cyathocephalus truncatus late spring and summer (Leong, 1975); Eubothrium rugosum March to June (Kuitunen-Ekbaum, 1933b) ; Proteocephalus exiguus late summer (Leong, 1975),May and June (Malakhova and Anikieva, 1975) with most intense infections during hot summers; P. jilicollis summer (Leong, 1975); P. percae March to mid-May, end of June all gone (Ieshko et at., 1976); and P. torulosus May to mid-August (Ieshko eta)., 1976). In the Triaenophorus species the main periods of oviposition were: T. crassus May (Ekbaum, 1937), April mainly and first half of May (Miller, 1943, 1952), mid-May (Miller and Watkins, 1946), April-early May (Libin, 1951), but as late as June or mid-July in Siberia (Kuperman, 1973); T. nodulosus end May and early June (Miller, 1943), but until the end of June or mid-July in Siberia, U.S.S.R. (Kuperman, 1973); and T. stizostedionis the first two weeks of June (Miller, 1945). Invasion of and presence in their fish definitive hosts was year round in these species of cestodes. The nematode species Camallanus lacustris (Malakhova, 1961 ; Shul’man et al., 1974), Cystidicola farionis (Leong, 1975; Valtonen and Valtonen, 1978), Haplonema hamulatum (Malakhova, 1961), Philometra obturans (Malakhova, 1961),and Raphidascaris acus were present in their respective fish definitive hosts at all seasons. One mature generation of R . acus per annum was seen in Lake Konche, Karelia, U.S.S.R. (Malakhova, 1961). Capillaria

HELMINTHS I N FRESHWATER FISHES

22 1

species undetermined and Philometra species undetermined were seen in winter and spring, and summer only, respectively (Malakhova, 1961). Rumyantsev (1965) reported Philonema sibirica during the summer, as did Shtein (1959a) for Rhabdochona denudata. The acanthocephalan parasites Acanthocephalus lucii (Malakhova, 1961; Shul’man et al., 1974), Echinorhynchus salmonis (Leong, 1975; Holmes et al., 1977; Valtonen, 1981a) and Neoechinorhynchus rutili (Malakhova, 1961) were present in some fish definitive hosts at all seasons. In Coregonus nasus N. rutili was considered an accidental parasite, present only owing to the seasonal feeding habits of the fishes and not reaching maturity (Valtonen, 1979). Gravid E. salmonis were found throughout the year; cystacanths from the intermediate host Pontoporeia afJinis were also present all year. Overall peak abundances were during the coldest time in winter (Leong, 1975). Changes in occurrence of E. salmonis in Coregonus nasus during the year could be related to and were explained by changing availability of P. afJinis during seasonal migrations of the host fishes (Valtonen, 1981 a, b). Bauer (1959a) studied Neoechinorhynchus tumidus in coregonids of the lower reaches of the River Yenisei, U.S.S.R., in summer. At the end of June and beginning of July (early summer) the acanthocephalans were small and sexually immature. In September (autumn) large worms were found, the females containing many shelled acanthors. D.

POLAR (CLIMATE ZONE

4)

1. Polar (Climate zone 4a)

Kuperman (1973) stated that the mature individuals of the cestodes Triaenophorus crassus and T. nodulosus persisted in the intestines of Esox lucius until the end of June or middle of July, owing to the low water temperatures (8-12°C) of the River Anadry, Chukotka, U.S.S.R., a habitat falling within this climate zone. 2. Ice-caps (Climate zone 4b)

Conditions such as are to be found on ice-caps would be unsuitable for freshwater cestodes, nematodes or acanthocephalans. However in areas like Greenland fish species including Salvelinus alpinus swim in the waters at the foot of ice-flows (Gittins, personal communication). E.

MOUNTAIN (CLIMATE ZONE

5)

Six habitats tabulated (see Tables 1-111, V) probably fall within areas which are properly placed within this category of climate zone, Babine Lake, British Columbia, Canada (Smith, 1973; Boyce, 1974), Lakes Melingen and Nedre

222

JAMES C . C H U B B

Fipling, Norway (Halvorsen and Macdonald, 1972), Lake Sevan, Armenia, U.S.S.R. (Vartanyan and Mkrtchyan, 1972; Begoyan, 1977), Suttle Lake, Cascade Range, Oregon, U.S.A. (Merritt and Pratt, 1964), and springs in Chilu-Chor Chashma, Tadzhikstan, U.S.S.R. (Daniyarov, 1975). This latter springs habitat is unique within this zone in having a constant year round water temperature of 18-20°C. The parasite fauna of the fishes was examined in summer and autumn, that in the autumn being much poorer, especially for species with complex life cycles, including Bothriocephalus acheilognathi (Cestoda) and Acanthogyrus cholodkowsky (Acanthocephala) (Daniyarov, 1975). At Lakes Melingen and Nedre Fipling the water surface was frozen from November to May. Samples of the cestodes Cyathocephalus truncatus, Eubothrium crassum and Profeocephalus species undetermined were collected by Halvorsen and Macdonald (1972) between June and October. C . truncatus was present throughout, with its lowest incidence in both lakes in August, during which month the frequency of unattached adult specimens in the intestines of Salmo trutta was highest (40 %). E. crassum freshwater race was seen in S. trutta from Lake Melingen in June only (7.2%), and in Nedre Fipling in June, July and September. Proteocephalus species was located in the same host fish: Lake Melingen June only (16.7 %); Nedre Fipling June (19.2 % and July (9.6 %) only. The biology of Eubothrium salvelini American race was studied in Babine Lake by Smith (1973) and Boyce (1974). Gravid worms in Oncorhynchus nerka were apparent from about 23 May onward (Smith, 1973). In Lake Sevan, Armenia, U.S.S.R., Begoyan (1977) studied Khawia armenica. An annual cycle was postulated, with invasion of fishes mainly spring and maturation in autumn, although the cestodes were in the intestine of Varicorhinus capoeta sevangi year round. The nematode Philonema agubernaculum (KO and Adams, 1969) was studied experimentally from collections made in this climate zone. Three species of acanthocephalans have also been investigated. Echinorhynchus baeri and Pomphorhynchus laevis were present in Coregonus lavaretus ludoga and C. lavaretus maraenoides at Lake Sevan in spring and autumn only, but not summer and winter (Vartanyan and Mkrtchyan, 1972); these incidences may reflect seasonal changes in the host feeding patterns. Finally Merritt and Pratt (1964) investigated the biology of Neoechinorhynchus rutili in Suttle Lake, Cascade Range, Oregon, U.S.A., Peak intensities of infection occurred in autumn, but almost all fishes were infected. In conclusion, it is apparent that seasonal changes of occurrence of fish parasites in mountainous areas are present as elsewhere in subtropical and mid-latitude climate zones. If any differences are present they are likely to be of timing, in that the colder water conditions of montane lakes may delay the onset of maturation of the parasites by some weeks compared with adjacent low land areas.

223

HELMINTHS I N FRESHWATER FISHES F.

SPECIES STUDIED IN MORE THAN ONE CLIMATE ZONE

Table VI lists the adult cestodes, nematodes and acanthocephalans that have been investigated for seasonal biology in more than one climate zone. Thirty-seven species of cestodes, 28 of nematodes and I I of acanthocephalans are included. TABLEVI Species of cestode, nematode and acanthocephalan studied ( S )for seasonal occurrence in more than one climate zone. The species are in alphabetical order.

Climate zone Adult species

3

2

a

b

ai

aii aiii

4

b

c

d

e

5

a

CESTODA

Amphilina foliacea Archigetes sieboldi Biacetabulum meridianum Bothriocephalus acheilognathi Bothriocephalus claviceps Bothriocephalus cuspidatus Caryophyllaeidesfennica Caryophyllaeus fimbriceps Caryophyllaeus Iaticeps Cyathocephalus truncatus Eubothrium crassurn Eubothrium rugosum Eubothrium salvelini Glaridacris catostomi Glaridacris laruei Hunterella nodulosa Isoglaridacris bulbocirrus Khawia sinensis Khawia species undetermined Manobothrium hunteri Monobothrium wageneri Proteocephalus ambiguus ProteocephalusamblopIitis Proteocephalus cernua Prateocephalus esocis Proteocephalus exiguus Proteocephalusfilicollis Proteocephalus macrocephalus Proteocephalus neglectus Proteocephalus osculatus Proteocephaluspearsei

S

S

S S S

s s s s s S s s s s s S s s

s s s s s s s s s s s s s s s s

s s s s s

S S

s s S s s

S S S

s s

S

s s

s s

S

S

S

s s S s s s s S S

s s s s s S s s s s s s

S S S S S

S S S S S S S

S S S S

S S S

224

JAMES C . CHUBB

TABLEVI (continued)

Climate zone

2

Adult species a Proteocephaluspercae Proteocephalus torulosus Proteocephalus species undetermined* Triaenophorus crassus Triaenophorus meridionalis Triaenophorus nodulosus

S

NEMATODA

Camallanus lacustris Camallanusoxycephalus Camallanus truncatus Capillaria brevispicula Capillaria coregoni Capillaria petruschewskii S Contracaecum bidentatum Cystidicola farionis Cystidicoloides tenuissima Paraquimperia tenerrima Philometra abdominalis Philometra obturans Philometra ovata S Philometra rischta Philometra species undetermined* Philometroides cyprini Philometroides sanguinea Philonema agubernaculum Raphidascaris acus S Rhabdochona cascadilla Rhabdochona denudata Rhabdochona gnedini Rhabdochona sulaki Spinitectus carolini Spinitectus gordoni Spinitectus gracilis Truttaedacnitis sphaerocephala Truttaedacnitis truttae S ACANTHOCEPHALA

Acanthocephalus anguillae Acanthocephalusjacksoni Acanthocephalus hcii Echinorhynchus salmonis Echinorhynchus truttae

3

b

ai aii aiii

b

s s s s

s s s s

S

S

s s s s

c

s s s s s s

d

e S S S

5

a

s s

s s s s

s s

S

S S

S

S

s s S s s

S S

s s S

S S

S

s s s

S

S

s s s s s s s s

s s s s s s s s s s S S s s S S s s s s s s s s S

S

s s S

S S

s s s S s s s s S

s s s s S s s s s

S

4

S S

S

s s s s

s . S

S

225

H E L M I N T H S I N F R E S H W A T E R FISHES

TABLEVI (continued)

Climate zone Adult species a Fessisentis friedi Neoechinorhynchus cylindratus Neoechinorhynchus rutili Pomphorhynchus bosniacus Pomphorhynchus bulbocolli Pomphorhynchus laevis

S

4

3

2

b ai aii aiii S S

b

c

s s s s s s s s S s s s s s s

d

e S

5

a S

S

* Includes more than one species It will have been noted in Sections IV C 1,2 and 4 especially that even within the climate zones there can be considerable differences in seasonal patterns of occurrence for some species. Accordingly, care must be taken in making interzone comparisons. In this section a number of species are discussed, selected to make what are considered relevant points. The cestode Bothriocephalus acheilognathi has been investigated in varying levels of detail in climate zones 2b, 3ai, 3aii, 3aiii, 3c and 5. Overall the adult cestodes were present in the respective fish hosts during all times of the year [2b, Liaoand Shih(1956); 3ai, Davydov(1978), Molnar(1968b); 3aii, Musselius (1973); 3aiii, Nakajima and Egusa (1977a); 3c, Iskov (1966), Klenov (1972); but perhaps not 5 (Daniyarov, 1975) although a year round investigation was not made in this last instance]. In the warmer winter conditions of climate zone 2b egg production continued year through (Liao and Shih, 1956),however in the colder conditions of the winters of the mid-latitude zones egg production ceased during this season [3ai, Molnhr (1968b); 3aii, Musselius (1973); 3aiii, Nakajima and Egusa (1977a)l. Musselius (1973), Nakajima and Egusa (1976) and Davydov (1978) have shown experimentally how cooling water conditions slow or ultimately prevent the development of the embryos in the egg, the procercoids in the copepods and the adult worms in the intestines of the definitive fish hosts. Owing to its low specificity for both intermediate and definitive hosts B. acheilognathi has been widely spread with cultured fishes (Bauer et al., 1969). Caryophyllaeides fennica has been studied in climate zones 2a, 3ai, 3aii, 3b, 3c and 3e. In climate zone 2a KaiiC (1970) observed mature C. fennica in January, April to a peak May, falling to July, with no worms present August to December. Cernova (1975) also found C. fennica spring only in this zone. However, by contrast, in some mid-latitude zones occurrence of the cestode was seen all year [3b, Chubb (1961), Davies (1967), Mishra (1966); 3e, Malakhova (1961)], whereas in others [3c, Kashkovski (1967), Komarova (1964)l incidences were apparently limited to January-September (Kashkovski, 1967) and April-June (Komarova, 1964). It could be suggested that these differences were explained by higher late summer water temperatures in zones 2a and 3c,

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JAMES C. C H U B B

but this explanation is probably doubtful, owing to the fact that Borgstrom and Halvorsen (1968) in climate zone 3b, from Norway, also found a distinct seasonal pattern for C.fennica, with worms present May-November and containing visible eggs June and August only. Unfortunately no experimental studies of the biology of C.fennica have been made so far so that the reasons for the different patterns of occurrence currently remain obscure. In Curyophyllaeus laticeps, examined in some detail in climate zones 2a, 3ai, 3aii, 3b and 3c, different patterns of occurrence and maturation were also seen. Thus, in zone 2a KaiiC (1970) found invasion of fishes to commence in November and end in April, whilst mature worms increased from January to a peak April, declined to July, with no C . luticeps in fishes August to October. A rather similar pattern, but with a longer period of absence, September to March, was seen in climate zone 3ai by Wunder (1939). Invasion commenced April, peaked May-June and declined to August. Again Lyubarskaya (1965, 1970) in zone 3aii observed infections most strongly during spring and summer, with no worms present during autumn. A clear annual cycle was demonstrated by Kennedy (1968) in climate zone 3b, with invasion mainly from December onward, gravid C . luticeps seen from January peaking in March-May and the population declining thereafter to disappear by July. Halvorsen (1972), in the same zone, observed occurrences May to August only, with progressive percentages of the worm population becoming gravid towards August. Again, at the boundaries of zones 3b and 3c Alvarez Pellitero et al. (1978a, b) found a clear cycle, with cestodes present December to July, gravid in spring. Finally, Dogie1 and Bykhovskii (1939), in zone 3c, observed maximal occurrence during the first half of summer, with invasion during spring and a decline in the population in late summer. It could be reasonably concluded from the preceeding paragraph that Caryophyllaeus luticeps had a well-defined seasonal pattern of invasion, growth and maturation through the range of its occurrence. It is, however, not as simple as that, as the following examples will show. In climate zone 3aii Izyumova (1958, I959b) found C. laticeps in principal fish hosts all year, although towards the end of winter their numbers were considerably reduced. Also within this zone Strizhak (1971) observed C. luticeps during all months, with invasion, growth and gravid worms present at all times. He compared a thermally polluted bay with a bay having natural water temperatures. The major differences were the higher incidences in the unheated bay all year, but more rapid maturation of the C. laticeps in the heated bay. Within zone 3b, again, presence of C. luticeps year round was seen by Mishra (1966), although with a clearly defined maturation cycle with gravid cestodes in May only, and Anderson (1974a) where invasion, growth and maturation to gravid worms occurred year round, although with the maximum percentage of the population gravid in summer. Anderson (1974a) experimentally determined that at 12°C C. laticeps developed to maturity in the fish intestine in about one month, but the survival rate of the worms decreased markedly during summer. Wierzbicka (1978) too, observed year round occurrence in climate zone 3b, as did Komarova (1964) in principal hosts in zone 3c.

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In climate zone 3ai Milbrink (1975) once again found year through presence of Caryophyllaeus laticeps. He observed identical cycles over four years, with peaks of occurrence in spring and autumn each year. The spring maximum commenced whilst water temperatures were still below 5"C, and the autumn peak was concurrent with lowered surface water temperatures to about 8°C. The summer levels of occurrence were low owing to warm water conditions (see Kennedy, 1971) and the winter levels low owing to reduced feeding activity of the fishes, Abramis brama (Milbrink, 1975). In conclusion, therefore, it can be seen that the patterns of incidence, intensity of occurrence and maturation of Caryophyllaeus laticeps vary considerably through its range of distribution in the climate zones, such patterns being determined by a spectrum of factors including availability of infected intermediate host tubificids (Sekutowicz, 1934; Kennedy, 1969a, 1972a; Milbrink, 1975), feeding of the definitive hosts on these tubificids (Scheuring, 1929; Reinsone, 1955), the effect of water temperature on establishment in the definitive host (Kennedy, 1971) and also on the length of time required for maturation of the adult worms (Anderson, 1974a). It is the combined effects of these factors, and others no doubt, that determine the seasonal patterns of occurrence, which in the instance of C. laticeps has been shown to be rather variable through its distributional range. The parenteric plerocercoids of Proteocephalus ambloplitis in Micropterus dolomieui migrate into the intestines of sexually mature individuals of that fish species prior to the growth of the cestode strobila and the production of gravid worms. This phenomenon occurs at different times through the range of occurrence of the species. In climate zone 2b, at Par Pond, South Carolina, U.S.A., Eure (1976a) deduced that the migration occurred from November onward (enteric adults present from December), whereas in climate zone 3aii, at Gull Lake, Michigan, U.S.A., the migration occurred about 20 May (Esch et al., 1975) and in Lake Opeongo, Ontario, Canada, during May, mainly, but also in June to a minor extent. The hypotheses to account for this annual migration of the parenteric plerocercoids have already been discussed earlier (pp. 83-85) and need not be repeated here. Whichever hypothesis is ultimately shown to be correct remains to be seen, but it is evident that some part must be played by the prevailing climatic conditions influencing water temperatures and other factors earlier in more southern latitudes. Willemse (1969) has shown experimentally that if Proteocephalus percae up to 5 cm long were taken from ambient winter water temperature conditions (0-3°C) and warmed slowly to 20°C in the laboratory, then after about ten days the genitaliadeveloped. Thus, if such a rise of water temperature initiates egg production, then the date of first appearance of gravid P . percae in natural conditions should also show a latitudinal distribution. Unfortunately the information provided by many authors is too general to allow a precise statement, but the following dates (periods) give an indication: zone 3ai, 18 April (Markowski, 1933),April(Moravec, 1979b);3b, April (Mishra, 1966;Wootten, 1974; Andersen, 1978), first week May (Rizvi, 1964) and May (Halvorsen, 1972); spring (Willemse, 1969; Wierzbicki, 1970); and 3e, most mid-May

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(Ieshko et al., 1976),spring (Malakhova et al., 1973). There is, however, a clear indication that the first appearance of gravid P. percae is linked with the advent of spring during April-May in the mid-latitude zones. It would be interesting to see if there was a precise relationship between water temperature and the production of the first eggs, so that critical laboratory experiments and field observations should be carried out. It is perhaps significant to note that Ieshko et al. (1976) pointed out that P.percae persisted in the definitive host as gravid worms for a longer time in the cold conditions of Northern Karelia U.S.S.R. (zone 3e), until mid-August, about one month, or more, later than in more southern zones [see for instance in zone 3b, all gravid worms gone by end of May (Wootten, 1974), during June (Mishra, 1966; Halvorsen, 1972; Priemer, 1979) and mid-July (Rizvi, 1964)]. In members of the cestode genus Triaenophorus the adult worms commence growth during autumn, accumulate eggs in their uteri in the winter and release them in spring. The release of the eggs and the loss of the gravid worms of Triaenophorus nocluiosus shows a fairly precise relationship with water temperature which was experimentally demonstrated by Kuperman and Shul’man (1972). A “total warmth” factor was involved, higher “total warmth” values being required at lower water temperatures. At 13-18°C the cestodes were shed in two to three days, but at 7-9°C only after 25 or more days. The shedding of the eggs was considered to be dependent on the water temperature and not on their maturity. In natural conditions there is some agreement with these experimental conclusions, although within most climate zones a variation of months exists : 3ai, April (Moravec, 1979b), mid-May (Michajlow, 1933), June (Scheuring, 1929) and end of June (Rosen, 1919); 3aii, May (Markova, 1958), May, mid-June (Kuperman, 1973), end of May, beginning of June (Tell, 1971); 3b, May (Copland, 1956), May-June (Rizvi, 1964), first half June (Borgstrom, 1970), June (Chubb, 1963a; Halvorsen, 1972); 3e, end of May, early June (Miller, 1943), to end of June, midJuly (Kuperman, 1973); and 4a, end of June, mid-July (Kuperman, 1973). Thus, there is some indication of a progression, south to north, warmer to colder mid-latitude zones, but once again, as indicated earlier in this section, more precise datings of these events are needed. The nematode Camallanus lacustris shows a uniformity of pattern of seasonal biology through the range of climate zones in which it has been studied, 3ai, 3aii, 3b, 3c and 3e. In all zones invasion of the fish hosts, growth of the worms to functional maturity and release of the next generation of larvae occurred year round [3ai, Zschokke (1884), Moravec (1979b); 3aii, Izyumova (1958, 1960), Rautskis (1970a, b); 3b, Mishra (1966), Wierzbicki (1970), Andrews (1977), Andersen (1978); and 3e Malakhova (1961), Shul’man et al. (1974)l. In zone 3c less full information is available (Dubinina, 1949; Komarova, 1964). A contradictory situation, with a clear annual cycle of invasion during summer, growth of the C. lacustris overwinter, with release of the next generation of larvae in spring was claimed by Tornquist (193I), but this observation was probably not based on detailed month by month counts of each stage of development, and should, therefore, be treated with caution.

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Of course temperature influences the rate of development of the C. Iacustris (Kupriyanova, 1954; Moravec, 1969) so that there will be a tendency for the warmer months to enhance the speed of development of all stages in the life cycle of C. lacustris. It was noted in Section IV A that Stromberg and Crites (1974b) were of the opinion that camallanids could reproduce constantly in tropical conditions. Clearly, such a situation applies to C. lacustris in all mid-latitude climate zones, and perhaps also to C. tuuncatus, although by comparison with C. lacustris, there is little detailed information available for this latter species. Some nematodes showed a remarkably constant annual pattern of development in all zones in which they have been investigated. Thus, Philometra ovata was shown by Molnhr (1966b) (zone 3ai) to have a regular annual life cycle adjusted almost to days within each year, and this situation applies, as far as details provided permit the comparison, also in climate zones 2a (KaiiC et at., 1977) and 3b (Wierzbicka, 1978). Unfortunately, in zones 3aii (Izyumova, 1958, 1960) and 3c (Dubinina, 1949; Mikailov, 1963; Komarova, 1964) the studies were of a seasonal faunistic nature and therefore do not provide detailed information for P. ovata. Many other philometrid nematodes have regular annual cycles of development, but not all. Philometra obturans adults, including females containing eggs and mature larvae, were found in Esox lucius at all seasons [zone 3ai, Molnhr (1976), Moravec and Dykovh (1978), Moravec (1979b); 3e, Malakhova (1961)l. The lack of seasonality of P. obturans in its definitive host was attributed by Moravec and Dykovh (1978) to the inclusion of a cyprinid reservoir host into the life cycle. The annual rhythms in the other species of philometrids were determined by the yearly fluctuations and generation patterns of the copepod intermediate hosts from which direct invasion of the definitive hosts occurred. Although some species of nematodes were present in their definitive hosts at all seasons of the year, nonetheless, there were distinct and limited periods when the worms were gravid. In Raphidascaris acus in some climate zones only one genveration of mature worms occurred each year [zone 2a, KaiiC (1970); 3ai, Zitfian (1973), Moravec (1970b, 1979b); 3aii, Tell (1971); 3b, Davies (1967); and 3e, Malakhova (1961)], whereas in others two generations, one spring and one during autumn, were reported [zone 3b, 3c, Cordero del Campillo and Alvarez Pellitero (1 976a), Alvarez Pellitero (1978), Alvarez Pellitero et al. (1978a); 3c, Supryaga and Mozgovoi (1974); and 3d, Engashev (1964b, 1966a, 1969)]. Presumably, the second generation is able to occur provided that the summer water temperature conditions are warm for long enough to allow for the complete adult development of the second generation of R. acus, some two months at 15°C (Moravec, 1970a). In addition, however, other factors will also contribute, for instance, the feeding regime of the definitive host fishes as the larvae of R. acus are acquired by these definitive hosts mainly from cyprinid fishes [see p. 55 of Part I11 of review, Chubb (1980)l. Thus, in climate zone 3b, where both one (Davies, 1967) and two generations per annum (Cordero del Campillo and Alvarez Pellitero, i976a) have been reported it may be this latter factor which is determinant.

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Many of the acanthocephalans were present in their definitive fish hosts at all seasons. Acanthocephalus lucii females contained shelled acanthors at all times of the year in some localities [climate zone 3ai, Moravec (1979b); 3b, Mishra (1966), Lee (1977), Andersen (1978); and 3e, Malakhova (1961), Shul'man et al. (1974)]. In these examples the warmer months favoured production of the shelled acanthors (Shul'man et al. 1974; Andersen, 1978; Moravec, 1979b) nevertheless, they were also present within gravid females during winter. However, in other areas a more defined summer cycle of maturation has been reported, perhaps by Zschokke (1884, zone 3ai), and by Komarova (1950) and Andryuk (1974a) (both zone 3aii). It would be interesting to know exactly what factors initiate the latter maturation pattern. Owing to the spread through the climate zones it seems unlikely to be a function of water temperature alone; perhaps the answer will lie in the generation patterns of the intermediate host Asellus aquaticus. Echinorhynchussalmonis also usually showed presence of worms, immature and gravid, at all seasons [climate zone 3aii, Bauer and Nikol'skaya (1957, samples July-November only), Amin and Burrows (1977), Amin (1978a) ; 3e, Leong (1975), Holmes et al. (1977)], although Tedla and Fernando (1969, climate zone 3aii) reported a single maturation period of early summer, after which the worms died. Tedla and Fernando (1970) pointed out that most E. salmonis matured when Perca $avescens, the host fish they were investigating, was spawning. They considered that it was unlikely that the hormonal effect was important, as parasites in fishes spawning in autumn also matured in spring (Bauer, 1959a). However, subsequently Amin (1978a) did find that E. salmonis in Oncorhynchus tshawytscha spawning during autumn were significantly more mature and posteriorly displaced than in non-spawning host individuals. Accordingly, he concluded that E. salmonis maturation might be enhanced by the sexual hormones of spawning fishes. Valtonen (1981a, b, climate zone 3e) has also demonstrated that seasonal migrations of the host fishes to and from areas of occurrence of the intermediate host Pontoporeia afinis can lead to seasonal invasion periods by E. salmonis. Thus Coregonus nasus in the north east Bay of Bothnia, Finland, were exposed to invasion for about six months of the year whilst in deep basins where P. afinis was abundant. Neoechinorhynchus rutili too showed distinct patterns of occurrence in some instances, but not others : distinct patterns of incidence, climate zone 3ai TesarEik (1970, 1972), 3b Steinstrasser (1936),vRobertson (1953), 0ien (1979), 3e Valtonen (1979); occurrence all year, 3ai Zitfian (1973), 3b Walkey (1967), Chappell (1969a), Bibby (1972), Halvorsen (1972), Mamer (1978), and 5 Merritt and Pratt (1964). However, where detailed assessments of maturity stages have been made, regardless of climate zone, the majority, or all, of the N . rutili were gravid in spring and summer: Steinstrasser (1936), Walkey (1967), TesarEik (1970, 1972), Halvorsen (1972) and probably 0ien (1979, full details not published). However, it is not thought that N. rutili differs in any fundamental manner from the other acanthocephalans discussed in this section, Acanthocephalus lucii and Echinorhynchus salmonis,

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23 1

because Walkey (1967) did find N . rutili containing shelled acanthors during all months over a two year period, despite the marked annual cycle of maturation. Indeed, the view of Walkey (1967) that while temperature initiated the seasonal maturation cycle, the overall size of the parasite population was largely determined by the availability of infected intermediate hosts, is thought to apply to most acanthocephalan species so far studied, regardless of the climate zone within which they occur. From the discussion of material presented in Section IV it is clear, as Halvorsen (1972) indicated, that the same species of parasite can exhibit a seasonal cycle of incidence and/or reproduction in one locality, but not in another, and that the timing of the cycles where they occur can be quite different. In Section V it is hoped to summarize some of the factors involved, and thereby indicate further why such variations in seasonal patterns of occurrence and maturation are to be found. V. A.

GENERAL CONCLUSIONS

INCIDENCE AND INTENSITY OF OCCURRENCE

As with the adult trematodes (see Section VIII A, Chubb, 1979) almost all of the adult cestodes, nematodes and acanthocephalans have at longest an annual turnover of occurrence in their hosts, so that invasion, establishment, growth, maturation of genitalia, egg or larva accumulation and loss of gravid worms are all achieved within a maximum period of 12 months. With some species from each of the three groups there are no clear generations, but a more or less constant recruitment, maturation and loss of worms. However, with both of these types of pattern of occurrence the data for incidence and intensity of presence of the parasites will give a meaningful indication of the changes in the population, provided that they are based on representative samples of fishes. Of course, ideally, for a full statement of the details of the seasonal biology of a parasite in its respective fish host the samples of fishes should be divided into year classes, and the occurrence and development of the parasite studied separately in each of these, owing to the changes of behaviour, ecology and physiology which occur in fishes during their growth from fry to reproductively functional adults. Unfortunately, it is frequently difficult enough to catch samples of fishes which are representative of even part of the adult host population, without regard for each year class. It is important to recognize that the localization of the parasite within the host body will to some extent influence the dynamics of that parasite. In this part of the review most of the parasites considered were from the lumen of the alimentary tract of their fish hosts, including all the cestodes and acanthocephalans, and many of the nematodes. The following species of nematodes were located within the somatic organs or spaces of their respective hosts: Capillaria acerinae, C . petruschewskii, Cystoopsis acipenseris, Philometra abdominalis, P . cylindracea, P . fujimotoi, P . k o t h i , P . nodulosa, P . obturans,

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P. ovata, P. rischta, Philometra species undetermined, Philometroides carassii, Ph. cyprini, Ph. huronensis, Ph. sanguinea, Philonema agubernaculum, P. oncorhynchi and P. sibirica. With all these species once infections were established in the host fishes at the appropriate time of the year (see Section V C) thereafter the numbers of worms present in the individual host would fall only owing to death of the nematodes, perhaps males post-copulation, or both sexes owing to host responses, until the season when the gravid females migrated out from the fishes in order to release their invasive first stage larvae into the habitat (see Section V D). No figures are available for the numbers of third stage larvae establishing in a host, compared with the numbers of adults eventually achieving sexual maturity, but it seems likely that quite a high proportion would ultimately reach their reproductive potential. There is not the situation seen in many of the alimentary species, where establishment in the definitive host in no way indicates that ultimate sexual maturity will be achieved, indeed as will be seen below, in s o a e species only quite a small percentage of worms establishing in the alimentary tract of the definitive host will ever reach a gravid condition, the others being lost during development. The dynamics involved in the seasonal occurrence of a fish parasite were first emphasised by Hopkins (1959) for the cestode Proteocephalus Jilicollis. Fig. 5 (p. 89) summarizes the pattern of incidence found. The steep rise in incidence in June-July represented the invasion phase, which reached a plateau, remaining there until November-December, at which time no further copepods containing procercoids were available in the habitat. Thereafter, until the following June-July, the population declined, owing to continuous loss of worms. Hopkins (1959) calculated from a consideration of the seasonal variation in incidence that the parasite population was in dynamic balance and that approximately 1 % of the P.jlicollis were lost daily from the fishes. Less than 1 % of the worms established in the Gasterosteus aculeatus survived to become gravid, probably around 0.5 %, or as Hopkins (1959) stated in other words, of every 200 worms to become attached in the intestine only one reached full maturity: the 199 died as a result of unknown causes. In the example of ProteocephalusJilicollis quoted above the invasion period of the host fishes was limited, SO that thereafter the rate of loss of worms could be seen. In the example of the cestode Triaenophorus nodulosus in Esox lucius studied by Chubb (1963a) invasion of the fishes occurred at all times of the year. Despite this, it was found that there was no increase in the numbers of worms in the intestines to a maximum at any time of the year, but rather there was a more or less constant number of worms in fishes of given length at all times of the year. Chubb (1963a) suggested, therefore, that a dynamic equilibrium existed at all seasons between gain of plerocercoids from the second intermediate host and loss of worms from the intestines of E. lucius. It should be noted that the dynamic situations reported by Hopkins (1959) and Chubb (1963a) applied regardless of the condition of maturity of the worms.

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From a study of the data for incidence and intensity of occurrence of the cestodes given in Section 111 of this review it is evident that such a dynamic gain and loss situation applied in most if not all instances. Many of the relevant authors have stressed this point, for instance for Caryophyllaeus laticeps Kennedy (1969a, 1972c), Anderson (1974a, b, 1976a, b), Milbrink (1975), Proteocephalus pearsei Tedla and Fernando (1969), Cannon (1973), P. torulosus Kennedy and Hine (1969), Kennedy (1972~)and Triaenophorus nodulosus Rizvi (1964). Of course the details of invasion, incidence and intensities of occurrence varied in each host-parasite interaction, nonetheless, such a dynamic state applied. A similar condition probably also pertained to the occurrence of alimentary nematodes. Instances may be found for Camallanus lacustris, where invasion and loss of parasites occurred year round (Andrews, 1977),and C. oxycephalus, where invasion of the definitive host fishes was seasonally limited, mainly to July-August (Stromberg and Crites, 1975b). The latter paper is an especially significant contribution to the systematic study of the seasonal biology of nematodes. The Acanthocephala too demonstrated the phenomenon of a state of dynamic equilibrium for their occurrence in the respective host intestines. Examples of studies where this has been shown include: Acanthocephalus clavula (Chubb, 1964a; Chubb et al., 1964); Acanthocephalus lucii (Chubb et al., 1964; Andersen, 1978; Moravec, 1979b); and Pomphorhynchus faevis (Kennedy, 1967, 1972c; Kine and Kennedy, 1974b). The study of the seasonal dynamics of occurrence of fish parasites leads naturally to the wider aspects of the concepts determining the population biology of host-parasite systems. During the past ten years much interest has been generated in this area. Of particular relevance to fish parasites are the contributions of Kennedy (1970, 1975, 1977), Anderson (1974a, b, 1976a, b, c) and Holmes et al. (1977). The studies of Crofton (1971a, b) served as a significant stimulus for the more rigorous application of mathematical methodology to the investigation of host-parasite interactions, and the rapid development and availability of computers has facilitated such a trend. Models have been utilized by Anderson (1974b) to describe the biology of Caryophyllaeus laticeps in its definitive host and by Holmes et al. (1977) to describe the flow rates of Echinorhynchus salmonis in ten species of fishes from Cold Lake, Alberta, Canada. B.

PRINCIPAL AND AUXILIARY HOSTS

The phenomenon of principal and auxiliary hosts and its relevance to seasonal biology of fish helminths has been indicated in the earlier parts of this review (Chubb, 1977, 1979, 1980). In this instance the following examples are quoted. The cestode Caryophyllaeus laticeps was much more abundant, present at higher levels of incidence and intensity and during all months sampled in its principal definitive host Abramis brama at the Dnepr Delta, U.S.S.R. However, in the auxiliary hosts at this locality, Blicca bjoerkna, Rutilus rutilus heckeli and Vimba vimba vimba natio carinata, by contrast

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occurrences were sporadic through the months, and at low levels of incidence and intensity (Komarova, 1964). Molnhr (1969b) demonstrated the host-parasite relationships for the nematodes Philometra abdominalis, P. kotlani and P. ovata. Only in the principal hosts was full maturation achieved: P. abdominalis in Gobio gobio; P. kotlani in Aspius aspius; and P. ovata in Abramis brama and Rutilus rutilus parasitized by ligulid plerocercoids. In auxiliary hosts various levels of retardation of development were seen. Similar examples can be quoted for the acanthocephalans of fishes. Oien (1976) observed that Acanthocephalus anguillae grew to a greater size in Leuciscus idus than in Rutilus rutilus and a different maturation cycle was suspected. Hine and Kennedy (1974a) and Kennedy et al. (1978) divided the definitive hosts of Pomphorhynchus laevis into three categories : those in which high intensities of occurrence, growth and gravid worms were usually found, Barbus barbus and Leuciscus cephalus, perhaps also Salmo gairdneri; those with fairly high intensities of infection, in which some growth occurred, but in which the worms seldom became gravid, Leuciscus leuciscus, Salmo salar, S. trutta; and those fishes in which lower infections were seen, little growth occurred and gravid worms were not found. This latter group included about ten species of fishes in the River Avon, Hampshire, England (Hine and Kennedy, 1974a). It is evident, therefore, how necessary it is to recognize the status of a particular fish species as a principal or auxiliary host, as occurrences are likely to be higher for a longer season with greater success of maturation in the principal hosts. C.

JNVASJON OF FISHES BY LARVAE

Almost without exception transmission of the last larval stage to the definitive fish host in the species of cestodes, nematodes and acanthocephalans considered in this review was by ingestion of the invertebrate or fish intermediate hosts. Accordingly, the levels and periodicity of infection of these intermediate hosts, their availability to the definitive host fishes, the feeding behaviour and migrations of these fishes and the success of the parasite larvae in establishing in the appropriate niche within the fish definitive host all played a part in determining the ultimate seasonal biology of the parasites. It would be ideal if all seasonal studies of the adults of helminth parasites in fishes simultaneously included a study of the biology of the intermediate stages and hosts in the life cycle. In some instances this has occurred, especially where the life cycle of the parasite was the prime aim of the investigation, with seasonality as a subsidiary interest, but also in a few examples where the investigators have realized the extra benefits to be obtained by making concurrent inquiry into all stages. Only in this latter situation will the full flow pattern of the life cycle of the parasite in the environment become manifest.

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The larvae of some of the species of helminths considered in this article were present in their intermediate hosts for a short period only, whereas others were available at all times of the year. Where the information was available, it has already been noted for each species included in Section 111; however, a few examples are quoted here. The philometrid nematode third stage larvae were mostly present in copepods for a matter of a month or two only (see Furuyama, 1934; Molnhr, 1966b, 1969a; Vismanis, 1970; Yashchuk, 1974; Molnhr and Fernando, 1975; Vasil’kov, 1976; Nakajima and Egusa, 1977c; and Uhazy, 1977b). However, many cestode and acanthocephalan larvae were available in their last intermediate hosts at all times of the year, for example the cestodes Caryophyllaeus laticeps in tubificids (Kennedy 1969b; Milbrink, 1975), some proteocephalid cestodes in copepods (Pecorini, 1959), Triuenophorus species in their respective fish intermediate hosts (summarized by Kuperman, 1973) and some acanthocephalans for instance, Echinorhynchus truttae Awachie (1965) and Pomphorhynchus laevis Hine and Kennedy (1974b). In the latter examples, where the helminth larvae were present through all the year, within this general condition there were changes in the relative abundance of these stages, determined by a number of factors, but especially by the generation patterns of both the helminth species and the intermediate host species. This point was perhaps best detailed by the study of Awachie (1965) for the interactions between Echinorhynchus truttae and Gammarus pulex, where the main changes in the composition of the E. truttae developmental stages in the fish host, Salmo trutta, were also reflected in the intermediate host, G. pulex. The presence of infected intermediate hosts in the environment does not necessarily mean that invasion of the potential definitive host fishes will actually occur. The parasite larvae must be in an invasive condition, the behaviour patterns of intermediate and potential definitive hosts must be such to bring them together, and the fishes must feed on the relevant intermediate hosts. Many authors have stressed the importance of fish feeding in the acquisition of cestode, nematode and acanthocephalan parasites, including, in general, Bauer (1959a, b), Rumyantsev (1975) and Kennedy (1977), and for particular species of parasites : cestodes, Caryophyllaeus fimbriceps Bauer (1957, 1959a), Kulakovskaya et al. (19659, C . laticeps Scheuring (1929), Reinsone (1955), Kennedy (1969b), Milbrink (1975), Anderson (1976a), Khawia sinensis Kulakovskaya et al. (1969, Kupchinskaya (1969), Proteocephalus exiguus Bauer and Nikol’skaya (1957), P.$licollis Hopkins (1959), Triaenophorus nodulosus Chubb (1963a) ; nematodes, Cystidicoloides tenuissima Moravec (197lc), Philometroides sanguinea Yashchuk (1975), Raphidascaris acus Moravec (1970b) ;and acanthocephalans, Acunthocephulus clailulu Chubb (1963b, 1964a), Andrews and Rojanapaibul (1976), Andrews (1977), Rojanapaibul (1977), Brattey (1982), A. jacksoni Muzzall and Rabalais (1975a), A . lucii Brattey (1980), A . parksidei Amin (1975), Neoechinorhynchus rutili Walkey (1967), 0ien (1976), and Pomphorhynchus laevis Hine (I 970), Kennedy (1 972c) and Rumpus (1975). Relevant details have been presented for each of these species, and others,

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in Section 111, and are not repeated here. In summary, it is suggested that it is the pattern of feeding of the potential piscine definitive hosts through the year which is the most important determinant factor in the seasonal occurrence of the adult forms of cestodes, nematodes and acanthocephalans of fishes. The success of establishment of the larvae once ingested by the potential definitive host fishes will be considered below in this section. The growth and maturation of the parasites is discussed in Section V D. The migrations of fishes will influence their feeding and perhaps thereby their exposure to invasion by the species of parasites considered in this review. Valtonen (1981 a, b) has demonstrated that the seasonal occurrence of Echinorhynchus salmonis in Coregonus nasus in the Bay of Bothnia, Finland, was determined by the fishes feeding on the intermediate host Pontoporeia afinis, which in this area was available most commonly in the deeper waters. The periods of maximum occurrence of the E. salmonis were shown to be coincident with the seasons when the fishes were in the deeper waters. The success of establishment of the parasites in their definitive hosts has been experimentally investigated by Kennedy (1971) for Caryophyllaeus laticeps in Leuciscus idus, by Awachie (1972a) for Echinorhynchus truttae in Salmo trutta and by Kennedy (1972b) for Pomphorhynchus laevis in Carassius auratus. In each instance low water temperatures facilitated establishment and retention of the worms and high water temperatures, above 12-13"C, decreased establishment and in some species increased the rate of loss of the already established parasites from the fish intestines. Moravec (1970a) had also experimentally observed that at 24°C Raphidascaris acus left the intestines of its definitive hosts. As a result of field observations on the occurrence of the cestode Proteocephalus torulosus Kennedy and Hine (1969) put forward the hypothesis that seasonal changes in Leuciscus leuciscus resistance to infection by tapeworms were themselves directly dependent on temperature; that in winter resistance of the fishes was at its lowest thus permitting establishment of invasions, that rising water temperatures during spring stimulated growth of already established parasites but increased resistance to current invasions of the fishes by parasite larvae, and that at the higher water temperatures of summer host resistance had reached the point where not only newly acquired larvae could not establish, but also all the already established worms were rejected. Kennedy and Walker (1969) and Kennedy (1972~)applied the same hypothesis to explain the seasonal pattern of occurrence of Caryophyllaeus laticeps in L. leuciscus in the River Avon, England. Although Anderson (1974b, 1976a) found year round occurrence of C. laticeps in the population of Abramis brama that he studied, nonetheless he too was able to demonstrate by calculation from field data that the parasite population death rates rose with increasing water temperatures (see Fig. 11). Additional field support for the hypothesis of Kennedy and Hine (1969) was shown by the results of Awachie (1966a) for the seasonal occurrence of Cyathocephalus truncatus in Salmo trutta. The mechanism has been invoked in many other instances since the hypothesis was put forward in order to explain summer loss of some adult

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helminth populations from the intestines of their definitive fish hosts, for example by Borgstrom (1 970) for the cestode Triaenophorus nodulosus, Moravec (1979b) for the nematode Raphidascaris acus and Eure (1976b) for the acanthocephalan Neoechinorhynchus cylindratus. However, according to Mudry and Arai (1973) such a temperature-dependent resistance response was not apparent in Catostomus commersoni in which Hunterella nodulosa was found during all months of the year. In H. nodulosa from Nose Creek, Alberta, Canada, Mudry and Arai (1973) found that invasion of C. commersoni occurred during spring and summer with the adults living until the following spring.

0.0 0

5

10 15 Water temperature

20

25

(“C)

FIG.11. The relationship between the death rate per parasite per month and water temperature for the cestode Caryophyllaeus laticeps in the intestine of Abramis brama from a gravel pit near Dagenham, Essex, England. Solid circles, observed data; solid continuous line, predictions of empirical model of the form p(T) = a exp(PT) y, where a = 01376, P = 0.1153 and y = 0.3667. (From Anderson (1976a), Fig. 7, p. 292.)

+

The times of invasion for each species where known have already been given in Section 111. However, it will have been recognized from the previous discussion that two factors apply, the period of presence of the invasive larvae in their intermediate hosts in each habitat, and the actual times during which these larvae become established in the definitive host fishes. Information about both these factors was not always available, nor do many authors separate the two. In the summary given here, where possible some comment was made about the relevance of each of these two elements which when acting in combination result in the accumulation of parasites within the fishes.

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It is possible to separate a number of groupings of species of cestodes, nematodes and acanthocephalans according to the time of year when the parasites become established in their definitive hosts. However, it must be recognized that these groupings are somewhat arbitrary, and that the time of establishment for some of the species of helminth can vary with host and habitat, especially in relation to geographic locations and climate zones (see Section IV). Nevertheless it is helpful to attempt to group species showing similar characteristics together, although it should be recognized that different causal factors may be involved in each specific instance. A number of the parasites first invaded their fish hosts at the onset of early spring, and establishment continued for a relatively short period of time thereafter, usually no longer than early summer. In this category fell the cestodes Archigetes brachyurus (Kulakovskaya, 1962a, b ;Marits and Vladimirov, 1969), A . iowensis (Calentine, 1964), A . sieboldi (Kulakovskaya, 1962a, 1964a; Calentine and DeLong, 1966), Biacetabulum rnacrocephalurn (Calentine, 1965a; Calentine and Fredrickson, 1965), Caryophyllaeides fennica (KaiiC, 1970), Caryophyllaeus laticeps (Dogie1and Bykhovskii, 1939;Wunder, 1939; Halvorsen, 1972), Monobothrium hunteri (Calentine, 1965b; Calentine and Fredrickson, 1965) and the acanthocephalans Acanthocephalus anguillae (Andryuk, 1974a), Neoechinorhynchus rutili (TesarEik, 1970, 1972), Pomphorhynchus bosniacus (KaiiC, 1970) and Tanaorhamphus longirostris (Jilek, 1978b). In some of the above species, perhaps all of the members of the genus Archigetes, these cestodes could be present in their intermediate hosts all year, so that some definitive host mediated mechanism was serving to limit their occurrence in the fishes (see Section V D). A second category included those helminths whose main period of establishment in their definitive fish hosts commenced during summer, and which continued thereafter until autumn, perhaps even early winter. This included the cestodes Bathybothrium rectangulum (Kulakovskaya, 1959), Caryophyllaeides fennica (Davies, 1967; Borgstrom and Halvorsen, I968), Caryophyllaeus laticeps (Mishra, 1966), Eubothriurn crassum freshwater race (Rosen, 1919), E. rugosum (Nybelin, 1922; Tell, 1971) E. salvelini American race (Sandeman and Pippy, 1967;Smith, 1973; Boyce, 1974), Glaridacris catostomi (Williams, 1979b), G . laruei (Williams, 1979b), Hunterella nodulosa (Mudry and Arai, 1973), Isoglaridacris bulbocirrus (Calentine and Fredrickson, 1965), Khawia iowensis (Calentine and Ulmer, 1961b), K. sinensis (Sapozhnikov, 1970, 1972), Proteocephalus Jilicollis (Hopkins, 1959; Willemse, 1965, 1967, 1969; Rladland, 1979), P. percae (Rizvi, 1964; Mishra, 1966; Willemse, 1967, 1969; Wootton, 1974; Ieshko et al., 1976; Andersen, 1978; Priemer, 1979), P. stizostethi (Connor, 1953), P. tetrastotnus (Willemse, 1967), P. torulosus (Wagner, 1917; Davies, 1967; Malakhova et al., 1978), Triaenophorus crassus (Ekbaum, 1937; Miller, 1943, 1952), T. nodulosus (Rosen, 1919; Scheuring, 1929; Miller, 1943; Copland, 1956, 1957; Tell, 1971), T. stizostedionis (Miller, 1945), nematodes Carnallanus oxycephalus (Stromberg and Crites, 1974a, 1975b), Philometra abdorninalis (Moravec, 1977b), P. kotlani (Molnhr, 1969a), P. ovata (Wierzbicka, 1978), Philometroides sanguinea (Yashchuk,

HELMINTHS I N FRESHWATER FISHES

239

1974, 1975), Raphidascaris acus (Tell, 197l), Rhabdochona denudata (Pereira Bueno, 1978), R. phoxini (Moravec, 1977a) and acanthocephalans Leptorhynchoides thecatus (De Giusti, 1949), Neoechinorhynchus tumidus (Bauer, 1959a), and Tanaorhamphus longirostris (Van Cleave, 1913,1916). The seasons of invasion in these examples were probably determined mainly by the generation patterns of the intermediate host species. Other helminths which also come into line with the above, but which had shorter summer seasons of invasion included the cestodes Eubothrium crassum marine Atlantic race (Fahy, 1980), Proteocephalus buplanensis (Amin and Mackiewicz, 1977) and nematodes Goezia ascaroides (KaiiC, 1970), Philometra abdominalis (Molnhr, 1967), P. cylindracea (MolnAr and Fernando, 1975), P. fujimotoi (Furuyama, 1934), P. ovata (MolnAr, 1966b), P. rischta (MolnAr, 1966b), Philometroides cyprini (Vasil’kov, 1964, 1968a, b, 1976; Vismanis, 1967, 1970), Ph. huronensis Uhazy, 1977b) and Ph. sanguinea (Wierzbicki, 1960). A smaller number of parasites have been reported as establishing in their definitive fish hosts mainly during the autumn, winter and early spring period : the cestodes Caryophyllaeus laticeps (Kennedy, 1968, 1969b; KaiiC, 1970), Cyathocephalus truncatus (Awachie, 1966a), Glaridacris catostomi (Calentine, 1965b; Calentine and Fredrickson, 1965), Khawia armenica (Begoyan, 1977), K. sinensis (Kulakovskaya, 1962b, 1964a), Monobothrium ulmeri (Grimes and Miller, 1976), Proteocephalus torulosus (Hine and Kennedy, 1969), nematodes Philonema oncorhynchi (KOand Adams, 1969), Raphidascaris acus (KaiiC, 1970; Moravec, 1979b), Rhabdochona gnedini (Pereira Bueno, 1978) and acanthocephalans Acanthocephalus jacksoni (Muzzall and Rabalais, 1975a), A. lucii (Komarova, 1950), A . parksidei (Amin, 1975), Echinorhynchus salmonis (Tedla and Fernando, 1969, 1970), Gracilisentis gracilisentis (Van Cleave, 1913, 1916; Jilek, 1978b), Neoechinorhynchus cylindratus (McDaniel and Bailey, 1974; Ewe, 1976b), N . rutili (Steinstrasser, 1936; 0ien, 1979) and perhaps Tanaorhamphus Iongirostris (Jilek, 1978b). In some of these instances the temperature-rejection hypothesis of Kennedy and Hine (1969) has been used as explanation, C. laticeps (Kennedy, 1968, 1969b), P. torulosus (Kennedy and Hine, 1969) and N . cylindratus (Eure, 1976b), and it will probably apply to further species. In other examples it seems likely that it was the availability of the intermediate host which was the relevant factor as with A . jacksoni (Muzzall and Rabalais, 1975a). Some of the nematodes had two generations of adults each year, accordingly also two separate periods of invasion per annum. These included Capillaria coregoni (Cordero del Campillo and Alvarez Pellitero, 1976a, Alvarez Pellitero et af., 1978a), Cystidicoloides tenuissima (Moravec, 1 9 7 1 ~Hare ; and Burt, 1975; Alvarez Pellitero, 1976b; Alvarez Pellitero et al., 1978a), Raphidascaris acus (Engashev, 1964b, 1966a, 1969; Supryaga and Mozgovoi, 1974; Cordero del Campillo and Alvarez Pellitero, 1976a; Alvarez Pellitero, 1978; Alvarez Pellitero et al., 1978a) and Spinitectus gordoni (Cordero del Campillo and AIvarez PeIIitero, I976a). In these instances it is probable that the climatic circumstances applicable in the areas where two generations per annum have been described allowed two generations of larvae to occur in the invertebrate intermediate hosts.

240

JAMES C. C H U B B

Finally, there were those helminths in which invasion and establishment in the fish definitive hosts could occur year round. These species included the cestodes Biacetabulurn meridianum (Grimes and Miller, 1976), probably Bothriocephalus acheilognathi (Liao and Shih, 1956; Davydov, 1978), Caryophyllaeides fennica (Chubb, 196l), Caryophyllaeus laticeps (Strizhak, 1971 ; Anderson, 1974a; Milbrink, 1979, Corallobothrium fimbriatum (Essex, 1927), C. giganteum (Essex, 1927), C. rninutium (Befus and Freeman, 1973), C. paraJimbriatum (Befus and Freeman, 1973), Cyathocephafustruncatus (Leong, 1975), Eubothrium crassum freshwater race (Wootten, 1972; Campbell, 1974), E. salvelini freshwater European race (Kennedy, 1978a), Glaridacris catostomi (Lawrence, 1970), Hunterella izodulosa (Calentine, 1965b; Calentine and Fredrickson, 1965), Zsoglaridacris longus (Calentine and Fredrickson, I965), probably I . wisconsinensis (Williams, 1979a), Penarchigetes species undetermined (Grimes and Miller, 1976), Proteocephalus ambiguus (Willemse, 1968), P. cernua (Molnkr, 1966a), P. exiguus (Malakhova and Anikieva, 1975), P. filicollis (Chappell, 1969a), P. juviatilis (Fischer, 1968), P. macrocephalus (KaiiC, 1970),P. osculatus (Dubinina, 1950), P. parallacticus (Freeman, 1964), P. pearsei (Tedla and Fernando, 1969), Spartoides wardi (Williams and Ulmer, 1970), Triaenophorus nodulosus (Michajlow, 1951; Markova, 1958; Chubb, 1963a, 1964b; Rizvi, 1964; Mishra, 1966; Borgstrom, 1970; Halvorsen, 1972; Kuperman, 1973), nematodes Camallanus lacustris (Mishra, 1966; Wierzbicki, 1970; Andrews, 1977; Andersen, 1978; Moravec, 1979b), Cystidicola farionis (Leong, 1975), Philometra obturans (Molnar," 1976; Moravec and Dykovi, 1978; Moravec, 1979b), Raphidascaris acus (Zitiian, 1973) and acanthocephalans Acanthocephalus anguillae (0ien, 1979), A . clavula (Chubb, 1964a; Andrews and Rojanapaibul, 1976; Rojanapaibul, 1977; Brattey, 1982), A . Iucii (Rizvi, 1964; Mishra, 1966; Andersen, 1978; Moravec, 1979b), A. parksidei (Amin, 1977; Amin and Burns, 1978, except June), Echinorhynchus lateralis (Sandeman and Pippy, 1967), E. salmonis (Amin and Burrows, 1977; Amin, 1978a), E. truttae (Awachie, 1965), Neoechinorhynchus rutili (Walkey, 1967), N . saginatus (Muzzall and Bullock, 1978), Paulisentis missouriensis (Keppner, 1974) and Pomphorhynchus laevis (Hine, 1970; Kennedy, 1972c; Rumpus, 1975). It must be stressed that, notwithstanding the year-round potential for invasion by the above species, nevertheless many established most abundantly at one period of the year; details where available have been given in Section 111. As will have been seen the above listings were not mutually exclusive. Some of the helminth species were included in two or more of the groupings, perhaps reflecting changed situations in different climate zones (see Section IV) and probably also indicating the evolutionary adaptability inherent in the genetic makeup of the species. Furthermore a few species in which special circumstances applied have not been included : Archigetes limnodrili, where a fish host was not required, see Section 111 p. 5 ; Proteocephalus ambloplitis, where the migration of parenteric pleroceroids into the host intestine occurred, see Section IT1 pp. 82-85; and species for which the information concerning invasion times was lacking.

HELMINTHS I N FRESHWATER F I S H E S D.

24 1

GROWTH AND MATURATION OF THE HELMINTHS

Once invasion of and establishment in the fish definitive host had been achieved, growth and maturation occurred provided the necessary conditions were present. It should be recalled, however, that for many of the species occupying niches in the alimentary tracts of the fishes a state of continuous loss of worms was manifest so that in the end only a proportion of the numbers establishing in the first instance would actually reach maturity (see Section V A). A few species of helminths were already sexually functional or gravid on arrival in the intestines of their definitive host fishes. Thus, some members of the genus Archigetes, A. bruchyurus (Kulakovskaya, 1962a, 1964a), A . limnodrili (Kennedy, 1965a) and A. sieboldi (Wihiewski, 1930; Kulakovskaya, 1962a, 1964a; Calentine and De Long, 1966) mainly arrive in their fish hosts containing eggs, which were probably shed within a short interval of time owing to the brief survival of these worms in the fish intestines (Nybelin, 1962). Individuals of Archigetes iowensis may have a longer survival time but even in this example Calentine (1964) never found immature specimens in fishes. Cyuthocephulus truncutus can also accumulate eggs whilst contained within the body of the intermediate host (Wihiewski, 1932a; Amin, 1978b) and Curyophyllueus luticeps can form fully developed genitalia which function at once on establishment in the fish host (Sekutowicz, 1934). The males of Acunthocephulus lucii contained active sperm in their last stage of development in the intermediate host, and the ovary of the female worms was already fragmented into ovarian balls (Brattey, 1980). However, for the majority of species of cestodes, nematodes and acanthocephalans considered here a period of growth in the fishes was required prior to accumulation of eggs, andlor larvae. Some species can re-establish in piscivorous fishes if their initial definitive host fish is taken as prey, and this has been demonstrated experimentally for Echinorhynchus sulmonis (Hnath, 1969). The cestodes relevant here are hermaphrodite, the nematodes and acanthocephalans dioecious. The cestodes with the exception of the caryophyllaeids produce a strobila, and many authors hake found it necessary to recognize and separate a series of stages to describe the successive development and maturation of these worms. Where appropriate, details have been provided in Section 111, but some of the species for which such stages have been devised include Archigetes limnodrili (Kennedy, 1965a), A . sieboldi (Nybelin, 1962), Curyophyllueides fennicu (Davies, 1967), Curyophyllueus luticeps (Mishra, 1966; Davies, 1967; Anderson, 1974a), Glaridacris luurei (Williams, 1979b), Monobothrium ulmeri (Grimes and Miller, 1976), Proteocephulusfilicollis (Hopkins, 1959), P. percue (Wootten, 1974), P. torulosus (Davies, 1967; Ieshko et ul., 1976) and Triuenophorus nodulosus (Chubb, 1963a; Mishra, 1966; Borgstrom, 1970; Kuperman, 1973). The stages certainly help in the description of the process of maturation, but regrettably, are often not readily comparable from one author to another even within one species without reference to the descriptive details supplied by each

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author (see for example, Triaenophorus nodulosus, stages of Chubb, 1963a, p. 58 and Kuperman, 1973, p. 61). It would help considerably if, in future, the stages described could follow a more uniform and universal pattern. It is recommended that the stages should be of universal application so far as possible, as this would facilitate comparison of field and laboratory studies. Thus the methods and phases described by Bell and Smyth (1958) form an ideal basis for the stages (see Table VII). Up to the present time such detail has not been sought in field studies, for example in the Chubb (1963a) scheme for T. nodulosus where Stage I1 included all the Bell and Smyth (1958) phases from cell multiplication (1) up to egg-shell formation and vitellogenesis (6). However, a more critical analysis of the field material would provide useful additional information about timing. Furthermore, the later stages in the Chubb (1963a) scheme would require sub-division of the Bell and Smyth (1958) phase 7, so that Chubb Stage 111 represented egg accumulation within T. nodulosus in the fish intestine, Stage IV a condition where egg release could be stimulated artificially, but was not occurring naturally within the fish, and Stage V where egg release was actually taking place from the worms whilst in the intestine of the living fishes. These stages could be described, as indicated above, and numbered VIIIa, VIIIb and VIIIc respectively (see Table VII). The presence, numbers, growth and maturation of helminths in fishes can be influenced by the sex of the individual host, by the stage of sexual development in the life cycle of the host and by the phase of gametogenesis as reflected by hormonal release and the action of hormones on the parasite. Unfortunately, although examples can be cited where positive relationships can be inferred, many others can also be quoted where, apparently, no relation to the sexual attributes of the host has been observed. Hence, no definitive conclusions can be reached, and there is a need for critical and detailed experimental investigations. Thomas (1964) in a seasonal study of helminth burdens of Salmo trutta observed that female fishes of three years of age and older at spawning, or during recovery from spawning, tended to have heavier infections of parasites than males. However, during the season of growth and maturation of the gonads this trend was reversed or became less marked. In the instance of S. trutta that were not spawning or spent the statistically significant differences showed the males to be more heavily infested than the females. The reasons for these differences were discussed, but no firm conclusions concerning the mechanisms producing the effects were possible, and more field and laboratory studies were urged (Thomas, 1964). Calentine (1962, 1964) observed that Archigetes iowensis occurred only in Cyprinus carpio during the spawning period of the fishes. Sexually mature C. carpio had a greater incidence and intensity of infection by A. iowensis than did immature individuals, and the only positive results obtained from experimental invasions of fishes were during May, when fish infections occurred in nature. Oligochaete intermediate hosts carried A. iowensis at all times of the year (Calentine, 1964). Borgstrom and Halvorsen (1968) implicated

TABLEVII Stages of maturation of adult Platyhelminthes The criteria recommended for the recognition of developmental phases in the trematode DipIostomum phoxini and the cestode DiphylIobothrium sp. in in vitro culture (after Bell and Smyth, 1958; Smyth, 1976), with additional comments to apply to the recognition of

these stages in field material. Development in experimental conditions, after Bell and Smyth (1958), Smyth (1976) Phase Criterion recommended Method of detection

proposed stage numbering

Additional comments pertaining to field material

0. No differentiation

Stage I

Compare with larvae from intermediate hosts

1. Cell multiplication

Mitoses counts

Aceto-orcein squashes after colchicine treatment 2. Segmentation or Division into proglottids Direct observation on living body shaping (Diphyllobothrium) or material or aceto-orcein regions (Diplostomum) squashes 3. Organogeny Appearance of uterus and Squashes or whole mounts testes primordia 4. Early gametogeny Appearance of “rosette” Squashes and “comma” stages in spermatogenesis 5. Late gametogeny Appearance of mature Squashes or unstained teases spermatozoa 6. Egg-shell formation Presence of egg-shell Histochemical tests Diazo +ve, and vitellogenesis precursors in vitelline Catechol +ve (if applicable cells for order) 7. Oviposition Appearance of fully Direct observation on living formed egg material or catechol-treated whole mounts (if applicable)

Stage I1 Stage I11 Stage IV Stage V Stage VI Stage VTI

I

In most “field stage schemes” to date these stages are lumped together, usually as Stage I1 (see for instance, Chubb, 1963a). Use of the methods of detection (column 3) allow separation in field material as in material obtained by in vitro or in vivo experiments

J

Stage VIIIa Accumulation of eggs in uterus Stage VIIIb Accumulated eggs released by artificial stimulus, placing worms in cold water h, Stage VIIIc Oviposition, evidence of egg release $ in intestine of host, e.g., empty uteri visible, eggs in faeces

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JAMES C. CHUBB

host sex to account for the absence of infection of Curyophyllueidesfennica in 25 male Rutilus rutilus and its presence in 12 of 118 females of the same species. Kennedy (1968, 1969b) considered that the maturation of Curyophyllueus luticeps in Leuciscus leuciscus was influenced by the host hormones ; however, this effect was not evident in other C. luticeps investigations. Lawrence (1970) pointed out a slight statistical significance in occurrence of Gluridacris luruei between male and female Cutostomus commersoni, but offered no explanation. A similar situation was described in more detail for Monobothrium ulmeri by Grimes and Miller (1976). Male Erimyzon oblongus had higher mean intensities of infection from February to May, but females acquired a progressively higher intensity from March to May and by June 1972 surpassed that of the males. Maturation of M . ulmeri was also related to host sex. Gravid worms in January and February 1972 were recovered from male E. oblongus only, although nearly twice as many female fishes were examined. In April gravid worms were first recovered from female fishes, from April to July 368 gravid cestodes were obtained from female, and 305 from male E. oblongus. The mean intensities and occurrence of gravid individuals of M . ulmeri in male and female fishes corresponded closely to the development of the secondary sexual characteristics, tubercles on the snout and fins of the male E. oblongus, and the testes and ovaries during the winter and early spring. Small blunt tubercles on the snout of male fishes were first seen in January 1972. In February, one male with large sharp tubercles was collected, and by March all male fishes displayed fully developed tubercles. Half of the males in April had mature tubercles and the other half displayed degenerating tubercles, whilst all male fishes from May to August 1972 exhibited degenerating tubercles on their snouts. Males with mature testes were collected February to April 1972, roughly corresponding to the period of tubercle development, whilst female fishes with ripe ovaries were not collected until April, after which only spent females were recovered (Grimes and Miller, 1976). However, as pointed out earlier in Section I11 (p. 26), the relationship could be concurrent rather than causal. Similar close relationships between the maturation of cestodes and that of their hosts have been stressed by R~rdland(1979) for Proteocephalus jilicollis-Gasterosteus aculeutus, Libin (1951) for Triaenophorus crussusEsox lucius and Halvorsen (1972) for T. nodulosus-E. lucius. Indeed Engelbrecht (1963) claimed that the loss of gravid proglottids of T. nodulosus from the intestine of E. lucius was decisively influenced by the host spawning time; however, Kuperman and Shul’man (1972) have demonstrated experimentally that water temperature was the causal factor. The study of Libin (1951) is of especial interest, because he attempted experiments with E. lucius and injected pituitary extract in order to separate the concurrent influences of water temperatures and host pituitary gland secretions. Unfortunately the experiments which have been described earlier (p. 57) were not conclusive, so that the matter remains unresolved. The occurrence of a period of rapid growth in the females of the nematode Cumallanus oxycephulus during the period when the host fishes, Morone

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245

chrysops, were spawning prompted Stromberg and Crites (1975b) to speculate that this might be stimulated by rising host hormone levels. Moravec (1971~) observed the loss of the autumn generation of Cystidicoloides tenuissima from the intestines of Salmo trutta during the host spawning period, November-January, but he attributed this to a reduction or suspension of host feeding. Again, Uhazy (1977b) observed that with Philometroides huronensis in Catostomus commersoni growth and production of eggs were concurrent with rising water temperatures and changes in the physiology of the hosts owing to spawning activity. Because of the fishes of the first age group being non-spawners, but also being infected, he speculated that the development of the nematodes might be independent of physiological changes associated with spawning, even if the events were coincident. In Philonema agubernaculum, however, Meyer (1960) suspected that the peak larval activity and release was simultaneous with the spawning of Salmo salar and Salvelinus fontinalis, and Platzer and Adams (1967) demonstrated a concurrence of host spawning and larval release in Philonema oncorhynchi. In this latter nematode the greater length of the development period was coincident with the maturation cycle of the Oncorhynchus nerka, and may have been dependent on the hormones of the fishes (see p. 149). In Salmo trutta in Czechoslovakia a rapid decline in intensity of occurrence of Raphidascaris acus during December to February was attributed to a cessation of feeding by the fishes at spawning in November to January (Moravec, 1970b).However, the maturation of Truttaedacnitis truttae larvae in transformer and metamorphosed adult Lampetra planeri (Moravec and Malmqvist, 1977; Moravec, 1979~)and L. lamottenii (Pybus et al., 1978b) was thought to be influenced by the hormones produced during the metamorphosis of the lampreys (Moravec and Malmqvist, 1977; Pybus et al., 197813). In the acanthocephalans Thomas (1964) found Neoechinorhynchus rutili to be more common in older female Salmo trutta than males both during and after the spawning season. He considered this difference to relate to differences in host physiological resistance rather than to behavioural or ecological differences of the two sexes. However Eure (1974) observed that female Micropterus salmoides were more heavily parasitized by Neoechinorhynchus cylindratus during every season, and Muzzall and Bullock (1978) observed gravid Neoechinorhynchus saginatus in small non-reproducing Semotilus corporalis which suggested that sex hormones did not influence the maturation of this acanthocephalan. With Echinorhynchus salmonis Tedla and Fernando (1970) observed that most of the acanthocephalans were mature when Perca javescens were spawning, but they did not regard any possible hormonal effect as important, as parasites in fishes spawning during autumn also matured in spring (Bauer, 1959a). Amin (1978a) subsequently examined autumn spawning Oncorhynchus tshawytscha and found that the female E. salmonis in spawning fishes were significantly more mature and posteriorly displaced than in non-spawning hosts and with proportionally fewer ,male parasites as was characteristic of acanthocephalans in the latter part of the infection cycle owing to their earlier elimination. A similar trend was ob-

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served by Amin (1975) for Acanthocephalus parksidei; hence Amin (1978a) considered host breeding to be a significant factor influencing the timing of acanthocephalan recruitment and mortality and thus their seasonal infection cycles. Another host factor which may or may not influence seasonality of occurrence of cestodes, nematodes and acanthocephalans is the fish immune response. Fish immune systems have been shown to be dependent on environmental temperature, in that they were most evident and rapid in operation above 10°C (Avtalion et al., 1973; Corbel, 1975; Cottrell, 1977). Claims that responses of the fish immune system were involved in seasonality of occurrence have been made by Wagner (1954) €or Proteocephaius tumidocollus, Kanaev (1956) for Caryophyllaeus jimbriceps in Cyprinus curpio, Kennedy and Walker (1969) for C. laticeps in Leuciscus leuciscus, and Williams (1 979b) for Glaridacris laruei in Catostomus commersoni. Kennedy and Walker (1969) failed to detect antibodies to the antigens of C. laticeps in infected L. leuciscus, but clearly demonstrated the temperature dependent rejection response, although the principle of operation was not known. The relevance of this response to seasonal cycles has been discussed earlier (p. 236). Harris (1970, 1972) showed that Leuciscus cephalus produced precipitins against Pomphorhynchus laevis, but these did not appear to affect the worm populations in any way, and he failed to demonstrate the production of skin-sensitizing antibody against C. laticeps by L. leuciscus (Harris, 1973). Even today the role of the fish immune system against helminth parasites remains uncertain (McArthur, 1978). Although the inability of a parasite to reach maturity in a particular fish has often been regarded as evidence of immunity, such conclusions are ill-founded, as arrested development may in fact represent the biochemical unsuitability of the host (Harris, 1972). The details of timing of growth, maturation and egg or larval release by the adult cestodes, nematodes and acanthocephalans have already been furnished in depth for many of the species in Section 111 and variations in timing within and between climate zones have been given for some of these species in Section IV. However, an attempt at a summary is presented here, but as will be appreciated, even within a single species, sometimes quite dramatic differences have been reported. This summary lists the main periods when gravid worms have been recorded. For each species the longest psriod is taken as representing the biological potential of that species. Four main categories can be distinguished, although as is usual in biological situations there are tendencies for overlap at the boundaries. 1. Gravid spring to early summer, i.e. within the first three months of the warm season in mid-latitude climate zones, April-June most commonly in the northern hemisphere, but May-July in the colder zones 3e and 4a, and earlier in the warmer zones 2a and 2b, perhaps March-May: cestodes Archigetes brachyurus (Kulakovskaya, 1962a, b ; Marits and Vladimirov, 1969), A . iowensis (Calentine, 1964), A. sieboldi (Kulakovskaya, 1962a, 1964a; Calentine and DeLong, 1966), Buthybothrium rectangulum (Kulakovskaya, 1959), Cyathoceplralus truncatus (Awachie, 1966a), Eubothrium rugosum

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(Nybelin, 1922; Kuitunen-Ekbaum, 1933b; Tell, 1971), Glaridacris catostomi (Calentine, 1965b; Calentine and Fredrickson, 1965; Lawrence, 1970), Proteocephalus buplanensis (Amin and Mackiewicz, 1977), P. exiguus (Malakhova and Anikieva, 1975), P. percae (Rizvi, 1964; Mishra, 1966; Willemse, 1967, 1969; Wootten, 1974; Ieshko et al., 1976; Andersen, 1978; Priemer, 1979), Triaenophorus amurensis (Kuperman, 1967b; 1973), T. crassus (Michajtow, 1932; Ekbaum, 1937; Miller, 1943, 1952; Miller and Watkins, 1946; Libin, 1951 ; Vik, 1959; Kuperman, 1973), T. meridionalis (Kuperman, 1973), T. nodulosus (Rosen, 1919; Nybelin, 1922; Scheuring, 1929; Miller, 1943; Michajlow, 1951 ; Copland, 1956, 1957; Markova, 1958; Chubb, 1963a; Engelbrecht, 1963; Rizvi, 1964; Mishra, 1966; Borgstrom, 1970; Tell, 1971 ; Halvorsen, 1972; Kuperman, 1973; Moravec, 1979b), T. orientalis (Kuperman, 1967b, 1973), T. stizostedionis (Miller, 1945), nematodes Contracaecum aduncum (KaiiC, 1970), Dichelyne bullocki (Kuzia, 1979), Philometra cylindracea (Molnar and Fernando, 1973, P. fujimotoi (Furuyama, 1934), P. kotlani (Molnhr, 1969a), P. ovata (Molnar, 1966b; Wierzbicka, 1978), P. rischta (Molnar, 1966b; Wierzbicka, 1978),Philometroides carassii (Nakajima and Egusa, 1977c), Ph. cyprini (Vasil’kov, 1964, 1968a, b, 1976; Vismanis, 1967, 1970), Ph. huronensis (Uhazy, 1977b), Ph. sanguinea (Wierzbicki, 1960; Yashchuk, 1974, 1975), Rhabdochona gnedini (Pereira Bueno, 1978 ; Alvarez Pellitero et al., 1978a), R. phoxini (Moravec, 1977c) and acanthocephalans Gracilisentis gracilisentis (Van Cleave, 1913, 1916; Jilek, 1978b). 2. Gravid late spring-summer, i.e., over the later months of spring and summer, a period of about four months of the warm season in mid-latitude climate zones, normally June to September, but longer in the warmer climate zones 2a and 2b and shorter in the colder zones 3e and 4a: cestodes Biacetabulum macrocephalum (Calentine, 1965a; Calentine and Fredrickson, 1965), B. meridianum (Grimes and Miller, 1976), Corallobothrium minutium (Befus and Freeman, 1973), C. paraJimbriatum (Befus and Freeman, 1973), Isoglaridacris bulbocirrus (Calentine and Fredrickson, I965), Khawia iowensis (Calentine and Ulmer, 1961b), K. sinensis (Sapozhnikov, 1970, 1972), Monobothrium hunteri (Calentine, 1965b; Calentine and Fredrickson, 1965), M. ulmeri (Grimes and Miller, 1976), Proteocephalus ambloplitis (Fischer and Freeman, 1969; Esch et al., 1975), P. dubius (Zschokke, 1884), P. fallax (Kraemer, 1892), P. fluviatilis (Fischer, 1968), P. osculatus (Dubinina, 1950), P. pearsei (Bangham, 1929, P. stizostethi (Connor, 1953), P. tetrasfomus (Willemse, 1967), P. torulosus (Wagner, 1917; Malakhova et al., 1978), nematodes Camallanus oxycephatus (Spa11 and Summerfelt, 1969; Stromberg and Crites, 1974a, 1975b), Cystidicola farionis (Leong, 1975), Philometra abdominalis (Moravec, I977b) and acanthocephalans Neoechinorhynchus cylindratus (Eure, 1974, 1976b), N . tumidus (Bauer, 1959a). 3. Gravid individuals found spring to autumn, i.e., over all the warmer months of the year, a period of some 6-8 months, April-November in many mid-latitude climate zones : Bothriocephalus acheilognathi (MolnQr,.1968b; Nakajima and Egusa, 1976, 1977a; Davydov, 1978-but all year in zone 2b Liao and Shih, 1956), B. claviceps (Chubb, 1961 ;KaiiC, 1970), Corallobothrium

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fimbriatum (Essex, 1927), C . giganteum (Essex, 1927), Glaridacris laruei (Williams, 1979b), Zsoglaridacris longus (Calentine and Fredrickson, 1965), I. wisconsinensis (Williams, 1979a), Proteocephalus cernua (Molnzir, 1966a; Willemse, 1969), P . parallacticus (Freeman, 1964), nematodes Capillaria acerinae (Thieme, 1964), and acanthocephalans Leptorhynchoides thecatus (De Giusti, 1949), Tanaorhamphus longirostris (Van Cleave, 1913, 1916; Jilek, 1978b). 4. Some gravid individuals present during every month of the year in mid-latitude climate zones, even though peak egg or larva production is probably during the warmer seasons : Caryophyllaeides fennica (Chubb, 1961; Mishra, 1966; Davies, 1967), Caryophyllaeus laticeps (Strizhak, 1971; Anderson, 1974a, I976a; Milbrink, 1975), Eubothrium crassum freshwater race (Wootten, 1972), marine Atlantic race (Fahy, 1980), E. salvelini freshwater European race (Kennedy, 1978a), Hunterella nodulosa (Calentine, 1965b;Calentine and Fredrickson, 1965), Penarchigetes species undetermined (Grimes and Miller, 1976), Proteocephalus jifilicollis (Chappell, 1969a), Spartoides wardi (Williams and Ulmer, 1970), nematodes Camallanus lacustris (Zschokke, 1884; Mishra, 1966; Wierzbicki, 1970; Andrews, 1977 ; Andersen, 1978;Moravec, 1979b), Capillariapetruschewkii (Molnzir, 1968b),Philometra obturans (Molnar, 1976; Moravec and Dykovh, 1978 ; Moravec, 1979b), Rhabdochona denudata (Pereira Bueno, 1978), acanthocephalans Acanthocephalus anguillae (Oien, 1979), A . clavula (Chubb, 1964a; Andrews and Rojanapaibul, 1976; Rojanapaibul, 1977; Andrews, 1977; Brattey, 1982), A . lucii (Rizvi, 1964; Mishra, 1966; Andersen, 1978; Moravec, 1979b), A. parksidei (Amin, 1977), Echinorhynchus lateralis (Sandeman and Pippy, 1967), E. salmonis (Leong, 1975; Amin and Burrows, 1977; Amin, 1978a), E. truttae (Awachie, 1965), Neoechinorhynchus rutili (Walkey, 1967), N . saginatus (Muzzall and Bullock, 1978), Paulisentis rnissouriensis (Keppner, 1974), and probably Pomphorhynchus bulbocolli (Lawrence, 1970), P. laevis (Hine, 1970; Kennedy, 1972c; Rumpus, 1975). A few additional remarks are required. Fahy (1980) suggested that Eubothrium crassum marine Atlantic race (category 4 above) might remain gravid for two years or longer. This is the only perennial adult cestode of fishes reported so far. The nematode species with two generations per annum were omitted above, they included : Capillaria coregoni (Cordero del Campillo and Alvarez Pellitero, 1976a; Alvarez Pellitero et al., 1978a), Cystidicobides tenuissima (Moravec, 1971c; Hare and Burt, 1975; Alvarez Pellitero, 1976b; Alvarez Pellitero et al., 1978a), Raphidascaris acus (Engashev, 1964b, 1966a, 1969; Supryaga and Mozgovoi, 1974; Cordero del Campillo and Alvarez Pellitero, 1976a; Alvarez Pellitero, 1978; Alvarez Pellitero et al., 1978a) and Spinitectus gordoni (Cordero del Campillo and Alvarez Pellitero, 1976a). The nematodes where host maturation and spawning and parasite spawning were coincident were also omitted, they included : Philonema agubernaculum (Meyer, 1960; Vik, 1964), P . oncorhynchi (Platzer and Adams, 1967; Lewis et al., 1974) and Truttaedacnitis truttae, at least in Lampetra species, if not whilst in other hosts (Moravec and Malmqvist, 1977; Pybus et al., 1978b).

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Other species discussed in Section I11 of the review, but not placed in the categories above, require further investigation. However Muzzall and Rabalais (1975a) did not find Acanthocephalus jacksoni during the period August to October in a detailed investigation, and the failure to find the worms at this time was attributed to the absence of the intermediate hosts Lirceus lineatus. In all probability, in other localities, A.jacksoni will be found to fall into category 4. The division of the helminths into the four categories represents the artificial separation of segments along a cline, ranging from species with year round continuous growth, maturation and egg or larval release in their definitive host fishes, with all of these stages normally manifest at every season, through to those species having a highly restricted pattern of growth, maturation and egg or larval release, with each of these stages normally limited to a rather precise season of the year. However, it is thought that there is a fundamental similarity of potential for growth and maturation in all the species. In any event probably all members of categories 3 and 4 can grow and mature in the fishes at any season provided that the water temperatures are within their range of tolerance. The remainder, categories 1 and 2, probably require more precise stimuli supplied through the agency of the host in order to initiate and allow the continuation of growth and maturation. In these latter categories, if the stimuli can be identified by experimental studies, then given the appropriate circumstances in an artificial situation it should be possible to obtain gravid worms at any time of the year. In a number of species migrations of the parasites within the host organs occur as egg or larval maturity is reached so as to result in a favourable site for the actual process of egg or larval release. With the tissue inhabiting philometrid nematodes this consists of a progressive developmental migration to a particular organ, for instance the fins in Philometroides sanguinea, prior to their final emergence from the host into the habitat to rupture and release the larvae (Wierzbicki, 1960). Even in the parasites inhabiting the alimentary tracts of their hosts, posterior maturational migrations have been observed, for instance in Camallanus oxycephalus (Stromberg and Crites, 1975b), C. sweeti (Moorthy, 1938), Rhabdochona phoxini (Moravec, 1977a), Acanthocephalus jacksoni (Bullock, 1963), A . parksidei (Amin, 1975), Echinorhynchus salmonis (Bauer and Nikol’skaya, 1957; Amin, 1978a) and E. truttae (Awachie, 1963a). E.

ABIOTIC FACTORS

Fischthal (1953), Bauer (1959a, b), Engelbrecht (1963) and others have considered the influence of both abiotic and biotic limnological factors on the life cycles and biology of fish parasites. Whilst depth, hydrogen ion concentration, light, oxygen content and salinity of waters will affect distribution of parasites, there is no evidence that they influence the seasonal occurrence of the adult stages of cestodes, nematodes or acanthocephalans

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in fishes. By contrast water temperature is an all important factor in the biology of these parasites. Almost invariably there is an inhibition of metabolism by low temperatures and a stimulatory effect, particularly for maturation, by high temperatures (Arme and Walkey, 1970). Shul’man (1979) has recently suggested that water temperature is the main factor influencing the seasonal dynamics of fish parasites. It influences the parasites both directly, and indirectly through the host. In the latter instance it can influence the feeding behaviour and resistance of the fishes to the presence of the parasites (Shul’man, 1979). However, as Kennedy (1975) has cautioned, although the general similarity in the times of maturation of different species in different hosts and the correlation with temperature suggests that the relationship may be a causal one (Chubb, 1967), this is not supported by any experimental evidence; thus whilst it may be true for some species there must be considerable doubt in other instances. In the present review temperature has been shown to influence parasite recruitment owing to changes in host feeding activity (see Section V C , p. 235), to effect establishment in the host (see Section V C , p. 236) and rejection of already established parasites from within the host (see Section V C , p. 236). It has been demonstrated to determine the length of time required for growth and maturation of many of the larval and adult stages of the parasites described in Section 111, to determine in a few instances the state of embryonation of the eggs on their release into the environment (Liao and Shih, 1956; Kuperman, 1973) and in the genus Triaenophorus to regulate the dates of mass oviposition into the habitat (Kuperman and Shul’man, 1972, 1974; Kuperman, 1973). Temperature has also been shown to influence in some manner the migration of the parental plerocercoids of Proteocephalus ambloplitis into the lumen of the intestine of Micropterus dolomieui (Fischer and Freeman, 1969, 1973; Esch et al., 1975) and M . salmoides (Eure, 1976a). It has been suggested earlier that it would be of interest to have further studies where constant water temperatures prevailed all year round in the habitat (see Daniyarov, 1975). The influence of artificial thermal pollution of the environment has been noted where appropriate in Section I11 (Strizhak, 1971; Eure, 1974, 1975, 1976a, b; Eure and Esch, 1974, 1975; Markevich et al., 1976; Pojmariska, 1976; Gruninger et al., 1977; Bauer and Solomatova, 1978; Kiseliene et al., 1978; and Pojmanska et al., 1978). In summary some helminths were of decreased and others of increased abundance depending on their thermal preferences, whilst seasonal fluctuations continued to be apparent regardless of changed water temperatures. The influence of climate zones has been discussed in Section IV. It is worth recalling once again that Levine (1978) emphasised that a clear distinction should be made between weather and climate. Weather is a composite environmental condition of temperature, precipitation, barometric pressure, humidity, wind direction and velocity, sunlight, cloud cover, and so forth, at a particular time and place. The climate determines which parasites are generally found in a particular locality, and weather determines which parasites

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will develop and infect their hosts in that locality at a particular time of a particular year (Levine, 1978). A few examples of the year to year variations in timing of annual events owing to weather conditions have been given in Section 111. Thus Geller (1957) noted the effect of a warm autumn followed by an early spring in promoting increased infections of Contracaecum bidentatum, whereas a cool autumn and a late spring abruptly decreased the incidences and intensities of occurrence. Shul’man et al. (1974) drew attention to the influence of a warm summer favouring the development of Acanthocephalus Iucii in Karelia, U.S.S.R., and Stromberg and Crites (1975b) noted that an abnormally cool summer in 1972 probably contributed to low population levels and late appearance of Camallanus oxycephalus by disrupting the timing of the parasite transmission in western Lake Erie, U.S.A. Cannon (1973) observed that at Lake Opeongo, Ontario, Canada, in 1967 there was a short spring, long summer and late autumn, but in 1968 summer came late and was short. Because of these differences many of the events in 1968 were displaced a month or more. Cannon (1973) stated that those events relating to diet occurred a month earlier and those relating to parasite incidence occurred a month later. Displacement of parasite cycles in relation to temperature has also been described by Dogie1 (1958). Clearly an understanding of the fluctuations of diet and parasites in freshwater fish populations will depend upon an appreciation of the influence of temperature upon the whole ecosystem (Cannon, 1973). Bauer (1959a) introduced the concept of degree-days from ecology into the study of fish parasites. This expression, the sum of degrees per day of development, has not been used in the present account, as it was not considered to assist in the understanding of the information presented. It is clear from the preceeding paragraphs that water temperature is the most important abiotic factor involved in the seasonal patterns of occurrence of fish parasites in freshwaters. Nevertheless, it is important to heed the warning of Kennedy (1975) as noted at the beginning of this section. An example will serve to illustrate the point. In the growth and maturation of the cestode Triaenophorus nodulosus, as in other members of the genus, growth commences at a time of falling water temperature and egg accumulation starts at some period about mid-winter. Egg release occurs during a period when water temperatures are rising in spring and early summer (Chubb, 1963a; Kuperman, 1973). It has been demonstrated by experiment that temperature influences egg release, by a “total warmth” factor, higher total warmth values being required at lower water temperatures (Kuperman and Shul’man, 1972), but the causal factors for the initiation of growth and egg production have not so far been clarified. Libin (1951) attempted to show experimentally the influence of host hormones on the development of Triaenophorus crassus, but his results were inconclusive. Although water temperature may be involved, it remains to be confirmed. A rather similar growth and maturation pattern, commencing about December, has also been shown for Proteocephalus percae (Wootton, 1974) and P. torulosus (Kennedy and Hine, 1969). As Wootten (1974) pointed out, Willemse (1965, 1969)

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experimentally demonstrated that when PercafEuviatiliswith natural infections of P.percae at an undifferentiated stage of development were moved from water temperatures of 0 4 ° C and placed in water at 20°C the cestodes developed proglottids and genitalia and rapidly increased in length within ten days. This result would suggest that an increase in water temperature was necessary for maturation of P . percae to occur. However, Wootten (1974) observed that in Hanningfield Reservoir, Essex, England, the maturation of the worm population began in December and January when water temperature ranged between 2-7.YC and was still falling. He suggested, therefore, that factors other than water temperature were involved in controlling the onset of maturation in P . percae. It was postulated by Wootten (1974), as discussed here in Section V D, that host hormonal levels might influence the maturation of this, and other cestodes. Such a mechanism could influence the maturation of P.percae in P.fEuviatilis as the cestode populations mature at the same time as the fishes become ripe and spawn (Wootten, 1974). In support of this view, Molnhr (1966a) observed mature P.percae only in one year and older Lucioperca lucioperca ; younger fishes contained undeveloped scolices. It is also of relevance to note that in the same study MolnAr (1966a) recovered small mature ProteocephaZus cernua, 1-3 cm long, in October in Gymnocephalus cernua, serving to remind us that a situation which applies in one host-parasite system may differ in another, even within the same genus. F.

BIOTIC FACTORS

The influence on seasonal changes of fish diet have already been discussed in Section V C (pp. 235-236). The effects of the life cycles of the intermediate host species have been indicated where known in Section 111. Overall, the levels of infection of invertebrates by helminth larval parasites are characterized by low incidences and local distribution, and seasonal changes in these populations are important in determining the occurrence of the adult parasites in the vertebrates. One example is recalled here. Awachie (1965) was able to closely and precisely relate the seasonal trends in the developmental stages of Echinorhynchus truttae in Salmo trutta with the cyclical changes of the parasite larval stages in the intermediate host Gammaruspulex (see p. 192). Interspecific interactions between parasites have been observed in some studies. Thus the positive relationship Abramis brama-Ligula intestinalis and/or Digramma interrupta-Philometra ovata was described by Molnhr (1966b, see p. 141), and Glaridacris catostomi and Isoglaridacris bulbocirrus were found together in Catostomus commersoni to a greater extent than could be attributed to chance alone (Lawrence, 1970, see pp. 21 and 24). These positive associations may result from the helminth species involved having the same intermediate hosts, or ones occupying similar niches in the habitat, and therefore being taken together preferentially during the feeding activity of the fishes. Forms of seasonal interspecific competitive exclusion have been demonstrated or postulated for the following: Biacetabulum macrocephalum

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excluded by Glaridacris catostomi in Castostomus commersoni (Calentine and Fredrickson, 1965; Williams, 1979b) (see pp. 9 and 21); B. meridianum excluded by Monobothrium ulmeri in Erimyzon oblongus (Grimes and Miller, 1976) (see pp. 10 and 25); Glaridacris laruei and G. catostomi may have interacted in C. commersoni (Williams, 1979b) (see pp. 21 and 22); Biacetabulurnbiloculoides and Proteocephalus buplanensis may have competed with Acanthocephalus parksidei for preferred niches along the intestine of Semotilus atromaculatus during May (Amin, 1975; Amin and Mackiewicz, 1977) (see pp. 85 and 188) and probably also G. catostomi and A. parksidei in C. commersoni (Amin, 1977); a similar partial separation was seen in the intestine of Gasterosteus aculeatus containing both Proteocephalus jilicollis and Neoechinorhynchus rutili (Chappell, 1969b)(see pp. 90 and 162). Andersen (1978) noted a significant negative correlation between the presence of Proteocephalus percae and Acanthocephalus lucii in Perca ,fEuviatilis.Except where one parasite species excludes another for a long season from a major portion of the host population these interactions are likely to be of rather small influence on the seasonal biology of the excluded species. Awachie (1967) studied the interactions of larvae of Echinorhynchus truttae and Polymorphus minutus in Gammarus pulex, but experimentally demonstrated that both simultaneous and successive co-invasions were possible. A result of interspecific competition was reported by Kulakovskaya (1964b) in the Ukraine, U.S.S.R. The introduced Khawia sinensis successfully competed with the indigenous species Caryophyllaeus$mbriceps in fish pond conditions, replacing it in Cyprinus carpio in certain regions of that part of the U.S.S.R. Kulakovskaya (1964b) suggested that this was partially explained by the wider spectrum of intermediate hosts utilized by K . sinensis and its ability to overwinter in the intestine of C . carpio. G.

LONG-TERM POPULATION STUDIES

Most of the seasonal studies reported in this review were undertaken over a one or two year period. It was assumed, therefore, that the fluctuations observed would be typical of most other years. It would be interesting to have longer-term studies in addition, but relatively few are in fact available. Milbrink (1 975) observed identical cycles in the system Abramis brama-Caryophyllaeus laticeps over a four year study. Partial observations, at intermittent intervals, were made of Eubothrium salvelini in Oncorhynchus nerka by Smith (1973). In this instance two periods of exceptionally low incidence were recorded, demonstrating that the usual rather stable levels could become disrupted and lower levels could then persist for several consecutive years. Stromberg and Crites (1975a) discussed the increase of the nematode Camallanusoxycephalus in WesternLakeErie, U.S.A.,from 1927comparedto 1957and 1972.Thevariations in incidenceof Raphidascarisacusin Esox lucius,Percafluviatilisand Salmo trutta at Loch Leven, Scotland, were observed from 1967 to 1972 by Campbell (1974). The most detailed long-term study to date is that of Kennedy and Rumpus

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(1977) on Pomphorhynchus laevis in Leuciscus leuciscus from the River Avon, Hampshire, England. Throughout the nine year investigation there was a similar pattern of distribution along the length of the river although at some sites abundance varied from year to year. At one specific locality levels of incidence and intensity of occurrence of P . laevis remained fairly constant over the nine year period, and annual variations fell within the natural range of monthly variation over any twelve month period. The frequency distribution showed a similar pattern over the period. Thus Kennedy and Rumpus (1977) concluded that the population size of P.laevis in L . leuciscus had not changed to any great extent over the nine years. They discussed the factors involved and concluded that either the population size was determined primarily by the climatic and ecological conditions of the habitat, with no feed-back system, and that these had remained constant over the nine year period of observation, or feed-back controls operated to regulate the population size, but had not yet been identified. Kennedy and Rumpus (1977) stressed the need for more similar information. H.

AN HYPOTHESIS FOR SEASONAL OCCURRENCE

The seasons are the divisions of the year determined by consistent annual changes of the weather. Apart from the tropics and polar regions the predominant feature of the annual cycle is a temperature fluctuation between a minimum and a maximum. This change results from the annual variation in the angle at which the rays from the sun reach the surface of the earth and from the annual variation in the duration of sunlight on the surface of the earth each day. As the earth moves in its orbit, its axis maintains a nearly constant orientation in space, inclined about 66"33' to the orbital plane. During the half of each orbit when the north pole is inclined towards the sun, a point in the Northern Hemisphere receives the rays of the sun at an angle closer to 90" than does a point in the Southern Hemisphere. This alIows greater heating and more hours of daylight. In the Northern Hemisphere this event occurs six months later than in the Southern Hemisphere, accordingly, the seasons are reversed in the two hemispheres. In essence, therefore, all seasonal phenomena result from the annual changes of photoperiod and temperature which in combination with the features of geomorphology at any particular point on the earth result in climate. Climatic conditions change with latitude and altitude, but remain consistent in a given area for long periods of time, whereas the weather conditions vary from year to year. The annual changes in photoperiod are unlikely to influence the helminths considered here directly, except perhaps the ectoparasitic Monogenea (Shul'man 1977). However, the lives of their invertebrate and vertebrate hosts are so influenced directly, and thus the helminths are liable to be secondarily affected. For example the changes in photoperiod can be a stimulus initiating the reproductive cycle in seasonally breeding species of fishes. Although the physiological and endocrinological changes involved in response to this environmental trigger mechanism have not been identified, it is probable

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that, where hormonal or breeding condition of the fishes has also been suggested as a trigger for the reproduction of the parasite, that we are seeing the indirect influence of photoperiod on the biology of the helminths. The annual changes in temperature, manifested by the cycle of warming and cooling of freshwaters, have profound and direct effects on the helminth seasonal biology. It is of course true that most of these relationships are coincident, not only with seasonal changes of temperature, but also with other changes in host biology, so that the direct causal influence remains to be shown by experiment in many instances. Nonetheless, studies on the development of the larval stages of the helminths in different temperature regimes have clearly shown, as for living material in general, that there are minimum, optimum and maximum temperatures for growth and maturation. Temperature also acts on the helminths indirectly in its influences on the biology of the host species. In particular, the feeding behaviour of the host can change with temperature and the temperature-dependent rejection response in fishes becomes more strongly manifest as the water temperatures increase above about 12°C. The interactions of the seasonal changes in status and behaviour of the populations of potential intermediate and definitive host species are also of vital importance in determining seasonal occurrence of the helminth parasites of fishes. These interactions, variable between climate zones, discrete habitats and principal and auxiliary hosts almost certainly explain the great variations in seasonal cycle patterns which can occur in some instances within a single species of helminth. In conclusion, it is necessary to construct for each species of helminth a summary of the relevant factors which have been demonstrated or postulated to control their seasonal patterns of occurrence. Owing to the evolutionary potential inherent in the genetic composition of every species the details of control mechanisms will vary from species to species and place to place. From the data obtained so far, water temperature acting directly on the helminth, or indirectly through the host behaviour and metabolism, seems to be the most important factor determining seasonal biology in the subtropical and mid-latitude climate zones of the world. It is unfortunate that there are so few studies from tropical regions, as in these areas factors other than water temperature must apply: presumably the host interactions will play the dominant role. I.

EXPERIMENTAL STUDIES

Although in Section I11 a range of experimental studies have been described they were usually concerned with obtaining the developmental stages of the cestode, nematode or acanthocephalan life cycle, and not with the demonstration of causal factors involved in the seasonal cycle and in the annual changes pertaining thereto. What is needed is a series of in vivo laboratory experiments carried out in carefully controlled conditions of photoperiod and water temperature in order to distinguish the specific

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determinant factors needed at each stage of development of a parasite. Ideally in vitro experiments should also be undertaken to exclude all host influence and thus separate environmental and host mediated causal factors. Unfortunately, it is often quite difficult to carry out anything more than the most elementary experimentation using material obtained from field sources, owing to the problems of collecting uninfected fishes and sufficient numbers of the invasive stages of the parasites. What is required is a number of species of helminths to serve as laboratory models. The appropriate hosts would need to be easily obtainable in sufficient quantity; it would be ideal to have a species which could be bred in the laboratory. The parasites themselves would need to have potential for easy maintenance and reproduction in the laboratory, so that large numbers could be produced when appropriate for experiments. In the field of trematode biology Transversotrema patialense has filled this niche. It is suggested that the cestode Bothriocephalus acheilognathi could be a species with useful potentials for laboratory study. It has a relatively simple life cycle, one intermediate and afish definitive host, and is capable of invading and developing in a wide range of species of copepods and cyprinid fishes. The nematodes Camallanus cotti and C. fotedari and no doubt others of the genus present in small tropical fishes, have been shown to be amenable t o maintenance in the laboratory (see p. 135). A number of the acanthocephalans are potentially suitable for experimental study. They have life cycles with two hosts, and most of the amphipod, isopod or ostracod intermediates can be readily bred in captivity. Unfortunately, many of the mid-latitude acanthocephalans infect fishes inconvenient to obtain and maintain in the laboratory, so that it would be convenient to find a suitable subtropical or tropical species. The recent success of manipulation of the duration of daily light/dark photoperiod cyclesand thereby condensing the breeding cycle of Salmo gairdneri into periods of as little as six months (Bromage and Whitehead, 1980) suggests that interesting experiments could be undertaken using one of the species of acanthocephalans known to be influenced by the host breeding condition, for example Echinorhynchus salmonis. ACKNOWLEDGEMENTS

I am grateful to the late Professor Ben Dawes for inviting me to write this series of reviews for Advances in Parasitology, and to the present editors for facilitating their completion. I wish to thank Professor 0. N. Bauer, Zoological Institute, Academy of Sciences, Leningrad, for his continued interest and advice. Dr L. F. Khalil, of the Commonwealth Institute of Helminthology provided very helpful informatiom concerning the genus Hepatospina. Dr E. T. Valtonen, Department of Zoology, University of Oulu, Finland, kindly allowed me to quote from two papers in press at the time of.writing this review.

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The following members of the University of Liverpool gave essential help without which the review could not have been completed: Mr T. A. Greenan, Department of Russian, translation of Russian, Mr A. V. Knowles, Department of Russian, geographical information, Mr F. Schafer, Department of Zoology, translation of German, Miss S. Tysoe and Miss C. J. Ludlow, Harold Cohen Library, inter-library loans, and Miss A. CalIaghan, Miss D. S. Paterson and Miss S . Scott, Department of Zoology, typing of manuscript. Professor C. J. Duncan, Department of Zoology, allowed me time and facilities which are greatly appreciated. Eleven figures are reproduced from other sources, by kind permission of the authors and publishers: Figs 1 and 3, Dr 0. P. Kulakovskaya and Academia, Prague, Figs 2 and 11, Dr R. M. Anderson and Cambridge University Press, London, Fig. 4, Cambridge University Press, London, Fig. 5 Dr C. A. Hopkins and Cambridge University Press, London, Fig. 6 , Dr R. Wootten and Academic Press Inc. (London) Ltd., Figs 7 and 9, Dr F. Moravec and Academic Press Inc. (London) Ltd. and Academia, Prague respectively, Fig. 8, and Dr L. S. Uhazy and the National Research Council of Canada, Ottawa, and Fig. 10, Dr C. R. Kennedy and Cambridge University Press, London.

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WiSniewski, L. W. (1932b). Cyathocephalus truncatus, Pallas-ein Fischparasit aus dem Vrelo Bosne. Ribarski List (Fischerbtatt) 7, (3/4), 4 pp. WiSniewski, L. W. (1933a). Cyathocephalus truncatus Pallas.-I. Die Postembryonalentwicklung und Biologie. Bulletin de l’dcademie Polonaise des Sciences et des Lettres. Classe des Sciences Mathkmatiques et Naturelles. Strie B. (II)7,237-252. WiSniewski, L. W. (1933b). Cyathocephalus truncatus Pallas.-11. Allgemeine Morphologie. Bulletin de I’Academie Polonaise des Sciences et des Lettres. Classe des Sciences Mathtmatiques et Naturelles. Strie B. (11) 8-10, 31 1-327. Wolf, E. (1906). Beitrage zur Entwicklungsgeschichte von Cyathocephalus truncatus Pallas. Zoologischer Anzeiger 30, 3745. Wootten, R. (1972). Occurrence of Eubothrium crassurn (Bloch, 1779) (Cestoda: Pseudophyllidea) in brown trout Salmo trutta L., and rainbow trout S. gairdneri Richardson, 1836, from Hanningfield Reservoir, Essex. Journal of Kelminthology 46,327-339. Wootten, R. (1974). Studies on the life history and development of Proteocephalus percae (Muller) (Cestoda: Proteocephalidea). Journal of Helminthology 48, 269-28 1. Wunder, W. (1939). Das jahreszeitliche auftreten des bandwurmes Caryophyllaeus Iaticeps Pall. im darm karpfens (Cyprinus carpio L.). Zeitschrift fiir Parasitenkunde 10,704-713. Yalinskaya, N. S. (1967). (Acanthocephalan larvae and dynamics of their infection of Gammarus in the water-reservoirs of the upper Dnestr river.) Problemj Parazitologii, Year 1967, pp. 223-225. (In Russian.) Yamaguti, S. (1934). Studies on the helminth fauna of Japan Part 4. Cestodes of fishes. Japanese Journal of Zoology 6, 1-1 12. Yamaguti, S . (1959). “Systema Helminthum Volume I1 The Cestodes of Vertebrates.” pp. i-vii, 1-860. Interscience, New York. Yamaguti, S. (1961). “Systema Helminthum Volume I11 The Nematode Parasites of Vertebrates.” Part I, pp. 1-679, Part 11, pp. 681-1261. Interscience, New York. Yashchuk, V. D. (1970). (Experimental infection of invertebrates with Philometra sanguinea larvae.) Byulleten’ Vsesoyuznogo Instituta Gel’mintologi im. K. I. Skryabina No. 4, 183-187. (In Russian.) Yashchuk, V. D. (1971). (Life-cycle of Philometra sanguinea of carp.) Veterinariya 48, 73-75. (In Russian.) Yashchuk, V. D. (1974). (Dynamics of Philometroides sanguinea infections in their intermediate hosts.) Veterinariya 1974, No. 6, 69-71. (In Russian.) Yashchuk, V. D. (1975). (Ecological links between the final hosts of Philometroides sanguinea.) In “VIII Nauchnaya Konferentsiya Parasitologov Ukrainy. (Tezisy dokladov). Donetsk, Sentyabr’ 1975. Ukrainskii Nauchno-Issledovatel’skii Institut, Nauchno-Teknicheskoi Informatsii, Kiev. pp. 202-204. (In Russian.) Yeh, L. S. (1955). (On a new tapeworm Bothriocephalus gowkongensis n. sp. (Cestoda: Bothriocephalidae) from freshwater fish in China.) Acta Zoologica Sinica 7, 69-74. (In Chinese.) Yeh, L. S. (1960). On a reconstruction of the genus Camallanus Raillet and Henry, 1915. Journal of Helminthology 34, 117-124. Zitiian, R. (1973). Helminty rfb DobSinskej (Hnileckej) priehrady a ich epizootologicki viznam. BioIogickC Prrice 19 (6), 1-87. Zschokke, F. (1884). Recherches sur l’organisation et la distribution zoologique des vers parasites des poissons d’eau douce. Archives de Biologie 5, 153-241. Zschokke, F. (1891). Die Parasitenfauna von Trutta salar. Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. Abteilung 1, Originale 10, 694-699, 738-745, 792-801, 829-838.

Current Concepts on The Biology, Evolution and Taxonomy of Tissue Cyst-forming Eimeriid Coccidia. WEDAD TADROS

and J. J. LAARMAN

Department of Parasitology, University of Amsterdam and Institute of Tropical Hygiene, Amsterdam I. General Introduction 11. Toxoplasmosis and T A, Introduction.. ........ ... ......... ....... ......... .. ....... .. ..... ........ ...... ... ..... .. B. The Source of Enteric Development of the Parasite in the Feline Host C. The Developmental Cycle of Zsosporu gondii in the Intestine of the Feline Final Host .............................................................................. D. Sexual Differentiation....... .. ....... ... .. .............. ... .. .. ........................ E. Genetic Research F. Immunity of the of Development of I. gondii .........__.... .......................................... G. Pathology of ToxopIasmid Coccidiosis in the FeIid Host .................. H. The Survival, Sporulation and Dispersal of Oocysts ......... ............... I. The Structure and Excystation of the Oocyst ................................. J. Host Cell Penetration .................................................................. K. Strain Virulence and Host Susceptibility... .. L. Recent Studies on Toxoplasmosis i M. Serological Diagnosis . ................... .. .. ..... ..... .... ... .... . ....... ..... .. ... ... N. Immunity in the Intermediate Host 0. Pathology of Human Toxoplasmosis ... . ..........., .............................

E. F.

294 296 296 297 301 303 305

304 309 310 310 311 312 3 14 318 321 327 329 332 335 335 337 .................... 337 340 342 345 352 352 358 383 osis in Primates and Carnivores .. ... ridiosis in the Intermediate Host ..... 386 Pathology of Surcocysris-inducedCoccidiosis in the Final Host.. .. .. . ..... 389 Serodiagnosis .. ... ..... .. ..... ... ..... .... ... .............. .. ............... ... ......... 389 293

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C. Development of Surcocystis in Cell Cultures .................................... H. Epidemiology and Epizootiology of Sarcosporidiosis and Surcocystisinduced Coccidiosis..................................................................... VII. Frenkeliosis and Frenkeliu-induced Coccidiosis ....................................... A. Introduction and Life Cycle B. Pathology ................................................................................. C . Serology and Chemotaxono D. Immunity ................................................................................. E. Epizootiology ......................................... VIII. Current Concepts on the Taxonomy and Nome forming Coccidia........................................................................ A. Families, Subfamilies and Genera ..... B. Nomenclatural Problems in Specific Des C. Specific Designation of the Genus Frenkelia .................................... IX. Phylogenetic Considerations on the Heteroxenous Eimeriid Coccidia ......... Acknowledgements .................. .... .....

.................................................................. 1.

39 I 392 397 391 401 40 1 402 402 403 403 406 409 410 41 1 412

GENERAL INTRODUCTION

Four tissue cyst-forming protozoan organisms have long been known to parasitize vertebrate hosts. These comprised : Toxoplasma, a ubiquitous parasite with a predilection for the central nervous system of numerous homeotherms, including man ; Besnoitia, which forms cysts in various tissues of ungulates, rodents and reptiles; Sarcocystis, which as the name implies, parasitizes predominantly the musculature and is remarkably common in mammals, birds and reptiles; and Frenkelia, which forms cysts in the brains of rodents belonging to several genera. Although it has been conclusively established that toxoplasmosis as well as besnoitiosis may be acquired by the ingestion of infected tissues, carnivorism failed to account for the wide prevalence of infection with these organisms amongst strictly herbivorous animals. The natural mode of dissemination of sarcosporidiosis and frenkeliosis remained even more obscure, as most attempts at the experimental transmission of these two organisms had met with complete failure. Until recently the life cycles and consequently the taxonomic identity of these four parasites were merely subjects for conjecture. The application of electron microscopy to the investigation of the morphology of the cystic form, which obviously represented an integral stage in the developmental cycles of these organisms, revealed that the individual elongate organisms, the cystozoites, enclosed within the tissue cysts of Toxoplasma, Besnoitia, Sarcocystis and Frenkelia all possessed an apical complex of organelles characteristic of the Sporozoa (Ludvik, 1956, 1963; Garnham et al., 1962; Stnaud, 1969: Tadros, 1970a, c). The ultrastructural details of the cystozoites of all four parasites were found to be strikingly similar to each other and to be strongly reminiscent of the fine structure of the merozoites of the intensively studied coccidian genus, Eimeria. In 1965 Hutchison, in Scotland, U.K., reported transmitting Toxoplasma to laboratory mice by feeding them water-incubated faeces of a domestic cat, fed two weeks previously with toxoplasmic cysts in brain tissue. However,

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it was to take five more years of intensive research to unravel the life cycle of this intriguing organism. The infective stage in the feline faecal matter was finally identified as a coccidian oocyst and, when discovered and described, the schizogonic and gametogonic stages in the feline intestinal tissues indisputably established the eimeriid coccidian nature of this organism (for fascinating reviews on the elucidation of the sexual cycle of Toxoplasma, see Garnham, 1971 and Jacobs, 1973). The schizogonic development preceding gametogony can be initiated in the intestinal tissues of susceptible cats, not only by the ingestion of toxoplasmic stages in the tissues of infected intermediate hosts, but also directly from cat to cat by the oral intake of mature oocysts, the life cycle thus being facultatively heteroxenous. When sporulated, the newly identified oocysts of Toxoplasma were found to be disporic, tetrazoic and were considered by Werner (1970) to be very closely related, and by Overdulve (1970) to be identical, to the oocysts of Isospora bigemina of cats. In 1976, Tadros and Laarman synonymized the genus Toxoplasma with Isospora, and in the present article Toxoplasma gondii will be referred to as Isospora gondii. Recently, the tissue cysts of three different species of Besnoitia have been demonstrated to constitute intermediate stages in the life cycles of isosporid coccidian parasites of Felidae (Peteshev et aE., 1974; Wallace and Frenkel, 1975; Smith and Frenkel, 1977). The developmental cycles of all three species were found to be similar to that of Isospora gondii; however, the parasites could not be transmitted directly from cat to cat by administration of oocysts, the life cycle being obligatorily heteroxenous. The present authors have likewise synonymized the genus Besnoitia with Isospora (Tadros and Laarman, 1976). Speculations on the coccidian nature of Sarcocystis and Frenkelia (Overdulve, 1970; Tadros, 1970a, b) were substantiated by interesting observations by Fayer (1970, 1972b) on the transformation of cystozoites of an avian species of Sarcocystis, in embryonic bovine cell lines, directly into macro- and microgametocytes, with the subsequent formation of structures resembling oocysts. Rommel et al. (1972), in Western Germany, fed Sarcocystis-infected mutton to cats and observed the excretion, starting 12 to 16 days later, of mature disporic, tetrazoic oocysts or free sporocysts. Similar coccidian oocysts and sporocysts were observed in the stools of human volunteers fed Sarcocystis-infected raw beef or pork (Rommel and Heydorn, 1972) and in the faeces of dogs and cats fed Sarcocystis-infected bovine oesophageal muscle (Heydorn and Rommel, 1972a). Subsequent research by these and other authors revealed that this type of sporocyst was not infective to the final host, but when fed to the respective specific intermediate host, initiated extra-intestinal schizogonic development, followed by the formation of the familiar sarcocysts in the muscular tissue. Since then, the elucidation of the life cycles of over 20 more species of Sarcocystis has confirmed the obligatorily heteroxenous pattern of the life history of this parasite (for general reviews, see Tadros and Laarman, 1976; Dubey, 1976b; Levine, 1977a; Rommel, 1978).

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More recently, the cystozoites of Frenkelia have also been seen to undergo gametogonic development, almost identical to that of Sarcocystis, in the intestinal tissues of a bird of prey, the common buzzard, Buteo buteo (Romme1 and Krampitz, 1975; Krampitz and Rommel, 1977). The sporocysts of Frenkelia are not directly infective to the final host, the tissue cyst in the intermediate rodent host constituting an essential phase in the obligatorily heteroxenous life cycle. Thus, in the short time lapse of about five years, the basic concept of the exact nature and the mode of dissemination of these parasites had to be radically revised. The recognition of the tissue cysts of all four organisms as intermediate stages in the heteroxenous life cycles of coccidian parasites of various carnivores, and the consequent pinpointing of the central role of the oocyst in their route of transmission, necessitates a reappraisal of our understanding of the epidemiology and epizootiology of infection with these organisms in the light of the dynamics of transmission of the classic eimeriid coccidia. The present review article deals with recent advances in the study of life cycles and other biological aspects of the tissue stage-forming eimeriid coccidians and attempts to throw some light on the thorny problem of their classification. 11. TOXOPLASMOSIS AND TOXOPLASMID COCCIDIOSIS A.

INTRODUCTION

In spite of the lapse of 15 years since Hutchison, in 1965, dangled the clue to feline faecal transmission of toxoplasmosis in front of a largely incredulous scientific community, and of over a decade since irrevocable proof was furnished for the coccidian nature of this organism (Hutchison et al., 1969; Work and Hutchison, 1969a, b; Frenkel et al., 1970; Sheffield and Melton, 1970; Overdulve, 1970; Janitschke, 1970; Weiland and Kiihn, 1970; Witte and Pierkarski, 1970), substantial gaps still exist in our knowledge of the development of the parasite in the feline final host. This is no doubt attributable to the problems of containing infections transmitted by faecal oocysts, and working with adequate numbers of germfree or gnotobiotic cats, as well as to the association of pathological manifestations of the infection (and hence, medical and veterinary interest) with tissue invasion and asexual proliferation rather than with the development of intestinal coccidiosis in the feline host. In view of the copious published literature (over 3000 papers examined for the present article), and the availability of recent reviews (Jacobs, L., 1973, 1976; Jacobs, M. R., 1977; Frenkel, 1973a, b, 1974a, b, c, 1975; Hartley, 1976; Turner, 1978; Corder0 del Campillo, 1975; Beverley, 1974, 1976; Higgins, 1976; Tadros and Laarman, 1976; Anderson and Remington, 1977; Scott, 1978; Beyer, 1977; Beyer et al., 1978a; Tadros, 1980), we are confining

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ourselves to the highlights in recent biological research with particular emphasis on the host-parasite interaction in the feline host and the role of cats in the maintenance and dissemination of infection. B.

THE SOURCE OF ENTERIC DEVELOPMENT OF THE PARASITE IN THE FELINE HOST

It is now generally accepted that, under natural conditions, the schizogonic and gametogonic development of Zsospora gondii is initiated in the intestinal epithelium of susceptible cats by the ingestion of toxoplasmic stages in the tissues of mammalian or avian intermediate hosts, or by the oral intake of mature oocysts from the faeces of other infected Felidae. However, the relative efficacy of (i) the rapidly proliferating endozoites of the acute phase of toxoplasmosis (Figs 1, 2), (ii) the slowly dividing cystozoites of the chronic phase of infection (Figs 3, 4) and (iii) the newly discovered faecal coccidian oocyst (Fig. 6), in inducing the gametogonic cycle remains subject to debate.* Thus, using sero-negative adult cats, Dubey et al. (1970a) reported excretion of oocysts by 28 out of 29 cats fed chronically infected mice, with a prepatency of 3-5 days; by two out of seven cats fed spleen and liver of mice (infected 4-5 days previously), with a prepatency of 8-10 days, and by five out of ten cats fed feline oocysts, with a prepatency of 21-27 days. Wallace (1973) induced oocyst shedding in five out of eight cats fed pigeons, killed on the 6th and 7th days of acute infection, and noted a prepatent period of 5-18 days. Overdulve (1978) fed gnotobiotic cats the brains of mice, intracerebrally injected two days previously with toxoplasmic endozoites from peritoneal fluid. When killed 1 to 60 hours later, none of the six cats exhibited either intestinal or extra-intestinal infection. The author concluded that cats do not become infected when fed proliferative forms, and that these stages are of little or no importance in the acquisition of infection by Felidae. Dubey and Frenkel(l974, 1976) correlated the initiation of schizogonic and gametogonic development in the intestine of cats with the age of acute or chronic toxoplasmic infection in ingested mice. Their results indicated that ingestion of mice with 1- to 2-day-old acute infections, during which proliferative endozoites were preponderant, induced infection in 33 % and oocyst excretion in 17% of cats, with an invariably prolonged prepatent period of 26-40 days. Consumption of carcasses of mice with 3-day-old acute infections, when newly formed cysts were morphologically identifiable in the tissues, resulted in infection of five out of 19 cats, four of which shed oocysts: two with a short prepatency of six and eight days, and the others with a long prepatency of 37 days. All cats which were fed tissues of mice, inoculated 7 to 13 days previously, shed oocysts with a short prepatency of three to six days. The dynamics of oocyst excretion were similar in cats fed mice infected 4 or 30 days previously. Similar endo-epithelial stages were observed

* The terminologyused for the stages of development of 1.gondii, namely, endozoites for the rapidly proliferating organisms of the acute phase, and cystozoites for the more slowly dividing organisms of the tissue cysts, is that proposed by Hoare (1972).

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in the intestines of cats fed mice with 5 to 7, or 30-days-old toxoplasmic infection. These observations indicate that, whereas cystozoites appear to be capable of directly initiating the entero-epithelial cycle in the feline final host, the longer period of prepatency before oocyst shedding following ingestion of proliferative endozoites, suggests generalization of infection preceding reinvasion of the intestine, probably by cystozoites, to initiate schizogony and gametogony. That invasion of the intestine can take place, following extra-intestinal proliferation, is corroborated by excretion of oocysts by 63 % and 40 % of cats, parenterally inoculated with endozoites and cystozoites respectively (Dubey and Frenkel, 1976). What are the physiological differences between the endozoite, on the one hand, and the cystozoite on the other, that can account for the striking discrepancies in their respective infectivity, their ability to initiate oocyst excretion in the cat and that further determine the length of the respective prepatent period of oocyst shedding? What are the factors that trigger the transformation of endozoites into cystozoites? Answers to these intriguing questions remain largely speculative. Morphologically, cystozoites possess more electron-dense rhoptries (althoughthey are less invasive), but fewer ribosomes than endozoites (Van der Zypen and Piekarski, 1967). The increased number of ribosomes reflects an enhanced rate of division and presumably rate of metabolism of the endozoite, a stage associated with the dynamic replication of the parasite in the initial phase of acute infection of the susceptible host, as compared to the “quiescent” state of the amylopectin-storing cystozoite in the tissue cyst of the chronic phase. A major physiological difference between the endozoite and the cystozoite is the greater resistance of the latter to peptic or tryptic digestion (Jacobs et al., 1960). It has recently been demonstrated that the tolerance of the cystozoite to peptic digestion, an obvious adaptation to transmission via the digestive tract, reflects an enhanced resistance to destruction by HCI, rather than by the enzyme pepsin; the cystozoite is apparently less permeable than the endozoite (Pettersen, 1979). In this context, it is interesting that Suzuki and Tsunematsu (1973), in a proposed modification of the dye test, suggested that antigen-sites or complement-receptor sites on the cell memFIGS.1-6. Isospora gondii and I . datusi.

FIG.1. Proliferative endozoites (arrowed) of I. gondii in Giemsa-stained smear of spleen of Microtus arvalis, 4 days after oral inoculation with oocysts ( x 1320). FIG. 2. Intranuclear endozoites in the same smear (arrowed). FQG. 3. Haematoxylin and eosin-stained section of toxoplasmic tissue cyst in mouse brain ( x 1000). FIG.4. I. gondii cyst isolated from the brain of infected laboratory mouse. Note elongate cystozoites spilling out through break in the cyst wall ( x 3300). FIG.5. I. datusi tissue cyst in haematoxylin and eosin-stained section of skeletal muscle of experimentally infected laboratory mouse ( x 1320). (Preparation kindly supplied by .Prof. M. Rommel.) FIG.6a, b, c, d. I . gondii oocyst: unsporulated, sporulated and rupturing oocysts and free sporocyst respectively ( x 1OOO).

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brane of the endozoite are covered with a trypsin-sensitive substance and that, consequently, trypsin-treatment increases their susceptibility to the action of antibodies and accessory factor. The facts that (i) functional cystozoites are detectable on the third day of acute infection, when circulating antibodies first make their appearance (Dubey and Frenkel, 1972a) and (ii) rapid proliferation of the parasite is resumed when cystozoites are subinoculated into clean uninfected mice, argue for a significant role of the host immune mechanism in the transformation of endozoites into cystozoites. However, cyst-like aggregates have been observed in older cell cultures (Hogan et al., 1960). Such tightly packed groups of organisms were shown by Jacobs and Melton (1965) and Jacobs (1967) to have an increased resistance to digestion by pepsin, as compared to younger forms. More recently, Hoff et al. (1977) cultured toxoplasmic endozoites in monkey fibroblasts and found a short period of prepatency of oocyst excretion in cats fed such infected cultures, thus ingeniously establishing the presence in hese cultures, as early as six days after infection, of physiologically identifiable cystozoites. The transformation of endozoites into functional cystozoites in vitro clearly indicates that the host immune response is not the major triggering factor, although there is evidence that antibodies may enhance the process of cyst formation (Shimada et al., 1974). It is also noteworthy that endozoites go on proliferating in patients, immunosuppressed with corticosteroids, in spite of the presence of antibodies and accessory factor (Frenkel et al., 1975a). The fact that tissue cysts appear behind the brain barrier within four to seven days after infection, but in visceral organs only after 21 to 30 days (Dubey and Frenkel, 1976), argues against a significant role of circulating antibodies in cyst induction and, as suggested by Dubey and Frenkel, may indicate a role of the parasitized host tissue in the process. Matsubayashi and Aka0 (1963) studied cyst development in mice, chick embryos and cultured cells and concluded that cysts are produced whenever multiplication of the parasite slows down. The loss of the tissue cyst-forming capacity by avirulent toxoplasmic strains, rendered virulent by rapid passage in mice and then attenuated by storage (Pettersen, 1977), and the tendency of cystozoites to lose their capacity to initiate oocyst excretion in the feline host after 30-40 rapid passages in the acute phase (Frenkel, 1973a), imply that both the capacity to induce tissue cysts in the intermediate host, as well as the physiological potential of the enclosed cystozoites to initiate the entero-epithelial cycle in the final host, are genetically coded for in the endozoite stage. It would seem that, should a cystozoite find itself in the intestinal tissue of a susceptible feline host, a sequence of events is set in motion, which culminates in the schizogonic and gametogonic cycles, but that in extra-intestinal tissues of the final host or in tissues of non-specific susceptible hosts, the cystozoites revert to the proliferative endozoite stage. This remarkable flexibility in the potential sequence of asexual stages is a marked contrast to the situation in conventional eimeriid coccidia, and must be largely responsible for the ubiquitous success of this organism.

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Studies in tissue culture on the lag period and generation times following inoculation with cystozoites, endozoites or sporozoites, like those undertaken by Kusunoki (1977), are of great interest as a useful method to test candidatestimuli determining the directional shift amongst the three labilely associated sporozoic, endozoic and cystozoic stages, particularly in feline intestinal epithelial cell lines.

c.

THE DEVELOPMENTAL CYCLE OF Zsospora gondii IN THE INTESTINE OF THE FELINE FINAL HOST

1. Following ingestion of tissue cysts Developmental stages of I. gondii in the intestinal epithelium of cats, fed toxoplasmic tissue cysts, have been observed under the light microscope by Weiland and Kuhn (1970), Zaman and Colley (1970), Piekarski and Witte (1971), Hutchison et al. (1970, 1971) and Walton and Werner (1970). However, by far the most detailed description of the intestinal stages was given by Dubey and Frenkel(1972a). Developmental stages were microscopically identified in histological sections of the small intestine of newly born to ten-week-old kittens, two hours to 27 days after infection. Dubey and Frenkel recognized asexual division in the intestinal stages by endodyogeny,endopolygeny and schizogony as well as “splitting”. The authors identified five division forms on the basis of structural details, type of division and time limited occurrence : type A (12 to 18 h), type B (12 to 54 h), type C (24 to 54 h), type D (32 h to 15 days), subdivided into three subtypes, and type E (3 to 15 days after infection). Overdulve (1978) fed chronically infected mouse brains to 6- to 9-week-old germfree or gnotobiotic kittens. The parasite was recovered by mouse inoculation from the whole length of the small intestine of the kittens, killed 5 hours after infection, and from extra-intestinal tissues 12 hours after infection. However, infectivity to mice of the smalI intestine decreased drastically between the 2nd and 3rd days after infection and was gradually regained during the following 2 to 3 days. In spite of the high infectivity to mice of the small intestine during the first two days, the author failed to detect microscopically any endo-epithelial toxoplasmic stages during the first three days after feeding cats with tissue cysts. However, an explosive appearance of profuse parasitization with all stages, including trophozoites, three different types of schizonts (referred to as S1-S3 with their respective merozoites being designated MI-M3), as well as macro- and microgametocytes was detected in the epithelium of the small intestine for the following seven to ten days. The author postulated that these schizonts do not develop directly from orally administered cystozoites, but that there exists an obligatorily intermediate extra-intestinal pre-gametogonic stage (EIPS). Overdulve attempted to test his hypothesis by intraperitoneai inoculation of an uninfected cat with homogenized mesenteric lymph nodes, spleen and liver of a cat, orally infected 4-$ days previously with brain cysts. Massive endo-

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epithelial invasion of the intestine of the inoculated cat was observed as early as two days after infection. The author ascribed the high initial infectivity to mice of the small intestine to the presence of microscopically undetected cystozoites that had just penetrated ; the diminished infectivity that followed was explained by the exodus of the cystozoites from the intestine to extraintestinal organs, to form the postulated EIPS. The lack of infectivity to mice of intestinal segments heavily parasitized with schizonts was attributed to the sexual differentiation of the M2 and M3 merozoites. More recently, Dubey (1979a) confirmed the earlier findings by Dubey and Frenkel(1972a) of the presence of dividing forms in the intestinal epithelium of cats as early as 23 hours after infection using two different strains of the parasite and newly born, as well as two-month-old kittens. In addition, he failed to corroborate Overdulve’s theory of “EIPS’ when he intraperitoneally inoculated six specific pathogen-free (SPF) cats with blood or homogenates of mesenteric lymph nodes, spleen and liver of other cats, fed 1 to 100 infected mouse brains one to four days previously, and did not observe oocyst shedding before 17 days. The gametogonic development of I. gondii is similar to that of other eimeriid coccidia as has been previously shown by Zaman and Colley (1970), Hutchison et al. (1971), Dubey and Frenkel (1972a) and more recently by Overdulve (1978). Further investigations on the schizogonic and gametogonic stages of I. gondii in the feline gut have been carried out by light microscopy (Bugaev and Bugaeva, 1976; Vrablic, 1977a, b; CatAr and Vrablic, 1978) and at the ultrastructural level by Ferguson et al. (1974, 1975), who compared their own results to those previously reported by Sheffield (1970), Colley and Zaman (1970), Piekarski et al. (1971) and Pelster and Piekarski (1971), as well as to similar stages of other eimeriid coccidia. Intensive cytochemical investigations on the different stages of the enteric development of I. gondii in the feline host were carried out by Beyer (1976) and Beyer et al. (1977, 1978b). “Oval cells”, believed to correspond to type D stage of Dubey and Frenkel(l972a), were found to have an RNA-rich and Feulgen-weak central nucleus. These cells had high cytoplasmic RNA content, exhibited high oxidase activity and possessed different types of dehydrogenases, constituting the most metabolically active stage in the intestine. The macrogametocyte had an RNA-rich nucleus and very low dehydrogenase activity, and it accumulated lipids as it matured. Large quantities of amylopectin were observed in the mature macrogametes, zygotes and the residual body of the microgametocyte. Immediately after fertilization, a sharp shift was observed in the oxidative metabolism of the zygote. Phosphatase activity was absent from all entero-epithelial stages, except for the microgametocyte, a fact interpreted by the authors to indicate that entero-epithelial stages of this parasite are more dependent than those of other coccidia on the host cell for their metabolism.

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2. Following ingestion of oocysts Kiihn et al. (1974) killed kittens 5 to 4 8 days after oral inoculation with 500 000 to 5 000 000 toxoplasmic oocysts. Entero-epithelial stages were not observed before the 20th day, although the cats had become infected, as evidenced by seroconversion and isolation of toxoplasmic stages from their intestines and extra-intestinal tissues by mouse inoculation. Young schizonts and merozoites were observed on the 20th and 24th, and schizonts and gametocytes on the 25th and 28th, days. Oocysts were excreted 25 to 38 days after infection. In spite of the development of dye-test titres starting seven days after infection, and the infectivity of mesenteric lymph nodes and intestines to mice, Overdulve (1 978) failed to detect faecal oocysts or entero-epithelial intestinal stages in eleven 11-14-week-old gnotobiotic kittens, killed 1 to 21 days after oral inoculation with oocysts. An intriguing observation was the failure to isolate toxoplasmic stages by mouse inoculation from the intestinal tissues during the first four days after infection and from the fresh contents of the small and large intestine of cats, even as early as one day after feeding with oocysts. Overdulve suggested that sporozoite penetration of the wall of the small intestine was rapid and that there was no local multiplication of the parasite during the initial four days of infection. It is now well established that, although the oocyst is highly effective in inducing toxoplasmic tissue cysts in a wide variety of birds and mammals, including cats, it is far less efficient than tissue cysts in initiating the schizogonic and gametogonic intestinal cycles in the felid final host (Dubey et al., 1970c; Wallace, 1973). Hutchison et al. (1971) and Piekarski and Witte (1971) reported a prepatent period of one to two weeks before shedding oocysts, following oral inoculation of cats with sporulated oocysts. However, most other investigators (Frenkel et al., 1970; Dubey et al., 1970a, b; Baldelli et al., 1971; Wallace, 1973; Kiihn et al., 1973) have recorded prepatent periods of three to seven weeks after feeding oocysts. The detection of enteroepithelial stages only 20 days or later after feeding with oocysts, as well as the observation of parasitaemia on the loth and 20th days after infection, led Kuhn et al. (1974) to postulate that the parasite proliferates in extraintestinal tissues before returning to the gut, to initiate the entero-epithelial cycle. The initiation of oocyst shedding in only 25 % of cats, successfully infected by parenteral inoculation with sporozoites (Dubey and Frenkel, 1976), seems to indicate that reinvasion of the intestinal epithelium from extraintestinal sites of proliferation is serendipitous, rather than a homing response. D.

SEXUAL DIFFERENTIATION

The terminal stage in the life cycle of I. gondii and other coccidia is sexual, culminating in the formation of the oocyst as a result of the fusion of the micro- and macrogamete. Two crucial questions have long intrigued cocci-

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diologists : (i) Is sex determination phenotypic or genotypic? In other words, is the trophozoite genetically committed, so that the progeny of each can produce only macro- or microgametes, or can the progeny of each produce gametes of either sex, the choice between the two pathways being determined by other, non-genetic factors? (ii) At which stage of the life cycle is sex determined ? The first question was elegantly resolved for I. gondii by Pfefferkorn et al. (1977). Pure clones of endozoites, obtained by repeated cloning by plaque formation in microwell cultures of human fibroblasts, were used to inoculate laboratory mice. The resultant tissue cysts were found to induce gametogony and oocyst formation in cats as early as, and as efficiently as, the uncloned original strain, clearly indicating that the genome of each endozoite contained the genetic potential for the formation of both macro- and microgametes. More recently, Cornelissen and Overdulve (1980) successfully induced oocyst shedding in cats fed tissue cysts from mice, inoculated with single oocysts or sporocysts, indicating that neither the oocyst nor the sporocyst is sexually differentiated and that, assuming meiotic division to occur at the first nuclear division during sporogony, sexual differentiation is not genetically determined. These results are hardly surprising as it has long been known that in the closely related genus Eimeria, the complete cycle can be initiated from a single oocyst. Lee et al. (1977) have demonstrated that the sporocyst is not sexually differentiated in E. tenella, and Shirley and Millard (1976) established infection in chick embryos with a single sporozoite of this species. E. maxima has since been successfully maintained by serial passage of single sporocysts (Shirley, 1980). Evidence for phenotypic differentiation of sex in the coccidia was provided by Grell as early as 1953, while working on Eucoccidium dinophili. He showed that sporozoites of this organism invariably transform into macrogametocytes, suggesting that development of microgametocytes was triggered by a stimulus from the macrogamete. A phenotypic effect was also demonstrated for Plasmodium gallinaceum by Bishop (1958), who showed that gametocytes of both sexes developed in clones arising from a single trophozoite. It is now believed that sexual differentiation of eimeriid coccidia takes place at least as early as the generation of merozoites which will form gametocytes. Cytochemical evidence was supplied by Canning (1 973) for two types of merozoites, destined to become male and female gametocytes respectively, in Barrouxia and Adelea. Klimes et al. (1972) claimed that E. tenella second generation schizonts, grown in culture, were sexually differentiated. Moreover, as they found both male and female gametocytes within the same cell, they argued against a phenotypic mechanism of sexual differentiation. Circumstantial evidence for sexual differentiation in E. tenella in the first generation merozoites was provided by McDougald and Jeffers (1976), who, by selecting for precociousness, succeeded in obtaining a strain which produced viable oocysts after only a single generation of schizogony. In the Haemosporina, gametocytes may arise from the exo-erythrocytic merozoites, or after several erythrocytic generations (Killick-Kendrick and Warren, 1968),

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whereas in the eimeriid coccidia a definite number of asexual generations is usually interposed before gametogony. McDougald and Jeffers’s selection results suggest a genetic factor determining the shift from asexual to sexual stages, whereas the artificial prolongation of asexual development in immunosuppressed chicks (Long and Rose, 1970) suggests an involvement of the host’s immune response in inducing sexual development. The actual mechanism of sexual determination remains unknown. E.

GENETIC RESEARCH

Pfefferkorn and Pfefferkorn, at the Darmouth Medical School in Hanover, New Hampshire, have pioneered genetic research on I. gondii, by isolating a number of temperature sensitive mutants, as well as other mutants deficient in uracil phosphoribosyl transferase or adenine kinase (Pfefferkorn and Pfefferkorn, 1976a, b ; 1977a, b, c; 1978; 1979). This has paved the way, using these mutations as genetic markers, for recombination experiments similar to those carried out on drug resistant mutants of Eimeria maxima (Joyner and Norton, 1975, 1977), and to the genetic recombination of precociousness and drug resistance in E. tenella (Jeffers, 1976; review by Ryley, 1980). F.

IMMUNITY IN THE FELINE FINAL HOST AGAINST THE ENTEROEPITHELIAL CYCLE OF DEVELOPMENT OF I . gondii

In view of the central role of Felidae in disseminating toxoplasmosis in nature, the course of development and duration of protective immunity and its effect on the excretion and potential re-excretion of oocysts by cats is of considerable interest to the epidemiologist and the individual pet cat owner alike. Earlier observations (Frenkel, 1973a) appeared to correlate inhibition of oocyst shedding with the development of circulating antibodies in cats, suggesting that recent infection was associated with solid immunity and remote infection with partial immunity. However, Sheffield and Melton (1974) infected 33 cats by oral inoculation with brain cysts and seven cats with faecal oocysts, and challenged them 8 to 84 days later, when the dye test titres ranged from negative to 1 in 4096. The results revealed that circulating antibodies played little if any role in preventing excretion of oocysts, but that oocyst-producing intestinal infection conferred a considerable degree of protective immunity against reshedding of oocysts after challenge. Resistance against reinfection with the sexual cycle had also been observed by Overdulve and de Roever-Bonnet (1973). Overdulve (1978) reported solid immunity against reshedding of oocysts by cats, which had shed even scanty numbers of oocysts during primary infection, when challenged by feeding with brain cysts 24 to 234 months later.

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Differences in the degree of immunity against intestinal reinfection of the feline host with homologous and heterologous toxoplasmic strains have been reported by Piekarski and Witte (1971), Dubey and Frenkel (1974) and Overdulve (1978). The clear-cut correlation between resistance to oocyst excretion and previous gametogonic development in the feline intestine suggests the development of local protective immunity against reinfection with the entero-epithelial cycle, at the level of the intestinal mucosa. The respective roles of the schizogonic and gametogonic antigens in stimulating intestinal immunity have not been appraised. However, there is evidence that in the related coccidian Eimeria, it is the second generation of schizonts that is essential for the development of protective immunity (Horton-Smith, 1949; Kendall and McCullough, 1952; Hammond et al., 1964), but that the gametogonic stages of several Eimeria species have little immunizing capacity (Rose, 1967). The immune response initiated by the schizogonic phase of toxoplasmic infection may well be the stimulus for large scale transition to the sexual phase, as postulated for Eimeria as early as 1933 by Wilson and Morley. The lack of host immune response was suggested by Rose (1973) as a possible explanation for the difficulty in obtaining sexual development of Eimeria in cell cultures. The mechanism of intestinal immunity in the cat has not yet been investigated. It is likely that local antibodies in the intestinal tract play a significant role in the protection of immune cats against reinfection. A protective role has been demonstrated for chicken copro-antibodies against infection with Eimeria, in vivo as well as in vitro (Orlans and Rose, 1972). In mammals, humoral immunity manifested in the gastrointestinal tract against harmful micro-organisms is due to the presence of secretory IgA antibodies; much of the IgA in the gut secretions is synthesized and released locally by the abundant plasma cells of the lamina propria (Cebra et ul., 1979). In mammals, the Peyer’s patches of the alimentary tract (which we have always found to be enlarged in cats infected with Sarcocystis-induced coccidiosis) are known to contain a population of lymphocytes especially rich in precursors of IgA plasma cells. The role of Peyer’s patches, which have the capacity to sample antigens, has as yet not been studied in relation to immunity against toxoplasmic infection in the cat. As Peyer’s patches have the capacity to accumulate IgA memory cells from elsewhere in the body (Pierce and Gowans, 1975), it would be most interesting to prime susceptible cats by intraperitoneal inoculation with toxoplasmic schizogonic antigen and to observe the reaction in the lymphoid tissue of the intestinal bed on oral challenge with brain cysts. It is not clear how local immunity in the intestine exerts its effect. In completely immune animals, excysted sporozoites may be prevented from penetrating the intestinal mucosa (e.g. E. nieschulzi and E. tenella; Leathem and Burns, 1967), or desiroyed soon after penetration (e.g. E. necatrix: Tyzzer et al., 1932; Leathem and Burns, 1967, 1968). In relatively immune

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birds, penetrated sporozoites retained their infectivity for 24 h, but had lost it by 48 h. Secretory IgA may be involved in the inhibition of cell penetration and subsequent development of the sporozoites of E. tenella (Davis and Porter, 1979). The fact that the period of patency and the total number of I . gondii oocysts shed by cats after repeated oral infection, on consecutive days, with brain cysts, are not significantly different from those following a single infective meal (Dubey and Frenkel, 1974), appears to indicate that the immune mechanism functions at the level of the intestinal mucosa very early on in the course of primary entero-epithelial development of the parasite. However, the higher dye-test titres attained in sera of cats fed repeatedly, as compared to those of cats fed once, as well as the occasional spontaneous re-excretion of oocysts observed three to four weeks after primary infection in cats fed cysts on two to five consecutive days (Dubey and Frenkel, 1974), appear to indicate that some degree of reinvasion of the intestinal epithelium and extra-intestinal tissues by fresh crops of ingested cystozoites does take place. This is most likely to occur during the first one or two days after primary infection probably before development of the schizogonic enteroepithelial stages. The slight shortening of the prepatent period before oocyst excretion, following repeated oral inoculation on consecutive days with brain cysts (Dubey and Frenkel, 1974), is puzzling. It may reflect enhancement of the local immune response proposed by Wilson and Morley (1933) as the stimulus for large scale transition from asexual development in conventional coccidia. This hypothesis is further supported by the interesting observation by Dubey and Frenkel (1974) of remarkably few gametocytes (less than 0.5 % of the later schizogonic forms) in a cat killed 12 days after relapse induced by treatment with corticosteroids. Cell mediated immune responses are also likely to be involved in protection against reinfection with the intestinal toxoplasmic cycle in cats. Delayed hypersensitivity occurs with Eimeria infections and there are also reports of positive results with the macrophage migration inhibition test (Rose, 1976). The observation by Dubey and Frenkel (1974) of reshedding of oocysts, accompanied by concomitant relapsing tissue toxoplasmosis, in 16 out of 29 cats injected with, or fed, methylprednisolon acetate (MPA), agrees with earlier findings on the abolition of existing immunity against Eimeria spp. by corticosteroid treatment (Rose, 1973); it does not reveal the exact nature of the intestinal immune response in the feline host, as corticosteroids affect resistance in a variety of ways. The finding of toxoplasmic schizonts in the bile duct epithelium of an MPA-treated cat (Dubey and Frenkel, 1974) suggests that the apparently strict site specificity of the entero-epithelial stages of I . gondii in the feline host is determined, at least in part, by the host’s immune response, as previously observed with homoxenous eimeriid coccidia (Long, 1970). Dubey et al. (1977b) found that male cats excreted more oocysts than did females, and cats under one year old shed more than older animals.

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An interesting effect of the age of cats, when exposed to primary infection, on the chance of shedding oocysts and the probability of re-excretion, when challenged two to 32 weeks later, was described by Dubey and Frenkel (1974). Selecting from their data the results obtained by natural routes of infection, namely oral inoculation with brain cysts, acutely infected tissues, or oocysts, the following pattern emerges : of 11 suckling kittens (1-3 weeks old), only the two which had been fed brain cysts shed oocysts after primary infection, although the other 9 became infected, as evidenced by their dye test titres. After challenge with brain cysts, only the latter nine kittens shed oocysts, the first two remaining refractory. Of 12 weaned 7-1 3-week-old kittens, eight shed oocysts at primary infection following ingestion of brain cysts (three out of three), acute stages (four out of five) or oocysts (one out of four). Following challenge with brain cysts, five of these re-excreted oocysts. All adult cats (six months or older) fed brain cysts or acute stages, excreted oocysts but failed to re-excrete any after challenge. In our opinion, it is likely that maternal antibodies passively acquired in milk, particularly of the IgA and IgM classes of immunoglobulins, may protect the intestine of suckling kittens against the entero-epithelial cycle. The amount of passively acquired maternal IgA is likely to be determined by the immune status of the lactating mother. Extra-intestinal toxoplasmic stages, however, proliferate more in very young kittens than in adult cats. Immunological responses mature with age : newly born mammals have few lymphoid cells in the intestinal lamina propria and their lymphoid follicles are poorly defined (Porter et af., 1979). The decline and termination of the protective function of maternal immunoglobulin is an important predisposing factor in the pathogenesis of post-weaning enteric syndromes (Porter et al., 1979). This may account for the diminished efficiency in resisting challenge, shown by oocyst excretion, in cats exposed to primary infection at an early age, as compared to adulthood. It had been largely assumed, in the past, that after the oocyst-producing primary infection, during which several millions of oocysts may be shed, chronically infected cats are subsequently safe as pets. Thus, Overdulve (1978) concluded that “The present results and those of others justify the opinion that under natural circumstances most cats will excrete oocysts only once during their life time.” However, Chessum (1972) had already reported the interesting finding that a cat, that had shed oocysts of I. gondii three months previously, started spontaneously reshedding oocysts of this parasite, ten days after it was orally infected with Isospora felis oocysts. That this was far from a chance occurrence was soon to be demonstrated. Dubey (1976a) fed ten seronegative, 3 to 34 month-old weaned kittens with toxoplasmic brain cysts and observed shedding of millions of oocysts by all infected kittens. Reshedding of considerable numbers of I. gondii oocysts was observed in nine out of ten of these kittens, nine to eleven days following oral inoculation with I. fefis oocysts 43 or 61 days after the primary infection with toxoplasmic brain cysts. Such a reactivation of oocyst shedding was, however, not observed following superinfection with I. rivolta, nor

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when infection with I. felis preceded toxoplasmic cyst inoculation (Dubey, 1978a). Dubey also demonstrated the persistence of toxoplasmic infective stages in feline intestinal mucosa or submucosa for 4 to 18 months after primary infection with toxoplasmic cysts (Dubey, 1977~).It is likely that persistent, latent intestinal tissue stages may be the source of the enteroepithelial oocyst-producing cycle in relapse infections, such as those occurring after superinfection with I . felis or treatment with corticosteroids. Felidae may support not only the intestinal gametogonic cycle of I. gondii, but their extra-intestinal tissues may also become heavily parasitized by asexual proliferative acute and chronic toxoplasmic stages. The complexity of the immune mechanism against this organism in the feline host, as compared to that against classic coccidia restricted to the intestinal tract, is therefore evident. While providing a constantly available source of infection for the intestinal epithelium, even in the absence of an extraneous source of infection, the latent toxoplasmic tissue stages may well serve to boost the immune response by providing antigenic stimulus. The extra-intestinal acute and chronic phases of toxoplasmosis proceed essentially similarly in immunocompetent infected cats and in non-feline intermediate hosts (Dubey and Frenkel, 1974), and are accompanied by a rise in dye test titre. The fact that titres develop in infected cats, whether or not the entero-epithelial cycle is completed, and do not protect against future infection of the intestine, renders this test of doubtful value in evaluating the past status of cats with reference to oocyst shedding, and hence, the chances of future oocyst excretion. G.

PATHOLOGY OF TOXOPLASMID COCCIDIOSIS IN THE FELID HOST

The pathological picture of feline infection with the entero-epithelial schizogonic and gametogonic stages of I. gondii is obscured by the fact that cats become concomitantly infected with extra-intestinal toxoplasmic tissue stages. The pathological effects appear to be determined largely by the route of inoculation, the dose of infective material and particularly by the age of the cat. Oral inoculation with large numbers of tissue cysts leads to severe diarrhoea, dehydration and death in newly born kittens. Weanling kittens do not appear to develop diarrhoea, but exhibit anorexia, weight loss and occasionally die after the end of patent oocyst shedding, suggesting that extra-intestinal lesions are a more likely cause of symptoms than the enteric development. Adult cats do not normally appear to develop clinical symptoms (Dubey and Frenkel, 1974). Infiltration of the lamina propria of the infected small intestine with granulocytes and lymphocytes, a flattening of the villi and irregularity of the epithelial lining cells, have been observed by Dubey and Frenkel (1974) and Overdulve (1978). At the ultrastructural level, a swelling and roughening of the endoplasmic reticulum and degeneration of the cristae of the mitochondria of parasitized cells were evident (Ferguson et al., 1976). Hutchison et al. (1979) published beautiful scanning electron

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micrographs of the mucosal changes in the intestinal epithelium of infected cats in which perforation sites and swelling of the infected cells are clearly visible. The clinical signs, gross lesions, diagnosis, treatment and prevention of infection in cats have been reviewed by Timoney (1976) and Frenkel (1978). Dubey and Hoover (1977) infected pregnant cats, ranging in age from eight to 51 months with I. gondii oocysts and observed no abortion or stillbirth. Of 54 foetuses or neonates examined, the parasite was recovered by mouse inoculation from only three out of one litter of six kittens. As not all the littermates were infected, the authors considered this as post-natal infection. However, this is perhaps not justified as Overdulve (1978) isolated the parasite from the brain of one of two littermates, killed immediately after birth, before suckling; the mother had a dye test titre of 1 in 16 at the time of birth, and another two littermates had titres of 0 and 1 in 4. H.

THE SURVIVAL, SPORULATION A N D DISPERSAL OF OOCYSTS

The effects of temperature, oxygen tension and several chemical reagents on the sporulation and viability of the oocyst, have been determined by Dubey et al. (1970a, c). Ito el al. (1975b) reported the inhibition of sporulation by exposure of the oocysts to 6O-7O0C, for as few as ten seconds, while the sporulated oocysts were rendered uninfective by exposure to 90°C for 30 sec. Exposure of unsporulated or incompletely sporulated oocysts to +4"C for 90 days, -5°C for 14 days or -20°C for one day resulted in the failure of the oocysts to sporulate when incubated at ambient temperature. However, sporulated oocysts retained their infectivity at -5°C for at least 120 days. Mature oocysts were rendered uninfective by storing at a relative humidity of 82% or 21% for 30 or three days respectively (Yamaura, 1976). The destructive effect of a large number of chemical agents on unsporulated and sporulated oocysts was reported by Ito et al. (197%). Frenkel et al. (1975b) studied the survival and dispersal of mature oocysts under natural conditions, by Geiger-tracing superficially buried Wr-labelled faeces of cats shedding oocysts. Following an initial local dispersal, accompanied by decline of the LD50 to mice, the infective content of the soil remained constant for over a year in Costa Rica, and 18 months, including a hot summer and two cold winters, in Kansas City. I.

THE STRUCTURE AND EXCYSTATION OF THE OOCYST

Ferguson et al. (1978, 1979a, b, c) studied sporulation of the oocyst by electron microscopy, applying the technique developed by Birch-Andersen et al. (1976) for obtaining ultra-thin sections of coccidian oocysts. The inner sporocystic layer was found to consist of four curved plates with marginal swellings, basically similar to that of the sporocysts of Isospora. canis and I. endocallimici (Speer et al., 1973, 1976) and that of Sarcocystis (Box et al., 1980).

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The infectivity of the oocyst of I . gondii for such a variety of unrelated mammalian and avian hosts, the finding of sporozoite-like structures in the stomach wall of cats fed mature oocysts (Kiihn et al., 1974), as well as the infectivity of the oocyst when injected intraperitoneally or subcutaneously, prompted Tadros and Laarman (1976) to suggest that the oocysts of this parasite may not require the bile-trypsin stimulus, normally needed for coccidian oocyst excystation. Christie et al. (1978) studied excystation of I. gondii oocysts in vitro by electron microscopy. 90 % to 95 % excystation was obtained by incubation in 5 % bovine bile in saline, at 37"C, without the addition of enzymes. Sporozoites became activated within two to twelve min and escaped from the sporocyst by separation of the sporocystic plates, and from the oocyst by rupture of its wall at one or more points. In a more detailed investigation of the fine structure, Ferguson et al. (1979d) described a basically similar process of excystation, but reported that it did not take place within the intact oocystic wall. J.

HOST CELL PENETRATION

The mechanism of host cell penetration by endozoites has been intensively studied by Jones et al. (1972a, b) and promises to throw light on cell invasion by motile stages of other coccidia. In areview, Jones (1979) reported that there is no evidence of secretion of membranolytic enzymes by the rhoptries, or of a mechanical boring function for the conoid in cell penetration. It is postulated that a substance, probably a basic charge-rich molecule, is secreted at the anterior end of the parasite and either remains there or streams over the body of the organism, facilitating attachment to the mammalian host cell membrane and entry into the cell. A substance that enhances cell penetration has been extracted from I. gondii endozoites (Norrby, 1971; Lycke et al., 1975), and appears to be produced in the region of the rhoptries and to affect the host cell membrane. According to Jones (1979), cell penetration appears to be a parasite-mediated phagocytic event. Endocytosis is followed by an enhancement in glucose uptake and rate of metabolism of the cell, and by a drop in pinocytosis. Takeuchi (1977) studied ceII penetration by endozoites of the RH strain into mouse peritoneal fluid cells at the ultrastructural level and concluded that the parasite was occasionally phagocytozed by a macrophage or an eosinophilic leucocyte, but that usually the endozoite, which, before penetration, was coated with a fuzzy film, entered by invaginating the plasmalemma of the host cell, without disrupting it. De Souza and Souto-Padr6n (1978) reported the presence of basic proteins in the conoid, rhoptries and micronemes, and discussed their role in cell penetration. Steriu and Dunareanu (1 976) described engulfment of toxoplasmic endozoites by pseudopodia put out by cultured mouse macrophages and fibroblasts, upon contact with the parasite ;they suggested that lysosomal enzymes released by the parasites sensitized the host cell membrane.

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Scanning electron microscopy (Aikawa et al., 1977) revealed that the process of cell entry was initiated by the parasite contacting the plasmalemma of the host cell and creating a shallow depression. A cylindrical structure extended from the pellicle of the parasite to the host cell and appeared to assist penetration. As the entry progressed, pseudopodia of the host cell extended to surround the parasite within a parasitophorous vacuole. Akinshina and Desmonts (1977) studied, by scanning electron microscopy, the penetration of mouse peritoneal macrophages in vitro and in vivo, and suggested a ‘mechano-secretory’ mechanism of invasion, directly correlated with strain virulence. Nguyen and Stadsbaeder (1979) studied, by phase contrast cinemicrography, endozoite penetration of mouse macrophages and HeLa cells. Parasites entered macrophages either by phagocytosis or by penetration, but invariably penetrated non-phagocytic cells. Active penetration was rapid, accompanied by brisk movement and flexion, and was not immediately followed by formation of a parasitophorous vacuole. The inhibitory effect of cytochalasin D on endozoite entry to both phagocytic macrophages and non-phagocytic tumour cells, was considered by Ryning and Remington (1978) as evidence that the host cell actively participated in the process, whereas Schupp et al. (1978) concluded that the parasite actively penetrated mouse erythrocytes. Tanabe et al. (1978, 1979) attributed the enhanced penetration of nucleated foetal erythrocytes by toxoplasmic endozoites, as compared to that of mature erythrocytes, to changes in the membrane properties of these cells with age. K.

STRAIN VIRULENCE AND HOST SUSCEPTIBILITY

Although a direct relationship has long been established between the invasiveness and rate of multiplication of a strain and its virulence to mice (Kaufman et al., 1958), the factors underlying the differences in virulence to laboratory animals of toxoplasmic strains isolated from man, other mammals or birds, are far from resolution. Recently, Pettersen (1977) elegantly confirmed Kaufman’s observations on the correlation of the proliferative rate of a strain and its virulence, by estimating that the generation time of an erstwhile avirulent strain, rendered virulent by rapid, repeated passage of endozoites, was gradually reduced from the initial 6.7 hours to 4.8 hours, a figure comparable to that obtained by Kaufman et al. (1958) for the RH strain. Akinshina et al. (1975) also observed rapid proliferation in cultured peritoneal macrophages of a virulent strain, 24 to 48 hours after infection by which time the endozoites of an avirulent strain had disintegrated. The problem of virulence of I. gondii strains is compounded by well established differences in host susceptibility. Abakarova and Akinshina (1975) observed more rapid penetration into, but slower multiplication of endozoites within, macrophages from rats, animals with a striking innate resistance to toxoplasmosis, than in macrophages from guinea pigs or mice, which are highly susceptible to infection. Considerable

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differences in virulence to mice, rats, guinea-pigs, rabbits and dogs of four strains of I. gorzdii, isolated as oocysts from the faeces of naturally infected cats, were observed by Ito et al. (1975a). The mechanism of pathogenesis of virulent strains has been studied by Henry and Beverley (1976). They described changes in lymph nodes, spleen and thymus, indicating an immunological response, in mice infected with strains of low virulence. A virulent strain, however, produced rapid lymphoid depletion in the three organs, associated with necrosis, suggesting a toxic effect on the reticulo-endothelial system, permitting unrestricted proliferation of the parasite. These results have since been confirmed by electron microscopic studies on changes in mouse thymus and spleen cells (Pelster et al., 1976; Pelster, 1980). Modification of parasite virulence by the immune competence of the host was suggested by Beverley et al. (1978); the virulence of a cyst-forming strain of I . gondii was enhanced in experimentally infected, as yet immuno-deficient, 1-day-old piglets. The virulence of a strain to a given host species may be altered by previous passage in another host species. Thus, a toxoplasmic strain, avirulent to mice and infective to pigs, was passaged in Mastomys and subsequently became virulent to miceand uninfective to pigs (De Meuter etal., 1975). Savina (1976a) found that enhancement of virulence of a cyst-forming strain was accelerated by passage through susceptible mice, very young mice or cortisone-treated mice, as compared with passage through mice belonging to normally resistant strains. In our opinion, rapid repeated passage in the same host species may well enhance virulence by selecting clones of more vigorously proliferating endozoites, combined with a propensity for invasiveness. Similar selective pressures may well prevail during passage in immunodeficient neonates or immunosuppressed animals. Walliker et al. (1976) have demonstrated that the virulence of the YM line of Plasmodium y . yoelii resulted from a genetic change, presumably a mutation, in the previously mild line. Whether changes in virulence of toxoplasmic strains after passage in experimental animals are genetic or non-genetic would be perhaps best investigated by cloning, followed by testing for the loss or retention of genetic factors conferring virulence after completion of the sexual cycle in the felid host. Savina (1975) studied the susceptibility of nine lines of pure bred mice to toxoplasmic strains of high and low virulence and classified the mouse strains as: (a) susceptible, (bj resistant to infection, (c) susceptible during the acute phase, and (d) susceptible during the chronic phase. Savina (1976c, 1978) demonstrated that the number of passages required to convert low virulence into high virulence was five in outbred mice, but eight and ten in the AKR and BalbC strains of mice respectively. Striking differences in susceptibility of seven inbred strains of mice to infection with I. gondii have also been reported by Araujo et al. (1976). Kamei et al. (1976) observed fatal acute toxoplasmosis in one mouse strain but chronic infection in another, in spite of similar antibody responses by both strains. The indication of involvement of genetic factors in the determination of murine susceptibility to toxoplasmosis has been confirmed by Williams et al. (1979), who investigated sus-

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ceptibility in inbred mice and their FI and F2 offspring, and concluded that susceptibility is affected by a t least two genes at the H-2 and H-3 loci respectively. According to these genetic studies, more than one mechanism of host resistance is involved. In the light of the recent demonstration of the capacity of the live endozoite, phagocytozed by a non-immune macrophage, to avoid the concerted effect of the oxidative metabolic outburst and lysosomes of the host cell (see page 322), it is tempting to speculate as follows: (i) genetic variations in cellular metabolism, e.g. the amount of H202 released into the parasitophorous vacuole, may account for differences in susceptibility to toxoplasmosis of different host species or strains ; (ii) the need for gradual adaptation by the parasite in its self-protective enzymic activity, e.g. of glutathione peroxidase and catalase, in response to a particular host species’ cellular environment, may account for the striking change in virulence of the same strain for a given host, after passage in another host species. L.

RECENT STUDIES ON TOXOPLASMOSIS IN FARM ANIMALS

1. Cattle

Although circulating antibodies to I . gondii have been repeatedly detected in cattle by a variety of serological methods (Hans, 1975; SogandaresBernal et al., 1975; Lucidi, 1976; Banite, 1976,1977; Chhabra and Mahajan, 1979; Costa and Costa, 1978; Costa et al., 1978; Rifaat et al., 1979; Polomoshnov and Peteshev, 1976a; to mention but a few more recent surveys), the parasite has usually eluded isolation (see also Jacobs, 1973). The few records of successful isolation include recovery of the organism from the diaphragms of eight out of 85 cattle in Czechoslovakia (Cathr et al., 1969), from the retina of eight out of 57 cattle in Italy (Zardi et al., 1964), also from the retina of 74 out of 304 Argentinian cattle (Mayer and Boehringer, 1967) and from colostrum and bovine viscera in Ohio, USA (Sanger et af., 1953). More recently, Dubey and Streitel (1976a) failed to induce oocyst shedding or seroconversion in SPF cats which were fed heart, diaphragmal and oesophageal muscle from 352 cattle, slaughtered in Ohio. Beverley et al. (1977) inoculated calves with toxoplasmic tissue cysts. Although circulating antibodies developed, the organisms could be recovered from the lymph nodes only, and then only during the first four weeks of infection. Skibo and Karpus (1978) injected an adult cow intramuscularly with 5400 tissue cysts and orally inoculated two more cows, each with six million oocysts. Lachrymation, salivation and depression were observed in the cattle six to seven days after inoculation and catarrhal rhinitis and conjunctivitis after 13 to 15 days. Similar symptoms of acute toxoplasmosis were observed in cattle by Timofeev and Golikova (1974), following subcutaneous inoculation with 50 million endozoites. Costa et al. (1977) orally inoculated three-month-old calves with 10 000 to 350 000 I. gondii oocysts from experi-

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mentally infected cats. Hyperthermia, respiratory embarrassment, conjunctival congestion, but no neurological symptoms were observed in all infected calves. Interestingly, though parasitaemia was first observed 6 days after infection in some animals, in others it was not detected until day 62, by which time the dye test titres had peaked at 9 to 21 days and then had often dropped drastically. Toxoplasmic tissue stages were isolated by mouse inoculation from the spleen, testes, intestine, skeletal muscle and retina, but not from the heart, brain, liver or kidney. Sboev (1975) attributed endometritis, dystrophy as well as cystic degeneration of the ovarian follicles of cattle to chronic toxoplasmic infection, but failed to isolate the parasite. Ferguson and Ellis (1979) described severe histopathological changes in a fatal case of acute toxoplasmosis in a young calf, born to a serologically negative cow, but which had been in close contact with kittens with high antibody titres. Munday (1978b) isolated the parasite from tissues of calves orally infected with oocysts or proliferative forms, but found no evidence of congenital transmission in calves, born to cows infected during pregnancy with 70 OOO oocysts or 150 tissue cysts. Stalheim et al. (1980) infected 22 pregnant cows by feeding oocysts or inoculation of endozoites, and subsequently isolated the parasite from the placenta of two, and from the brain and liver of four cows. A single abortion took place and intra-uterine infection occurred in two foetuses. Timofeev (1977) did not succeed in isolating the parasite from the semen of seropositive bulls and failed to transmit the parasite from a bull to cows by artificial insemination, 2 to 44 days after experimental infection of the bull. It would thus appear that, although cattle have been shown to be susceptible to infection with I. gondii, the parasite is not readily transmitted across the placenta, does not appear to be seriously pathogenic and is probably rapidly eliminated. 2. Sheep Recent serological surveys (Arnaudov et al., 1976; Riemann et al., 1977; Valder et al., 1977; Waldeland, 1977c; Willadsen, 1977; Paniagua Andres, 1978; Tizard et al., 1978; Perry et al., 1978; Morsy et al., 1979) confirm the global prevalence of toxoplasmic infection amongst sheep. Unlike that in cattle, ovine infection is readily demonstrated by isolation of the parasite from seropositive animals. Jn Norway, 10 to 15% of lambs and 25 to 37% of sheep had muscular infections detectable by peptic digestion (Waldeland, 1976~).The parasite was isolated by mouse inoculation from seven out of 26 apparently healthy sheep in Japan (Hagiwara et al., 1978). Acute infection of ewes during the first 30 days of pregnancy often results in abortion or foetal mummification (Jacobs, 1973). Toxoplasmosis is a frequent cause of abortion and neonatal death of lambs (Hartley and Marshall, 1957; Frei, 1975; Rifaat et al., 1976b; Arnaudov, 1977; Pohl, 1977; Nicolas et al. 1978; Waldeland, 1976b, 1977a; Pestre-Alexandre et al., 1978; review by Linklater, 1979). Congenital toxoplasmosis in sheep occurs with a remark-

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ably high frequency in New Zealand, Australia and England (Hartley and Moyle, 1968; Watson and Beverley, 1971). In a recent disastrous outbreak, 141 of the lambs born to 373 pregnant ewes, imported to Colombia from the UK, died at birth with symptoms of toxoplasmosis (Perry et al., 1979). A recent observation that sheep with haemoglobin type B had higher dye test titres, during the first six months of toxoplasmic infection, than sheep with type A or AB (Waldeland, 1976a), raises the question of whether genetic factors in British breeds of sheep, which presumably also contributed to the Australian and New Zealand stock, may play a role in this enhanced susceptibility. Intraperitoneal inoculation of five ewes, 110 to 120 days after conception, with toxoplasmic endozoites, resulted in the death of two ewes and the abortion of two foetuses. Parasitaemia was detected four to six days after infection and the parasite was recovered from the peritoneal fluid of all ewes and the placental material of the aborted foetuses. The acute phase was characterized by depression, anorexia, nasal and ocular discharge (Sharma and Gautam, 1978). The copious nasal and ocular discharge observed in these sheep may be very significant in the light of the demonstration of the survival of infective endozoites for four to five days in saliva and tears (Saari and Raisanen, 1977). Beverley et al. (1975) reported abortion in ewes 28 days after oral inoculation with 10 000 oocysts. The persistence of infectivity of oocysts that had passed unexcysted through the gut of sheep, was proven by mouse inoculation. The course of acute and chronic infection with toxoplasmosis induced in sheep by oral inoculation with oocysts has also been studied by Polomoshnov and Peteshev (1 976b), Iglmanov and Polomoshnov (1978) and by Dubey and Sharma (1980a). The last-named authors observed only transient parasitaemia but persistence of infective stages in various tissues, particularly the skeletal musculature, for from seven to 109 days after infection. The marked natural susceptibility of sheep to persistent toxoplasmosis was demonstrated by Munday and Corbould (1979), who noted the persistence of elevated titres in sheep, but their transience in cattle, grazed for 4&years on common pasture in Tasmania. In Norway, ovine infection appeared to be lower in summer than winter, possibly associated with the winter restriction of grazing to the vicinity of the farmsteads, where contamination of feed with feline faeces may be more likely (Waldeland, 1977b). Recovery of the parasite from the semen of rams, subcutaneously inoculated seven to 32 days previously with cystozoites, was recorded by Spence et al. (1978). However, Janitschke and Niirnberger (1975) failed to establish a correlation between positive titres in rams and infectivity of testicular extracts to mice. 3. Goats Although not intensively studied, caprine toxoplasmosis, occasionally with pathological manifestations, has been well documented (Munday and Mason, 1979). Goats have also been shown to be highly susceptible to con-

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genital toxoplasmosis (Calamel and Giauffret, 1975). Interest has recently been revived in the topic by the modern trend in the USA to keep goats and to drink raw, unpasteurized goat’s milk. Circulating antibodies were detected in 23 % of goats from California (Ruppanner et al., 1978). In Canada, 63 % of 399 goats from southern Ontario exhibited serological evidence of toxoplasmic infection (Tizard et al., 1977). Riemann et al. (1975b) described a case of acute toxoplasmosis in a seven-month-old child, reared on raw goat’s milk. Although the parasite was not isolated from milk, indirect haemagglutination (IHA) titres of up to 1 in 512 were detected in the lactating goats. A toxoplasmic strain, highly pathogenic to mice from the very first passage, was isolated from the muscle of a goat in Ohio, by inoculation into mice and its developmental cycle was completed in a cat (Dubey, 1980). An interesting observation was the detection of toxoplasmic organisms, by mouse inoculation, in the semen of 3 male goats for as long as 59 days after oral inoculation with oocysts of this strain (Dubey and Sharma, 1980b). Oocysts of the same strain were infective to elk and induced congenital infection (Dubey e f al., 1980). 4. Pigs

Recent serological surveys (Ryu et al., 1975; Amaral et al., 1976a; Schenk et al., 1976, 1977; Schaal and Kleikamp, 1976; Wynne de Martini and Martin, 1977; Manuel and Tubongbanua, 1977; Santos et al., 1978; Garcia et al., 1979), as well as successful isolation of the parasite from porcine tissues (Katsube et al., 1975; Lee et al., 1975; Hellesnes et al., 1978), confirmed the prevalence of latent toxoplasmosis in swine. Although infection with the parasite does not usually attain the epidemic scale commonly encountered in ovine toxoplasmosis, the parasite is of considerable economic importance, particularly in Japan, where several outbreaks have recently been reported. Moriwaki et a/. (1976) isolated the parasite from various tissues of six stillborn piglets, from a herd with frequent abortions and still-births. Sasaki et al. (1976) reported a serious outbreak of acute toxoplasmosis affecting 74 of 137 pigs, of which almost all animals weighing 45 to 120 kg died within four days of acquiring infection. All piglets born one to two months after the outbreak were found to be infected. Another outbreak of acute toxoplasmosis, with morbidity of 37.5 % and mortality of 11.8 %, involving sows, boars, piglets, porkers and weaners was described in Singapore (Koh et al., 1978). Hansen et al. (1977) described an outbreak of fatal toxoplasmosis, thought to be of congenital origin, in piglets in Sweden. The significance of cats as an indirect source of human infection in a pig breeding region of Japan has been stressed by Kobayashi et al. (1976). Ito and Tsunoda (1975) reported an outbreak of acute toxoplasmosis in a piggery in Japan. Severe clinical symptoms appeared simultaneously in 103 pigs and seven wild boars and culminated in the death of 13 animals. I. gondii oocysts were isolated by flotation from the soil at the periphery of a leaf-mould heap, used to supplement the hogs’ feed (It0 et al., 1975d). The authors gave a detailed description of the symptoms and pathological findings in piglets,

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experimentally infected with oocysts of two different strains of I. gondii (It0 et al., 1974b; Ito and Tsunoda, 1975). The diagnosis of acute toxoplasmosis in piglets, born on a farm in Indiana, USA, with a large number of roaming cats, was confirmed by electron microscopic identification of the parasite in mesenteric lymph nodes (Dubey et al., 1979). Ambrosi et al. (1975) and Tadros and Laarman (1977b) isolated I. gondii from, respectively, pigs in Italy and wild swine in the Netherlands, by passage through cats. 5. Horses Ishizuka et al. (1975) reported significant indirect fluorescent antibody (IFA) and dye-test titres in, respectively, 90 and 75 sera from 100 thoroughbred horses in SBo Paulo, Brazil. Dye-test titres were detected in 24 horses with motor incoordination and in 23 mares with a history of abortion or excessive irritability, but in only one out of 25 clinically healthy animals (Macruz et al., 1975). In the USA, the prevalence of IHA titres in horses varied from 2 % at the age of one year to 18 % at two years and 38% at 12 years; it varied also from 0 to 67 % with the individual ranch, being generally higher (30%) in cooler, wetter regions of California than in hot dry areas (13%) (Riemann et al., 1975~).An increase in the number of seropositive animals with age was also recorded in Texan horses by Eugster and Joyce (1976). Al-Khalidi and Dubey (1979) isolated five strains of I. gondii by feeding to cats pooled tissues of 128 horses, with negative dye-test titres, slaughtered in Ohio, U.S.A., and two more strains by inoculating mice with tissues from two of 24 horses with titres of 1 in 8 and 1 in 32, respectively. However, horses orally inoculated experimentally with I . gondii oocysts beveloped high dye-test titres, but did not appear to retain the parasite for long in their tissues (Altan et al., 1977). A natural resistance to infection with I . gondii is also indicated by the omission of mention of symptoms amongst horses in an outbreak of oocyst-induced toxoplasmosis amongst 37 members of a horse riding club in Atlanta (Teutsch et al., 1979). In the stable quadrant with maximum incidence of human infection, only three out of 19 horses had dye-test titres. M.

SEROLOGICAL DIAGNOSIS

The most useful and widely applied techniques for the serodiagnosis of toxoplasmosis in man and animals are the Sabin-Feldman dye-test (SFT), the complement fixation test (CFT), the indirect haernagglutination test (IHA) and the indirect immunofluorescent antibody test (IFA), including the immunoglobulin M (IgM) IFA. These, together with less commonly used serological methods like Fulton and Turk’s direct agglutination technique and flocculation tests using acrylic, bentonite or latex particles, have recently been reviewed and their interpretation lucidly and succinctly discussed by

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Jacobs (1976). The advantages and disadvantages of the SFT, IFA and CFT for the diagnosis of human toxoplasmosis, as well as the influence of standardization of the SFT and the CFT on the results of serological diagnosis, have been appraised by Berger and Piekarski (1976) and Piekarski (1979). The number of papers that have appeared over the last five years on modification or comparative efficacy of the various techniques for serosurveys is far too great to review here. Mention, however, must be made of the new enzyme-linked immunosorbent assay (ELISA), which is rapidly gaining favour in the serodiagnosis of parasitic infections (Voller et al., 1976a, b). Originally designed by Engvall and Perlmann (197 1) for the quantitative determination of antibodies and antigens in body fluids, the ELISA involves coating polystyrene tubes, or the wells of polystyrene microplates in the micro-ELISA method (Voller et al,, 1974; Ruitenberg et al., 1975), with soluble antigen. Appropriate dilutions of the test or control sera are incubated in the tubes or wells. Anti-host species immunoglobulin labelled with an enzyme such as horseradish peroxidase is added, and reacts with the antigenantibody complex (if present). Thus, enzyme remaining in the tubes or wells after washing indicates the presence of specific antibody in the test serum. The enzyme is rendered visible by addition of an appropriate, usually chromogenic, substrate. Ruitenberg and van Knapen (1 977) successfully applied the ELISA to discriminate between sera with clinically significant and insignificant IFA titres, but reported differences in individual titres obtained by the two methods. Excellent specificity and correlation with IFA titres have been reported by Capron et al. (1975), Kramai and Kozojed (1977), Walls et al. (1977). Ambroise-Thomas et al. (1978) compared the ELISA with IFA and IHA tests and immunoelectrophoresis, for the serodiagnosis of toxoplasmosis and infection with four other parasitic organisms, and confirmed the specificity of the ELISA. Recent studies on the antigenic structure of the endozoites of I . gondii (Handman and Remington, 1980; Handman et al., 1980; Hughes et al., 1980) promise to improve the specificity of serological tests and to facilitate the interpretation of results obtained by different serodiagnostic techniques. Ruitenberg et al. (1976) and Denmark and Chessum (1978) have described the mechanization of the ELISA. Van Knapen and Panggabean (1977, 1978) successfully used the ELlSA to detect circulating toxoplasmic antigen in the blood of human beings and mice. Antigen was detected in 5.7% of sera from persons suspected of having acute toxoplasmosis, with high, low or even negligible antibody titres. Antigen was believed to be present in the blood during the acute phase of infection only. More recently, Araujo and Remington (1980) detected antigenaemia in 63.6 % of individuals with recently acquired acute toxoplasmosis. Failure to detect antigen in some overt cases with lymph node involvement was attributed to the possibility of periodic antigen release, necessitating repeated testing, and the same authors are studying the effect of high dye test titres on the formation and precipitation of antigen-antibody complexes and, hence, on the detectability of antigenaemia. The potential of the ELISA for the detection of circulating antigen is particularly promising in cases of

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suspected acute toxoplasmosis in which the routine serological tests remain inconclusive, or when the host’s immune mechanism is impaired by disease or immuno-suppressive therapy. Antigens were also detected by the ELISA in the amniotic and cerebrospinal fluids of a considerable percentage of congenitally infected human neonates (Araujo and Remington, 1980). A new, so-called stick-ELISA technique has been developed and tried out on a number of sera and antigens (Felgner, 1978). The technique entails coating sticks of polystyrene with antigens from several parasitic organisms. It is certainly promising and facilitates serosurveying and, when combined with antigens of other organisms acquired by ingesting raw meat, e.g. Taenia and Sarcocystis, may reveal interesting epidemiological associations. The detection of IgM antibodies by the IgM-IFA test, developed by Remington et al. (1968a), has become widely accepted as a useful, reliable serological indicator of recently acquired acute toxoplasmosis (Remington et al., 1968b; Welch et al., 1980) and of congenital infection (Remington and Desmonts, 1976). Negative results sometimes obtained with such sera have been attributed to a blocking effect of high levels of IgG (Pyndiah et al., 1979). This assumption seems to have been confirmed as Filice et al. (1980a, b) found that separation by gel filtration of IgM from IgG antibodies resulted in a significant increase in the sensitivity of the IgM-IFA test for the diagnosis of acquired and congenital toxoplasmosis. However, Frenkel and Remington (1980) have drawn attention to the technical expertise required to read the IgM-IFA test and advised the sending of sera to reference laboratories for confirmation. An exciting new technique, with promising potential application for purification of toxoplasmic antigens and their immunological and biochemical characterization, is the recently reported successful establishment of functional hybridomas between myeloma cells and spleen cells from mice, hyperimmune to I. gondii. Cloned hybridomas secreted into the culture medium antitoxoplasmic antibodies of the IgG class and, after suitable manipulation, those of the IgM class (Sethi et al., 1980). Araujo et al. (1980) have advocated the use of monoclonal antibodies to I. gondii in the ELISA test for detection of antigens in sera and other body fluids. With reference to the Sabin-Feldman dye-test, an important recent finding is the discovery that the heat-labile accessory or activator factor, required for the action of antibody on I. gondii endozoites in this test, is the classical complement system. Sera from persons genetically deficient in C5, C6, C7 and C8 were ineffectual as activators. The properdin system was shown, after all, to play no role in the reaction (Schreiber and Feldman, 1980). There is evidence for cross reaction in the SFT, CFT and ELISA between I. gondii and I. datusi, using mouse sera (Wallace, 1974; Weiland et al., 1979). Cross reaction was, however, not detected between I. gondii and Sarcocystis in the dye test (Mas Bakal, 1959), IFA (Tadros et al., 1974, I975c) or in the ELISA (Tadros et al., 1979, I98 1).

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IMMUNITY I N THE INTERMEDIATE HOST

Active proliferation of endozoites during the acute phase of infection proceeds in the susceptible host with no apparent affinity or tropism for a specific organ, tissue or cell type, until the host dies or the parasite is checked by the development of immunity. The virulence at this stage depends largely on the invasiveness and rate of multiplication of the strain of the parasite. With the acquisition of immunity, the proliferative forms drop drastically in numbers; the parasite assumes an antigenically “low profile” within the tissue cysts, localized largely in the brain and eye, protected from circulating antibodies, but also in cardiac and skeletal muscles, not likewise shielded. The parasite is known to persist for remarkably long periods of chronicity, during which it is detectable solely in the tissue cyst. However, a number of observed facts argue convincingly for the persistence of proliferative forms, as well as tissue cysts, during the chronic phase of infection. These include: (i) the prolonged persistence of dye-test antibody titres during the chronic phase; titres may remain high long after the end of the acute phase; (ii) the persistence of parasitaemia in man (Miller et al., 1969) and other animals, sometimes in the absence of antibody titres (Costa et al., 1977); (iii) the marked immunosuppression in animals, chronically infected with toxoplasmosis, of humoral antibody production in response to vaccinationattributed by Strickland et al. (1973) to possible antigenic competition; and (iv) persistence of stimulation of the lymphoid cells and macrophages in mice during chronic toxoplasmosis, evidenced by the maintenance of nonspecific protection against a number of other pathogenic organisms and tumours (McLeod and Remington, 1977). Boosting of the host immune response during the chronic stage of infection, by occasional rupture of tissue cysts, cannot be ruled out. Small cysts are sometimes seen together with larger ones (Lainson, 1958; Waaij, 1959; personal observations). The observation by Norrby and Eilard (1976) of recurrent cerebral toxoplasmosis in a previously healthy young woman, with repeated serological and parasitological relapses, is relevant. It is also interesting that the formation of abnormally thin cyst walls in mice of the CC57Br strain, renders these mice extremely sensitive to avirulent toxoplasmic strains, with massive cerebral infection attributed to rupture of brain cysts and reinvasion of other cells. The thorny problem of the respective importance of the humoral and the cell-mediated immune response in conferring protection against toxoplasmosis has been discussed by Jacobs (1973). Natural resistance, the acquisition of immunity, the role of immunity in the pathogenesis of toxoplasmosis, immunodeficiency and infection have been thoroughly reviewed by Frenkel (1973a), who has personally contributed considerably to this field of research, and more recently by Remington and Krahenbuhl(l976) in a comprehensive article with over 200 cited literature references, and by Araujo (1977). Current concepts favour cell-mediated immunity as playing the major role in host defence against toxoplasmosis. Before reviewing the more recent

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literature on the topic, it may be mentioned that electron microscopic (Jones et al., 1972b) and fluorescence phase contrast studies (Khavkin and Freidlin, 1977) have demonstrated that the parasitophorous vacuole containing live toxoplasmic organisms is prevented from fusing with the host cell’s lysosomes, by a parasite-induced accumulation of host mitochondria and endoplasmic reticulum (Jones, 1979). The ability of this parasite to prevent the transfer of lysosomal enzymes into the parasitophorous vacuole is a significant step in aborting the host’s first line of defence, and thus constitutes an important factor in determining pathogenicity. Jones el al. (1975) studied in vitro the action of humoral and cell-mediated immune responses of mice, infected with an attenuated toxoplasmic strain. Heat-inactivated immune serum markedly inhibited the ability of the parasite actively to penetrate fibroblasts or HeLa cells, and greatly enhanced their destruction in phagolysosomes after phagocytosis by macrophages. Intracellular parasites were, however, unaffected by the addition of antibody. Peritoneal macrophages, derived from mice during the first months following immunization, markedly reduced the multiplication rate of invading proliferative forms. Thereafter, this direct expression of cellular immunity was lost; in order to induce maximal inhibition of parasite multiplication, it was necessary to expose the macrophages to immune lymphocytes and toxoplasmic antigen or to supernatants of cultures in which they had interacted. Athymic, nude mice were apparently no more susceptible to acute infection with virulent toxoplasmic strains, than normal mice. However, whereas normal mice recovered following prophylactic medication with sulphadiazine, and developed high levels of antibody and protective immunity, athymic mice failed to develop antibody, relapsed and died, indicating a significant role of thymus-derived lymphocytes in protective immunity against this parasite (Hof et al., 1976). When nude mice were injected intraperitoneally with thymus cells from hirsute littermates, they developed immunity to I . gondii during drug prophylaxis. However, the injection of bone marrow cells or high titre specific antibody did not prolong survival of athymic mice after drug therapy was discontinued (Lindberg and Frenkel, 1977a). Masihi and Werner (1977; 1978a) reported a 55 % reduction in numbers of brain cysts and a survival rate of 89% in mice given anti-toxoplasmic rabbit serum intraperitoneally, intravenously, or orally 48 hours before being challenged with lethal doses of a cyst-forming strain. Animals given the immune heterologous serum 48 hours after infection, exhibited an enhanced rate of survival, but curiously had larger numbers of tissue cysts in their brains than the untreated controls. In an extension of this work, Werner et af. (1978) attempted immunotherapy in chronically infected mice by giving inactivated rabbit anti-toxoplasmic hyperimmune sera orally, intraperitoneally or intravenously ; they observed an appreciable reduction in number of brain cysts. However, closer investigation revealed that the initial reduction in cyst numbers was in fact due to activation of the cystozoites and rupture of brain cysts. Four weeks after the end of therapy, an increase

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in number of cysts was observed, presumably due to de novo formation of cysts by the liberated cystozoites. Passively transferred antibodies may affect antibody forming cells. Thus, a marked reduction in number of spleen rosette-forming cells has been observed in antibody-treated mice (Masihi and Werner, 1976, 1978b). On the other hand, in vitro in the absence of a cell-mediated immune response, antibody enhanced cyst formation (Hoff et al., 1977). Using hamsters as an experimental model, Hoff and Frenkel(1974) reported a pronounced specificity of inhibition of I. gondii and I. besnoiti by macrophages, both in vivo and in vitro. Immunized hamsters reduced the homologous organism 100- to 10 000-fold, whereas the heterologous organism multiplied as in the nonimmunized controls. In vitro, peritoneal cells from immune hamsters significantly prolonged the replication time of the homologous parasite. Macrophages immune to I. besnoiti reduced growth of I. gondii by half, whereas I. besnoiti replicated normally in I. gondii-immune and nonimmune macrophages. Co-cultivation experiments with macrophages and lymphocytes indicated that macrophages, instructed by specifically committed lymphocytes, reduced the homologous organism 10-fold, whereas the heterologous organism was reduced only 2-fold. It was concluded that the specificity of intracellular inhibition of I. gondii and I. besnoiti was conferred on the macrophages by lymphocytes. The ability of lymphocytes specifically to “arm” macrophages was abolished by cortisone, at a concentration that failed to interfere with the inhibition of multiplication of the parasites by pre-“armed” macrophages (Lindberg and Frenkel, 1977b). Thus, by separating the process of “arming” from that of expression of inhibition of multiplication of the parasites, these authors demonstrated that the specificity of inhibition was a function that could be attributed to the macrophages. However, McLeod and Remington (I 977) failed to demonstrate any specificity in the ability of peritoneal macrophages from mice infected with I. gondii or I. jellisoni to kill either organism in vitro. It was further established that the strain of host, the strain of parasite, the route of infection, and the stage of development of the donor’s immune response, did not appreciably affect the ability of the macrophages nonspecifically to inhibit the parasites in vitro. However, in vivo, protection was very much enhanced when the animal was challenged with the homologous organism. The specificity of the microbicidal effect of activated macrophages has recently been further discussed by Krahenbuhl et al. (1 980). Macrophages from mice infected with the phylogenetically unrelated Corynebacterium parvum nonspecifically killed both I . gondii and I. jellisoni proliferative forms in vitro (McLeod and Remington, 1977). However, intracardiac inoculation of a vaccine strain of Mycobacterium tuberculosis did not protect hamsters against challenge with I. gondii or I. jellisoni. Hamsters immunized against I. datusi survived challenge with l o 4 lethal doses of I. gondii proliferative endozoites, but were only marginally protected against I. jellisoni (Dubey, 1978d). Cross immunity between I . gondii and I. datusi had previously been demonstrated by Frenkel and Dubey (1975a) and by Christie and Dubey (1977).

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Rats, chronically infected with I. gondii, exhibited greatly reduced parasitaemia when infected with Plasmodium berghei. This protection was abrogated by inoculation of the rats with anti-rat thymocyte serum before challenging with P.berghei. The rate of phagocytosis of Plasmodium-infected erythrocytes by normal macrophages in vitro was significantly stimulated by the addition of lymphokines resulting from incubation of I. gondii-immune lymphocytes with toxoplasmic antigen, confirming the nonspecificity of this stimulation (Omata et al., 1979). Jones et al. (1975) and Jones (1977) demonstrated that lymphocytes from the spleens or peritoneal cavities of mice, immune against I. gondii infection, when incubated with toxoplasmic lysate antigen, released a substance that induced inhibition of multiplication of toxoplasmic organisms within macrophages. This substance was distinct from interferon and interacted with the macrophage, initiating RNA synthesis and inhibition of parasitic replication; it was assumed to be a lymphokine, designated “Toxoplasma-growth inhibiting factor” (Toxo-GIF) and was found to depend on cellular metabolic effects of the T-lymphocytes (Shirahata et al., 1975, 1976, 1977). Rocklin et al. (1980) have reviewed the concept of lymphokines in general. Jones (1977) concluded that the cell-mediated immunity against I. gondii resulted from lymphocyte-macrophage interaction, which induced a toxoplasmacidal or a toxoplamastatic action by the macrophage. The relatively nonspecific toxoplasmacidal effect was attributed to the release of substances from the macrophage, that killed the parasite and permitted its phagocytosis and digestion. The more obscure toxoplasmastatic effect required interaction between lymphokine and the macrophage surface, and involved protein synthesis by the cell. As pointed out by Remington (1980), it is as yet unclear how the parasite is killed in the absence of phagosome-lysosome fusion in the activated cell (Jones and Byrne, 1980). Parasitophorous vacuoles have been shown to fuse with lysosomes when the parasite is degenerate (Khavkin and Freidlin, 1977). Evidence has been presented for a role of serine esterase in the ability of activated macrophages to inhibit or kill I. goizdii endozoites (Krahenbuhl et al., 1980). Lymphokine is apparently ineffective on non-macrophage cells, e.g. HeLa cells (Jones and Byrne, 1980). In 1978, Chinchilla and Frenkel isolated and characterized a “mediator” substance from antigen-treated lymphocytes, derived from hamsters immune to I. gondii, which specifically protected not only macrophages, but also cultured fibroblasts and kidney cells, by inhibiting proliferation of the parasite. Cell mediated immunity against toxoplasmic antigen in human beings can be demonstrated in vitro by antigen-specific lymphocyte transformation (Krahenbuhl et al., 1972). Lymphocyte transformation in response to toxoplasmic antigen has also been shown to be useful in the diagnosis of congenital toxoplasmosis during infancy (Wilson et al., 1980a). Lymphocyte transformation does not occur in all patients with acute toxoplasmic infection, although it was demonstrated in patients chronically infected for up to 19 years (Remington and Krahenbuhl, 1976). Andersen et al. (1979) con-

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firmed the absence of transformation in some patients during acute infection, but found eventual transformation in all patients. In view of the current evidence that cell mediated immunity plays a major role in host defei.ce against toxoplasmosis, the apparent impairment of lymphocyte responsiveness during the acute phase of infection is puzzling. The authors drew attention to the paradoxical situation in I. gondii-infected mice, where, on the one hand, the immune response against totally unrelated organisms is enhanced, while, on the other, the same animal concomitantly exhibits immunosuppression, revealed by impaired humoral antibody response to vaccine. It has recently been suggested that the latter effect of the parasite may impede vaccination of infected sheep against Clostridium and louping-ill virus (Buxton ef al., 1979). Toxoplasmic infection confers a remarkable degree of nonspecific resistance against infection with autochthonous and transplanted tumours (Hibbs et al., 1971). Conley and Remington (1977) demonstrated that chronic toxoplasmic infection in mice resulted in nonspecific inhibition of ependymoblastoma tumour growth and enhanced necrosis within the tumour. However, the inhibitory effect of chronic toxoplasmosis on virally produced tumour growth has not been demonstrated for chemically induced neoplasms, in livers of rats treated with 3’-methyl-dimethylaminoazobenzene; their growth was delayed but not prevented (Frenkel and Reddy, 1977). The finding that the tumouricidal effect of activated macrophages from mice infected with I. gondii is inhibited by endocytosis of erythrocytes, haemoglobin, or haemoglobin degradation products (Weinberg and Hibbs, 1977), is significant in view of the fact-often overlooked-that aged red cells are destroyed by phagocytes in the spleen, bone marrow and liver, before eventually being excreted as bile by the liver. Pelster and Piekarski (1979) have demonstrated that toxoplasmic endozoites can invade and multiply in all the exudate cells that migrate into the peritoneal cavity of mice during infection with acute toxoplasmosis, namely macrophages, lymphocytes, neutrophilic and eosinophilic granulocytes. They also confirmed the prevention of fusion between parasitophorous vacuoles, containing live parasites, and host cell lysosomes. The apparent survival of toxoplasmic endozoites within normal human mononuclear phagocytes, has led to the generally accepted concept that these cells may not only shelter the parasite against circulating antibodies, but also may transport them around the body and across the placenta during pregnancy (Remington and Krahenbuhl, 1976). Wilson and Remington (1979a) have now clearly demonstrated that replication of the parasite is almost completely inhibited within human circulating phagocytes and that the parasite is rapidly destroyed in both peripheral blood monocytes and polymorphonuclear leucocytes. The microbicidal effect of human granulocytes and monocytes is believed to be linked to the production of potentially lethal reactive oxygen metabolites by these cells during phagocytosis (Babior, 1978). The failure of normal human macrophages to destroy phagocytozed toxo-

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plasms has been shown to be the result of the failure by the parasite to trigger the oxidative metabolic burst in these cells, but to stimulate it in granulocytes (Wilson et al., 1980b). Murray (1980) has shown that toxoplasmic parasites are resistant to the lethal action of hydrogen peroxide (H,O,) in macrophages, due to the presence, in this parasite, of considerable concentrations of glutathione peroxidase and catalase. The parasite appears to avoid triggering the macrophage’s oxidative burst by failing to stimulate the macrophage’s production of the precursor of H,O,. Increased phagosome-lysosome fusion during phagocytosis by monocytes or activated macrophages suggests that lysosomal contents may act in concert with reactive oxygen metabolites, as a first line host defence mechanism, whereby the parasite is destroyed in mononuclear phagocytes. Yoshizumi (1977) noted the absence of lysosomal enzyme within the vacuoles of macrophages containing toxoplasmic endozoites in experimentally infected rabbit retinal tissue, but suggested that the abundant lysosomal activity in the cytoplasm of infected macrophages may contribute to cellular destruction of surrounding tissue when these cells burst to release the parasite. Gardner and Remington (1977) described a marked increase in susceptibility to toxoplasmic infection in aged mice of two different strains. Interestingly, transfer of normal serum from aged mice to young or old mice increased susceptibility to infection, suggesting the loss with age of a parasite-inhibitory serum factor. Aged mice had significantly reduced humoral antibody response during acute and chronic infection, compared to four month-old mice (Gardner and Remington, 1978). The influence of age on the immune mechanism in general has recently been reviewed by Makinodan and Kay (1980). Thymic lymphatic mass decreases in both man and animals with age, primarily as a result of atrophy of the cortex, Normal immune functions can begin to decline as early as the onset of sexual maturity. The most visible cellular target of ageing appears to be the T-cells. Several attempts at developing a vaccine against toxoplasmosis, with a varying degree of success, have recently been reported (Seah and Hucal, 1975; Mikhailova et al., 1976;Mas Bakal and in ’t Veld, 1979).Werner (1977) demonstrated that previously infected mice, with circulating antibodies, were susceptible to reinfection, exhibiting parasitaemia between 24 and 352 hours later. The author failed to detect transplacental transmission of the parasite in chronically infected rabbits, challenged during pregnancy ; whereas in mice, congenital infection was observed in six out of 11 strains tested. Attempts to immunize rabbits with toxoplasmic antigens before conception, followed by induction of primary infection during pregnancy, resulted in congenital infection in 55% of foetuses, compared to 79% foetal infection following passive immunization with hyperimmune serum. Studies recently undertaken by Wilson and Remington (1979b), on the effects of monocytes from human neonates on lymphocyte transformation, promise to provide useful information about regulation of immune responses in the foetus or newborn baby to congenital or perinatally acquired toxoplasmosis.

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PATHOLOGY OF HUMAN TOXOPLASMOSB

The pathological manifestations of toxoplasmosis are largely associated with active proliferation of the endozoites during the acute phase of infection, in the absence of protective immunity in a susceptible host. The symptoms vary with the natural susceptibility of the host species, the virulence of the strain of parasite, the stage establishing infection (endozoite, cystozoite or oocyst), and the route by which the parasite gains entry. Under natural conditions, human toxoplasmosis is probably usually acquired by the ingestion of a small number of oocysts, or tissue cysts in raw meat, and is generally asymptomatic. However, even asymptomatic infection may result in transplacental transmission to the foetus. With the development of protective immunity, the infection localizes largely in the central nervous tissues or elsewhere, e.g. cardiac and skeletal musculature, where latent tissue stages may persist for years without invoking any host tissue reaction, or, under certain conditions, e.g. following immunosuppressive therapy, may lead to an intense hypersensitive inflammatory reaction. In the latter case, resulting necrotic lesions in the brain may lead to chronic encephalitis, and ocular lesions in the retinal tissue to retinochoroiditis (Frenkel, 1973a). The pathogenesis of congenital infection is basically similar t o that of acquired toxoplasmosis ; however, the severity of the lesions and the protracted course of prenatally acquired infection is aggravated by the immaturity and incompetence of the immune system of the foetus and the neonate, leading to more profound parasitization of the eye and brain, which may culminate in encephalitis, hydrocephaly, etc. Various aspects of the pathology of toxoplasmosis in man and animals have been reviewed by Frenkel (1973a, b), who has been instrumental in developing animal models for investigating the mechanisms of pathogenesis of this disease (Frenkel, 1955, 1961, 1969, 1977a), and by Turner (1978). Medical aspects of the disease have also been thoroughly reviewed by Desmonts (1978) and by Piekarski (1978). The pathology and pathogenesis of congenital infection have been described and discussed by Frenkel (1974d), Beverley (1977) and Couvreur and Desmonts (1977). Various aspects of congenital infection of the human foetus have been discussed by, amongst others, Alford et al. (1974), Gromova (1976), Kotova-Balakina (1976), Mulatova (1976), Restrepo et al. (1976), Roch Ubiria (1976), Shevkunova et al. (1976a), Dumez (1977), LeautC and Montis (1977), Martinon-Sanchez et al. (1977), Mau et al. (1977), Sever and Fucillo (1977), Stray-Pedersen and LorentzenStyr (1977), Williams (1977), Aspock et al. (1978), El Dasouqui (1978), Munday (1978a) and Thalharnmer and Heller-Szollosy (1979). Stern and Romano (1978) reported congenital ocular toxoplasmosis in two siblings. In view of the current assumption that chronic toxoplasmosis in humans does not result in transplacental transmission it is noteworthy that Awan (1978) diagnosed toxoplasmic retinochoroiditis in three siblings of a young mother, who had lost two earlier children with symptoms indicative of congenital toxoplasrnosis, and suggested perinatal infection from the chroni-

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cally infected uterine wall. This report is interesting in the light of (i) the identification of tissue cysts in vaginal and cervical smears from seven women (Dominguez, 1976; Dominguez and Girbn, 1976), (ii) the recent evidence for a fall in humoral antibodies against toxoplasmic antigen during pregnancy (Phcsa and Pejtsik, 1977, 1978) and (iii) the possibility that the cellular immune mechanism of the foetus may inhibit the maternal cell mediated immune response (Oldstone et al., 1977). In mice, vertical transmission in chronically infected animals has been observed for up to the ninth generation (Beverley, 1973). The susceptibility of the young human foetus to oocyst-induced acute maternal toxoplasmosis has recently been demonstrated by isolating the parasite by amniocentesis from a pregnant female patient, who subsequently underwent therapeutic abortion (Teutsch et al., 1979, 1980). Marked differences in the clinical course of congenital toxoplasmosis in dizygotic twins have been reported by Statz et al. (1978). Not all primates appear to be equally susceptible to intra-uterine infection. Thus, Wong et al. (1979) inoculated Macaca arctoides with four strains of the parasite, before or during pregnancy. Although IHA titres developed in all maternal sera, the parasite could not be isolated from two stillborn foetuses or two babies born dead. Acute clinical toxoplasmosis was observed in only one neonate, following intra-uterine inoculation of the female. Serological, but no clinical evidence was obtained for transplacental transmission in two out of 18 progeny. Liver involvement, presenting as hepatitis, has been repeatedly reported in acquired toxoplasmosis (Pahissa et al., 1977; Vethanyagam and Bryceson, 1977; Briickner, 1978; Weitberg et al., 1979). Unusual symptoms associated with acquired toxoplasmosis included purpuric telangiectasia (Binazzi et al., 1977), and dermatomyositis in a case with a biopsy-confirmed muscle cyst (Topi et al., 1979). Fatal, chronic, acquired toxoplasmosis was reported by Tavolato et al. (1978) and Menges et al. (1979). Human infection attributed to direct contact with an acutely infected cow was documented by Saari et al. (1976), in Finland. The severe symptoms in this patient included rhinitis, sore throat, muscular pains, fatigue, cervical lymphadenopathy, cardiac symptoms and toxoplasmic chorioretinitis. Generally assumed to be too vulnerable to fluctuations in environmental conditions to contribute significantly to natural transmission of toxoplasmosis, the proliferative endozoic stage of the parasite has recently been shown to withstand a significant range of osmotic pressures and to survive for as long as 15-29 days in hyper- and hypotonic solutions (Raisanen and Saari, 1976, 1978). Toxoplasmosis has recently been implicated in the fatal outcome of several cases of Hodgkin’s disease receiving prolonged immunosuppressive therapy (Whiteside and Regent, 1975; van Berkel et al., 1976; Slavick and Lipman, 1977; Hoerni et al., 1978). Frenkel et al. (1975a) described the histological identification of toxoplasmic endozoites within necrotic brain lesions in two patients with Hodgkin’s disease and in another with multiple myeloma, all of whom had received prolonged treatment with antineoplastic drugs. They

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discussed the clinical aspects of these and 30 previously studied cases, gave experimental data on the effect of cyclophosphamide and urethane on the course of chronic toxoplasmosis, and suggested recrudescence of chronic infection as the cause of lesions in these patients. Frenkel et al. (1978) demonstrated that, in contrast, vinblastine and bleomycin interfered only slightly with the development of immunity in toxoplasmosis. The clinical course and diagnosis of toxoplasmic infection in the compromised host has been reviewed and discussed by Schimpef (1979). The potential value of computerized tomography in the diagnosis of toxoplasmic brain lesions was recently demonstrated, when purulent abscesses detected by this method in the brain o f a heart transplant patient wereaspirated and shown to contain toxoplasmic organisms (McLeod et al., 1979). Evidence is rapidly accumulating to indicate that even asymptomatic chronic toxoplasmosis is far from harmless. Piekarski et al. (1978b) and Witting (1979) reported a significant impairment of learning ability of rats, and particularly mice, chronically infected with the parasite. BaniC et a[. (1976) found a statistically significant link between latent toxoplasmosis and lower IQ levels in 409 eleven-year-old children. Alford et al. (1974) associated infection with impaired motor behaviour and low IQ in young children. Langset (1975) found a remarkably high incidence of infection (71-5%) in a group of children assessed as slow learners. Hutchison et al. (1980a, b) demonstrated a marked, selective effect on different categories of animal behaviour of I . gondii infection in mice. Infection appeared to increase the amount of general movement but suppressed response to novel stimuli. In addition, infection appeared to alter the pattern of bouts of behaviour. Werner (1980) suggested a possible mechanism of damage to the central nervous system; he showed that metabolic products of the cyst may be toxic, causing inflammatory granulomatous changes in perivascular tissues with eventual occlusion and sclerosis of the vessel. We wonder about the effect of such behavioural abnormalities on the chances of infected rodents falling prey to the felid final host. P. THE ROLE OF CATS IN THE DISSEMINATION OF HUMAN TOXOPLASMOSIS

The infectivity of the feline faecal 1. gondii oocyst to man per 0s has been clearly established by accidentally acquired laboratory infections (Hubner and Uhlikova, 1971; Miller el al., 1972; Overdulve, 1978). Earlier parasitological surveys estimated the natural prevalence of oocyst excretors amongst cats, from various geographical origins, as 0.4-2 % (Wallace, 1971, 1973; Hubner and Uhlikova, 1971 ; Janitschke and Kuhn, 1972; Werner and Walton, 1972; Dubey, 1973; Knoch et al., 1974). More recently, oocysts have been recovered from the faeces of 1.2% of stray cats, but from none of 52 pet cats, in Czechoslovakia (Jira and Roudna, 1977; Roudna, 1979); from 4.4% of 91 stray cats from southern Slovakia (ZastCra et al., 1977); and from 3.8% of stray cats in Odessa, U.S.S.R. (Kovbasyuk et al., 1976). Ruiz

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and Frenkel (1977) recovered I. gondii oocysts from two out of nine feline faecal samples deposited in false attics of houses in Costa Rica. In Egypt, Rifaat et al. (1976a) reported spontaneous oocyst excretion by eight out of a total of 318 cats investigated. Amaral et al. (1976b) recovered oocysts from one out of 20 feline faecal samples in SZo Paulo. Dubey et al. (1977a) isolated seven strains of the parasite from the faeces of 1000 cats in Ohio. Ito et al. (1974a), in Tokyo, recovered I. gondii oocysts from four out of 244 stray kittens weighing 500 g or less, but from none out of 202 cats weighing over 500 g. Serological surveys of cats indicate a wide discrepancy in rates of natural infection with I. gondii, from as low as four out of 108 in Saskatchewan, Canada (Nation and Allen, 1976) to as high as 88.7% in Czechoslovakia (Zastkra et al., 1977). Local regional variation of antibody prevalence from 96% to 53% was observed in Japan, with higher values amongst cats frequenting piggeries or slaughter houses (Sakurai 1976). A significant difference in prevalence of toxoplasmic antibodies was reported in sera of wild Lynx rufus, Felis concolor and F. catus from different areas in California, with strikingly higher values in coastal regions than in central and mountainous ones (Riemann et al., 1975a). Franti et d. (1976) detected serological evidence of infection in 38% of 47 rural domestic cats in North Carolina. The highest prevalence of IHA titres amongst carnivores, sheep and rodents was in the coastal region below 1000 ft [300 m] elevation, where the weather is cool and damp, and the lowest was in mountainous regions, where climatic extremes prevail. In Taiwan, about 28 % of 47 domestic pet cats were positive by the IHA, but none of 11 feral cats (Durfee et al., 1975). In Borneo, 41 of 69 cats were positive by the same test (Durfee et al., 1976). In Tokyo, 50% of 93 house cats had IHA titres (Murosaku, 1976), and 26 % of 1000 in Ohio, USA had IFA titres (Claus et al., 1977). Surveys of human sera by Ulmanen and Leinikki (1975), in Finland, detected no difference in CFT or IFA titres between owners of pet cats and others. However, a significantly higher prevalence of antibody was observed in sera of owners of pedigree cats. Infrequent hunting in the wild and more frequent consumption of raw meat by the cats, and closer contact between them and their owners, were suggested as possible explanations for this. In Czechoslovakia, circulating antibodies were detected in 54% of cat owners and in 42.7% of other persons. However, amongst teenagers, the incidence of antibodies was 39.5 % amongst cat-owners, but only 16 % amongst those without cats (Jindiichova et al., 1975). In Panama, contact with cats was associated with serological evidence of toxoplasmic infection in 13 of 46 siblings of patients with toxoplasmic lymphadenitis (ChavesCarballo, 1976). Sengbusch and Sengbusch (1976) reported antibodies in the sera of 18.3 % of animal-hospital workers, who had a varying degree of contact with cats, but in none of 60 people selected for lack of contact with felids. 50 % of the inmates of a psychiatric hospital in Madrid had IFA titres, with higher titres in younger and newly admitted patients, compared with a prevalence of 24 % in the general population ; this was circumstantially

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associated with gardening in the cat-infested grounds (Aparicio Garrido al., 1978). A most interesting account by Teutsch et al. (1979), of an outbreak of clinical toxoplasmosis amongst 37 patrons of a horse riding stable in Atlanta, Georgia, has been referred to in Section 11, L, 5. No meal had been communally eaten by the patients, the infection was directly correlated with the frequency of visits and the duration of time spent at one end of the stable, where cats had defaecated, two out of three of the stable cats were serologically positive, and toxoplasmic tissue stages were isolated from two kittens and four mice from the vicinity. Therefore, this outbreak of human toxoplasmosis, with a 95 % rate of clinical disease, must be attributed to direct contact with oocysts from feline faeces and warns against too hasty dismissal of the significance of cats in the acquisition of human infection. In view of additional possible sources of acquired human toxoplasmosis, such as ingestion of raw infected meat (Kean et al., 1969; Knaus, 1975; Masur et al., 1978) or raw infected milk (Riemann et al., 1975b), and direct contact with acutely infected animals (Saari et al., 1976), an accurate assessment of the role of the oocyst in human toxoplasmic infection remains elusive. However, the following facts must be considered. (i) Even pampered pet cats are difficult to confine and relish the occasional wild mouse or bird. (ii) Raw meat, particularly pork and mutton, which may be consumed by cats as pet food or as dustbin scraps, is not infrequently infected with tissue stages of the parasite. (iii) Following a single infective meal, a cat may shed, in a single bowel motion, up to 2 x lo7 oocysts; these readily become infective after sporulation and remain viable for many months; handling heavily contaminated soil may result in human beings picking up 10 to 100 oocysts under their fingernails (Frenkel et al., 1975b). (iv) Once infected, cats appear to harbour toxoplasmic stages in their intestinal tissues for a very long time (Dubey, 1977c) and may re-excrete oocysts at unpredictable intervals, e.g. following infection with I. felis (Chessum, 1972). (v) The antibody titre of a cat is a poor guide to its potential for oocyst excretion or re-excretion ; cats may develop circulating antibodies without shedding oocysts and, conversely, may shed oocysts in spite of a circulating antibody titre (Sheffield and Melton, 1974). (vi) Contamination of the environment by oocysts from naturally infected cats has been proven sufficient to induce severe illness in human patients (Teutsch et af., 1979) and to pose a very real threat to the young foetus of the acutely infected mother (Teutsch et af., 1980). The central role of Felidae in the epidemiology and epizootiology of toxoplasmosis is indicated by the following facts: (i) no serological evidence of human infection was found on cat-free Pacific atolls (Wallace, 1969); (ii) the prevalence of positive serological reactions in human sera was 4.7 % in a cat-free Siberian village, but four times this figure in neighbouring cater

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infested villages (Rogatykh, 1976); (iii) antibodies occur commonly in lifelong vegetarians. Feline faecal oocysts must also play an important role in the epidemiology of human toxoplasmosis by disseminating infection in meat and dairy farm animals, particularly sheep, in Australia and New Zealand, which cannot become infected by the congenital route alone. The high prevalence of infection in these countries with Sarcocystis gigantea (Collins and Crawford, 1979a, b), an obligate heteroxenous parasite of cats and sheep not readily transmitted across the placenta, supports the hypothesis that populations of feral cats may easily maintain high levels of ovine infection with I. gondii by faecal contamination of pastures. Local variations in the relative significance of the oocyst versus consumption of raw, infected meat or direct contact with infected animals are to be expected. Thus, amongst 2643 human beings in the U.S.S.R., the prevalence of antibody was generally higher amongst those in contact with cats (57%) than in those in contact with dogs only or with neither dogs nor cats (39 %) ; however, in three districts, direct contact with sheep and fur bearing animals was more significant than contact with pets (Shevkunova et al., 1976b). Seasonal variations in prevalence of human serological reactions (Tizard et al., 1976) and toxoplasmic lymphadenopathy (Fleck, 1978) may possibly reflect the dynamics of oocyst infection. 111. Isospora datusi (syn. Hammondia hammondi) Frenkel, Dubey and Wallace (1974) reported that Toxoplasma-like oocysts, isolated from the faeces of naturally infected cats from Hawaii and Iowa, induced elongate, thin-walled aseptate cysts (Fig. 5), predominantly in muscle and rarely in brain tissue of orally inoculated laboratory mice. Unlike those of I. gondii, neither the endozoites nor the cystozoites of this organism were readily infective to other mice by direct inoculation; nor could the mature oocysts initiate the gametogonic cycle in orally inoculated, susceptible cats, the life cycle being obligatorily heteroxenous (Frenkel et al., 1974; Frenkel and Dubey, 1975a, b). The parasite was designated Hammondia hammondi in a paper read by Professor Frenkel at the Third International Congress of Parasitology, held in Munich, in August 1974, while the detailed description of the parasite was written by Frenkel and Dubey (1975a). We synonymized Hammondia with the genus Zsospora (Tadros and Laarman, 1976). In order to avoid homonymy with Isospora hammondi of the marsh rice rat, Overdulve (1978) proposed the specific name datusi for this species. We shall therefore refer to the parasite as Zsospora datusi. The developmental stages of I. datusi in the intestinal tract of the feline final host are reminiscent of those of Z. gondii. No stage was observed in the intestinal tissues of cats during the first 70 h following oral inoculation with cystinfected mouse skeletal muscles. Schizonts were first observed 96 h after infection located within epithelial cells of the villi and glands. Gametocytes

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were observed between days five and ten after infection. The prepatent period was five to six days and shedding of oocysts lasted for 12 to 28 days. Unlike I. gondii, no tissue cyst or other extra-intestinal stage was detected in the final host histologically or by oral administration of muscular tissues or visceral organs of infected cats to susceptible kittens. However, pieces of small intestine of two cats, infected 35 and 85 days previously, were fed to four uninfected cats, two of which subsequently excreted oocysts (Frenkel and Dubey, 1975a). This suggested chronic infection of the intestinal tract, with as yet uncharacterized latent stages. This assumption is borne out by the spontaneous shedding of oocysts by feral cats, following immunosuppressive treatment. Dubey and Streitel (197613) demonstrated that early tissue stages in mice, one to nine days after oral inoculation with oocysts, were not infective to cats. The same authors failed to transmit this parasite transplacentally in mice. Eydelloth (1977) attempted to obtain the complete gametogonic cycle of a strain of the parasite, isolated in Germany, in foxes, lions, tigers, pumas, bobcats, jungle cats and the European wild cat. Of these, only the European wild cat, Felis silvestris, excreted oocysts. Wallace (1975) reported that mice, given cortisone acetate before oral inoculation with homogenates of mouse muscle containing I. datusi cysts, failed to exhibit histologically detectable muscle cysts ; however, when fed to a cat, they induced oocyst shedding. The same author subinoculated homogenates of liver, spleen and abdominal muscle of mice (inoculated intraperitoneally eight days previously with one million excysted sporozoites of the Hawaiian strain of I . datusi) into another laboratory mouse; the latter was fed 35 days later to a cat which subsequently excreted oocysts. Endozoites of the same strain from the peritoneal fluid of mice, previously inoculated intraperitoneally with massive numbers of excysted sporozoites, were transmitted to mice by intraperitoneal inoculation. Subsequent passage of the parasite was, however, not possible. Frenkel and Dubey (1975a) failed to transmit the Iowan strain from mouse to mouse by inoculation of cystozoites. They inoculated cortisone-treated mice with endozoites contained in mesenteric lymph nodes, from a mouse fed one million oocysts nine days previously. Rapid, repeated intraperitoneal subinoculation of homogenates of the lymph nodes, spleen and liver into more cortisone-treated mice failed to transmit the parasite. Following ingestion of mature oocysts, rats, hamsters and guinea-pigs were shown to be experimental intermediate hosts for I. datusi by the infectivity of their tissues to cats ; multimammate rats and white-footed mice developed dye-test titres (Frenkel and Dubey, 1975a, b). The list of potential intermediate hosts of I. datusi was recently extended to include several species of rodents (Apodemus Jtavicollis, A. sylvaticus, Clethrionomys glareolus, Microtus agrestis, M . arvalis), a lagomorph (Oryctolagus cuniculi) and even pigs, as demonstrated by experimental recycling of the parasite in cats (Eydelloth, 1977). Oocyst excretion did not follow oral administration to cats of muscle and visceral organs of A. agrarius, sheep, cattle,

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pigeons or Japanese quail (Frenkel and Dubey, 1975a; Wallace, 1975). Chickens (Dubey and Streitel, 1976b) also apparently do not serve as suitable intermediate hosts for this organism. Dogs were fed sporulated oocysts ; no tissue cyst was seen in sections of their extra-intestinal tissues, but pieces of these organs induced oocyst shedding when fed to susceptible kittens (Dubey, 1975a). Sporulated oocysts were fed to single specimens of Sanguinus nigricollis, Mucuca fascicularis, M . mulutta and Cercocebus utys. All the monkeys developed transient dye-test titres against toxoplasmic antigen; apparently only S. nigricollis harboured tissue stages, as demonstrated by excretion of oocysts by a cat, orally inoculated with pooled tissues of this animal (Dubey and Wong, 1978). It is interesting to note that of all animals shown to harbour extraintestinal stages of I. dutusi, tissue cysts were histologically detected only in mice (Frenkel et ul., 1974; Frenkel and Dubey, 1975a; Wallace, 1975) and in hamsters (Eydelloth, 1977),which permits the speculation that "hypnozoites", i.e. resting or dormant sporozoites, rather than tissue cysts may be involved in several of these intermediate hosts. Cross reaction against toxoplasmic antigen was detected in the dye test, using sera of mice experimentally infected with this parasite, but not sera of cats harbouring the gametogonic stages (Frenkel et ul., 1974; Frenkel and Dubey, 1975a; Wallace, 1975). The last author detected low titres against I. datusi cystozoites by the IFA technique in sera of patients with clinical toxoplasmosis. A remarkable degree of cross protective immunity against toxoplasmosis was shown by the survival of mice, experimentally infected with tissue stages of I. datusi, when challenged with up to lo5 LDS0of I. gondii oocysts (Frenkel and Dubey 1975). Similar observations were made in mice and hamsters by Christie and Dubey (1977). Hamsters previously infected with I. dutusi survived challenge with the lethal dose of I. jellisoni (Dubey, 1978d). However, chronic infection of mice with I . gondii did not prevent subsequent infection with the Hawaiian strain of I. datusi (Wallace, 1975). Quantitative data on the degree of protective immunity are apparently not available for intermediate hosts, infected with I. gondii and challenged with I. datusi. Frenkel and Dubey (1975a) failed to reinfect 13 out of 14 cats with this parasite and reported no cross immunity between I. datusi and I. gondii in the feline final host. The absence of such cross immunity was also noted by Wallace (1975). However, Dubey (1975b) observed excretion of oocysts by cats after a first, second and even a third oral inoculation with I. dutusi tissue cysts in mouse muscle. Spontaneous shedding of oocysts was observed at irregular intervals for up to 120 days after infection. I . dutusi has been isolated from the faeces of naturally infected cats in the U.S.A. (Christie et al., 1977) and in Germany by Rommel and von Seyeri (1976), who detected no, or only low dye-test titres against toxoplasmic antigen, and by Schulze and Vocke (1978), who found no cross reaction with toxoplasmic antigen in the complement fixation text (CFT). A strain of the parasite has been isolated in Australia from the faeces of cats fed wild

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Rattus rattus and Mus musculus (Mason, 1978); this is perhaps the first identification of natural intermediate hosts. Hendricks et al. (1979) reported isolating large, unsporulated oocysts (40.8 x 28-5pm) from a naturally infected ocelot (F. pardulis). The sporulated oocysts were not directly infective to Felidae, but induced tissue stages in mice infectiveper os to ocelots and other feline carnivores. The parasite was named Hammondiapardalis. However, the tissue stages described in the mice 10 to 12 days after infection, clearly represent two consecutive generations of schizonts. The morphology of these, their location in histiocytes of the lung, as well as the severe symptoms in mice, frequently with a fatal outcome, strongly suggest the acute schizogonic phase of sarcosporidiosis, rather than infection with Hammondia, which undergoes schizogony solely in the intestinal tissues of the felid final host (Frenkel and Dubey, 1975a, b). We (Tadros and Laarman, 1976) interpreted the association of sarcosporidiosis in mice with oral inoculation of I.felis-like oocysts, from cats, reported by Powell and McCarley (1975), as due to mixed infection with I . .felis and undetected sarcosporidian sporocysts in the feline faecal inoculum; an interpretation since vindicated by further research (Last and Powell, 1978). We believe that Hendricks and colleagues (1979) were dealing with a mixed infection of an I . heydorni-like coccidian of Felidae, which forms latent sporozoites in the rodent host, and undetected sporocysts of a species of Sarcocystis with a feline-murine cycle. AND BESNOITIAN ISOSPORIASIS IV. BESNOITIOSIS

A.

GENERAL ASPECTS

Since the discovery by Besnoit and Robin (1912), of conspicuous, thickwalled subspherical cysts in a Pyrenean cow, with visceral and cutaneous lesions, several species of Besnoitia have been recognized, primarily on the basis of geographical incidence and identity of susceptible hosts. B. besnoiti has been reported in cattle, impala, blue wildebeest and kudu in South Africa (Hofmeyr, 1945; Pols, 1960; Basson et al., 1965), cattle in Kazakhstan (Vsevolodov, 1961) and cattle and sheep in Israel (Neumann and Nobel, 1960). B. bennetti has been recorded in horses, mules and asses in Africa (Bennett, 1939; Bigalke, 1970a), burros in Mexico (Jones, 1957.; Terrell and Stookey, 1973) and mules in Kazakhstan (Zolotareva, 1965). Another species, B. tarandi, infects reindeer and caribou in Alaska and Canada (Hadwen, 1922; Choquette et ul., 1967; Wobeser, 1976) and has also been recorded at Tajmyr and Jamal in arctic Siberia (Nikolaevsky, 1961; Golosov and Mitzkevitch, 1964; Klimontov, 1966). B. darlingi was first observed in the common opossum in Panama (Darling, 1910) and was rediscovered in the same host by Schneider (1967a). Probably the same species was described in opossums from Kentucky (Conti-Diaz et al., 1970), Missouri and Illinois (Flatt et a/., 1971) and Kansas City (Smith and Frenkel, 1977). B. jellisoni,

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first discovered in the white-footed mouse, Peromyscus maniculatus, in Idaho (Frenkel, 1953; Jellison et al., 1956) has since also been described from three species of kangaroo rats in California and Utah (Ernst et al., 1968). An unnamed species of Besnoitia was reported in another rodent, Microtus torques, in Peru (Jellison et al., 1960). B. sauriana was named by Garnham in 1966 from naturally infected lizards (Basiliscus vittatus) in Belize. In the same month of the same year, Schneider (1965) found a similar parasite in the lizards B. basiliscus and Ameiva ameiva, in Panama. Unlike Garnham’s parasite, this species was readily transmissible to mice and was named B. panamensis. An unnamed besnoitian organism has recently been identified as the causative agent of an epizootic among knots, Calidris canutus, in Florida (Simpson et al., 1977), the first record of besnoitian tissue cysts in an avian host. The recognition of B. bennetti as a species distinct from B. besnoiti has been justified by the strict host specificity of these two organisms (Bigalke, 1970a). However, the validity of recognizing so many other species remains subject to debate. Thus, Schneider (1967a) succeeded in adapting B. panamensis of lizards and B. darlingi of opossums to mice, and found the two species to be practically identical, except in virulence. These findings, together with the complete cross immunity between the two organisms, led the same author (Schneider, 1967b) to conclude that B. panamensis was a synonym of B. darlingi. Schneider (1967a) regarded B. sauriana as another synonym of B. darlingi. Stabler and Welch (1961) referred the parasite they isolated from opossums to B. jellisoni, while Conti-Diaz et al. (1970) believed that B.jellisoni and B. darlingi were synonyms. In the following text, Besnoitia will be referred to as Isospora (see Tadros and Laarman, 1976). The relationship of the besnoitian parasite of African wild antelopes to that of cattle was investigated in South Africa by Bigalke et al. (1967), who studied the susceptibility of rabbits, cattle and sheep to antelope strains, and their subsequent protection to challenge with bovine strains. Although there were biological differences between the two types of strains, infection with those from wild antelope protected antelope, cattle and rabbits against challenge with the bovine strain. The authors concluded that the antelope parasites constituted distinct strains or races of I. besnoiti. Frenkel (1 973a) remarked that studies of serological cross reactions amongst besnoitian species were greatly hampered by differences in susceptible hosts, and we believe that decisions about the validity of different specific designations must await elucidation of sexual cycles and identification of definitive hosts. Thus, the recent identification of the cat as the final host of I. darlingi (Smith and Frenkel, 1977) but not of I. jellisoni (Wallace and Frenkel, 1975) argues strongly for their separate taxonomic status. However, as tissue cysts of Isospora gondii can lose the ability to initiate gametogony in cats, following repeated syringe passage in rodent intermediate hosts (Frenkel et al., 1976), attempts at experimental infection of cats and other potential final hosts with I. jellisoni should be carried out with cysts

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from naturally infected rodents. Iso-enzyme characterization would, in our opinion, furnish the most reliable information for comparing isolates, derived from tissue cysts in hosts of different geographical origin, of strains which complete their gametogonic cycles in the same final host species. Besnoitiosis has an acute phase, during whxh rapidly proliferating endozoites are usually found in the peritoneal fluid, blood and visceral organs (Bigalke, 1970b; Frenkel, 1973a). This stage, which is comparable to acute toxoplasmosis, may be pathogenic, even fatal. Alternatively, it may give way to chronic infection, in the course of which the besnoitian tissue cyst develops in various tissues (Figs. 7-9). This cyst has a characteristic, conspicuous, fibrillar wall of host origin, enclosing the multinucleate, usually vastly hypertrophied, parasitized host cell. Besnoitian endozoites and cystozoites are morphologically indistinguishable, by light and electron microscopy, from the corresponding toxoplasmic stages ; asexual reproduction, likewise, takes place by endodyogeny or endopolygeny (Sheffield, 1966; Stnaud, 1969; Scholtyseck et al., 1974; Stnaud et al., 1974; Stnaud and Mehlhorn, 1977). The development of the tissue cyst of I. jellisoni has been intensively studied by light microscopy (Frenkel, 1953, 1970) and by electron microscopy (Sheffield, 1968 ; Stnaud, 1969). I . besnoiti has been similarly studied by light microscopy (Pols, 1954, 1960; Schulz, 1960; Basson et al., 1970) and electron microscopy (Fedoseenko, 1976). Degeneration of cysts (Fig. lo), accompanied by cellular infiltration, has been described for I . jellisoni by Frenkel(l961) and for I. besnoiti by Basson et al. (1970). B.

SEROLOGY

A serological comparison of Isospora darlingi, I . jellisoni and different strains of I . gondii by indirect immunofluorescence, complement fixation and indirect haemagglutination (Suggs et al., 1968), revealed various degrees of affinity amongst and even within each species. Tadros et al. (1975~)reported the absence of cross reaction between I. besnoiti and toxoplasmic endozoites, but slight cross reaction of besnoitian endozoites with sarcocystic and frenkelian cystozoite antigens in the IFA test. Sera from mice infected with I. wallacei cross reacted slightly with I . jellisoni, but not with I . gondii, in the dye test; however, the same sera cross reacted with I . gondii and, slightly more strongly, with Sarcocystis muris in the IFA test (Frenkel, 1977b). Weiland and Kaggwa (1976) reported comparable IFA and ELISA titres in the sera of rabbits with acute or chronic infections with I. besnoiti or I . jellisoni. C.

IMMUNITY

Golden hamsters, chronically infected with I. jellisoni, become immune to challenge intraperitoneally or subcutaneously, the acquisition of immunity being accompanied by a sharp decrease in the number of parasites (Frenkel

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and Lunde, 1966). Giving cortisone subcutaneously (but not intraperitoneally or orally) brings about a relapse in immunized hamsters in 7 to 14 days; this effect of corticoids, only evident in partially or completely immune animals, did not accelerate death during primary infection. Antibody levels, estimated by the dye test and haemagglutination, remained stable in chronically infected hamsters throughout the period of corticoid-induced relapse ending in death, immunity to besnoitiosis being largely cell-mediated (Frenkel and Lunde, 1966; Frenkel, 1977a). This immune mechanism, in hamsters chronically infected with besnoitiosis, being susceptible to corticoids, was proposed as a useful model for studying infectious diseases such as pneumocystosis, emerging as relapses rather than primary infections during corticoid therapy. Frenkel(l967) demonstrated that intact (but not lysed) cells from the spleen and lymph nodes transfer specific immunity against I. jellisoni among hamsters, whereas bone marrow, thymus, liver or kidney cells from immune donors were ineffective. Antiserum showed a slight protective effect and appeared to enhance the immunity transferred by cells. Frenkel and Wilson (1972) studied cell-mediated immunity against I. jellisoni in golden hamsters following total body irradiation. Active immunization was inhibited by 600 rads, delivered 22 days before to 27 days after experimental infection. Antibody production was impaired by 600 rads delivered four or 24 hours after infection. Allogeneic recipients receiving 800 rads or more were no longer capable of benefiting from adoptive immunization. Although elicited, interferon appeared ineffective against besnoitiosis (Frenkel, 1973a). Hoff and Frenkel (1974) studied in vitro the interaction of besnoitian endozoites and host cells in hamster macrophages and lymphocytes. Peritoneal lymphocytes from immunized hamsters failed to neutralize extracellular parasites in v i m , lymphokine being apparently not cytotoxic for such extracellular organisms. However, sensitized lymphocytes appeared FIGS7-12. Isosporu species inducing besnoitiosis in intermediate hosts. FIG.7. Macroscopically visible tissue cysts (+) of I. besnoiti in the jugular vein of naturally infected wildebeest from South Africa. Note translucent, pearl-like appearance of cysts. FIG.8. Fresh preparation of intact, micro-isolated tissue cyst of I.jelZisoni from experiand absence of internal mentally infected laboratory mouse. Note cyst wall (+) septation ( x 330). FIG.9. Massive infection of bovine skin with I . besnoiti tissue cysts. Haematoxylin and eosinstained section ( x 132). FIG.10. Leaking cyst of I.jelhoni in hamster tissue (+), PAS-stained section ( X 346). Note intense host cell reaction. FIG.11. Schizogonic stage of I. wallucei. Note convoluted rows of developing merozoites (+). Haematoxylin and eosin-stained section of feline ileum ( x 560). FIG.12. I. wallucei gametocytes (+) in goblet cells of the small intestine of the feline final host. Haematoxylin and eosin-stained section ( x 560). . (FIGS10, 1 1 and 12 from transparencies kindly supplied by Prof. J. K. Frenkel; FIGS7 and 9 by courtesy of Prof. R. D. Bigalke.)

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to instruct macrophages specifically to destroy besnoitian organisms in vitro. Specific besnoiticidal information was transferred with immunized lymphocytes, but not in supernatant medium, to non-immune macrophages in culture. The authors concluded that a number of distinct processes mediated by lymphoid cells including delayed hypersensitivity, macrophage activation and specific cellular immunity, act simultaneously during latent besnoitian infection in hamsters. Lymphocyte activity was inhibited by addition to the cultures of 5 pg ml-l cortisone, macrophage activity was inhibited by 20 pg ml-l, while 50 pg ml-' inhibited macrophage effects even on organisms treated with specific antibody (Lindberg and Frenkel, 1977b). More recently, a mediator that inhibited intracellular proliferation of the parasite was isolated from immune lymphocytes in contact with specific antigen (Chinchilla and Frenkel, 1978). This mediator was parasite- and host-specific, resisted heating at 56°C for 30 min, was sensitive to chymotrypsin, but resistant to ribonuclease and deoxyribonuclease. The mediator conferred immunity not only on macrophages but also on fibroblasts and kidney cells. Inhibition of viral carcinogenesis and of the growth of transplanted tumours has been reported to occur in mice, chronically infected with I . jellisoni (Hibbs et al., 1971; Lunde and Gelderman, 1971). Macrophages, activated by I . jellisoni, have been shown to kill tumour cells and inhibit incorporation by these cells of 3H-thymidine (Frenkel and Reddy, 1977). The same authors found that induction of liver neoplasms in rats with 3'-methyl-dimethylaminoazobenzene is delayed, but not prevented, in animals chronically infected with this parasite. The feasibility of developing a vaccine against bovine besnoitiosis was investigated by Bigalke et al. (1967, 1973, 1974). Laboratory and field trials used a strain of I. besnoiti isolated from blue wildebeest and repeatedly passaged in rabbits. The parasite, in lamb kidney cell cultures, was stored as a deep frozen stabilate until used as a live vaccine. A single dose protected cattle against clinical besnoitiosis, following experimental challenge with 100 x the vaccine dose of bovine I . besnoiti, for at least one and up to four years. The immunogenicity of the wildebeest stabilate was studied in rabbits (Bigalke et al., 1974). Rabbits that survived subcutaneous inoculation with 1-2 x lo5 organisms, were protected against challenge, one to six months later, with 10 to 100 000 times this number of bovine besnoitian parasites. D.

PATHOLOGY

The pathological changes associated with acute and chronic besnoitiosis are largely dependent on the species of parasite, the virulence of the strain, the history of its laboratory maintenance, the species of host infected, and the type of parasitized tissue. Subacute and chronic besnoitiosis of naturally infected cattle has been studied by Pols (1960), Schulz (1960) and Basson et al. (1965). Following the

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discovery that rabbits are susceptible to infection with endozoites of I. besnoiti (Pols, 1954), as well as cystozoites (Bigalke, 1960), Basson et al. (1970) carried out extensive histopathological investigations to compare the course of acute and chronic besnoitiosis in rabbits and cattle. Generalized, pronounced anasarca, accompanied by degenerative and necrotic vascular lesions, vasculitis and thrombosis, was associated with the proliferation of bovine strains of the parasite in the endothelium of the blood vessels during the acute phase. These lesions gave rise to oedema, dystrophic changes and occasionally infarction, particularly in the skin and the testis, the latter resulting in orchitis and decreased fertility in bulls and rabbits. Antelope strains of the parasite were generally less pathogenic to rabbits; however, repeated passage in the latter led to enhancement of pathogenicity and to eventual loss of the ability of the parasite to form tissue cysts (Bigalke, 1968). Massive infection with besnoitian cysts, during the chronic phase of infection, manifested itself clinically in cattle as scleroderma, characterized by a granulomatous reaction and accompanying fibrosis around the numerous cysts in the stratum papillae as well as hyperkeratosis and acanthosis. Rabbits infected with the antelope strains exhibited internal rather than skin lesions. This difference in cyst site predilection of strains originating from antelope and cattle had previously been observed by McCully et a f . (1966), who found cysts, in naturally infected cattle, predominantly close to the superficial veins of the head, skin and extremities, whereas in the antelope they usually infected the endocardium and intima of the heart. The course of infection with I. jellisoni has been comprehensively investigated by Frenkel (1956a, 1961, 1965 and reviewed by Frenkel, 1973a). In view of the regular occurrence of retinal involvement in hamsters, the same author suggested besnoitiosis in this animal as a useful model for the investigation of toxoplasmic retinochoroiditis in man (Frenkel, 1965). Frenkel also drew a parallel between chronic besnoitiosis in hamsters and certain cases of tuberculosis and histoplasmosis, in that necrosis of the adrenal gland may be observed as the predominant active site of progressive infection; he suggested besnoitiosis in the hamster as a model for studying Addison’s disease in man (Frenkel, 1956b, 1977a). I. darlingi, isolated from wild opossums in Panama, exhibited enhanced virulence for mice and hamsters following passage in mice. Fulminating, often fatal infections accompanied by hypothermia, inflammation of the intestine and mesentery, were observed in hamsters and mice, while infected guinea-pigs remained asymptomatic. Acute, rapidly fatal infection followed intraperitoneal inoculation of the parasite into squirrels, marmosets, a woolly opossum and a four-eyed opossum, while laboratory rats, rhesus and night monkeys remained refractive to infection (Schneider, 1967~).Another strain of I. darlingi, isolated by Conti-Diaz et al. (1970), gave rise to fatal infection in hamsters, accompanied by bloody peritoneal and pleural exudates and gross lung lesions, but was asymptomatic and perhaps even non-infective to white mice.

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Severe chronic besnoitiosis of reindeer leads to “corn meal” disease, named because of the gritty feel of the skin, which renders the flesh unfit for human consumption. Pathologic lesions were described in a naturally infected woodland caribou, found dead in Saskatchewan, in Canada (Wobeser, 1976). Precirrhotic and cirrhotic liver changes have been associated with besnoitiosis in chamois, in Switzerland (Burgisser, 1975). E.

TRANSMISSION, LIFE CYCLE AND EPIZOOTIOLOGY

Besnoitiosis induced by, e.g., I. besnoiti, I. jellisoni or I. darlingi is readily transmissible to various laboratory animals by inoculation of endozoites or cystozoites, while other species, e.g. I. wallacei, appear to be refractory. I. jellisoni has been successfully cultivated in vitro in bovine kidney, spleen and trachea (Fayer et al., 1969); in porcine and rabbit kidney (Akinchina and Doby, 1969a, b); and in chicken fibroblast cell lines (Doby and Akinchina, 1968; Akinchina and Doby, 1969b). I. besnoiti from South Africa has been cultivated in bovine, lamb and Vero monkey kidney cell lines and in embryonated chicken eggs (Bigalke, 1962; see also Neuman, 1974). 1. besnoiti cystozoites from the skin of cattle in Kazakhstan were cultured in bovine kidney cell lines (Poluboyarova and Yaps, 1978). The mode of natural transmission of besnoitiosis has intrigued veterinary parasitologists for well over half a century. I. besnoiti of cattle was successfully transmitted by intravenous inoculation of large volumes of blood from acutely infected cattle (Cuillt et al., 1936;Pols, 1954). Bigalke (1960) demonstrated mechanical (non-cyclical) transmission of besnoitiosis during the acute phase by blood sucking tabanid and stable flies. On the basis of finding besnoitian cysts in the walls of blood vessels, McCully et al. (1966) revived the postulation of Besnoit and Robin (1912) that cystozoites from ruptured cysts may maintain parasitaemia in chronically infected cattle. In 1967, Bigalke succeeded in transmitting I. besnoiti from chronically infected cattle to calves and rabbits by inoculation of cystozoites. Bigalke established that cysts may remain viable for up to nine years in the skin of chronically infected cattle, and suggested that they may constitute a reservoir for arthropod transmission of besnoitiosis to uninfected cattle. The suggestion by McCully et al. (1966), that periodic release of cyst organisms into the blood circulation of wild antelopes would make available cystozoites for mechanical transmission by blood sucking arthropods, has not been substantiated by experimental evidence. Khvan (1968) pointed out that cattle in Kazakhstan may become infected with besnoitiosis during winter, when flying Diptera are completely absent, and suggested that ixodid ticks may bring about mechanical transmission of the parasite. The observation that I. jellisoni is transmissible amongst rodents by the consumption of acutely or chronically infected tissues (Jellison et al., 1956) and the greater resistance of the cystozoites to digestive enzymes ascompared to endozoites (Ernst et al., 1968) indicated that cannibalism or carnivorism

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may play an important role in the transmission of this organism, and of I. darlingi and other species with a fairly loose intermediate host specificity. Congenital infection with besnoitiosis has been reported in an aborted calf, in Uganda (Bwangamoi, 1968). Venereal transmission of besnoitiosis has not been recorded, in spite of the remarkable frequency of occurrence of besnoitian tissue cysts in the reproductive organs of both sexes, e.g. I. besnoiti in cattle and goats in Kazakhstan (Peteshev et al., 1974) and in cattle in Israel (Neuman et al., 1978), Z.jellisoni in kangaroo rats (Ernst et al., 1968) and in mice (Frenkel, 1965) and I. darlingi in opossums (Smith and Frenkel, 1977) in the U.S.A. Direct acquisition of besnoitiosis by the ingestion of acutely or chronically infected tissues provided a feasible explanation for transmission to rodents, carnivores or carrion feeders, e.g. opossums, but failed to account for its acquisition by herbivores, e.g. cattle, sheep and horses. In 1974, Peteshev et al. resolved this enigma by demonstrating cyclical transmission through Felidae of I. besnoiti parasitizing cattle in Kazakhstan. Besnoitian cysts from naturally infected cattle were fed to wolves, dogs, korsak foxes, ground squirrels, goats, lambs, hedgehogs, white mice, rooks, domestic cats and a wild spotted cat, Felis lybica. The canine animals, the hedgehogs and the rooks apparently failed to become infected. The ground squirrels died with acute besnoitiosis, while the goats, lambs and mice developed chronic besnoitiosis. Thirteen to 16 days after being fed with besnoitian tissue cysts, all three cats shed oocysts, measuring 11-5-14.2 x 14.2-16.0 pm, during a patent period of three to five days. The spotted cat died on the 13th day after infection, but was not examined for intestinal or extra-intestinal stages. The domestic cats remained in good health. When sporulated, the oocysts were disporic and tetrazoic. The oral inoculation of feline oocysts after incubation in water for from six days to six months induced besnoitiosis in ground squirrels, mice, goats, sheep and a calf. White mice were experimentally infected with besnoitiosis, either by oral administration of bovine besnoitian tissue cysts or by inoculation with blood from febrile goats, themselves experimentally infected with feline oocysts. The brains of the mice were fed to individual kittens, which later excreted oocysts, infective after sporulation to ground squirrels. More recently, Peteshev and Polomoshnov (1976a, b) established that Ondatra zibethica, Microtus arvalis, Rhombomys opimus, Lepus tolai and Passer montanus were reservoir hosts of I. besnoiti in Kazakhstan. Khvan et al. (1976) reported severe clinical infection in sheep and fatal infection in Saiga tatarica, following experimental infection with I . besnoiti endozoites. Pak (1976) inoculated besnoitian cystozoites from skin cysts of I. besnoiti of cattle from Kazakhstan into laboratory mice and susliks (CitelZusfulvus). Parasites proliferated in the peritoneal cavity and showed a predilection for the viscera but not for skin, subcutaneous tissues or brain of the rodents. The isosporan coccidian nature of besnoitia has since received additional confirmation by the isolation of a new species, namely I. wallacei from mice, fed isosporan oocysts shed by a naturally infected Hawaiian cat (Wallace

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and Frenkel, 1975; Frenkel, 1977b). The oocysts, which measured on average 12 x 17 pm, induced the formation of besnoitian cysts in the wall of the intestine, following oral inoculation, and in the peritoneum, following intraperitoneal inoculation, in laboratory mice and in laboratory as well as Polynesian rats, but were apparently not infective to hamsters or to Rattus rattus. Curiously enough, endozoites could not be microscopically detected during the acute phase of infection of the rodent hosts, nor was the parasite readily transmissible from rodent to rodent during this stage by intraperitoneal inoculation of peritoneal fluid. Laboratory rats and mice failed to develop tissue cysts or circulating antibodies following oral or intraperitoneal inoculation of tissue cysts; Rattus exulans appears to be susceptible but does not always develop tissue cysts, indicating that the natural intermediate host has yet to be identified. The oral administration of experimentally induced tissue cysts successfully initiated oocyst excretion by young kittens, with a prepatency of 12 to 15 days and a patent period of 5 to 12 days. No intestinal stage was detected one to four days after infection in experimentally infected kittens, an observation reminiscent of that reported by Overdulve (1978) on experimental infection of cats with 1. gondii. Large, asynchronously maturing schzonts (Fig. 11) were observed within endothelial or intimal cells of the blood vessels of the lamina propria, as well as within hepatic sinusoids. Gametogony appeared to take place in the goblet cells of the small intestine (Fig. 12). The parasite could not be transmitted directly from cat to cat by oral administration of mature oocysts, the cycle being obligatorily heteroxenous. Although schizonts were found in extra-intestinal sites, such as liver sinusoidal cells, in contrast to I . gondii, this parasite does not appear t o form tissue cysts in the feline final host. Cats developed significant IFA titres at the end of patency of the primary infection, but remained susceptible to a second and third infection (Frenkel, 1977b). Oocysts attributed to I. wallacei were recently recovered from the faeces of cats fed wild Rattus norvegicus and R . rattus, in Australia. The parasite was successfully cycled in laboratory rats and mice (Mason, 1980). Recently Ito et al. (1978) reported isolating isosporan oocysts from feral cats, which induced besnoitian tissue cysts in rats, mice and Mongolian gerbils. The schizogonic and gametogonic stages in the feline host were similar to those of 1. wallacei (Frenkel, 1977b). In 1977, Smith and Frenkel demonstrated the cyclic transmission of yet another species of the parasite, I. darlingi of common opossums, through the domestic cat. Oral administration of chronically infected tissues from a naturally infected opossum, induced the shedding of immature coccidian oocysts, measuring 11.9 x 12.3 pm on average, by a cat but not by a dog. When sporulated, the disporic tetrazoic oocysts were infective to mice via the subcutaneous, oral and intraperitoneal routes. Recycling of the parasite in kittens was demonstrated with a prepatency of 11 to 14 days and a patent period of 5-8 days. The parasite was readily transmissible to hamsters and mice by inoculation of endozoites or cystozoites. A single challenged cat failed to excrete oocysts.

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Our present knowledge of the epizootiology of besnoitiosis indicates an interestingly complex spectrum of possibilities for the natural transmission of besnoitian organisms belonging to different species. Mechanical transmission by blood sucking arthropods of circulating endozoites (during the acute phase) or cystozoites from cysts in the skin (during the chronic phase) is probably of appreciable significance in the maintenance of besnoitiosis in domesticated cattle in regions like South Africa, where blood sucking Diptera are abundant for several months of the year. However, except during the transient acute phase of infection, haematophagous Diptera can hardly play a significant role in the transmission of besnoitiosis of wild African antelopes, the tissue cysts of which have a distinct predilection for inaccessible, deeper blood vessels. Furthermore, transmission by biting arthropods is probably of little importance in maintaining bovine besnoitiosis in regions like Kazakhstan, where ixodid ticks are the only biting arthropods active during several months of the year, during which besnoitian infection is known to occur (Khvan, 1968), as no experimental evidence is available for prolonged survival of besnoitian organisms in poikilothermic invertebrates or transovarian transmission of the parasite, comparable to that of Babesia. The establishment of cyclical transmission of three species of parasites with besnoitian tissue cysts and obligatorily heteroxenous life cycles, confirmed the major biological significance of the tissue cyst stage in the maintenance of besnoitiosis. The failure of attempts to complete the developmental cycle of the African parasite of cattle in cats or dogs, in South Africa (Bigalke, personal communication) or in dogs, cats, a serval, vultures or maribou, in Uganda (Rommel, 1975) is puzzling. The parasite in Asian cattle has several additional natural intermediate hosts, e.g. Microtus, Ondatra and Passer montanus (Peteshev and Polomoshnov, 1976a), which facilitate regular cyclical transmission via Felidae ; in Africa no rodent or avian natural intermediate host has been identified, so transmission may be only via the abundant blood sucking Diptera, with gradual selection for strains with accessible skin tissue cysts. Mechanical passage of such strains by insects may have resulted in a partial loss or change of the genome, rendering them unable to complete gametogonic development in cats, as has been observed in rapidly syringe-passaged I . gondii (Frenkel et al., 1976). The deeper location of besnoitian tissue cysts in the cardiovascular system of wild African antelopes is strongly suggestive of transmission via a carnivore. In spite of numerous biological similarities between the antelope and cattle parasites in Africa (Bigalke et al., 1967), it may still transpire that two separate species are involved. V. OTHERISOSPORAN

PARASITES WITH EXTRA-INTESTINAL TISSUE STAGES

The elucidation of the isosporan coccidian nature of Toxoplasma focused attention on other isosporan parasites, particularly of cats and dogs. Research has since revealed that the life cycles of several of these diverge from the

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previously assumed simple, eimerian pattern. In the present article we are primarily interested in reporting advances in research on isosporan coccidian organisms, which form extra-intestinal stages in the same or in one or more intermediate hosts. In 1950, Garnham erected the new genus Atoxoplasma for small intraleucocytic parasites of numerous avian hosts, which had previously been referred to the genera Hepatozoon, Haemamoeba, Haemogregarina or Toxoplasma (for detailed reviews, see Baker et al., 1972; Tadros and Laarman, 1976). In 1967, Box, in the U.S.A., established a direct correlation between the degree of parasitaemia and pathological manifestations due to these intra-leucocytic organisms in sparrows, and exposure to sporulated oocysts of Isospora excreted by these birds. She later confirmed the isosporan nature of the intra-leucocytic organisms by inducing the appearance of so-called “Atoxoplasma” in uninfected sparrows (Passer domesticus) or canaries (Serinus cararius) by feeding them sporulated isosporan oocysts, recovered from the droppings of naturally infected sparrows and canaries respectively (Box, 1975). For many years, isosporan parasites from passerine birds were catalogued on the basis of the morphology of the oocyst and loosely designated I. lacazei. Following further transmission experiments, Box (1975, 1977) recognized two separate species of Isospora in S. canarius. Oral administration of mature oocysts of I. serini to canaries was followed by prolonged schizogonic development, comprising five asexual generations in extra-intestinal mononuclear phagocytes (Figs 13-1 5), with two additional schizogonic generations and gametogony occurring in the intestinal epithelium. The other species, which was designated I . canaria, was found to have a conventional coccidian type of life cycle, with all asexual generations and gametogony restricted to the epithelial cells of the duodenum. While the patency of infection with I. canaria did not exceed 14 days, oocysts of I. serini continued to be shed for as long as 231 days. Intensive investigations have been carried out by light and electron microscopy on the developmental cycle of a species of Isospora, referred to as I. lacazei, from the passerine bird, Carduelis (Hernandez Rodriguez and Martinez Gomez, 1975; Hernandez Rodriguez et al., 1976a, b, 1978; Calero Carretero et al., 1977). The fine structure of the oocyst wall of I. lacazei of sparrows has been studied by scanning and transmission electron microscopy (Speer et al., 1979). FIGS13-1 5. Hornoxenous isosporan parasites of passerine birds with extra-intestinal stages. FIG.13. Merozoites (+) of Isospora serini in the spleen of a naturally infected canary: Giemsa-stained smear ( x 1OOO). RG.14 Merozoite of I. lmuzei-like parasite within macrophage in spleen of a golden finch, Curduelis curduelis. Electron micrograph ( x 21 OOO). Note micropores (-). FIG. 15. Merozoite of I. lucuzei-like parasite of C. curduelis within macrophage of hepatic sinusoid capillary. Electron micrograph ( x 21 000) HCN = host cell nucleus. (FIG.13. by courtesy of Prof. P. Zwart; FIGS14 and 15 from negatives kindly supplied by Prof. S. Hernandez Rodriguez.)

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Frenkel and Dubey (1972) and Dubey and Frenkel (1972b) fed mature oocysts of Isospora felis and I . rivolta, recovered from the faeces of domestic cats, to laboratory mice and rats. Oral administration of the spleen, liver and lung tissues of these rodents to cats initiated the excretion, one week later, of the corresponding type of oocyst. The authors observed “ensheathed” single or paired, haemogregarine-like organisms in histological preparations of these tissues. Mehlhorn and Markus (1976) carried out electron microscopic studies on these curious tissue stages in mesenteric lymph nodes of mice, 25 days after oral infection with I.felis oocysts. The organisms occurred singly within parasitophorous vacuoles in the host cell, were not surrounded by a true cyst wall and were structurally identifiable as sporozoites. These tissue stages, which were also observed in chickens (Markus, 1977), remained infective to cats for up to 67 days (Frenkel and Dubey, 1972; Markus, 1977) and were identifiable within lymph nodes by light microscopy for up to 15 months (Frenkel, 1974a). Markus proposed the term “dormozoite” for such resting extra-intestinal stages of isosporan coccidia in intermediate hosts. However, Garnham regarded the term as an undesirable etymological hybrid and recommended “hypnozoite” (Markus, 1978a). Latent stages of I. felis and I. rivolta have been demonstrated in the tissues of calves, 26 to 115 days after oral inoculation with mature oocysts, by infecting cats (Fayer and Frenkel, 1979). Wolters et al. (1980) also reported latent stages of I. felis in cattle. Asexual development, by endodyogeny and possibly endopolygeny, of I. rivoltu and I. felis was observed in feline, canine and bovine kidney cells, as well as in a variety of human cells (Fayer, 1972a; Fayer and Thompson, 1974). Endodyogeny has also been observed as the predominant method of asexual multiplication of I. felis in epithelial cells of the small intestine of the cat by Ferguson et al. (1980c), who also carried out ultrastructural observations on the micro- and macrogametogenesis of I. felis in the epithelial cells of the small intestine, eight to nine days after experimental infection of SPF cats (Ferguson et al., 1980a, b). The number of excreted I. felis or I . rivolta oocysts, and the prepatency and patency of infection in cats infected via the intermediary of mice, were comparable to those in cats infected directly by oocysts, except that the prepatent period of I. felis was shortened by an average of 2.2 days, following infection via mice (Dubey and Streitel, 1976~). Fahmy et ul. (1976) reported a 100% rate of infection with I . felis amongst 55 stray cats in Assiut, Egypt. The presence of infection in 4-day-old kittens suggested to the authors congenital transmission. Dubey (1977a) concluded that transplacental transmission of I. felis or I. rivolta was unlikely. However, as in his experiment the queens were mated only nine days after the end of patency of oocyst shedding, congenital infection during the acute intestinal phase of coccidiosis cannot be ruled out. A new species of Isospora, I. frenkeli, has recently been named from the domestic cat in Costa Rica (Arcay de Peraza, 1976). The parasite underwent development in the intestinal epithelium of immunosuppressed mice and its

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FIG. 16. Stages in the sporulation of oocysts (24 x 21 pm), presumably of Isosporu ohioensis, recovered from the faeces of a naturally infected dog. Fresh preparation.

FIG.17. In vitro development of IsosporafrenkeZi Arcay de Peraza, 1976 of the cat in chorioallantoic membrane of chick embryo ( x 1000).(a) schizont; (b) macrogamete; (c) zygote (all arrowed). (By courtesy of Prof. L. Arcay de Peraza.)

sporozoites successfully infected the chorioallantoic membrane of chick embryos (Fig. 17). Oocysts of I.felis and I. rivolta, recovered from naturally infected cats and allowed to sporulate, failed to induce infection in dogs following direct oral inoculation ; feeding tissues of mice previously orally inoculated with oocysts also failed to transfer the infection to dogs (Guterbock and Levine, 1977). Dubey (1975d) established the separate specific identities of feline and canine I. rivolta, retaining the designation I . rivolta for the feline parasite and assigning the new specific name I. ohioensis to the parasite in the dog (Fig. 16). While gametogonic development of these two species could not be initiated in the heterologous host by oral introduction of the oocyst, the oocysts successfully excysted in the heterologous hosts ; the released sporozoites remained viable in feline or canine extra-intestinal tissues and could initiate gametogonic development and shedding of oocysts when fed to the homo-

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logous host. The life cycle of I. ohioensis was studied in detail in experimentally infected dogs by Dubey (1978b). Feeding mesenteric lymph nodes and spleen homogenate of mice, orally inoculated 17 days previously with I. ohioensis oocysts, induced gametogony in the intestinal tissues of young puppies. The prepatent period before oocyst excretion was 24 hours shorter in dogs infected via mice, compared to those fed oocysts. In later experiments Dubey and Mehlhorn (1978) reported that dogs fed homogenates of mouse brain, cardiac or skeletal muscles shed oocysts with a prepatency of nine to 15 days, as compared to only four days in dogs fed mouse spleen or lymph node homogenate. They concluded, however, that oocyst excretion, following ingestion of non-lymphoid tissue, was due to spontaneous infection in puppies acquired from infected litter mates. Mouse tissues other than intestine became infective to dogs one day after oral infection of the mice with oocysts, and remained infective for up to 21 1 days. Sporozoites were identified under the light microscope in lymph node cells for up to 374 days after infection. The fine structure of hypnozoites of I. ohioensis in mesenteric lymph nodes of mice (Dubey and Mehlhorn, 1978) was practically identical to that of I. felis (Mehlhorn and Markus, 1976). The sporozoites increased in size with time, but did not multiply in number during this dormant phase. Following observations on a fatal case of coccidiosis in a puppy, with diarrhoea, dehydration and weight loss accompanied by histiocytic infiltration of the lamina propria and multifocal cryptitis, close to schizonts and gamonts of a coccidian resembling I. ohioensis (Dubey et al., 1978b), Dubey 1978c) studied the pathology of I. ohioensis infection in dogs. He reported diarrhoea in five out of 18 newly born pups, but no pathological symptom in weaned puppies. Necrosis and desquamation of the tips of the ileal villi were observed in suckling pups, 96 hours after experimental infection with I. ohioensis. The extra-intestinal stages of I. ohioensis as well as I. canis of dogs in tissues of experimentally infected mice have also been studied by Markus (1977). Dubey (1975~)demonstrated that cats and mice, orally inoculated with I. canis oocysts, developed tissue stages which initiated the enteric cycle of development when ingested by susceptible dogs. Limited asexual development of I. canis was obtained by Fayer and Mahrt (1972) in cultured canine intestinal and bovine kidney and tracheal cells. Jensen and Edgar (1978) observed penetration of I. canis sporozoites into cultured embryonic bovine tracheal cells. Electron microscopy revealed indentation of the intact cell plasmalemma, and incorporation of the sporozoite within a parasitophorous vacuole. The rhoptries and micronemes, which seemed to be part of the same network of tubes, appeared to empty during the penetration process. Ultrastructural studies on the entero-epithelial stages of I. canis were carried out by Hilali et al. (1979). A coccidian parasite of dogs, resembling I. rivolta, was investigated by Mahrt (1967), and was compared with I. ohioensis (Dubey and Mahrt, 1978). On the basis of differences in the site of development and in morphology of

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the endogenous stages, it was assigned the new specific name I. neorivolta. In 1978, Trayser and Todd described and named yet another species of canine Isospora, I. burrowsi, which differs from I. ohioensis and I. neorivolta in the size of the oocyst and details of the endogenous development. Bledsoe (1976) succeeded in transmitting I. vulpina from silver foxes to dogs. Evidence for resting intermediate stages of this species in rodents was obtained by the same author when the tissues of mice, orally inoculated with oocysts of I. vulpina, were fed to dogs and foxes and induced oocyst excretion (Levine, personal communication). In 1973, Heydorn reported the shedding of unsporulated isosporan oocysts by 12 out of 15 dogs fed bovine oesophageal muscle. These oocysts corresponded to the so-called small form of I. bigemina of dogs (Wenyon, 1926) and were morphologically indistinguishable from feline toxoplasmic oocysts. It has been experimentally established that this parasite was not I . gondii (Heydorn, 1973, 1974; Heydorn et al., 1975a; ZukoviC et al., 1973). Tadros and Laarman (1976) excysted oocysts of the parasite in bovine bile-trypsin solution after pretreatment with carbon dioxide. Using freed sporozoites as antigen, we demonstrated no cross reaction with I. gondii by immunofluorescence even at a 1 in 20 serum dilution (unpublished observations). Heydorn (1973) did not succeed in infecting dogs by feeding them sporulated oocysts, even after treatment with immunosuppressive agents. However, dogs fed the muscle tissue of dogs, sheep or cattle, orally inoculated six to eight weeks previously with canine oocysts, became infected and shed oocysts. The schizogonic and gametogonic developmental cycles of the parasite in intestinal epithelial cells of experimentally infected puppies have been described by Heydorn (1974) and Heydorn et al. (1975a). We found this parasite in naturally infected dogs in the Netherlands, named it I. heydorni and completed its life cycle by feeding muscles of dogs, previously orally inoculated with canine faecal oocysts, to uninfected dogs (Tadros and Laarman, 1976). We also reported a single direct transmission from dog to dog by oral inoculation of I. heydorni-like oocysts, isolated from a naturally infected dog, and suggested that more than one species with morphologically indistinguishable oocysts may parasitize dogs, or that I. heydorni may resemble I. gondii, oocyst transmission of which, from cat to cat, is known to be inconsistently successful. Repeated attempts to identify the infective tissue stages in smears or histological sections of mesenteric lymph nodes, liver, spleen and muscles of dogs, orally inoculated with oocysts, failed (unpublished observations). Dubey and Fayer (1976) studied the developmental cycle of I. heydorni in dogs. Sporulated oocysts from naturally infected dogs in the U.S.A. were not infective to cattle, cats or mice ; following ingestion of naturally infected cattle diaphragm and heart, however, dogs occasionally shed oocysts morphologically identical to I. heydorni. The parasite was not transmissible from dog to dog by oocyst ingestion. However, the gametogonic cycle was successfully completed in the intestines of dogs fed flesh of other dogs, previously orally inoculated with oocysts. Excretion of oocysts resembling those of I . heydorni by a dog ten days after oral infection with oesophageal

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muscle from a buffalo in Malaysia was reported by Dissanaike and Kan (1977). More recently, moose and goats have been shown to act as suitable intermediate hosts for I. heydorni (Dubey and Williams, 1980). In our opinion, the unsporulated isosporan oocysts shed by foxes following ingestion of ovine flesh (Ashford, 1977), by dogs after eating roe deer flesh (Entzeroth et al., 1978) and by dogs fed buffalo diaphragm muscle (Gill et al., 1978) were oocysts of I . heydorni and not Hammondia, as assumed by some authors. Zsospora arctopitheci, originally described from a short-tusked marmoset (Rodhain, 1933), was reported in a capuchin monkey and marmosets from Panama (Hendricks, 1974). The formation of resting intermediate stages by this species in widely different hosts was demonstrated when tissues from mice and newly hatched chicks, fed 21 to 40 days previously with mature I. urctopitheci oocysts, were fed to marmosets, which then excreted oocysts (Henricks and Walton, 1974). The significance of carnivorism, with rodents and birds as important reservoir hosts, was discussed in connection with the arboreal habit of the primate hosts. The parasite has since been found to induce oocyst excretion in a remarkably wide range of host animals, comprising 12 species belonging to six genera of New World nonhuman primates, six genera of carnivores and one marsupial species (Hendricks, 1977). Another Isospora of primates, I . belli, isolated from human faeces, has been transmitted to a chimpanzee (Laarman and Tadros, 1980b). At least two different mechanisms of excystation are known to occur in oocysts of the genus Isospora. In species with a stieda body, sporozoites escape from the sporocyst in a manner analogous to that of many Eimeria species, whereas the sporozoites of several other species, lacking a stieda body, are released following the collapse of the sporocystic wall into a number of plates. The latter mode of excystation has been observed in sporocysts of I. canis (Speer et ul., 1973), I . endocallirnici (Speer et al., 1976), I. heydorni (Tadros and Laarman, unpublished observations), I. gondii (Christie et al., 1978), I. arctopitheci (Duszynski and Speer, 1976) and several species of Sarcocystis. This mode of excystation was discussed in detail by Box et al. (1980), who advocated the mechanism of excystation as an important criterion for determining taxonomic relationships amongst the coccidia.

VI.

SARCOSPORIDIOSIS A N D

SarCOCyStiS-INDUCED

COCCIDIOSIS

A . GENERAL ASPECTS

The elucidation of the life cycle of Sarcocystis has stimulated intensive studies on the natural rate of incidence of sarcosporidiosis in domesticated and wild animals, in all five continents. Of these numerous recent surveys, mention may be made of investigations on the occurrence of sarcosporidiosis in Norway, in reindeer (Poppe, 1977) and in domestic pigs (Greve, 1974);

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the Netherlands, in cattle (Tadros et al., 1975a), in pigs and wild boar (Tadros and Laarman 1976),and sheep (De Kruijf and Bibo, 1976); Germany, in cattle (Laupheimer, 1978; Drost and Brackmann, 1978), pigs (Mannewitz, 1978; Heydorn et al., 1978), wild swine and roe deer (Erber, 1978; Erber et al., 1978b), red, fallow and roe deer (Drost and Graubmann, 1975; Drost, 1977 a, b), sheep (Boch et al., 1979), and zoo-maintained vertebrates (Ippen et al., 1974; Henne et al., 1977); Switzerland, in chamois (Burgher, 1975); Sardinia, in sheep, cattle, pigs, donkeys and horses (Arru and Cosseddu 1976); Austria, in cattle (Hinaidy et al., 1979; Kepka and Osterreicher, 1979), in pigs (Hinaidy and Supperer, 1979); Czechoslovakia, in red, Virginian, sika, fallow and roe deer, as well as in moufflon and chamois (Blaiek et al., 1976, 1978a), and in small mammals (Sebek, 1975); Hungary, in roe, red and fallow deer, wild boar and moufflon (Kavai and Sugar, 1976); Bulgaria, in roe deer, wild boar, hares, rats and long-tailed field mice (Meshkov, 1978a), and in sheep (Meshkov, 1973; Meshkov and Kotomindov, 1976); Turkey, in sheep (Goksu, 1975); Jordan, in sheep, cattle, goats, camels, horses and chickens (Sherkov et al., 1977); the U.S.S.R., in cattle (Gadaev, 1976a; Kislyakova, 1976), in cattle, sheep and pigs (Vel’yaminov, 1976; Gadaev and Abidzhanov, 1978), in pigs (Balutsa 1975; Bogush, 1976, 1978), in goats (Gadaev, 1976b), and in ducks, chickens, geese and turkeys (Golubkov, 1979); Morocco, in cattle and sheep (Fassi-Fehri et al., 1978); the Central African Republic, in African buffalo (Perrotin et al., 1978); in Tanzania, in large herbivores in the Serengeti National Park (Sachs, 1977); in East African game animals (Kaliner, 1975); Sri Lanka, in cattle and goats (Seneviratna et al., 1975a); Malaysia, in feral rodents (Lai, 1977; Sinniah, 1979); Japan, in cattle (Fujino et al., 1979); Fiji, in cattle and pigs (Raju and Munro, 1978); Australia, in sheep, cattle and pigs (Munday, 1975),in sheep (McMahon, 1978), in Australian wild mammals, birds, reptiles, amphibians and fish (Munday et al., 1978, 1979); New Zealand, in pigs, domestic goats, red deer, European rabbits, possums, red-necked walIaby, rats and mice (Collins and Charleston, 1979b); the USA, in pigs (Dubey, 1979b), in sheep and white-tailed deer (Prestwood et al., 1976), in free-ranging mule and white-tailed deer, elk and bison (Pond and Speer, 1979), in cattle, pigs, and sheep (Seneviratna et al., 1975b), in ducks (Hoppe, 1976; Broderson et al., 1977), and in brown-headed cowbirds (Box and Duszynski, 1977); Canada, in different species of wild birds (Drouin and Mahrt, 1979); El Salvador, in cattle (Rice and Calderon, 1979); Venezuela, in cattle (Godoy et al., 1977); and Brazil, in pigs (Schenk et al., 1977). The natural incidence of Sarcocystis-induced coccidiosis amongst carnivores has also received some attention over the past few years. The prevalence of Sarcocystis or Sarcocystis-like endosporulating oocysts or sporocysts has been investigated in dogs, foxes and cats, in Sardinia (Arru et al., 1976); dogs, in Germany (Bohm, 1979; Boch et al., 1979); dogs and foxes, in the U.K. (Farmer et al., 1978); dogs, in Yugoslavia (SibaliC et al., 1977); red foxes and wolves, in Bulgaria (Golemansky, 1975) and in jackals (Meshkov, 1978b); in cats, dogs and coyotes, in the USA (Christie et al., 1976; Streitel and Dubey, 1976; Dubey et al., 1978a); and dasyurid marsupials, feral cats

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owls, falcons and elapid snakes, in Australia (Munday et al., 1978, 1979). Reviews on the life cycles of Sarcocystis species of domestic herbivores include those by Markus ef al. (1974), Suteu (1975), Dubey (1976b), Levine (1977a), Perrotin and Graber (1977), Markus (1978b) and Rommel et a/. (1979). The biology, life cycles and taxonomy of Surcocystis and related tissue cyst-forming coccidians have been reviewed by Tadros and Laarman (1976), Tadros (1976b), Beyer (1977), Vershinin (1977), Rommel (1978) and Tadros (1980). The literature on the epidemiology of infection with tissue cystforming and other coccidia has been surveyed by Tadros and Laarman (1977~)and Fayer (1980). Papers on the ultrastructural morphology of Sarcocystis have recently been reviewed by Mehlhorn and Heydorn (1978a). Comparative studies have been made on the ultrastructure of cyst walls of different Sarcocystis species by Bergmann and Kinder (I 975a, b), Tadros et al. (1975a), Mehlhorn et al. (1976), Tadros and Laarman (1978d) and Laarman and Tadros (1980a). Of the 93 named species of Sarcocystis (for an up-to-date check list, see Levine and Tadros, 1980), the life cycles of at least 30 species have been elucidated. Although only a few of these cycles have been intensively studied, the fact that the amassed data encompass muscular sarcosporidiosis in intermediate hosts ranging in variety from birds to cattle, with reptiles, birds of prey and a motley of carnivorous mammals serving as definitive hosts for the various Sarcocystis species, permits the emergence of a general life cycle pattern. Coccidians, belonging to the genus Sarcocystis, have an obligatorily heteroxenous life cycle, with gametogony and sporogony taking place in the intestinal tissues of suitable definitive host(s) and asexual proliferation by schizogony in the internal organs and, at a later stage, by endodyogeny within the sarcocyst in the muscular tissue of the specific intermediate host. Following ingestion of mature sarcocysts in raw flesh by the specific definitive host, the released cystozoites invade the intestinal tissues and transform directly, without preceding schizogonic development, into male and female gametocytes. Gametogony takes place usually in the sub-epithelial intestinal tissues and the process is generally completed within 18 to 24 hours; however, it may occur, as in reptiles, at a slower rate withn the epithelial intestinal cells. Fertilization of the macrogamonts by the biflagellate microgametes ensues, with the formation of young oocysts. Sporogony and sporulation take place in situ, resulting in the formation of two oval sporocysts, each enclosing four sausage-shaped sporozoites and a coarse residual body, which is compact in newly formed sporocysts, but becomes dispersed in sporocysts shed later during patency. The sporocysts, which lack a stieda body, are enclosed within an oocyst, which lacks a micropyle and has a delicate, colourless wall, which often collapses or ruptures, releasing the sporocysts. Mature oocysts or, more commonly, free sporocysts are shed in the faeces sporadically for a prolonged period of patency, with a prepatent period

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usually exceeding that required for sporogony and sporulation. The mechanism of expulsion of the sporocysts from the lamina propria into the lumen of the intestine is still not fully understood. Ingestion of the viable sporocyst by the specific intermediate host and its subsequent exposure to the specific bile-trypsin stimulus, leads to rupture of the sporocystic wall into four plates along longitudinal suture lines of structural weakness, and the release of the activated sporozoites. The sporozoites presumably invade the intestinal wall and are transported, probably via the blood circulation, to different organs. Schizogony takes place in the vascular endothelium of the liver and other organs or within parenchymal liver cells, depending on the species; up to two consecutive generations of schizonts have been observed, with up to 250 merozoites being produced per schizont. In species which are seriously pathogenic for the intermediate host, the major symptoms appear to be associated with the second generation of schizonts and the penetration of the muscular tissue by the merozoites. The pathological manifestations may be associated with an inflammatory reaction of the host against the foreign antigens, destruction of host cells and/or toxic products of schizogony. The merozoites, released from the last generation of schizonts, are carried presumably via the blood circulation to the musculature, where they finally invade muscle cells, round up, each surrounded by a parasitophorous vacuole, and transform into metrocytes. The single unit membrane boundary of the parasitophorous vacuole soon becomes lined on its inner surface with an interrupted layer of osmiophilic material, to constitute the so-called primary cyst wall of the sarcocyst. This wall becomes invaginated, giving rise eventually to the cyst wall pattern of protrusions characteristic of the mature sarcocysts of a given species (Figs 18-22). The interior of the young cyst and the cores of the cyst wall protrusions become filled with an amorphous granular matrix. The metrocytes multiply by endodyogeny, giving rise to more metrocytes and eventually to the elongate cystozoites, which continue dividing by endodyogeny, resulting in numerous pockets of tightly packed cystozoites and peripherally scattered metrocytes. Remnant strands of the structureless matrix, in the form of the so-called septa, separate groups of cystozoites, constituting a meshwork, along which nutrient materials may well diffuse from the surrounding host tissue into the interior of the cyst, the cyst wall projections vastly augmenting the surface area available for absorption. The rate of growth of the sarcocyst and the maximum size attained may vary with the type of invaded tissue, e.g. muscle versus brain, or cardiac versus skeletal muscle, and the details of the cyst wall pattern may alter with the age of the cyst. However, barring these fluctuations, all three features appear to be hereditary characters, typical of any particular species (Figs 26-32). In our experience, different species of Sarcocystis may exhibit a pronounced predilection for certain muscle sites, e.g. S . cruzi for cardiac muscle and S. hominis and S. hirsuta for lower oesophageal muscle of cattle.

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B. RECENT KNOWLEDGE ON THE DEVELOPMENTAL CYCLES OF

Sarcocystis SPECIES

Due t o the appreciable bulk of data rapidly accumulated during the past five years on various aspects of a growing number of Sarcocystis species which have been derived from widely diverse geographic and hostal origins, the recent findings on sarcosporidiosis and Sarcocystis-induced coccidiosis are here reviewed, grouped for convenience under the identity of the final and intermediate hosts. The specific designations used are in accordance with those of Levine and Tadros (1980). 1. Sarcocystis species undergoing gametogony in primate lzosts

(a) Species with human-bovine cycle. First observed in human subepithelial intestinal tissue by Virchow in 1860, endosporulating disporic tetrazoic oocysts, commonly shed in faeces as free, tetrazoic sporocysts, were designated Isospora hominis by Wenyon in 1923. They have been repeatedly recovered from human stools (Laarman, 1962, 1968; Laarman and Goedbloed, 1968; Manschot et al., 1968; Callot et al., 1971; Doby and Beaucornu, 1972; Plotkowiak and Klasa, 1973; Piotkowiak, 1976). In 1972, Rommel and Heydorn demonstrated that the mature oocysts and sporocysts of the socalled I. hominis constituted the end product of sexual development, in the human intestine, of two separate species of Sarcocystis, parasitizing the musculature of cattle and swine respectively. The sporocysts shed by man following ingestion of the bovine species, Sarcocystis hominis (Fig. 53), are distinguished by their larger size from the porcine species and correspond in dimensions to the sporocysts recovered from the vast majority of previously recorded natural cases of human infection. The ultrastructure of the cyst and cyst contents was studied by Heydorn et al. (1975~).The development of S. hominis in the musculature of experimentally infected calves was studied under the electron microscope by FIGS18-22. Different types of cyst wall in Sarcocystis species; all in fresh preparation ( x 1OOo). FIG. 18. Smooth cyst wall of S. sebeki from the field mouse, Apodemus sylvaticus. FIG.19. Short stubby projections of S.putorii from Microtus arvalis. FIGS20, 21. Conspicuous long regular finger-like protuberances of S. cuniculi from the common European rabbit (FIG.20) and from the monkey Cercopithecus aethiops (FIG.21). FIG. 22. Hair-like processes of S . cruzi from cattle. FIGS23-25. The three types of Sarcocystis parasitizing cattle: fresh preparations of microisolated sarcocysts ( x 1OOO). (a) = part of cyst; (b) = cystozoites. FIG.23. S. cruzi from cardiac bovine muscle. Note numerous very fine, hair-like projections of cyst wall. Species infective to dogs. FIG.24. S. hirsuta sarcocyst most readily seen in the oesophageal and diaphragmal muscle. Note thick, bending finger-like cyst wall projections. Species infective to cats. FIG.25. S. hominis cyst most readily observed in the oesophageal and diaphragmal muscle. Note long, upright cyst wall projections. Species infective to man.

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Mehlhorn et al. (1975a, d), Tadros (1977) and Tadros and Laarman (19770, 1978d) (Figs 26 and 27). The species is distinguishable from the other two bovine species of Sarcocystis in fresh preparations under the light microscope by having long, erect, palisade-like protrusions of the primary cyst wall (Figs 23-25) (Tadros and Laarman, 1976). In 1976, Heydorn and colleagues successfully infected rhesus monkeys and baboons, Papio cynocephalus, with S. hominis. Tadros and Laarman (1977b, d) and Laarman and Tadros (1978) confirmed the identity of S. hominis with the larger sized sporocysts of I. hominis, when they isolated these sporocysts from the stools of a naturally infected child and successfully induced S . hominis sarcocysts in a young calf. A distinct predilection of these sarcocysts for the lower oesophageal muscles and the diaphragm confirmed our previous, repeated observations on the distribution of this species in naturally infected cattle. The parasite was successfully cycled in three human volunteers and two rhesus monkeys. A young chimpanzee was fed 100 micro-isolated S. hominis sarcocysts from the same calf, in banana pulp; it started passing blood-stained watery stools 6 h after infection, and continued doing so for 24 h, but did not shed sporocysts during a period of observation of three weeks (Tadros and Laarman, unpublished observations). However, natural shedding of sporocysts, similar in size to those of S . hominis, has been observed in a pet chimpanzee (Rijpstra, 1967). Few details are available about the gametogonic development of S. hominis in the human final host. Mature oocysts of this species have, however, been repeatedly observed exclusively in the lamina propria of the human small intestine in autopsy material (Laarman, 1962). (b) Species with human-porcine cycle. Detailed studies on the development, in the domestic pig intermediate host, of S . suihominis, the other species infective to man, have been carried out by Heydorn (1977a) and Heydorn and Ipczynski (1978). Piglets, each fed 50 000 to 5000 000 sporocysts shed by experimentally infected human volunteers, became ill 12 days later; they revealed first generation schizonts in the liver six days after infection, and second generation schizonts in most organs between days 14 and 17. The schizonts of both generations were located in the vascular endothelium. In ultrastructural studies of the schizonts, the merozoites were described as being formed simultaneously, using the outer membrane of the mother cell pellicle as their own outer pellicular membrane (Heydorn and Mehlhorn, 1978). The sarcocysts of this species were studied by light and electron microscopy in experimentally infected piglets (Mehlhorn and Heydorn, 1977), and in naturally infected pigs (Tadros and Laarman, 1978d).The mature sarcocysts were characterized by very long, slender, trailing cyst wall projections, tightly compressed against the cyst wall. In the Netherlands, this species is extremely rare in slaughtered pigs and was not observed in over 100 investigated carcasses of wild boars. However, the description of one of the two species recorded by Bergmann and Kinder (1976) in wild swine in Eastern Germany (WI according to their classification) unmistakably represents S. suihominis.

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Experimental infection of human volunteers with the intestinal stages of this species and a description of the associated pathological manifestations were reported by Heydorn (1977b) and Piekarski et al. (1978a). In the Netherlands, where the natural incidence of Sarcocystis-induced human coccidiosis has been intensively investigated since 1962, only large sporocysts, conforming to the size range of S. horninis, have as yet been observed (Laarman, 1964; and Laarman and Tadros, 1978). However, the dimensions of the sporocysts (12.35 x 8-91 pm), recovered from the stools of a 12-year-old Slovakian girl and identified as I. horninis (Giboda and Rakir, 1978), correspond with those of the sporocysts of S. suihorninis; this constitutes, to our knowledge, the first published record of natural human infection with this species. Fayer et al. (1979) succeeded in cycling S. suihorninis in Macaca rnulatta, M. iris, and chimpanzees. All primates shed sporocysts 13 to 15 days after infection for at least 30 days and all remained in good health. Macrogamonts and oocysts were observed in the lamina propria of the small intestine of a rhesus monkey 48 hours after infection. The gametogony of this species has also been studied in cultured human cells (Mehlhorn and Heydorn, 1979).

2. Sarcocystis species undergoing gametogony in Canidae (a) Species with canine-bovine cycle. It has been established that dogs act as final hosts to one of the three species of Sarcocystis known commonly to FIG.26. Light micrograph of S. horninis sarcocyst micro-isolated from muscular tissue of experimentally infected calf. Fresh mount preparation ( X 1OOO). FIG.27. Electron micrograph of longitudinal section through cyst wall projection (WP) of sarcocyst of the same species ( x 8700) showing serrated surface of protrusions () and fibrils (f) within the core of the projections. Note contact of cyst protrusions (WP) with host muscle tissue (MT) and nucleus (HN); GS = granular substance of cyst. FIG. 28. Sarcocystis sp. of the lizard Alabuia multicarinata: (a) fresh mount preparation ( x 150) exhibiting smooth cyst wall outline and conspicuous septa (S); (b) ( x 3400) and (c) ( x 23 800) electron micrographs of the same species. Note granular layer (GL) and a fibrillar Iayer (FL) separating the primary cyst wall (PW) and cyst contents (Cc) from the host muscular fibrils (Mf).Note also irregular outline of the primary wall with invaginations of the unit membrane at osmio-lucid points (+ ). Elongate cystozoites (EC) are embedded in granular substance (GS) of the cyst; N = nucleus, rh = rhoptry of cystozoite. FIGS 29-32. Light and electron micrographs of cyst wall structure of several species of Sarcocystis.

FIG.29. Light micrograph of micro-isolated sarcocyst of S. sebeki. Fresh mount preparation ( x 400). Note slight undulations (+ ) of smooth cyst wall and septa (S). FIG. 30. EIectron micrograph of longitudinal section through cyst wall of same species ( x 34 O00). Note deep invaginations (d ) of the limiting unit membrane (um) coinciding with interruptions in the osmiophilic layer (01) and vesicles (v) within the ground substance (GS); EC denotes elongate cystozoite; Mf = muscle fibre; n = FIG.31. Light micrograph of micro-isolated sarcocyst of S. cuniculi. Fresh mount preparation ( x 1500). Note long slender cyst wall projections (+). FIG.32. Electron micrographs of longitudinal sections through cyst protrusions (WP) of same species; (a) x 7500; (b) x 67 500. Note toothed outline of projections (+ ) and microtubules (mt) which collect into bundles (b) at the bases of projections within the granular substance (GS).

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parasitize the musculature of cattle (Heydorn and Rommel, 1972a; Fayer and Johnson, 1973, 1974; Mahrt, 1973; Suteu and Coman, 1973; Rommel et al., 1974; Gestrich et al., 1975a; Tadros and Laarman, 1976). In addition, coyotes (Fayer and Johnson, 1975), wolves and foxes (Rommel et al., 1974) and raccoons (Fayer et al., 1976a) constituted suitable final hosts for this species; but hyenas or bears (Rommel et al., 1974), cats, monkeys, swine, skunks, ferrets, rats, guinea-pigs or rabbits (Fayer et al., 1976a) did not. Pigs, monkeys, rats, mice, rabbits and lambs could not be infected with the muscular stage (Fayer et al., 1976a). The old designation S. cruzi has been selected for this parasite (Levine, 1977a; Levine and Tadros, 1980). Fayer and Johnson (1 973) detected numerous schizonts in the endothelial cells of blood vessels in the adrenals, bladder, caecum, cerebellum, cerebrum, diaphragm, oesophagus, heart, kidneys, liver, lung, lymph nodes, pancreas, small intestine and spleen, 26 to 33 days after infection with 250000 to 1000 000 sporocysts. Fayer (1977) detected an earlier generation of schizonts in endothelial cells of the arteries of the caecum, large intestine, kidney, pancreas and cerebrum of calves on days 15 and 16, but not on day 17, after oral infection with 200 000 sporocysts of the canine-bovine species. The fine structure of the schizonts of this species was studied by Pacheco and Fayer (1977). The sarcocysts of this species are fusiform in shape and are invested with shaggy, hirsute cyst wall projections, best visible in fresh preparations under oil immersion objectives (Fig. 23a). A striking predilection of this species for bovine cardiac muscle, to the exclusion of the other two bovine species, has been observed in our laboratory in thousands of samples from naturally infected, slaughtered cattle. The morphology of the developmental stages of these sarcocysts was studied by light and electron microscopy, following experimental infection of calves (Heydorn et al., 3975d; Mehlhorn et ul., 1975b, d ; Pacheco et al., 1978). Sporogony of this species was observed by Fayer (1974) and by us (unpublished observations) in the lamina propria of the small intestine of experimentally infected dogs (Fig. 33). Sheffield and Fayer (1978) studied by electron microscopy, the oocyst in the lamina propria of dogs; they saw immature oocysts as early as 24 hours after infection. The developmental cycle of S . cruzi has repeatedly been confirmed in dogs, in our own laboratory, and also in the U.S.S.R. (Vershinin, 1974), Spain (Martinez-Fernandez et al., 1975) and Brazil (Ogassawara et al., 1978), as well as in foxes and wolves in the U.S.S.R. (Gadaev and Abidzhanov, 1977). (b) Species with canine-bubaline cycle. Shah (personal communication) identified dogs as the final host of a species of Sarcocystis with microscopic sarcocysts, which he found in eight out of ten carcasses of water buffalo, Bubalus bubalis, examined from around Jabalpur, in India. In the following year, Dissanaike et al. (1977a, b) recognized two different species of Surcocystis in the water buffalo in Malaysia, both distinct from those in cattle, Bos taurus. One species, with microscopic sarcocysts and finger-like projections from the cyst wall, completed its gametogonic cycle in dogs and

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was designated S. levinei (Dissanaike and Kan, 1978). The ultrastructure of the sarcocysts of this species was studied by Kan and Dissanaike (1978) and its sporogony was studied in canine intestinal tissue by Dissanaike et al. (1 977a) and Chauhan et al. (1977). Gametogony of a Sarcocystis species from buffaloes in the Philippines was reported from dogs by Tongson and Pablo (1979). (c) Species with canine-gazelline cycle. Janitschke et al. (1976) completed gametogonjc development in the domestic dog of a Sarcocystis species of Grant’s gazelle (Gazella granti), shot in Tanzania. (d) Species with canine-ovine cycle. The dog was identified as the definitive host of an ovine species of Sarcocystis with microscopic sarcocysts and finger-like projections from the cyst wall (Ford, 1974, 1975; Munday and Corbould, 1974; Rommel et at., 1974). Free merozoites of this species were detected in the blood, and intact schizonts in the vascular endothelial cells, of experimentally infected lambs. Schizonts were found within the kidney glomeruli, liver and heart, 25 and 29 days after infection (Heydorn and Gestrich, 1976) and in the liver, small intestine, spleen, choroid, lung, kidney, optic nerve and skeletal muscles after 24-29 days (Leek et al., 1977). Munday et al. (1975) described an earlier generation of schizonts, 15 days after infection, and reported the persistence of later generation schizonts for up to 42 days in the brain tissue of experimentally infected lambs. The development of the sarcocysts in ovine musculature was studied, by light and electron microscopy, by Mehlhorn et al. (1975~).Munday et al. (1975) studied intestinal development of this parasite in experimentally infected dogs, 1-1 7 days after infection. Macro- and microgametocytes were discernible 24 hours after infection. Ashford (1977), in the U.K., followed the sporogonic development of what was possibly this species of Sarcocystis, in experimentally infected foxes. We fed two puppies with oesophageal muscle of naturally infected sheep, containing exclusively microscopic sarcocysts with finger-like projections (Fig. 34), and found numerous mature oocysts in the lamina propria of the tips of the villi of the anterior two-thirds of their small intestines 14 days later. (e) Species with canine-caprine life cycle. Collins and Crawford (1978, 1979) reported the shedding of mature sporocysts by dogs fed Sarcocystisinfected flesh from feral goats, Capra hircus, captured at Hawk’s Bay in New Zealand. Collins et al. (1980) described the pathogenic acute phase of infection with schizonts in all organs but particularly in the kidneys, I8 and 19 days after infection with 6 x lo6 sporocysts derived from dogs. Up to 34 x lo6 schizonts were estimated to parasitize the renal glomeruli of a single goat. Sheep were not susceptible to infection with this parasite. Chhabra and Mahajan (1978) found microscopic sarcocysts in the musculature of domestic goats in India, which they cycled in puppies; they erroneously concluded that the parasite was identical to that with microscopic sarcocysts in sheep. FIG.33. Stages in the sporulation of Surcocystis cruzi of cattle in the lamina propria of experimentally infected puppies: (a) 4 days, (b) 5 days, (c) and (d) 10 days after infection. All fresh preparations; (a), (b) and (c) x 1200, (d) x 2500.

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Pethkhar (personal communication) examined 650 domestic goats in India and found exclusively microscopic sarcocysts, of which 97% had “radially striated” cyst walls, while 3 % had hair-like projections. Dogs, but not cats, could be experimentally infected, with a prepatent period before sporocyst-shedding of 9-21 days and a patency of over 40 days. Two goat kids, fed 1000 000 and 50 000 sporocysts respectively, died 21 and 23 days later and schizonts were found in the endothelial cells of the blood vessels of all internal organs. Macrogamonts and oocysts were observed in the intestinal lamina propria of experimentally infected dogs, one to 15 days after infection. A very similar life cycle was described independently in Germany, for a caprine Sarcocystis species, forming microscopic cysts with finger-like cyst wall projections, by Fischer (1 979), who recognized two schizogonic generations in the vascular endothelial cells of goat kids 12 and 19-23 days after experimental infection. Sheep could not be infected with this species, nor were goats susceptible to infection with the microscopic ovine species. The species described by Fischer is probably the same as that studied by Collins and Crawford (1978) a year earlier. The fact that the latter authors described the sarcocysts from New Zealand goats as “thin-walled’’ may be due to their having examined stained sections, in which the cyst wall projections are difficult to discern. A Sarcocystis species was recorded in the ibex, Capra ibex, from the Gran Paradiso National Park, Italy, where dogs are not permitted, but where foxes regularly scavenge (Biocca et al., 1975). The parasite induced sporocyst shedding in dogs, foxes, wolves, but not in a lion, domestic cats or a kestrel. As the sarcocysts had finger-like cyst wall projections and the size range of the sporocysts overlapped that of the forms derived from Capra hircus, both parasites may belong to the same species. Fischer (1979) designated a microscopic type of sarcocyst with finger-like cyst wall projections, completing its cycle in dogs, as a new species S. capracanis. Erber (1980) pointed out that both macroscopic and microscopic species of Sarcocystis of sheep, goat and chamois are difficult to distinguish morphologically. In view of Erber’s successful transmission of the parasite forming microscopic cysts in chamois muscle to a sheep and a goat following cycling in dogs, as well as that of S. tenella from sheep to one out of two goats, it is evident that thorough cross infection experiments need to be carried out before deciding on the specific designation of these parasites. Should the Sarcocystis spp. of goats and chamois be proven to be distinct from those of sheep, as pointed out by Levine and Tadros (1980), the old available names S. moulei and S. orientalis must be used before any new specific designations are coined. (f) Species with canine-cervid cycle. Two species of Sarcocystis, one with short, bulbous cyst wall nodulations, and another with long, erect, thick finger-like protrusions, giving the appearance of a thick cyst wall, have been described from roe deer, Capreolus capreolus, in Germany, by Bergmann and Kinder (1976). Schramlovi and Blaiek (1978) and Blaiek et al. (1978b, c)

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described the same thick-walled species, as well as another with long, fine trailing cyst wall projections in roe deer from Czechoslovakia. The latter species was shown to complete its gametogonic cycle in dogs, but not in cats, with a prepatency of 11 days, resulting in the shedding of sporocysts 15.3 x 10-0pm (Blaiek et al., 1978~). Erber et al. (1978b) described all three species in roe deer from Bavaria. They reported completing the cycles of the species with long, fine cyst wall projections (designated by the authors S. capreolicanis sp. n.) and that of the species with the short, thick cyst wall projections, referred to as S. gracilis in dogs and foxes. (S. gracilis was named by Rhtz (1909) from roe deer and not, as erroneously deduced by Levine and Tadros (1980), from red deer.) Both species developed in fawns but have not been separated in the intermediate host. Entzeroth et al. (1978) fed roe deer flesh infected with Sarcocystis to a cat, a fox and a dog and reported shedding of sporocysts (14.5 x 8-4 pm) by the fox after a prepatent period of eight days, and (15.6 x 10.0 pm) by the dog after ten to 14 days. The cycle(s) was (were) not confirmed by infecting roe deer. Entzeroth (1980) carried out electron microscopic studies on the gametogonic development of these species in the intestinal tissues of dogs. As pointed out by Levine and Tadros (1980), in designating the new species S. capreolicanis, Erber et al. (1 978b) have ignored two existing specific names: S. capreoli Levchenko, 1963 and S. sibirica Machul'skii, 1947, both described from C . cctpreolus. Coyotes, Canis latrans, and domestic dogs have been shown to act as suitable definitive hosts for a species of Sarcocystis of mule deer, Odocoileus hemionus, in the U.S.A. (Hudkins-Vivion et al., 1976). The species, named S. hemionilatrantis by Hudkins and Kistner (1977), is not infective to cattle or sheep. During the seriously pathogenic acute phase, 27 to 39 days after infection, schizonts were described within macrophages, between muscle fibres and close to blood vessels in the oesophagous, heart, tongue, diaphragm and skeletal muscles. Canis familiaris was pinpointed as the definitive host of a Sarcocystis species of yet another cervid ungulate, namely the red deer Cervus elaphus, by Navarrete et al. (1978) in Spain. The sarcocysts measured 150-200 pm and had a smooth cyst wall, 0.5 pm thick, and induced the shedding of sporocysts ( 1 6 ~ 1 0 . 9pm) by dogs, but not human beings or cats, with a prepatent period of 11-12 days (Hernandez Rodriguez et al., in press). In the same publication, the authors assign a new specific name for this parasite. Margolin and Jolley (1979) reported infecting dogs with microscopic sarcocysts from a naturally infected wapiti, C. elaphus (syn. C. canadensis) from Wyoming, U.S.A., and recovering sporocysts measuring 16.5 x 11.1 pm. This species may well be the same as that described from red deer in Spain.

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(g) Species with canine-porcine cycle. Rommel and Heydorn (1972) demonstrated that the dog also acts as a definitive host for a species of Sarcocystis in domestic pigs (Sus scrofa dornestica). Tadros and Laarman (1976, 1977e) found that pigs slaughtered in the Netherlands were practically free from infection with Sarcocystis; however they recorded a 100% rate of infection with a sarcocyst, macroscopic when mature and having erect, finger-like cyst wall projections, in wild Sus scrofa ferus, ranging in age from yearlings or younger to 5-year-old adults. The parasite was infective to dogs and foxes, but not to chimpanzees, rhesus monkeys or cats. Following successful cycling in domestic piglets, this parasite was assigned the old specific name S. miescheriana. An identical parasite was described from wild swine in Western Germany and cycled in dogs, foxes and wolves (Erber and Boch, 1976). Morphological comparison by light and electron microscopy of the cyst wail of the canine and human species of porcine Sarcocystis was undertaken by Tadros and Laarman (1976; 19770; 1978d), Erber (1977), Gobel et al. (1978a) and Katz (1978). The schizogonic phase of this species and its pathological manifestations were studied in experimentally infected piglets by Erber and Geisel (1979). (h) Species with canine-equine cycle. The domestic dog was found to be a suitable h a 1 host for a Sarcocystis species of horses in Germany, with cysts measuring up to 350 pm and with a thin cyst wall. The parasite was named S. equicanis by Rommel and Geisel (1975). Martinez Fernandez et al. (1977) described cycling an equine species from Spain in wolves. A different species of Sarcocystis, with cysts measuring up to 900 pm and finger-like cyst wall projections, was recorded in horses, slaughtered in the U.S.A. The parasite was reported to be infective to dogs and given the new specific name S. fayeri by Dubey et al. (1977~).As pointed out by Tadros and Laarman (1976) and Levine and Tadros (1980), the old specific name S. bertrami Doflein, 1901 is available and, according to the law of priority, must be assigned to an appropriate equine species. Studies on the fine structure of S . equicanis (Gobel, 1976; Gobel and Rommel, 1980) have confirmed the absence of cyst wall projections in this species. However, the large sarcocyst of S. fayeri, with prominent cyst wall projections as described from light microscopy by Dubey et al. (1977~)and confirmed since by electron microscopy (Tinling et ai., 1980), adequately fits Doflein’s original description. Thus S.fayeri is a junior synonym of S. bertrami. The finding of S. bertrami in the U.S.A. is not surprising in view of the relatively recent introduction of Eguus caballus into the New World. (i) Species with canine-rodent cycle. A new species of Sarcocystis from the suslik, Citellus fulvus, was shown to undergo gametogony and sporogony in the intestines of the foxes Vulpus vulpus and V . corsac, and named S. citellivulpes (Pak et al., 1979). (j) Speciespossibly with canine-avian cycle. Munday et al. (1977) fed muscles of domestic chickens, suffering from lameness and myositis due to a heavy infection with Sarcocystis species (possibly S. horvathi), to a domestic dog and

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observed the shedding of a few mature sporocysts seven days later. The parasite could, however, not be recycled in chickens. Golubkov (1979) recorded sarcocysts in the domestic chicken in the U.S.S.R. and claimed completion of the cycle in dogs and cats; this, if verified, would indicate the involvement of at least two species. The same author, in the same paper claimed transmitting a Sarcocystis species of the domestic duck to Canis familiaris. Sarcosporidiosis of poultry has been reviewed by Springer (1978). 2. Sarcocystis species undergoing gametogony in Felidae (a) Species withfeline-bovine cycle. Heydorn and Rommel(l972a, b) established the domestic cat as the definitive host of a species of Sarcocystis of cattle, with macroscopic sarcocysts and thick, bending finger-like cyst wall projections (Fig. 24). In our experience, this species of Sarcocystis, assigned the old specific name S. hirsuta (Levine, 1977a; Levine and Tadros, 1980), has a 100% rate of infection in cattle slaughtered in the Netherlands; it does not occur in cardiac muscle of naturally infected cattle but exhibits a distinct predilection for the muscles of the lower oesophagus. The fine structure of the sarcocysts of this species, shown not to be pathogenic by Gestrich et al. (1975a), was investigated in experimentally infected calves 98 and 106 days after infection (Gestrich et al., 1975b; Mehlhorn et al., 1975d). Heydorn and Rommel (1972a, b) described the development of macrogamonts and sporogony of this species in the lamina propria of the small intestine of kittens, killed 4, 6 and 8 h and 1, 2, 3, 4, and 5 days after infection. (b) Species with feline-bubaline cycle. In revising the nomenclature of the Sarcosporidia, Tadros and Laarman (1976) drew attention to the fact that the specific designation S.fusiformis, which had been applied indiscriminately by numerous authors to Sarcocystis spp. of cattle, had originally been described and named by Railliet in 1897 from the water buffalo (Bubalus bubalis). Dissanaike et al. (1977a) and Tongson and Pablo (1979) reported successful cycling in cats of S. fusiformis from water buffaloes in Malaysia and the Philippines respectively. The fine structure of macroscopic sarcocysts with cauliflower-like cyst wall foldings was described from B. bubalis in Malaysia by Kan and Dissanaike (1978) and from Egypt by Ghaffar et al. (1978). The sporogonic stages in feline intestinal tissues were observed by Dissanaike et al. (1977b). Scholtyseck and Hilali (1978) described the fine structure of micro- and macrogamonts of S.fusiformis, from Egyptian water buffaloes, in the intestinal tissues of experimentally infected cats. However, as the cats were sacrificed as late as 13 to 14 days after infection and, as in our own and other workers' experience, gametogonic development of Sarcocystis, in vivo and in vitro, is completed within 18 to 24 h, accidental infection of these experimental cats with another coccidian is probable. (c) Species withfeline-gazelline cycle. One of the two species of Sarcocystis parasitizing Grant's gazelles in Tanzania was found to induce excretion of mature sporocysts in orally inoculated cats (Janitschke et al., 1976).

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(d) Species with feline-ovine cycle. Rommel et al. (1972, 1974) demonstrated that the domestic cat is the final host of the macroscopically visible sarcocysts (Figs 35-37), which so regularly parasitize the oesophageal musculature of adult sheep, and for which the specific name S. gigantea Railliet, 1886 has been resurrected by Ashford (1977). Feeding microisolated sarcocysts of this species led to the excretion of mature sporocysts by all 16 experimentally infected cats, but by none of ten dogs. Re-infection occurred in all challenged cats (Rommel et al., 1974). We observed numerous fully sporulated oocysts in the lamina propria of a kitten killed 13 days after being fed with 50 micro-isolated S. gigantea sarcocysts from naturally infected sheep (unpublished observations). This species was one of the very first to have the fine structure of its cyst wall and cyst contents investigated, because of the large conspicuous size of the sarcocysts and their availability (Ludvik, 1956; Mehlhorn and Scholtyseck, 1973; Scholtyseck et al., 1974; Mehlhorn et al., 1975e). Strikingly beautiful and remarkably detailed electron micrographs of the cystozoites, following negative staining, were published by Porchet-HennerC (1975), who established the presence of only a single pair of rhoptries, and discrete sarconemes shaped like rice grains. The cyst surface, the septa and the intimate arrangement of the cystozoites within the compartments were brilliantly demonstrated by scanning electron microscopy by PorchetHeme& and Ponchel (1974), and Porchet and Torpjer (1977) applied to advantage the technique of freeze-fracturing. The fine structure of the oocysts and sporocysts has been described by Mehlhorn and Scholtyseck (1974). In addition to conspicuous sarcocysts in the oesophageal muscle, Collins et al. (1976) detected two other morphological types of macrocysts, differing from each other in length/width ratio, in the skeletal muscle of sheep; they suggested that two or even three species may be involved. Collins et al. (1979) found that all three types of sarcocysts were infective to cats, resulting in the shedding of morphologically identical sporocysts. Differences were, however, observed in the fine structural details of the cyst walls of the two types of sarcocysts from ovine skeletal musculature. Although these results remain to be confirmed by the separation of the two forms in intermediate and final hosts, supportive evidence for this claim has been supplied by the finding of distinct mobilities of the enzymes phosphoglucomutase and 6-phosphogluconate-dehydrogenase by thin-layer starch electrophoresis

FIGS34-37. Ovine species of Sarcocystis; fresh preparations. FIG.34. S. tenella cyst in muscle of a naturally infected sheep ( x 1OOO). Note conspicuous cyst wall projections ( +) and septa (S). FIG. 35. Micro-isolated S. gigantea cyst. Note inconspicuous irregular cyst wall outline (+) and fibrillar layer ())) intimately investing the sarcocyst ( x 1OOO). FIG.36. Conspicuous septa ( S ) and characteristic arrangement of cystozoites of S. gigantea within sarcocyst compartments ( x 2000). FIG.37. Cystozoites of S. giganfeu ( X 2000). Note crescentic shape.

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(Atkinson and Collins, in press). The name S. medusiformis has been suggested for the smaller macrocyst of sheep by Collins et al. (1979). (e) Species withfeline-porcine cycle. Golubkov et al. (1974) in the U.S.S.R. -not Dubey (1976b), as sometimes erroneously assumed, or “Golubkovan and Kislyakova” as is repeatedly misquoted-reported completing the cycle of a porcine species of Sarcocystis in domestic cats. Coccidia-free kittens, fed porcine oesophageal muscle massively infected with sarcocysts, started shedding sporocysts (measuring 13.5 x 7.6 pm) after a prepatent period of eight days and continued for 10 to 15 days. These sporocysts were administered orally to eight piglets on nine consecutive days. The authors did not study the acute phase of infection, but reported pathological symptoms starting three to seven days after infection and lasting for two weeks. At autopsy 89 to 107 days after infection the piglets, some of which had exhibited paralysis of the hind legs, revealed intense muscular sarcosporidiosis with macroscopically visible sarcocysts in the thigh and diaphragmal muscles. This parasite, which has not yet been reported in Western Europe or the U.S.A.,has been named S.porcifelis by Dubey (1976b). (f) Species with feline-lagomorph cycle. Macroscopic sarcocysts (Figs 20, 57, 58), with cyst wall projections up to I1 pm in length, were described by Tadros and Laarman (1977a, f) in the skeletal muscles of common European rabbits, shot in the Netherlands. This parasite, identified as S. cuniculi Brumpt, 1913, completed its gametogonic development in cats, but not in dogs, foxes, weasels or kestrels. Shedding of sporocysts started 10 days after infection and lasted for up to 105 days, the peak of excretion occurring unusudly late (40-55 days) (Tadros and Laarman, 1978a). Male and female gametocytes were detected in goblet cells and the subepithelial lamina propria of the small intestine of young kittens, 9 to 12 h after infection. The parasite was cycled in cats and rabbits (Tadros and Laarman, 1979b). The fine structure of the cyst wall was described by Tadros (1977) and Tadros and Laarman (1978d) (Figs 31, 32), and the early gametogonic development was studied in feline fibroblast cell lines (Tadros and Laarman, 1979c, 1980b) (Figs 59-61). A scanty number of macroscopic sarcocysts with thin cyst walls, devoid of cyst wall projections and with cystozoites 8-9 pm long, were occasionally encountered in naturally infected wild rabbits. The final host of this species, which is clearly distinct from S. cuniculi, is as yet unknown, but the morphology of the sarcocysts and the small size and slender shape of the cystozoites, suggest it is likely to be a bird of prey, e.g. buzzards. Crum and Prestwood (1977) detected macroscopic sarcocysts in the muscle of a cottontail rabbit, Sylvilagus Jloridanus, from Virginia. Feeding infected muscle to two domestic cats resulted in the excretion of mature sporocysts, 13.2 x 9.7 pm, 14 days after infection. Only scanty sporocysts were shed (an average of five per gram of faeces), until autopsy on day 73, when intestinal stages were not detected. In an addendum to this paper, the authors mentioned that they fed more heavily infected rabbit muscle to a raccoon, which shed sporocysts (12.8 x9.1 pm) after a prepatent period of 14 days. It is likely that

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two species of Sarcocystis are involved. Macroscopic and microscopic sarcocysts have been observed in cottontail rabbits by Crawley (1914), who attributed the differences in size to the age of the sarcocysts. Fayer and Kradel (1977) reported the shedding of sporocysts (13.6 x 9.4 pm) by 18 cats, but none of eight dogs, fed flesh of cottontail rabbits infected with Sarcocystis. The oral administration of 200-75 000 sporocysts to laboratory rabbits, Oryctolagus cuniculus, failed to induce muscular sarcosporidiosis. The authors of both papers referred the parasite of Syl. floridanus to Sarcocystis leporum. (g) Species withfeline-rodent cycle. Macroscopic sarcocysts were observed in the skeletal muscles of a house mouse by Miescher as early as 1843. The old specific designation S. muris for this parasite was erroneously attributed to Blanchard (1885) until Ashford (197%) discovered that it was Railliet (1886) who had named the species. Frenkel (1974) cited independent reports by Azab, in Egypt, and Ruiz, in Costa Rica, of the cat as the final host of S. muris of the house mouse. Ruiz and Frenkel(l976) found that the cystozoites of this species underwent gametogony in the goblet cells of the small intestine of the cat, 9-24 h after infection. Mature sporocysts were shed by cats for up to 80 days. Oral inoculation of laboratory mice resulted in asexual proliferation of the parasite by schizogony, 11 to 17 days later in the parenchymal cells of the liver, followed by invasion of muscular tissue and development of sarcocysts, which attained infectivity for cats only 76 days after infection. Cats and mice could be reinfected but S. muris was not infective to rats, hamsters or guinea pigs. The fine structure of the sarcocyst was studied by Sheffield et al. (1977). Rifaat et al. (1978a, b) described schizonts of an Egyptian isolate of S. muris in the spleen, liver and pancreas of mice, 13 to 21 days after infection. At least one other species of Sarcocystis has Mus musculus and Felis catus as intermediate and final hosts respectively, namely the parasite described by Wallace (1973, 1975) with microscopic, smooth-walled sarcocysts in the musculature of mice, fed with faeces from a stray cat in Hawaii. Yet another species parasitizing M . musculus but with an as yet unidentified final host was described by Cosgrove (quoted by Ruiz and Frenkel, 1976) as forming microscopic sarcocysts, with prominent radial spiny cyst wall projections, in the musculature of a laboratory mouse. Ashford (1978a) found a species of Sarcocystis with macroscopic, smooth walled sarcocysts in Rattus norvegicus, captured in Wales, U.K. The gametogonic cycle of this parasite, which was designated S. cymruensis, could be completed in domestic cats, but not in dogs or ferrets. As the number of sporocysts shed by cats was scanty, the author concluded that another carnivore probably serves as a more natural definitive host. Ashford (1978a) failed to infect mice with this species. However, Atkinson (1978) reported successful transmission of apparently the same species to laboratory mice. (h) Species with feline-avian cycle. Golubkov (1979) in the U.S.S.R. claimed completion of the gametogonic cycles of Sarcocystis from the domestic chicken and ducks in the cat.

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4. Sarcocystis species undergoing gametogony in mustelids Sporocysts, measuring 10-5-124 x 7.5-9.6 pm, were recovered from the faeces of five out of six common European weasels, Mustela nivalis, trapped live in the Netherlands and induced muscular sarcosporidiosis in the voles Microtus arvalis and M . agrestis, but not in Clethrionomys glareolus. Two generations of schizonts were detected in the lymph nodes, spleen, and particularly the liver parenchymal cells, 12 and 37 days after infection, when the youngest sarcocysts were seen in muscle (Tadros and Laarman, 1975a). The mature macroscopic sarcocysts (Fig. 19) exhibited conspicuous cyst wall projections with enclosed fibrils. They were identical, under the light and electron microscopes (Tadros and Laarman, 19770, 1978d), to a species previously described from naturally infected M . agrestis in the U.K. (Tadros, 1970a). Earlier attempts at the transmission of this parasite k o m vole to vole by oral or intraperitoneal inoculation, or at recycling through cats, had failed (Tadros, 1976a). The parasite was successfully recycled in coccidia-free weasels (Tadros and Laarman, 1975b), demonstrating a prepatent period of seven to eight days and a patency of up to 60 days. Ferrets and polecats were susceptible to this parasite, but shed fewer sporocysts than the weasel. The same parasite was isolated in voles fed sporocysts shed by the stoat, M . erminea. However, two adult mink, M . lutreola, could not be infected. Male and female gametocytes were observed in the lamina propria of the last third of the small intestine of experimentally infected ferrets. Mature oocysts were detected in the lamina propria chiefly near the tips of the villi in naturally infected weasels. The parasite was assigned the specific name S. putorii (syns. Isospora putorii, Coccidium bigeminum var. putorii) by Tadros and Laarman (1978~). Recently, Rommel (1979) reported cycling, in a ferret, S . muris of the house mouse, for which the cat is known to be the natural definitive host.

5. Sarcocystis species undergoing gametogony in marsupials The opossum, Didelphis virginiana, was found by Duszynski and Box (1978) to be a definitive host for, probably, the same species of Sarcocystis from three genera of icterid birds-cowbirds (Molothrus ater) and grackles (Cassidix mexicanus and Quiscalus quiscula). Box and Duszynski (1980) gave this parasite the name S. debonei Vogelsang, 1929 (syn. Isospora boughtoni Volk, 1938). Morphologically similar sporocysts were shed by opossums fed Sarcocystis-infected muscle from each of the three avian host genera. Sporocysts passed by the opossums after ingesting S. debonei from grackles or cowbirds induced sarcocysts, 12 to 20 weeks later, in passerine birds from two different families, exhibiting remarkable looseness of intermediate host specificity. Schzonts were observed 11 to 16 days after infection in the vascular endothelium of the lungs of sparrows and canaries, which died or became moribund. Box et al. (1980) studied the morphology of the sporocyst of this species by phase contrast microscopy as well as by scanning and transmission electron microscopy.

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6. Sarcocystis species undergoing gametogony in birds of prey Oral inoculation of a rodent Apodemus sylvaticus, with mature oocysts from intestinal scrapings of a tawny owl chick, found dead in the nest, induced intense muscular sarcosporidiosis (Tadros and Laarman, 1976). The parasite, designated S. sebeki, was cycled in uninfected owls and laboratorybred A . sylvaticus (Tadros and Laarman, 1977b, g). Intense schizogonic proliferation was seen 6-7 days later exclusively in the hepatic parenchymal cells of A . sylvaticus fed 500000 sporocysts. It was accompanied by numerous foci of necrosis and often resulted in death of the host (Tadros and Laarman, 1980a, c, e). The mature sarcocyst had a slightly convoluted cyst wall, but no light or electron microscopically visible cyst wall projections (Figs 29-30) (Tadros and Laarman, 1978d). The cystozoites of this species were strikingly reminiscent in size and shape to those of Frenkelia. Using this species as a model, Tadros and Laarman (1979d) demonstrated the transmissibility of sarcosporidiosis amongst members of the intermediate host species by intra-peritoneal inoculation of merozoites from mature schizonts. The lightness of infection in rodents inoculated with liver homogenates containing schizonts suggested that mature merozoites did not undergo further proliferation by schizogony, but directly invaded the muscle. S. sebeki has since been successfully transmitted to laboratory mice, but not to Clethrionomys glureolus or Microtus arvalis (Tadros and Laarman, 1980e). Endosporulating oocysts, recovered from the droppings of barn owls Tyto alba, in Czechoslovakia, induced schizogony in the liver parenchymal cells, and sarcocyst formation in the musculature of laboratory mice, but not of Microtus arvalis (Cerna, 1976, 1977c; Cerna et al., 1978a). The parasite was cycled in Tyto alba and Asio otus. The goshawk, Accipiter gentilis, was mentioned as a final host of this species by Cernh (1977b), but not in later publications. The parasite was named S . dispersa by Cerni et al. (1978a), but as the name first appeared in print in a paper by Cerna and Sknaud (1977), it must be attributed to the latter authors. This cycle has since been confirmed in our own laboratory (Figs 38-42) (Tadros and Laarman, I980f). Electron microscopic studies on the schizogonic proliferation of this parasite, by synchronous multiple endopolygeny, have been carried out by eernh and Stnaud (1978) and by Tadros and Laarman (1980a, b). The cyst wall and cyst contents of S. dispersa were investigated by light and electron microscopy by Senaud and Cernh (1978) and by Tadros and Laarman (1980a). Munday (1977) reported elucidating the cycle of a species of Sarcocystis in a mouse (Mus musculus) and owls (Tyto novaehollandiae and T . alba) in Australia. Endosporulated sporocysts recovered from a naturally infected tawny owl, Strix aluco, induced muscular sarcosporidiosis in laboratory mice, but not in Apodemus sylvaticus, Microtus urvalis or Clethrionomys glweolus (Tadros and Laarman, 1980a, g). The parasite was designated S. scotti by Levine and Tadros (1980).

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Cerna and LouEkova (1976, 1977) and Cerna (1977a) induced macroscopic sarcocysts in the skeletal musculature of Microtus arvalis by oral inoculation with mature oocysts, shed by common kestrels, Falco tinnunculus. The schizogonic phase of the parasite was confined to the liver parenchymal cells. The morphology of the sarcocysts and the host specificity of this parasite, named S . cernae by Levine (1977b), was investigated by Cernh et al. (1978b). We recovered the same parasite from naturally infected juvenile kestrels in the Netherlands, confirmed its life cycle (Figs 4349) and carried out light and electron microscopic studies on the development of the sarcocyst, demonstrating that schizogony in the liver takes place by synchronous endopoloygeny (Tadros and Laarman, 1980a, d ; Tadros, 1981). We also reported excystation of the sporocysts by the rupture of the sporocystic wall into four vertical plates, following exposure to Microtus bile-trypsin solution at 39°C (Fig. 45). Laarman and Tadros (1980a) and Tadros and Laarman (1980a, c) found that the species of Sarcocystis of rodents which complete their gametogonic development in birds of prey, share the following common features : (i) a very rapid rate of growth of the sarcocysts; (ii) slender, small, elongate cystozoites but large metrocytes; (iii) absence of cyst wall projections; (iv) absence of a parasitophorous vacuole around the schizont, and division during schizogony by synchronous endopolygeny in the liver parenchymal cells; (v) pathogenicity of the schizogonic phase in heavy infections. 7. Sarcocystis species undergoing gametogony in reptiles Rzepczyk (1974) recovered mature sporocysts (9.6 x 6.6 pm) from the faeces of five out of seven carpet snakes, Morelia spilotes variegata, caught in south-east Queensland, in Australia. Oral administration of these sporocysts to laboratory-bred Rattusfuscipes resulted in lethargy, bloody ocular exudate and death, 10 to 11 days after infection. “Cysts” with “zoites”, 13-34 x 7-16 pm, presumably schizonts containing merozoites, were found in the capillaries of the cardiac and skeletal, muscles. Sarcocystis-infected muscle from a wild R.fuscipes was fed to a captive carpet snake and induced the formation of the FIG.38. Very heavy muscular sarcosporidiosis in a laboratory mouse orally inoculated 6 months previously with 250 OOO sporocysts of Sarcocystis dispersa from Tyro albu. Note remarkable swelling of muscles of the fore limbs.

FIGS39-42. Sarcocystis dispersa of Mus musculus, which completes its sexual cycle in the barn owl, Tyro alba ( x 1320).

FIG.39. Massive Sarcocystis-induced coccidiosis in the lamina propria of the small intestine of a naturally infected barn owl. Fresh preparation. FIG.40. Young schizont in wet-fixed, Giemsa-stained liver smear of laboratory mouse, 4 days after oral infection with sporocysts. FIG.41. Mature schizont in wet-fixed Giemsa-stained liver smear of laboratory mouse, 7 days after oral infection with sporocysts. FIG.42. Two merozoites within parasitophorous vacuoles in macrophage from wet-fixed Giemsa-stained liver smear, 8 days after oral infection with sporocysts.

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same type of sporocyst in the intestinal tissues. Mice could not be experimentally infected with the muscular stage, nor could gametogonic development be established in mice, laboratory rats or kittens. Rzepczyk and Scholtyseck (1976) described the fine structure of the sarcocysts of two species of Sarcocystis in R. fuscipes, with strikingly different cyst wall structures, but declined to identify the species infective to the carpet snake. However, in their published electron micrographs, type “A” sarcocysts exhibit a cyst wall structure remarkably similar to that of S. singaporensis, which also completes its cycle in a reptile (Zaman and Colley, 1975). Zaman and Colley (1975) recovered sporocysts (7-1 1 x 7-10 pm) from the faeces of the Malaysian reticulated python, Python reticulatus. Oral administration of heavy doses of these sporocyststo laboratory-bred Rattus norvegicus resulted in illness and death of 28 out of 30 animals, 5-12 days later. Four to nine days after infection, banana-shaped “zoites”-presumably free merozoites from an early schizogonic generation-were detected free in the plasma or within polymorphonuclear leucocytes in blood smears. These merozoites, which were observed in most organs except the brain, were occasionally seen to have two nuclei, suggesting division by endodyogeny. Small schizonts, measuring 5-6 pm, with a maximum of eight nuclei were observed exclusively in the lungs. Macroscopic sarcocysts were found in the skeletal musculature of two rats, killed two months after experimental infection with sublethal doses of sporocysts. The light and electron microscopic structure of these sarcocysts was described in detail. The parasite, originally named S. orientalis (Zaman and Colley, 1975) and renamed S. singaporensis (Zaman and Colley, 1976), was compared with S.proechimyos of the spiny rat and S. oryzomyos of the rice rat, described from Brazilian rodents by Shaw and Lainson in 1969, and S. booliati of the moon rat described in Malaysia by Dissanaike and Poopalachelvam (1975) and by Kan and Dissanaike (1975). A very similar species of Sarcocystis was described by Kan and Dissanaike (1977) from R.rattus diardii, in Malaysia. Zaman and Colley (1975) also described the light and electron microscopic structure of male and female gametocytes of S. singaporensis,from naturally infected pythons. Unlike most studied species of Sarcocystis, the gamonts of this species were located in the epithelial, rather than the sub-epithelial, tissues of the small intestine. The life cycle of S . singaporensis has been confirmed by Brehm and Frank (1980), who succeeded in infecting laboratory rats, but not Mus musculus, Meriones unguiculatus, Mastomys natalensis, Microtus arvalis, hamsters, guinea-pigs, chickens or pigeons with sporocysts isolated from a recently imported reticulated python. The authors recognized two consecutive generations of schizonts on the 6th and 16th days after infection. Reticulated pythons were experimentally infected by feeding on Sarcocystis-infected rat muscle, and gametogonic stages described in the epithelial and sub-epithelial layers of the duodenum and anterior third of the small intestine in biopsies. Sporulating oocysts were first observed on the 4th day after infection; shedding of sporocysts started on the 8-12th days and lasted for up to 117 days.

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Bledsoe (1979, 1980) recovered sporocysts from the great basin gopher snake, Pituophis melanoleucus deserticola, a common predator on deer mice, Peromyscw maniculatus, in Idaho, where 40.8 % of these rodents harboured muscular sarcosporidiosis. Oral administration of the sporocysts to deer mice was followed by schizogonic development in hepatocytes, 2-10 days later. Metrocytes were first observed in the muscular tissue 11 days after infection, while elongate cystozoites became discernible 34 days after infection. Direct transformation of cystozoites into micro- and macrogamonts was observed, starting five days after feeding gopher snakes with Sarcocystisinfected deer-mouse carcasses. Gametogonic development occurred in the epithelial and sub-epithelial layers of the small intestine and the anterior part of the large intestine. While the gametogonic phase appeared to be harmless to the snakes, the acute phase of infection (the schizogonic stage) was highly pathogenic for the rodent intermediate host. The parasite, which could not be transmitted to laboratory mice or to white-footed mice, was named S. idahoensis by Bledsoe (1 980). We have recently confirmed the cycle of S. idahoensis, using mature oocysts recovered from a gopher snake imported into the Netherlands two months previously (Figs 50-52). Our findings on the pathogenicity and stages of development of the schizogonic and sarcocystic stages in the deer mouse agree with those of Bledsoe (1980). Munday and Mason (1980) isolated mature sporocysts from the tiger snake, Notechis ater, in Australia, and observed sarcocysts in orally inoculated laboratory rats. The parasite, designated S. murinotechis, was not infective to cats, masked owls or quollis. F’IGS4 3 4 9 . Sarcocystis cernae of Microtus arvalis, which completes its sexual cycle in the kestrel, Falco tinnunculus. FIG.43. Young ganietocytes (+) in wet-fixed Giemsa-stained smear of scrapings of small intestine of kestrel, 18 h after feeding with Sarcocystis-infected vole muscle ( x 1320). FIG.44.Mature disporic tetrazoic oocyst in fresh preparation of scrapings of small intestine of kestrel, 7 days after feeding with S. cernae. Note intact oocystic wall and compact sporocystic residual body ( x 1320). FIG.45. In vitro excystation of sporocyst following incubation in solution of Microtus bile and trypsin at 39°C. Note the “splintering” of the sporocystic plates ( W ) and one of the released sporozoites (+). Another sporocyst ())) in the same field is still intact. Fresh preparation ( x 1320). FIG.46. Immature schizont dividing by multiple endopolygeny in parenchymal cell. Note host cell nucleus (HCN). Giemsa-stained smear of liver of Microtus 6 days after feeding with sporocysts ( x 1320). HG.47. Two young sarcocysts (+) within the same muscle fibre of M. arvalis, 12 days after oral infection with sporocysts. Note absence of septa and elongate cystozoites. Conspicuous rounded metrocytes fill interior of cysts. Fresh squash preparation ( X 1320). FIG.48. Massive infection with macroscopically visible sarcocysts in skeletal muscle of M. arvalis, 30 days after oral infection with 10 OOO sporocysts. Fresh squash preparation ( x 1320). FIG. 49. Slender, elongate cystozoites (+) and leaf-shaped metrocytes ( ))I escaping from rupturing sarcocyst. Fresh preparation ( x 1320).

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MUSCULAR SARCOSPORIDIOSIS IN PRIMATES AND CARNIVORES

1. Human muscular sarcosporidiosis

Human muscular sarcosporidiosis (Fig. 56) poses a specially intriguing problem. Sarcocysts were allegedly first reported in human tissues by Lindemann in 1863, and designated S. lindernanni by Rivolta in 1878, under which name the sarcocysts, subsequently recorded from human muscle, have generally been classified. Jeffrey (1 974) comprehensively reviewed previously recorded cases and dismissed the original records by Lindemann from the heart valves, kidneys and hairs of Russian patients as being probably mycotic in nature. In discussing the incidence of Sarcocystis in human muscle, we (Tadros and Laarman, 1976) pointed out that it is unlikely that man acts as a natural intermediate host of a sarcocystic coccidian parasite of a predator, but is most likely to acquire the infection by ingesting sporocysts infective to another primate, e.g. apes or monkeys. This suggestion, that human sarcosporidiosis is zoonotic in nature, has recently been substantiated by a thorough review of all known cases of human sarcosporidiosis by Beaver et al. (1979), who found that three of the four recognizable morphological types of sarcocysts observed in human skeletal musculature, strikingly resembled Sarcocystis species of monkeys. It was suggested by these authors that species of Sarcocystis in Cercopithecus talapion, Macaca mulatta and M . fasciculuris may be the source of zoonotic infection of man in Uganda, India and south-east Asia respectively. Beaver et al. (1979) cite the cycling of S. suihominis from man to swine and then from swine to non-human primates by Fayer et uf. (1979) as corroborative evidence for the loose host specificity of Sarcocystis, and hence as a justification of the assumption of zoonotic infection of man with Sarcocystis species of monkeys. The example of S. suihominis was an unfortunate choice as, in this cycle, man acts as the final host supporting the gametogonic intestinal stages, and not the far more strictly host specific muscular sarcocystic stage. A more relevant example of the possible looseness of host specificity of the sarcocystic stage in the intermediate host is provided by the experimental transmission of S. debonei from icterid birds, via the opossum as final host, to passerine birds of two different families (Box and Duszynski, 1978). In view of the differences in the specific identity and geographic range of the possible simian sources of human infection in different regions of the globe, e.g. China, Africa, south-east Asia, India, Europe and the U.S.A., we FIGS50-52. Sarcocystis idahvensis Bledsoe, 1980, which completes its cycle in gopher snakes and deer mice. FIG.50. Stages in the endosporulation of oocysts, in fresh preparations of scrapings of the small intestine of a naturally infected gopher snake Pituophis melanvleucus ( x 2000). FIG. 51. Massive infection with sporulated oocysts in the lamina propria of the small intestine of the same snake ( x 450). FIG. 52. Two merozoites in Giemsa-stained smear of liver of Peromyscus maniculatus, 6 days after oral inoculation with S . iduhensis sporocysts ( x 2000).

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are of the opinion that more than one type of carnivore will be found to act as the specific final host of Sarcocystis species responsible for zoonotic human muscular sarcosporidiosis. From the descriptions of the sarcocysts and the size of the enclosed cystozoites, it may transpire that mammalian, avian and even reptilian final hosts may be involved. Human infection with simian species of Sarcocystis must be assumed to occur by accidental ingestion of mature sporocysts shed in the faeces of the specific final host(s) that prey(s) regularly on Sarcocystis-infected monkeys. Human beings may ingest infective sporocysts directly by hand to mouth from soil, tree trunks or leaves soiled with sporocyst-infected predator faeces, when they invade natural monkey habitats, or they may consume contaminated fruits or vegetables collected from regions where monkeys and their predators interact. It is interesting to note here that we have recorded remarkably brilliant immunofluorescence at high titres in sera of Amerindians from Surinam, who regularly hunt monkeys. Such high titres, and such brilliance, are totally inconsistent with infection with intestinal stages of Sarcocystis, and have been seen by us previously only in sera of animals harbouring muscular sarcocysts. The consumption of wild-trapped reptiles, a common practice in Chinese restaurants in places like Singapore, where many cases of human sarcosporidiosis have been recorded, may lead to the consumption of sporocysts in raw or insufficiently cooked snake flesh, or the contamination of the utensils and kitchen cutlery with sporocysts during evisceration of the snakes. 2. Muscular sarcosporidiosis of other primates

Two species of Sarcocystis, S. kortei and S. nesbitti, are recognized in Old WorId monkeys. The literature on muscular sarcosporidiosis in non-human primates has been reviewed by Karr and Wong (1975), who recognized four distinct types of sarcocysts in Old World monkeys. These authors found 21% of 375 wild-caught Old and New World monkeys, but none out of 369 laboratory-born ones, infected with muscular Sarcocystis. Mehlhorn et al. (1977) described the similar, though distinct ultrastructure of the wall of sarcocysts from M. mulatta, Papio cynocephalus and Saguinus oedipus. All three types of cyst had thin walls and very small cystozoites. Kan et al. (1979) described the fine structure of Sarcocystis species from FIGS53-56. Sarcosporidiosis and Surcocystis-induced coccidiosis in primates. FIG.53. Mature oocyst of S. horninis. Natural infection ( x 2200). FIG. 54. Unsporulated oocyst ( I ) ) and sporulated disporic, tetrazoic oocysts in the subdemal connective tissue of a naturally infected Cercopithecus aethiops ( x 1OOO). FIG. 55. Fresh squash preparation of a sarcocyst with conspicuous finger-like wall projections within muscle fibre of the same monkey ( x 1200). FIG.56. Sarcocyst in haematoxylin and eosin-stained section of human muscle. Note the considerable length of the cyst and internal septation ( x 132).

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M. fascicularis, which, according to Beaver et al. (1979), was identical to that reported by Karr and Wong (1975) in M . arctiodes and M . nemestrina. Tadros and Laarman (1976, 1977i) reported concomitant infection of the muscles of wild-caught Cercopithecus with sarcocysts as well as mature disporic tetrazoic oocysts (Figs 54, 55). 3. Muscular sarcosporidiosis in carnivores

As the muscle cyst has to be eaten by a specific carnivorous final host for the life cycle of the parasite to be completed, muscular sarcosporidiosis in large mammals, like whales (Akao, 1970) and black bears (Crum et al., 1978), or in carnivores that are not normally prey, such as viperid snakes (Parenzan, 1947), python (Tiegs, 1931), buzzards (Eble, 1961), weasel (Tadros and Laarman, 1977j, 1979a), skunks (Erdman, 1978), badgers, genets, or mongooses (Markus and Daly, 1980), appears to constitute a dead end. It is likely that carnivores acquire sarcosporidiosis accidentally by ingesting sporocysts shed by other carnivores. The muscular sarcocysts detected in European weasels were remarkably similar to those of the species infecting the rodent Apodemus sylvaticus, which undergo gametogony in tawny owls. An owl, fed sarcocyst-infected mustelid muscle, shed scanty sporocysts (Tadros and Laarman, 1979a). Evidence is emerging for a looser host specificity of the intermediate stages of Sarcocystis than has been assumed over the past few years (Box and Duszynski, 1978; Erber, 1980). It may yet transpire that some species of Sarcocystis form extra-intestinal stages in the same host, in which they complete the intestinal gametogonic cycle; if so, as pointed out by Tadros and Laarman (1976) and Markus and Daly (1980), fundamental revision of our current concept of the life cycle of Sarcocystis would become necessary. D.

PATHOLOGY OF SARCOSPORIDIOSIS IN THE INTERMEDIATE HOST

Until recently, sarcosporidiosis was considered to be of little veterinarysignificance and the infection in farm animals was largely ignored by veterinarians and meat inspectors alike. The elucidation of the life cycle has permitted experimental infection of domesticated herbivores under controlled conditions, which has revealed that, far from being completely innocuous, at least some species of Sarcocystis may lead .to severe and even fatal disease in the intermediate host. Of the three species of Sarcocystis parasitizing cattle, that which completes its cycle in Canidae appears to be by far the most pathogenic (Gestrich et al., 1975a). The pathological manifestations of this species in young calves experimentally infected with heavy doses of sporocysts have been studied by Fayer and Johnson (1973, 1974) and Johnson et al. (1975), who reported loss of weight, anorexia, anaemia and prostration. The symptoms were most severe, often culminating in death, during the schizogonic proliferation 26 to 33 days after infection, and were associated with post mortem

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findings of lymphadenopathy, hydrothorax, hydropericardium, ascites, ecchymotic or petechial haemorrhage in the heart, brain, alimentary and urinary tracts. Histopathological changes included haemorrhage, mononuclear cell infiltration and oedema in cardiac, brain, liver, lung, kidney and striated muscle tissue. Several calves also exhibited necrotizing myocarditis and inflammation of the meninges and cerebral glial nodules. Fayer et al. (1976b) reported bovine abortion associated with experimentally induced acute sarcosporidiosis, but failed to detect the parasite in aborted foetuses. However, Munday and Black (1976) detected Sarcocystislike schizonts in the brains of two, and the placental tissue of four, bovine foetuses, accompanied by placentitis, myocarditis, pulmonary vasculitis and encephalitis. Abortion was also observed by Stalheim et al. (1977) in seven out of 13 cows, experimentally infected with canine sporocysts during the second trimester of pregnancy. Advanced post mortem autolysis was noted in two foetuses in the uteri of cows that had become moribund 35 to 37 days after infection with 1 x lo6 sporocysts of canine origin (Procter et al., 1977). The same authors reported abortion in two out of 5 pregnant cows, orally inoculated with 200 000 sporocysts of the same species of parasite. Jungmann etal. (1977) orally inoculated ten calves, one week old, with 2 x lo6 sporocysts excreted by dogs. All calves exhibited severe symptoms, followed by death, 14 to 29 days later. Anorexia, anaemia, fever and weight loss were associated with petechial haemorrhage and degenerative or inflammatory reactions in the liver, kidneys and muscle. The schizonts were examined by electron microscopy. Mahrt and Fayer (1975) carried out haematologic studies on calves, experimentally infected with the canine-bovine species of Sarcocystis. Blood, collected soon before death, 29 to 34 days after infection, was watery in consistency; packed cell volume, haemoglobin levels and erythrocyte numbers were reduced while levels of serum glutamic oxaloacetic transaminase, lactic dehydrogenase and creatine phosphokinase were raised. Pathologic manifestations of infection with the canine-bovine species are not confined to calves experimentally infected with massive doses of sporocysts, but have been observed under field conditions. Thus, spontaneous fatal sarcosporidiosis was reported in a two-week old calf in Oregon, U.S.A., associated with extensive schizogonic development in the renal cortex and endothelium of the arteries of the lungs, liver and myocardium (Schmitz and Wolf, 1977). Severe Sarcocystis-induced eosinophilic myositis was reported in a cow, in Finland (Rimaila-Parnanen and Nikander, 1980). Sporocysts from a dog that had been fed on uncooked beef were incriminated as the cause of severe anorexia and weight loss of six, and the death of two young heifers with which the dog had been housed. Typical sarcocystic schizonts were seen in the vascular endothelium of the heifers’ viscera (Frelier et al., 1977, 1979). In 1963, Corner and colleagues reported on an outbreak of “Dalmeny disease” amongst Canadian cattle in eastern Ontario, and attributed it to infection with an unknown protozoon. Abortion occurred in 10 out of 17 pregnant cows, and 17 out of 25 died or became moribund.

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There is little doubt that the causative organism was the schizogonic phase of the canine-bovine species of Sarcocystis. Similar outbreaks amongst herds of young cattle have since been reported in central Ontario (Meads, 1976), in England (Clegg et al., 1978) and in Norway (Landsverk, 1979). Severe histopathological changes associated with experimental infection of mule deer fawns with S. hemionilantrantis have been studied by Koller et al. (1977). The pathogenicity for lambs of the ovine species of Sarcocystis, with Canidae as final hosts, has been demonstrated by Gestrich et al. (1974, 1975a), Heydorn and Gestrich (1976), Leek et al. (1977), Munday et al. (1975) and Munday (1979). Infection with 100 000 or more sporocysts resulted in acute illness characterized by anaemia, inappetance, weight loss, fever, reduced serum proteins and haemorrhage in the muscles and visceral organs, coinciding with vigorous schizogonic proliferation of the parasite in the vascular endothelium. Infection of pregnant ewes with more than 50 000 sporocysts of this parasite led to abortion or stillbirth (Leek and Fayer, 1976, 1978). Goats fed sporocysts, shed by dogs after ingesting Sarcocystis-infected goat meat, became ill within three weeks, presenting fever and anaemia associated with schizogony of the parasite in the vascular endothelium of all internal organs. Several of the goats died during the acute phase of infection (Fischer, 1979; Collins and Crawford, 1979; Collins et af., 1980). Erber and Geisel (1979) orally inoculated 6-18-week-old pigs with 50 000 to 1 x lo6 sporocysts of S. miescheriana, shed by dogs. They reported fever coinciding with the schizogonic development of the parasite, 4-1 5 days after infection, and post mortem findings of haemorrhagic diathesis and capillary thrombosis of the heart. Pregnant sows, infected with 50 000 sporocysts, aborted (Erber et aE., 1978b). In our own laboratory, eight-weekold piglets, each fed 500 000 sporocysts of S. miescheriana derived from an experimentally infected fox, had elevated temperatures between 6 and 14 days later. The pigs remained otherwise healthy. When killed three months after infection, all the pigs revealed extensive muscular sarcosporidiosis, absent from three control animals. This may well indicate the existence of differences in the virulence of different strains of the same species of Sarcocystis, an aspect that has to date hardly been considered. Severe pathological manifestations were observed in 29 piglets, 12 days after oral inoculation with 50 000 to 5000 000 sporocysts of S . suihominis. Half of the animals died, with petechial haemorrhages in all organs and schizonts in the endothelial cells of veins (Heydorn, 1977a). Experimental infection of Microtus arvalis with 1 x lo6 sporocysts of S. putorii, shed by weasels, resulted in loss of condition, inappetance, hunched posture and extreme thirst, culminating in coma and death (Tadros and Laarman, 1975b). These symptoms coincided with schizogony in the liver and other viscera. Massive doses of S. cernae, S. sebeki and S. dispersa of birds of prey have been shown to be severely pathogenic and fatal for the respective rodent intermediate hosts (CernA and Louzkovh, 1976; Tadros and Laarman, 1979d, 1980a, c). Dose-related pathogenicity, manifested as fever, enlargement of lymph nodes, rapid respiration and diarrhoea, was observed in rats fed

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300-10 000 sporocysts of S. singaporensis,shed by a python snake. All animals receiving the higher dose died, with anaemia and petechial bleeding, after 9-20 days (Brehm and Frank, 1980). Acute hepatitis was observed in deer mice infected with 15 000 or more sporocysts of S. idahoensis (Bledsoe, 1980). Symptoms accompanying the schizogonic phase included dyspnoea, anorexia and ataxia, often culminating in death 6-8 days after infection. Post mortem findings included hepatosplenomegaly, petechial haemorrhages of the serosa and the cut surface of the liver and diffuse coagulative necrosis with cellular infiltration. E.

PATHOLOGY OF

SUrCOCyStk-INDUCED COCCIDIOSIS IN

THE FINAL HOST

Little evidence is available on the pathogenicity of Surcocystis-induced coccidiosis in the final definitive host. Dubey (1976b) stated that the parasite is not pathogenic to the definitive host, but Craige (1977) claimed that in every case where he had found Sarcocysris sporocysts in the faeces, there had been a chronic intestinal disorder. Although dogs and cats apparently suffer no ill effects from repeated experimental infection with different Surcocystis species, not all definitive hosts remain unaffected by the intestinal phase of infection. Thus, human volunteers, after ingesting raw beef infected with S. hominis, experienced abdominal pain and diarrhoea on the first day after infection and during the peak period of excretion of sporocysts (Heydorn et al., 1976; Heydorn, 1977b; Laarman and Tadros, 1978). More severe symptoms, including dyspnoea and increased pulse rate, were observed in human volunteers fed raw pork infected with S. suihominis (Heydorn, 1977b, Piekarski et al., 1978a; Kimmig et al., 1979). In our own laboratory, three dogs, fed wild swine flesh heavily infected with S.miescheriana, exhibited vomiting, diarrhoea and aggressive behaviour during the subsequent 48 hours. The pathological effects of consuming large numbers of sarcocysts may well be toxic, rather than parasitic in origin. Feeding deep frozen sarcocysts to volunteers should throw light on this point. Tadros and Laarman (1976) attributed the death of young tawny owl chicks to intensive intestinal infection with S. sebeki. During the summer of 1978 many juvenile kestrels, Falco tinnunculus, were found dying or dead in the Netherlands. The birds appeared emaciated but no viral, bacteriological or toxicological cause of death could be determined. The small intestines of all birds were massively packed with sporocysts and oocysts of S. cernae (Tadros and Laarman, 1980 c, d). Experimental infection of adult kestrels with S. cernae led to extrusion of blood stained strands of intestinal tissue, packed with sporocysts (unpublished observations) ; this was also observed in adult tawny owls, experimentally infected with S. sebeki. F.

SERODIAGNOSIS

Tadros et al. (1974) adapted the IFA test for detecting circulating antibodies against Sarcocystis. Using as antigen either cystozoites of s. cruzi of

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cattle infective to dogs, or excysted sporozoites of the corresponding sporocystic stage of the same parasite, passively acquired circulating antibodies were detected in the sera of newly born babies. These antibodies faded by the third month and babies remained serologically negative until the age of 9-10 months, when conversion to positive was noticeably high. These findings correspond with the report of parasitological isolation of S. hominis sporocysts from the stools of babies in the Netherlands at about nine months of age (Laarman and Mas Bakal, 1971). With the exception of a total life-long abstainer from all animal protein, sera from adult Dutch donors were all positive in dilutions of 1/20 and 1/40. Titres of sera of the general population were usually lower than those of excretors of S . hominis sporocysts, but only slightly higher than those of vegetarians (Laarman et al., 1975a). Antibodies against Sarcocystis were not detected in cow milk whey. Heat resistant antigens in milk were suggested as an explanation for the positive reactions in life-long vegetarians. Human volunteers, experimentally infected with intestinal stages of S. hominis, failed to exhibit a significant rise in IFA titre against Sarcocystis antigen (Tadros and Laarman, 1977b; Laarman and Tadros, 1978). Aryeetey and Piekarski (1976, 1978) confirmed the passive transfer of IFA-detectable antibodies to human babies from the mother, and demonstrated circulating antibodies in the sera of rats, fed with ovine sarcocysts. Litters, born to serologically positive female rats, had levels of circulating antibodies equivalent to those in the maternal sera, and converted to seronegative within three months. Piekarski et al. (1978a) detected titres of up to 1/1000 in human sera, 14 days after the donors had ingested S. suihominis; the titres dropped to 1/64, or even as low as 1/4, within 70 days. Thomas and Dissanaike (1978), in Malaysia, applied the IFA test to 243 sera from Orang Asli, Malays, Chinese and Indians, and found the highest titres among the Orang Ask Remarkably high titres and strikingly bright fluorescence, possibly indicating muscular sarcosporidiosis, were detected in the sera of Amerindians from the interior of Surinam, whereas very low titres were observed in the sera of Creoles from the coastal region of the same country (Tadros and Laarman, 1976 and unpublished results). We failed to detect significant IFA titres in sera of dogs or cats, repeatedly infected with, respectively, S. cruzi of cattle or S . cuniculi of rabbits, using either cystozoites or excysted sporozoites of the homologous species as antigen. Lunde and Fayer (1977) also failed to demonstrate IHA titres in sera of dogs, experimentally infected with S. cruzi. Tadros et al. (1975b) detected no circulating antibody in the sera of newly born, pre-colostral calves from serologically positive cows ; colostrum contained higher concentrations of antibodies than the corresponding bovine blood sera. Calves, purchased when 1-7 days old and maintained in stables on an artificial diet up to the age of eight weeks, had only a slight reaction in the 1/20 serum dilution, attributed to passively acquired maternal antibodies. All cattle that had grazed in the open, for even one season, were serologically positive, with IFA titres of 1/160 to 1/320. However, heifers that had been

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39 1

pastured for two years on grassland on a recently reclaimed Dutch polder, had remarkably few sarcocysts and very low IFA titres (unpublished observations). Nedjari et at. (1976) also used the IFA test for serodiagnosis of bovine sarcosporidiosis, and Jungmann et al. (1978) showed that calves developed significant IFA titres 4-5 weeks after experimental infection with S. cruzi. The titres persisted for 25 to 30 days and superinfection 60 weeks after the primary infection induced a rapid increase. Lunde and Fayer (1977) successfully applied the IHA reaction and the agar gel diffusion test, using soluble antigen from the cystozoites of S. cruzi, for detecting circulating antibodies in cattle. IHA titres began to rise at 30 days, and reached levels of 1/39 000 at 90 days, after infection with 200 000 sporocysts. IHA titres of 1/486 were regarded as clinicalIy insignificant. An initial decrease in the total serum or plasma protein levels, reflecting reduced serum albumin, followed by a subsequent rise in immunoglobulin level of both the IgM and IgG fractions, was observed in calves experimentally infected with S. cruzi (Fayer and Lunde, 1977). Shukla and Victor (1976) used the complement fixation test, with sarcocyst extracts as antigen, for serodiagnosis of sarcosporidiosis in cattle and buffaloes. Arru et al. (1978) detected significant IFA titres in sera of sheep and pigs naturally infected with sarcosporidiosis, but failed to establish a correlation between titres and the extent of muscular infection. Weiland et al. (1980) reported the development of IFA, IHA and enzyme-linked immunosorbent assay (ELISA) titres in sera of sheep and calves, 4-14 days after infection with S. tenella and S. cruzi respectively; the titres reached a peak at days 21 to 86 and thereafter declined, A remarkable degree of cross reaction in the IFA was noted amongst species of Sarcocystis parasitizing rodent, lagomorph and bovine hosts (Tadros and Laarman, 1976 and unpublished observations). Strong cross reaction with Frenkelia was also noted (Tadros et at., 1975c) and confirmed by Cerni and Kolhfova (1978), but not with I . gondii. Tadros et al. (1979, 1980b) adapted the ELISA for detecting circulating antibodies against Sarcocystis. Our results indicated (i) complete absence of cross reaction with toxoplasmic antigen (Tadros et al., 1981), (ii) good correlation with IFA results in human and bovine sera, and (iii) strong cross reactions amongst S. cruzi, S. hominis, S . hirsuta, S . sebeki, S . cernae, and S. cuniculi. G.

DEVELOPMENT OF

Sarcocystis I N CELL CULTURES

Interestingly enough, the first concrete evidence for the coccidian nature of Sarcocystis was obtained by Fayer (1970, 1972) while attempting to culture an avian species of Sarcocystis; he noted the direct transformation of cystozoites into male and female gametocytes, with the formation of coccidian oocysts, in bovine, canine, chicken and turkey cell lines. This remarkable looseness of specificity of host cells supporting gametogonic development has not been observed with other species of Sarcocystis. Thus,

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Dubremetz et al. (1975) failed to obtain development of S. gigantea of sheep in embryonic ovine kidney cells. More recently, Becker et al. (1979) seeded human fibroblast, feline lung, canine kidney and swine kidney cell lines with cystozoites of S. suihominis, S. tenella, S. muris and a Sarcocystis species of goats completing its cycle in dogs; cystozoites penetrated all available cell types, but gametogonic development, which was completed within 18-22 hours, took place exclusively in the cell line from the host which supported the gametogonic cycle in nature. In this context, it is interesting to remark that a Sarcocystis species of grackles, probably the species originally cultured by Fayer, has been shown to have a remarkably loose intermediate host specificity (Box and Duszynski, 1978). Mehlhorn and Heydorn (1978b, 1979) described the fine structure of gametogonic development of S. suihominis in newly isolated human fibroblasts and embryonic human intestinal cells ; the latter were destroyed by cystozoite penetration within six hours. Tadros and Laarman (1979~) reviewed the literature on earlier unsuccessful attempts at culturing Sarcocystis and described the differentiation of male and female gametocytes of S. cuniculi of European rabbits in an embryonic feline fibroblast cell line (Figs 59-61). In addition to facilitating ultrastructural studies of the gametogonic stages, the successful culturing of Savcocystis has permitted detailed cytological and cytochemical studies of these stages (Vetterling et al., 1973; Fayer and Thompson, 1975).

H.

EPIDEMIOLOGY AND EPIZOOTIOLOGY OF SARCOSPORIDIOSIS AND SUrCOCyStiS-INDUCED COCCIDIOSIS

In spite of the obvious close relationship between Sarcocystis and homoxenous coccidia, like Eimeria, certain aspects that have emerged as characteristic of the obligatorily heteroxenous sarcosporidia impinge directly or indirectly on our understanding of the epizootiology and epidemiology of infection with these organisms. FIGS57, 58. Sarcocystis cuniculi of the common European rabbit, which completes its sexual development in Felis catus. FIG.57. Fresh preparation of micro-isolated sarcocyst ( X 130). FIG.58. Higher magnification of cyst wall of live sarcocyst, showing cyst wall projections resembling thick carpet pile ( x 3300). FIGS59-61. S. eunicufi in an embryonic feline fibroblast cell line ( x 1000). FIG.59. Two cystozoites within the same cell, 2 h after infection. FIG.60. Mature microgametocyte with 16 discernible microgametes and a disc-like residual body, 18 h after infection; HCN=host cell nucleus. FIG.61. Mature macrogamete, 18 h after infection (arrowed).

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1. The obligatorily heteroxenous type of life cycle Although the assumption of the heteroxenous mode of life cycle imposes the need for regular encounter between the specific intermediate and the final host species in a predator-prey relationship, as a prerequisite for cycle completion, it brings certain obvious biological advantages. It is evident that coccidia, like Sarcocystis, which have evolved the capacity not only to excyst, but extensively to augment their numbers and to retain their viability for months or even years within latent cysts in the tissues of suitable prey animals, have a substantial survival advantage over homoxenous coccidia of carnivores. The shift of the schizogonic phase of asexual development from the final to the intermediate host has a considerable impact on the dynamics of infection with sarcosporidia. This shift exerts far reaching effects on immunological considerations, as well as on the determination of the degree of host specificity in the final and intermediate hosts. (a) Immunological considerations. It has been established that in some species of Eimeria, e.g. E. maxima and E. tenella, it is the second generation of schizonts that stimulates the host’s immune response (Horton-Smith, 1949; Kendall and McCullough, 1952; Rose and Hesketh, 1976). Interestingly enough, attenuated strains of E. tenella that have been selectively bred to develop precociously, directly from first generation schizogony to gametogony without an intervening second generation of schizonts, failed to induce any protective immunity. The omission of the schizogonic stage of development of Sarcocystis from the final host has reduced to an absolute minimum the interaction between the parasite and the cells at the intestinal site of gametogonic development in the final host. The ingested cystozoites invade the subepithelial layer of the small intestine and transform within 18-22 hours into zygotes, which are rapidly enclosed within a presumably immunologically inert oocystic wall. The exclusion of a prolonged pei?od of schizogony with its attending enhancement of host-parasite interaction has no doubt reduced the extent of protective immunity in the final host, as is evident from the susceptibility of the same animal to repeated infection with Sarcocystisinduced coccidiosis. That is not to say, however, that some protective immunity against the intestinal stages of Sarcocystis does not eventually develop in the final host. By counting the total number of sporocysts excreted at primary infection and after repeated challenge, we have clearly demonstrated the progressive development of protective immunity, e.g. against Sarcocystis infection in cats (Tadros and Laarman, 1978a) and weasels (Tadros and Laarman, 1976), and against FrenkeZia in buzzards (Tadros, 1977). The mechanism of this immunity is so far not fully understood. No significant rise in circulating antibodies could be demonstrated by the IFA test or the ELISA in sera of humans, cats or dogs, following infection with, respectively, S. hominis, S. cuniculi or S. cruzi (Laarman and Tadros, 1978; Tadros and Laarman, 1978a; Tadros et al., 1979 and unpublished observations). It is likely therefore that locally produced antibodies of the IgA class of immunoglobulins and/or cell-mediated immune mechanisms are involved. Circumstantial evidence for the possible implication of local IgA

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antibody is provided by our repeated observation of prominent Peyer’s patches of the intestines of dogs and cats, experimentally infected with S. cruzi and S. cuniculi respectively. Peyer’s patches are known to be rich in precursors of IgA plasma cells, believed to secrete much of the IgA antibody in the gut (Cebra et al., 1979). While it is largely assumed that, in partially immune hosts, those Eimeria parasites which complete the life cycle are normal in every way and the length of the prepatent period of oocyst shedding is unaffected (Rose, 1973), in our own experience with S . cuniculi in cats, S. putorii in weasels and F. glareoli and F. microti in buzzards, very many of the sporocysts excreted by animals challenged with the homologous species were abnormal, vacuolated and obviously not viable; furthermore, the prepatent period was often prolonged and patency of sporocyst excretion significantly shortened. In both Sarcocystis and Frenkelia, the wrestling of the parasite with the host’s immune mechanism during the immunologically provocative schizogonic stages has been displaced to the internal organs of the intermediate host, where one or more schizogonic generations in intimate contact with the blood-engorged visceral organs induce impressive rises in titre in the IFA test in rabbits (Tadros and Laarman, 1978a) and IHA test in calves (Lunde and Fayer, 1977). Protective immunity in the intermediate host against reinfection with muscular sarcosporidiosis has as yet not been systematically investigated. It may be added that, unlike the asexual proliferation in the life cycle of Eimeria, the duration of which is determined, at least in part, by the host immune response, asexual development in the obligatorily heteroxenous Sarcocystis proceeds leisurely within the sarcocysts in the intermediate host, with gradual augmentation in number of infective cystozoites. (b) Host specificity. Eimeria species are generally assumed to be highly host specific. However, this meticulously stringent degree of specificity has been judged largely on the basis of oocyst production by the abnormal host. Sporulated oocysts of E. tenella of chickens excysted and the sporozoites invaded the intestinal epithelium of mice to undergo one generation of-albeit abnormal-schizogony (Haberkorn, 1970). These observations suggest that it is the second generation of schizogony, during which it is speculated that sexual differentiation takes place (Klimes et al., 1972), that is the most exigent stage of the life cycle. This may well explain the general assumption, based on experimental observation, that the asexual stages of development of Sarcocystis in the intermediate host are generally more strictly host specific than the gametogonic stages in the final host. The relative looseness of specificity of the definitive host, so that not only dogs, but also foxes, wolves, coyotes and raccoons can support gametogonic development of a given species, e.g. S . cruzi of cattle, is a factor of appreciable significance in the local, as well as the global, distribution of Sarcocystis species. 2. The subepithelial site of development of gametocytes

Available evidence indicates that Sarcocystis species with mammalian or avian final hosts, undergo gametogony not preceded by schizogony in the

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sub-epithelial lamina propria tissues of the small intestine. This single feature of the life cycle has profound effects on the epizootiology of infection with this group of organisms, as it permits endosporulation of the oocysts, which protects the young oocysts from uncertain environmental conditions during the critical process of sporulation, and prolonged excretion of the sporocysts. The subepithelial location of the oocysts renders the rate of oocyst excretion independent of the short life span of the intestinal epithelial cells and permits the gradual “trickling out” of mature sporocysts in voided stools, for a prolonged period of patency. This ensures renewed contamination of the terrain with fresh crops of sporocysts and maximum dissemination of these within the territorial limits of the final host, as well as along migratory routes, e.g. of birds of prey. The mechanism of excretion of the oocysts or sporocysts from the lamina propria into the lumen of the intestine remains obscure. We have discussed this problem and suggested the possible involvement of an active mechanism of expulsion, which may be set in motion by the host’s immune response (Tadros and Laarman, 1976). 3. Sporocyst survival and excystation

Due to their sporulation within the intestinal tissue of the final host, sarcosporidian sporocysts appear to be remarkably resistant to environmental conditions. Thus, sporocysts of S. cernae and S. dispersa, recovered from carcasses of barn owls and kestrels that had been deep-frozen at -20°C for 24 to 48 hours, retained their infectivity for the respective intermediate rodent hosts (unpublished personal observations). Similarly, Heydorn and Rommel reported survival of sporocysts of Sarcocysz‘is and Frenkelia after repeated freezing and thawing (unpublished discussion at the Fifth International Congress of Protozoology, New York, 1977). Evidence for exposure to bile of the specific intermediate host as a necessary stimulus for excystation of Sarcocystis sporocysts has been obtained by Fayer and Leek (1973), Cerna et al. (1978b) and Tadros and Laarman (1979b, 1980d). The mechanism of excystation of the sporocysts of S. debonei has been investigated by scanning and transmission electron microscopy by Box et al. (1980) and appears to be similar to that of I . gondii and other species of Isospora of carnivores. 4. Prevention of sarcosporidiosis and Sarcocystis-induced coccidiosis The dynamics of transmission of muscular sarcosporidiosis in farm animals and the acquisition of Sarcocystis-induced intestinal coccidiosis by man and his carnivorous pet animals have been discussed in detail and measures for preventing both types of infection outlined by Tadros and Laarman (1976).

TISSUE C Y S T - F O R M I N G E I M E R I I D C O C C I D I A

VII. FRENKELIOSIS AND Frenkelia-INDUCED A.

39 I

COCCIDIOSIS

INTRODUCTION AND LIFE CYCLE

Since its discovery in the brains of short-tailed voles at Lake Vyrnwy, in Wales, by Findlay and Middleton (1934), this parasite, which is closely related to Sarcocystis but exhibits a striking predilection for the central nervous system of the host, has been recorded in several genera of rodents, belonging mainly to the family Cricetidae and occasionally to the families Muridae and Chinchillidae. Round to oval frenkelian cysts, measuring up to 1 mm in diameter, have been described in Europe from different species of Clethrionomys and from the water vole (Erhardova, 1955; Zasukhin, 1958; Cern6, 1959; Sebek, 1962; Enemar, 1963; Ludvik, 1963; Doby et al., 1965; Tadros, 1968; Kepka and Krampitz, 1969; Tadros and Laarman, 197%). Another, larger, deeply lobulated type of cyst, identical or similar to that originally described by Findlay and Middleton, has been reported as a natural infection in wild specimens of different species of Microtus in Europe and in the U.S.A., in musk rats in Canada, and in lemmings in Sweden (Findlay and Middleton, 1934; Elton et al., 1935; Frenkel, 1953; Sebek, 1962, 1963; Enemar, 1964; Karstad, 1963; Tadros, 1968; Krampitz and Rommel, 1977; Tadros and Laarman, 1977k, l), as well as in a laboratory albino rat (Hayden et al., 1976) and in chinchillas (Meingassner and Burtscher, 1977; Bestetti and Frankhauser, 1978). In our own laboratory, lobulate frenkelian cysts have been repeatedly observed, generally together with the rounded type, in the brain tissue of naturally infected bank voles, Clethrionomys glareolus, trapped in the Netherlands (Fig. 66) (Marks, 1978; Tadros and Laarman, 1977m). Both types of frenkelian cysts are septate afid enclose rounded (metrocytic) and slender, elongate cystozoites, the fine structural details of which are practically identical to those of Sarcocystis. Both types of cystozoites reproduce by endodyogeny (Kepka and Scholtyseck, 1970; Scholtyseck et al., 1970; Tadros, 1970a, c; Tadros et al., 1972). In 1968, Biocca named the parasite which forms lobulated cysts in the brain of M. agrestis, Frenkelia microti, as type species of a new genus; he designated the species forming rounded cysts in the brain tissue of C.glareolus as F. glareoli. All attempts at experimental transmission of frenkeliosis directly from vole to vole by intraperitoneal, intracerebral or oral inoculation of cystozoites, even following corticosteroid treatment or splenectomy of recipient animals, have met with complete failure (Tadros, 1970a). The cystozoites of Frenkelia, like those of Sarcocystis, are completely refractory to transmission by these routes. Circumstantial evidence has been obtained for congenital transmission of frenkeliosis in the bank vole (Tadros and Laarman, 1977p, 1978e). Attempts to complete the gametogonic cycle in the intestinal tissue of a carnivore, by feeding Frenkelia-infected Microtus or Clethrionomys to cats, foxes, mustelids, tawny and long-eared owls or kestrels (Tadros, 1970a, b ;

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Tadros and Laarman, 1976) or foxes, cats, martins, weasels, kestrels and a goshawk (Kepka and Skofitsch, 1979) failed. In 1975, Rommel and Krampitz fed naturally infected bank vole brains to cats, dogs, kestrels, common buzzards, goshawks, barn owls, long eared and tawny owls. The gametogonic cycle was successfully completed, as evidenced by the excretion of sporocysts, only in the common buzzard, Buteo buteo. The sporocysts, which measured 11.3-13.8 x 7.7-10.0 pm, were shed after a prepatent period of 7-9 days, for 7-57 days. Oral administration of these sporocysts to bank voles resulted in cerebral frenkeliosis. The parasite could not be transmitted to laboratory mice or M . arvalis. Schizogonic stages were detected in hepatic parenchymal cells of bank voles 5-8 days after infection with sporocysts. Intraperitoneal inoculation of uninfected voles with liver homogenate from voles, infected with Frenkelia seven days previously by oral administration of sporocysts, resulted in transmission (Krampitz et al., 1976). The life cycle of F. glareoli (Figs 63-65) has been confirmed in our own laboratory (Tadros and Laarman, 1976) and the parasite has been repeatedly cycled since in laboratory-bred bank voles and common buzzards. Vole to vole transmission was successfully accomplished in all of four bank voles by intraperitoneal inoculation of a saline suspension of liver homogenate containing schizonts, but in none of four by its oral inoculation. Brain cysts, measuring up to 45 pm in Giemsa-stained smears, were first detected on the 17th day after oral inoculation with experimentally induced buzzard sporocysts. Originally rounded and enclosing only groups of metrocytes, the cysts increased in size linearly with time to reach 360 pm in the course of the following six months, and became occupied predominantly by elongate cystozoites. Older cysts usually exhibited the characteristic empty central compartments. 7 Investigations on the fine structure of asexual multiplication of Frenkelia in the liver of bank voles were carried out by Gobel et al. (1978b) and by ourselves (Tadros et al., 1980a and unpublished observations). These revealed that the schizonts were in direct contact with the cytoplasm of the parenchymal cells, i.e. a parasitophorous vacuole was absent, and that the wall of the schizont was folded. Asynchronous maturation of merozoites within a single schizont was described by Gobel et al. (1978b); however, our FIGS62-66. Stages in the life cycle of Frenkelia. FIG.62. Sporocyst shed by Buteo buteo 8 days after being fed with lobulate frenkelian cyst in the brain of a naturally infected vole Microtus agrestis ( x 1320). FIG. 63. Mature schizont of Frenkelia in liver parenchymal cells of a bank vole, 7 days after infection. Haematoxylinand eosin-stained section( x 1320); HCN = host cell nucleus. FIG.64. Young stage of rounded type of cyst in Giemsa-stainedsmear of brain of bank vole, 21 days after infection with sporocysts ( x 1320); HCN = host cell nucleus. FIG. 65. Cystozoites released from a rounded cyst isolated from the brain of bank vole ( X 1320). FIG.66. Mixed infection with rounded and lobulate types of Frenkelia in fresh squash preparation of brain of naturally infected bank vole ( x 1320).

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own studies revealed synchronous endopolygeny. A host cell reaction was detectable in the formation of a thick border of mitochondria and endoplasmic reticulum. Rommel et al. (1977) made a detailed study of the sexual development of Frenkelia from bank voles in the intestinal tract of the avian definitive host. Male and female gamonts were detected within the basal portion of epithelial cells of the anterior half of the small intestine of the buzzard 21 to 24 h after infection. Mature microgametocytes contained 10 to 14 biflagellate microgametes. Young oocysts were observed immediately under the epithelial cells three days after infection. The cystozoites of the lobulated type of frenkelian cyst of M . agrestis have been shown also to complete their sexual cycle in the intestinal tissues of B. buteo, with a prepatent period of 7-8 days and a patency of up to seven weeks (Krampitz and Rommel, 1977). In our own laboratory, brains of naturally infected common European voles, M . arvalis, captured in the Netherlands, were fed to uninfected buzzards. Mature sporocysts were first shed nine days after infection and were excreted for 60 days. Schizogony was confined to the liver parenchymal cells of the intermediate host (Tadros and Laarman, 19771; Laarman et al., 1979). The parasite was also successfully transmitted to laboratory rats, musk rats and Apodemus sylvaticus. Preliminary observations in our laboratory indicated an inverse correlation between the number of orally inoculated F. microti sporocysts and the number of voles that acquired infection, as well as the number of cysts that developed in their brains. it remains to be ascertained whether this parasite is identical to that infecting M . agrestis. A fascinating feature of the parasite with the lobulate type of frenkelian cyst is its loose intermediate host specificity. In marked contrast to Sarcocystis, where the intermediate host is generally much more strictly specific than the final host, this frenkelian species is known. to cohplete its gametogonic cycle exclusively in common buzzards, but is transmissible by oral administration of sporocysts to M . arvalis, common and golden hamsters, musk rats, three species of Apodemus, laboratory rats and mice, multimammate rats, chinchilIa and the European rabbit (Krampitz and Rommel, 1977; Rommel and Krampitz, 1978; Tadros and Laarman, 1977k, 1). Rommel and Krampitz (1 978) reported that C.glareolus resisted infection with sporocysts of the parasite with lobulated cysts in M. agrestis. However, in our own laboratory, lobulated cysts of the F. microti type have been encountered on several occasions in naturally infected bank voles (Marks, 1978; Tadros and Laarman, 19771, m); these cysts were invariably few in number and small in size, and were usually found mixed with rounded cysts of the F. glareoli type. Recently, a pure infection with a scanty number of lobulated cysts was found in a wild-caught bank’vole. The brain was fed to an uninfected buzzard. Sporocysts (Fig. 62) were shed after a prepatent period of nine days, for 18 days, and were used to infect six bank voles and six M. arvalis. Young cysts, measuring 40-50 pm in diameter, were detected in Giemsa-stained smears of the brain of a bank vole, killed four weeks after infection. The other five bank

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voles died within three months and were found to harbour small lobulated cysts. The cause of death could not be ascertained at autopsy. All six infected Microtus survived until killed six months after infection and all were heavily infected with macroscopic brain cysts. Differences between the results obtained by Rommel and Krampitz (1978) and by us may indicate a difference in strain or, possibly, even species of the parasites harboured by M. arvalis and M . agrestis respectively.

B.

PATHOLOGY

Although cysts may constitute up to 3.6% of the volume of a heavily infected brain of a bank vole (Enemar, 1963), frenkeliosis does not appear to result in paralysis or severe nervous disturbances in this host. Diuresis is a common symptom of frenkelian infection and is assumed to be due to involvement of the hypothalamus. Naturally infected bank voles have occasionally been observed to hold the head slightly to one side and to exhibit unidirectional circling motion (Tadros, 1970a). Curiously, such animals are usually found not to be very heavily infected (personal observations). Similarly, only relatively light infection was detected in the brains of two experimentally infected multimammate rats exhibiting paralysis or impaired locomotion (Rommel and Krampitz, 1978). Hepatic necrosis, probably due to destruction of the parasitized host cells after release of merozoites from mature schizonts (Gobel et al., 1978b and personal observations), has been observed in bank voles. Histopathological changes brought about by the schizogonic development in the liver and the frenkelian cyst in brain tissue have been studied by Geisel et al. (1978). Kepka and Skofitsch (1979) suggested that frenk%liosismay shorten the life span of infected bank voles and inferred -that mixed infection with Frenkelia and I . gondii brain cysts exacerbated the pathological manifestations of infection with these organisms.

C.

SEROLOGY AND CHEMOTAXONOMY

Investigations carried out on a small number of sera indicated strong cross reactions by indirect immunofluorescence between Frenkelia and Sarcocystis (Tadros et al., 1975~).These findings have recently been confirmed by Cernh and Kolhfova (1978). Our preliminary observations (unpublished) indicate cross reaction between Frenkelia and Sarcocystis in the ELISA. Cross reaction was, however, not demonstrated between Frenkelia cystozoite and I. gondii endozoite antigen in the IFA (Tadros et al., 1975~).Gel fractionation for protein and LDH isoenzyme analysis indicated differences, but an overall affinity, between Frenkelia of bank voles and an ovine species of Sarcocystis (Kepka and Rezaeian, 1976).

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IMMUNITY

Following the observation that buzzards, used for maintaining Frenkelia strains, eventually become refractory to further infection, we have recently carried out investigations on the development of immunity in the final host (Tadros, 1977; Tadros and Laarman, 1977 1; Laarman et al., 1979). A considerable degree of protective immunity developed, following repeated homologous challenge of buzzards three weeks after the end of patency of the previous infection ; there was a progressive, dramatic drop in the total number of excreted sporocysts, from hundreds of thousands after primary infection to none after the fourth challenge. A high proportion of sporocysts shed by partially immune buzzards was morphologically abnormal and appeared non-viable ; similar abnormal sporocysts were seen in the intestinal scrapings of a naturally infected wild buzzard. Preliminary observations indicated some cross immunity between F. glareoli and F. microti in the final host (Tadros, personal observations). There is some circumstantial evidence that bank voles may become naturally reinfected with Frenkelia (Kepka and Skofitsch, 1979). In our own laboratory, cysts belonging to two clearly distinct size populations, were repeatedly observed in naturally infected bank voles (Marks, 1978, 1979). We have also repeatedly observed degeneration of older cysts in brains of naturally as well as experimentally infected bank voles. Controlled experimental investigations on the development of protective immunity in the intermediate rodent host against frenkeliosis have as yet not been reported. E.

EPIZOOTIOLOGY

Investigations on the epizootiology of frenkeliosis of the bank vole have been carried out in the Netherlands, in an enzootic area where the migratory buzzard final host is known to overwinter, but is invariably absent during summer (Tadros, 1977; Marks, 1978, 1979; Laarman et al., 1979; Tadros et al., 1980a). Investigations on 300 live wild caught bank voles indicated no significant difference in natural prevalence of frenkeliosis between the two sexes; prevalence reached 100 % in voles trapped in February-March and was lowest during summer. Over 50% of the naturally infected animals acquired frenkeliosis before the age of three months. Voles may acquire infection even in the absence of the buzzard; however, the majority become infected in autumn, soon after the arrival of the buzzard in the region; there was a higher rate of infection in voles captured along the edges of woods, close to resting and roosting perches of the buzzard. Voles may become naturally reinfected with Frenkelia. Extensive observations on natural infection of bank voles with Frenkelia have also been carried out by Kepka and Skofitsch (1979) in enzootic areas in Germany and Austria, where the buzzard appears to be a permanent resident. Of particular interest is their report of an inverse correlation between dye-test titres against toxoplasmic antigen and the parasitological demonstration of cerebral frenkeliosis.

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TAXONOMY AND NOMENCLATURE OF TISSUECYST-FORMING COCCIDIA

CURRENT CONCEPTS ON THE

A.

FAMILIES, SUBFAMILIES A N D GENERA

The elucidation of the sexual phase of the life cycle of the tissue cystforming sporozoa has finally legitimized the coccidian taxonomic status of these organisms. There is general agreement at present to place these organisms in the suborder Eimeriorina LCger, 1911, of the order Eucoccidiorida Ltger and Duboscq, 1910, class Sporozoasida Leuckart, 1879, of the subphylum Apicomplexa Levine, 1970. Controversy is, however, rife about the generic designation and the choice of criteria for grouping these genera into families and subfamilies. In 1973, Levine placed the classical coccidia, i.e., Eimeria and Isosporu, in the family EIMERIIDAE Minchin, 1903. He relegated the atypical tissue cyst-forming organisms to the family SARCOCYSTIDAEPoche, 1913, recognizing three subfamilies. Toxoplasma Nicolle and Manceaux, 1908 and Frenkelia Biocca, 1968, which form thin-walled tissue cysts predominantly in brain tissue, were grouped in the subfamily TOXOPLASMATINAE. On the basis of the distinctive cyst wall, Besnoitia Henry, 1913 was placed as the only genus in the subfamily BESNOITIINAE Garnham, 1966, while Sarcocystis Lankester, 1882 was placed in the subfamily SARCOCYSTINAE Poche, 1913 on the basis of the elongate, septate morphology of the tissue cyst. Following the discovery of a new Toxoplasma-like organism, given the generic name Hammondia by Frenkel (1974a), and the elucidation of the sexual phase of Sarcocystis by Rommel and Heydorn (1972), Frenkel(1974a) selected the type of life cycle (homoxenous or facultatively or obligatorily heteroxenous) as the main criterion for grouping these organisms into three families. The genera Zsospora and Atoxoplasma were included, together with Eimeria, in the family EIMERIIDAE. Organisms with facultatively heteroxenous life cycles were assigned to the family TOXOPLASMATIDAE and those with obligatorily heteroxenous cycles relegated to the family SARCOCYSTIDAE. We (Tadros and Laarman, 1976) reviewed the taxonomy of the group and criticized the schemes of classification of Levine (1973) and of Frenkel (1974a) on the basis that the former proposal, based on tissue cyst location, lumped together Toxoplasma and Frenkelia, in spite of fundamental differences in the life cycle, while in the latter proposal Toxoplasma and Hammondia, which share very many basic morphological and physiological features, were split apart and placed into separate families. On the basis of the obligatorily heteroxenous type of cycle, and refractoriness of the cystozoites to transmission by inoculation, Hammondia was joined with Sarcocystis, which lacks a schizogony preceding gametogony in the final host, demonstrates strict intermediate host specificity, undergoes sporulation in the intestinal host tissues, and in addition has a different cyst wall structure and two morphologically distinct types of cystozoites. Tadros and Laarman (1 976, 1978b) drew attention to the erroneous biological conclusions that may

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result from such a scheme, contending that the degree of heteroxenity within a dynamically evolving group, like these tissue cyst forming eimeriid coccidians, may be too subtle and variable to constitute a reliable criterion for classification. The desirability of maintaining a uniform scheme for the classification of all eimeriid coccidians was stressed (see also Hoare, 1956), and it was pointed out that this objective is not served by erecting genera and families for toxoplasmid coccidia on the basis of the tissue stages, while retaining the end product of sexual reproduction as the main criterion for the taxonomic classification of the rest of the eimeriid coccidia. We emended the definition of the family Eimeriidae Minchin, 1903 to encompass also coccidia with tissue stages in the same or intermediate host(s) (Tadros and Laarman, 1976). The subfamily Eimeriinae Wenyon, 1926 was re-erected and redefined to include eimeriid coccidia shed as unsporulated oocysts, with schizogony preceding gametogony in the intestinal developmental cycle in the final host. The genera Toxoplasma, Hammondia and Besnoitia were synonymized with the genus Isospora Schneider, 1875, which was appropriately redefined to include also disporic, tetrazoic eimeriid coccidia, typically shed unsporulated, which may form tissue stages in intermediate hosts. It was recommended that the terms toxoplasmosis and besnoitiosis should be retained for the well known infections with these organisms. Frenkel (1977b) compiled an informative comparative table of characters of the tissue cyst-forming organisms and revised his earlier classification. Abandoning the degree of heteroxenity as a major criterion for recognizing families and subfamilies, Frenkel included I. serini of canaries, which has a homoxenous life cycle, in the family Eimeriidae, together with the genus Eimeria. All heteroxenous tissue cyst-forming organisms were pooled in the family Sarcocystidae. The genera Sarcocystis- and Frenkelia were finally grouped together in the subfamily Sarcocystinae, and Toxoplasma, Besnoitia and Hammondia in the subfamily Toqoplasmatinae. A new genus, Cystoisospora, placed in the same subfamily, was erected for species of Isospora, like I . felis, ingestion of the sporulated oocysts of which has been shown to confer on the tissues of nonspecific hosts, like mice, the capacity to initiate enteric gametogonic development in the final host. Frenkel et al. (1979) have since created a new subfamily, CYSTOISOSPORINAE, with the characters of the only genus. However, we deplore the erection of the new genus Cystoisospora, for the following reasons. (i) Species of Isospora, like I. felis, I. rivolta, I. neorivolta, I . ohioensis and I. vulpina are split up and placed in a different family from obviously closely related species, e.g. I. serini, on the flimsy basis of the ability of the oocysts of the former group to excyst, and of their sporozoites to remain viable, in the tissues of nonspecific intermediate hosts, within which they may be opportunistically ingested by the specific final host. In our opinion, it has by no means been sufficiently established that the sporozoites of homoxenous species of Isospora and Eimeria do not excyst, and retain their viability, in the tissues of nonspecific hosts. The negative preliminary results obtained by Markus (1979), regarding the lack of formation of such latent sporozoite

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stages of E . tenella, E. acervulina and E.flavescens in mice, are interesting but far from conclusive; it is obviously the Eimeria species of birds of prey or carnivores, rather than domestic fowl or rabbits, that are likely to benefit from such an adaptation. The latency of sporozoites of a given coccidian genus in the tissues of the laboratory white mouse is a highly artificial criterion. Latent infective stages are formed by the canine I . heydorni in the extra-intestinal tissue of dogs and cattle that ingest mature oocysts, but not in those of laboratory mice. It is currently accepted that the process of excystation of the Eimeria oocyst is nonspecific. Species of Eimeria like E. chinchillae not only excyst but undergo their complete life cycles in the guts of no less than seven species of wild rodents, as well as laboratory rats and mice (De Vos, 1970). With reference to the finding of latent sporozoites of I. felis-like species in the lymph nodes of orally inoculated rodents, it is relevant that, when Eimeria gets in the “wrong” host, e.g. ovine Eimeria species in goats, asexual stages are often located in the mesenteric lymph nodes. This was demonstrated by Lotze et al. (1964), who concluded that stages of Eimeria may well be disseminated widely throughout the body via the host’s lymphatic system. Are we to create new genera and subfamilies for such Eimeria species? (ii) We object to the erection of a new genus Cystoisospora for species of Isospora, that have clearly been shown not to form tissue cysts. Electron microscopic studies (Mehlhorn and Markus, 1976) have established that the cyst-like structures, observed under the light microscope by Frenkel and Dubey (1972), are practically unaltered sporozoites. As the parasite does not apparently undergo further development or divide in the rodent host, it may be more accurate to consider the rodent as a transport host, rather than an intermediate host. Dubey (1977b) added to the confusion by creatifig yet another generic name, “Levinea”, for those Isospora species resembling I. fetis. Dubey went even further than FreAkel(1977b) and restricted the generic name Isospora to species like 1.canaria, which are not only homoxenous, but the complete life cycle of which takes place exclusively in the gut. Where, may one ask, does I. serini, with its homoxenous cycle but extra-intestinal stages, fit in this scheme? The eagerness to erect new generic names is already creating confusion, even amongst the authorities in this field who have themselves coined and defined the new generic names. Thus, after defining his new genus Hammondia as forming elongate cysts with slender bradyzoites in skeletal and cardiac muscle and brain tissue, Frenkel (1974a, 1977b) implied that the coccidian parasite of dogs, previously known as Isospora bigemina and since designated 1. heydorni (Tadros and Laarman, 1976), may be a species of Hammondia (Frenkel, 1977b). However, this species has an obligatory heteroxenous dog-cattle-dog or, curiously enough, dog-dog-dog cycle, but no tissue stage, and certainly no tissue cyst has been seen, in spite of intensive searching (Heydorn et al., 1975a; Tadros and Laarman, 1976). Dubey goes further by referring to this parasite as Hammondia heydorni (Dubey et al., 1978b), although in a recent paper (Dubey and Williams, 1980),

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it is clearly stated that “no Hammondia-like organisms were found in tissue sections from the herbivores”. A practical problem, arising from basing the generic denomination on the tissue cyst stage in a hypothetical intermediate host, is the designation of naturally occurring disporic, tetrazoic oocysts. Thus, Gill et al. (1978) described unsporulated oocysts from the faeces of dogs fed diaphragmal muscle from the water buffalo but, not having carried out extensive studies, could not assign the organism a generic name! The restrictive definition of the genus Zsospora by both Frenkel(1977b) and Dubey (1977b) has also been rejected by Overdulve (1978). Levine (1977~) synonymized the new genus Hammondia with the genus Toxoplasma. Desser (1977) and Frank (1976) independently proposed that Toxoplasma, Besnoitia, Hummondia, Sarcocystis and Frenkeliu be given subgeneric status within the genus Zsospora. More recently, Overdulve (1978) considered Hummondia as a synonym of Toxoplasma; he believed that differences between Toxoplasma and other Zsospora species are adequately taxonomically expressed at the subgeneric level, and quoted similar examples in Plasmodium and Trypanosoma. According to this scheme, Toxoplasma is designated Isospora (Toxoplasma) gondii. By synonymizing Hammondia with the genus Isospora, Tadros and Laarman (1976) inadvertently created a homonym of I. hammondi of the marsh rice rat. Overdulve (1978) proposed the specific name I. datusi for this species. Thus, H. hammondi becomes Zsospora (Toxoplasma) datusi according to the proposal by Overdulve (1978), and I. datusi according to the proposal by Tadros and Laarman (1976). Differences in the mechanism of excystation of the sporocysts of I . canis and I. felis from that of Eimeria, and similarities to that of sarcocystic sporocysts, have recently ,been advocated as a criterion for the classification of these coccidia (Box et al., 1980). Although the topic warrants further interest and investigation, the dearth of knowledge of the excystation of isosporid coccidia renders as premature the use of this character for classification. In 1976, Tadros and Laarman applied to the Commission on Zoological Nomenclature to suppress the generic name Sarcocystis in favour of a newly erected genus Endorimospora (Greek : internally maturing fruit), on the basis of endosporulation of the oocysts and lack of a schizogony preceding gametogony in the final host. The new genus was meant to include both Sarcocystis and Frenkelia. Our personal contribution to the confusion about the generic designations was the inadmissible selection of the type species of the genus Surcocystis, S. rniescheriuna, as type species of the new genus. In view of this, and in deference to the general desire to retain the genus Sarcocystis, we have not pursued the matter further. B.

NOMENCLATURAL PROBLEMS IN SPECIFIC DESIGNATION OF THE GENUS

Surcocystis The recalcitrant nature of the problem of specific designation within the genus Surcocystis stems from a combination of the following four issues.

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(i) Until recently (Kalyakin and Zasukhin, 1975), it had generally been assumed that each host genus may harbour only a single species of Sarcocystis, and that related host genera may be parasitized by the same species. Thus, the specific name S. fusiformis became generally applied to the sarcosporidia of cattle as well as the buffalo. Following the discovery of the life cycle of Surcocystis, however, it transpired that a host genus may harbour the muscular stage of several species of Surcocystis and, due to the fairly strict host specificity of the sarcocystic stage, even closely related animals, like cattle and buffaloes, usually harbour distinct species. (ii) Consultation of the old literature revealed that various authors had at different times frequently attributed different specific names, sometimes with inadequate description, to the sarcosporidian parasites of the same host. (iii) On the other hand, before the elucidation of their sarcocystic identity, the endosporulating oocysts and sporocysts encountered in the intestinal tissues or faeces of carnivores, had been attributed to genera other than Sarcocystis, like Coccidium or Isospora, and assigned specific names largely on the basis of the identity of the host. In other words, different generic and specific names had in the past been frequently attributed to the muscular and intestinal stages of the same parasite. (iv) To complicate matters further, it emerged that the same carnivore may harbour intestinal stages of up to several distinct Sarcocystis species, and oocysts and sporocysts of different species of Sarcocystis from the same final host may be morphologically indistinguishable and had, in the past, often been erroneously given the same specific name. The problem of unambiguous specific designation became acutely felt in the mid seventies, when an urgent need aroFe for the differentiation of the various Surcocystis species of farm animals, She life cycles of which were rapidly being elucidated. Heydorn et al. (1975b) sought to solve this problem by scrapping the old specific names and starting afresh-assigning neatly appropriate new specific names, formed by compounding parts of the latin names of the intermediate and final host species of each parasite. Thus, a species with a human-cattle cycle would, according to this proposal, be referred to as S. bovihominis. The proposal was made public at the round table discussion on Isospora, Toxoplasma, Sarcocystis and related organisms, held on the 3rd September 1975,during the Second European Multicolloquium on Parasitology, in Trogir. The attractive convenience of this system was generally acknowledged. However, in the ensuing discussion, the following serious reservations were expressed by Prof. P. C. C . Garnham, Prof. J. M. Doby, Prof. H. Madsen, Dr G. E. Ford and one of us (W. Tadros): (i) in spite of its convenience, the proposal flagrantly contravened the Law of Priority and accepting it would set up a most undesirable precedent; (ii) it failed to take into account the probability of more than one Sarcocystis species completing its life cycle in the same intermediate and final hosts; and (iii) the likelihood of tongue-twisting names like clethrionomyobuteonis, resulting from adherence to this system. There was a general consensus of opinion of the imperative need to retain the old, available specific designa-

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tions and resolve the problem of many species infecting one host by the timehonoured taxonomic procedure of restricting the application of an old name, arbitrarily if necessary, to one of the newly differentiated species and assigning new names only to previously unnamed species. In view of the strong opposition, the proposers of the new scheme announced that the matter would be referred to the International Commission on Zoological Nomenclature. The following year we published a monograph, attempting to resolve some of these nomenclatural problems (Tadros and Laarman, 1976). After intensive consultation of the original descriptions, we assigned the appropriate old specific names to those species of Sarcocystis, the life cycles of which had been elucidated. The type species of Sarcocystis, S. miescheriana Kuhn, 1865, was recognized as the porcine species completing its sexual cycle in Canidae. After obtaining expert taxonomic advice, we synonymized Isospora bigemina with Sarcocystis miescheriana (see Tadros and Laarman, 1976,1978cand Levine and Tadros, 1980). Levine (1977a) reviewed the old, available specific names for Sarcocystis of the ox and sheep and for faecal coccidia of the dog and cat, and arrived at similar conclusions except that, by attributing the name S. hirsuta Mould, 1888 to the bovine-feline parasite and S. cruzi Hasselmann, 1926 to the bovine-canine species, he reversed the conclusion of Tadros and Laarman (1976). In the interest of promoting nomenclatural stability and universality, we decided to defer to Professor Levine’s choice of specific names for these two parasites (Levine and Tadros, 1980). During the course of the Fifth International Congress of Protozoology (New York, June-July 1977), in a discussion in which Prof. P. C. C. Garnham, Dr R. S. Bray, Mr R. V. Melville, Dr R. Killick-Kendrick and one of us (W. T.) participated, the resolution of the problem by the designation of neotypes was strongly advocated. The vexed question of the need for more than one stage of the complex cycle of Sarcocystis to be represented in the description of a given type species was raised, by analogy with Plasmodium. Consequently the validity of the requirement by article 72b of the International Code of Zoological Nomenclature (edn 2) stipulating that a type be designated by a single specimen, was discussed separately at the same Congress. As a result of this, a committee was set up, with Mr R. V. Melville, Secretary of the International Commission on Zoological Nomenclature, as chairman. Its main task was to devise a way to designate types for species of parasitic protozoa in which more than one stage in the life cycle is necessary for unequivocal identification. The Committee duly submitted its report to the International Commission of Protozoology and Zoological Nomenclature. The Committee on typification of species of protozoa has since recommended that the type material of such species, where necessary in the interest of stability of nomenclature, need not be a single individual, but may be a series of exhibits representing stages in a life cycle, which must, however, be directly related. The term “hapantotype” was coined by the Committee for such a composite of type specimens. These proposals have been incorporated into the draft third edition of the Code and, if accepted by the Commission, will render it possible to construct “neohapantotypes” for

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earlier-named species (Melville, 1980 and personal communication). The case for multiple type specimens is discussed by Garnham et al. (1979) and by Melville (1979, 1980). Frenkel et al. (1979) declared S. hirsuta, S. cruzi, 1. hominis (=S. hominis), S. tenella, S. bertrami, S. miescheriana, and I. bigemina (=S. bigemina) to be nomina dubia, and synonymized them with the following names recently proposed by Heydorn et al. (1975b) : S. bovifelis, S. bovicanis, S. bovihominis, S. ovifelis, S. ovicanis, S. equicanis and S. suicanis. Frenkel et al. (1979) also proposed S. muris as the new type species of the genus, replacing S. miescheriana. An application to this effect has been submitted by these authors to the International Commission on Zoological Nomenclature. This may eventually be published in the Bulletin of Zoological Nomenclature and will then become available for comment by interested parties. In due course, the Commission will vote on the proposal and the outcome will be published as an opinion. In a recent, concise but highly informative article, Melville (1980) remarked on the proposal by Frenkel et al. (1979), pointing out that the new composite specific names were proposed without adequate diligence in resorting to conventional taxonomic methods available (e.g. the designation of neotypes or the arbitrary restriction of the application of an old name to one of the newly defined species) to make these old names more meaningful and less ambiguous. Also, “by their confident synonymizing of their new names with the older, correct names, the authors have themselves destroyed whatever logical basis their proposal may have had”, and are required by the Law of Priority to use the older names. As the replacement of type species can be brought about only by the Commission, the type species of Sarcocystis Lankester, 1882 remains Synchitrium miescherianum Kuhn, 1865 until otherwise ruled (Melville, 1980). As other means exist to remove doubts about the application of the old specific designations in the genus Sarcocystis, particularly the imminent adoption of the concept of hapantotypes and hence neohapantotypes, the declaration as nomina dubia, of the old specific names of Sarcocystis does not, as pointed out by Melville (1980), provide sufficient grounds for the Commission to suppress them. Therefore, use of the new names S. bovifelis, S. bovihominis, etc., is illicit. In 1980, Levine and Tadros published a revised check list of 93 named species of Sarcocystis, based on exhaustive efforts to define the old specific names. This we hope will form a basis for efforts to resolve the problem within the context of the International Code of Zoological Nomenclature. C.

SPECIFIC DESIGNATION OF THE GENUS

Frenkelia

The specific designation of Frenkelia is equally problematic. Until recently, two specific names, F. glareoli and F. microti, were recognized on the basis of morphology of the cyst. Following the elucidation of the life cycle, and in accordance with the proposal of Heydorn et al. (1975b) for specific designations of the sarcosporidia, the specific name F. clethrionomyobuteonis was

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coined by Rommel and Krampitz (1975) for the frenkelian parasite of the bank vole completing its sexual development in the common European buzzard. In reviewing the classification of heteroxenous coccidia we (Tadros and Laarman, 1976) synonymized the specific names F. glareoli and F. clethrionomyobuteonis with the older specific designation F. buteonis, originally applied as Zsospora buteonis to endosporulating sporocysts in buzzards and owls, in the U.S.A. (Henry, 1932). In a recent publication, Frenkel et al. (1979) concluded that, due to geographic isolation, it is unlikely that any American buzzard would transmit Frenkelia to European rodents*. They also considered I. buteonis as nomen dubium in view of the insufficient original description. In our opinion, as both the European and American lobulated type of frenkelian cysts are referred to as F. microti, it must be assumed, until proven otherwise, that they may complete their gametogonic cycle in the same final host buzzard. If so, the specific designation F. microti would have to be synonymized with F. buteonis. If not, the American parasite should be assigned a different specific name. Although several genera of birds of prey appear to be refractory to intestinal infection with either Frenkelia species, no species of buzzard other than Buteo buteo has been tried. Sporocysts recovered by us from a naturally infected rough-legged buzzard, Buteo lagopus, induced rounded frenkelian cysts in bank vole brains (unpublished observations). IX. PHYLOGENETIC CONSIDERATIONS ON

THE

HETEROXENOUS EIMERIID COCCIDIA

The heteroxenous coccidia with tissue stages are obviously closely related to the classic homoxenous coccidia, like Eimeriu. The phylogenetic relationship between the two groups is however subject to speculation. We have traced a spectrum of subtly increasing degree of heteroxenity amongst disporic tetrazoic coccidia, as follows. (i) In the homoxenous Zsosporu cunaria, all development appears to be restricted to the intestinal tract of the specific host. (ii) Z. serini is homoxenous, but undergoes extra-intestinal as well as intestinal development. (iii) Species like I.felis, which is transmitted from cat to cat by ingestion of mature oocysts, can excyst in a number of nonspecific “carrier” hosts and use them to transport its sporozoites into the intestine of the carnivorous feline host. (iv) Z. gondii, which is still transmissible by oocyst ingestion amongst members of the felid final host species, but which also multiplies in non-specific hosts, these intermediate stages being adapted to infect the final host when ingested in prey animals. (v) Z. besnoiti and I. datusi can no longer be transmitted directly from cat to cat by the oocyst, and an intermediate host has become obligatory for the completion of the cycle. (vi) Finally, in Sarcocystis and Frenkelia all asexual development takes place in the intermediate host, only gametogony occurring *We have since cycled Frenkelia from the European vole, Microtus arvalis, in the American buzzard, Buteo borealis.

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in the intestine of the final host (Tadros and Laarman, 1976, 197711). We saw in this ascending series, evidence for evolutionary adaptation from a simpler homoxenous cycle to a more complex heteroxenous cycle, with obvious accruing advantages for the coccidia of carnivores, and concluded that the coccidia forming tissue stages have evolved from the intestinal homoxenous coccidia, a conclusion independently reached by Baker (1969). We still favour this hypothesis, which is supported by the following facts. (i) The accessibility of the intestinal tract to invading parasitic organisms. (ii) The relative simplicity of the homoxenous, compared to the heteroxenous, cycle. It is generally accepted that a highly sophisticated evolutionary process is needed to develop life cycles with more than one compulsory host, and that heteroxenity represents progress in evolutionary and ecological terms from original homoxeny (Odening, 1976). (iii) The absence of heteroxenity in the genus Eimeria, which is prevalent amongst herbivores. (iv) The basic similarity of gametogonic stages of heteroxenous and homoxenous coccidia in general suggesting that the intestinal cycle was the “backbone” of subsequent evolution. (v) The central role of Felidae (Heydorn, 1979) as final hosts for so many of these parasites (I. gondii, I . datusi, I. besnoiti, and several other species of Isospora and Sarcocystis) is strongly suggestive of dynamic evolution within eimeriid intestinal coccidia of this group of carnivores. (vi) The greater pathogenicity to Felidae of toxoplasmic tissue stages of I . gondii, compared to the intestinal stages, suggests an older evolutionary link between the host and the entero-epithelial stages, compared with the extra-intestinal stages. (vii) In Sarcocystis spp., there are remarkable similarities in cyst wall structure and size of the cystozoite amongst species completing their gametogonic development in final hosts which are .phylogenetically related, e.g., respectively, reptiles, birds of prey, and mammalian carnivores. Had the tissue stage been more primitive in evolution, one would have expected phylogenetically related animals, e.g. rodents, to have similar sarcocysts, irrespective of the final host, which is not the case. However, Landau (1974) has put forward an interesting alternative hypothesis, in which she suggests that Coccidiomorpha of vertebrates may have evolved from parasites of the coelomic cavity or tissues of mesoblastic origin of invertebrates. In the course of adaptation to vertebrate hosts, the Eimeriidae became localized in the reticuloendothelial system and later became adapted to endodermal tissues of the intestine and liver parenchyma. In other words, the simpler homoxenous eimerian cycle is postulated to have arisen from the heteroxenous cycle by secondary simplification.

ACKNOWLEDGEMENTS We wish to express our deep indebtedness to Dr Basil Khoudokormoff for his indefatigable enthusiasm and unfailing moral support, his generosity with time and effort in assisting with every stage of the preparation of the

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manuscript as well as his constructive criticism and excellent translation of the Russian, German, Spanish and Italian literature. We extend our gratitude to Mr R. Linger for his excellent technical assistance and invaluable help with the compilation of the literature, to Dr R. H. A. Wessels and the rest of the library staff of the Royal Dutch Academy of Sciences, Amsterdam, for their help with computer-screening literature, and to the staff of the Commonwealth Institute of Helminthology, at St Albans, England, (particularly Dr Angela Towle) for supplying some less accessible reprints. It is a pleasure to acknowledge the assistance of Mr B. Lawson and Mr H. W. van Rinsum of the Royal Tropical Institute for printing the photographs. We are grateful to Prof. J. van de Noorda and Ms W. Maris of the Department of Electron Microscopy in the Laboratory of Medical Microbiology, University of Amsterdam for providing facilities. We gratefully acknowledge permission by the Editorial Board of the Acta Leidensia to publish Figs 6 , 18-25, and by the Editorial Board of the Proceedings of the Royal Dutch Academy of Sciences, Amsterdam to publish Figs 26-32. REFERENCES Abakarova, E. G. and Akinchina, G. T. (1975). Interaction between macrophages of various origin and Toxoplasma gondii under conditions in vitro. Acta Parasitologica, 22, 195-200.

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467

Weiland, G., Roscher, B. and Reiter, I. (1980). Serodiagnostic procedures in experimental bovine and ovine sarcosporidiosis. Proceedings of the Third European Multicolloquium of Parasitology, Cambridge, September 7-13, 1980, p. 54. Weinberg, J. B. and Hibbs, J. B. Jr (1977). Endocytosis of red blood cells or hemoglobin by activated macrophages inhibitst heir tumoricidal effect. Nature, London, 269,245-247. Weitberg, A. B., Alper, J. C., Diamond, 1. and Fligiel, Z. (1979). Acute granulomatous hepatitis in the course of acquired toxoplasmosis. New England Journal of Medicine, 300, 1093-1096. Welch, P. C., Masur, H., Jones, T. C . and Remington, J. S. (1980). Serologic diagnosis of acute lymphadenopathic toxoplasmosis. Journal of Infectious Diseases, 142, 256-264. Wenyon, C. M. (1923). Coccidiosis of cats and dogs and the status of the Isospora of man. Annals of Tropical Medicine and Parasitology, 17, 231-288. Wenyon, C. M. (1926). “Protozoology”. Baillikre, Tindall and Cox, London. [Reprinted 1965.1 Werner, H. (1970). Beitrag zur Entwicklung und systematischen Stellung von Toxoplasma gondii:.Zeitschr$t fur Parasitenkunde, 34, 8-9. Werner, H. (1977). Uber die Wirkung von Toxoplasma-Antikorpern auf T. gondii nach Reinfektion. 2. Untersuchungen iiber das Auftreten von Toxoplasmen im peripheren Blut nach Primar- u. Sekundarinfektion. Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene, I. Abteilung, Originale, A, 238, 122-127. Werner, H. (1980). Latent Toxoplasma infection as a possible risk factor for CNS disorders. Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene, I. Abteilung, Referate, 267, 294-295. Werner, J. K. and Walton, B. C. (1972). Prevalence of naturally occurring Toxoplasma gondii infections in cats from US military installations in Japan. Journal of Parasitology, 58, 1148-1 150. Werner, H., Masihi, K. N. and Meingassner, J. G. (1978). Investigation on the effect of immune serum therapy on cysts of Toxoplasma gondii in latent infected mice. Zentralblatt fir Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene, 1. Abteilung, Originale, A, 242, 405-413. Whiteside, J. D. and Regent, R. H. J. (1975). Toxoplasma encephalitis complicating Hodgkin’s disease. Journal of Clinical Pathology, 28, 443-445. Willadsen, C. M. (1977). Ovine toxoplasmosis: literature review and seroepidemiological observations. Kongelige Veterinaer- og Landbohmkole Aarsskrift, Copenhagen, 1977, pp. 177-178 [abstract of dissertation]. Williams, H. (1977). Toxoplasmosis in the perinatal period. Postgraduate Medical Journal, 53, 614-617. Williams, D. M., Grumet, F. C. and Remington, J. S. (1979). Genetic control of murine resistance to Toxoplasma gondii. Infection and Immunity, 19, 416-420. Wilson, I. D. and Morley, L. C. (1933). A study of bovine coccidiosis 11. Journal of the American Veterinary Medical Association, 35, 826-850. Wilson, C. B. and Remington, J. S. (1979a). Activity of human blood leukocytes against Toxoplasma gondii. Journal of Infectious Diseases, 140, 890-895. Wilson, C. B. and Remington, J. S. (1979b). Effects of monocytes from human neonates on lymphocyte transformation. Clinical and Experimental Immunology, 36, 511-520. Wilson, C. B., Desmonts, G., Couvreur, J. and Remington, J. S. (1980a). Lymphocyte transformation in the diagnosis of congenital Toxoplasma infection. New England Journal of Medicine, 302, 785-788.

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Subject Index Page numbers

hi

bold indicafe illustration

A Acanthocephalus sp. (cont.) Abramis brama, A . tenuirostris, 189 A . brachyurus, 4-5 host depth effects on, 187 sexual maturation, 182, 241 Acanthocephalans auxiliary hosts, 233-234 temperature tolerance, 25 1 classification, 3 Acanthogyrus sp. climatic zone occurrence, 164-1 76, climatic zone occurrence, 28-37 199-231 habitats, 164, 176, 200, 201, 222 intermediate hosts, 159 host species, 164, 176 seasonal biology, 159 seasonal biology, 4-8 Acanthocephalus sp. procercoids, 7 mid-latitude, 29-37 A. (Acanthosentis) cholodkowskyi, 159 mountain, 37 A. (Acanthosentis) indica, 159 A . (Acanthosentis) tilapiae, 159 polar, 37 mid-latitude, 165-175, 204-221 sub-tropical, 28-29 more than one zone, in, 224-225 tropical, 28 mountain, 176, 221-222 host species, 28-37 intermediate hosts, 3 polar, 175, 221 sub-tropical, 164, 202-203 morphology, 3 tropical, 164-165, 199-202 seasonal biology, 3 gravid worms, 246-249 Accipiter gentilis, 375 growth and maturation, 241-249 Acipenser, helminth parasites, 3 host body location, 231-233 Acipenseridae, helminth parasites, 105, host species, 164-176 126, 219 interspecific interactions, 253 Addison’s disease, 341 length groups, 182, 186 Adelca, sexual differentiation, 304 life cycle, 183 Adenophorea, seasonal biology, maturation cycle, 183, 186, 234 102- 105 maturational migration, 249 Afon Terrig, Wales, 41, 104, 154, 155, mortality, 246 192, 193, 194, 195 population dynamics, 183 Agar gel diffusion test, 391 recruitment, 246 A. iowensis, 5-7 seasonal biology, 181-189 A. limnodrili, 5 A . anguillae, 181-182 A . sieboldi, 7-8 A . clavula, 182-184 sexual maturation, 241 A . dims, 184 survival time, 241 A . jacksoni, 185 taxonomy, 4 A . lucii, 185-188, 230 Albino rats, 397 A. parksidei, I 88- 189 Algonquin Park, Ontario, 68, 71, 81

469

470

SUBJECT INDEX

Alosa finta, helminth parasites, 100 Ameiva ameiva, 336 A. meridianus, helminth parasites, 215 Amerindians, 385 Amphicotylidae, seasonal occurrence, 64-70 Amphilina foliacea climatic zone ocurrence, 29, 35, 204, 217,223 host species, 29, 35 seasonal biology, 3 Amphilinidea Anguilla anguilla, helminth parasites, 55, 91, 202, 215 Anguillicolidae, seasonal biology, 136 Anisakidae, seasonal biology, 105, 123-126 Anarya water system, Trarndelag,41,65,67 helminth parasites, 8, 11, 12, 14, 103, 142, 212, 218, 227, 233 interspecific interactions, 252 long-term population studies, 253 mortality rate, 16, 236 population dynamics, 16 seasonal feeding activity, 17 temperature-dependent resistance response, 237 Antelopes, besnoitiosis in, 336, 345 Anthelmintics, 92 Anti-neoplastic drugs, 328 Anti-rat thymocyte serum, 324 Anti-toxoplasmic rabbit serum, 322 Apicomplexa, 403 Apodemus ffavicolis, 333 Archigetes sp. climatic zone occurrence, 29, 31, 34, 36,204, 208, 212, 217,223 development stages, 5, 7,241 gravid worms, 246 host species, 29, 31, 34, 36 invasion time, 238 sex influence, 242 annual cycle, 186 climatic zone occurrence, 165, 167, 169-172, 174, 175, 206, 207, 210, 211,215,219,221,224, 230 development stages, 182 gravid worms, 187, 248, 249 incidence patterns, 182, 184, 186, 187, 188, 233

Archigetes sp. (cont.) intermediate hosts, 1, 182, 185, 187, 188, 189,249 inerspecific competition, 252-253 life cycle, 1 principal hosts, 233-234 seasonal occurrence, 1 et sey. abiotic factors, 249-252 biotic factors, 252-253 experimental studies, 255-256 hypothesis for, 254-255 incidence and intensity, 231-233 Artificial thermal pollution, 250 Ascaridida, seasonal biology, 105, 123-129 Asellus aquaticus, helminth parasites, 187, 230 Asio otus, 375 Asses, 335 A. sylvaticus, 333, 358, 375, 386, 400 Atoxoplasma, 346 taxonomy, 403

Atractolytocestus huronensis climatic zone occurrence, 31,208-209 host species, 31, 165-167, 169-172, 174, 175 establishment period in, 239, 240 invasion time, 238, 240 intermediate hosts, 4, 7, 238 seasonal biology, 26 B Babesia, 345 Baboons, 359 Badgers, 386 Baildon Moor, Yorkshire, 89 Bank voles, frenkeliosis in, 397, 399, 400,401, 410 epizootislogy, 402 immunity, 402 pathology, 401 reinfection, 402 Barn owls, 375 Rarrouxia, sexual differentiation, 304 Rasiliscus vittatus, 336 Rathybothrium rectangulum climatic zone occurrence, 47, 205 gravid worms, 246 host species, 47

SUBJECT INDEX

Bathybothrium rectangulum (cont.) establishment period in, 238 seasonal biology, 64 sexual maturation, 64 Bays Bothnian, 154, 190, 230, 236 Chesapeake, 143 Hawk's, 365 Quinte, 161, 190 Bears, 363 Bellshill, North Lanarkshire, 88, 89 Besnoitia, 294, 335 see also Zsospora classification, 404, 406 synonyms, 295, 336, 404 taxonomy, 403 tissue cysts, 294, 295 B. bennetti, hosts, 336 B. besnoitia, hosts, 335, 336 B. darlingi hosts, 335 synonyms, 336 B. jellisoni hosts, 335 synonyms, 336 B. panamensis hosts, 336 synonyms, 336 B. sauriana hosts, 336 synonyms, 336 B. tarandi, hosts, 335 Besnoitian isosporiasis, 335-345 Besnoitiinae, 403 Besnoitiosis, 294, 335-345 acute phase, 337 development cycle, 345 epizootiology, 342-345 host immunity, 337, 339-340 hosts, 335-337 intermediate hosts, 345 life cycle, 342-345 pathology, 340-342 serology, 337 transmission, 342-345 vaccine development, 340 venereal transmission, 343 Biacetabulum sp. climatic zone occurrence, 29.. 31.. 203., 205, 208, 223

47 1

Biacetabulum sp. (cont.) development stages, 9 embryonation, 9 gravid worms, 247 host species, 29, 31 invasion time, 238, 240 intermediate hosts, 9 interspecific interactions, 252, 253 length classes, 10 maturation period, I0 procercoids, 9, 10 seasonal occurrence, 8-1 0 B. biloculoides, 8 B. carpiodi, 8 B. infrequens, 8 B. macrocephalum, 9 B. meridianum. 9-10 Birds of prey, sarcosporidiosis in, 375, 378. 388 Black bears, 386 Blicca bjoerkna, helminth parasites, 8, 218 Blood sucking arthropods, 345 Bobcats, 333 Bos taurus, 363 Bothriocephalidae, seasonal biology, 42-45, 55-56 Bothr iocephulus sp. climatic zone occurrence, 46, 47, 49, 50-52, 54,201, 202-204, 205, 208-210, 213, 218,222, 223, 225 egg development, 43, 45, 55 fecundity, 45 gravid worms, 55, 247 host species, 46, 47, 49, 50 -52, 54 establishment period in, 240 incidence patterns, 44 intermediate hosts, 43, 45, 55 life cycle, 43, 44, 45, 55 population growth, 43 procercoids, 43, 45 seasonal biology, 42-45, 55-56 B. ucheilognathi, 42-45, 225 B. claviceps, 45, 55 B. cuspidatus, 55-56 synonyms, 42 temperature tolerance, 44, 45 Brown-headed cowbirds. 353 Bubulus bubalis, 363

472

SUBJECT INDEX

Buffalo, sarcosporidiosis in, 353, 363, 365, 369 serodiagnosis, 391 Burros, 335 Buteo buteo eimeriid coccidian parasites, 296 frenkeliosis in, 398, 41 0 sporocyst excretion, 399 B. lagopus, 410 Buzzards, 372, 386, 394, 395 frenkeliosis in, 398, 400, 409, 410 immunity, 402

Canals Clyde, 187 Grand, County Dublin, 187 Shropshire Union, 5, 13, 130, 186, 212 Volga-Don, 12 Canaries, 404 Canis familiaris, 367 C. latrans, 367 Capillaria sp. climatic zone occurrence, 106, 109, 113, 116, 119, 121, 202, 206, 209, 214,217,219,220-221,224 development stages, 103 C gravid worms, 248 Caecidotea communis, helminth host body location, 231 parasites, 21 1 host species, 106, 109, 113, 116, 119, Calidris canutus, 336 121 Camallanidae invasion time, 239 habitats, 199 life cycle, 104 seasonal biology, 129-1 36 seasonal biology, 102-105 Camallanus sp. C. acerinae, 103 annual cycle, 131 C. brevispicula, 103-104 climatic zone occurrence, 107, 108, C. coregoni, 104 113, 116, 119, 121, 200, 206, 209, C. lewaschofi, 104 214,219,220,224,228,229 C. petruschewskii, 104 copulation, 133 taxonomy, 102 gravid worms, 247-248 Capillariidae, seasonal biology, 102-1 05 growth, 244 Capingentidae, seasonal biology, 40 host species, 107, 108, 113, 116, 119, Capra hircus, 366 121 Capreolus capreolus, 366, 367 establishment period in, 238, 240 Capuchin monkeys, 352 incidence patterns, 130, 134, 135, 233 Carassius auratus, helminth parasites, intermediate hosts, 129, 132 197, 203 larval stages, 129, 130 C. cavassius, helminth parasites, 147 life cycle, 129, 131 Carduelis carduelis, 346 long-term population studies, 253 Caribou, 335, 342 maturational migration, 249 Carpet snakes, 378 population structure, 132, 133 Carpoides sp., 40 seasonal biology, 129-136 C. carpio, helminth parasites, 9, 21 C. cyprinus, helminth parasites, 8 aquarium fish, in, 135 Caryophyllaeidae, seasonal biology, C. lacustris, 129-1 31, 228-229 4-26 C. oxycephalus, I 31-1 34 Caryophyllaeides fennica C. sweeti, 134 annual cycle, 27 C. truncatus, 134 climatic zone occurrence, 28, 29, 31, larvae, 134-135 34,36,37,202,204,212,217,218, sex ratio, 132 220,223,225,226,227 temperature tolerance, 251 development stages, 241 Camels, 353 egg production, 27

SUBJECT INDEX

Caryophyflaeidesfennica (cont .) gravid worms, 248 host species, 28, 29, 31, 34, 36, 37 establishment period in, 238, 240 host sex influence, 244 invasion time, 238, 240 incidence patterns, 27 maturation stages, 27 seasonal biology, 26-27, 225-226 Caryophyllaeus sp . auxiliary hosts, 11, 233, 234 climatic zone occurrence, 29, 30, 32, 35, 36, 202, 204, 205, 208, 209, 217, 218, 223, 226 control mechanisms, 15 development stages, 13, 14, 241 developmental time lags, 18 egg production, 18 genitalia, 12, 13 gravid worms, 14, 248 growth rate, I5 host-parasite system stability, 18 host species, 12, 29, 30, 32, 35, 36 age structure, 18 establishment period in, 236, 238, 239, 240 immune response, 246 infection resistance, 236 invasion time, 238 temperature-dependent resistance response, 237 incidence patterns, 13, 233 intermediate hosts, 10, 11, 15 interspecific interactions, 253 invertebrate intermediate hosts, 15 larval invasion of fish, 235 life cycle, 17, 18 life span, 14 long-term population studies, 253 mortality rate, 16 occurrence patterns, 14 peak incidence, 12, 13, 16 population dynamics, 13, 14, 16, 17, 18 mathematical model, 19, 233 principal hosts, 233 procercoids, 11, 12 recruitment patterns, 14, 16 seasonal biology, 10-19 sexual maturation, 241

473

Caryophyllaeus sp. (cont.) temperature tolerance, 236 C . brachycollis, 10 C . jimbriceps, 10-1 1 C . laticeps, 11-19, 226 survival patterns, 15 temperature tolerance, 15, 16 Caryophyllidea climatic zone occurrence, 28-37 mid-latitude, 29-37 mountain, 37 polar, 37 sub-tropical, 28-29 tropical, 28 host species, 28-37 incidence dynamics, 4 interspecific interactions, 4 maturation cycle, 4 seasonal biology, 3-40 Caspian Sea, 12 Cassidix mexicanus, 374 Catostomus commersoni helminth parasites, 8, 9, 19, 20, 21, 22, 23, 24, 25, 40, 145, 146, 188 host sex influence, 244 immune response, 246 infection resistance, 237 interspecific interactions, 252, 253 spawning influence, 245 seasonal lesions, 146 Cats besnoitiosis in, 343, 344 isosporan coccidiosis in, 348, 350 sarcosporidiosis in, 353, 369-373 antibodies, 390, 394 avian species, 373 bubaline species, 369 bovine species, 369 gazelline species, 369 lagomorph species, 372 ovine species, 371-372 pathology, 389 porcine species, 372 protective immunity, 394 rodent species, 373 sporocysts excretion, 395 toxoplasmid coccidiosis in, 297-301 antibodies, 305, 330 corticosteroid treatment. 307

474

SUBJECT INDEX

Cats (cont.) cystozoic stages, 299, 300, 301 development, 297-301 endo-epithelial stages, 297-299 endozoic stages, 299, 300, 301 entero-epithelial stages, 307, 308 gametogonic development, 297 human toxoplasmosis dissemination, role in, 329-331 immune response, 300, 306 cell mediated, 307 immunity, entero-epithelial cycle against, 305-309 intestinal epithelium mucosal changes, 310 intestinal reinfection, 306 Isospora datusi-induced, 333 Isospora gondii-induced, 301-303,305-309, 329 infection rate, 330 maternal antibodies, 308 oocyst excretion, 297, 300, 303, 305, 306, 307, 331, 333, 334 age effects, 308 infectivity, 329, 330 reactivation, 308, 331 viability, 331 pathology, 309-310 Peyer’s patches, role of, 306 primary infection, 308 reinfection resistance, 305 Sarcocystis-induced, 306 serological surveys, 330 schizogonic development, 297 source and enteric development, 297-301 sporozoic stages, 301 Cattle besnoitiosis in, 335, 336 congenital infection, 343 Isospora besnoiti-induced, 342 pathology, 341, 342 sarcosporidiosis in, 353, 358-359, 362-363, 369 abortion studies, 387 circulating antibodies, 390, 391 eosinophilic myositis induction, 387 haematological studies, 387 pathology, 386, 387

Cattle (cont.) serodiagnosis, 390, 391 toxoplasmid coccidiosis in, 314-31 5, 328, 333 circulating antibodies, 314 pathology, 315 tissue cyst inoculation, 214 Cercocebus atys, 334 Cercopithecus, 386 C. aethiops, 358 C. talapion, 383 Cervus canadensis, 367 C. elaphus, 367 Cestodes auxiliary hosts, 233-234 classification, 3 climatic zone occurrence, 28-37, 46-54, 72-80, 199-23 1 mid-latitude, 29-37, 47-54, 73-80, 204-221 more than one zone, in, 223-224 mountain, 37, 54, 80, 221-222 polar, 37, 54, 80, 221 sub-tropical, 28-29, 46, 72, 202-203 tropical, 28, 46, 72, 199-202 growth and maturation, 241-249 gravid worms, 246249 host body location, 231-233 intermediate hosts, 1 interspecific competition, 252-253 larval stages, 2 life cycle, 1 principal hosts, 233-234 seasonal occurrence, 1 et seq. abiotic factors, 249-252 biotic factors, 252-253 experimental studies, 255-256 hypothesis for, 254-255 incidence and intensity, 231-233 Chamois, 353, 366 Chickens, 334, 353, 368, 373 Chilu-Chor Chashma, Tadzhikstan, 159, 222 Chimpanzees, 359, 362 Chinchillas, 397, 400 Chirk Fish Hatchery, Clwyd, 92, 104 Chironomids, helminth parasites, 123 Chitaldrug District, Mysore, 134 Citrellus fulvus, 343, 368

S U B J E C T INDEX

Clarias batrachus, helminth parasites, 40 Clethriommys, 397 C. glareolus, 333, 374, 375 frenkeliosis in, 397, 400 Climatic zone occurrence, helminths mid-latitude, 204-221 desert, 2 19-220 east coast, 210-21 1 humid cool summers, 208-210 humid warm summers, 204-208 marine west coast, 21 1-217 semi-desert, 217 sub-polar, 220-221 more than one zone, in, 223-225 mountain, 221-222 polar, 221 ice caps, 221 sub-tropical, 202-203 humid, 203 Mediterranean, 202 tropical, 199-202 highland, 201 rainy, 200 savanna, 200-201 semi-desert, 201 Clostridium, 325 Coccidiomorpha, 41 1 Coccidium, 407 C . bigeminum var. putorii, 374 Columbian Park Lagoon, Lafayette,

160 Common buzzard, 296 Complement fixation test (CFT), 318, 319, 391 Congenital toxoplasmosis, 320 Contracaecum sp. climatic zone occurrence, 106, 109, 114, 202, 205, 209, 224 eggs, 123 gravid worms, 247 host species, 106, 109, 114 seasonal biology, 105, 123 C . aduncum, 105 C . bidentatum, 105, 123 temperature tolerance, 251 Corallobothrium sp. climatic zone occurrence, 73, 75, 205, 209 development stages, 71 ~

475

Corallobothrium sp. (cont.) gravid worms, 247, 248 host species, 73, 75 establishment period in, 240 incidence patterns, 81 life cycle, 81 procercoids, 71 seasonal biology, 71, 81-82 C .fimbriatum, 71 C. giganteum, 71 C . minutium, 71, 81 C . parafmbriatum, 81 C . parvum, 81 Coregonus albula, helminth parasites, 87,91 C . clupeaformis, helminth parasites, 42, 88,192 C. fera, helminth parasites, 100 C . lavaretus, helminth parasites, 100-101,222 C.nasus, helminth parasites, 221, 230 Corn meal disease, 342 Cortisone, 339 acetate, 333 Corynebacterium parvum, 323 Cottontail rabbits, 372, 373 Cottus gobio,helminth parasites, 195 Cotylodes, seasonal biology, 3-70 Cowbirds, 374 Coyotes, 353, 363 sarcosporidiosis in, 367 Creeks Buncombe, 157 Bushkill, Pennsylvania, 40 Johnson, New Hampshire, 126 Johnson County, Missouri, 179 Mud, Illinois, 184 Nose, 237 Cricetidae, 397 Ctenopharyngodon idella, helminth parasites, 43, 44,218 Cucullanidae, seasonal biology, 126-128 Cucullanus dogieli climatic zone occurrence, 109, 205 host species, 126 seasonal biology, 126 Cyathocephalidae. seasonal biology, 4022

476

SUBJECT INDEX

Cyathocephalus truncatus Cystidicoloides tenuissirna (cont.) abundance peaks, 42 invasion time, 239 annual cycle, 41 incidence patterns, 155, 156 climatic zone occurrence, 46, 47, 5 1, intermediate hosts, 156 life cycle, 155 53, 54, 202, 205, 208, 213, 220, 222, 223 seasonal biology, 155-1 57 egg development, 41 Cystoisospora, 404, 405 gravid worms, 246 Cystoisosporinae, 404 host species, 46, 47, 51, 53, 54 Cystoopsidae, seasonal biology, 105 establishment period in, 239, 240 Cystoopsis acipenseris infection resistance, 236 host body location, 231 incidence patterns, 41, 42 seasonal biology, 105 intermediate hosts, 42 Cytochalasin D, 312 life cycle, 41 morphology, 40 D procercoids, 41 ‘Dalmeny disease,’ 387 seasonal biology, 4 0 4 2 Dasyurid marsupials, 353 sexual maturation, 241 Deer mice, 381, 382, 389 temperature tolerance, 42 Degree-days concept, 251 Cyclops bicuspidatus, helminth parasites, Dentitruncus truttae 215 habitats, 164, 202 C. strenuus, helminth parasites, 67, 86 host species, 164 Cyprinids, helminth parasites, 11, 12 seasonal biology, 179-180 Cyprinus carpi0 Dichelyne sp. epizootics, 1I climatic zone occurrence, 109, 114, helminth parasites, 6, 8, 10, 12, 26, 115, 205, 209, 21 1 38,44, 210,218 gravid worms, 247 age dependent immunity, 11 host species, 109, 114, 115 immune response, 246 seasonal biology, 126 infection rate, 39 D. (Cclcullanellus)bullocki, 126 interspecific interactions, 253 D. (Cucullanellus) cotylophora, 126 seasonal burdens, 242 D. (Dichelyne) robustus, 126 pathogens, 10 Didelphis virginiana, 374 Cystidicolafarionis Digramrna interrupta, 252 climatic zone occurrence 114, 117, Diphyllobothrium sp., 243 122,209, 214, 220,224 Diplostomurn phoxini, 243 gravid worms, 247 Diptera, 345 host species, 114, 117, 122 Dnepr Delta, 12, 57, 86, 98, 103 establishment period in, 240 Dogs incidence patterns, 154 besnoitiosis in, 343 intermediate hosts, 154 isosporan coccidiosis in, 349, 350 seasonal biology, 154-1 55 Isopora heydorni-induced, 351, 352 Cystidicolidae, seasonal biology, oocysts excretion, 351 154-1 58 sarcosporidiosis in, 362-369 Cystidicoloides tenuissirna antibodies, 390, 394 climatic zone occurrence, 109, 115, avian species, 368 117, 119, 211, 214, 217, 224 bovine species, 362-363, 386, 387 generations, 156, 245 bubaline species, 363, 365 gravid worms, 248 canine-avian cycle species, 368-369 host species, 109, 115, 117, 119 caprine species, 365-366

S U B J E C T INDEX

Dogs (cont.) cervid species, 366-367 equine species, 368 gazelline species, 365 ovine species, 365 pathology, 389 porcine species, 368 rodent species, 368 toxoplasmid coccidiosis in, 334 Donkeys, 353 Dorosoma cepedianum, helminth parasites, 160 Ducks, 353, 369, 373 Dunnefjorden, Norway, 213

477

Echinorhynchus (cont.) E. salmonis, 190-192, 230 E. truttae, 192-195 shelled acanthors, 194 temperature tolerance, 194, 236 Eimeria, 294, 352, 392, 394 classification, 404 excystation, 405 host immune response, 306, 307, 394 host specificity, 395 life cycle, 395 phylogenetic relationships, 410 schizonts, 394 sexual differentiation, 304 taxonomy, 403,405 E E. acervulina, 405 East African game animals, 353 E. chinchillae, 405 Echinorhynchidae, seasonal biology, E. flavescens, 405 181-195 E. maxima, 394 Echinorhynchus sp. mutants, 305 climatic zone occurrence. 165. 167. sexual differentiation, 304 170, 171, 173-176,202, 206,207, E. necatrix, 306 210, 211, 216, 217, 221, 222, 224, E. nieschulzi, 306 230 E. tenella, 394 copulation, 194 classification, 404 development stages, 193, 194 mutants, 305 flow rates, mathematical model, 192 schizogony, 395 gravid worms, 248 sexual differentiation, 304 host species, 165, 167, 170, 171, sporozoites, 306, 307 173-176 Eimeriid coccidia, biology, 293 et seq. establishment period in, 236, 239, Eimeriidae, 403 240 Eimeriinae, 404 incidence patterns, 190 Elapid snakes, 353 dynamic equilibrium, 195 Elk, 353 intermediate hosts, 189, 190, 192, Endoparasite-host system, control 195, 236 mechanisms (model), 197 ' Endorimospora, 406 intraspecific crowding, 194 Enoplida, seasonal biology, 102-105 interspecific interactions, 253 larval invasion of fish, 235 Enzyme-linked immunosorbent assay life cycle, 192 (ELISA), 319, 391 maturation, 190, 245 circulating toxoplasmic antigen maturational migration, 249 detection, 320 mortality, 191 stick-ELISA technique, 320 population dynamics, mathematical Eoacanthocephalans model, 233 classification, 3 seasonal biology, 159-1 63, 177-1 79 seasonal biology, 189-195 Ephemeroptans, helminth parasites, E. baeri, 189 E. borealis, 189-1 90 152, 156 Equus caballus, 368 E. lateralis, 190

478

SUBJECT INDEX

Erimyzon oblongus, helminth parasites, 9, 25, 26 host sex influence, 244 interspecific interactions, 253 Esocinema bohemicum climatic zone occurrence, 109, 205 host species, 109 seasonal biology, 136 Esox americanus, helminth parasites, 21 1 E. lucius helminth parasites, 56-58, 59, 60-63, 94, 96, 101, 207, 218, 220, 221, 229, 232 long-term population studies, 253 maturation relationships, 244 pituitary gland secretion, 57 Estuarine amphipods, helminth parasites, 179 Eubothrium crassum climatic zone occurrence, 47-49, 51, 54, 205, 208, 209, 213, 220, 222, 223 gravid worms, 65, 248 host species, 47, 48, 49, 51, 54 establishment period in, 238, 239, 240 intermediate hosts, 65 life cycle, 64, 66 plerocerciforms, 65, 66 procercoids, 65, 70 seasonal biology, 64-67 freshwater race, 64-66 marine Atlantic race, 66 marine Pacific race, 66-67 E. rugosom climatic zone occurrence 48, 49, 5 1, 53,213, 220,223 host species, 48,49, 51, 53 seasonal biology, 67 E. salvelini climatic zone occurrence, 50, 51, 53, 54,208, 211, 220, 223 gravid worms, 246 host species, 50, 51, 53, 54 life cycle, 68, 70 long-term population studies, 253 procercoids, 68 seasonal biology, 67-70 American race, 68 freshwater European race, 67-68

Eucestodes, seasonal biology, 70-1 02 Eucoccidiorida, 403 Eucoccidium dinophili, 304 European wild cat, 333

F Falco tinnunculus, 378, 389 Falcons, 353 Fallow deer, 353 Felis catus sarcosporidiosis in, 373 toxoplasmid coccidiosis in, 330 F. concolor, toxoplasmid coccidiosis in, 330 F. Iybica, besnoitiosis in, 343 F. silvestris, toxoplasmid coccidiosis in, 333 Feral rodents, 353 Ferrets, 363, 373, 374 Fessisentidae, seasonal biology, 181 Fessisentis friedi climatic zone occurrence, 167, 206, 211, 225 host species, 167 seasonal biology, 181 Fifth International Congress of Protozoology, 408 Fish helminth parasites, 2, 85 immune response, 245,246 temperature-dependent rejection responses, 255 migration, 236 reproductive cycle initiation, 254 Fish farms Movanagher, County Antrim. '102 South Bohemian, 177 Foxes, 333, 353, 363 Frenkelia, 294,- 394 asexual development, 398, 400 classification, 404, 406 coccidiosis, 397402 cross reactions, 391, 401 cystozoites, 296, 375, 397, 399 final host immunity, 402 gametogony, 397 generic designation, 406 host immune response, 395 intermediate hosts, 400 life cycle, 295, 397-398, 400401 merozoites, 398

SUBJECT I N D E X

Frenkelia (cont.) phylogenetic relationships, 410 sexual cycle, 400 schizogony, 398, 399 specific designation, 409-410 sporocysts, 398, 399,400,402 taxonomy, 403 tissue cysts, 294, 397, 399 F. buteonis, 410 F. clethrionomyobuteonis,409 synonyms, 410 F. glareoli, 395, 397, 409 life cycle, 398, 399 synonyms, 410 F. microti, 395, 397, 400, 409 specific designation, 410 Frenkeliosis, 397-402 chemotaxonorny, 401 epizootiology, 402 life cycle, 397-401 pathology, 401 serology, 401 Freshwater fish, helminth parasites, 1 et seq. Fulton and Turk's direct agglutination technique, 318

G Gammaruspulex, helminth parasites, 41, 192, 193, 194, 216, 217, 235 interspecific interactions, 253 Gasterosteus aculeatus, helminth parasites, 88, 89, 90, 213 interspecific interactions, 253 maturation relationships, 244 Gazella granti, 365 Geese, 353 Genets, 386 Gerbils, 344 Glaridacris sp. climatic zone occurrence, 29, 32, 33, 203, 209,210, 223 annual cycle, 21 development stages, 20, 241 egg viability, 19 gravid worms, 20, 241, 248 host species, 29, 32, 33 establishment period in, 238, 239, 240 host sex influence, 244

479

Glaridacris sp. (cont.) immune response, 246 incidence patterns, 21 intermediate hosts, 19 interspecific interactions, 252, 253 larval development rate, 19 life cycle, 20 peak incidence, 21, 22 procercoids, 19, 22 seasonal biology, 19-22 G. catostomi, 19-21 G. confusus, 21 G. laruei, 21 G. vogei, 22 temperature tolerance, 22 Goats besnoitiosis in, 343 sarcosporidiosis in, 353, 365-366,388 sarcocysts, 365, 366 toxoplasmid coccidiosis in, 316-3 17 circulating antibodies, 317 congenital factors, 317 Gobio gobio, helminth parasites, 8 Goezia ascaroides climatic zone occurrence, 107, 202 host species, 107 establishment period in, 239 seasonal biology, 123 Golden finches, 346 Golden hamsters, 400 Gopher snakes, 38 1, 382 Goshawks, 375 Gracilisentis gracilisentis climatic zone occurrence, 167, 207 gravid worms, 247 host species, 167 establishment period in, 239 seasonal biology, 160 Grackles, 374, 392 Grant's gazelles, sarcosporidiosis in, 365, 369 Ground squirrels, 343 Guinea-pigs, 16 besnoitiosis in, 341 toxoplasmid coccidiosis in, 3 12, 313, 333 virulence, 312 Gulf of fin land,^ 185 Gymnocephalus cernua, helminth parasites, 214, 252

480

SUBJECT INDEX

H Habroleptoides modesta, helminth parasites, 151 Haemamoeba, 346 Haemogregariiza, 346 Hammondia classification, 404, 405, 406 synonyms, 404,406 taxonomy, 403,405 H. hammondi see Isopora datusi H. heydorni, 405 Hamsters besnoitiosis in, 337, 339, 340 immunity, 339 macrophage inhibition, 340 pathology, 341 toxoplasmid coccidiosis in, 323, 333 cell-mediated immunity, 324 Isopora datusi-induced, 334 macrophage inhibition, 323 Haplonema hamulatum climatic zone occurrence, 122, 220 host species, 122 seasonal biology, 128 Hares, 353 Hedgehogs, 343 Helminths auxiliary hosts, 233-234 climatic zone occurrence 1 et seq. acanthocephalans, 164-177, 199-231 Amphilinidea, 28-37, 199-231 Caryophyllidea, 28-37, 199-23 1 cestodes, 28-37, 46-54, 72-80, 199-23 1 incidence and intensity, 231-233 nematodes, 106-122, 199-231 Proteocephalidea, 72-80, 199-23 1 Pseudophyllidea, 46-54, 199-23 1 Spathebothridea, 46-54, 199-231 fish invasion, larvae, by, 234-240 gravid worms, 246-249 growth and maturation, 241-249 host body location, 231-233 interspecific competition, 252-253 laboratory studies, 255-256 long-term population studies, 253-254 principal hosts, 233-234 seasonal occurrence, 1 et seq. incidence and intensity, 231-233 world climatic zones, in, 199-231

Hepatozoon, 346 Heteroxenous coccidia, phylogenetic relationships, 410-41 1 Hodgkin's disease, 328 Hooghley Estuary, 159 Horses besnoitiosis in, 335 sarcosporidiosis in, 353, 368 toxoplasmid coccidiosis in, 318 Host species Amphilinidea, 28-37 acanthocephalans, 164-176 Caryophyllidea, 28-37 nematodes, 106-122 Proteocephalidea, 72-80 Pseudophyllidea, 46-54 Spathebothridea, 46-54 Host-parasite interactions, mathematical models, 233 Human beings, sarcosporidiosis in antibodies, 394 antigens, 390 bovine species, 358-359 circulating antibodies, 390 infection, 385 geographic range, 383 muscular, 383, 385 pathology, 389 porcine species, 359, 362 review, all known cases, of, 383 serodiagnosis, 390 sexual development, 358 sporocyst excretion, 389, 390 zoonotic infection, 383, 385 Human beings, toxoplasmid coccidiosis in acquisition sources, 331 antibodies, 330, 332 asymptomatic infection, 327, 329 cat-free areas, in, 331 cell-mediated immunity, 324, 325, 328 circulating antigens, 319, 328, 330 congenital infection, 327, 328 diagnosis, 319, 324, 328, 329 by computerized tomography, 329 direct contact infection, 328 dissemination, role of cats in, 329-332 foetal infection, 328 Hodgkin's disease, and, 328 horse riding patrons, in, 318, 331

SUBJECT INDEX

Human beings (cont.) host tissue reaction, 327 immune response, 326, 327 infection, 327 intra-uterine infection, 328 IQ impairment, 329 liver involvement, 328 macrophage inhibition, 325, 326 motor behaviour impairment, 329 oocyst role in, 331 phagocyte inhibition, 325 pathology, 327-329 protective immunity, 327 sera surveys, 330 transplacental transmission, 327 Hunterelfa nodulosa climatic zone occurrence, 33, 34, 37, 209, 210,223 gravid worms, 248 host species, 33, 34, 37 establishment period in, 238, 240 infection resistance, 237 larval development, 22 life span, 23 procercoids, 23 seasonal biology, 22-23 size classes, 23 Hyenas, 363 Hypentelium nigricans, helminth parasites, 24

I Ibex, 366 Icterid birds, 374 Illiosentidae, seasonal biology, 179-180 Immunoelectrophoresis, 3 19 Immunoglobulin IgM-IFA test, 318, 320 Impala, 335 Indirect haemagglutination test (IHA), 318, 390, 391 Indirect immunofluorescent antibody test (IFA), 318, 319, 389, 390, 391 Insular Newfoundland, 190 Interferon, 339 International Code of Zoological Nomenclature, 408 International Commission on Zoological Nomenclature, 406, 408

48 1

Iowa Falls, 5 Isoglaridacris s p . annual cycle, 24 climatic zone occurrence, 33, 34, 208, 209, 210, 219, 223 egg production, 23 gravid worms, 24, 247, 248 host species, 33, 34 establishment period in, 238, 240 incidence patterns, 23, 24 interspecific interactions, 252 maturation stages, 24 seasonal biology, 23-25 I . bulbocirrus, 23-24 I . folius, 24 I. Iongus, 24 I . wisconsinensis, 24-25 temperature tolerance, 25 Isopora classification, 404, 405, 406 oocyst excystation, 352 phylogenetic relationships, 410 synonyms, 295,404 taxonomy, 403 I . arctopitheci excystation, 352 oocysts, 352 reservoir hosts, 352 I. besnoiti, 410, 41 1 antelope strains, 336, 341 cultivation, 342 cystozoites, 341, 342 endozoites, 341, 342, 343 inhibition of host macrophages by, 323 reservoir hosts, 343 strains, 336 tissue cysts, 337, 338 transmission, 342, 343 vaccines against, 340 virulence, 341 I. bigemina, 409 development cycles, 351 oocysts, 295, 351 synonyms, 408 I . boughtoni, 374 I . burrowsi, 351 I . buteonis, 410 I. canaria, 410 classification. 405 life cycle, 346

482

SUBJECT INDEX

I. canis asexual development, 350 classification, 406 entero-epithelial stages, 350 excystation, 352 oocysts, 350 sporozoites, 310, 350 I. darlingi cats, in, 336 endozoites, 342 serology, 337 transmission, 342-344 virulence, 341 I. datusi, 332-335, 406, 410, 411 cross immunity, 323 cystozoites, 334 cysts, 299 development cycle in cats, 332, 333 gametogonic stages, 333 Hawaiian strain, 333, 334 intermediate hosts, 333, 334, 335 isolation, 334, 335 morphology, 335 synonyms, 332 I. endocalimici excystation, 352 sporocysts, 3 10 I. felis, 410 asexual development, 348 cats, in, 348 classification, 404, 405, 406 latent stages, 348 oocysts, 308, 348, 349 sporozoites, 405 I. frenkeli development stages, 348, 349 sporozoites, 349 I . gondii, 391, 41 1 cattle, in, 314-315 cell-mediated immunity against, 321, 322, 324 cross immunity, 323 cysts, in mice, 298 cystozoites, 298, 299, 300 development cycle in cats, 301-303 asexual division, 301 enteric development, 302 entero-epithelial stage, 303, 305-309

I . gondii (cont.) extra-intestinal pregametogonic stage (EIPS),301 faecal oocysts, 303 gametogonic stages, 302 oocyst ingestion, following, 303 schizogonic stages, 302 tissue cyst ingestion, following, 301-302 endozoites, 298,299, 311, 324 antigenic structure, 319 enteric development cycle, 297-301 excystation, 311, 352 gametogonic stages, 309 genetic research on, 305 horses, in, 318 life cycle, 303 lymphocyte-macrophage interaction in immunity against, 324 macrophage inhibition, 324 mutants, 305 oocysts, 298, 308, 314, 317, 318 feline faecal, 329, 330 pigs, in, 317, 318 sexual differentiation, 303 sporocysts, 396 strain virulence, 312, 313 pathogenesis, 313 I. hammondi, 406 I . heydorni classification, 405 development cycle, 351 excystation, 352 life cycle, 351 I. hominis, 409 I. idahoensis, 389 I. jellisoni cell-mediated immunity against, 339 cultivation, 342 endozoites, 342 hamsters, in, 339 inhibition of host macrophages by, 323, 340 serology, 337 tissue cysts, 337, 338 transmission, 342 I. lacazei, 346 development cycle, 346 merozoites, 346 oocysts, 346, 348

SUBJECT INDEX

I. neorivoita classification, 404 oocysts, 351 I. ohioensis classification, 404 hypnozoites, 350 life cycle, 350 oocysts, 349 sporozoites, 350 I. putorii, 374 I . rivoIta asexual development, 348 classification, 404 latent stages, 348 oocysts, 348, 349 I. serini, 404, 410 classification, 404, 405 merozoites, 341 oocysts, 346 I . vulpina classification, 404 oocysts, 351 I. wailacei endozoites, 344 gametocytes, 338, 344 isolation, 343 schizogonic stage, 338, 344 serology, 337 I . (Toxoplasma) datusi, 406 I. (Toxoplasma)gondii, 406 Isosporan coccidian parasites, extraintestinal stages with, 345-352 morphology, 346 Isoporid coccidia feline hosts, development in, 297-301 life cycle, 295 sexual differentiation, 303-305 Ixodid ticks, 345

J Jackals, 353 Jackson Cutoff, Ohio, 185 Japanese quail, 334 Jungle cats, 333 K Kangaroo rats, 336, 343 Kestrels, 372, 378, 389 Khavia sp. annual cycle, 38, 40

483

Khavia sp. (cont.) climatic zone occurrence, 30-35, 37, 208-210, 212, 217, 222, 223 gravid worms, 38, 247 host species, 30, 33, 34, 35, 37 establishment period in, 238, 239 incidence patterns, 39 intermediate hosts, 38 interspecific interactions, 253 procercoids, 38, 39 seasonal biology, 3 8 4 K. armeniaca, 38 K. iowensis, 38 K . sinensis, 38-39 Knots, 336 Korsak foxes, 343 Kudu, 335 Kwangtung Province, China, 203

L Lagomorphs, 333 Lakes Amu Darya Basin, 124, 189, 220 Babine, 68, 69, 221 Balaton, 86, 131, 139, 141, 142, 143 Billy, 81 Biwa, 96 Bogstad, 27, 60, 61, 62, 212 Carl Blackwell, 8 1, 126, 131, 150, 157, 158 Cold, 42, 88, 90, 154, 191, 192, 233 Crab Orchard, 160, 179 Cultus, 149 Dabie, 142, 143 Dargin, 94, 96, 130, 187 Decatur, 157 Druzno, 12, 26 Dusia, 86 Dvin-Velinsk, 125 Dzhapana, 202 Eagle Mountain, 150 Erie, 93, 96, 97, 132, 134, 251, 253 Fort Smith, 55, 85, 157 Frongoch, 177 Galstas, 131 Galwe, 94, 101 Geddes, 26 Goldapiwo, 91, 94 Gull, 83, 84, 181, 196, 208, 227 Horns, 102

484

SUBJECT lNDEX

Lakes (cont.) Lakes (cont.) Texoma, 9, 21, 157 Huron, 42, 145, 146 Track, 146 Kagwe, 104 Uros, 87 Kals, 14, 96 Ussuri, 189 Kamchatka area, 70 Vendursk, 87 Kivu, 201 Vbrtsjarv, 67, 124 Kok-Su, 220 Vyrnwy, 397 Konche, 27, 42, 67, 101, 105, 124, Wilno Region, 101 128, 130, 190,220 Yahara River, 55, 93, 126, 180 Konin region, Poland, 63, 143 Zaria, 159 Ladoga, 62, 87, 154, 189, 190, 219 Lampetra lamotteni, helminth parasites, Lakeview, 158 127 Lansk, 91 L. planeri, helminth parasites, 214, 215, Uman, 11, 57, 86, 88, 100, 102, 150 245 Lena, 189 Laurel Creek, Ontario, 138 Lesser Slave, 56, 58, 62, 63 Law of Priority, 409 Lucerne, 88 Lemmings, 397 Macha, 61, 96, 124, 136, 140, 187 Lepomis cyanellus, helminth parasites, Maggiore, 100, 204 188 Makpalkul, 220 L . macrochirus, helminth parasites, 162 Malaren, 14, 15, 205 Leptorhynchoides sp. Mamry Pblnocne, 94 climatic zone occurrence, 167, 170, Melingen, 42, 102, 221, 222 206, 210, 211 Mendota, 180 gravid worms, 248 Michigan, 21, 70, 88, 126, 189, 191 host species, 167, 170 Mun, 87 establishment period in, 239 Maruski, 91 life cycle, 180 Nedre Fipling, 42, 102, 221-222 seasonal biology, 180-1 81 Neuchbtel, 57, 62 L. plagicephalus, 180 Obelija, 131 L . thecatus, 180-1 8 1 Oneida, 55 Leptorhynchoididae, seasonal biology, Ontario, 93, 161, 190 180-181 Opeongo, 82, 83, 91, 92, 93, 126, 158, Lepus rolai, 343 227, 251 Lerceus lineatus, helminth parasites,. 0vre Heimdalsvatn, 102 185, 249 Oyeren, 182 Leuciscus cephalus, helminth parasites, Paleostomi, 104 11,98, 212 Pushaw, 21, 24, 196 immune response, 246 Raleigh, 4, 9, 25, 26 L . leuciscus, helminth parasites, 13, 15, Rangeley, 148 98, 212 Reryetjern, 130, 186 antibody resistance, 16 Sevan, 38, 189, 222 hormone influence, 244 Shlavantas, 131 infection resistance, 236 Shoecraft, 85 long-term population studies, 254 Skadar, 27, 91, 105, 123, 124, 142, Levinea, 405 195,202 Ligula intestinalis, 252 Skrwilno, 146 Limnodrilus sp., helminth parasites, 5, 6 Stevenson (near), 96 L. claparedeianus, 22 Shuttle, 163, 222 L. hofmeisteri, 7, 10, 19, 22, 23, 25 Syam, 151 Taimyr, 189 L . udekemianus, 19

SUBJECT INDEX

Lions, 333 Live-box tether experiments, 196 Lizards, 336 Llyn Celyn, Wales, 104 Llyn Tegid, Wales, 27, 55, 58-60, 26, 101, 104, 128, 130, 155, 158, 182-1 84 Loch Leven, 65, 105, 125, 253 Lota lota, helminth parasites, 42 Louping-ill virus, 325 Lower Volga Basin, 3 Lucioperca lucioperca, helminth parasites, 218 Lynx rufus, toxoplasmid coccidiosis in, 330 Lytocestidae, seasonal biology, 26-40 Lytocestus sp. climatic zone occurrence, 28, 200 host species, 28 incidence patterns, 40 intermediate hosts, 40 seasonal occurrence, 40

485

Mice (cont.) circulating antigens, 319 immune response, 313, 322, 323, 324, 326 immunotherapy, 322 Isospora datusi-induced, 333, 334 laboratory infection, 294, 295 learning ability impairment, 329 macrophage inhibition, 323, 324 nonspecific inhibition of tumour growth, 325 strain virulence, 312, 313 sarcospori diosis, 335 survival rate, 322 susceptibility, 313, 314 vaccine experiments, 326 vertical generation transmission, 328 Micropterus sp., 250 M. dolomieui, helminth parasites, 82, 83, 90, 91 M . salmoides, helminth parasites, 161, 162, 245 M Microtus, 345, 397 Macaca arctoides, 328, 386 M . agrestis, 333, 374, 397, 400, 401 M . fascicularis, 334, 383, 387 M. arvalis, 333, 343, 374, 375, 378, 380, M. irus, 362 382, 388,400,401 M. mulattu, 334, 362, 383, 385 M. erminea, 374 M. nemistrina, 386 M. lutreola, 374 Malham Tarn, Yorkshire, 65 M. torques, 336 Maribou, 345 Minks, 374 Marmosets, 341, 352 Molothrus uter, 374 Marsh rice rats, 332 Mongooses, 386 Marsupials, sarcosporidiosis in, 374 Monkey fibroblasts, toxoplasmic Mastomys, 313 endozoite culture in, 300 3‘-Methyl-dimethylaminoazo-benzene, Monkeys 325 sarcosporidiosis in, 385-386 Methylprednisolon acetate (MPA),307 toxoplasmid coccidiosis in, 334 Mice Monkton, County Durham, 163 besnoitiosis in, 336 Monobothrium sp. macrophage inhibition, 340 climatic zone occurrence, 31, 33, 34, pathology, 341 35, 204, 208, 210, 212, 223 isosporan coccidiosis in, 350 development stages, 241 sarcosporidiosis in, 353, 313, 376 embryonation, 25 toxoplasmid coccidiosis in, 297, 300, gravid worms, 247 301, 304, 332 host sex relationship, 26 age susceptibility, 326 host species, 31, 33, 34, 35 behavioural modification, 329 establishment period in, 239 cell-mediated immunity, 324, 325 host sex influence, 244 drug therapy, 322 invasion time, 238

486

SUBJECT INDEX

Monobothrium sp. (cont.) incidence patterns, 25, 26 intermediate hosts, 25 gravid worms, 25, 26 interspecific interactions, 253 length classes, 25 maturity groups, 25 procercoids, 25 seasonal biology, 6, 25-26 M. hunteri, 25 M. ingens, 25 M . ulmeri, 25-26 M. wageneri, 26 sexual development, 26 Moon rats, 379 Morelia spilotes variegata, 378 Morone chrysops, helminth parasites, 245 M. saxatilis, helminth parasites, 21 1 Moufflon, 353 Moxostroma sp., helminth parasites, 8, 24 Mule deer, 367, 388 Mules, 335 Multimammate rats, 400 Multiple myeloma, 328 Muridae, 397 Mus musculus, 335,373, 375 Musk rats, 397, 400 Mustela nivalis, 374 Mycobacterium tuberculosis, 323

N Naididae, helminth parasites, 123 Nematodes auxiliary hosts, 233-234 classification, 3 climatic zone occurrence, 106-122, 199-23 1 mid-latitude, 107-122, 204-221 more than one zone, in, 224 mountain, 122, 221-222 polar, 122,221 sub-tropical, 106, 202-203 tropical, 106-107, 199-202 gravid worms, 246-249 growth and maturation, 241-249 host body location, 231-233 host species, 106-122 intermediate hosts, 1

Nematodes (cont.) interspecific competition, 252-253 larval stages, 2 life cycle, 1 long-term population studies, 253-254 principal hosts, 233-234 seasonal occurrence, 1 et seq. abiotic factors, 249-252 Adenophorea subclass, 102-105 biotic factors, 252-253 experimental studies, 255-256 hypothesis for, 254-255 incidence and intensity, 231-233 Secernentea subclass, 105, 123-158 Neoechinorhynchidae, seasonal biology, 160-163, 177-179 Neoechinorhynchus SQ. annual population changes, 161 climatic zone occurrence, 164, 165, 167, 171, 173, 175, 176, 201, 203, 207, 210, 211, 216, 219, 221, 222, 225, 230, 231 development stages, 163 gravid worms, 247,248 host species, 164, 165, 167, 171, 173, 175, 176 establishment period in, 239, 240 host sex influence, 245 infection resistance, 237 invasion time, 238, 240 incidence patterns, 177 intermediate hosts, 161 interspecific interactions, 253 life cycle, 161, 162 maturation patterns, 161, 163, 178 population density, 162 recruitment patterns, 161, 162 seasonal biology, 160-163, 177-178 N . cylindratus, 160-162 N. rutili, 162-163, 177, 230-231 N. saginatus, 177-178 N. topseyi, 178 N . tumidus, 178 temperature tolerance, 162, 177 New World monkeys, 385 North Lanarkshire, Scotland, 213 Notechis ater, 381

SUBJECT INDEX

48 7

0 Paulisentis missouriensis Ocelots, 335 climatic zone occurrence, 168, 207 gravid worms, 248 Octospinifer sp. host species, 176 climatic zone occurrence, 21 1 establishment period in, 240 seasonal biology, 178 seasonal biology, 178-1 79 0. macilentis, 178 Penarchigetes sp. shelled acanthors, 178 climatic zone occurrence, 205 Odocoileus hemionus, 367 gravid worms, 248 Old World monkeys, 385 seasonal biology, 240 Oncorhynchusnerka, helminth parasites, Perca Bavescens, helminth parasites, 55, 68, 148, 149, 215,222 93, 190, 191,230 hormone influence, 245 spawning influence, 245 infection dynamics, 69 P. fluviatifis,helminth parasites, 58, 60, long-term population studies, 253 62, 86, 94, 101-102, 184, 186, 0. tshawytscha, helminth parasites, 191, 213,215, 252 230,245 interspecific interactions, 253 Ondatra, 345 long term population studies, 253 0 . zibethica, 343 maturation stages, 95 Opossums Peromyscus maniculatus, 335, 382 besnoitiosis in, 335, 336, 341, 343, Peyer’s patches, 306, 395 344 Philometra sp. sarcosporidiosisin, 374 annual cycle, 138, 139, 141, 142, 143 Oryctofagus cuniculi, 333, 373 auxiliary hosts, 234 Ostracods, helminth parasites, 160, 162 climatic zone occurrence, 107, 109, Owls, 353 110, 114, 116, 117, 119, 120, 122, sarcosporidiosisin, 375 202,206,209,211, 214,219,220, 221, 224, 229 P copulation, 140 Palaeacanthocephalans egg production, 142 classification, 3 gravid worms, 247,248 seasonal biology, 179-199 host body location, 231-232 Pallisentis (Farzandia) nagpurensis host-parasite relationships, 234 seasonal biology, 159-1 60 host species, 107, 109, 110, 114, 116, habitats, 200 117, 119, 120, 122 Papio cynocephalus, 359, 385 establishment period in, 238, 239, Par Pond, Savannah River Plant, 55, 240 84, 161, 162, 203,208,227 incidence patterns, 138, 140 Paraquimperia tenerrima interspecific interactions, 252 climatic zone occurrence, 109, 117, larval stages, 137, 138, 140, 141 205, 214, 224 life cycle, 137, 138, 141 host species, 109, 117 principal hosts, 234 seasonal biology, 128-129 seasonal biology, 137-143 Paratenuisentis ambiguus P. abdominalis, 137-1 38 climatic zone occurrence, 21 1 P . cylindracea, 138 seasonal biology, 179 P. fujimotoi, I39 Passer domesticus, 346 P. kotlani, 139-140 P. moprtanus, 343, 345 P. nodulosa, 140 Passerine birds, isosporan coccidiosis, P. obturans, 140-141,229 346, 347 P . ovara, 141-143, 229

488

SUBJECT INDEX

Philometra sp. (cont.) Pigs P. rischta, 143 toxoplasmid coccidiosis in, 313, Philometridae, seasonal biology, 317-318, 333 136-1 50 pathology, 3 17 sarcosporidiosis in, 352, 353, 359, Philometroides sp. 362, 368 climatic zone occurrence, 107, 111, pathology, 388 115, 117, 203, 206, 209, 214, 224 Plasmodium, 406 egg production, 146, 245 P. berghei, 324 development stages, 147 gravid worms, 247 P. gallinaceum, 304 growth, 245 P. y . yozlii, 313 host body location, 232 Platyhelminthes, 313 host species, 107, 111, 115, 117 Plecoglossus altivelis, helminth parasites, establishment period in, 238, 239 203 incidence patterns, 146 Polecafs, 374 infection dynamics, 147 Polymorphus minutus, 253 intermediate hosts, 145, 147 Pomphorhynchidae, seasonal biology, larval stages, 145, 146, 147 195-199 life cycle, 144, 145, 146 Pomphorhynchus sp. maturational migration, 249 annual calendar, 197 morphology, 144 climatic zone occurrence, 165, 168, seasonal biology, 144-148 171, 174-176, 202, 207,210, 211, P. carassii, 144 217, 219, 222, 225 P. cyyrini, 144-145 endoparasite-host system (model), P. huronensis, 145-146 197 P. sanguinea, 146-148 gravid worms, 248 taxonomy, 144 host reaction, 198 temperature tolerance, 144, 147 host species, 165, 168, 171, 174, 175, Philonema sp. 176 climatic zone occurrence, 116, 117, establishment period in, 236, 240 122, 211, 215, 221, 222, 224 immune response, 246 functional bursting, 149 incidence patterns, 233 gravid worms, 248 intermediate hosts, 196 host body location, 232 larval invasion of fish, 235 host species, 122 larval stages, 199 establishment period in, 239 long-term population studies, 254 invasive stages, 149, 150 mortality, 198 larval release, 245 population dynamics, 198 larval stages, 148, 149 principal hosts, 234 life cycle, 148 recruitment rate, 196 seasonal biology, 148-150 seasonal biology, 195-199 P . agubernaculum, 148 P. basniacus, 195 P . oncorhynchi, 148-150 P . bulbucolli, 196 P. sibrica, 150 P. Iaevis, 196-199 Phosphoglucomutase, 37 1 P. rocci, 199 6-Phosphogluconate dehydrogenase, shelled acanthors, 196, 197 371 temperature tolerance, 197, 236 Photoperiod, annual changes, 254 Pontoporeia offinis, helminth parasites, Pigeons, 334 221, 230, 236

489

SUBJECT INDEX

Poultry, sarcosporidiosis in, 368-369, 373 Precipitins, 246 Priddy Pool, Somerset, 183 Procamallanus sp. climaticzone occurrence, 106,200,201 host species, 106 seasonal biology, 135-136 P. clarias, 135 P . laeviconchus, 135-136 P. parvulus, 136 Proteocephalidea climatic zone occurrence, 72-80 mid-latitude, 73-80 mountain, 80 polar, 80 sub-tropical, 72 tropical, 72 evolutionary history, 70 host species, 72-80 seasonal biology, 70-102 Proteocephalus sp. annual cycle, 88 climatic zone occurrence, 72-80, 202-205,208-210,212,213, 218-220, 222-224, 227, 228 development stages, 82,87,90,98,241 egg viability, 91 genetic variation, 101 gravid worms, 88, 89, 92, 99, 247, 248 growth rates, 92, 93, 251 host species, 72-80, 90 host invasion period, 232 P. fluviatilis, 90-91 P. longicollis, 9 1 P. macrocephalus, 91 P. neglectus, 92 P . osculatus, 92 P. parallacticus, 92-93 P. pearsei, 93 P . percae, 93-96, 227-228 P. pinguis, 96 P. plecoglossi, 96 P. primaverus, 96-97 establishment period in, 238, 239,

Proteocephalus sp. (cont.) population dynamics, 99 incidence patterns, 84, 86, 88, 89, 93,94, 101, 232, 233 intermediate hosts, 82, 83, 86, 87, 91, 93,94 interspecific interactions, 253 juveniles, 102 life cycle, 82, 86, 91, 96 maturation stages, 94, 95 paratenic hosts, 92 plerocercoids, 83, 84, 85, 89,91, 92, 93 procercoids, 94, 97 seasonal biology, 82-102 P. arnbiguus, 82 P . ambloplitis, 82-85, 227 P. buplanensis, 85 P. cernua, 85-86 P. dubius, 86 P . esocis, 86 P. exiguus, 87-88 P. fallax, 88 P. jilicollis, 88-90 P. stizostethi, 97 P. tetrastomus, 97 P. torulosus, 97-99 P. tumidocollus, 99-100 sexual maturation, 93, 251, 252 temperature tolerance, 84, 85, 95, 99, 250,251, 252 Protozoans, 294 Psammoryctes barbatus, helminth parasites, 15 Pseudophyllidea climatic zone occurrence, 46-54 mid-latitude, 47-54 mountain, 54 polar, 54 sub-tropical, 46 tropical, 46 seasonal biology, 42-45, 55-70 Pumas, 333 Pyrenean cattle, besnoitiosis in, 335 Python reticulatus, 379

240

immune response, 246 infection resistance, 236 maturation relationships, 244

Q

Quadrigyridae, seasonal biology, 159-1 60

490 Quimperiidae, seasonal biology, 128-129 Quiscalus quiscula, 374

SUBJECT INDEX

Reservoirs Dubossary, 5, 126 Edgbaston, 88 Fern Ridge, 22 R Hanningfield, 65, 94, 95, 252 Ivan’kovsky, 209 Rabbits besnoitiosis in, 336, 340 Kanev, 56 pathology, 341 Lipno, 61 sarcosporidiosis in, 372-373, 393 Mingechaur, 92, 150, 219 toxoplasmid coccidiosis in, 313 Old, 181 macrophage inhibition, 326 Palisades, 148 vaccine experiments, 326 Rybinsk, 56, 61, 62, 86, 94, 98, 103, Raccoons, 363, 372 134, 182, 186 Raphidascaris acus Reticulated pythons, 379 climatic zone occurrence, 107, 115, Rhabdochona sp. age composition, 151 117, 120-122, 202,206,209, 214, 217, 219, 220, 224, 229 annual cycle, 150, 151, 152, 153 development stages, 124 climatic zone occurrence, 111, 112, gravid worms, 248 118, 120, 121, 206,214, 217, 219, host species, 107, 115, 117, 120, 121, 221, 224 122 gravid worms, 247, 248 establishment period in, 239, 240 host species, 111, 112, 118, 120, 121 infection resistance, 237 establishment period in, 239 invasion time, 239 incidence patterns, 150 spawning influence, 245 intermediate hosts, 151, 152 length range, 125 larval stages, 152 life cycle, 123 life cycle, 151, 152 long-term population studies, 253 maturational migration, 249 maturation period, 125 seasonal biology, 150-1 54 seasonal biology, 123-126 R. acuminata, 150 temperature tolerance, 236 R. cascadilla, 150 Rats R. decaturensis, 150 frenkeliosis in, 400 R. denudata, 150-151 sarcosporidiosis in, 353, 373 R. gnedini, 151 pathology, 388, 389 R. hellichi, 151-152 toxoplasmid coccidiosis in, 312, 333 R. phoxini, 152-1 53 immune response, 324 R. sulaki, 153 learning ability impairment, 329 Rhabdochonidae, seasonal biology, 150 macrophage inhibition, 324 Rhesus monkeys, 359 virulence, 313 Rhombomys opimus, 343 Rattus exulans, 344 Rice rats, 379 R. fusc@es, 378, 379 Rivers R. norvegicus, 344, 373, 379 Ain, 199 R. rattus, 335, 344 AIbarine, 199 R. rattus diardii, 379 Alyn, 42, 92, 128, 155 Red deer, 353, 367 Amur, 43, 56, 63 Reindeer, 335, 342 Anadry, 221 sarcosporidiosis in, 352 Avon, Hampshire, 13, 14, 98, 99, Reptiles, sarcosporidiosis in, 378-379, 196, 197, 198, 212, 234, 236, 254 381 Bosna, 41

SUBJECT INDEX

Rivers (cont.) Bow, 23 Bystrice, 124, 155, 156 Cedar, 24 Dabie, 99 Danube, 3, 55, 57, 86, 99, 102, 104, 105, 139, 140, 143, 152, 154, 180, 190 Dnepr, 12, 57, 86, 98, 103, 182, 186, 187, 190,233 Dniestr, 64, 195 Donets, 26 Duero, 27, 40, 104, 150, 217 Exe, 66 Fraser, 149 Glomma, 14, 190,212,215 Huron, 26 Illinois, 160, 179 Iowa, 6, 8, 9, 20, 23, 25, 38 Kentucky, 71 Kure, 219 Ledn Province, 157, 217, 219 Little, 157, 161 Little Sioux, 38 Lugg, 13,27, 98, 124, 212 Lupawa, 155 Nile, 135, 201 Oka, 58 Oyster, 177 Pike, 85, 188 Po, 195 Punkva, 189 Red Cedar, 7, 21, 22 Reda, 155 Rhine, 66 Rhone, 189 Rock, 71 RokytnB, 137 Sil, 27, 40, 104, 150, 217 South Platte (North Fork), 150 Stensan, 128 Stryi, 64 Syre, 195 Teify, 128 Tennessee, 26 Thames, 5 Tirino, 180, 202 Tisza, 64, 139, 140 Trino, 42, 128 Vltava, 61

49 1

Rivers (cont,) Volga, 10, 12, 57, 62, 92, 94, 103, 105, 126, 185, 189, 190, 219 Yenisei, 189, 221 Roe deer, 353 sarcosporidiosis in, 366-367 Rokytka Brook, Czechoslovakia, 138, 152, 153 Rooks, 343 Rutilus rubilio, helminth parasites, 27 R. rutilus, helminth parasites, 13, 27, 101, 142, 212, 218, 220 host sex influence, 244

S Sabin-Feldman dye test (SFT), 318-320 Saiga tatarica, 343 Salmo clarki, helminth parasites, 96, 97 S. gairdneri, helminth parasites, 100, 102,212 laboratory studies, 256 S . salar, helminth parasites, 220, 245 S . trutta, helminth parasites, 41, 42, 64, 65, 92, 102, 104, 155, 192, 193, 202,216, 222,245 host sex influence, 242 infection resistance, 236 long-term population studies, 253 migration and, 66 seasonal burdens, 242 spawning influence, 245 Saguinus nigricollis, 334 Salvelinus alpinus, helminth parasites, 41, 220, 221 S. narnaycush, helminth parasites, 92 S. oedipus, 385 Sarcocystidae, 403, 404 Sarcocystinae, 403, 404 Sarcocystis, 294, 397 antigens, 320 asexual development, 394 biology, 354 birds of prey, gametogony in, 375,378 Canidae gametogony, in 362-369 caninebovine species, 362-363,386, 387, 388 caninebubaline species, 363,365 canine-caprine species, 365-366, 388 canine-cervid species, 366367 canine-equine species, 368

492

SUBJECT INDEX

Sarcocystis (cont.) canine-gazelline species, 365 canine-ovine species, 365, 370, 388 canineporcine species, 368, 388 caninerodent species, 368 cell culture development, 391-392 circulating antibodies, 389 classification, 404, 406 coccidiosis, 352-396 epidemiology, 392, 394-396 epizootiology, 392, 394-396 final host, pathology in, 389 prevention, 396 cross reactions, 391, 401 development cycle, 358-382 excystation, 352 Felidae, gametogony in, 369-373 felineavian species, 373 felinebovine species, 369 feline-bubaline species, 369 feline-gazelline species, 369 feline-lagomorph species, 372-373 felineovine species, 370, 371-372 feline-porcine species, 372 feline-rodent species, 373 gametocytes, subepithelial development, 395-396 gametogony, 354, 386, 391, 395, 411 generic designation, 406 ‘hapantotypes’, 408 heteroxenous life cycle, 394-396 host immune response, 395 host specificity, 383, 386, 394 human-bovine species, 358-359 human-porcine species, 359, 362 intermediate host, pathology in, 386-389 intermediate host, development in, 355 known species, 354 life cycle, 295, 352, 354, 394-395 marsupial, gametogony in, 374 merozoites, 355 mustelids, gametogony in, 374 named species, 409 ‘neohapantotypes’, 408 phylogenetic relationships, 410 primates, gametogony in, 358-362 reptiles, gametogony in, 378-379, 381

Sarcocystis (cont.) sarcocysts, 355, 356,357,360 schizogony, 355,394 serodiagnosis, 389-391 sexual phase, 403 specific designation, nomenclatural problems, 406-409 sporocysts, 310, 354, 355, 394 excystation, 396 survival, 396 sporogony, 354 taxonomy, 354, 403 tissue cysts, 294 type species, 409 S. bertrami, 368, 409 S. bigemina, 409 S. booliati, 379 S. bovicanis, 409 S. bovifrlis, 409 S. bovihominis, 407, 409 S. capracanis, 366 S. capreolicanis, 367 S. cernae, 378-388, 391 gametocytes, 380 life cycle, 380 oocysts, 389 sarcocysts, 380, 382 schizonts, 380 sporocysts, 378, 381, 389, 396 S. citellivulpes, 368 S. clethrionomybuteonis, 407 S. cruzi, 390, 391, 394, 395, 408, 409 cystozoites, 389, 391 development cycle, 363 final hosts, 363 gametogony, 395 sarcocysts, 355, 356, 357, 363 schizonts, 363 sporogony, 363 sporozoites, 390 sporulation, 364 S. cuniculi, 390, 391, 394, 395 cystozoites, 393 gametogony, 372, 392 sarcocysts, 356, 361, 372, 393 sporocysts, 395 S.cymruensis, 373 S. debonei, 374, 383 sporocysts, 396

SUBJECT INDEX

S . dispersa, 375, 388 merozoites, 377 schizonts, 377 sporocysts, 376,377, 396 S. equicanis, 368,409 S. fayeri, 368 S. fusiformis, 369 specific designation, 407 S. gigantea, 332 cell culture, 392 cystozoites, 370, 371 gametogony, 392 macrocysts, 371 oocysts, 371 sarcocysts, 370, 371 sporocysts, 371 S. gracilis, 367 S. hemionilatrantis, 367, 388 S. hirsuta, 369, 391, 408,409 sarcocysts, 355, 357, 369 S. hominis, 391, 394, 409 gametogony, 359 oocysts, 359, 384 sarcocysts, 355, 357,360,384 sporocysts, 358, 389, 390 S. idahoensis, 381 merozoites, 382 oocysts, 382 S. kortei, 385 S. leporum, 373 S. levinei gametogony, 363 sarcocysts, 365 S. moulei, 366 S. lindemanni, 383 S. medusiformis, 312 S. miescheriana, 368, 388, 389, 406, 409 synonyms, 408 S. murinotechis, 381 S. muris, 373, 374, 409 cystozoites, 392 gametogony, 373 sarcocysts, 313 sporocysts, 373 S. nesbitti, 385 S. ovicanis, 409 S. ovifelis, 409 S . orientalis, 366 sarcocysts, 379 sporocysts, 379

S. oryzomyos, 319 S. proechimyos, 319 S. putorii gametogony, 374 sarcocysts, 356 sporocysts, 388, 395 synonyms, 374 S. scotti, 315 S. sebeki, 375, 388, 389, 391 cystozoites, 375 gametogony, 375 sarcocysts, 356, 361 sporocysts, 389 S. singaporensis, 379 cystozoites, 381 gametogony, 381 life cycle, 379 metrocytes, 381 sporocysts, 38 1, 389 S. suicanis, 409 S. suihominis, 389, 390 cystozoites, 392 development cycle, 359, 362 gametogony, 362 sarcocysts, 359 schizonts, 359 sporocysts, 388 S . tenella, 366, 409 cystozoites, 392 sarcocysts, 370 Sarcosporidiosis, 352-396 epidemiology, 392, 394-396 epizootiology, 392, 394-396 final host, pathology in, 389 intermediate host, pathology in, 386-389 muscular, 383-386 human, 383, 385 primates, in 385-386 carnivores, in, 386 prevention, 396 serodiagnosis, 389-391 Seas Azov, 126 Baltic, 66, 94, 154 Caspian, 126 Irish, 66 White, 66 Secernentea, seasonal biology, 105, 123-158

49 3

494

S U B J E C T INDEX

Second European Multicolloquium on Parasitology, 407 Semotilus atromacylatus, helminth parasites, 188, 210 interspecific interactions, 253 S. corporalis, helminth parasites, 245 Serinus cararius, 346 Serodiagnosis techniques for toxoplasmosis, 3 18-320 Servals, 345 Sheep besnoitiosis in, 335 sarcosporidiosis in, 353, 365, 371 pathology, 388 serodiagnosis, 391 toxoplasmid coccidiosis in, 31 5-31 6, 333 congenital factors, 315 genetic factors, 316 immune response, 325 ovine infection, 315, 316 pathology, 3 15, 3 16 Short-tailed voles, 397 Sika deer, 353 Silurotaenia siluri habitats, 204 seasonal biology, 102 Silurus glanis, helminth parasites, 219 Silver foxes, 351 Skin-sensitizing antibodies, 246 Skogsfjordvatnet, 67 Skrjabillanus scardinii climatic zone occurrence, 206 seasonal biology, 136 Spartoides wardi climatic zone occurrence, 209 gravid worms, 248 seasonal biology, 40, 240 Spathebothridea climatic zone occurrence, 46-54 mid-latitude, 47-54 mountain, 54 polar, 54 sub-tropical, 46 tropical, 46 seasonal biology, 40-42 Spinitectus sp. climatic zone occurrence, 107, 112, 115, 118, 121, 203, 206, 209, 214, 217, 224

Spinitectus sp. (cont.) gravid worms, 248 host species, 107, 112, 115, 118, 121 invasion time, 239 larval stages, 158 life cycle, 157 seasonal biology, 157-158 S . carolini, 157 S. gordoni, 157 S. gracilis, 157-158 S. inermis, 158 Spiny rats, 379 Spirurida, seasonal biology, 129-1 58 Sporozoasida, 403 Squirrels, 341 Sticklebacks, 91 Stoats, 374 Strix aluco, 375 Sungei Besar, Malaysia, 135 Sus scrofa domestica, 368 S . scrofa ferus, 368 Susliks, 343, 368 Sylvilagus floridanus, 372, 373 Synchitrium miescherianum, 409 T Taenia, 320 Tanaorhamphus longirostris climatic zone occurrence, 168, 207 gravid worms, 248 host species, 168 establishment period in, 239 invasion time, 238 seasonal biology, 179 Tawny owls, 375, 386, 389 Tenuisentidae, seasonal biology, 179 Third International Congress of Parasitology, 332 3H-Thymidine, 340 Tigers, 333 Tiger snakes, 381 Tinca finca, helminth parasites, 7 , 8, 26 Tissue cyst-forming coccidia, 293 et seq. families, 403-406 genera, 403-406 subfamilies, 403-406 taxonomy and nomenclature, current concepts, 403-410

SUBJECT INDEX

Toxoplmma, 294, 345, 346 classification, 404, 406 growth inhibiting factor, 324 life cycle, 295 tissue cysts, 294 synonyms, 295, 404 taxonomy, 403 T. gondii, see Isospora gondii Toxoplasmatidae, 403 Toxoplasmatinae, 403, 404 Toxoplasmic lysate antigen, 324 Toxoplasmid coccidia, 296-332 cattle, in, 314-315 farm animals, in, 314-318 feline faecal transmission, 296 feline hosts, development in, 297-301 Isospora gondii development, 301-303 pathology, 309-310 genetic research, 305 goats, in, 316-317 horses, in, 318 host cell penetration, 31 1-312 host susceptibility, 312 inhibition of host macrophages, 323 inhibitory effects on tumour growth, 325 intermediate host, immunity in, 321-326 cell-mediated response, 321, 322, 324, 325 endozoite proliferation, 321 humoral response, 321, 322, 326 macrophages inhibition, 323, 324 OOCyStS, 310-31 1 dispersal, 310 excystation, 310-31 1 sporulation, 310 structure, 310-31 1 survival, 310 pigs, in, 317-318 serological diagnosis, 318-320 sexual differentiation, 303-305 sheep, in, 315-316 strain virulence, 312-3 14 pathogenetic mechanism, 313 vaccine development, 326 ToxopIasmosis, 294, 296-332 human, 327-332

49 5

ToxopIasmosis (cont.) cats, role in dissemination, 329-332 pathology, 327-329 Transversotremapatialense, 256 Trematodes, 256 Triaenophoridae, seasonal biology, 5664 Triaenophorus sp. annual growth patterns (histogram), 59

climatic zone occurrence, 48-50, 52-54,202, 205, 209, 213, 218-221, 224, 228 development stages, 56, 58-60, 61, 241, 242 distribution patterns, 58 egg release, 56, 57, 58, 251 embryonic development, 56 genital development, 58, 59, 60 gravid worms, 56, 58, 60, 62, 63, 247 growth, 62, 251 host species, 48, 49, 50, 52, 53, 54 establishment period in, 238, 240 immune response, 62 infection resistance, 237 invasion period, 232 maturation relationships, 244 incidence patterns, 57, 58, 60, 233 larval invasion of fish, 235 length groups, 58, 59, 61 plerocercoids, 58, 60, 62 procercoids, 58 proglottids, 60 seasonal biology, 56-64 T. amurensis, 56 T. crassus, 56-57 T. meridionalis, 57 T. nodulosus, 57-63, 228 T. orientalis, 63 T. stizostedionis, 63 sexual differentiation, 62 sexual maturation, 56-57, 59, 60-63, 25 1 strobilization, 58, 60 temperature tolerance, 62, 63, 228, 250, 251 Tripol’ye Power Plant, 55-56 Trivandrum, Kerala, 159 Trout Brook, New Brunswick, 156

496

SUBJECT INDEX

Truttaedacnitis sp. climatic zone occurrence, 107, 113, 115, 118, 121, 202, 206, 214, 215, 219,224 gravid worms, 248 host species, 107, 113, 115, 118, 121 intermediate hosts, 126 larval stages, 127 life cycle, 126, 127 maturation, 245 seasonal biology, 126-128 T. sphaeuocephala, 126 T. stelmioides, 126-128 T. truttae, 128 Trypanosoma, 406 Tubifex sp. helminlh parasites, 8 seasonal biology, 9 T. barbatus, 12 T. templetoni, 19, 22 T. tubifex, 10-12, 19 Tubificids, helminth parasites, 8, 9 Tubificidae, helminth parasites, 123 Turkeys, 353 Tyto alba, 315, 316 T. novaehollandiae, 375 U Ukraine, 19, 20, 38, 45 fish farms, 7, 10, 39, 43

V Varicorhinus capoeta sevangi, helminth parasites, 222 Viperid snakes, 386 Virginian deer, 353 Voles, 374 frenkeliosis in, 397, 398, 399, 400 Vulpus corsac, 368 V. vulpus, 368 Vultures, 345

W Wallaby, 353 Water buffaloes, 363, 369 Water voles, 397 Weasels, 372 sarcosporidiosis in, 374, 386, 388, 395 Whales, 386 White-footed mouse, 335 White mice, 343 White-tailed deer, 353 Wild boar, 353, 359 Wildebeest, 335, 340 Wolves, 343, 353 sarcosporidiosis in, 368

Z Zooplankton, 85, 97

Cumulative Index of Titles Anisakis and Anisakiasis, 16, 93 Arrested Development of Nematodes and some related Phenomena, 12, 280 Aspects of Acanthocephalan Reproduction, 19, 73 Aspects of the Host-Parasite Relationship of Plant-Parasitic Nematodes, 13, 225. Aspidogastrea, especially Multicotyle purvisi Dawes, 1941, 10, 78 Avian Blood Coccidians, 10, 1 Babesiosis : Non-specific Resistance, Immunological Factors and Pathogenesis, 17, 49 Behavioural Analysis of Nematode Movement, 13, 7 1 Biological Aspects of Trypanosomiasis Research, 3, 1 Biological Aspects of Trypanosomiasis Research, 1965; a Retrospect, 1969, 8, 227 Biological and Distribution of the Rat Lungworm, Angiostrongylus cantonensis, and its Relationship to Eosinophilic Meningoencephalitis and other Neurological Disorders of Man and Animals, 3, 223 Biology of the Acanthocephala, 5, 205, 11, 671 Biology of the Hydatid Organisms, 2, 169, 7, 327 Biology of Nanophyetus sulmincola and “Salmon Poisoning” Disease, 8, I Brugian Filariasis : Epidemiological and Experimental Studies, 15, 244 Carbon Dioxide Utilization and the Regulation of Respiratory Metabolic Pathways in Parasitic Helminths, 13, 36 Caryophyllidea (Cestoidea) : Evolution and Classification, 19, 139 Cell-Mediated Immunity Against Certain Parasitic Worms, 13, 183 Chagas Disease and Chagas Syndromes: The Pathology of American Trypanosomiasis, 6, 63 Circadian and other Rhythms of Parasites, 13, 123 Clonorchis and Clonorchiasis, 4, 53 Coccidia and Coccidiosis in the Domestic Fowl and Turkey, 1, 67 Coccidia and Coccidiosis in the Domestic Fowl, 6, 313 Conception and Terminology of Hosts in Parasitology, 14, 1 Control of Arthropods of Medical and Veterinary Importance, 11, 115 Copepoda (Crustacea) Parasitic on Fishes : Problems and Perspectives, 19, 1 Cultivation Procedures for Parasitic Helminths, 3, 159 Cultivation Procedures for Parasitic Helminths : Recent Advances, 9, 227 Current Concepts on the Biology, Evolution and Taxonomy of Tissue Cystforming Eimeriid Coccidia, 20, 293 497

498

C U M U L A T I V E I N D E X OF TITLES

Dracunculus and Dracunculiasis, 9, 73 Dynamics of Parasitic Equilibrium in Cotton Rat Filariasis, 4, 255 East Coast Fever: Some Recent Research in East Africa, 15, 83 Ecological and Physiological Aspects of Helminth-Host Interactions in the Mammalian Gastrointestinal Canal, 12, 183 Electron Transport in Parasitic Helminths and Protozoa, 8, 139 Embryogenesis in Cestodes, 4, 107 Epidemiology of Amoebiasis, 6, 1 Epidemiology of Babesial Infections, 17, 1 15 Epidemiology and Control of Some Nematode Infectionsof Grazing Animals, 7, 211, 14, 355 Evolutionary Trends in Mammalian Trypanosomes, 5, 47 Epidermis and Sense Organs of the Monogenea and Some Related Groups, 11, 193 Experimental Chemotherapy of Sclzistosomiasis mansoni, 6, 233, 12, 369 Experimental Epidemiology of Hydatidosis and Cysticercosis, 15, 3 12 Experimental Fascioliasis in Australia, 7, 96 Experimental Research on Avian Malaria, 1, 1 Experimental Studies on Entamoeba with Reference to Speciation, 4, 1 Experimental Trichiniasis, 1, 213, 6, 361 Fascioliasis: the lnvasive Stages of Fusciola hepatica in Mammalian Hosts, 2, 97 Fascioliasis: the Invasive Stages in Mammals, 8, 259 Feeding in Ectoparasitic Acari with Special Reference to Ticks, 3, 249 Fine Structure of the Monogenea especially Polystomoides Ward, 13, 1 Functional Morphology of Cestode Larvae, 11, 396

Giardia and Giardiasis, 17, 1 Genetic Control of Susceptibility and Resistance to Parasitic Infection, 16, 219 Global Problems of Imported Disease, 11, 75 Hookworm Infection in Man, 17, 315 Host-Parasite Interface of Trematodes, 15, 201 Host-Parasite Relationshipsin the Alimentary Tract of Domestic Birds, 14,96 Host-Parasite Relationships of Plant-Parasitic Nematodes, 7, 1 Host Specificity and the Evolution of Helminthic Parasites, 2, 1 Immunity to Ticks, 18,293 Immunity to Trypanosoma Cruzi, 18, 247 Immunology of Schistosomiasis, 7, 41, 14, 399 Industrial Development and Field Use of the Canine Hookworm Vaccine, 16, 333 Infectious Process, and its Relation to the Development of Early Parasitic Stages of Nematodes, 6, 327

C U M U L A T I V E INDEX O F T I T L E S

499

Infective Stage of Nematode Parasites and its Significance in Parasitism, 1, 109 Intramolluscan Inter-trematode Antagonism: a Review of Factors Influencing the Host-Parasite System and its Possible Role in Biological Control, 10, 192 Larvae and Larval Development of Monogeneans, 1, 287, 6, 373 Leishmania, 2, 35 Liver Involvement in Acute Mammalian Malaria with Special Reference to Plasmodium knowlesi Malaria, 6, 189 Lungworms of the Domestic Pig and Sheep, 11, 559 Malaria in Mammals Excluding Man, 5, 139 Metabolism of the Malaria Parasite and its Host, 10, 31 Meteorological Factors and Forecasts of Helminthic Disease, 7, 283 Nematode Sense Organs, 14, 165 New Knowledge of Toxoplasma and Toxoplasmosis, 11, 631 Numerical Analysis of Enzyme Polymorphism; A New Approach to the Epidemiology and Taxonomy of the Subgenus Trypanozoon, 18, 175 Onchocerciasis, 8, 173 Ontogeny of Cestodes and its Bearing on their Phylogeny and Systematics, 11,481 Paragonimus and Paragonimiasis, 3, 99, 7, 375 Paramphistomiasis of Domestic Ruminants, 9, 33 Parasitic Bronchitis, 1, 179, 6, 349 Parasitism and Commensalism in the Turbellaria, 9, 1 Pathogenesis of Mammalian Malaria, 10, 49 Phylogeny of Life-cycle Patterns of the Digenea, 10, 153 Physiological Aspects of Reproduction in Nematodes, 14, 268 Post-embryonic Developmental Stages of Cestodes, 5, 247, 11, 707 Problems in the Cultivation of some Parasitic Protozoa, 5, 93 Prospects for the Development of Dead Vaccines against Helminths, 16,165

Recent Advances in Antimalarial Chemotherapy and Drug Resistance, 12,69 Recent Advances in the Anthelmintic Treatment of the Domestic Animals, 2,221 Recent Experimental Research on Avian Malaria, 6,293 Recent Research on Malaria in Mammals Excluding Man, 11, 603 Regulation of Respiratory Metabolism in Parasitic Helminths, 16, 31 1 Relationships between the Species of Fasciola and their Molluscan Hosts, 3, 59, 8, 251 Relationship between Circulating Antibodies and Immunity to Helminthic Infections, 8, 97

500

C U M U L A T I V E I N D E X O F TITLES

Role of Tick Salivary Glands in Feeding and Disease Transmission, 18, 315 Sarcosporidia (Protozoa, Sporozoa): Life Cycle and Fine Structure, 16, 43 Schistosoma mansoni: Cercaria to Schistosomule, 12, 115 Schistosomiasisand the Control of Molluscan Hosts of Human Schistosomes with Particular Reference to Possible Self-regulatory Mechanisms, 11, 307 Seasonal Occurrence of Helminths in Freshwater Fishes, Part I, Monogenea, 15, 133; Part 11, Trematoda, 17, 141; Part 111, Larval Cestoda and Nematoda, 18, I ; Part IVYAdult Cestoda, Nematoda and Acanthocephala, 20, 1. Snail Control in Trematode Diseases : the Possible Value of Sciomyzid Larvae Snail-Killing Diptera, 2, 259 Snail Problems in African Schistosomiasis, 8, 43 Some Tissue Reactions to the Nematode Parasites of Animals, 4, 321 Speciation in Parasitic Nematodes, 9, 185 Species of Leucocytozoon, 12, 1 Structure and Composition of the Helminth Cuticle, 4, 187 Structure of the Helminth Cuticle, 10, 347 Taeniasis and Cysticercosis (Taenia saginata), 10, 269 Taxonomy and Transmission of Leishmania, 16, 1 Tick Feeding and its Implications, 8, 275 Toxoplasma and Toxoplasmosis, 5, 1 Trichomonas vaginalis and Trichomoniasis 6, 1 17 Trypanosomes of Anura, 11, 1 Ultrastructure of the Tegument of Schistosoma, 11, 233 Vaccination Against the Canine Hookworm Disease, 9, 153 Vector Relationships in the Trypanosomatidae, 15, 1 Veterinary Anthelmintic Medication, 7, 350

Cumulative Index of Authors A

Donnelly, J., 17, 115

Adler, S., 2, 35 Alicata, J. E., 3, 223 Anya, A. O., 14,268 Arthur, D. R., 3, 249, 8, 275

E Elsdon-Dew, R., 6, 1 Erasmus, D. A., 15, 201 F

B

Fallis, A. M., 12, 1 Fletcher, A., 10, 31, 49 Freeman, R. S., 11, 481

Baker, J. R., 10, 1 Bardsley, J. E., 11, 1 Beesley, W. N., 11, 115 Bennett, G. F., 10, 1 Berg, C. O., 2, 259 Berrie, A. D., 8, 43 Bertram, D. S., 4, 255 Binnington, K. C., 18, 315 Bishop, A., 5, 93 Boray, J. C., 7, 96 Brener, Z., 18, 247 Brocklesby, D. W., 17, 49 Bruce-Chwatt, L. J., 11, 75 Bryant, C., 8, 139, 13, 36, 16, 31 1

G Garnham, P. C. C., 5, 139, 11,603 Gemmel, M. A., 15, 312 Gibson, W. C., 18, 175 Gibson, T. E., 2, 221, 7, 350 Godfrey, D. G., 18, 175 H

C

Cameron, T. W. M., 2, 1 Chubb, JI C., 15, 133, 17, 141, 18, 1, 20, I Clark, G. W., 10, 1 Clegg, J. A., 16, 165 Coleman, G. S., 18, 121 Croll, N. A., 13, 71 Crompton, D. W. T., 14, 96, 19, 73

D Dawes, B., 2, 97, 8, 259 Denham, D. A., 15,244 Desser, S. S., 12, 1 De Vasconcellos Coelho, M., 16, 1

Hansen, E. L., 9, 227 Harmsen, R., 11, 1 Hawking, F., 13, 123 Heydorn, A. O., 16,43 Hevneman, D., 10, 192 Hoare, c*A*, 5, 47 Hockley, D. J., 11, 233 Horak, I. G., 9, 33 Horton-Smith, C., 1, 67, 6, 313 Huff, C. G., 1, 1, 6, 293 Hughes, D. L., 2, 97, 8, 259

I Inglis, W. G., 9, 185

J Jacobs, L., 5, 1, 11, 631 Jennings, J. B., 9, 1 501

502

C U M U L A T I V E I N D E X OF AUTHORS

Jirovec, O., 6, 117 Johnstone, P. D., 15, 312 Joyner, L. P., 17, 1 1 5 K Kabata, Z., 19, 1 Katz, N., 6, 233, 12, 369 Kemp, D. H., 18, 315 Kendall, S. B., 3, 59, 8, 251 Khan, R. A., 12, 1 Knapp, S. E., 8, 1 Koberle, F., 6, 63 Komiya, Y., 4, 53

Laarman, J. J., 20,293 Laird, M., 10, 1 Larsh, J. E., Jr., 1,213,6,361,13,183 Lee, D. L., 4, 187, 10, 347 Lim, H. K., 10, 192 Llewellyn, J., 1, 287, 6, 373 Long, P. L., 1, 67, 6, 313 Lumsden, W. H. R., 3, 1, 8, 227 Lyons, K. M., 11, 193

M McGreevy, P. A., 15, 244 McLaren, D. J., 14, 195 Mackiewicz, J. S., 19, 139 Maegraith, B., 6, 189, 10, 31, 49 Marshall, T. F. DE. C., 18, 175 Mehlhorn, H., 16, 43 Mettrick, D. F., 12, 183 Meyer, E. A., 17, 1 Michel, J. F., 7, 211, 12, 280, 14, 355 Millemann, R. E., 8, 1 Miller, T. A., 9, 153, 16, 333, 17, 315 Molyneux, D. H., 15, 1 Muller, R., 9,73

N Neal, R. A., 4, 1 Nelson, G. S., 8, 173 Nesheim, M. C., 14,96

Nicholas, W. L., 5, 205, 11, 671

0 Odening, K., 14, 1 Ollerenshaw, C. B., 7, 283 P Parshad, V. R., 19, 73 Pawlowski, Z., 10, 269 Pearson, J. C., 10, 153 Pellegrino, J., 6, 233, 12, 369 Peters, W., 12, 69 PetrB, M., 6, 117 Podesta, R. B., 12, 183 Poynter, D., 1, 179, 4, 321, 6, 349 Purnell, R. E., 15, 83 R Radnlescu, S., 17, 1 Rogers, W. P., 1, 109, 6, 327 Rohde, K., 10, 78, 13, 1 Rose, J. H., 11, 559 Rybicka, K., 4, 107 S Schultz, M. G., 10, 269 Silverman, P. H., 3, 159, 9, 227 Sinclair, 1. J., 8, 97 slais, J., 11, 396 Smith, J. W., 16, 93 Smith, L. P., 7, 283 Smith, M. A., 16, 165 Smithers, S. R., 7, 41, 14, 399 Smyth, J. D., 2, 169, 7, 327 Sommerville, R. I., 1, 109, 6, 327 Stirewalt, M. A., 12, 115 T Tadros, W., 20,293 Terry, R. J., 7,41, 14, 399 Thomas, J. D., 11, 307 V

Voge, M., 5, 247, 11, 707

503

CUMULATIVE INDEX OF AUTHORS

Y

W

Wakelin, D., 16, 219 Weatherly, N. F., 13, 183 Webster, J. M., 7, 1, 13, 225 Willadsen, P., 18, 293 Williams, P., 16, 1 Wootten, R., 16,93

Yokogawa, M., 3,99,7, 375 Z Zwart, D., 17, 49

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