Seasonal Occurrence of Helminths in Freshwater Fishes Part II. Trematoda*

Seasonal Occurrence of Helminths in Freshwater Fishes Part 11. Trematoda* JAMES C. CHUBB

Departmetit of Zoology, University of Liverpool, Liverpool L69 3BX, Etiglatid Introduction ............................................................... Classification of Trematodes.. .................... Seasonal Studies of Metacercariae ................................. IV. Seasonal Studies of Metacercariae in World Climatic Zones ... ............................... A. Tropical .... B. Subtropical ........................... ........ .... C . Mid-latitude ......................................................... D. Polar .................................................................. E. Mountain ............................... F. Species Studied in more than one V. General Conclusions, Metacercariae .............................. ...... A. Incidence and intensity of Occurrence ... .... .... . ................ ... . _... _ ...... B. Principal and Auxiliary Hosts ................................. shes by by Cercariae Cercariae .............................. . .................. C. Invasion of Fishes ....... .................. D. Formation of Metacercariae .................................... ....... .........._....... E. MorphologicalI Differences ................ F. Longevity .................... G . Disappearance of Heavily H . Sporadic Population Changes ................................. ............... I . Seasonal Studies in World Climate Zones .................. ............... J . An Hypothesis for Seasonal Occurrence. K. Experimental Studies ..... .............................. VI. Seasonal Studies of Adult Treniato

I.

11. 111.

C. Subclass Digenea .................... .................... VII. Seasonal Studies of Adult Trematodes rld Climatic Zo A. Tropical ......... B. Subtropical .............................. .................... C . Mid-latitude ..................................... ................................................... D. Polar ........... .............................. E. Mountain ............................... .............................. F. Species Studied in more than one Climate Zonee ......... VIII. General Conclusions, Adult Trematodes ........................ ......................... A. Incidence and lntensity of Occurrence ... .... B. Principal and Auxiliary Hosts ................................. C. Invasion of Fishes ......... .................................

142 143 144 191 191 191

192 199 200 200 202 202 205 205 209 210 210 21 1 212 212 213 21 3 215 215 215 216 264 264 265 266 210 210 210 216 216 283 284

* This review will be completed by Part 111 to appear in “Advances in Parasitology” Vol. 18. 141

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D. E. F. G. H. I. J.

Maturation of Trematodes ......................................................... Abiotic Factors ........................................................................ Biotic Factors ........................................................................... Long-term Population Changes ................................................... Seasonal Studies in World Climatic Zones ....................................... An Hypothesis for Seasonal Occurrence.. ........................................ Experimental Studies in Controlled Conditions ................................. References ..............................................................................

286 290 290 29 1 292 292 295 296

I. INTRODUCTION It was originally hoped to consider the trematodes, cestodes, nematodes and acanthocephalans in one article, but in the event the amount of literature rendered this impossible within the time available. Accordingly this part of the review is limited to the Class Trematoda and the third part will cover the remaining groups. Most members of the Subclass Aspidogastrea have a direct life cycle without intermediate hosts. The incomplete knowledge of the life cycles of the Subclass Didymozoidea also suggests that development is direct without an intermediate host. The lifz cycles of the Subclass Digenea normally require one or two intermediate hosts. The variety of life cycles that have been described for digeneans are reviewed by Heyneman (1960). Of the species of digeneans considered here, the metacercariae in fishes are normally in the second and last intermediate host and the adult worms in fishes are in the definitive host. The terms used follow the style of the first part of this review (Chubb, 1977). Tncidence refers to percentage infection of the fish hosts and intensity of infection to the numbers of parasites found on or in each host. The maturation of the adult trematodes is normally described by the division of what is a continuous process into a number of relatively discrete stages which are used to define the state of development achieved in relation to time. The term invasion is used to describe the actual process of acquisition of the parasites by the host. In an ideal study of the host-parasite relationship the fishes should be divided into age classes and length groups because parasitization is not uniform through the population. However, this ideal is achieved relatively infrequently. As is discussed in the body of the review the absence of such information can weaken explicit assessment of data for incidence and intensity of infection Section I1 of the review outlines the arrangement of the families. Sections 111-V consider the seasonal occurrence of metacercariae and Sections VIVIII that of adult trematodes in fishes. There are marked differences in the biology of the two stages as the fishes are intermediate hosts for metaceicariae and definitive hosts for adult trematodes. Section 111 reports the seasonal studies of metacercariae and Section VI the seasonal studies of adult trematodes. These sections aim to summarize the relevant information and to be as comprehensive as possible. Unfortunately, material has been omitted for two reasons: literature was not available

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al the time the review was written, 01 through ignorance of the publication by the author. It is hoped that a reasonable cover of the literature has been achieved. Section IV for metacercariae and Section VII for adult trematodes relate the seasonal studies to the major climatic zones of the world. Sections V (metacercariae) and VIII (adult trematodes) have the aim of gatheling together the current knowledge into meaningful conclusions and to recommend areas where further information could be collected to assist our understanding of the seasonal dynamics of the trematodes. 11. CLASSIFICATION OF TREMATODES

Owing to the great diversity of form, the finding of many undescribed species each year and an incomplete knowledge of life cycles the classification of the trematodes is in an unstable state, especially at the higher levels. Accordingly the present account treats seasonal occurrence under families as listed below. Species are in alphabetical order. The data for metacercariae are in Section I l l and for adults in Section VI. Class Trematoda Subclass Aspidogastrea Family Aspidogastridae (Section VI) Subclass Didymozoidea Family Didymozoidae (Section VI) Subclass Digenea Family Allocreadiidae (Section VI) Azygiidae (Section VI) Bucephalidae (Sections I11 and VI) Bunoderidae (Section V1) Clinostomatidae (Section 111) Cryptogonimidae (Section VI) Cyathocotylidae (Section 111) Diplostomatidae (Section 111) Echinostomatidae (Section I l l ) Fellodistomatidae (Section VI) Gorgoderidae (Section VI) Halipegidae (Section VI) Hemiuridae (Section V1) Heterophyidae (Section 111) Lecithasteridae (Section V1) Lissorchidae (Section VI) Monorchidae (Section VI) Nanophyetidae (Section 111) Opecoelidae (Section VI) Opisthorchidae (Section I I I ) Orientocreadiidae (Section VI) Paramphistomidae (Section VI) Plagiorchidae (Section V1) Prohemistomatidae (Section 111)

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Sanguinicolidae (Section VI) Strigeidae (Section Ill) Transversotrematidae (Section VI) Walliniidae (Section V1) 111. SEASONAL STUDIES OF METACERCARIAE

1. Family Bucephalidae

Baturo (1977) experimentally demonstrated the life cycles of the two bucephalid species and found that the cercaria originally described by Baer (1827) as Bucephaluspolymorphus and up to the present time regarded as the cercaria of the fish trematode known by the same name, was in fact a larval stage of Rhipidocotyle illense. This fact created a complex problem of taxonomy and synonymy for both the species, and the matter has been referred to the International Commission on Zoological Nomenclature. However, in the account of the life cycles given by Baturo (1977), and in the following seasonal data, existing usage of the specific names is preserved. Bucephalus polymorphus Baer, 1827 Baturo (1977) reported that the sporocysts and cercariae were present in Dreissena polymorpha from April to October in Lakes Gostawickie and Slesinskie, Poland. The greatest cercarial emergence was during June to September. A rapid increase in water temperature caused a mass emergence of cercariae, whereas a fall in temperature stimulated a short-lived but intense emergence followed by a break in emission lasting several days. Cyprinid fishes of all sizes were infected by the metacercariae. Entry was by way of the skin, full development being completed after 15 days. The metacercariae died after 5 months in the fish. Dubinina (1949) reported the occurrence of B. polymorphus in Abramis brama and Cyprinus carpio in the Volga Delta, U.S.S.R. In A . brama the incidences were: spring 1940, 5.9%; summer 1940, 25%; winter 1941, 35.7%; spring 1941, 26.7%. In C. carpio the incidences were: spring 1940, 14.3%; summer 1940, 6.7%; winter 1941, 13.3%; spring 1941, 0%. No clear pattern of incidence was evident. Marits and Tomnatik (1971) and Marits and Vladimirov (1969) found these metacercariae in A . brama and Vimba vimba vimba natio carinata in the Dubossary Reservoir, Moldavia, U.S.S.R., during spring to autumn. Maximal incidence was in spring in A . brama (25%) but in summer in V . v. vimba natio carinata, although maximal intensity of metacercariae was in summer in both species of fishes. Vojtkova (1959) also reported maximal incidence in A . brama in the summer (July and August) in the River Svratka, Czechoslovakia. Lyubarskaya (1970) also reported a maximal, but low, incidence (4.3%) of metacercariae in A . brama during the summer, and none during the other seasons, in the Kuybyshev Reservoir, U.S.S.R., whereas Titova (1957) at Lake Ubinsk, Siberia, U.S.S.R. recorded the highest incidence (20%) in autumn in 3 f A . brama. As a contrast to the observations noted above, lzyumova (1959a)

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found the metacercariae only during the winter in Gymnocephalus cernua (4.4%) at the Rybinsk Reservoir, U.S.S.R. Bucephalus (species undetermined) Komarova, T. I. (1964) found Bucephalus sp. metacercariae in Abramis brarna, Blicca bjoerkna, Pelecus cultratus, Rutilus rutilus heckeli and Vimba vimba vimba natio carinara at the River Dnepr Delta, U.S.S.R. She examined fish from February to August and in October. Metacercariae were present during all these months, although not in each of the species of fish examined. In A. brarna the metacercariae were found in February (26.6%), March (2073, June (6.6%) and October (20%) but not in April, May, July and August. By contrast, they were found in all months in V. v. viniba natio carinata: February, 46.6%; March, 13.2%; April-May, 40%; June-July, 80%; October, 33.3%. Peak incidences in the other fish species were: B. bjoerkna, June, 40%; P. cultratus, July-August, 33.3 %; R . rutilus keckeli, June, 53.3%. Rhipidocotyle illense (Ziegler, 1883) According to Baturo (1977) the sprocysts and cercariae were present in Unio pictorum from May to October in Lake Slesinskie, Poland. The maximum incidence was in July and August. The water temperature greatly affected cercarial emergence, the greatest emission followed a thermal fluctuation. The cercariae entered the fish by way of the mouth and mainly encysted in the cephalic region. All sizes of fishes were infected and the metacercariae died about 5 months after entering the host. Kozicka (1958) found the metacercariae in the fins of Abramis brarna, Blicca bjoerkna, Cyprinus carpio, Rutilus rutilus and Scardinius erythrophthalrnus in Lake Druino, Poland. It was noted that towards the winter there were fewer and fewer mobile, living metacercariae. Single specimens from the muscles, connective tissues and gills degenerated less frequently. Molnar (1966) reported the metacercariae from Gyrnnocephalus cernua in Lake Balaton, Hungary in February (21.8 %) and June (6.2 %). They were not found during the other months when this species of fish was examined (January, March, July, August and October). 2. Family Clinostomatidae Clinostornum cornplanaturn (Rudolphi, 1814) Grabda-Kazubska (1974) noted that Clinostomatidae were normally found within the annual isotherm 10°C, and in warmer regions. Adult C. cornplanaturn were reported in more northern regions in herons returning from their winter regions. In the Rybinsk Reservoir, U.S.S.R. Shigin (1957) found adult clinostomes only in the spring, and not at other seasons. GrabdaKazubska (1974) noted similar occurrences of adult C. complanatiim in herons in Poland. However, in LichCnskie Lake, near Konin, in central Poland, the water was utilized in the cooling system of a power station and had average monthly water temperatures of 7.87"C in February and 29.16"C in July, which greatly exceeded the temperatures of unwarmed lakes in that country. At this warmed habitat metacercariae of C. cornplanatum were

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found in Perca fluviatitis and Rutilus rutilus. Grabda-Kazubska (1974) speculated that the increased water temperatures in Lake Lichenskie had allowed hatching of the eggs of C. complanatum, and that the limiting factor was most probably at this stage in the life cycle of the parasite. Pojmariska (1976) provided a summary of this and other studies in progress on parasites in the artificially warmed lakes in Poland. Yoshino (1940) attributed the annual fluctuations in occurrence of metacercariae of C. complanatum in Carassius auratus in Okayama Province, Japan to water temperatures. Dubinina (1949) found the metacercariae of Clinostomum sp. in Cyprinus carpio in the Volga Delta, U.S.S.R. in the spring of 1941, and at no other time (spring, summer, 1940, winter, 1941). Moln6r (1966) found one metacercaria of C. complanatum in Gymnocephalus cernua at Lake Balaton, Hungary in June 1961, and in no other month. At the Balkhash-Alakol’ Basin, Kazakhstan, U.S.S.R. Galieva (1971) found variations in infection rate of Perca schrenki according to season, region and fish size. Heavy infections in the fishes were seen in areas of large populations of fish-eating birds, in particular Ardea cinerea, the definitive host of these trematodes. The data of Galieva were from three lakes, for the months May, June, August and September. Clinostomum marginatum (Rudolphi, 1819) Fischthal (1949) established an experiment on 16 October, 1944 at a fish hatchery in Spooner, Wisconsin, U.S.A. Thirty fishes, one Ambloplites rupestris rupestris, six Lepomis gibbosus, four L. macrochirus macrochirus and 19 Perca j7avescens contained 324 C. marginatum metacercariae and were kept at the hatchery for 6 months, over the winter. At the end of the experiment, 24 April 1945, 14 metacercariae had gone (4.3 %). Fischthal concluded that the overwintering loss of metacercariae was negligible. Lepomis gulosus and L. macrochirus were examined from Lake Fort Smith, Arkansas, U.S.A. from July 1970 to June 1971 (Cloutman, 1975). Owing to the very low incidence of C. marginaturn at this habitat no meaningful conclusion is possible. 3. Family Cyathocotylidae Cyathocotyle (species undetermined) Yoshino (1 940) investigated a species of Cyathocotyle in Carassius auratus in the Okayama Province, Japan and speculated that annual fluctuations were largely dependent on temperature. Lee (1968) examined two species, Cyathocotyle species 1 and Cyathocotyle sp. 2, from a number of species of fishes in the Kum-Ho River, Korea. In Gnathopogon coreanus, Pseudogobio esocinus, Pseudorasbora parva and Pungtungia herzi the occurrence of metacercariae apparently was not influenced by season. Holostephanus luehei Szidat, 1936 Metacercariae were found from July to March in Pungitius pungitius from Pont-y-gwew Reen, Wentloog Level, near Cardiff, Wales (Pike, 1965). The incidence rose from nothing in June, through to 90% in October and from then until March it fluctuated at a high level (70-90%). From June to Septem-

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ber the average length of fish examined increased steadily, but from October to January more small fish appeared in the samples, from a summer-spawned generation. It was expected that the infection rate would drop during the winter and then fall again in spring after the adult fish had spawned and died. A gradual increase in metacercariae should then follow from May or June when cercariae were available to infect the new generation of P . pungitius (Pike, 1965). Mesostephanus appendiculatus (Ci urea, 1916) Marits and Tomnatik (1971) reported metacercariae of this species from Abramis brama (6 % incidence) in summer, but not spring and autumn, from the Dubossary Reservoir, Moldavia, U.S.S. R. Paracoenogonimus ovatus Katsurada, 1914 Includes Diplostomurn (Neodiplostomum) hughesi for which seasonal data were provided by Bogdanova (1954, Dubinina (1949) and Komarova (1957). In summary, where metacercariae had a high incidence and intensity of occurrence they were found in all seasons, for instance, in Abramis brama, River Volga (Bogdanova, 1958), River Volga Delta (Dubinina, 1949) and Kuybyshev Reservoir, U.S.S.R. (Lyubarskaya, 1970); Cyprinus carpio, River Volga Delta, U.S.S.R. (Dubinina, 1949); Esox lucius, River Volga (Bogdanova, 1958), River Dnepr Delta (Komarova, T. I., 1964) and Lake Dusia, Lithuania, U.S.S.R. (Rautskis, 1970b); and Lucioperca lucioperca, River Volga Delta, U.S.S.R. (Dubinina, 1949). In localities and species of fishes with a low incidence and intensity of infection by metacercariae of P. ovatus the time of occurrence was sporadic: Abramis ballerus, Blicca bjoerkna, Rybinsk Reservoir, U.S.S.R., autumn (Izyumova, 1960); Gymnocephalus cernua, Rybinsk Reservoir, U.S.S.R., winter (Izyumova, 1959a); Perca Jluviatilis, Lake Dusia, Lithuania, U.S.S.R., April-May (Rautskis, 1970a); and Tinca tinca, River Donets, U.S.S.R., April, July, October (Komarova, M. S., 1957). The distribution of the metacercariae in the host organs was reported by Bogdanova (1958). There were no major variations in the high incidence of the cysts in the muscle and fins of Abramis brama and Esox lucius examined in July/August, February/March and May. The variations in intensity were over a wider range, but without regular pattern. In other organs examined there were lower, sporadic, incidences and intensities of occurrence of the metacercariae of P. ovatus without seasonal significance. Paracoenogonimus viviparae (Linstow, 1877) The metacercariae of P. viviparae were reported from Rutilus rutilus in the Rybinsk Reservoir, U.S.S.R. in winter (9.6 %), summer (7.7 %) and autumn (17.4%). None were found in the spring (Izyumova, 1959a). 4. Family Diplostomatidae Crassiphiala bulboglossa Van Haitsma, 1925 Hoffman (1956) reported that a Pimephales pimephales pimephales infected by both C. bulboglossa and Uvulifer ambloplitis was kept for 37 months. At post-mortem, all metacercariae of both species were still alive.

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The mollusc Helisorna anceps is the intermediate host in North Dakota, U.S.A. Hoffman (1956) postulated that it was likely that most infected H . anceps died during the year, but that those infected late in the season probably survived the winter, as the sporocysts developed slowly and then produced cercariae for a while the next spring. Diplostornurn adarnsi Lester and Huizinga, 1977 Lester (1977) examined this species in Perca jlavescens from the Bay of Quinte, Lake Ontario, Canada from May to November. The evidence suggested that in both light and heavy infections, once the parasite reached the retina it remained there alive for the rest of the life of the fish. Diplostornurn gasterostei Williams, 1966 According to Sudarikov (1971) D. gasterostei is a synonym of D. pungiti (Shigin, 1965). However, as specimens from Llyn Tegid, Wales, differ from D. pungiti in a number of details, D. gasterostei is considered separately. The seasonal occurrence of D. gasterostei in British waters has been investigated by Chappell (1969), Kennedy (1975a), Kennedy and Burrough ( 1977) and Pennycuick ( 1971a, b, c). Chappell (1969) examined Gasterosteus aculeatus from a pond on Baildon Moor, Yorkshire, England at bi-monthly intervals. Incidence was constant in all samples except August, when it fell from 95% in May/June to 41 % in August. The fall was related to the presence of uninfected young fish at this time. Intensity of infection was relatively constant throughout (averages 3.3 to 5.6). Pennycuick (1971~)also examined G. aculeatus, from the Priddy Pool, Somerset, Emgland. The parasite had an overdispersed distribution, and the advantages of this to the host and parasite populations were discussed (Pennycuick. I97 Ic). The metacercariae were studied from October, 1966 to April, 1968. Between October and December, 1966 the percentage of infected G. aculeatus rose slightly showing that some fishes were acquiring infections. The mean number of parasites per fish was more or less constant, whereas the variance decreased steadily. This indicated that small numbers of heavily infected fishes were being removed from the population. As dead fishes picked up at this time did not have a higher mean number of metacercariae than living ones, predation must have been the chief cause of death. Pennycuick (197 Ic) speculated that as the temperature of the water decreased and food became more scarce, heavily infected G. aculeatus would be susceptible to predation. On 25th January, 1967 the mean and variance were raised by the presence of one very heavily infected fish (275 D. gasterostei). Otherwise, there was a slight decrease in mean and variance in December, 1966 and January, 1967, although the percentage incidence did not fall until February. According to Pennycuick (1971~)this showed that the number of heavily infected fish was continuing to decrease but that relatively few fishes were involved. Pennycuick (1971~)found a slight increase in mean, and more particularly in the variance, in March, owing to a new infection. Only a small number of fish were involved, however, as the percentage of incidence did not increase. As large numbers of cercariae were produced from one infected snail it was usual for small numbers of fishes t o acquire large numbers of Diplostomurn.

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In April the mean, variance and percentage infection all decreased to a low level owing to a decrease in numbers of heavily infected G . aculeatus. In May and June there was a large increase in the mean and percentage infection as many fishes acquired new infections. Pennycuick (1971~)noted that at this time the snail population was increasing and she presumed that many cercariae were being released. The variance increased only slowly at first showing that the cercariae were quite widely distributed and many fishes were picking up small numbers. Between July and October the mean number remained fairly constant, whereas the percentage incidence decreased slightly and variance increased rapidly. A few G. aculeatus were therefore acquiring large numbers of D. gasterostei showing that the distribution of cercariae was patchier. There was a sharp decrease in variance in November and December but the mean and percentage infections remained more or less constant. Once again heavily infected fishes were being removed from the population, probably owing to predation. As the mean did not decrease, a light infection was continuing. Between January and March the variance continued to decrease rapidly as did the mean. The percentage incidence fell slightly, thus heavily infected fish were still being removed but no new infections were occurring. In the final sample there was a small increase in the percentage incidence, mean and variance which indicated the start of a new phase of infection (Pennycuick, 197 1b). Thus the infections of D. gasterostei were acquired from March to December, with a maximum increase in May and June. Pennycuick (1971b) also reported that during early 1968 there was a decrease in intensity of the D. gasterostei infection, to about the same level as in 1967, which suggested that fishes were unable to survive a high level of infection under the cold conditions of winter. Kennedy (1975a) and Kennedy and Burrough (1977) examined the occurrence of D. gasterostei in Percafluviatilis at Slapton Ley, Devon, England. No very obvious pattern of changes was apparent. Incidence appeared to decline slightly between November and March and more obviously in midsummer (June or July/August). In both the years of observation a temporary rise in spring (March-May, 1974 and April-June, 1975) and obvious rises at the end of the summer were taken to indicate periods of infection. Diplostomum murrayense (Johnston and Cleland, 1938) Metacerariae were found in 15 species of native fishes in the lower Murray River, South Australia each month from November to May, but not during June, August and October (Johnston, T. H. and Angel, 1941). Adult D . murrayense were recovered from the marsh tern Chlidonias leucopareia from November to March. Cercariae were taken from October to April (summer in the Southern Hemisphere). It was suggested that the snails became infected in September or October by eggs that had overwintered in the swamps, or that were present in the faeces of the earliest terns to arrive, unless the infection had persisted in snails during the winter. However, it was observed that cercariae were available to infect fishes from October and that fully developed diplostomulae were present in fishes in November when terns became infected. F

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Diplostomum paraspathaceum Shigin, 1965 Banina and Isakov (1972) examined Gasterosteus aculeatus and Pungitius pungitius from a reservoir on the River Chernaya, Neva Delta, U.S.S.R. In G. aculeatus and P. pungitius metacercariae were present all year, although fishes were not examined in December-January during ice cover. Variations in incidence from month to month were explained by mortality of heavily infected fishes. High incidences were found in April (60 %), May (70 %), July (90%) and November (100%) in G. aculeatus and in June (62%), July (93.779, August (83-5%), September (77%) and October (89%) in P. pungitius. Diplostomum phoxini Faust, 1919 It should be noted that according to experiments carried out by Arvy and Buttner (1954) the metacercariae produce adult D. phoxini, but contrary to this, Rees (1955) also performed experiments using D. phoxini metacercariae and claimed that the resulting adult worms were Diplostomum pelmatoides. Thus D. phoxini may include metacercariae of two species of Diplostomum. Bibby (1972) studied the occurrence of D. phoxini in Frongoch Lake, Wales. There was a 100% incidence throughout the year, with a variable intensity, 4 to 1120 metacercariae in a single fish, having no correlation with season. Female fishes had heavier infections than males, but it was suggested this might be related to the larger size of many females. The average intenstiy increased with size of fish. Sten’ko (1976b) found cercariae of D. phoxini in Radix auricularia in the River Burul’chi, Crimea, U.S.S.R. In November the incidence was 16.3 %, but no cercariae were found in spring or summer. The definitive host, Mergus merganser was not found in the area. Berrie (1960a), in the Glasgow area of Scotland, found Lymnaea peregra to be the first intermediate host. Diplostomum scudderi (Oliver, 1941) Includes Diplostomum baeri eucaliae Hoffman and Hundley, 1957. In the fish Eucalia inconstans, metacercariae were accumulated through the life of the host. Experimentally infected fishes, with at least 101 metacercariae, were kept for 1 year and the larvae remained alive, and it was believed that they would have lived much longer. It was stated that the infection did not overwinter in snails (Hoffman and Hundley, 1957). Diplostomum spathaceum (Rudolphi, 1819) Diplostomum jlexicaudum (Cort and Brooks, 1928) and D. huronense (La Rue, 1927) are included as synonyms of D.spathaceum. Shigin (1976) has pointed out that until comparatively recently all metacercariae of the genus that were parasites in the eyes of freshwater fishes in the U.S.S.R. were assigned to this species. This situation is also true elsewhere, so that some of the records included here as D. spathaceum may relate to other species or to mixed infections. Aspects of the seasonal occurrence of D. spathaceum metacercariae have been studied by many authors especially in the U.S.S.R. These include: Bauer (1957a,b, 1959a), Bauer and Nikol’skaya (1957), Bauer et al. (1964), Bogdanova (1958), Dubinina (1949), Izyumova (1958, 1959a, 1960), Kash-

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kovskii (1967), Komarova, T. I. (1964), Lyubina (1970), Malakhova (1961), Marits and Tomnatik (1971), Markova (1958), Mindel (1963), Oun and Sirak (1973), Rautskis (1970a,b), Semenova (1966), Shigin (1964), Titova (1957) and Vartanyan and Mkrtchyan (1972). Other authors in other countries include: British Isles-Berrie (1960b), Chappell (1969), Crowden (1976), Erasmus (1958), Mishra (1966), Robertson (1953), Sweeting (1974), Wootten (1974); Germany-Schaperclaus (1954), Timmermann (1936); Hungary-Molnhr (1966, 1968); Poland-Wierzbicki (1970, 1971). In North America seasonal occurrence has been studied by Becker and Brunson (1966), Becker (1967) (as D. jexicaudum), Noble (1970) and Tedla and Fernando (1969) (as D. huronense). Table 1 indicates the species of fishes examined in the relevant climate zones. In general, young fish become infected by the cercariae of D spathaceum at an early age. As an example, Bauer (1957a) studied the dynamics of infection of Salmo salar fingerlings in swimming hatcheries in the River Narova, U.S.S.R. No D. spathaceum were found 14-15, 18,21 or 29-30 June, or 5 July, 1955 but from the 8 July onward to the 22 August the intensity of infection increased from 0.6 (8 July) to 5.4 (22 August). The cercariae originated from the river. Once infection of young fishes has occurred, reinfection may be continued through life, if exposure to cercariae was also continued. Thus Titova (1957) in Lake Ubinsk, Siberia, U.S.S.R., found that until the fishes were 5 years old the percentage infection rose, reaching a maximum in the autumn, but in older fishes the infection decreased considerably. In this instance, however, intensity of infection was slight. Where the intensity of infection reached higher levels, there may be a 100% incidence throughout, as in Coregonus lavaretus ludoga and C. lavaretus maraenoides in Lake Sevan, Armenia, U.S.S.R. (Vartanyan and Mkrtchyan, 1972). Often there was a tendency for incidence of metacercariae to increase by autumn, as for example, in Esox lucius in the Oka River, U.S.S.R. (Markova, 1958) and Percajuviatilis in Lake Dusia, Lithuania, U.S.S.R. (Rautskis, 1970a). Many authors have noted no significant seasonal changes in the overall incidence of D. spathaceum metacercariae, as in E. lucius, Lota Iota, P. Jluviatilis and Rutilus rutilus in Lake Konche, Karelia, U.S.S.R. (Malakhova, 1961), in Abramis brama, E. lucius, P.fluviatilis and R. rutilus in the Shropshire Union Canal, Cheshire, England (Mishra, 1966), and in Perca javescens in Oneida Lake, New York, U.S.A. (Noble, 1970) and in the Bay of Quinte, Lake Ontario, Canada (Tedla and Fernando, 1969). In habitats where a range of species of fishes have been examined there was considerable variation in incidence and intensity of infection by metacercariae of D. spathaceum. Izyumova (1958, 1959a, 1960) examined nine species from the Rybinsk Reservoir, U.S.S.R. No constant pattern was reported. Incidences of less than 10% were found in all seasons in Abramis brama, Esox lucius, Lucioperca lucioperca and Pelecus cultratus. High incidences and intensities of metacercariae were seen in Gymnocephalus cernua (minimal incidence 19 % summer, maximal 66.7 % autumn, maximal intensity 4-46 winter), in Perca Jluviatilis (minimal incidence OctoberNovember 50 %, maximal January-April 87.1 %) and in Rutilus rutilus

TABLE1 Studies on seasonal occurrence of metacercariae of trematodes listed in the climate zones of the World (see map Fig. I , Chubb, 1977) The species are in alphabetical order

Climate zones 1. Tropical

la. RAINY (humid climate) 1b. SAVANNA (humid climate) lc. HIGHLAND (humid climate) Id. SEMI-DESERT (dry climate) le. DESERT (dry climate) 2. Subtropical 2a. MEDITERRANEAN

Metacercariae species

Host species

Locality

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

Diplostomurn murrayense Posthodiplostomum minimum

15 species of native fishes Ictalurus nebulosus Lepomis cyanellus Lepomis macrochirus Micropterus salmoides floridens Pomoxis annularis Lepomis macrochirus

References

scrub, woodland, olive Lower Murray River, Johnston, T. H. and S. Australia Angel (1941) Lower Otay Reservoir, Colley and Olson (1963) San Diego County, California, U.S.A.

Lower Otay and Lake Murray Reservoirs, San Diego County, California, U.S.A.

Kellogg and Olson (1963)

Climate zones 2b. HUMID

Metacercariae species

Clinostomum complanatum Clonorchis sinensis

Host species

Carassius auratus Carassius auratus Hemiculter kneri Pseudorasbora parva Pseudorasbora parva Gnathopogon coreanus Pseudogobio esocinus Pseudorasbora parva Pungtungia herzi Carassius auratus

Cyathocotyle sp. 1 and 2

Cyathocotyle sp. B Echinochasmus beleocephalus Exorchis oviformis

Gnathopogon coreanus Pseudogobio esocinus Pseudorasbora parva Pungtungia herzi Carassius auratus Carassius auratus Gnathopogon coreanus Pseudogobio esocinus Pseudorasbora parva Pungtungia herzi Carassius auratus

Locality deciduous forest Okayama Province, Japan Sun Moon Lake, Taiwan

References Yoshino (1940) Fang and Lin (1975)

Kongkuan-pei, Taipei, Taiwan Kum-Ho River, Korea

Huang and Khaw (1964)

Okayama Province, Japan Kum-Ho River, Korea

Yoshino (1940).

Okayama Province, Japan Okayama Province, Japan Kum-Ho River, Korea

Yoshino (1940)

Okayama Province, Japan

Yoshino (1940)

Lee (1968)

Lee (1968)

Yoshino (1940) Lee (1968)

TABLE 1 (continued) Climate zones 2b. (continued)

Metacercariae species

Metacercaria hasegawai Metacercaria hasegawai a and c Metagonimus yokagawai

Metagonimus sp.

Posthodiplostomirrn minimum Pseudoexorchis major Uvulifer ambloplitis

3. Mid-latitude 3a. i. HUMID WARM SUMMERS

Apophallus muehlingi

Host species

Pseudogobio esocinus Pseudorasbora parva Pungtungia herzi Carassius auratus Carassius carassius Milvus migrans lineatus Carassius auratus Gnathopogon coreanus Pseudogobio esocinus Pseudorasbora parva Pungtungia herzi Lepomis cyanellus Lepomis humilis Lepomis macrochirus Lepomis megalotis Carassius auratus Lepomis cyanellus Lepomis humilis

Gyrnnocephalus cernua Lucioperca lucioperca Phoxinus phoxinus

Locality

References

Kum-Ho River, Korea

Lee (1968)

Okayama Province, Japan Kyoto, Japan

Yoshino (1940)

Okayama Province, Japan Kum-Ho River, Korea

Yoshino (1940)

Yamaguti (1939)

Lee (1968)

Little River, McDaniel and Bailey Buncombe Creek and (1974) Lake Texoma, Oklahoma, U.S.A. Okayama Province, Yoshino (1940) Japan Little River, McDaniel and Bailey Buncombe Creek and (1974) Lake Texoma, Oklahoma, U.S.A. temperate grassland, mixed forest Lake Balaton, Hungary Lake Balaton, Hungary

Molnar (1966) Molnar (1968)

~

Climate zones 3a. i. (continued)

Metacercariae species Bucephalus polyrnorphus

Host species Cyprinidae Abramis brama Vimba vimba vimba natio carinata Abramis brama

Clinostomum complanatum

Perca fluviatilis Rutilus rutilus Gymnocephalus cernua

Clinostomum marginatum

Lepomis gulosus Lepomis macrochirus

Diplostomurn spathaceum

Abramis brama Gymnocephalus cernua Phoxinus phoxinus

Diplostomurn sp.

Lepomis gibbosus

Diplostomdurn scheuringi

Lepomis gulosus Lepomis macrochirus Micropterus salmoides

~~~

Locality

References

Lakes Goslawickie and Slesinskie, Poland Dubossary Reservoir, Moldavia, U.S.S.R. Dubossary Reservoir, Moldavia, U.S.S.R.

Baturo (1977)

River Svratka, Czechoslovakia Lichenskie Lake, near Konin, Poland

Vojtkova (1959)

Lake Balaton, Hungary Lake Fort Smith, Arkansas, U.S.A.

Molnar (1966)

Dubossary Reservoir, Moldavia, U.S.S.R. Lake Balaton, Hungary Lake Balaton, Hungary Durham, North Carolina, U.S.A. Lake Fort Smith, Arkansas, U .S .A.

Marits and Tomnatik (1971) Marits and Vladimirov (1969)

Grabda-Kazubska (1974)

Cloutman (1975) Marits and Tomnatik (1971) Molnar (1966) Molnar (1968) Holl (1932) Cloutman (1975)

TABLE 1 (continued) Climate zones 3a. i. (continued)

Metacercariae species

Host species

Echinostoma sp.

Gymnocephalus cernua

Hysteromorpha triloba

Ictalurus melas Abramis brama

Ichthyocotyliirus pileatus

Abramis brama Cymnocephalus cernua

Mesostephanus appeildiculatus Posthodiplostomum brevicaudatum Posthodiplostomum cuticola

Posthodiplostomum minimum

Rhipidocotyle illense

Abramis brama

9 species, mostly Cyprinidae Cyprinidae Abraniis brama Vimba vimba vimba natio carinata Lepomis gulosiis Lepomis macrochirus Micropterus salmoides Pomoxis annularis

Cyprinidae Gymnocephalus cernua

Locality Lake Balaton, Hungary Spring Lake, Illinois, U S A . Dubossary Reservoir, Moldavia, U.S.S.R. Dubossary Reservoir, Moldavia, U.S.S.R. Lake Balaton, Hungary Dubossary Reservoir, Moldavia, U.S.S.R. Federsee, Germany

References Molnar (1966) Hugghins (1954b, 1956) Marits and Tomnatik (1971) Marits and Tomnatik (1971) Molnar 1966) Marits and Tomnatik (1971) Donges (1965)

Federsee, Germany Dubossary Reservoir, Moldavia, U. S.S.R. Dubossary Reservoir, Moldavia, U.S.S.R. Lake Fort Smith, Arkansas, U.S.A.

Doonges (1964) Marits and Tomnatik (1971) Marits and Vladimirov (1969) Cloutman (1975)

Lake Carl Blackwell, Oklahoma, U.S.A. Lake Slesinskie, Poland Lake Balaton, Hungary

Spa11 and Summerfelt (1969, 1970) Baturo (1977) Molnar (1966)

Climate zones 3a. i. (continued)

Metacercariae species Strigeids undetermined Tylodelphys clavata

Host species Lepomis gibbosus Leiomis gulosus Abramis brama Cymnocephalus cernua Abramis brama

3a. ii. HUMID COOL SUMMERS

Uvulifer ambloplitis

Lepomis macrochirus

Bucephalus polyniorphus

Cymnocephalus cernua Abramis brama

Clinostonium marginatum

Crassiphiala bulboglossa Diplostomuni adamsi

Ambloplites rupestris rupestris Lepomis gibbosus Lepomis macrochirus macrochirus Perca flavescens Pimephales pimephales pimephales Perca flavescens

Diplostomuni paraspathaceuni

Casterosteus aculeatus Pungitius pungitius -

Locality

References

Durham, North Carolina, U.S.A. Dubossary Reservoir, Moldavia, U.S.S.R. Lake Balaton, Hungary

Holl (1932)

River Svratka, Czechoslovakia Leetown, West Virginia, U.S.A. temperate grassland, mixed forest Rybinsk Reservoir, U .S.S.R . Kuybyshev Reservoir, U.S.S.R. Fish hatchery, Spooner, Wisconsin, U.S.A.

Vojtkova (1959)

Marits and Tomnatik (1971) Molnar (1966)

Hoffman and Putz (1965) Izyumova (1959a) Lyubarskaya (1970) Fischthal (1949)

North Dakota, U.S.A.

Hoffman (1956)

Bay of Quinte, Lake Ontario, Canada Neva Delta Reservoir, U.S.S.R.

Lester (1977) Banina and Isakov ( I 972)

TABLE 1 (continued) Climate zones 3a. ii. (continued)

Metacercariae species

Host species

Diplostomurn scudderi

Eucalia inconstans

Diplostomurn spathaceum

Salmo salar Coregonus albula ladogensis Coregonus lavaretus baeri natio ladogae Coregonus lavaretus maraenoides Stenodus leucichthys nelma cubensis Salmo salar sebago Salmo trutta Abramis brama Esox lucius Abramis brama Lucioperca lucioperca Pelecus cultratus Perca Jluviatilis Gymnocephalus cernua Rutilus rutilus Abramis ballerus Blicca bjoerkna Esox lucius Carassius auratus gibelio Carassius carassius

Locality

References

Hoffman and Hundley (1957) Narova River, U.S.S.R. Bauer (1957a) Yazhelbitsy hatchery Bauer (1957b) ponds, U.S.S.R. Bauer and Nikol'skaya Lake Ladoga, USSR (1957) Narva Fish Hatchery, Bauer et al. (1964) U .S.S.R .

North Dakota, U.S.A.

River Volga, U.S.S.R.

Bogdanova (1958)

Rybinsk Reservoir, U.S.S.R.

Izyumova (1958)

Rybinsk Reservoir, U.S.S.R. Rybinsk Reservoir, U.S.S.R.

Izyumova (1959a)

Lake Bol'shoe, Omsk Region, U.S.S.R.

Izyumova (1960) Lyubina (1970)

~

Climate zones

Metacercariae species

3a. ii. (continued)

Host species

Locality River, Oka U.S.S.R. Leningrad Region, U.S.S.R. Fish farms, Estonia, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R. Experimental Bay of Quinte, Lake Ontario, Canada Estonia, U.S.S.R. Kuybyshev Reservoir, U.S.S.R. Trumbull Lake, Iowa, U.S.A. Oakwood Lakes, South Dakota, U.S.A. Lake Ladoga, U.S.S.R.

Esox lucius Cyprinus carpio Salmo gairdneri Perca fluviatilis

Esox lucius Rutilus rutilus Perca flavescens Diplostomum sp.

Cyprinus carpio Abramis brama

Diplostomulum sp.

Pimephales promelas

Hysteromorpha triloba

Ictalurus melas

Zchthyocotylurus erraticus

Corregonus lavaretus baeri natio ladogae Abramis brama Esox lucius Abramis brama Lucioperca lucioperca Pelecus cultratus Gymnocephalus cernua Rutilus rutilus

Zchthyocotylurus pileatus

-

River Volga, U.S.S.R.

~~

References Markova (1958) Mindel (1963) Oun and Sirak (1973) Rautskis (1970a) Rautskis (1970b) Shigin (1964) Tedla and Fernando (1969) Kasesalu (1974) Lyubarskaya (1970) Meyer (1958) Hugghins (1957) Bauer and Nikol’skaya (1957) Bogdanova (1958)

Rybinsk Reservoir, U.S.S.R.

Izyumova (1958)

Rybinsk Reservoir, U.S.S.R.

Izyumova (1959a)

TABLE 1 (continued) Climate zones

Metacercariae species

3a. ii. (continued)

Host species

References

Abramis ballerus Blicca bjoerkna

Rybinsk Reservoir, ' U.S.S.R.

Izyumova (1960)

Abramis brama

Kuybyshev Reservoir, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R. River Volga, U.S.S.R.

Lyubarskaya (1970)

Perca fluviatilis Ichthyocotylurus platycephalus Ichthyocotylurus platycephalusl Ichthyocotylurus variegafus (as Tetracotyle percaefluviatilis)

Locality

Perca fluviatilis Abramis brama Esox lucius Perca fluviatilis

Rautskis (1970a) Rautskis (1970a) Bogdanova (1958)

Rybinsk Reservoir, U.S.S.R.

Izyumova (1958)

Neascus sp.

Ambloplites rupestris Lepomis gibbosus Lepomis macrochirus Perca flavescens

Fish hatchery, Spooner, Wisconsin, U.S.A.

Fischthal (1949)

Neodiplostomulum sp.

Gymnocephalus cernua Rutilus rutilus

Rybinsk Reservoir, U.S.S.R.

Izyumova (1959a)

Esox lucius

Lake Dusia, Rautskis (1970b) Lithuania, U.S.S.R. Irtysh and Om Rivers, Goryachev (1958) U.S.S.R. River Donets, U.S.S.R. Komarova (1957)

Opisthorchis felineus

Cyprinidae Tinca tinca

Climate zones

Metacercariae species

3a. ii. (continued)

Paracoenogonimus ovatus

Paracoenogonimus viviparae Posthodiplostomum brevicaudatum

Posthodiplostomum cuticola Posthodiplostomum minimum Tylodelphys clavata

Host species Abramis brama Esox lucius Gymnocephalus cernua

Locality River Volga, U.S.S.R.

Rybinsk Reservoir, U.S.S.R. Abramis ballerus Rybinsk Reservoir, Blicca bjoerkna U.S.S.R. Tinca tinca River Donets, U.S.S.R. Kuybyshev Reservoir, Abramis brama U.S.S.R. Perca fluviatilis Lake Dusia, Lithuania, U.S.S.R. Esox lucius Lake Dusia, Lithuania, U.S.S.R. Rutilus rutilus Rybinsk Reservoir, U.S.S.R. Carassius auratus gibelio Lake Bol’shoe, Omsk Carassius carassius Region, U.S.S.R. Perca fluviatilis Lake Dusia, Lithuania, U.S.S.R Yahara River lakes, Perca fluviatilis Wisconsin, U.S.A. Not given Experimental Gasterosteus aculeatus Pungitius pungitius Abramis brama

Neva Delta Reservoir, U.S.S.R. River Volga, U.S.S.R. ~

~~

References Bogdanova (1958) Izyumova (1959a) Izyumova (1960) Komarova, M. S. (1957) Lyubarskaya (1970) Rautskis (1 970a) Rautskis (1970b) Izyumova (1 959a) Lyubina (1 970) Rautskis (1970a) Pearse (1924) Hoffman (1950) Banina and Isakov (1972) Bogdanova (1958)

TABLE1 (continued) Climate zones

Metacercariae species

3a. ii. (continued)

Host species

Locality

Lucioperca lucioperca Pelecus cultratus Perca fluviatilis

Rybinsk Reservoir, U.S.S.R.

Izyumova (1958)

Gymnocephalus cernua Rutilus rutilus

Rybinsk Reservoir, U .S.S.R .

Izyumova (1959a)

Abramis ballerus Blicca bjoerkna Esox lucius

Rybinsk Reservoir, U.S.S.R.

Izyumova (1960)

Carassius auratus gibelio Lake Bol’shoe, Omsk Carassius carassius Region, U.S.S.R. Tinca tinca Perca jluviatilis

Esox lucius Uvulifer amploplitis

References

Semotilus atromaculatus atromaculatus Salvelinus fontinalis

3a. iii. EAST COAST Diplostomum spathaceum

Perca flavescens

Tetracotyle sp.

Perca jlavescens

Lyubina (1970)

Lake Dusia, Lithuania, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R. Turtle River, North Dakota, U.S.A.

Rautskis (1970a)

Sturgeon River, Michigan, U.S.A. temperate grassland, mixed forest Lake Oneida, New York, U.S.A. Lake Oneida, New York, U.S.A.

Krull (1934a)

Rautskis (1970b) Hoffman (1953)

Noble, R. L. (1970) Noble, R. L. (1970)

Climate zones 3b. MARINE WEST COAST

Metacercariae species

Host species

Apatemon gracilis

Gasterosteus aculeatus

Diplostomum gasterostei

Gasterosteus aculeatus Perca fluviatilis Gasterosteus aculeatus

Diplostomum phoxini Diplostomum spathaceum

Phoxinus phoxinus Gasterosteus aculeatus Gasterosteus aculeatus Leuciscus leuciscus Anguilla anguilla Cobitis taenia Gasterosteus aculeatus Rutilus rutilus Salmo trutta Abramis brama Esox lucius Perca fluviatilis Rutilus rutilus

Locality temperate grassland, deciduous forest near Vancouver, Canada Pond, Baildon Moor, Yorkshire, England Slapton Ley, Devon, England

References

Lester (1974) Chappell (1969)

Kennedy (1975a), Kennedy and Burrough (1977) Priddy Pool, Somerset, Pennycuick (1971a,b,c) England Frongoch Lake, Wales Bibby (1972) Berrie (1960b) Mossend Railway Station and Loch Lomond, Scotland Chappell (1969) Pond, Baildon Moor, Yorkshire, England Crowden (1976) River Thames, England Erasmus (1958) Roath Park Lake, Cardiff, Wales

Shropshire Union Canal, Cheshire, England

Mishra (1966)

TABLE 1 (continued) Climate zones

3b. (continued)

Metacercariae species

Host species Salmo trutta Gasterosteus aculeatus

Locality Dunalastair Reservoir, Scotland Leeds-Liverpool Canal, England Lake Dargin, Poland Haminfield Reservoir, Essex, England

Perca jluviatilis Anguilla anguilla Gymnocephalus cernua Noemacheilus barbatulus Perca fluviatilis Pungitius pungitius Rutilus rutilus Salmo gairdneri Salmo trutta Holostephanus luehei Pungitius pungitius Wentloog Level, near Cardiff, Wales Ichthyocotylurus erraticus Salmo trutta Loch Leven, Scotland Salmo gairdneri Hanningfield Reservoir, Salmo trutta Essex, England Oncorhynchus kisutch Nanophyetus salmincola Bowmans Bay Station, Washington State, Oncorhynchus tshawytscha Oncorhynchus kisutch Salmo gairdneri

U.S.A. Elokomin River, Washington State, U.S.A. Beaver, Mill and Sam Creeks, Oregon, U.S.A.

References Robertson (1953) Sweeting (1974) Wierzbicki (1970, 1971) Wootten (1974)

Pike (1965) Campbell (1974) Wootten (1973a) Farrel et a / . (1964) Farrel et al. (1964) Milleman and Knapp (1970)

~

Climate zones 3b. (continued)

Metacercariae species

Host species

Posthodiplostonzuni brevicaudatum

Perca fluviatilis Cyprinidae

Prohemistomuluni sp.

Esox lucius

Rhipidocotyle illense

Abramis brama Blicca bjoerkna Cyprinus carpio Rutilus rutilus Scardinius erythrophthalmus

Tetracotyle sp.

Perca Jluviatilis

Tylodelphys clavata

Perca jluviatilis Perca Jluviatilis Gymnocephalus cernua Perca Jluviatilis Pungitius pungitius Rutilus rutilus Salmo gairdneri Salmo trutta

Tylodeelphyspodicipina

Perca Jluviatilis Cyninocephalus cernua Perca Jluviatilis Salnio gairdrieri

Locality

References

Lake Dargin, Poland Lake Druzno, Poland Shropshire Union Canal, Cheshire, England Lake Druzno, Poland

Wierzbicki (1971) WiSniewski (1958a) Mishra (1 966)

Rostherne Mere, Cheshire, England Slapton Ley, Devon, England Lake Dargin, Poland Hanningfield Reservoir, Essex, England

Rizvi (1964)

Kozicka (1 958)

Kennedy and Burrough (1977) Wierzbicki (1970, 1971) Wootten (1974)

Lake Dargin, Poland Wierzbicki (1970) Hanningfield Reservoir, Wootten (1974) Essex, England

TABLE1 (continued) Climate zones

3 ~ .SEMI-DESERT

Metacercariae species Apophallus muehlingi Bucephalus polymorphus

Host species Blicca bjoerkna Lucioperca lucioperca Abramis brama Cyprinus carpio

Locality

References

prairie and steppe Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Volga Delta, U.S.S.R.

Dubinina (1949)

Bucephalus sp.

Abramis brama Blicca bjoerkna Pelecus cultratus Rutilus rutilus heckeli Vimba vimba vimba natio carinata

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Clinostomum sp. Diplostomurn spathaceum

Cyprinus carpio Salmo gairdneri

Volga Delta, U.S.S.R. Canal Lake, etc., Washington State, U.S.A. Canal Lake, Washington State, U.S.A. North Park, Colorado, U.S.A. Volga Delta, U.S.S.R.

Dubinina (1949) Becker (1 967)

Iriklin Reservoir, River Ural, U.S.S.R.

Kashkovski (1967)

Salmo gairdneri Salmo gairdneri Abramis brama Cyprinus carpio Lucioperca lucioperca Silurus glanis Rutilus rutilus

Becker and Brunson (1 966) Davies, R. B. et al. (1973) Dubinina (1 949)

Climate zones

Metacercariae species

Host species

Locality

References

Abramis brama Blicca bjoerkna Esox lucius Lucioperca lucioperca Rutilus rutilus heckeli Vimba vimba vimba natio carinata

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Abramis brama Blicca bjoerkna Esox lucius Ichthyocotylurus erraticus Oncorhynchus kisutch Salmo gairdneri Thymallus arcticus Ichthyocotylurus pileatus Abramis brama Lucioperca lucioperca Abramis brama Blicca bjoerkna Esox lucius Lucioperca lucioperca Pelecus cultratus Rutilus rutilus heckeli Vimba vimba vimba natio carinata

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Georgetown Lake, Montana. U.S.A.

Olson (1970)

Volga Delta, U.S.S.R.

Dubinina (1949)

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Abramis brama Blicca bjoerkna Lucioperca lucioperca Pelecus cultratus

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

3c. (continued)

Hysteromorpha triloba

Metagonimus y okoga wai

~~

TABLE 1 (continued) Climate zones

Metacercariae species

3c. (continued) Opisthorchis felineus Paracoenogonimus ovatus

Posthodiplostom~m cuticola

Host species Rutilus rutilus heckeli Vimba vimba vimba natio carinata Abramis brama Pelecus cultratus Abramis brama Cyprinus carpio Lucioperca lucioperca Esox lucius Cyprinidae Abramis brama Cyprinus carpio Abramis brama Alburnus alburnus Rutilus rutilus caspicus Cyprinidae, 25 species Abramis brama Blicca bjoerkna Pelecus cultratus Rutilus rutilus heckeli Vimba vimba vimba natio carinata Cyprinidae

Locality

Referznces

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Volga Delta, U.S.S.R.

Dubinina (1949)

Dnepr Delta, U.S.S.R. Astrakhan State Reserve, U.S.S.R. Volga Delta, U.S.S.R.

Komarova, T. I. (1964)

Volga Delta, U.S.S.R.

Kamenskii (1969)

Bauer et al. (1 964) Dubinina (1949)

Lower Volga, U.S.S.R. Kamenskii (1971) Dnepr Delta, U.S.S.R. Komarova, T. I. (1964)

Astrakhan State Reserve, U.S.S.R.

Vladimirov (1960)

Climate zones

Metacercariae species

3c. (continued)

Pseudamphistomum truncatum Tylodelphys clavata

Host species

Abramis brama

Volga Delta, U.S.S.R. Dubinina (1949) Iriklin Reservoir, Kashkovski (1967) River Ural, U.S.S.R. Dnepr Delta, U.S.S.R. Komarova, T. I. (1964)

Clinostornuni complanatum

Perca schrenki

Bucephalus polymorphus

Abramis brama

Diplostomurn spathaceum

Esox lucius Lota Iota Perca jluviatilis Rutilus rutilus

Diplostomurn sp.

Komarova, T. I. (1964)

Dnepr Delta, U.S.S.R.

Abramis brama Blicca bjoerkna Esox lucius Lucioperca lucioperca Rutilus rutilus heckeli Vimba vimba vimba natio carinata

3e. SUB-POLAR

References

Blicca bjoerkna

Rutilus rutilus

3d. DESERT

Locality

cool desert Balkhash-Alakol’ Basin, U.S.S.R. coniferous forest Lake Ubinsk, Siberia, U.S.S.R. Lake Konche Karelia. U.S.S.R.

Galieva (1971) Titova (1957) Malakhova (1961)

Abramis brama Leuciscus idus Leuciscus leuciscus

Lake Ubinsk, Siberia, U.S.S.R.

Titova (1957)

Rutilus rutilus

Kuito Lakes, Karelia, U.S.S.R.

Rumyantsev (1975) ~~

~~~

~~

~ _ _ _

TABLE 1 (continued) Climate zones 3c. (continued)

Metacercariae species Ichthyocotylurus pileatus

Esox lucius

Zchthyocotylurus platycephalus] Zchthyocotylurus variegatus (as Tetracotyle percaefluviatilis) Postlzodiplostomum brevicaudatum Tylodelphys clavata

Perca J7uviatiIis

4. Polar

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

Host species

Perca fluviatilis

Esox lucius Lota Iota Perca fluviatilis Rutilus rutilus

no seasonal studies no suitable habitats for freshwater trematodes Coregonus lavaretus ludoga Coregonus lavaretus maraenoides Ichthyocotylurus erraticus Coregonus lavaretus Iudoga Coregonus lavaretus maraenoides Coregonus lavaretus Tylodelphys clavata ludoga Coregonus Iavaretus maraenoides

Diplostomum spathaceum

Locality Lake Konche, Karelia, U.S.S.R. Lake Konche, Karelia, U.S.S.R.

Lake Konche, Karelia, U.S.S.R. Lake Konche, Karelia. U.S.S.R.

References Malakhova (1961) Malakhova (1961)

Malakhova (1961) Malakhova (1961)

tundra icefields and glaciers heath, rocks and scree Lake Sevan, Armenia, U.S.S.R.

Vartanyan and Mkrtchyan (1972)

Lake Sevan, Armenia, U.S.S.R.

Vartanyan and Mkrtchyan (1972)

Lake Sevan, Armenia, U.S.S.R.

Vartanyan and Mkrtchyan (1972)

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

171

(minimal incidence 38 % spring, maximal 63.5 % winter, maximal intensity 8-40 spring). In two species of fishes, Abramis ballerus and Blicca bjoerkna, there were high autumn incidences and intensities (35.3 %, 4-8 and 43.4 %, 2-18 respectively) with a low winter occurrence in A . ballerus (4.3 %, 1) and D. spathaceum metacercariae were not found in this fish in spring or summer. In B. bjoerkna there was a low winter occurrence (6.6%, 12), metacercariae were not found in spring, but were of increased abundance in summer (22 %, 1-12) through to the autumn peak (Izyumova, 1960). Komarova, T. I. (1964) investigated six species of fishes in the River Dnepr Delta, U.S.S.R. In this locality the maximum incidence and intensity of D. spathaceum metacercariae was in B. bjoerkna in March (53.3%, 2-40) and also in V. v. vimba natio carinata during the same month (46%, 1-10). In L. lucioperca maximal occurrence was in June (20 %, 4-8) and in Rutilus rutilus heckeli in July/August (26.6 %, 4-18), however, in all the six species, there were months when no D. spathaceum were found. If incidence and intensity of infections of D. spathaceum metacercariae in fishes are high, seasonal patterns in the life cycle of the trematode are hidden, nonetheless they occur. Sampling of the fishes without regard to the different zones within the habitat may also mask seasonal patterns. Wierzbicki (1970) observed two peaks of incidence and intensity of occurrence of D. spathaceum metacercariae in Perca puviatilis in Lake Dargin, Poland. The spring peak was slightly higher than that occurring in the autumn. Wierzbicki (197 1) noted this seasonal trend with regard to the three zones in the lake, littoral, shallow and the deepest parts. The maximum seasonal variation was in the littoral zone, the greatest intensity per fish being in spring and early autumn. Otherwise, metacercariae were present all year in all zones. According to Shigin (1964) the life span of metacercariae in experimentally infected Abramis brama and Rutilus rutilus may exceed 33 years. His experiments terminated at this time, but the metacercariae at this age had early stages of degeneration. Shigin (1964) discussed his results, and the observations of other workers, and suggested that the life span of D. spathaceum metacercariae in its principal host, Rutilus rutilus rutilus, was about 4 years, but considered that it was much shorter in other species of fishes, depending on the degree of adaptation of the parasite to the particular species of fish. This length of life of the metacercariae also obscures the seasonal patterns in the life cycle of D. spathaceum. The seasonal aspects of the life cycle of D. spathaceurn include the occurrence of the adult trematodes in the avian hosts and the larval stages in the snail hosts. In areas with mild winters, such as the British Isles, avian hosts, typically gulls (Laridae), are present on freshwaters all year. In other areas, for instance North Park, Colorado, U.S.A. where Larus calgornicus has been shown to be the most important host (Davies, R. B. et a]., 1973), the gulls arrived about 1st April each year and remained until the lakes were completely frozen, in October or November. Infections were found from July to September, 1970, and with a lighter level of infection in the spring of 1971. In Norway a similar occurrence of adult D. spathaceum has been reported by

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Bakke (1972a, b). The gulls, Larus canus, arrived in the Agdenes area in April, when adult D. spathaceum was absent from them, but the adult worms occurred thereafter, with increased incidence of infection in SeptemberOctober. The gulls departed from August to October. Mindel (1963) has studied the biology of the larval stages of D. spathaceum in molluscan hosts in the Leningrad region of the U.S.S.R. The parasite overwintered not only as expected as metacercariae in the fishes, but also in snail hosts. Lymnaea stagnalis and Radix ovata kept in the laboratory at 18°C shed cercariae throughout winter, and development of metacercariae occurred at this time in Cyprinus carpio kept at 13°C in aquaria, although maximum size was not reached for 45 to 50 days, as compared with 14 days in the summer months at 17-20°C. According to Bauer (1959a) cercariae emerged from snails at water temperatures from 10°C, with a maximum at 18°C. The most effective invasion of fish occurred at 18°C and higher. Much of this information was quoted from Timmermann (1936). In natural waters, infections of fishes by cercariae occurred once the water temperature had risen above the minimal level for cercarial emergence, from early summer through to autumn (Bauer et al., 1964). Wootten (1974) showed that the increase in infection of newly introduced Salmo gairdneri occurred in Hanningfield Reservoir, England from May to November, 1968. Water temperature was above 10°C from April to November. In North Park, Colorado, U.S.A. fingerling S. gairdneri stocked in April were first found infected by D. spathaceum metacercariae in midJuly and by mid-August they were all infected (Davies, R. B. et al., 1973). Oun and Sirak (1973) noted that the extraordinarily warm summer of 1972 produced an almost 100% incidence of D. spathaceum metacercariae in 1 and 2 year old S. gairdneri in fish farms on the islands of Hiiumaa and Saaremaa, Estonia, U.S.S.R. Under cold winter conditions in Lanarkshire, Scotland, no transmission of cercariae occurred from Lymnaea peregra to Gasterosteus aculeatus, although snails carried the infection in January (Berrie, 1960b). However, Becker and Brunson (1966) and Becker (1967) observed that Salmo gairdneri in lakes in Washington State, U.S.A. were infected by spring. An alternative method of transmission, which occurred primarily during the winter when few if any cercariae were emerging, was proposed (Becker and Brunson, 1966). The S. gairdneri acquired the parasite when feeding extensively on Lymnaea palustris nuttalliana and Physa propinqua which contained precocious metacercariae. These authors placed some precocious metacercariae in the stomachs of experimental S. gairdneri in winter. Only 4 % reached the lens, and no cercariae were seen. Control fish did not become infected. In the field, a gradual increase in intensity of infection was observed overwinter, in planted S. gairdneri, and only precocious metacercariae were found in wintering snails when the lake was icebound and homothermic at 0-4°C. Early work, such as that of Robertson (1953), did not reveal whether or not D. spathaceum metacercariae overwintered in fish. However, Bauer, (1957b) demonstrated overwintering in Coregonus albula ladogensis in hatchery ponds near Leningrad, U.S.S.R.

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Erasmus (1 958) described the morphology of metacercariae recovered from experimentally infected fish after periods of from 7 to 544 days postinfection. At 15°C the larvae possessed the full complement of metacercarial characters after 93 days. Chappell (1969) attempted to demonstrate seasonal variations in invasion of D. spathaceum in Gasterosteus aculeatus in a pond at Baildon Moor, Yorkshire, England, by considering metacercariae measuring 0.2 mm to represent recent infections. He found that both O + and 1+ fish had small metacercariae. He concluded that the main period of infection was about August, when 50% of the metacercariae were small. However, small metacercariae at other times of the year indicated that either infection could occur all year, or that some larvae had a retarded rate of overwinter growth. The latter conclusion was supported by the work of Sweeting (1974) who studied the development of cercariae to metacercariae in Xenopus laevis and six species of fishes. In experiments at 12°C the developmental times in days were: Carassius auratus, 40-45 ; Gobio gobio, 28 ; Perca fluviatilis, 120; Phoxittus phoxittus, 28; Rutilus rutilus, 35-40; and Salmo trutta, 60-85 days (Sweeting, 1974). Experiments with Xenopus laevis, at a range of eight temperatures gave the following developmental times in days: 5"C, 102; 9"C, 86; 12"C, 65; 15°C 54; 18"C, 47; 22"C, 29; 25"C, 15; 29"C, 12 days. At 5 and 9"C, the experiments were terminated after 102 and 86 days respectively, as there was no development of cercariae. Sweeting (1974) noted that it followed that natural infections of cercariae, occurring between June and September in the Lancaster and Leeds-Liverpool Canals, may not complete the transformation to metacercariae before the winter. Low winter temperatures may retard any further development until spring of the following year. The possibility of infection of the definitive host was thus delayed by 1 year. Sweeting (1974) observed that the pattern of occurrence of metacercariae in Gasterosteus aculeatus in the field supported ideas worked out from the experimental infections of Xenopus laevis, with delays in development occurring at low winter temperatures. Thus the cercarial-metacercarial intermediates (see Fig. 1) were found throughout the year, reaching a peak in late summer with the influx of newly released cercariae. It was followed by a gradual decline to the following May when a few intermediate forms persisted. This pattern of infection and development prevented the clear-cut separation of successive years' infections and was complicated by some cercariae undergoing complete development to metacercariae within a few weeks or months. The transience of the intermediate forms of the parasite made them suitable for some seasonal studies that were not possible with metacercariae. However, Sweeting (1974) noted that such studies were difficult in Gobio gobio owing to the presence of large numbers of moribund, partly developed metacercariae throughout the year. Unlike the parasites of the gut or gills, which can be expelled, or tissue parasites, which can become encapsulated, dead larvae of D. spathaceum in the lens of the eye underwent slight autolysis but otherwise remained intact (Sweeting, 1974). It is noteworthy that D. spathaceum metacercariae cause mortality of fishes, as for example, that seen by Bauer et al. (1964) in Coregonus lavaretus

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JAMES C . CHUBB

maraenoides and other species in the Narvafish hatchery, U.S.S.R. Fishes were destroyed from early summer, but mortality reached 100% by the end of June in ponds with a great number of molluscs. Crowden (1976) observed that in the River Thames at Reading, England, Leuciscus leuciscus were 100% infected with metacercariae of D.sparhaceum. The mean number of parasites per fish fell during the winter months, and this was attributed to the disappearance of heavily infected fishes from the samples, owing to mortality or predation. Crowden also observed that the more heavily infected fish spent more time in the surface layers of the water, and were probably more vulnerable to predation by birds, notably gulls, the definitive hosts of D. spathaceum (Crowden, 1976). Diplostomum (species undetermined) Data of seasonal occurrence for undetermined species of Diplostomum have been provided by Holl(I932), Kasesalu (1974), Lyubarskaya (1970) and Rumyantsev (1975). (4

1-2 days

(b)

(c)

15 days

30

days

fqj

(d 1 40-45 days

(4 50

days

(f) 65 days

FIG.1. Stages in the development of metacercariae of Diplosiomum spathaceum in the lens of experimentally infected Xenopus laevis at 12°C. (a)-(e) intermediate stages, (f) a metacercarial form. [Reproduced from Sweeting (1974), Fig. 2, p. 296.1

Kasesalu (1974) observed the occurrence of D. sp. in Cyprinus carpio from a rearing pond (June to October), a wintering pond (November to May) and a fattening pond (June to October) in a fish farm in Estonia, U.S.S.R. During this time the incidence of D. sp. climbed from nothing in June/July, to 45 % by October of the first year, to 100% by June of the second year. Rumyantsev (1975) found the highest intensity of infection in Rutilus rutilus at the end of the summer in the Kuito Lakes, Northern Kareiia, U.S.S.R. At this time a maximum level of cercariae was present. According to Gvozdev (1971, 1972), who worked in the same locality, the first peak of mollusc infections in mid-August was caused by cercariae that developed in molluscs infected in the preceding year and which had overwintered, and

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the second, at the end of September, represented the infection of the mollusc juveniles of the current year. Rumyantsev (1975) also noted that the relatively low infection of Coregonus albulu in the Kuito Lakes at the end of summer was related to the pelagic mode of life of these fish, which prevented contact with the first intermediate hosts, the molluscs. Diplostomulum scheuringi Hughes, 1929 According to Hoffman (1960, 1967) this diplostomulum occurs in the vitreous humor of the eyes of fishes and the adult is unknown. Sudarikov (1974) considered it to be a species of Tylodelphys. Cloutman (1975) tabulated the occurrence of D. scheuringi in Lepomis gulosus, L. macrochirus and Micropterus salmoides from Lake Fort Smith, Arkansas, U.S.A. from July, 1970 to June, 1971. Peak infection (expressed as average number of diplostomulae per fish) was in L. gulosus in January. The infection in L. gulosus and L. macrochirus rose from September, 1971 to a peak January, 1972 and declined towards June, 1972. Diplostomulum (species undetermined) Meyer (1958) studied the occurrence of a Diplostomulum type larva in Pimephales promelas in Trumbull Lake, Iowa, U.S.A. P. promelas became scarce in the late summer of 1954, but the degree of infection did not change. In early July, 1955, P. promelas were again abundant, but at this time the degree of infection was low. This fact, coupled with the shortage of age group IT fish, led him to suggest that few of the infected fish had survived from the preceding year. In 1955, at the start of summer in early July the incidence was 15%, and as the summer progressed, the incidence climbed rapidly until late August when it had reached 90% plus, the level of the preceding year. Meyer (1958) observed a sex differential in incidence in the fish collected in 1955. In 1954 both sexes were uniformly infected (92% in males, 94.9% in females). In mid-July 1955, however, 57.5% of the female P. promelus were infected compared with 28.8% of the males. By August, 1955, the incidence had climbed to 90 % and both sexes were equally infected. At the same time the numbers of P. promelas showed an abrupt drop similar to that of 1954. The two events seemed too closely correlated to be of mere chance, and as Meyer (1958) had also provided evidence on the pathology of the infection, he concluded that the rise in parasitism definitely hastened the disappearance of this group of fish. Hysteromorpha triloba (Rudolphi, 1819) Hugghins (1954a, b, 1956, 1957) has described many aspects of the biology of H. trilobu. In Spring Lake, Illinois, U.S.A., the snail Gyraulus hirsutus was infected only during the warm summer months. At these summer temperatures development of larvae in the snail was completed in about 14-15 days post-infection. Cercariae mostly emerged in the early morning. The metacercariae occurred in the muscle of the fish Ictulurus melus and were mature in about 12 weeks. Their survival over the winter, and their infectivity to Phalacrocorax auritus auritus were demonstrated experimentally (Hugghins, 1954b). The cormorants arrived at Spring Lake in late March, early April and remained until the lake froze, usually late November (Hugghins, 1956). The development of the trematode eggs was temperature-dependent (Hugg-

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JAMES C . C H U B B

hins, 1954a). The fishes, I. melas, were heavily infected by metacercariae (Hugghins, 1956). At Oakwood Lakes, South Dakota, U.S.A. the three hosts in the life cycle were also the snail Gyraulus hirsutus, the fish Ictalurus melas and the cormorant Phalacrocorax auritus (Hugghins, 1957). The snails did not carry the infection over the winter, but acquired it after the return of cormorants in the spring. Metacercariae were found in fishes eaten by cormorants in April and May, 1954. The cormorants abandoned the rookery in 1955, and with their departure, the infection in G . hirsutus virtually disappeared in the same season. Komarova, T. I. (1964) reported the occurrence of metacercariae of H . triloba in Abramis brama, Blicca bjoerkna and Esox lucius in the River Dnepr Delta, U.S.S.R. Metacercariae were found in most months when fishes were examined (February-May, October) but not all (June-August). The incidence varied without apparent pattern, but intensity was low throughout (maximum 12 in A. brama). In A . brama in the Dubossary Reservoir, Moldavia, U.S.S.R. Marits and Tomnatik (1971) found metacercariae in the spring, summer and autumn. Peak incidence (13.4%) and intensity (8) were in summer. Neascus (species undetermined) Neascus larvae, 200 at the start of the experiment, were overwintered in one Ambloplites rupestris rupestris, six Lepomis gibbosus, four L. macrochirus macrochirus and three Percaflavescens at a fish hatchery, Spooner, Wisconsin, U.S.A. (Fischthal, 1949). Only six metacercariae (3 %) were not found after the 6 months so that it was concluded that the overwintering loss of metacercariae was negligible. Neodiplostomulum (species undetermined) Neodiplostomulum metacercariae were found by Izyumova (1 959a) at the Rybinsk Reservoir, U.S.S.R. in Gymnocephalus cernua winter (1 1.1 %) and summer (4.8%) only and in Rutilus rutilus autumn (4.3%) only. In Esox lucius Neodiplostomulum metacercariae were found in autumn (6.25 %) and winter (6.66%) only. At Lake Dusia, Lithuania, U.S.S.R. Rautskis (1970b) found Neodiplostomulum metacercariae in Esox Iucius in JanuaryMarch (9 %) but not at other times. Posthodiplostomum brevicaudatum (Nordmann, 1832) Donges (1965) has provided full details of the biology of P . brevicaudaturn. The life cycle can be completed in 80 days under favourable conditions, but may be delayed for as long as 4 years. Temperature affects development. In Phoxinusphoxinus the maximum life of a metacercaria was 5 years 1 month 2 days. The occurrence of metacercariae was reported for Perca fluviatilis from Lake Konche, Karelia, U.S.S.R., by Malakhova (1961). They were present in all seasons, autumn 22.2%, winter 24.7%, spring 36.6% and summer (maximum) 42.2%. Maximal intensity (41) was also seen in the summer. Rautskis (1970a) investigated P.fluviatilis in Lake Dusia, Lithuania, U.S.S.R. At this habitat a low incidence was seen in January-March and in OctoberNovember (6.6% in each period), a high incidence in April-May (38.4%),

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but none were found in June-July. Wierzbicki (1971) noted the presence of the metacercariae all year in Lake Dargin, Poland. P. brevicaudatum was dominant in the littoral zone of the lake. Peak intensities in the three zones of the lake were as follows: littoral, October 1959, May 1960; shallows, January and July, 1960; and in deep waters, May, 1959, January and August, 1960. Lyubina (1970) investigated Carassius auratus gibelio and C. carassius at Lake Bol’shoe, Omsk Region, U.S.S.R. In C. auratusgibelio no metacercariae were found summer 1965, or spring 1966. However, in the winter of 1966 40.3 % were infected, 48.6 % in the summer and 15 % in the autumn of 1966. In young C. carassius compared with adult fish the winter infections were young 84.6%, adult 15.3 % and in summer, young loo%, adult 5.5%. WiSniewski (1958a) observed that the development of the cercariae into metacercariae took 7-8 weeks at summer water temperatures. Posthodiplostomum cuticola (Nordmann, 1832) The stages in the life cycle have been described by Vladimirov (1960, 1961a,b) and Donges (1964). The parasite occurs mainly in the south of the U.S.S.R. (Bauer, 1968). The life cycle can be completed in one summer in southern regions, but in more northern areas of the U.S.S.R. it may need two summers (Bauer et a f . , 1969). According to Donges (1964) in optimum conditions the life cycle can be completed in 98 days, but if ecological conditions determined it, the duration could be up to 5 years. P . cuticola eggs can be spread over long distances by birds (Kamenskii, 1971). At 0-1°C eggs died within 3-4 days, they matured at water temperatures above 10°C and development was accelerated with increased temperature, so that at 28°C miracidia hatched in 9-12 days (Bauer et al., 1964). The eggs had a short or a long period of maturation, depending on the age of the metacercariae from which the adult worms were developed. The development time of eggs from adult worms produced from metacercariae of the same summer was shorter (30-40 days at 16°C and 9-12 days at 28°C) than that of eggs from adults of metacercariae that had overwintered in fishes (85-95 days at 16°C and 25-30 days at 28°C) (Vladimirov, 1961a). The intermediate mollusc hosts were Planorbis planorbis and P . carinatus (Vladimirov, 1960; Donges, 1964; Kamenskii, 1971). The highest infection was in P. planorbis during June to mid-July (Vladimirov, 1960). Massrelease of cercariae occurred at 28°C (Bauer et al., 1964). It was suggested by Kamenskii (1969) that the main contact between the cercariae and the fishes in the Lower Volga was during March to August when young fishes inhabited shallow, warm backwaters. Cyprinidae were the most frequently infected of 25 species of fish in the Lower Volga, because in spring and summer they preferred the same habitat, shallow, weedy waters, as P . planorbis and P . carinatus. The cercariae of P . cuticola showed morphological variations in relation to temperature. At 15°C they were larger than at 24°C (Donges, 1964). The sporocysts can overwinter in the mollusc host (Bauer et al., 1964; Donges, 1964; Kamenskii, 1971). The optimum temperature for the development of metacercariae in fishes was 2628°C (Vladimirov, 1960). Metacercariae were infective in young

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Cyprinidae after 3 months at 16°C and 1 month at 24°C (Vladimirov, 1960). At 22°C they were infective at 35 days (Donges, 1964). Metacercariae survived the cold season in fishes (Bauer et af., 1964; Donges, 1964) and had a longevity of at least 3 years and 5 months (Donges, 1964). In the Lower Volga, the dissemination of the species was furthered by the longevity of metacercariae in fishes that migrated long distances (Kamenskii, 1971). Seasonal records of metacercariae included those of Pearse (1924) from Perca juviatilis in the Yahara River Lakes, Wisconsin, U.S.A. June 1917 to May 1918, Dubinina (1949) from Abramis brama and Cyprinus carpi0 in the Volga Delta, U.S.S.R., spring and summer 1940 and winter and spring 1941, Komarova (1 964) in Abramis brama, Blicca bjoerkna, Pelecus cultratus, Rutilus rutilus heckeli and Vimba vimba vimba natio carinata in the Dnepr Delta, U.S.S.R., Marits and Vladimirov (1969) in V. v. vimba natio carinata and Marits and Tomnatik (1971) in A. brama at the Dubossary Reservoir, Moldavia, U.S.S.R. Kamenskii (1969) provided data for young A. brama, Alburnus alburnus and Rutilus rutilus caspicus for March to November in the Volga Delta. He observed the highest incidence in 1-2 year old Cyprinidae (Kamenskii, 1971). Posthodiplostomum minimum (MacCallum, 1921) According to Hoffman (1967) in experimental infections a cyprinid line will not infect centrarchids and a centrarchid line will not infect cyprinids and other fish families. It was suggested therefore that this species complex consisted of at least two subspecies, P. minimum centrarchi and P. m. minimum (in cyprinids). The seasonal studies reported relate to P. minimum centrarchi. In normal conditions, the life cycle of P. minimum required about 4 months for completion (Yamaguti, 1975). The cercariae were not released from the mollusc hosts Physa gyrina and P. sayii below 15°C and they were not invasive at this temperature. They emerged at 18°C and above and were infective at 18-27°C (Hoffman, 1958). Spall and Summerfelt (1969, 1970) examined the occurrence of metacercariae of P. minimum in Pomoxis annularis in Lake Carl Blackwell, Oklahoma, U.S.A. Male fish had a statistically higher infection than females in summer, autumn and winter samples, but in the spring there was no statistically significant difference. However, analysis of the data for the whole year, when the fish were stratified by age, season and site of capture, showed that there was no significant variation between sexes in infection by metacercariae. In both sexes the incidence of metacercariae was greater in the summer than at other seasons. The rise in spring and summer was related to the expected increase in numbers of infected snails and the release of cercariae (see Hoffman, 1958, above). The decrease in the average intensity of infection observed during the summer by Spall and Summerfelt (1969, 1970) was attributed to mortality of heavily infected fish. It implied that host mortality was proportional to the number of invading cercariae. A decline in incidence was seen in early autumn, followed by a decline in intensity 1 month later. Thereafter incidence gradually increased through late autumn, winter and spring. Spall and Summerfelt (1969, 1970) postulated that this seasonal pattern may have resulted from a summer mortality of

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P. annularis, owing to high intensity of cercariae, followed by a gradual rise in the incidence of infection, owing to the presence of low numbers of cercariae during the remainder of the year. The establishment of an equilibrium between the numbers of successful invasive cercariae and the numbers of degenerating metacercariae was indicated by the stability found in the average intensity through the autumn and winter (Spa11 and Summerfelt, 1969, 1970). In older fish increased incidence, but constant intensity, supported the establishment of an equilibrium. McDaniel and Bailey (1974) studied P. minimum metacercariae in Lepomis cyanellus, L. humilis, L. macrochirus and L. megalotis at Little River, Buncombe Creek and Lake Texoma, Oklahoma, U.S.A. The incidence of infection declined sharply through March, to be followed by a gradual increase throughout the remainder of the year. Cloutman (1975) examined Lepomis gulosus, L. macrochirus and Micropterus salmoides at Lake Fort Smith, Arkansas, U.S.A. The results were tabulated as average number per fish, but are difficult to relate to the other data reported here. Hoffman (1950) observed that the metacercariae of P. minimum survived at least 11 months in naturally infected fish kept in aquaria, and Hoffman (1958) stated that they lived for at least 16 months. The infectivity of the metacercariae of P. minimum to chicks after exposure to low and high temperatures was assessed by Colley and Olson (1963). The Lepomis macrochirus were treated as follows: one group was kept at 15-20°C (room temperature), one cooled to 1.5"C, one to 3~5°Cand two heated to 36°C. Temperature changes of about 1°C were made daily, and the experimental temperatures maintained for 48 h before recovery of metacercariae, which were then fed to l-day-old unfed chicks. Each chick received 150 metacercariae from one of the groups of fishes. At 72 h post-infection egg-bearing adult P. minimum were recovered, the percentage survival rate for each temperature being: 1.5"C, 3.7 %; 3.5"C, 36%; room temperature, 63.6%; 36"C, 21.9%. Colley and Olson (1963) concluded that the figures indicated an optimum temperature at which the metacercariae were most viable, apparently within the normal range of temperature of Lower Otay Reservoir, California (10-29°C) and probably close to the optimum temperature range for L. macrochirus. Since the reservoir never reached the extremes of temperature achieved in the experiments, they concluded that the metacercariae of P. minimum from the reservoir probably were infective to herons the year round with a high survival rate. However, further experiments were made by Kellogg and Olson (1963). The infectivity of the metacercariae was tested after maintenance at various temperatures in vitro, and a comparison was also made of infectivity of metacercariae from various organs within the fishes. The temperatures in vitro, and the average number of adult P. minimum recovered from chicks were: 1*5"C, 15.11; 4"C, 3.44; 5"C, 5 . 5 ; 1O"C, 14.33; 22"C, 1.08; and 36"C, 0.25. An average of 37.5 adults were obtained from metacercariae (100 to 150) fed directly from L. macrochirus kept at 22°C. Thus maintenance in vitro reduced infectivity. Metacercariae from the liver were more infective than those from the kidney of L. macrochirus. Kellogg and Olson (1963) concluded that the temperature affected

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the larval parasites only indirectly through the metabolism of the fish host. The metabolic activity of the organs from which the cysts originated was considered to influence the infectivity of the P. minimum metacercariae. Spall and Summerfelt (1969) had observed that cysts in winter were less viable, smaller and more opaque with less active larvae, than those seen from late spring and summer. The presence of old and degenerated cysts together with fresh and viable cysts from late spring collections indicated a recurring seasonal infection. Tylodelphys clavata (Nordmann, 1832) Diplostomulum clavatum is included here, on the basis of the studies of Kozicka and Niewiadomska (1960) and Niewiadomska (1960, 1963a,b,c, 1964). It should be noted, however, that doubts about the identity of these metacercariae as T. clavata were formerly expressed, for example, by Bykhovskaya-Pavlovskaya and Petrushevskii (1959, 1963) and Sudarikov (1 960). Seasonal studies have been carried out on T. clavata metacercariae (as D. clavatum) by Banina and Isakov (1972), Bogdanova (1958), Dubinina (1949), Izyumova (1958, 1959a, 1960), Kashkovski (1967), Komarova, T. I. (1964), Lyubina (1970), Malakhova (1961), Marits and Tomnatik (1971), Rautskis (1970a,b), Vartanyan and Mkrtchyan (1972) and Vojtkova (1959), and under the name T. clavata by Kennedy and Burrough (1977), Molnar (1966), Wierzbicki (1970, 1971) and Wootten (1974). In some species of fishes in some habitats, occurrence of metacercariae of T. clavata was sporadic, as in the following instances : Gasterosteus aculeatus, 80 % incidence July, 8 % September, not found in the remainder of the year, Pungitius pungitius, 15.4 % September, not found during other months, River Neva Delta, U.S.S.R. (Banina and Isakov, 1972); Abramis brama, JulyAugust 6.6 %, not found February-March, May, River Volga, U.S.S.R. (Bogdanova, 1958); Abramis brama, found winter, not spring or summer, River Volga Delta, U.S.S.R. (Dubinina, 1949); Lucioperca lucioperca, January-April, 3.7 %, not found May-August, October-November, Pelecus cultratus, January-April, 3.8 %, not found May-July, or October-November, Rybinsk Reservoir, U.S.S.R. (Izyumova, 1958); Abramis ballerus, autumn, 5.8 :(, not found winter, spring, summer, Blicca bjoerkna, autumn, 4.3 %, not found winter, spring or summer, Rybinsk Reservoir, U.S.S.R. (Izyumova, 1960); Lucioperca lucioperca, June, 26.6 %, July/August, 33.3 %, not found April, May, October, Pelecus cultratus, March, 6.6 %, not found February, April/May, July/August or October, Dnepr River Delta, U.S.S.R. (Komarova, T. I., 1964); Tinca tinca, spring only, not found winter, summer or autumn, Lake Bol’shoe, Omsk Region, U.S.S.R. (Lyubina, 1970); Abramis brama, summer, 6%, not found spring or autumn, Dubossary Reservoir, Moldavia, U.S.S.R. (Marits and Tomnatik, 1971); and Gymnocephalus cernua, May only, Lake Balaton, Hungary (Molnhr, 1966). In these examples the low incidence can be attributed to a number of non-seasonal factors. In species of fishes with a high incidence and intensity of T. clavata metacercariae, in general there were no marked changes over the year. Such

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examples are: Abramis brama, Dnepr River Delta, U.S.S.R. (Komarova, T. I., 1964); Blicca bjoerkna, Dnepr River Delta, U.S.S.R. (Komarova, 1964); Carassius auratus gibelio, Lake Bol’shoe, Omsk Region, U.S.S.R. (Lyubina, 1970); Coregonus lavaretus ludoga, C. lavaretus maraenoides, Lake Sevan, Armenia, U.S.S.R. (Vartanyan and Mkrtchyan, 1972); Esos lucius, Rybinsk Reservoir, U.S.S.R. (Izyumova, 1960), Dnepr River Delta, U.S.S.R. (Komarova, T. I., 1964), Lake Konche, Karelia, U.S.S.R. (Malakhova, 1961), and Lake Dusia, Lithuania, U.S.S.R. (Rautskis, 1970b); Gasterosteus aculeatus, Hanningfield Reservoir, Essex, England (Wootten, 1974); Gymnocephalus cernua, Rybinsk Reservoir, U.S.S.R. (Izyumova, 1959a), Hanningfield Reservoir, Essex, England (Wootten, 1974) ; Lota Iota, Lake Konche, Karelia, U.S.S.R. (Malakhova, 1961); Perca jluviatilis, Rybinsk Reservoir, U.S.S.R. (Izyumova, 1958), Lake Konche, Karelia, U.S.S.R. (Malakhova, 1961), Lake Dusia, Lithuania, U.S.S.R. (Rautskis, 1970a), Hanningfield Reservoir, Essex, England (Wootten, 1974); Rutilus rutilus, Rybinsk Reservoir, U.S.S.R. (Izyumova, 1959a), lriklin Reservoir, U.S.S.R. (Kashkovski, 1967), Lake Konche, Karelia, U.S.S.R. (Malakhova. 1961), Hanningfield Reservoir, Essex, England (Wootten, 1974); R. r u t i h heckeli. Dnepr River Delta, U.S.S.R. (Komarova, T. I., 1964); and Salmo trutta, Hanningfield Reservoir, Essex, England (Wootten, 1974). The biology of Tylodelphys clavata in Perca fluviatilis at Slapton Ley, Devon, England (Kennedy and Burrough, 1977) is of special interest owing to the appearance of the parasite in the habitat immediately before the study. T. clavata was absent from the lake from 1961 to 1973. It was found in October 1973, its appearance probably being related to the resumption of breeding by the definitive host Podiceps cristatus. The incidence of T. clavata declined from November 1973 until all the metacercariae had disappeared by July 1974. A new period of incidence commenced in August 1974 and it increased until November, to decrease thereafter to reach its lowest level (60%) in April 1975. By October 1975, 100% ofthe P.fluviatilis were infected. Kennedy and Burrough (1977) suggested that the decline in incidence in both years between November and April represented a loss of metacercariae, and that the increase in late summer was owing to this time being the main period of infection by cercariae. Kennedy and Burrough (1977) considered it probable that T. clavata was an annual parasite, with a life span of 1 year, that infected the fish in the summer of 1 year and died in the next. This cycle was evident in the first year after the occurrence of the parasite in Slapton Ley, but was obscured by increased variation in development times and infection periods in subsequent years (Kennedy and Burrough, 1977). Seasonal periodicity of invasion by cercariae of T. clavata can be seen in young or stocked fishes. Wootten (1974) observed the progressive infestation of 2-year-old Salmo gairdneri stocked into Hanningfield Reservoir, Essex, England. There was an increase in incidence of T. clavata from 16.7 % in May up to 100% by September, although the mean intensity did not exceed 6.0 per fish. The water temperature in the reservoir was above 10°C from April to November, and Wootten (1974) postulated a release of cercariae from May through to November.
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Seasonal changes in the occurrence of T. clavata metacercariae in Perca puviatilis in littoral, shallow and deep waters of Lake Dargin, Poland were studied by Wierzbicki (1971); they were present in all zones through the year. T. clavata metacercariae were most abundant in the littoral zone, with a 100 % incidence in all months, and of slightly lower incidence in P. JIuviatilis in the shallow and deep zones. Lucky (1973) also observed higher incidence and intensities of T. clavata in P.Jluviatilis in still bodies of water than in rivers or deep lakes. Tylodelphys podicipina Kozicka and Niewiadomska, 1960 Wierzbicki (1970) did not note any seasonal changes of infestation in Perca Jluviatilis in Lake Dargin, Poland. At Hanningfield Reservoir, Essex, England, Wootten (1974) found T. podicipina metacercariae in Gymnocephalus cernus, Perca jluviatilis and Salmo gairdneri. There was no evidence of seasonal patterns of incidence. The majority of metacercariae occurred in P. Jluviatilis in the first year of life, after which the metacercariae apparently survived for about 2 years before disappearing. Uvulifer ambloplitis (Hughes, 1927) The metacercariae of U . ambloplitis in Lepomis cyanellus and L. humilis in Little River, Buncombe Creek and Lake Texoma, Oklahoma, U.S.A. had a maximum incidence in January (about 80 %), thereafter falling t o nothing by September (McDaniel and Bailey, 19743. The absence of increased incidence in September was attributed to the lack of opportunity of the host to form the black melanin deposit by which means the metacercariae were counted. There was an increase in metacercariae through the life span of the fish owing t o repeated periods of recruitment. McCoy (1928a) noted that U . ambloplitis metacercariae developed more slowly at low temperatures. Hoffman and Putz (1965) confirmed that the larvae developed to only a slight degree when the fish hosts were kept a t 12-13"C, after infection at summer temperatures (24°C). At 1 3 ° C growth was inhibited considerably and after 92 days there was little growth, but at 20°C, maturity was achieved by 43+ days and in 22 days at 24°C. Metacercariae maintained at 12°C were still alive after 44 years. Hoffman (1953) observed that U . ambloplitis metacercariae were acquired during the first 2 years of life of the host, and that the small fish had an average intensity of infection similar to that of larger fish. Krull (1934a) studied metacercariae tentatively identified as I/. (Neascus) ambloplitis and noted that they degenerated in June.

5. Family Echinostomatidae Echinochasmus beleocephalus (Linstow, 1875) This species was studied by Yoshino (1940) in Carassius auratus at Okayama Province, Japan (as E. japonicus). The annual fluctuations in incidence of metacercariae were considered t o be largely dependent on temperature. Echinostoma (species undetermined) Molnhr (1966) noted a single incidence of this undetermined species in Gymnocephalus cernua at Lake Balaton, Hungary in June 1960. I t was not found during the other 9 months.

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6. Family Heterophyidae

Apophallus muehlingi (Jagerskiold, 1889) The seasonal occurrence of the metacercariae of A . muehlingi has been studied by Komarova, T. I. (1964) and Molnar (1966). In Blicca bjoerkna from the Dnepr River Delta, U.S.S.R. incidence was 0 % in February, 6.6 % in March, 20% in April, 13.2% in May, 18.7% in June and 6.6% in October. Intensity of occurrence was maximal in May and June, 4-6 and 2-6 respectively (Komarova, T. I., 1964). The incidences in Gymnocephalus cernua from Lake Balaton, Hungary were: 1960, June, July, 0 % ; August, 31.2%; 1961, January, 50%; February, 15.6%; May, 38%; June, 0 % ; July, 50%; August, 78.2 %; October, 100% (Molnar, 1966). Molnar (1966) additionally observed the incidence in Lucioperca lucioperca, May to October, in fry and young. The details were: fry, 20-75 mm, May-July, not found, 55-75 mm, August, 28.5 %; young fish, 64-190 mm, July, 14.3 %, August, September and October, not found. Komarova, T. I. (1964) found the metacercariae in L. lucioperca in the Dnepr River Delta in April (6.6%) only. Molnhr (1968) recorded a similar minimal incidence (3.7%) in Phoxinus phoxinus from Teich T., Lake Balaton, Hungary, in September. Exorchis oviformis Kobayashi, 1915 Yoshino (1940) studied this species in Carassius auratus from Okayama Province, Japan. Lee (1968) examined four species of fishes, Gnarhopogon coreanus, Pseudogobio esocinus, Pseudorasbora parva and Pungtungia herzi from the Kum-Ho River, Korea. The incidence of metacercariae in spring did not differ significantly from autumn. Metagonimus yokagawai (Katsurada, 1912) Includes Metagonimus takahashii Suzuki, 1929 (see Komiya, 1965). Yamaguti (1939) observed that black-pigmented areas around metacercariae were especially apparent in winter on the scales and fins of Carassius carassius and Milvus migrans lineatus in Japan. When the metacercariae were experimentally fed to cats and kites, eggs of M . takahashii and M . yokagawai were recovered. Yoshino (1940) noted the annual fluctuations of metacercariae of M . takahashii in Carassius auratus in Okayama Province, Japan, which were believed to be largely dependent on temperature. Komarova, T. I. (1964) observed the incidence and intensity of infection of six species of fishes by the metacercariae of M . yokagawai in the Dnepr River Delta, U.S.S.R. The examinations were carried out February to October. No consistent pattern of occurrence was seen in four fish species. In Abramis brama, no metacercariae were noted in March and October, maximum incidence (21.3 %) was in July/August, otherwise it was fairly constant, in April 6.6 % and in February, May and June, all 13.2 %. Similar incidences were noted in Blicca bjoerkna, minimum (6.6 %) in February, April and October and maximum incidence in March 40%, otherwise May 20% and June 25%. With Lucioperca lucioperca, incidence was 6.6% in April, May, July/August and October, 0 % in June, and Pelecus cultratus also showed a similar situation, 6.6 % in March and October, but higher (13.2 %)

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in July/August, and 0 % in February and April/May. In contrast t o the above species of fishes, Riitilus rutilus heckeli and Virnba vimba vimba natio carinata demonstrated a pattern of incidence: R. rutilus heckeli, February OX, March and April 6.6%, May 13.2%, June 53.3%, July/August 26.6% and October 6.6 %; V . v. vimba natio carinata, February 0 %, March 6.6 %, ApriI/May I2 %, June/July 20% and October 13.2%. Metagonimus (species undetermined) Lee (1968) studied a n undetermined species of Metagonimus in four species of fishes in the Kum-Ho River, Korea, but stated that the incidences seemed not to be influenced by the seasons, spring and autumn. Pseudoexorchis major (Hasegawa, 1935) Yoshino (1940) related the seasonal fluctuations of the metacercariae in Carassius auratus from Okayama Province, Japan t o temperature. The species was given as Exorchis major. I . Family Nanophyetidae Nanophyetus salmincola (Chapin, 1926) The seasonal data available for this species pertains to young Oncorhynchus kisutch and Salmo gairdneri from three coastal streams in Oregon, U.S.A. Millemann and Knapp (1970) reported that Mr. J. Bender, their student, had collected fishes from March through October and found that few 0. kisutch that emerged from the gravel in March were infected, but that all fishes collected in mid-April and thereafter were infected. The average number of parasites per fish, and per gram of fish, increased rapidly from mid-April until early July, then the infection level tended t o be stable until early September, when a further increase occurred. Bender observed that S. gairdneri emerged from the gravel in mid-April and all fish collected then, and subsequently, were infected. The intensity of infection of 0. kisutch and S. gairdneri, 50-60 mm long in September, was 400-1565 and 1735-2002 respectively. Farrel (personal communication in Hoffman and Putz, 1965) noted that the metacercariae lived at least 3 years in salmon. Farrel et a/. (1964) kcpt Oncorhynchus kisutch infected with metacercariae in seawater at Bowmans Bay Station, near Anacortes, Washington State, U.S.A. for up to 33t months. Control fishes demonstrated that infection did not occur during this time. Tests at 12, 24 and 33: months, by feeding metacercariae to experimental dogs, demonstrated the continued infectivity of the metacercariae. A tagged Oncorhynchus tshauytscha was recovered from the Elokomin River, Washington State, after 4 years at sea. Viable metacercariae were seen in its kidneys; these were fed to a dog which became sick and died. Adult N . salmincola were found at post-mortem examination.

8. Family Opisthorchidae Clonorchis sinensis (Cobbold, 1875) The annual fluctuations of metacercariae in Carassius auratus in Okayama Province, Japan were largely related t o temperature (Yoshino, 1940). The

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observations of Huang and Khaw (1964) confirmed this. At Kongkuan-pei (lake), Taipei, Taiwan the incidence and intensity of infection of Pseudorasbora parva was: summer (June-August) incidence loo%, intensity 418 metacercariae per fish (average) ; autumn (September-November) 96.6 %, 309 per fish; winter (December-February) 80%, 96 per fish; and spring (March-May) 83.3 %, 227 per fish. There was a sudden increase in intensity of infection in May, from 152 per fish (average) in April to 313 per fish in May. Cercariae changed to metacercariae in 1 month, hence invasion by cercariae was postulated from April when the weather became warm. In the Kum-Ho River, Korea the incidence of metacercariae of C. sinensis in Gnathopogon coreanus, Pseudogobio esocinus, Pseudorasbora parva and Pungfungia herzi was high, and was essentially the same in spring and autumn. There was an increased intensity of infection related to length (Lee, 1968). Fang and Lin (1975) studied Carassius auratus, Hemiculter kneri and Pseudorasbora yarva in Sun Moon Lake, Taiwan. In H . kneri the incidence was 100% throughout, but intensity was heavier in August 1973 than in April 1973 or November 1974. Opisthorchisfelineus ( Rivolta, 1884) According to Bauer (1959a) the development of 0. ,felineus was studied in great detail by Kh. Fogel' in the Kaliningrad Region, U.S.S.R. In the mollusc Birhynia learhi, cercarial emergence commenced towards the end of the second month post-infection. However, in western Siberian conditions, at 18-20°C, Goryachev (1958) observed that cercariae matured only after 10-12 months. Bauer (1959a) attributed this difference to the milder climate of the Kaliningrad Region compared with western Siberia. In western Siberia the continental climate produced low night temperatures in the short summer, thus larval development was completed in the spring after invasion. According to Fogel' and Goryachev, at 1 8-20°C, the metacercariae were infective 40-42 days after invasion (Bauer, 1959a). The minimal duration of the life cycle was 45 months. Goryachev (1958) studied the occurrence of the metacercariae of 0.felineus in the flood plains of the Rivers Irtysh and Om, Siberia, U.S.S.R. Thedevelopment and infection of cyprinids by this parasite were decisively influenced by the level of the flood in the river, its duration and the degree of filling of the bottomland water reservoirs. The level of the flood promoted, or prevented, the eggs of 0. ,felineus from reaching the reservoirs and thereby infecting the snails and fishes with the larvae. In dry years, 1951 for instance, the reservoirs were disconnected from the rivers, or dried out completely, and the fishes caught in the rivers were uninfected, whereas 12 % were infected in wet years. According to Goryachev (1958) the metacercariae remained in the fishes for a number of years. Komarova, M. S. (1957) studied the occurrence of 0. ,felineus in Tinca tinca in the Donets River, U.S.S.R. The incidence varied little, 1952, April 3.3%, July 3.3%, October 5%, December 3.3%, 1953, April 5.0%, July 3.3%, but fell to 0 % in October and December, 1953. In the Dnepr River Delta, U.S.S.R., Komarova, T. I . (1964) examined the infections in Abramis brama and Pelecus cultratus. In both species incidence

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was 0 % in February and March. In A. brama in April and May it rose to 33.3 % (intensity 4-8) and 26.6 % (3-10) respectively, and in P. cultratus April/ May the infection was 22.2% (3-12). In June the infection of A. brama was 33.3% (2-14), but P. cultratus was not examined. In July/August the infections of A. brama were 14.2 % (2-14) and P . cultratus 33.3 % (2-1 l), however, the occurrence returned to 0 % in both species of fishes by October. Pseudamphistornum truncatum (Rudolphi, 1819) The metacercariae were recorded in Blicca bjoerkna from the Dnepr River Delta, U.S.S.R. by Komarova, T. I. (1964). The incidences (and intensities) of infection were: February, 13.2% (4-6); March, 26.6% (3-9); April, 0 % ; May, 26.6% (3-1 1); June, 49.6% (3-8); and October, 18.6% (4). 9. Family Prohemistomatidae Prohemistomulum (species undetermined) Mishra (1966) observed an undetermined species of Prohemistomulum in the fins and muscle of Esox lucius in the Shropshire Union Canal, Backford, Cheshire, England. Incidence was lowest (12.5 %) in July-September, highest (42.8 %) in October-December, and at an intermediate level in JanuaryMarch (28 %) and in April-June (25 %). 10. Family Strigeidae Apatemon gracilis (Rudolphi, 1819) Three types of metacercarial cyst were distinguished in Gasterosteus aculeatus from near Vancouver, British Columbia, Canada by Lester (1974). Type 1 occurred mainly in muscle tissue, but rarely in the body cavity, type 2 was in the brain and body cavity and type 3 in the eye. In Queen Elizabeth Park, type 2 was found in over 30% of the fish for several years, but type 1 was rare. N o further details of seasonal occurrence were given. lchthyocotylurus erraticus (Rudolphi, 1808) Includes Tetracotyle intermedia Hughes, 1928 according to Olson (1970), although he noted that the Russian T, intermedia as described by Bykhovskaya-Pavlovskaya in Bykhovskaya-Pavlovskaya et a/. (1962) differed from the specimens of Hughes (1928) and his material. However, Razmashkin (1963, 1966) related T. intermedia metacercariae from Lake Pskov-Chud, U.S.S.R. to I. erraticus by experimental feeding to gulls. Niewiadomska and Kozicka (1970) also experimentally confirmed that T. intermedia from Poland corresponded to I . erraticus. Bauer and Nikol’skaya (1957) reported the occurrence of T. intermedia in Coregonus lavaretus baeri natio ladogae in Lake Ladoga, U.S.S.R. from July to November. Minimal occurrence was in July (incidence 18 %, intensity average 0.4) with a peak in September (80%, 10.3) and falling through October to November (20%, 1). At Lake Sevan, Armenia, U.S.S.R., Vartanyan and Mkrtchyan (1972) examined Coregonus lavaretus ludoga and C. lavaretus maraenoides for the metacercariae of T. intermedia. There was a 100 % incidence in all seasons (May, June-July, October-November and

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December-January) with a peak intensity in October-November of 11 to 302 metacercariae (average 78.2). The incidence and intensity of infection of 1. erraticus in Oncorhynchus kisutch, Salmo gairdneri and Thymallus arcticus that had inhabited Georgetown Lake, Montana, U.S.A. for less than 6 months were examined by Olson (1970). In July, 1 to 2 months post-stocking, the infections were: 0. kisutch 50 %, 0-2 metacercariae, S. gairdneri 69.2 %, 0-1 3, T. arcticus 83.3 %, 0-30. By September, 4 to 5 months post-stocking, the incidence was 100% for the three species of fishes, with intensities of 125-200 (average 160) for 0. kisutch, 38-250 (average 97) for S. gairdneri and 85-600 (average 275) for T. arcticus. The surface water temperature of the lake, July to September, was 18-21°C. In laboratory maintained S. gairdneri the metacercariae encysted in 2-3 weeks at 21°C. The lake was ice-covered usually from midNovember to mid-May, but at least some molluscs, Valvata lewisi, carried the infection over the winter, as the stocked fish became infected in early July. In the British Isles, Campbell (1974) observed the incidence of I . erraticus in Salmo trutta in Loch Leven, Scotland. During 1967 to 1970, there was a lower level of incidence (50-60%) during the summer months, with a high incidence (90-100%) during the winter. However, from late 1970 to the end of the period of observation, this pattern was replaced by widely differing values (from 30 to 90 %) occurring over the whole year. In general, S . trutta of length over 29.5 cm had a 70-100 % incidence of metacercariae throughout. Wootten (1973a) studied the infection of Salmo gairdneri and S. fruffa in Hanningfield Reservoir, Essex, England. Both species of fishes were stocked into the reservoir in April, 1968. They were uninfected in May, but metacercariae were found in June. Wootten (1973a) suggested that release of cercariae must have commenced in late May or early June (water temperature 12-15°C). Infection continued throughout the summer and early autumn. Wootten (1973a) postulated that the majority of infections in the fishes in Hanningfield Reservoir resulted from cercariae released from snails that had survived the winter carrying the parasite. In S. trutta the incidence rose from 12.5% in June to 100% in November (intensity from 1.0 in June to a maximum of 19-0 in September) for newly stocked 2 + fish. In s. gairdneri the incidence varied in an irregular manner throughout the year, 100% in March and July, minimal in May at 8.3 %. Mean intensity ranged from 5.8 in June to 134-0 in May. Successive infections were superimposed, with an increase in incidence and intensity of infection as the fish aged. Ichthyocotylurus pileatus (Rudolphi, 1802) Includes Tetracofyle variegata (Creplin, 1825) according to BykhovskayaPavlovskaya and Petrushevskii (1 959, 1963). Razmashkin (1963, 1966) related T. variegata and T. diminuta to I. pileatus in Lake Pskov-Chud, U.S.S.R. The seasonal occurrence of T. variegafa has been studied by Dubinina (1949) in the Volga Delta, and Bogdanova (1958) in the River Volga, U.S.S.R., Izyumova (1958, 1959a, 1960) in the Rybinsk Reservoir, U.S.S.R. and Malakhova (1961) in Lake Konche, Karelia, U.S.S.R. Dubinina (1949) found metacercariae in the Volga Delta in Abramis brama (6.7%) in spring 1941,

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but not in the spring or summer of 1940 or the winter of 1941. However, in

Lucioperca lucioperca from the same locality an incidence of 13.3 % occurred

in summer 1941,20% in winter and 13.3% in spring 1941. Bogdanova (1958) examined A . brama in July/August 1956,February/March and May 1957 and found metacercariae in February/March and May. Esox Iucius were examined in August 1956, February/March and May 1957 and metacercariae were present in May and August. Izyumova (1958) investigated Abramis brama, Lucioperca lucioperca and Pelecus cultratus for the periods January-April, May-August (May-July for P. cultratus) and October-November. In A. bratna there was no infection January-April, with a peak incidence (26.4%) in October-November. In P. cultratus the incidence was low January-April (3.8%) and May-July (3.5%) but again higher in OctoberNovember (37.5%). With L. Iucioperca maximum incidence was JanuaryApril (44%), minimum in May-August (3.7%) and higher again in OctoberNovember (18.7%). In Gymnocephalus cernua there was a 100% incidence in all seasons and a high intensity throughout (Izyumova, 1959a). By contrast, Rutilus rutilus had a low incidence and intensity in the spring and autumn only (4.7%, 1 and 4.3%, 3 respectively) and the parasite was not found otherwise (Izyumova, 1959a). Abramis ballerus had a low autumn infection only (1 1.7 1-2) and Blicca bjoerkna a high winter infection (46.6%, l-9), a low spring infection (5%, 2), no metacercariae were found in summer, but there was a high infection in autumn (39%, 2-12) (Izyumova, 1960). Malakhova (1961)recorded a low infection of T. variegata (l.14%, I ) in summer in Esou lucius in Lake Konche. Komarova, T. I. (1964)examined seven species of fishes from the Dnepr River Delta, U.S.S.R. and found metacercariae of fchthyocotylurus pileatus in them all. Blicca bjoerkna was infected throughout the year (FebruaryJune, October), minimum incidence in April (6.6%), maximum in March (53.3%). Abramis brama had a maximal incidence in March (20%), was not found at all in February and June and otherwise had a low incidence (6.6%. April, May, October; 7.1 %, July/August). Rutilus rutilus heckeli was not infected in February t o April or October, but had low incidences in May (6.6%) and July/August ( 1 3.2%) with a maximum occurrence in June (20%). Pelecus cultratus was not infected February, but the incidence increased thereafter (March, 6.6%; April-May, 16.6%) t o a peak in July-August (26.6%) to fall again by October (6.6%). Esox lucius, Lucioperca lucioperca and Vimba vimba vimba natio carinata all had low incidences, E. lurius March only (2073,L. lucioperca July/August and October only (6.6% in each instance) and V . vimba vimba natio carinata June/July and October only (again 6.6% on each occasion) (Komarova, T. I., 1964). Also in the U.S.S.R., Lyubarskaya (1970)examined Abramis brama from the Kuybyshev Reservoir. Maximal incidence was in winter (46.6%), minimal in summer (8.6%) and an intermediate level occurred in spring (20.5%) and autumn (28.5%). As a complete contrast, Marits and Tomnatik (1971) found metacercariae of I . pileatus in A. brama at a low incidence (473, in summer only, at Dubossary Reservoir, Moldavia. In Lake Dusia, Lithuania, Rautskis (1970a) found Perca jfuviatilis t o be infected January-

x.

HELMINTHS IN FRESHWATER FISHES

189

March (46.6%), not in April-May, and infected June-July (74.4%) and October-November (74.4 %). At Lake Balaton, Hungary, Molnar (1 966) investigated Gytmocephalus cernua June-August, 1960 and February, June-August and October, 1961. A low incidence of I . pileatus metacercariae was found in January (3.3 %) and In May (4%) only. There is a very marked contrast between the high incidence of metacercariae in G. cernua in the Rybinsk Reservoir (100% throughout) (Izyumova, 1959a) and the very low incidence in Lake Balaton (Molnar, 1966). Ichthyocotyhus p/atycephaltrs (Creplin, 1825) and fchtl~yocotylurusrariegatus (Creplin, 1825) Razmashkin (1966) fed Tetracotylepercae~uviaiilis, found in Gymtiocephalus cernua and Percapuviatilis from Lake Pskov-Chud, U.S.S.R., to gull chicks and they developed into adult I . platycephalus. Rautskis (1968) stated that 70 % of all the Tetracotyle cysts from P. juviatilis in the Kurskiy Zaliv and Kaunas reservoirs in Lithuania, U.S.S.R. were T. percaepuriatilis. In the gull, Larus ridibundus, an experimental infection of 165 cysts resulted in the recovery of 109 I. platycephalus, 41 1. pileatus and one Cotylurus syrius. As 1. platycephalus was predominant, Rautskis (1968) considered it to be the adult form of T. percaefluviatilis. Odening et a/. (1969) demonstrated the life cycle of 1. platycephalus. The metacercariae were encysted in the body cavity, mainly close to the heart, in Gymtiocephalus ceriiua, Lucioperca lucioperca and Osrnerus eperlatius. However, Odening and Bockhardt (197 1) also experimentally demonstrated the life cycle of fcl~thyocoty/uruswriegafus. In this instance they stated that the metacercariae occurred in G y n i ~ ~ o c e p l ~ acertiua, lus Perca fluviatilis and Lucioperca lucioperca and were known as Tetracotyle percaejuviatilis. Dubois (1968, in litt., quoted from Blair, 1977) did not consider Cotylurus (I.) variegatus a valid species, but Blair (1977) agreed with Odening and Bockhardt (1971) that it was a distinct species, on the basis of his own observations (Blair, 1974 Ph.D. thesis, quoted from Blair, 1977). Owing to the divided opinions, and the allocation of the metacercariae of Tetracotyle percaejuviatilis to both adult species, they are included together i n this review. Bogdanova (1958), lzyumova (1958) and Malakhova (1961) presented some seasonal data about the occurrence of the metacercariae of T. percuefluviatilis. Bogdanova ( 1 958) found the metacercariae in Abramis brama and Esox lucius in the River Volga, U.S.S.R. It occurred in A . brarna in J u l y / August, 1956, but not i n FebruaryIMarch or May, 1957. In E. lucius it was noted in February/March, 1957, but not in August, 1956 or May, 1957. Izyumova (1958) found incidences in Perca j u v i a t i l i s at the Rybinsk Reservoir, U.S.S.R. in January-April (46 %), May-July (73.3 %) and OctoberNovember (30%). Fishes were not examined during other months. Malakhova (1961) examined P. j u v i a t i l i s in Lake Konche, Karelia, U.S.S.R. at all seasons. Metacercarial incidence varied little, autumn 94.4 %, winter 95.7 %, spring 95.5 % and summer 94.4 %; however, maximum intensity of infection was in the spring, 1-219, average 52.7 metacercariae.

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Rautskis (1970a) found an incidence of Ichthyocotylurus platycephalus metacercariae in Perca JIuviafilis of Lake Dusia, Lithuania, U.S.S.R. in all seasons: January-March 80 % (intensity 3-28, average 8.5), April-May 30.7% (1-3, 1.5), June-July 93.3 % (4-19, 9.1) and October-November 80% (2-41, 19.6). Peak incidence was in June-July, but peak intensity was in October-November. Strigeids (species undetermined) Holl, 1932 Holl (1932) observed seasonal occurrence of undetermined strigeid cysts from Lepomis gibbosus and Lepomis gulosus in a settling pond, near Durham, North Carolina, U.S.A. In L. gulosus, the percentage of hosts infected was highest in winter, there being a gradual increase to that maximum during the autumn. In L. gibbosus the cysts were found in all individuals examined. The average intensity of infection was variable, with no periodicity. Tetracotyle (species undetermined) Noble (1970) reported that the incidence of Tetracotyle metacercariae in Percajavescens in Lake Oneida, New York, U.S.A. was greater and they occurred in larger numbers in August and September than at other times. Tetracofyle (species undetermined) Rizvi (1964) found Tetracotyle metacercariae in Perca JIuviatilis at Rostherne Mere, Cheshire, England all year with a variable intensity from month to month. 1 1. Undetermined species of metacercariae Seasonal data on a number of undetermined species of trematode metacercariae are available, for example, in Kornarova, T. I. (1964) and Molnar (1968). These are omitted in this account. Evans, H. E. and Mackiewicz (1958) examined 35 species of fishes from seven families, in New York State, U.S.A. during the period 1 1 November 1949 to 14 January 1950. The 3-month winter sample did not show any pronounced month to month fluctuation in metacercarial cyst counts. Metacercaria hasegawai Yoshino (1940) listed two metacercaria a and c from Carassius auratus in Okayama Province, Japan, and attributed annual fluctuations in the species he studied to temperature changes. Lee (1968) observed M . hasegawai in Pseudogobio esocinus, Pseudorasbora parva and Pungtungia herzi in the Kum-Ho River, Korea. The incidence of the metacercariae was similar for each host species in spring and autumn. There appear to be three species, with the adults unknown, according to Komiya (1965): Metacercaria hasegawai a Komiya and Tajimi, 1941 (unidentified metacercaria A of Hasegawa, 1934); Mefacercaria hasegawai b (metacercaria B of Hasegawa, 1934); and Metacercaria hasegawai c (metacercaria C of Hasegawa, 1934). Metacercaria hasegawai a has cercariae that suggest that it belongs to the Family Heterophyidae (Komiya, 1965). According to Sudarikov (1974) they correspond to Holostephanus metorchis Yamaguti, 1939 (a), H. nipponicus Yamaguti, 1939 ( c ) and Cyathocotyle orientalis Faust, 1922 (b).

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191

IV. SEASONAL STUDIES OF METACERCARIAE I N WORLDCLIMATE ZONES It is suggested (Section V, J) that water temperature may be the most significant factor for understanding the seasonal dynamics of the metacercariae in fishes of the mid-latitude climate zones of the world. Whether this view is correct or not, available temperature data are too limited to permit correlation of the worldwide seasonal patterns of occurrence of the metacercariae. However, climate affects parasites directly with respect to temperature, and temperature is the most important single extrinsic factor to influence parasites (Noble and Noble, 1976). Accordingly, as in the first part of this review (Chubb, 1977), the seasonal studies of the trematodes are related to the major climate zones of the world (Fig. 1, Chubb, 1977). It is hoped that this will gather the species together into meaningful headings. It certainly provides a clear statement of the regions of the world where no seasonal studies of metacercariae have been made. Table 1 lists the studies on seasonal occurrence of metacercariae in the world climate zones. (CLIMATE ZONE 1) As far as the author is aware no seasonal studies on metacercariae have been carried out in the tropical zones of the world. A.

B.

TROPICAL

SUBTROPICAL

(CLIMATE

ZONE

2)

1. Mediterranean (Climate zone 2 a)

Only one species, Diplostomum murrayense, has been investigated in the field. It is relevant that the study was made in the southern hemisphere, so that the summer months are November to May. Cercariae were found rarely in October, then in November to May inclusive. The diplostomulae were observed in November to May, but not in June, August and October. Johnston, T. H. and Angel (1941) suggested that the snails were infected in September and October by eggs that had overwintered in the swamp, or by eggs from the terns that arrived in the area in the spring. Adult worms were seen in terns in November to March. The metacercariae were not found in fishes during the winter months and thus the following seasons infections must have originated from some other source. The process of invasion of the fishes by metacercariae during the warm months was similar to that found in the mid-latitude climate zones (see Section IV C). Metacercariae of Posthodiplostomum minimum were studied by Colley and Olson (1963) from the Lower Otay Reservoir, California, U.S.A., but not in the field. However, they stated that the seasonal range of water temperature was 10 to 29°C. As Hoffman (1958) has shown that the cercariae of P . minimum were infective from 18 to 27°C it should mean that the invasion

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JAMES C . C H U B B

of the fishes in the Lower Otay Reservoir ceased for the winter months when the water temperature fell below 18°C. 2. Humid (Climate zone 2 b) The information available for the species investigated in this climate zone is not extensive. McDaniel and Bailey (1974) found seasonal changes in incidence in Posthodiplostomum minimum and Uvulifer ambloplitis. In P. minimum incidence declined sharply through the winter to March, to be followed by a progressive increase through the rest of the year. The decline in winter was not explained, but it was noted that the incidence increased with fish age. With U. ambloplitis, there was a maximum incidence of metacercariae in January, falling to nothing by September. The zero incidence in September was probably spurious. McDaniel and Bailey (1974) stated that U. ambfoplitis was only visually detectable after the host had had an opportunity to deposit melanin, and this was probably the reason why no increased incidence was detected by September. Lee (1968) studied Cyathocotyle sp., Clonorchis sinensis, Exorchis oviformis, Metagonimus sp. and Metacercaria hasegawai in fishes of the Kum-Ho River, Korea; there was little difference between incidences in spring and autumn. Yoshino (1940) provided data for Cyathocotyle sp., Clinostomum

complanatum, Echinochasmus beleocephalus, Clonorchis sinensis, Exorchis oviformis, Metagonimus yokagawai, Pseudexorchis major and Metacercaria hasegawai a and c and speculated that the annual fluctuations were largely

dependent on temperature. Huang and Khaw (1964) found a clear change in both incidence and intensity of infection with season in Pseudorashova parva in Taiwan. Infections were highest in summer and lowest in winter. A sudden increase in intensity of infection in May was considered to correlate with cercarial invasion commencing in April at the onset of warm weather. Fang and Lin (1975), also working in Taiwan, found 100% incidence throughout the year, but maximal intensity in August. c.

MID-LATITUDE (CLIMATE ZONE

3)

1. Humid warm summers (Climate zone 3 a i) The studies of Bucephalus polymorphus, Rhipidocotyle illense (Baturo, 1977), Hysteromorpha triloba (Hugghins, 1954b), Posthodiplostomum brevicaudatum (Donges, 1965), P. cuticola (Donges, 1964), P. minimum (Spall and Summerfelt, 1969) and Uvulifer ambloplitis (Hoffman and Putz, 1965) have shown in field and experimental conditions that the invasion of fishes by the cercariae occurred during the warm months of the year. Furthermore, the development of the metacercariae in the fish host was speeded up by increased levels of temperature, as in P. brevicaudutum (Donges, 1965), P. cuticola (Donges, 1964) and Uvulifer ambloplitis (Hoffman and Putz, 1965). The

HELMINTHS I N FRESHWATER FISHES

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infective metacercariae have been shown to survive for periods from 5 months, B. polymorphus, R . illense (Baturo, 1977), overwinter, H . triloba (Hugghins, 1954b) and P. minimum (Spall and Summerfelt, 1969) or for a varying period of years, P. brevicaudatum 5 years (Donges, 1965), P. cuticola 34 years (Donges, 1964) and U . ambloplitis at least 44 years (Hoffman and Putz, 1965). In most species the metacercariae served to overwinter the parasite, but Donges (1964) noted that the sporocysts of P . cuticola lived through the winter in the snail host and probably the eggs of the fluke would also survive the cold season. The incidences of metacercariae in fishes in climate zone 3 a i can be divided into three groups. The first group includes the metacercariae that are found all year: Bucephalus polymorphus, Rhipidocotyle illense in cyprinids (Baturo, 1977); strigeid cysts undetermined in Lepomis gibbosus (Holl, 1932); Diplostomum spathaceum in Gymnocephalus cernua (Molnir, 1966), Diplostomulum scheuringi in Lepomis gulosus, L. macrochirus and Micropterus salmoides (Cloutman, 1973, Hysteromorpha triloba in Ictalurus melas (Hugghins, 1954b, 1956), Posthodiplostomum brevicaudatum in cyprinids (Donges, 1965), P. cuticola in cyprinids (Donges, 1964), P. minimum in Lepomis gulosus, L. macrochirus and Micropterus salmoides (Cloutman, 1975) and Pornosis annularis (Spall and Summerfelt, 1969) and Apophallus muehlingi in Gymnocephalus cernua (Molnir, 1966). The second group of metacercariae includes those with a low or sporadic incidence. The low incidence may mean that the fish species investigated was not the principal host, for instance Rhipidocotyle illense in Gymnocephalus cernua (Molnar, 1966), or Diplostomum spathaceum and Apopliallus muehlingi in Phoxitius phoxinus (Molnar, 1968). The rarity of Clitiostomum complanatum metacercariae in PercaJIuviatilis and Rutilus rutilus in Poland was explained by the parasite having a more southern distribution (Grabda-Kazubska, 1974) and the same explanation may apply to its occurrence in G. cernua in Lake Balaton (Molnar, 1966). An explanation was not offered for the sporadic incidences of Ichthyocotylurus pileatus in Abramis brama (Marits and Tomnatik, 1971) or G. cernua (Molnir, 1966), Tylodelpliys clavata in A. brama (Marits and Tomnatik, 1971) or G. cernua (Molnhr, 1966), Mesostephanus appendiculatus in A. brama (Marits and Tomnatik, 1971), Clinostomum marginatum in Lepomis gulosus and L. macrochirus (Cloutman, 1975) and Echinostoma sp. in G. cernua (Molnar, 1966). However, it is suggested that the explanations will be attributable to non-seasonal phenomena. The third group of metacercariae represents those for which winter observations were not made at the particular habitats, Bucephalus polymorphus (Marits and Tomnatik, 1971 ; Marits and Vladimirov, 1969; Vojtkova, 1959), Diplostomum spathaceum, Hysteromorpha triloba (Marits and Tomnatik, 1971), Posthodipfostomum cuticola (Marits and Tomnatik, 1971 ; Marits and Vladimirov, 1969) and Tylodelphys clavata (Vojtkova, 1959). The evidence of their occurrences, spring through to autumn, suggests that the metacercariae were present all year. Detailed comments about seasonal patterns of incidence and intensity are reserved until Section V A.

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JAMES C. CHUBB

2. Humid cool summers (Climate zone 3 a ii) The climate zone covers a large part of the U.S.S.R. where extensive investigations have been carried out. Accordingly a great amount of information is available. Development of the larvae in snails and the infection of fishes by cercariae occurred during the warm months of the year. Salmo salar fry were infected by D. spathaceum metacercariae from July onward through the summer (Bauer, 1957a), and cercarial-induced mortality of fishes was seen from early summer (Bauer et al., 1964). The metacercariae were infective in 15 to 8 months, dependent on water temperatures (Bauer, 1959a). The larvae in the snails overwintered in the Leningrad region (Bauer, 1959a; Mindel, 1963), and cercariae were released in the laboratory during the winter if the snails were kept at 13°C; the metacercariae achieved maturity in 45 to 50 days at this temperature compared with 14 days in summer at 17-20°C (Mindel, 1963). A hot summer facilitated larval development and heavy incidences of D. spathaceum in fishes (Oun and Sirak, 1973); however, the cercariae emerged above 10°C, to a maximum at 18°C (Timmermann, 1936, quoted from Bauer, 1959a). Kasesalu (1974) showed that infection of young Cyprinus carpio by Diplostomum sp. climbed from 0 % in June/July to about 45 % by October, and reached 100% by June the following year. Meyer (1958) also reported a rapid increase in infection of Pimephales promelas by Diplostomulum sp. during summer. Survival of the infection overwinter in snails has been reported above for D. spathaceum, and this probably occurred with Crassiphiala bulboglossa (Hoffman, 1956). Overwintering of the larvae of 0.felineus in snails was also found in Siberian conditions where two summers were needed to complete cercarial development (Bauer, 1959a). However, with Diplostomum scudderi the infection probably did not persist during the cold months in snails (Hoffman and Hundley, 1957) and it did not in Hysteromorpha triloba (Hugghins, 1957). In this latter instance the metacercariae overwintered in the fish host, and an infection of the snails occurred after the return of the cormorants, the definitive host, in the spring (Hugghins, 1957). Most species of metacercariae survive for at least 12 months in the fish host. Crassiphiala bulboglossa metacercariae in a naturally infected host were kept for 37 months and were still alive (Hoffman, 1956). Lester (1977) was of the opinion that metacercariae of Diplostomum adamsi survived the rest of the life of Perca jlavescens, and Tedla (1969, quoted from Lester, 1977) showed survival at 11°C for several months. D. scudderi was kept alive for 1 year and probably survived longer (Hoffman and Hundley, 1957). A considerable amount of information is available for D. spathaceum. It lived at least overwinter (Bauer, 1957a,b) and 9-10 months in some fishes (Bauer, 1959a). Spring infections started to die by autumn in coregonids (Bauer et a/., 1964; Mindel, 1963) but Shigin (1964) showed that they lived longer than 35 years in Rutilus rutilus, a principal host, but less in other species of fishes. Tedla and Fernando (1969) also postulated survival for more than 1 year. Fischthal

HELMINTHS IN FRESHWATER FISHES

195

(1949) showed that only 3 % of Neascus sp. and 4.3% Clinostomum marginatum metacercariae were lost during 6 months over the winter. Posthodiplostomum minimum centrachi metacercariae lived at least 11 months in fishes kept in aquaria (Hoffman, 1950), and P. cuticola metacercariae had a survival time of at least 18 months and the complete life cycle required two summers in the more northern parts of the U.S.S.R. (Bauer et al., 1969). In Uvulifer arnbloplitis metacercarial cyst degeneration was seen in summer (Krull, 1934a). All the metacercariae that have incidences throughout the year are likely to survive in the fish host for at least 9 months. These include, in this climate zone : Ichthyocotylurus pileatus in Abramis brama (Izyumova, 1958; Lyubarskaya, 1970), in Blicca bjoerkna (Izyumova, 1960), in Gymnocephalus cernua (Izyumova, 1959a), in Lucioperca lucioperca and Pelecus cultratus (Izyumova, 1958), and in Percajuviatilis (Rautskis, 1970a); I. platycephalus in P. fluviatilis (Rautskis, 1970a); I. platycephalus/I. variegata in P. juviatilis (Izyumova. 1958); Crassiphiala bulboglossa in Pimephales promelas promelas (Hoffman, 1956); Diplostomum adamsi in Perca flavescens (Lester, 1977); D. paraspathaceum in Gasterosteus aculeatus and Pungitius pungitius (Banina and Isakov, 1972); D. scudderi in Eucalia inconstans (Hoffman and Hundley, 1957); D. spathaceum in A . brama (Bogdanova, 1958; Izyumova, 1958), in B. bjoerkna (Izyumova, 1960), in Carassius auratus gibelio (Lyubina, 1970), in Esox lucius (Izyumova, 1960), in G. cernua (Izyumova, 1959a), in L . lucioperca and P. cultratus (Izyumova, 1958), in P.flavescens (Tedla and Fernando, 1969), in P. juviatilis (Izyumova, 1958; Rautskis, 1970a); Diplostomum sp. in A . bramae (Lyubarskaya, 1970); Posthodiplostomum cuticola in P.juviatilis (Pearse, 1924); TylodeIphys clavata in C. auratus gibelio (Lyubina, 1970), in Esox lucius (Rautskis, 1970b), in G. cernua (Izyumova, 1959a), in P. juviatilis (Izyumova, 1958; Rautskis, 1970a) and in R. rutilus (Izyumova, 1959a); Paracoenogonimus ovatus in A . brama (Bogdanova. 1958; Lyubarskaya, 1970) and E. lucius (Bogdanova, 1958; Rautskis, 1970b); and Opisthorchis felineus in Tinca tinca (Komarova, M. S., 1957). Low and sporadic incidences of metacercariae are not discussed for this and following climate zones because it was suggested in Section 1V C 1 that the explanations for these are likely to be related to non-seasonal phenomena. Likewise, incomplete data are omitted. However, it is of interest to note that both Markova (1958) at the Oka River and Rautskis (1970b) at Lake Dusia, U.S.S.R. found Diplostomum spathaceum metacercariae in Esox lucius from April to November only. 3. East coast (Climate zone 3 a iii) Very little work has been carried out in this climate zone. Noble (1970) reported a higher incidence of Tetracotyle sp. in August and September, but saw no apparent seasonal trends in the incidence of Diplostomum spathaceum metacercariae in Oneida Lake, New York State, U.S.A. Evans, H. E. and Mackiewicz (1958) examined samples of 35 species of fishes from seven families through 11 November to 14 January 1950, but the 3 month winter

196

JAMES C. CHUBB

sample did not show any pronounced month to month fluctuation in metacercarial cyst counts. 4. Maritie n,est coast (Climate zone 3 b) Studies in this climate zone have been carried out in the British Isles, the more maritime regions of Poland and the western coast areas of Canada and the U.S.A. This zone has mild winters and summers, without extremes of temperature. As will be seen below this allows a long period, something of the order of 7 or 8 months each year, during which cercarial invasion can occur. Wootten (1973a) showed that Salmo gairdneri and S. trutta stocked into Hanningfield Reservoir, Essex, England, in April had no infection of Ichthyocotylurus erraticus in May, but infection commenced in June and continued until early autumn. Water temperature in the reservoir was above 12°C from late May t o November. The complete cycle might be completed in one summer, or as temperatures fell in the autumn, might continue to a second summer. Chappell (1969) attempted to discover the invasion period for Diplostomum gasterostei in Gasterosteus aculeatus by examining the infections in the fishes for large and small metacercariae. It was assumed that small metacercariae would represent recent invasions, but it was not possible to subdivide the larvae into groups. However, Pennycuick (1971b) was able to determine the periods of infection for D. gasterostei in G. aculeatus in England. Light infection occurred October-December 1966, then stopped during January and February 1967. Further light infection recommenced March to achieve a peak in May-June, and then decreased J d y to October. In November and December 1967 light infection continued. Berrie (1960b) noted shedding of cercariae of D. spathaceum from snails in Scotland during August and September, but did not sample in other months. Chappell (1969) was successful in dividing the metacercariae of D. spathaceun? into recent (small) and older infections (large metacercariae). In Yorkshire, England in G. aculeatus small metacercariae were present all year, although there was a marked (50 %) incidence in August, which probably represented the peak time of invasion. Chappell (1969) concluded that either invasion of G. aculeatus occurred all year, or that the growth of recent infections of metacercariae was retarded overwinter. The latter explanation is probable. Sweeting (1974) expanded the study of cercarial-metacercarial intermediate stages of D. spathaceum, and found that their incidence rose from 25% in April/May to 91.5% in August/September in G. aculeatus in the LeedsLiverpool Canal at Kirkstall, England. Wootten (1974) in the stocked S. gairdneri and S. trutta mentioned above, found infection of D. spathaceum t o occur from May to November. A similar situation applied t o Tylodelphys clavata, and Wootten (1974) suggested that cercariae were liberated from the snails from May to November. With Holostephanus luehei in Pungitius pungitius in South Wales, Pike (1965) also found a long period of infection, from May through to November. In Canada, Bender (in Millemann and Knapp, 1970) observed that

H E L M I N T H S IN FR ESH WA TE R FISHES

197

Oncorhynchus kisutch fry had a low incidence of infection by Nanopliyetus salmincola when they emerged from the gravel in March, but all were infected

by April, thereafter intensity reached a peak in early July, then stabilized. t o be followed by another increase in September. Salmo gairdneri fry were already all infected by N. salrnincola when they emerged from the gravel in mid-April. The infections thereafter followed a similar pattern to that described for 0. kisutch. The survival of the metacercariae varied considerably, depending on digenean species. Rhipidocotyle illense metacercariae in the fins of cyprinids at Lake Druino, Poland, died as winter approached, but single individuals in the muscles, connective tissues and gills degenerated less frequently (Kozicka, 1958). The metacercariae of Diplostomum gasterostei in Gasterostem aculeatus and Perca Jluviatilis never showed any evidence of deterioration (Pennycuick, 1971b and Kennedy and Burrough, 1977 respectively). nor did those of D. spathaceum in G. aculeatus (Sweeting, 1974). In both fish species these metacercariae survived for the life of the host. Erasnius (1958) showed that D. spathaceum metacercariae lived at least 14 years. Kennedy and Burrough (1977) considered that the metacercariae of Tylodelphys clavata survived for about I year, and Wootten ( 1 974) found Tylodelphys potlicipina was a parasite of young Perca Jluviatilis and thought that the metacercariae survived for about 2 years. Nanophyetus salmincola metacercariae from Oncorhynchus kisutch were infective to dogs after 12,24 and 334 months, and metacercariae from an individual 0. tshavtytscha were infective after the fish had been at sea for 4 years. Almost all the species of metacercariae occurring in this climate zone have been shown to have an incidence in the fishes throughout the year. Owing to the mild winters the sampling of fishes is easier than in the continental zones, which have very cold winters. Incidence all year has been reported for the following metacercariae : Ichthyocotylurus erraticus in Salmo trutta (Canipbell, 1974; Wootten, 1974), in s. gairdneri (Wootten, 1974); Tetracot.yle sp. in Perca Jluviatilis (Rizvi, 1964); Diplostomurn gasterostei in Gasterosteus aculeatus (Chappell, 1969; Pennycuick, 1971a,b,c), in P e r m fiuriatilis (Kennedy, 1975a; Kennedy and Burrough, 1977); D. phorini in Phosinus phoxinus (Bibby, 1972); D. spathaceum in Abramis brama and Em\- lirciirs (Mishra, 1966), in G. aculeatus (Berrie, 1960b; Chappell, 1969; Sweeting, 1974), in Gymnocephalus c e r m a (Wootten, 1974); in Leuciscus leuciscits (Crowden, 1976); in P. Jluviatilis (Mishra, 1966; Wierzbicki, 1970. 1971 ; Wootten, 1974); in Pungitius pungitius (Wootten, 1974); in Rutilus rutilus (Mishra, 1966; Wootten, 1974); and in S. gairdneri and S. trutta (Wootten, 1974); Posthodiplostomum brevicaudatuni in P. Jluviatilis (Wierzbicki, 1971); Tylodelphys clavata in G. cernua (Wootten, 1974), in P.jluviatilis (Wierzbicki, 1970, 1971; Wootten, 1974; Kennedy and Burrough, 1977), in P. pungitius, R . rutilus, S. gairdneri and S. trutta (Wootten, 1974); T. podicipiiia in G. cernua (Wootten, 1974), in P. Jluviatilis (Wierzbicki, 1970, 1971 ; Wootten, 1974); Holostephanus Iuehei in P. pungitius (Pike, 1965); Prohemistomulum sp. in E. lucius (Mishra, 1966); and Nanophyetus salinincola in Oiicorhynchus kisutch and 0. tshawytscha (Farrell et al., 1964).

I98

JAMES C . C H U B B

5. Semi-desert (Climate zone 3 c> Although the term semi-desert is applied to this zone, it must not be taken t o imply that it is totally arid. The terms prairie or steppe may convey a better impression of the conditions in this zone. The infection of fishes by cercariae of Ichthyocotylurus erraticus was studied by Olson (1970) at Georgetown Lake, near Anaconda, Montana, U.S.A. With stocked Oncorhynchus kisutch, Salmo gairdneri and Thymcrllus arcticus, incidence of I. erraticus metacercariae was high by July, and 100% by September-October. Georgetown Lake was usually ice-covered from midNovember to mid-May, and at least some snails, Valvata lewisi, carried the infection overwinter as some fishes were infected by early July. The surface water temperature was 18-21°C from July to September, and at 21°C the metacercariae were encysted in 2-3 weeks. A similar period of infection also prevailed at North Park, Colorado, U.S.A., where Davies, R. B. et al. (1973) reported that the lake was ice-covered from October/November to about 1st April each year. Gulls, Larus californicus, arrived about this latter time, t o remain until the water was frozen again in the autumn. Fingerling Salmo gairdneri stocked in April were first seen to be infected with Diplostomum spathaceum in mid-July, and by mid-August all were infected. The L. calfornicus had light spring infections of adult D. spathaceum, and heavier occurrences in July t o September. Davies, R. B. et al. (1973) suggested that the adult worms did not overwinter in the gulls. Bauer et al. (1964) noted that the optimum temperature for infection of cercariae of Posthodiplostomum cuticola was 2628°C. Kamenskii (1969, 1971) suggested that in the Volga Delta, U.S.S.R., the main contact between the cercariae and the fishes was during March to August, when the snails Planorbis carinatus and P. planorbis and the young fishes, chiefly Cyprinidae, shared shallow, warm and weedy backwaters. The infections survived overwinter in both the snails and fishes. Vladimirov (1960) found the highest infection of P. planorbis by P. cuticola in the Astrakhan State Reserve, U.S.S.R. from June t o mid-July. It has been noted above that snails infected by Ichthyocotylurus erraticus and Posthodiplostomum cuticola can carry the infection through the winter. Becker (1967) and Becker and Brunson (1966) reported that Salmo gairdneri in Canal Lake, Washington State, U.S.A. that overwintered were severely affected by Diplostomum spathaceum by the following spring. An alternative method of transmission to the fish by means of precocious metacercariae during the winter was proposed and shown t o occur experimentally. Many of the metacercariae studied in climate zone 3 c have been shown t o occur in the fish hosts during all the year, for example: Bucephalus polymorphus in Abramis brama and Cyprinus carpio (Dubinina, 1949); B. sp. in Vimba vimba vimba natio carinata (Komarova, T. I., 1964); ZchthyocotyIurus pileatus in Blicca bjoerkna (Komarova, T. I., 1964) and Lucioperca lucioperca (Dubinina, 1949); Diplostomum spathaceum in A. brama (Dubinina, 1949), in B. bjoerkna (Komarova, T. I., 1964), in C . carpio (Dubinina, 1949), in Rutilus rutilus (Kashkovski, 1967) and R. rutilus heckeli (Komarova, T. I., 1964); Posthodiplostomum cuticola in A. brama (Dubinina, 1949), in B.

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bjoerkna (Komarova, T. I., 1964) and C. carpio (Dubinina, 1949); Tylodelphys clavata in A. brama, B. bjoerkna, Esox lucius, and R. rutilus heckeli (Komarova, T. I., 1964) and R. rutilus (Kashkovski, 1967); Paracoenogonimus ovatus in A. brama and C. carpio (Dubinina, 1949) and E. lucius (Komarova, T. I., 1964); Pseudoamphistomum truncatum in B. bjoerkna (Komarova, T. I., 1964); Apophallus muehlingi in B. bjoerkna (Komarova, T. I., 1964); and Metagonimus yokogawai in A. brama, B. bjoerkna, L. luciopercae and R. rutilus heckeli (Komarova, T. I., 1964). 6. Desert (Climate zone 3 d) The investigation of the biology of Clinostomum complanatum in Perca schrenki in the Balkhash-Alakol’ Basin, U.S.S.R. by Galieva (1971) is within this climate zone. The percentage incidence varied from 6-1 to 92.8 according to habitat, but investigations were made from May to September only. 7. Sub-polar (Climate zone 3 e) This zone is characterized in particular by its long winters and short summers. The highest intensity of infection of Rutilus rutilus by Diplostomum sp. metacercariae was seen in the Kuito Lakes in Karelia, U.S.S.R., during the end of the summer, at the time of maximum cercarial activity (Rumyantsev, 1975). According to Gvozdev (1972), who worked in the same locality, there were two peaks of infection of the molluscs Lymnaea peregra and Gyraulus acronicus by trematode larvae. The first peak, in mid-August, was caused by mature cercariae that developed in molluscs infected in the preceding year. The second peak, at the end of September, represented the infection of the mollusc juveniles. Titova (1957), at Lake Ubinsk, Siberia, U.S.S.R., also found highest incidences of Bucephalus polymorphus and Diplostomum spathaceum in the autumn, but the differences between autumn and the other seasons were slight. Malakhova (1961) studied the occurrence of a number of species of metacercariae in the fishes of Lake Konche, Karelia. The incidences were more or less uniform throughout the year in the following species: fchthyocotylurus platycephalus in Perca fluviatilis; Diplostomum spathaceum in Esox lucius, Lota Iota, P. fluviatilis and Rutilus rutilus; Posthodiplostomum brevicaudatum in P. fluviatilis; and Tylodelphys clavata in E. lucius, L. Iota, P. fluviatilis and R. rutilus. D.

POLAR (CLIMATE ZONES

4a

AND

4 b)

N o seasonal studies of metacercariae from the polar climate zones are known to the author. Fishes occur in freshwater at least during the summer in parts of Greenland (climate zone 4 a) but it is not known whether they are infected by freshwater parasites.

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JAMES C . C H U B B

E.

MOUNTAIN (CLIMATE ZONE

5)

Lake Sevan, Armenia, U.S.S.R., 1914 m above sea level, may be considered to be a mountain lake. Between 1834 and 1954 the lake froze on ten occasions. The surface water temperature falls t o 1.6"C in winter and rises t o 17.7"C in summer. At depths below 49 m the temperature remains at 3.8"C all year. Vartanyan and Mkrtchyan (1972) studied Ichthyocotylurus erraticus, Diplostonium spathaceum and Tylodelphys clavata in Coregonus lavaretus ludoga and C. lavaretus maraenoides. I. erraticus and D. spathaceum had a 100% incidence all year, with a peak intensity for I . erraticus in OctoberNovember. The intensity of infection by D. spathaceum was more or less uniform through the year, although slightly higher in December-January. Tylodelpliys clavata was present all year, but the incidence was 20 % in May, fell to 13.6 % in June-July, to rise to 26.6 % in October-November and fall t o a minimum of 6.6 % in December-January. Palmieri et a/. (1977) noted for Diplostomum spathaceum in Utah, U.S.A. that the low rate of infection in high alpine lakes was probably due t o a lack of prevalence of the gull hosts combined with the low water temperatures (below 4.4"C) which would make completion of the life cycle difficult. F.

SPECIES STUDIED IN MORE THAN ONE CLIMATE ZONE

Table 2 gives a list of species that have been studied in more than one climate zone. As far as analysis of the data allows, it is clear that the majority of these species have similar patterns of occurrence in all climate zones. The metacercariae were present in the fish hosts throughout the year, regardless of the climatic conditions. However, in the climate zones with longer periods of warm temperatures, invasion of the fishes by cercariae may occur for a longer season. Precise comparative data for each species are not available, indeed the information is fragmentary (see Section V C). None the less, as increasing water temperature is known to stimulate the hatching of the eggs, the development of the larval stages in the molluscs, the release of the cercariae and the speed of development of the metacercariae in the fish hosts it is probable that the warmer climate zones will facilitate a more rapid completion of the life cycle. As an instance of this, Bauer et a/. (1969) noted that the life cycle of Posthodiplostomum cuticola could be completed in one summer in the southern regions of the U.S.S.R. but required two summers further north. Such a situation is likely to apply t o many of the other species of trematodes with metacercariae in freshwater fishes. Overwintering of the trematode larvae in the snail hosts appears to be unrelated to climate zone, but to be a function of the biology of the particular species of parasite and mollusc. Thus Gvozdev (1971, 1972) found that Gyraulus acronicus and Lymnaea peregra carried the trematode infections through the winter in Northern Karelia, U.S.S.R. (climate zone 3 e), whereas Hugghins (1954b) found that Gyraulus hirsutus was infected by Hystero-

TABLE 2 Species of rnetacercariae studied ( S )for seasonal occussence in more than one climate zone

The species are in alphabetical order Climate zone

2 Metacercariae species Apophallus muehlingi Bucephalus polymorphus Clinostomum complanatum Clinostomum marginatum Diplostomurn spathaceuni Hysteromorpha triloba Ichthyocotylurus erraticus Ichthyocotylurus pileatus Ichthyocotylurus platycephalrrsl Ichthyocotylurus variegata Metagonimus yokogawai Opisthorchis felineus Paracoenogonimus ovatus Posthodiplostomum brevicaudatuni Posthodiplostomum cuticola Posthodiplostomum mininirrni Rhipidocotyle illense Tylodelphys clavata Uvulifer ambloplitis

a

b

S

ai

S S S S S S S

S

S

-~--__

3

S S

S S S S S S

aii

aiii

b

S S

S

S S S S S S S S S S S S S

C

S

S S

S S S

S S S S

S S S S S

d

S

~-

5

e

S S S S

S S

S

S

S

202

JAMES C . C H U B B

morpha triloba only during the warm summer months in Illinois, U.S.A. (climate zone 3 a i). It is probable that in the colder climate zones it is more important that the molluscs are able to maintain the trematode infections over the winter as the shorter summer period of optimum temperatures may not permit complete development of the larvae during their first summer. A further factor related to climate zone is the duration of occurrence of the definitive hosts of the metacercariae. In a number of instances conditions are such that the definitive hosts leave the habitat for the cold winter months. Three examples are quoted : Larus califurnicus, one of the definitive hosts for Diplostomum spathaceum at North Park, Colorado, U.S.A. (climate zone 3 c), which arrived at about 1st April each year, to remain until the lakes were completely frozen in October or November (Davies, R. B. et al., 1973); Lams canus, also a definitive host for D. spathaceum, at Agdenes, Trondheimsfjord, Norway (climate zone 3 b), which arrived April and left from August to October (Bakke, 1972a); and Phalacrocorax auritus auritus, a definitive host for Hysteromorpha triloba at Spring Lake, Illinois, U.S.A. (climate zone 3 a i), which arrived at the lake in late March to early April to remain until the lake froze, usually late November (Hugghins, 1956). As a contrast, Larus species and Phalacrocorax carbo are present all year at Llyn Tegid, Wales (climate zone 3 b), where during all normal winters ice cover is absent. As the periods of absence of the potential definitive hosts coincide with the times when low temperatures prevent significant development of the trematodes in the waters of the habitats, they are unlikely to affect the occurrence of the metacercariae in the fishes. Marked effects on the presence of the metacercariae in the fishes do occur, however, when there is a change of status of the definitive hosts [see Section V H, Hysteromorpha triloba (Hugghins, 1957) and Tylodelphys clavata (Kennedy and Burrough, 1977)l. V. GENERAL CONCLUSIONS, METACERCARIAE A.

INCIDENCE AND INTENSITY OF OCCURRENCE

The data for incidence and intensity for each species are given in Section

111. For an understanding of these data it is important to appreciate their

limitations. In at least 37 of the 48 or so species reviewed the metacercariae were found in the fishes during all seasons of the year. This suggests, especially when related to other data pertinent to longevity (see Section V F), that metacercariae of these species normally survive in the body of the fishes for at least 12 months, frequently for longer and sometimes even for the remainder of the life of the fish. This means that most fishes greater than 1 year of age are likely to have been exposed to infection by cercariae during more than one season of invasion (see Section V C ) . Thus the metacercariae present may be of several different ages. Unfortunately, it is rarely possible to separate the metacercariae of different year classes by morphological or other characteristics (see Section V E).

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203

In virtually all the investigations quoted in Section I11 the authors have not attempted to correlate seasonal data with age of fishes, However, there are numerous papers where length or age of fishes were related to incidence and intensity of infection by metacercariae, but as these papers have no direct seasonal component they are not reviewed here. It is important to note the relationships between the potential for successive seasonal invasions by cercariae, the longevity of the metacercariae and the age of the fishes. Fig. 2 attempts to show these relationships for a year class of fishes hatched in 1977 and exposed to cercarial infection for three summers, 1977 to 1979. It is assumed for the purpose of the example that the metacercariae have a longevity of about 18 months. It is evident that some of the young fishes acquire metacercariae (M) during their first summer. The seasonal rate of acquisition of these metacercariae can be studied without complication. However, in the

.,

FIG.2. The relationships between successive seasonal invasions of fishes by cercariae, the longevity of the metacercariae and the age of the fishes. See text p. 203 for full explanation. 1978 0 , 1979A. Year classes of Year of origin of cercariae and metacercariae: 1977 fishes shown by dates within fishes. Maximum metacercarial longevity assumed to be about 18 months.

summer of 1978 the 1977 year class of fishes are exposed to a second potential invasion by cercariae (a),provided that they do not migrate away from the range of occurrence of the cercariae. At the end of the second season of invasion, autumn 1978, the 1977 year class of fishes will be infected by 1977 metacercariae (W) which are still living and by 1978 ( 0 )metacercariae. The two year classes of metacercariae are indistinguishable, so that the seasonal

204

JAMES C. CHUBB

rate of acquisition of metacercariae by the 1977 yea1 class of fishes cannot be seen directly because of the presence of the 1977 year class of metacercariae. In the summer of 1979, the 1977 year class of fishes are exposed to a third potential invasion by cercariae (A). At the end of the third season of invasion, autumn 1979, the 1977 year class of fishes will be infected by the 1978 ( 0 ) metacercariae and the 1979 metacercariae (A).In this example the 1977 metacercariae (m), owing to their assumed longevity of about 18 months, will now have disappeared. However, even in the third year of life ( 2 + ) of the fishes the acquisition of 1979 cercariae by the 1977 year class of fishes cannot be seen directly because of the presence of metacercariae from 1978. If the metacercariae live for more than the 18 months quoted for the purpose of this example, as many do, then at any one time in an individual fish nietacercariae of up to perhaps 5 years of age may be present, acquired over four or five seasons of invasion. It follows from the above example that the actual processs of seasonal acquisition of metacercariae can only by studied directly in fishes in the following circumstances: during their first year of life, after a mortality eliminates a year class, if a perturbation changes the status of the parasite in the environment, or if fishes are stocked. If older fishes are to be studied for acquisition of new infections of metacercariae on a seasonal basis, it is necessary to sample and study the history of a particular year class over and during several years. The data of each previous year augments the current season’s study. As far as the author is aware, such a field study has not been attempted. It is important to note that for the study of the acquisition and accumulation of long-lived somatic parasites such as metacercariae, host age is the relevant parameter, not host length. Length groups, especially of older fishes, will contain individuals of several ages (year classes) which will confuse an understanding of the data. I n any event, to compare data from several habitats, age is a constant, whereas length will vary according to growth rates which can change dramatically from one habitat to another. The study of Titova (1957) on Abvamis brama in Lake Ubinsk, Siberia, U.S.S.R. was nearer the ideal given above than most: 227 A . brania were dissected, at three seasons, summer, autumn and winter, and the data examined in relation to nine age groups. However, once the 227 fish were divided between the seasons and age groups, the problem of inadequate numbers of fishes in each subdivision appeared. Thus Titova (1957) was able to conclude that Diplostomum spathaceum infection reached its maximum in the autumn until the fish were 5 years old, thereafter the incidence decreased considerably. The incidence of both D. spatliaceurn and Tylodelpliys clavata increased from summer to autumn. The studies of the infection of fishes in their first year of life, after mortalities of fishes, perturbations in the environment or the stocking of fishes are reserved for discussion in Sections V C and C. As most authors have not provided age data for the fish samples studied the seasonal changes of the metacercariae as expressed by incidence and intensity refer to unrecognizable sections of the fish populations. As incidence

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

205

and intensity details for each species of metacercariae have been given in Section I l l , they are not discussed further here. Tt was noted earlier in this section that many authors, not reviewed here, had studied age of fishes in relation to incidence and intensity of occurrence of metacercariae. One example is quoted to show the general pattern. Maksimova ( 1958) observed the occurrence of Tylodelphys clavata in Perca,puviatilis of Lake Sunukul', U.S.S.R. The percentage incidence increased from 27.5 % in O+ fishes to 91.8% in 3 + fishes and remained about 100% in P..puviatilis 4 + to l o + . Intensity of infection, maximum and average, increased from O + through to 7 + (maximum) and 8 + (average) to remain more or less level thereafter to 10f fishes. B.

PRINCIPAL A N D AUXILIARY HOSTS

It is useful to recall at this stage in the discussion the phenomenon of principal and auxiliary hosts (Dogiel, 1964). Many trematode metacercariae have a relatively wide specificity, but none the less the phenomenon applies. Shigin (1964) showed that the life span of Diplostomum spathaceum metacercariae in its principal host was about 4 years, but was much shorter in other species of fishes depending on the degree of adaptation of this parasite to the particular host species. More recently, Sweeting (1974), who also investigated D. spathaceum, has shown the same phenomenon in the British Isles. In general Cyprinidae were more susceptible than Percajuviatilis both naturally and experimentally. The fact that at 12°C development of metacercariae was completed in 28 days in Phoxitius phoxinus and Gobio gobio. and in 35-40 days in Rutilus rutilus, but required 120 days in Percajuviatilis, clearly demonstrates one difference between principal and auxiliary hosts. I n many examples quoted in Section 111 the data refer to principal hosts, as frequently these are the species with high incidences and intensities of infection. However, where sporadic infections are reported either the fishes may be auxiliary host species, or the parasite species may be of limited occurrence owing to some other aspect of its biology. C.

INVASION OF FISHES BY CERCARIAE

Erasmus (1972) presented a recent account of the ecology of the life cycles of trematodes. In general there is a seasonal variation in the level of infection of freshwater, marine and terrestrial molluscs by cercarial stages. These seasonal variations were found in tropical zones (Ogambo-Ongoma, 1971 : Onabamiro, 1972; Mathavan, 1973; George and Nair, 1974; Mohandas, 1974), in sub-tropical zones (Chatterji, 1933; Singh, 1959; Mukherjee, 1966) and in mid-latitude zones (Cort, 1922; Rees, 1932; Wesenberg-Lund, 1934: Ginetsinskaya, 1959; Kupriyanova-Shakhmatova, 1961 ; Zdarska, 1964: Kendall, 1965; Pike, 1965, 1968; Probert, 1966; Aristanov, 1970; Katkov, 1971 ; Erlandson, 1972; Gvozdev, 1972; Natsvlishvili, 1973; Dremkova and Adel'shin, 1974). In the tropical zones the temperatures varied only slightly during the year and had no observable effect on snail population density (Onabamiro, 1972).

206

JAMES C. CHUBB

The relevant factors were the occurrence of seasons of high rainfall (Onabamiro, 1972; Mathavan, 1973; Mohandas, 1974) or of low rainfall (Ogambo-Ongoma, 1971 ; Onabamiro, 1972; Mohandas, 1974) dependent on the species of snail. Other factors, for example low estuarine water salinity, were also important (George and Nair, 1974). In sub-tropical zones factors other than temperature also applied, for instance the life span of the snails and the migratory habits of the definitive hosts (Singh, 1959) although the wetter and cooler conditions of the sub-tropical winter season sometimes favoured an increase in incidence of infection by cercarial stages (Mukherjee, 1966). In mid-latitude zones temperature is an important factor in determining incidence of cercariae and cercarial liberation. Kendall (1965) stated that the effect of temperature on the development of trematodes within their molluscan hosts had been studied quite extensively and that there was a fairly direct relationship between the rate of development of the parasites and the environmental temperature. However, other parameters are also involved, including the pattern of life cycle of the mollusc host (Sewell, 1922; Rees, 1932; Dubois, 1929; Pike, 1965, 1968; Probert, 1966), and the level of incidence of the trematode in its definitive host (Dubois, 1929; Pike, 1965, 1968; Probert, 1966), as well as other environmental factors. The most common times for peaks of high incidence of cercarial stages are late spring and late summer (see for example, Probert, 1966; Pike, 1968; Gvozdev, 1972; Natsvlishvili, 1973), although summer peaks (June, July, or July/ August) (Kupriyanova-Shakhmatova, 1961) or autumn peaks (Dremkova and Adel’shin, 1974; Ginetsinskaya, 1959) are also reported. It is clear that the timing of these peaks is determined by a combination of factors, especially host species and climate zones. Rees (1932), in South Wales (climate zone 3 b) found peaks for Lymnaeapalustris and L. peregra in May and September, but in June and October for Lymnaea tvuncatula. By comparison, in Karelia, U.S.S.R. (climate zone 3 e), Gvozdev (1972) found peaks of infection in Gyraulus acronicus and Lymnaea peregra in August and at the end of September. The long cold winters of Karelia delayed the occurrence of the first peak of incidence of infection until August. In some species of trematodes mature infections of cercariae were found in all seasons (McCoy, 1928b). However, in mid-latitude conditions the lowest incidences in molluscs were found during the winter months. The largest proportion of winter infections were composed of immature sporocysts and rediae, the development of which had been arrested by the low temperatures, and few or no mature cercariae were found (Probert, 1966). The seasons of invasion of fishes by the species reviewed here have been studied in a relatively small number of species, and most of these in midlatitude climate zones. Baturo (1977) found sporocysts and cercariae of Bucephalus polymorphus and Rhipidocotyle illense from April to October and May to October respectively. Peak emergences of cercariae were June to September ( B .polymorphus) and July/August ( R . illense). Johnston, T. H. and Angel (1941) found cercariae of Diplostomum murrayense from October to April (their summer, in the southern hemisphere). Bauer et a/. (1964) observed D . spathaceum in

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molluscs all year. The cercariae emerged above 1O"C, invaded fishes from 13-16"C, but more easily above 18°C (Bauer, 1959a). Berrie (1960b) noted cercariae of D. spathaceum in August and September, and found that they were not released during the cold months. Mindel (1963) showed that snails kept a t 18°C in the laboratory over the winter continued to shed cercariae of D. spathaceum and that they were infective to Cyprinus carpio. Hugghins (1954b, 1957) only saw snails infected by Hysteromorpha triloba during the warm summer months. Cercariae of Posthodiplostomum cuticola had a maximal incidence in snails in June to mid-July (Vladimirov, 1960). The minimum temperature for development was 10°C, optimum 24°C (Bauer, 1968; Bauer et a/., 1964, 1969). A mass release of cercariae occurred at 28°C. Kamenskii (1969) suggested that the main contact between P. cuticola cercariae and the cyprinid hosts was during March to August in the Volga Delta. The cercariae of Posthodiplostomum minimum did not emerge at 15"C, but were infective from 18-27°C (Hoffman, 1958). The season of invasion has also been determined by the observation of recently established metacercariae in fry, young and stocked fishes exposed to infection for the first time. MolnLr (1966) did not find Apophallus muehlingi nietacercariae in fry of Lucioperca lucioperca from May to July, but by 9th August 28.5 % were infected. Metacercariae were found in young L. lucioperca (64-190 mm long) on 1st July (14.3 % incidence). Bauer et al. (1964) reported mortality of juvenile fishes caused by cercariae of Diplostomum spathaceum from early summer, up to 100% by the end of June. Salmo salar fry were infected by D. spathaceum from early July onwards (Bauer, 1957a). Davies, R. B. et al. (1973) observed that Salmo gairdneri fingerlings stocked in April were infected by D. spathaceum by midJuly, and the incidence had reached 100 % by mid-August. Two-year-old Salmo gairdneri stocked into Hanningfield Reservoir in the spring had a 10.4 % incidence of D. spathaceum by May which reached 36.4% by November. From April to November the water temperature was above 10°C (Wootten, 1974). The same S. gairdneri were also invaded by Ichthyocotylurus erraticus (also in some stocked Salmo trutta) and Tylodelphys clavata. I. erraticus metacercariae were first found in June, which suggested that invasion commenced in late May or early June, and the incidence increased throughout the summer and early autumn (Wootten, 1973a). The incidence of T. clavata was 16.7% in May and had increased to 100% by September 1968 (Wootten, 1974). The release of the cercariae of these three trematodes may have occurred throughout the period May to November. Olson (1970) also observed invasion of stocked salmonids by I. erraticus. I n July the incidences were: S . gairdneri 69.2%, Thymallus arcticus 83.3 %, Oncorhynchus kisutch 50 %; by SeptemberOctober there was a 100 % incidence in the three species of fishes. The surface water temperatures, July to September, were 18-21°C. Kasesalu (1974) followed the invasion of Cyprinus carpio in fish farm ponds by Diplostomum sp. Incidence in the rearing pond (June to October) climbed from 0 % in June/July to about 45 % by October. Meyer (1958) was able to follow the invasion of Pimephales promelas by a Diplostomulum type larva in a circumstance where mortality caused by the

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larvae appeared t o have eliminated most of the infected fishes from the preceding year. At the start of the summer (early July) the incidence was below 15%, however, it rose rapidly until in late-August it had reached 90%. Holostephanus luehi was studied by Pike (1965) in Pungitius pungitius. The incidence rose from 0 % in June to 90% by October. During this time the average length of the fishes examined increased steadily, although from October to January more small P. pungitius appeared, possibly from a summer spawning. Bender (quoted from Millemann and Knapp, 1970) found that all Salmo gairdneri fry emerging from the spawning gravel in mid-April in Oregon coastal streams were already infected by Nanophyetus salmincola. Few Oncorhynchus kisutch fry that emerged from the gravel in March were infected, but by mid-April all these were also invaded. The intensity of infection increased rapidly from mid-April to early July, then remained stable until early September when another increase occurred. Pennycuick (197 1b) utilized the relationships between seasonal incidence, intensity and variance to deduce the season of invasion of Gasterosteus aculeatus by Diplostomurn gasterostei. There was evidence of a light invasion by cercariae in March, but in May and June there were indications of many fishes acquiring new infections from cercariae that were widely distributed. During July to October invasion continued with a few fishes acquiring large numbers of D. gasterostei, showing that the distribution of cercariae was patchier. A light invasion continued to December, but ceased between January and March. Kennedy (1975a) and Kennedy and Burrough (1977) suggested that an increase in incidence of D. gasterostei and Tylodelphys clavata in PercaJluviatilis in the spring and at the end of the summer demonstrated periods of invasion by cercariae. Chappell (1969) attempted to relate the occurrence of small (less than 0.2 mm) metacercariae of Diplostomum spathaceum with periods of invasion of Gasterosteus aculeatus. Small metacercariae were present in all samples, but predominated in August (50%). Their presence all the year indicated either that infection could occur throughout, or that some larvae had a retarded rate of overwinter growth. A further study of D. spathaceum metacercarial intermediates in G. aculeatus was made by Sweeting (1974) (see Fig. 1). I n this instance the invasion by cercariae occurred in June/July and August/September. The incidence of the cercarial/metacercarial intermediates rose from 25% in April/May to 91.5% in August/September and the intensity from 4-6 in April/May to over 20 in August/September. Sweeting (1974) concluded that the transformation to metacercariae might not be completed before winter, and for these individuals ability to infect the definitive host was postponed until the next year. In the conditions of Karelia, Rumyantsev (1975) observed that the maximum invasion of Rutilus rutilus by Diplostomum sp. was at the end of the summer. This corresponded t o the peak of mullusc infection observed in the same area by Gvozdev (1971, 1972). The observations summarized above indicate that cercariae are released only at times of the year when temperatures exceed a minimum applicable

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to each species of trematode. In temperate climates this minimum will be exceeded from spring through t o autumn. However, Becker (1967) and Becker and Brunson (1966) observed that the invasion of Salmo gairdneri by Diplostomurn spathaceurn continued over the winter in Canal Lake, Washington State, U.S.A. An alternative method of transmission by means of precocious metacercariae frcm the mollusc hosts was shown to occur during the winter. The fishes ingested the diplostomulae from the snails, and an experiment during the winter demonstrated that only 4 % of the larvae reached the site in the lens. D.

FORMATION OF METACERCARIAE

After cercariae have penetrated the fishes they migrate through the tissues to the preferred sites (see e.g. Erasmus, 1959 for Diplostomurn spathaceum). At these sites within the tissues a period of development occurs to form the infective metacercariae. The length of time of the transformation from cercariae to metacercariae is determined by the host species and temperature. A recent and comprehensive account of the transformation of the cercariae of Diplostomum spathaceum t o metacercariae has been provided by Sweeting (1974). The variation of time of development according to host species has already been noted in Section V B and is not repeated here. Sweeting (1974) utilized Xenopus laevis as an experimental host and studied the time of development required. At 5" and 9°C the experiments were terminated after 102 and 86 days respectively and no development of cercariae had occurred. At 12°C the transformation was completed in 65 days, and as experimental temperatures were increased the time required for development declined, until at 29°C fully developed metacercaria were obtained in 12 days. Development times have been determined for other species of metacercariae. Apatemon gracilis took 28 days at 15"C, but the development of the metacercariae was not synchronous (Blair, 1976). At summer temperatures Bucephalus polymorphus metacercariae were fully developed I 5 days post-entry (Baturo, 1977). Bauer (1957a, 1959a), Erasmus (1958), Mindel (1963) and others have quoted various development times for Diplostomum spathaceurn according to host species and temperature. At summer temperatures Hugghins ( 1 954b) found that Hysteromorpha triloba metacercariae were fully formed in about 84 days. lchthyocotylurus erraticus nietacercariae were encysted in 14-21 days at 21°C in Salmo gairdneri (Olson, 1970). Posthodiplostornum brevicaudatum needed 49-56 days at summer temperatures (WiSniewski, 1958a) to complete development. More complete data are available for Posthodiplostornum cuticola: below 10-12°C no development occurred, at 16°C transformation was completed in about 84 days and at 24°C in about 30 days (Vladimirov, 1960; Bauer et a/., 1964). Donges (1964) found completed development of P. cuticola in 35 days at 22°C. Similar data were provided by Hoffman and Putz (1965) for Uvulifer ambloplitis: at 12-13°C slight development occurred, and completed transformation occurred in 92 days at 13"C, 43+ days at 20°C and 22 days at 24°C.

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If transformation of the cercaria to metacercaria was delayed by the onset of winter, it could be completed at the return of higher temperatures the following spring (Bauer, 1959a). Cercarial/metacercarial intermediates were found by Chappell (1969) and Sweeting (1974) during all times of the year (see Section V C for details). E.

MORPHOLOGICAL DIFFERENCES

Some authors have reported different morphological forms of metacercarial cysts. Lester (1974) noted three types for Apatemon gracilis in Gasterosteus aculeatus but these were found at all times of the year and possibly have no seasonal significance. Spall and Summerfelt (1969) observed that the cysts of Posthodiplostomum minimum in Pomoxis annularis were smaller, more opaque and the larvae less active during the winter. From late spring both degenerate and fresh cysts were seen in the livers, indicating a recurring seasonal invasion. F.

LONGEVITY

It was suggested in Section V A that in at least 37 of the species reviewed the metacercariae probably survived in the fish host for at least 12 months. Actual observations on longevity of the metacercariae tend to confirm this view. The effect of principal and auxiliary hosts on metacercarial longevity has been noted in Section V B, with principal hosts probably providing maximum survival times. Longevity has been seen to be as little as 5 months in Bucephalus polymorphus and Rhipidocotyle illense (Baturo, 1977). However, a longer survival time for R . illense may be achieved in some organs. Kozicka (1958) saw that fewer and fewer metacercariae from the fins were living as winter approached, although single metacercariae in the muscles, connective tissues or gills degenerated less often. Survival of metacercariae overwinter, from one season of invasion to the next, has been demonstrated for the following species: Clinostornum marginatum (Fischthal, 1949); Diplostomum spathaceum (Bauer, 1957a,b) ; Hysteromorpha triloba (Hugghins, 195417); Neascus sp. (Fischthal, 1949); and Posthodiplostomum cuticola (Bauer et al., 1969; Kamenskii, 1971). Infectivity of the overwintered metacercariae to the definitive host was experimentally tested by Hugghins (1954b). Longer survival times reported were: Crassiphiala bulboglossa, 37 months (Hoffman, 1956); Diplostomum scudderi, 12 months (Hoffman and Hundley, 1957); D. spathaceum, at least 18 months (Erasmus, 1958) and 33 years (Shigin, 1964); Nanophyetus salmincola, 334 months and 48 months (Farrell et al., 1964); Posthodiplostornum brevicaudatum, 61 months (Donges, 1963); P. cuticola, 41 months (Donges, 1964); P. minimum, a t least 11 months (Hoffman, 1950) or 16 months (Yamaguti, 1975); Tylodelphys podicipina, 24 months (Wootten, 1974); and Uvulijer ambloplitis, 54 months (Hoffman and Putz, 1965).

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Some authors thought that the metacercariae could survive for the remainder of the life of the fish host: Diplostomum adamsi in Percaflavescens (Lester, 1977); D. gasterostei in Gasterosteus aculeatus (Pennycuick, 1971b); and D. spathaceum in G. aculeatus (Sweeting, 1974). In fish species with short life spans, e.g. G. aculeatus, which lives for 3 t o 4 years, the normal duration of life of the fish is similar to the known life span of D. spathaceum metacercariae. Probably the longer lived the fish species, the less likely it is that metacercariae will survive for the life of the oldest host individuals. Degeneration and death of metacercariae have been reported for Bucephalus polymorphus (Baturo, 1977), Diplostomum spathaceum (Bauer et a/., 1964; Shigin, 1964) ; Posthodiplostomum minimum (Spall and Summerfelt, 1969); Rhipidocotyle illense (Baturo, 1977; Kozicka, 1958); and Uvulifer ambloplitis (Krull, 1934a). The establishment of a n equilibrium between the numbers of successful invasive cercariae and the numbers of degenerating metacercariae was indicated by the stability found in the average intensity of infection of Pomosis annularis by Posthodiplostomum minimum through the autumn and winter (Spall and Summerfelt, 1969). In the relationship between all the metacercariae and their fish hosts it is obvious that there will be a relationship between invasion by cercariae, presence of infective metacercariae and the death of metacercariae. An account of this relationship has been given in Section V A and it is also of significance to the general hypothesis for the seasonal occurrence of metacercariae in freshwater fishes (Section V J). Johnston, T. H. and Angel (1941) reported finding the diplostomulae of Diplostomum murrayense in the eyes of fishes from November to May (Australian summer) but not in June, August or October. The reasons for the absence of metacercariae from the fishes in the latter months needs investigation. G.

DISAPPEARANCE OF HEAVILY INFECTED FISHES

A number of authors have speculated that fishes heavily infected by metacercariae were selectively removed from the host populations by predation or death influenced by the presence of the metacercariae (see e.g., Diplostomum gasterostei in Perca Juviatilis (Kennedy, 1975a), D. paraspathaceum in Pungitius pungitius (Banina and Isakov, 1972), D. spathaceum in Leuciscus leuciscus (Crowden, 1976) and Posthodiplostomum minimum in Pomoxis annularis (Spall and Summerfelt, 1969, 1970). The postulated deaths occurred in summer ( P . minimum) or winter ( D . gasterostei, D. paraspathaceum and D. spathaceum). Pennycuick (1 97 1a,b) examined 89 dead Gasterosteus aculeatus infected by D. gasterostei collected October 1966-April I967 and September 1967-March 1968. The mean intensity of infection was 9.05, slightly less than for living fish at the same time (9.35). However, Pennycuick (1971a) did find five dead G. aculeatus each with over 100 D. gasterostei and concluded that there was some evidence t o suggest that D. gasterostei caused death of the fish when present in very large numbers. Horoszewicz (1972) included Diplostomulum and Tylodelphys metacercariae amongst the “illness

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factors” that affected the ability of Abramis brama to withstand increased temperature in artificially heated lakes in Poland. The helininths were thought to contribute directly or indirectly to more rapid fatigue of infected fishes, to accelerating their metabolism and reducing their resistance to high temperatures. A comparable helminth stress might also occur at low temperatures. H.

SPORADIC POPULATION CHANGES

There are few long-term population studies of metacercariae in freshwater fishes. Campbell (1974) observed the occurrence of Ichthyocotylurus erraticus in Salmo trutta from Loch Leven, Scotland during the period April 1967 to March 1972. From 1967 to 1970 the pattern of incidence was 50-60% during the summer months, and 90-100 % during the winter. However, from late 1970 to March 1972 this pattern was replaced by widely differing incidences (from 30 to 90 %) occurring irregularly over the whole year. Changes of status of a host species may occur in a habitat and thereby change the status of a population of metacercariae. Kennedy and Burrough (1977) studied the seasonal occurrence of Tylodelphys clavata in Perca jluviatilis at Slapton Ley, Devon, England at a time when this species of trematode appeared in the habitat. For at least 12 years before their study the definitive host Podiceps cristatus had not been present at the lake. A reverse situation was seen by Hugghins (1957) for metacercariae of Hysteromorpha triloba at Oakwood Lakes, South Dakota, U.S.A. In this instance the definitive hosts Phalacrocorax auritus abandoned the nesting site in 1955 and left the habitat. With the disappearance of the birds the infections in the snail host Gyraulus hirsutus had virtually disappeared by the end of the same summer (September). Goryachev (1958) observed the effects of the level of flooding of the Rivers lrtysh and Om, U.S.S.R., on the occurrence of metacercariae of Opisthorchis ,felineus in cyprinids. The level of flooding in each year either promoted or prevented the parasite eggs getting into the bottomland water reservoirs, and thereby increased or decreased the levels of infection of the snails and the cyprinids with larvae of 0. felineus, and subsequently, the infection of the mammalian definitive hosts. I.

SEASONAL STUDIES IN WORLD CLIMATE ZONES

Section IV attempted an assessment of seasonal studies of metacercariae of freshwater fishes in relation to the world climate zones. As can be seen from Table I , no seasonal studies have been carried out in the tropical zones of the world. Investigations are therefore urgently needed, and are likely to have significance to our understanding of the occurrence of metacercariae in both subtropical and mid-latitude zones. Something of the order of 12 species have been investigated in the subtropics and 40 species in midlatitude climates. Nonetheless, more data are needed, especially if the field data are carefully related to concurrent laboratory experimentation.

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J.

213

AN HYPOTHESIS FOR SEASONAL OCCURRENCE

Tn Section V A, the progress of infection of a year class of fishes by metacercariae has been outlined. The periods of invasion of fishes by cercariae of some species were given in Section V C and the times required for the formation of the metacercariae were discussed in Section V D. The longevity of the metacercariae was indicated in Section V F. It is possible therefore to understand the general patterns of invasion, development to infectivity and length of life of metacercariae in fishes. The single most significant seasonal factor in mid-latitude climates appears to be temperature. Although determined for only a few species, there is a minimum temperature below which development of larvae in the snail host will not occur, cercariae will not be released or invade the fish host, and at which the formation of metacercariae within the fishes will cease. Clearly, temperature is not the only factor to produce seasonal patterns of occurrence, but in mid-latitude climate zones it will determine the overall period of the year when these processes indicated above can occur. Within this period of the year other factors may come into play and determine additional changes in the occurrence of the metacercariae. Fig. 3 attempts to show the season of invasion for a species that requires a minimum temperature of 10°C for development. The example is related to the northern hemisphere, and Fig. 3 shows that development could occur all year from the equator to a point at about 38" latitude. From this latitude north to about 70" latitude a season of invasion occurs, which becomes progressively shorter in northern latitudes. Eventually, in the far north the species would not occur as at no time of the year would temperatures be high enough for development. The broad pattern indicated above must be related to local climate, altitude of the habitat and detailed biology of host species involved in the life cycle, as well as the precise requirements for the species of metacercariae. Nevertheless, the generalization remains valid, that water temperatures determine the season of development in mid-latitude climates in both the mollusc and fish hosts. In tropical climates low temperature ceases to determine a season of development, although high temperatures might; however, with metacercariae in freshwater fishes there is no evidence for this. As indicated in Section V J, unfortunately there are no field or experimental studies of seasonal occurrence of metacercariae in freshwater fishes in tropical climate zones so that no comment can be made. It is probable, however, as noted in Section V C, that as temperatures vary only slightly during the year other factors, such as seasonal rainfall, will come into operation. K.

EXPERIMENTAL STUDIES

I n order to fully understand the patterns of occurrence of metacercariae in natural populations of freshwater fishes it is important to obtain experiH

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mental data about as many aspects of the biology of the metacercariae as possible. Unfortunately relatively little experimental work has been attempted, although some has been described in earlier sections. Summer

atitude North pole

00

I

Invasion by cerco riae

- - - - - - ---

-1-

too low for invasion

70

60

Temperatures

Temperatures below IO'C I

create a season of

50

invasion

40

30 20

t

Temperatures

of Cancer -Tropic ----- -- I

-

do not

I

create a

I 10

0

I

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I I

invasion

I -Equator - - - - - - - - 1---------J

I

F

I

M

I

A

I

M

I l l

J J Month

I

A

I

S

I

O

1

N

I

D

Invasion assumed abovf 10°C

FIG. 3. The season of invasion for a species of metacercaria that requires a minimum temperature of 10°C for development in the fish host. The example is shown for the northern hemisphere. See text p. 213 for full explanation.

Experimental studies are needed to determine the minimum, optimum and maximum temperatures for liberation of cercariae, invasion of the fish hosts and formation of the metacercariae. The length of time for development of the metacercariae at a range of temperatures should also be determined. The length of life of the metacercariae, and the period for which infectivity of the metacercariae to the definitive host is maintained should also be investigated experimentally. The effect of other abiotic factors such as day length, which may be important in determining seasonal occurrence, should also be examined experimentally.

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Abiotic factors, including the amount of light entering the water, the depth, hydrogen ion concentration (pH), oxygen content, salinity and the factor of standing or running water (Bauer, 1959a, b; Engelbrecht, 1963) are all important in the biology of the trematodes, but so far they have not been shown to be significant in determining seasonal occurrence of metacercariae. The experimental evidence thus far has shown water temperature to be the most significant single factor in controlling seasonal patterns of occurrence of metacercariae in freshwaters.

VI. SEASONAL STUDIES OF ADULTTREMATODES A.

SUBCLASS ASPIDOGASTREA

1 . Family Aspidogastridae Aspidogaster limacoides Diesing, 1835 Seasonal incidence and intensity of infection of four species of fishes by A. limacoides in the Dnepr Delta, U.S.S.R., was reported by Komarova, T. I. (1964). I n Blicca bjoerkna incidence and intensity rose from 337( (2-18) in February to a peak of 100% (4-18) in May, to fall a little in June, 68.7 % (2-40) and more by October, 60% (1-6). A similar pattern of incidence and intensity was seen in Rutilus rutilus heckeli, rising from 13.2% (1) in February to a peak intensity (1-30) in May and peak incidence in June (93-3%), followed by fall in October, 53.3% (1-21). In Abramis brama and Vimba vimba vimba natio carinata occurrence was sporadic, but within the overall pattern found in B. bjoerkna and R. rutilus heckeli. Dubinina ( 1 949) found A. limacoides in Abramis brama, Cyprinus carpio, Lucioperca lucioperca and Silurus glanis in the Volga Delta, U.S.S.R., during the spring of 1941, but not in the spring or summer of 1940 or the winter of 1941. Marits and Tomnatik (1971) and Marits and Vladimirov (1969) reported A. limacoides in A . brama and Vimba vimba vimba natio carinata respectively from Dubossary Reservoir, Moldavia, U.S.S.R., during summer and autumn. N o infections were seen in the spring. The Aspidogastridae have a simple development, without metamorphosis. The larva emerges from the egg with the adult form except for the possession of two cephalic glands to facilitate penetration into host tissues and a simpler structure of the holdfast disc (Bykhovskaya-Pavlovskaya, in BykhovskayaPavlovskaya et al., 1962). B.

SUBCLASS DIDYMOZOIDEA

1. Family Didymozoidae

Ovarioneniatobothrium texomensis (McTntosh and Self, 1955) The species was described as Neniatobothrium texomensis by Mclntosh and Self (1955) but was placed in a new genus Ovarionematobothrium by Yamaguti (1 97 I). The seasonal pattern of occurrence has been described by Self et al. (1961, 1963) from Lake Texoma, Oklahoma, U.S.A. The fishes infected were

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Ictiobus bubalus, 1. cyprinellus and I. niger. The worms were found in the ovaries of fishes examined between 15 November and 1 July. The November worms were sexually mature and contained eggs, but they were not gravid. At that time the ovaries of the fishes were well developed preparatory to the spring spawning season. In February there were extensive brown streaks of eggs visible i n the worms. The fishes spawned as early as late February, or as late as June. As long as the fish ovaries were gravid and healthy the 0. texomensis remained alive but after spawning only fragments of the worms remained. This, together with the presence of worms extending from the genital pore of the female fishes, was considered as evidence by Self et al. (1963) that the eggs of the worms were liberated primarily by disintegration of fragments discharged from the fishes with their eggs. A common occurrence of pieces of dead worms in spawned female fishes suggested that entire worms were seldom aborted. Self et a/. (1963) induced a gravid female fish to spawn artificially. After the spawning a worm fragment about 4 0 c m long was found in the aquarium indicating that this was the method for liberation of the eggs of 0. texomensis from its host. When the host did not spawn, and the eggs were resorbed, the trematodes died and disintegrated. The worm eggs remained viable for several weeks but there was no evidence that any escaped from the fishes. The remains of worms and eggs persisted into the next year as relics of previous infections. It is noteworthy that Self et a/. (1961, 1963) did not find immature worms. N o viable eggs were seen over the period 10 August t o 15 November. Tshii (1935) postulated a direct life cycle for the Family, and described such a cycle for Didymocytis katsuvc~onicola.Baer and Joyeux (196 I ) regarded the family as a subclass, rather than a group within the digenetic trematodes, and this is the arrangement that has been used here. C.

SUBCLASS DIGENEA

1. Family Allocreadiidae Allocreadium fasciatusi Kakaji, 1969 Dr Madhavi has kindly allowed me to summarize her observaticns on this species which at the time of writing this review were in press (Madhavi, 1979). A . ,fasciatusi was studied in Aplocheilus melastigma in a stream at Waltair, India. The snail host in the life cycle was Amnicolu frara/7corica, and cercariae were released all year. However, transmission to A . melastigma was through several species of copepod intermediate hosts, which were most abundant in September after the seasonal rains of July and August. Although immature and mature A. .fasciatusi were present in the fishes all year, there was a seasonal cycle of peak invasion, incidence, intensity and maturation of the trematodes. Maximum invasion of the fishes from copepods occurred in September, and small A . jusciatusi were especially common at that time. The recruitment in September and October exceeded loss of worms from the fishes, hence there was a high incidence and intensity of infection, to give the peak population size, which fell in November t o remain more or less constant

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

217

until August of the following year. During the period of constant population there was a dynamic balance between recruitment to and loss from the trematode population. The maturation of A . fasciatusi also followed a seasonal pattern for the majority of individuals. In September most were small and immature, indeed from May t o October the greater proportion of the population was without eggs. From November to April mature trematodes predominated, but gravid individuals were most abundant from January to April. Mature worms seen during August t o December contained fewer eggs. The maximum number of eggs were shed during January t o April. Madhavi showed that temperature did not play an important role in the seasonal occurrence of A . fasciatusi in the conditions at Waltair. Although invasion, occurrence and maturation of the trematodes could occur all through the year, none the less there was a seasonal periodicity for a large proportion of the population of A . fasciatusi that was related to the peak incidence of the copepod intermediate hosts in September. The peak occurrence of copepods created a period of peak transmission of the trematode to the fishes, which thereby in turn established peak periods of growth, maturation and egg release. Allocreadium isoporum (Looss, 1894) A comprehensive investigation of seasonal occurrence of this species in Leucisciis cephalus, L. leuciscus and Rutilus rutilus at the River Lugg. Herefordshire, England was made by Davies, E. H. (1966, 1967). The patterns of incidence and intensity of occurrence were similar in the three host species. The incidence and intensity were lowest in L. cephalus and L. leuciscus in August (23%, mean 4 and lo%, mean 1 respectively) but in R. rutilus in August and September (7%, mean 2 and 0 respectively). In L. cephalus and L. leuciscus the incidence and intensity tose again in September and October, but not until October in R . rutilus, to remain high until August of the following year. Peak incidences and intensities were: L. cephalus, April 93 %. July, October, mean intensity per infected fish 21; L . leuciscus, October 71 %, May 22; R. rutilus, June 47 %, April 133. The maturation cycle was studied for A . isoporum. Davies, E. H. (1967) distinguished four stages. Stage I, parasites small, gonad rudiments, but no vitelline glands present; Stage 11, gonads well-developed, vitelline glands present, but no eggs in uterus; Stage 111, gonads and vitelline glands welldeveloped, eggs in uterus; and Stage IV, gonads regressed, eggs in uterus. The data obtained by Davies, E. H. (1967) are given in Fig. 4 for L. cephalus shown as the number of each developmental stage expressed as a percentage of the total trematodes examined each month. The results obtained for the other hosts were the same. It can be seen that there was an annual pattern of maturation, the cycle of which commenced from July onward, with maximum egg production in March to August. After egg production was completed the trematodes passed out from the fish. Young A . isoporum dominated the population between August and November, which indicated invasion of the fishes. Many of these individuals were subsequently lost, but those that remained produced eggs the following spring and summer.

218

JAMES C . CHUBB

Kennedy (1972) investigated A . isoporum in Leuciscus leuciscus at the River Avon, Hampshire, England. A low incidence was found in November, which increased to a maximum in March, to decrease through April to June. Trematodes were not found in July to October. Halvorsen (1972) studied A . isoporurn in Abramis brama and Rutilus rutilus in the River Glomma, Norway. The trematodes were found in May, June and July only, and in R. rutilus maximum gravid worms were seen in June. Halvorsen (1972) postulated that ecological conditions probably prevented infection at other times, for instance in the River Clomma low water temperatures in October/ November might prevent invasion until spring. Kozicka (1959), at Lake Druino and other lakes in Poland, was unable to observe a distinct periodicity of A . isoporurn but it was very common in the summer months, July,

IV

yI

111

u I3

-

B

u)

II

I

J

F

M

A

M

J

J

A

S

O

N

I

D

Months

FIG.4. The maturation of Allocveadiiim isopoviitn in Leiiciscris cephaliis in relation to the time of year. The data are shown as the number of each developmental stage expressed as a. percentage of the total trematodes examined each month. The developmental stages are described on p. 217. [The data are reproduced from Davies, E. H. (1967), Fig. 4.1, and were collected from the River Lugg, Herefordshire, England.]

August and even September. However, Koval’ (1952, quoted from Bauer, 1959a) found a clear-cut annual cycle in Cyprinus carpio in the middle reaches of the River Dnepr, U.S.S.R. Invasion of the fishes occurred in July and August and sexual maturation and accumulation of eggs in the uteri during winter. The fishes were free of infection by May to June of the following year. In contrast to the above observations, Malakhova (1961) reported A . isoporum from R. rutilus during all seasons in Lake Konche, Karelia, U.S.S.R.: autumn 1.1 % incidence, average intensity 2, winter 1.1 %, I , spring 3.3 %, 14 and summer 6-7%, 15.2. Occasional records of A. isoporum include those of Bogdanova (1958) in Esox Iucius from the River Volga, U.S.S.R. where A. isoporurn was found in February/March, but not in May or August, Hausmann (1897) in Abrarnis brama and Barbus barbus from Basel, Switzerland, where it occurred in March and May to August, and Lyubarskaya (1970) in Abrarnis brama from the Kuybyshev Reservoir, U.S.S.R. where a low infection (2.1 %) was seen in summer, but not in the other seasons. These instances refer perhaps to

HELMINTHS I N FRESHWATER FISHES

219

secondarily established infections (E. lzrcius) or auxiliary hosts ( A . brama and B. barbus). Allocreadium lobatum Wallin, 1909 This species can produce viable eggs by progenetic development in the intermediate hosts Crangonyx gracilis and Gammarus pseudolimnaeus or in the fish hosts Catostomus commersonnii commersonnii and Srmotilus atromaculatus atromaculatus in the normal manner (De Giusti, 1962). A. lobatum was studied in a stream in Michigan, U.S.A., where the mollusc Pisidium sp. was intermediate host. Cercariae occurred late in the summer coinciding with the height of the young G. pseudolimnaeus population. The gammarid in the stream studied appeared to have an annual cycle. Progenetic development of A. lobaturn occurred in G. pseudolimnaeus, so that at the death of the adult shrimp generation large numbers of A. lobatum eggs were released to infect the molluscan host. Mature trematodes were seen in G. pseudolimnaeus from November to February. Adult A. lobatum also occurred in the fish hosts from early March to July (De Giusti, 1962). Allocreadium markewitschi Koval’, 1949 Koval’ (1952, quoted from Bauer, 1959a) found that the invasion of Chondrostoma nasus in the River Dnepr, U.S.S.R. occurred in early spring, March and April, but rarely in May, and that there were no parasites in the fishes from December to February. Allocreadium transversale (Rudolphi, 1802) Some information about A. transversale was collected by Davies, E. H. (1967) from the River Lugg, Herefordshire, England. Thymallus thymallus were infected in February, April, May, July and December. The stages of maturity of the trematodes (see A . isoporum for descriptions) were: February and April, Stage 1, one; Stage 2, six and Stage 3, one; May, Stages 314, seven. They suggested that the life in the fish host was based on an annual maturation cycle similar to that of A. isoporum. 2. Family Azygiidae Azygia lucii (Miiller, 1776) Markova (1958) studied the seasonal occurrence in Esox lucius from the River Oka, U.S.S.R. The incidence was highest in January (60%) to March 93.3 %), through May to December it fluctuated between 11.1 (October) and 45.5 % (June). Intensity was high (expressed as average infections) in January (53), February (5.7) and March (15.5) and low (1.7 down to 0.2) otherwise. Small (1-5 mm long) A. lucii were maximal in January (29.1 % of population) and also found in February, March and July. A. lucii 6-15 nim long were found in most months, but increased from January (48.1 %) to May and June (loo%), remained high in July (94.1 %) and August (100%) to fall thereafter (October, 21.4, November 39.3 and December 87.5 %). Trematodes longer than 15 mm were found in October (78.6%), November (60.7%), December (12.5 %), January (22.8 %), February (8.1 %) and March (8.6 %). Markova (1958) concluded that the invasion of E. lucius occurred from January to March, growth and development during the following months

220

JAMES C . CHUBB

and the loss of this generation from December to March, concurrent with the invasion by the following generation. The relatively clear annual pattern of occurrence seen in the River Oka was not found by Halvorsen (1968) in €sox lucius in Bogstad Lake, Norway. Small, immature, A . lucii were found at all seasons, and as no crowding effect was seen, they were interpreted as newly acquired invasions. Owing to the pronounced seasonal changes of temperature and light at Bogstad Lake, which would restrict cercariae to the summer, Halvorsen (1968) concluded that there must be a second intermediate host in the life cycle. At the River Glomma, Norway, Halvorsen (1972) also found A . lucii in E. iucius at all times of the year. The percentage of gravid worms increased from May to June, but was very high all the time. Even in December more than 20% of A . lucii were gravid. Tell (1971), at Lake V6rtsjarv, Estonia, U.S.S.R., found A . Iucii in Esox lucius, Lucioperca lucioperca and Percafluviatilis. At the end of April and beginning of May the A. lucii were of maximum size and gravid, with high incidence and intensity of occurrence. At the end of May and beginning of June the worms disappeared from the fishes; the incidence and intensity was very low by the end of June/early July, but thereafter increased again until the following spring. Ginetsinskaya (1958) noted that the life cycle of A . lucii had a single intermediate host. Szidat (1932) considered that young E. lucius could serve as transport hosts to achieve invasion of larger E. lucius. Odening and Bockhardt ( 1976), at Beetzsee, near Brandenberg, Germany, showed that E. lucius became invaded by A . lucii cercariae directly as fingerlings up to 30 mm long, but older E. lucius acquired infections by eating infected individuals of the same or other species. The first route of invasion was seasonally limited and affected only fishes in their first year of life. The second route of invasion was not seasonally limited. Odening and Bockhardt (1976) found large A . Iucii in older E. lucius throughout the year. Other authors have found incidences of A . lucii during all seasons, IZYUmova (1958) at the Rybinsk Reservoir, U.S.S.R., in Lucioperca lucioperca and Perca fluviatilis, Izyumova (1960) in Esos lucius, Malakhova (1961) at Lake Konche, Karelia, U.S.S.R., in E. Iucius, Lota Iota and P. fluviatilis, and Ruszkowski (1926) at Warsaw, Poland, in E. lucius. Seasonal data of more sporadic occurrences have been given by Bogdanova (1958), Hausniann (1897), Izyumova (1959a) and Komarova, T. I. (1964). The host fishes and localities are given in Table 3. 3. Family Bucephalidae Bucephalus polymorphus Baer, 1821 The occurrence of metacercariae in fishes is reported in Section 111. The adult worms have been reported from the intestines of Esox lucius at all seasons of the year in the Oka River, U.S.S.R. (Markova, 1958). Observations by other authors, such as Bogdanova (1958) in the River Volga and Komarova, T. I. (1964) in the Dnepr Delta, U.S.S.R., have con-

TABLE3 Studies on seasonal occurretice of adults of trematodes listed in the climate zones of the World (see map Fig. I , Chubb, 1979)

The species are in alphabetical order Climate zones 1. Tropical la. RAINY (humid climate)

1b. SAVANNA (humid climate)

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

Trematode species

Host species

Locality

References

tropical forest Transversotrema patialeme

Macropodus cuparius

Batalagoda, Sri Lanka

Macropodus cupanus Ophiocephalus putictatirs Tilapia mossambica

Batalagoda, Sri Lanka

Crusz and Sathananthan (1 960) Crusz et al. (1964)

tropical grassland Waltair, India River Hooghly, India River Hooghly, India tropical highland

Allocreadium fasciatusi ' Aplocheilus melastigma Aphanurus monolecithus Hilsa ilisha Orientophorus brevichrus Hilsa ilisha no seasonal studies

Madhavi (1 979) Pal (1963) Pal (1963)

no seasonal studies

hot semi-desert

no seasonal studies

hot desert

no seasonal studies

scrub, woodland, olive deciduous forest Yoshino (1940) Okayama Province, Japan

Asymphylodora titicae

Carassius auratus ~

~~~~

~

-

~~

TABLE 3 (continued) Climate zones 2b. (continued)

Trematode species Crepidostomirni cooperi

Host species

Locality

Lepomis cyanellus Lepomis megalotis Aphredoderus sayanus

Crepidostoniuni isostomum Hilsa ilisha Lecithaster extralobus Hilsa ilisha Lecithaster indicus Orientophorus brevichrirs Hilsa ilisha 0 varionematobothri~~m Ictiobius bubalus Ictiobius cyprinellirs texomensis Ictiobius niger Aphredoderus sayanus Phyllodistomum pearsei Sangirinicola arniata

3. Mid-latitude 3a. i. HUMID WARM SUMMERS

Sangiiinicola magnits

Little River, Oklahoma, U.S.A. Whisky Bay, Louisiana, U.S.A. Allahabad, India Allahabad, India Allahabad, India Lake Texoma, Oklahoma. U. S.A.

McDaniel and Bailey (1 974) Elkins and Corkum (1976) Srivastava (1 935a) Srivastava (1935a) Srivastava (1935b) Self et al. (1961, 1963)

Whisky Bay, Louisiana, U.S.A. Taihu, China

Elkins and Corkum (1976) Cheng-Yen et al. (1965)

Aristichthys nobilis Cyprinus carpio Hypophthalmichthys molitrix Mylopharyngodon piceus Ctenopharyngodon idella Taihu, China

Acetodextra aniiuri

fctalurus punctatus

Allocreadium isoporum

Abramis brama Barbus barbus Ictalurus natalis

Alloglossidium corti

References

Cheng-Yen et al. (1965)

temperate grassland, mixed forest River Wabash, Indiana, U.S.A. Basel, Switzerland Durham, North Carolina, U.S.A. ~~~

~

__

Perkins (1950, 1951, 1956) Hausmann (1 897) Holl (1932) -

~

___

Climate zones

Trematode species

3a. i. (continued)

Host species

Ictalurus natalis Aspidogaster liniacoides

Abramis brama

Asymphylodora imitans

Vimba viniba vimba natio carinata Abramis brama

Asynlphylodora tincae Azygia lucii Bucephalus polymorplius Bunodera luciopercae

Vimba viniba vimba natio carinata Barbus barbus Tinca tinca Tinca tinca Esox lucius Esox lucius Lucioperca Iucioperca Lucioperca lucioperca Perca fluviatilis Perca Juviatilis Perca fluviatilis Esox lucius Perca fluviatilis Gymnocephalus cernua Perca fluviatilis

Locality Ramona Lake, St. Louis, Missouri, U.S.A. Dubossary Reservoir, Moldavia, U.S.S.R. Dubossary Reservoir, Moldavia, U.S.S.R. Dubossary Reservoir, Moldavia, U.S.S.R. Dubossary Reservoir, Moldavia, U.S.S.R. Basel, Switzerland

References McCoy (1928a) Marits and Tomnatik (1971) Marits and Vladimirov (1969) Marits and Tomnatik (1971) Marits and Vladimirov (1969) Hausmann (1 897)

Warsaw, Poland Basel, Switzerland Warsaw, Poland Basel, Switzerland Lake Balaton, Hungary Czechoslovakia Basel, Switzerland Lake Wigry, Poland Warsaw, Poland

Ruszkowski (1926) Hausmann (1897) Ruszkowski (1926) Hausmann (I 897) Molnar (1 966)

Pod6 brady, Czechoslovakia

Sramek (I 901)

~

~~

-

~

Dyk et a/. (1954) Hausmann (1897) Milicer (1938) Ruszkowski (1926)

TABLE 3 (continued) ~

Climate zones

Trematode species

3a. i. (continued)

Host species

Perca fluviatilis Crepidostomum cornutum Crepidostonium farionis

Crepidostomum ictaluri

Lepomis gulosus Lepomis macrocliirus Micropterus salmoides Salmo trutta Salvelinus fontinalis Salmo trutta Ictalurus punctatus

Lissorchis fairporti

Ictiobus bubalus Ictiobus cyprinell~is

Nicolla skrjabini

Vimba vimba vimba natio carinata Gymnocephalus cernua Lucioperca lucioperca Gymnocephalus cernua

Nicolla wisniewskii Phyllodistomum elongatum

Salmo trutta Thymallus thymallus Vimba vimba vimba natio carinata Abramis brama

Locality River Svratka, Czechoslovakia Lake Fort Smith, Arkansas, U.S.A.

References Vojtkova (1959) Cloutman (1975)

Lakes Nove Strbske, PopradskC, StrbskC, High Tatra, Czechoslovakia Czechoslovakia Lake Carl Blackwell, Oklahoma, U.S.A. Fairport Biological Station, Iowa, U.S.A.

Dyk (1957, 1958)

Dubossary Reservoir, Moldavia, U.S.S.R. Lake Balaton, Hungary Lake Balaton, Hungary Transcarpathian area, U.S.S.R. Dubossary Reservoir, Moldavia, U.S.S.R. River Svratka, Czechoslovakia

Marits and Vladimirov (1969) Molnar (1 966)

Dyk et al. (1954) Spall and Summerfelt (1 969) Magath (1918)

Ponyi et al. (1972) Koval’ et al. (1973) Marits and Vladimirov (1969) Vojtkova (1 959)

Climate zones

3a. i. (continued)

Trematode species

Host species

Phyllodistomum lacustri

Ictalurus punctatus

Phyllodistomum pearsi

Enneachanthus gloriosus

Phyllodistomum staffordi

Ictalurus natalis

Pisciamphistoma stunkardi Lepomis gulosus Lepomis macrocliirus Micropterus salmoides Lepomis gibbosus Lepomis gulosus Rhipidocotyle illense Lucioperca lucioperca Sanguinicola inermis

Cyprinus carpio Cyprinus carpio

Sphaerostoma bramae

Cyprinus carpio Cyprinus carpio Cyprinus carpio Abramis brama Rutilus rutilus Scardinius erythrophthalmus Abramis brama

Locality

References

Lake Carl Blackwell, Oklahoma, U.S.A. Lakeview, North Carolina, U.S.A. Durham, North Carolina, U.S.A. Lake Fort Smith, Arkansas, U.S.A.

Spa11 and Summerfelt (1969) Holl (1932)

Durham, North Carolina, U.S.A. Lake Balaton, Hung ary Western districts of Ukraine, U.S.S.R. Lvov, Ukraine, U.S.S.R. Czechoslovakia Ukraine, U.S.S.R. Germany Dubossary Reservoir, Moldavia, U.S.S.R. Warsaw, Poland

Holl (1932)

River Svratka, Czechoslovakia

Holl (1932) Cloutman (1975)

Molnar (1 966) Ivasik (1953, 1957) Ivasik and Svirepo (1971) Lucky (1964) Sapozhnikov (1976) Scheming (1923) Marits and Tomnatik (1971) Ruszkowski ( 1 926) Vojtkova (1959)

TABLE 3 (continued) Climate zones

Trematode species

3a. i. (continuedj

3a. ii. HUMID COOL SUMMERS

Host species

Locality

References

Basel, Switzerland

Barbus barbus Chondrostonia nasus Gobio gobio Leuciscus cephalus Scardinius erythrophthalmus

Hausmann (1897)

temperate grassland, mixed forest River Volga, U.S.S.R. River Dnepr, U.S.S.R. Kuybyshev Reservoir, U .S.S.R .

Bogdanova (1958) Koval’ (1952) Lyubarskaya (1970)

Allocveadium isoporum

Esox lucius Cyprinus carpio Abramis brama

Allocreadium lobatum

Catostomus c. commersoni Semotilus a. atromaculatus Chondrostoma nasus

Michigan, U S A .

De Giusti (1962)

River Dnepr, U.S.S.R.

Koval’ (1 952)

Blicca bjoerkna Tincu tinca

Rybinsk Reservoir, Izyumova (1960) U.S.S.R. River Donets, U.S.S.R. Komarova, M. S. (1957)

Tinca tiiica

River Dnepr, U.S.S.R.

A llocreadium marke witschi Asymphylodova imitans Asymphylodora kubanicum Asymphylodora tincue

Komarova, M. S. (1951b) River Donets, U.S.S.R. Komarova, M. S. (1957) Lake Bol’shoe, Omsk Lyubina (1970) Region, U.S.S.R.

Tinca tinca Tinca tinca ~~

___

~

Climate zones 3a. ii. (continued)

Trematode species

Host species Esox lucius Lucioperca lucioperca Pelems cultratus Perca fluviatilis Cymnocephalus cernua

Azygia Iucii

Esox lucius

Bucephalus polymorphus

. Bunodera Iuciopercae

Esox Iucius Esox lucius Lucioperca lucioperca Perca fluviatilis Esox lucius Esox lucius Esox lucius Perca flavescens Lucioperca lucioperru Perca fluviatilis Lucioperca Iucioperca Perca fluviatilis Cymnocephalus cernuu

Esox lucius

Locality

References

River Volga, U.S.S.R. Rybinsk Reservoir, U.S.S.R.

Bogdanova (1958) Izyurnova (1958)

Rybinsk Reservoir, U .S.S.R . Rybinsk Reservoir, U.S.S.R. River Oka, U.S.S.R. Lake Vbrtsjarv, Estonia, U.S.S.R.

Izyurnova (1959a)

River Volga, U.S.S.R. River Oka, U.S.S.R. River Volga, U.S.S.R. Lake Opeongo, Ontario, Canada Lakes Seliger and Senezh, Moscow Canal Reservoirs, U.S.S.R. Rybinsk Reservoir, U.S.S.R. Rybinsk Reservoir, U .S.S.R . Rybinsk Reservoir, U.S.S.R.

Izyurnova (1960) Markova (1958) Tell (1971) Bogdanova (1958) Markova (1958) Bogdanova (1958) Cannon (1971, 1972, 1973) Chertkova (1971)

Izyumova (1958, 1959b) Izyurnova (1959a) Izyurnova ( I 960)

TABLE 3 (continued) Climate zones

Trematode species

Host species Percidae Perca fluviatilis Lucioperca lucioperca Perca fluviatilis Esox Iucius Perca flavescens

3a. ii. (continued)

Perca fluviatilis Esox lucius

Perca flavescens

Locality River Dnepr, U.S.S.R. River Dnepr, U.S.S.R. Lake Seliger, U.S.S.R.

Lake Dusia, Lithuania, Rautskis (1970b) U.S.S.R. Bay of Quinte, Lake Tedla and Fernando Ontario, Canada (1969) Lake Vbrtsjarv, Estonia, U.S.S.R.

Tell (1971) Cannon (1971, 1972, 1973) Cannon (1972, 1973)

Bunodera sacculata Crepidostomum cooperi

Perca flavescens

Nicolla skrjabini

Gymnocephalus cernua

Lake Opeongo, Ontario, Canada Lake Opeongo, Ontario, Canada River Dnepr, U.S.S.R.

Palaeorchis incognitus Phyllodistomum angulatum

Gymnocephalcis cernua Rutilus rutilus Lucioperca lucioperca Perca fluviatilis

River Dnepr, U.S.S.R. River Dnestr, U.S.S.R. Rybinsk Reservoir, U.S.S.R.

~~~

Komarova, M. S. (1941) Koval’ (1955a,b) Lyaiman (1940)

River Oka, U.S.S.R. Markova (1958) Yahara River lakes, Pearse (1924) Wisconsin, U.S.A. Lake Dusia, Lithuania, Rautskis (1970a) U.S.S.R.

Esox Iucius Lucioperca Iucioperca Perca fluviatilis Perca flavescens

~~~

References

Komarova, M. S. (1 951a) Koval’ (1952) Kulakovskaya (1955) Izyumova (1958, 1959b)

Climate zones 3a. ii. (continued)

Trematode species Phyllodistomum conostomum Phyllodistomum elongaturn

Host species Coregonus lavaretus baeri natio ladogae Abramis brama Abramis brama Rutilus rutilus Abramis ballerus Blicca bjoerkna

Phyllodistonium folium

Esox luciiis Esox lucius Abvaniis bvania

Esox lucius Esox lucius Esox lucius Phyllodistomuni pseudofoliuni Phyllodistomuni sp. Rliipidocotyle illerise

Gymriocephalus ceviiiia Gasterosteus acwleatits Pungitius pungitiiis Perca fliii~iatilis

Locality

References

Lake Ladoga, U.S.S.R. Bauer and Nikol’skaya (1957) River Volga, U.S.S.R. Bogdanova (1958) Rybinsk Reservoir, Izyurnova (1958) U.S.S.R. Rybinsk Reservoir, Izyurnova (1959a) U .S.S.R . Rybinsk Reservoir, Izyumova (I 960) U.S.S.R. River Volga, U.S.S.R. Rybinsk Reservoir, U.S.S.R. Kuybyshev Reservoir, U .S.S.R . River Oka, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R. Lake Vbrtsjarv, Estonia, U.S.S.R. Rybinsk Reservoir, U.S.S.R. Neva Delta Reservoir, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R.

Bogdanova (1958) Izyumova (1 960) Lyubarskaya (1970) Markova (1958) Rautskis (1970b) Tell (1971) Izyumova ( I 959a) Banina and Isakov (1 972) Rautskis (1970a)

TABLE3 (continued) Climate zones

Trematode species

Host species

3a. ii. (continued)

Esox luciiis

Sangiiitiicola inermis

Cyprinus carpio Cyprinus carpio Cyprinus carpio Cyprinus carpio

Sanguinicola volgensis

Esox lucius

Sphaerostonia bramae

Abramis brama Esox lucius Abramis brama Pelecus cultratus Rutilus rutilus Abramis ballerus Blicca bjoerkna Esox luciiis Cypri nidae Leuciscus cephahrs Abramis brama Perca Jluviatilis Esox lucius

~~~~~

~

~~

.~

~~

~~

Locality Lake Dusia, Lithuania, U.S.S.R. U.S.S.R. Byelorussia, U.S.S.R. Moscow region, U.S.S.R. Moscow region, U.S.S.R. Rybinsk Reservoir, U.S.S.R. River Volga, U.S.S.R.

References Rautskis (1970b) Bauer (1 959a), Bauer et al. (1969) Chechina (1959) Lyaiman (1951) Naumova (1961a,b,c) Izyumova (1 960) Bogdanova (1 958)

Rybinsk Reservoir, U.S.S.R. Rybinsk Reservoir, U.S.S.R. Rybinsk Reservoir, U.S.S.R.

Izyumova (1958, 1959b)

River Dnepr, U.S.S.R. River Dnestr, U.S.S.R. Kuybyshev Reservoir, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R. Lake Dusia, Lithuania, U.S.S.R.

Koval’ (1 952) Kulakovskaya (1 955) Lyubarskaya ( 1 970)

Izyumova (1959a) Izyumova (1960)

Rautskis (1 970a) Rautskis (1970b)

Climate zones

Trematode species

Host species

Locality

3a. iii. EAST COAST

3b. MARINE WEST COAST

Bunodera luciopercae

Perca Jlavescens

Crepidostomum cooperi

Perca flavescens

Rhipidocotyle septpapillata

Lepomis gibbosus

Allocreadium isoporum

'

temperate grassland, mixed forest Lake Oneida, New York, U.S.A. Lake Oneida, New York, U.S.A. River Potomac, Virginia, U.S.A.

Leuciscus cephalus Leuciscus leuciscus Rutilus rutilus Abramis brama Rutilus rutilus Leuciscus leuciscus Cyprinidae

AlIocreadium transversale Thymallus thymallus Asyniphylodora kubanicum

Rutilus rutilus ~

_

_

_

_

temperate grassland, deciduous forest River Lugg, Herefordshire, England River Glomma, Norway River Avon, Hampshire, England Lakes Druzno, Labedzie and Marnry Polnocne, Poland River Lugg, Herefordshire, England Worcester-Birmingham Canal, England

References

Noble, R. L. (1970) Noble, R. L. (1970) Krull (1934b)

Davies, E. H. (1966, 1967) Halvorsen (1 972) Kennedy (1 972) Kozicka (1 959)

Davies, E. H. (1967) Evans, N. A. (1977b, 1978)

TABLE 3 (continued) Climate zones

Trematode species

3b. (continued)

Asymphylodora markewitschi Asymphylodora tincae

Azygia lucii

Host species

References

Abramis bratna Rutilus rutiliis

Shropshire Union Canal, Cheshire, England

Alburnus alburnus Scardinius erythrophthalmiis Titica tincu

Lake Mamry Polnocne, Kozicka (1959) Poland

Tinca tiricu Tinca tinca Esox lucius Esox lucius

Esox lucius Bucephalus polymorphus Bunodera luciopercae

Locality

Lucioperca Iucioperca Perca fluviatilis Perca jhviatilis Perca fluviatilis Perca fluviatilis Other predatory fishes Perca f l u viatilis

Lakes Druzno, Labqdzie, Tajty and Oiwin, Poland Lake Klawoj, Poland Olsztyn Region, Poland Lake Bogstad, Norway River Glomma, Norway Beetzee, Germany Lake Druzno, Poland Llyn Tegid, Wales Loch Leven, Scotland River Glomma, Norway Lake Druzno, Poland Shropshire Union Canal, Cheshire, England ~

~~~

Mishra (1966)

Kozicka (1959) Wierzbicka ( I 964) Wierzbicka (1970) Halvorsen (1968) Halvorsen (1972) Odening and Bockhardt (1976) Kozicka (1959) Andrews (1 977) Campbell (1974) Halvorsen (1 972) Kozicka (1959) Mishra (1966) ~

Climate zones

Trematode species

3b. (continued)

Host species

Esox liccius Perca fluviatilis Perca fluviatilis

Crepidostomum farionis

Perca fluviatilis Gymnocephalus cernua Perca fluviatilis Salmo trutta Salmo trictta Thymallus thymallus Thymallus thymallus Salmo trutta Salmo salar (parr) Salmo trutta

Crepidostornum metoecus

Salmo trutta Salmo tvutta Salnio trutta

Locality Rostherne Mere, Cheshire, England Forest lake, near Oslo, Norway Lake Dargin, Poland Hanningfield Reservoir, Essex, England Afon Terrig, Wales Rivers Wharfe and Yore, Yorkshire, En g1and Llyn Tegid, Wales Dunalastair Reservoir, Scotland Rivers Pysgotwr, Rheidol and Teify, Wales Chirk Fish Hatchery, Llyn Celyn, Tegid, Wales Afon Terrig, Wales Dowles Brook, Worcestersh i re, England

References Rizvi (1964, 1968) Skorping (1976) Wierzbicki (1970, 1971) Wootten (1973b) Awachie (1963, 1968) Brown (1927) Chubb (1961) Robertson (1953) Thomas (1958a, 1964) Aderounmu (personal communication) Awachie (1963, 1968), Awachie and Chubb ( 1 964) Britain (1971)

TABLE3 (continued) ~

Climate zones

Trematode species

3b. (continued)

Host species Salmo trutta Salmo trutta S a h o trutta Thymallus thymallus Thymallus thymallus

Salmo trutfu Salmo salar (parr) Salmo trutta Mucrolecitkus pupilliger Nicolla gallica

Phoxinus phoxinus Cottus gobio

Phyllodistomum folium

Gasterosteus aculeatus Esox lucius TI1y mallus thymallus

Pliyllodistoniimi simile Rhipidocotyle illense

Gasterosteus aculeatus Salmo trutta Esox lucius

Locality Loch Strathbeg, Scotland Loch Leven, Scotland Llyn Tegid, Wales

References Bwathondi (1976) Campbell (1974) Chubb (1961)

River Lugg, Herefordshire, England

Davies, E. H. (1967)

Dowles Brook, Worcestershire, England Rivers Pysgotwr, Rheidol and Teify, Wales Frongoch Lake, Wales River Avon, Hampshire, England Pond, Baildon Moor, Yorkshire, England River Lugg, Herefordshire, England Experimental River Teify, Wales River Glomma, Norway

John (1973) Thomas (1958a, 1964) Bibby (1972) Rumpus (1975) Chappell (1969) Davies, E. H. (1967) Johnston, J. M. (1967) Thomas (1 958b, 1964) Halvorsen (1972)

Climate zones

Trematode species

3b. (continued)

Sphaerostoma bramae

Host species

References

Esox lucius Gyninocephalus cernua Perca fluviatilis

Lake Druzno, Poland

Kozicka (1959)

Perca fluviatilis

Lake Dargin, Poland

Wierzbicki (1970)

Leuciscus cephalus Leuciscus leuciscus Rutilus rutilus

River Lugg, Herefordshire, England

Davies, E. H. (1967)

Rutilus rutilus

Worcester-Birmingham Evans, N. A. (1977a,b) Canal, England River Avon, Kennedy (1972) Hampshire, England Lakes Druzno and Kozicka (1959) Mamry Polnocne, Poland

Leuciscus leuciscus Abramis brama Blicca bjoerkna Esox lucius Rutilus rutilus

3 ~ .SEMI-DESERT

Locality

Sphaerostonia globiporum

Misgurnus fossilis Rutilus rutilus Scarditiius erythrophtlialmus

Aspidogaster limacoides

Abramis brama Cyprinus carpio Lucioperca lucioperca Silurus glanis

Rostherne Mere, Cheshire, England Lakes Druino and Mamry Polnocne, Poland prairie and steppe Volga Delta, U.S.S.R.

Rizvi (1964) Kozicka (1 959)

Dubinina (1949)

TABLE 3 (continued) Climate zones

3c. (continued)

Trematode species

Host species

Abramis brama Blicca bjoerkna Rutilus rutilus heckeli Vimba vimba vimba natio carinata Asyniphylodora detneli Rutilus rutilus heckeli Asymphylodora iniitans Abramis brama Abramis brama Blicca bjoerkna Pelecus cultratus Rutilus rutilus heckeli Vimba vimba vimba natio carinata Asynlphylodora kubanicum Abramis brama Cyprinus carpio Abramis brama Blicca bjoerkna Rutilus rutilus heckeli Vimba vimba vimba natio carinata Esox lucius Azygia lucii Lucioperca lucioperca Lucioperca lucioperca Bucephalus polyniorphus Esox luciiis Lucioperca Iucioperca Pelecus cubratus

Locality

References

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Dnepr Delta, U.S.S.R. Volga Delta, U.S.S.R. Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964) Dubinina (1949) Komarova, T. 1. (1964)

Volga Delta, U.S.S.R.

Dubinina (1949)

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Volga Delta, U.S.S.R. Dnepr Delta, U.S.S.R.

Dubinina (1949) Komarova, T. I. (1964)

Climate zones 3c. (cotititiirecl)

Trematode species Buriocotyle cingrtlata Butiodera Iuciopercae

Crepidostotnrrnifarionis Nicolla slirjabini

Host species Silirrus glatiis Lucioperca lucioperca Esox Iircius Liicioperca lucioperca Lucioperca Iucioperca Salmo trrrtta

Abramis brama Esox lucius Lucioperca lucioperca Pelecus cultratirs . Silurus glanis Orientocreadium siluri Palaeorchis iticognitsrs Blicca bjoerkna Rutilus rutilirs heckeli Palaeorchis utiicus Blicca bjoerkna Phyllodistomum angulatum Lucioperca lucioperca Phyllodistomum elorigatuni Abramis brama Cypritiiis carpio Abramis brarna Blicca bjoerkna Rutilus rutilus heckeli Viniba vimba viniba natio carinata Pltylloclistomrmi foliirni Esox lucius Pelecirs cultratirs

Locality

References

Volga Delta, U.S.S.R. Volga Delta, U.S.S.R. Dnepr Delta, U.S.S.R.

Dubinina (1949) Dubinina (1949) Komarova, T. I. (1964)

River Volga, near Saratov, U. S.S.R. South Platte River, Colorado, U.S.A. Dnepr Delta, U.S.S.R.

Lavrov ( I 955)

Komarova, 7'. I. (1964)

Volga Delta, U.S.S.R. Dnepr Delta, U.S.S.R.

Dubinina (1949) Komarova, T. I. (1964)

Dnepr Delta, U.S.S.R. Volga Delta, U.S.S.R. Volga Delta, U.S.S.R.

Komarova, T. I. (1964) Dubinina (1949) Dubinina (1949)

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Dnepr Delta, U.S.S.R.

Komarova, T. I. (1964)

Voth et a/. (1974)

TABLE 3 (contimied) Climate zones

Trematode species

~

3c. (continued)

Locality

References

~

Sphaerostonia braniae

Abrarnis brarna Blicca bjoerkna Pelecus cultratus Rutilus rutilus heckeli no seasonal studies

3d. DESERT 3e. SUB-POLAR

Host species

Allocreadium isoporuni

Rutilus rutilus

Azygia lucii

Esox lurius Lota lota Perca fluviatilis Perca fluviatilis

Bunodera luciopercae

Esox Iucius Lota lota Perca fluviatilis Perca fluviatilis

Perca fluviatilis Phyllodistornuni elongaturn Abrarnis brarna Sphaerostonia braniae

Esox lucius Lota lota Perca fluviatilis Rutilus rutilus

Dnepr Delta, U.S.S.R. Komarova, T. I. (1964)

cool desert coniferous forest Lake Konche, Karelia, U.S.S.R. Lake Konche, Karelia, U.S.S.R.

Malakhova (1961) Malakhova (1961)

River Yenisei, U.S.S.R. Androsova and Bauer ( 1947) Lake Konche, Karelia, Malakhova (1961) U .S.S.R . Lake Konche, Karelia, Malakhova (1963) U.S.S.R. Karelian lakes, Shul’man et al. (1974) U .S.S.R . Lake Ubinsk, Siberia, Titova (1957) U.S.S.R. Lake Konche, Karelia, Malakhova (1961) U.S.S.R.

Climate zones

Trematode species

3e. (coritiwed)

Host species RirtiIris rirtilits

Sphaerostonra globipovirni Rirtilrts vutilia

Locality Lake Konche, Karelia, U.S.S.R. Karelian lakes, U.S.S.R.

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

no seasonal studies no suitable habitats for freshwater trematodes

tundra icefields and glaciers

5. Mountain

no seasonal studies

heath, rocks and scree

References Malakhova (1963) Shul’man et al. (1974)

240

JAMES C. CHUBB

firmed this. lncidence and intensity of occurrence varied widely from month to month, for example from Komarova, T. 1. (1964), February 73.3% incidence, intensity 4-250, March 60%, 5-190, April/May, 37 %, 3-41 and October 20 %, 6-38. In Lucioperca lucioperca a similar all-season occurrence has been found. Hausmann (1897), at Basef, Switzerland, observed B. polymorplzus in April, July, September and December. Dubinina (1949) found it during summer, winter and spring in the Volga Delta, U.S.S.R., Komarova, T. I. (1964) in the Dnepr Delta, U.S.S.R., from April to October, and Molnar (1966) in Lake Balaton, Hungary, in July t o October. Highest incidence was in spring (Dubinina, 1949; Komarova, T. I., 1964). Kozicka (1959) at Lake Druino, Poland, found fully adult specimens of B. polyinovphus filled with eggs in June, July and August. Rlzipidocotyle illense (Ziegler, 1883) The occurrence of metacercariae in fishes is given in Section 111. Halvorsen (1972) at the River Glomma, Norway, found metacercariae in cyprinids all year, but observed the adults in Esox lucius from July t o October only, when almost all the worms were gravid. Kozicka (1959) at Lake Druino, Poland, studied R. illense in E. lucius, Perca j7uviatilis and rarely Gyunnoceplialus cernua from April t o November. She discovered single specimens that were only in the first stage of maturation in June, but found large numbers of adult specimens filled with eggs several times in July and August. However, Kozicka (1959) remarked that it was noteworthy that specimens not quite sexually mature were in the majority. Molnar (1966) at Lake Balaton, Hungary, did not find R . illense in Lucioperca lucioperca fry from May t o August, but did see infections in young fishes 64-190 mm long as follows: 1 July, 57.1 % ([-lo), 9 August, 93.3% (1-40), 12 September, 100% (4-6) and 14 October, 50% (21). In Lake Dusia, Lithuania, Rautskis (1970a,b) found R. illense during April-May only in both E. lucius and P.,puviatilis, but Wierzbicki (1970) at Lake Dargin, Poland, found the adult parasites in P. fluviatilis in the summer. Rhipidoco tyle septpapillata K rull , 1934 Krull (1934b) studied the life cycle of this species in the Potoniac River, near Alexandria, Virginia, U.S.A. The metacercariae were encysted in the muscles of Fundulus diaphanus diaphanus and Lepomis gibbosus; the latter species was also the definitive host. Krull (1934b) experimentally established infections of adult worms in L. gibbosus. Some fishes were infected during both summer and winter months. Temperature influenced not only the rate of growth but also the length of life of R . septpapillata in the definitive host. During warm weather (37.8"C and above) the worms matured i n 5-7 days and were eliminated soon after reaching maturity, whereas in the coldest weather (as low as 7.2"C) they matured in 10-12 days and remained in the fishes for 30 days while miracidia developed in the eggs (Krull, 1934b). 4. Family Bunodevidae Bunodera luciopercae (Miiller, 1776) B. luciopercae is probably one of the most intensively studied of the fish

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

24 1

trematodes, owing t o the widespread range of its principal definitive host, Perca fluviatilis, and its high levels of occurrence within that fish species. The following authors provided some seasonal data about B. luciopercae: Hausmann (1897), Sramek (1901), Pearse (1924), Ruszkowski (l926), Milicer (1938), Dubinina (1949), Dyk et a/. (1954), Koval‘ (1955a,b), Bogdanova (1958), lzyumova (1958, 1959a,b, 1960), Markova (1958), Vojtkova (1959), Malakhova (1961), Komarova, T. I. (1964), Rizvi (1968) Rautskis (1970a,b), Noble (1970), Chertkova (1971) and Shul’man et a/. (1974). These papers are not reviewed further here, although all provided evidence in support of the general pattern of annual cycle found for B. luciopercac. The localities of study and the fish species investigated are given in Table 3. The details of the annual pattern of occurrence of Bunodera luciopercue were first given by Lyaiman (1940) from Lake Seliger, U.S.S.R. Essentially the same annual pattern was subsequently found by Komarova, M. S. (1941) in the River Dnepr, U.S.S.R., Androsova and Bauer (1947) in the River Yenisei, U.S.S.R., Lavrov (1955) in the River Volga, U.S.S.R.. Kozicka (1959) in Lake Druino, Poland, Malakhova (1963) in Lake Konche. U.S.S.R., Rizvi (1964) in Rostherne Mere, England, Mishra (1966) in the Shropshire Union Canal, Cheshire, England, Tedla and Fernando (1969) in Lake Ontario, Canada, Wierzbicki (1970) in Lake Dargin, Poland, Tell (1971) in Lake Vortsjarv, U.S.S.R., Cannon (1971, 1972, 1973) in Lake Opeongo, Canada, Halvorsen (1972) in the River Glomma, Norway, Wootten (1973b) in Hanningfield Reservoir, England, Campbell ( I 974) in Loch Leven, Scotland, Skorping (1976) in a lake near Oslo, Norway, and Andrews (1977) in Llyn Tegid, Wales. In order t o follow maturation of the trematode through the seasons, the majority of these authors have recognized a number of stages of sexual development. Details of these are given in Section VlIl D, but Fig. 5 shows the six stages recognized by Malakhova (1963). The pattern of annual occurrence usually involved a period during the summer months when B. luciopercae were absent from the definitive host. This period can be seen from Fig. 6 which shows the incidence of young and gravid B. luciopercae in fishes from 16 habitats. The months in which the trematodes were most frequently absent from the fish host were June and July, but in some habitats, e.g. Llyn Tegid (Andrews, 1977), Loch L.even (Campbell, 1974), Rostherne Mere (Rizvi, 1964), Hanningfield Reservoir (Wootten, 1973b) and the River Dnepr (Komarova, M. S., 1941) B. luciopercae was found in fishes during all months, although with a greatly reduced incidence during summer. The exact timing of the period of absence can vary from year to year (see Cannon, 1972) related to water temperature for each particular year. The uptake by the definitive host of inetacercariae of B. luciopercae from cladoceran, copepodan and ostracodan second intermediate hosts (see WiSniewski, 1958b) commenced from June in the River Dnepr (Komarova, M. S., 1941), late June in Lake Opeongo (Cannon, 1971, 1972) and Lake Vbrtsjarv (Tell, 1971), July in Loch Leven (Campbell, 1974), the Shropshire Union Canal (Mishra, 1966), Rostherne Mere (Rizvi, 1964), Lake Dargin

243

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

(Wierzbicki, 1970), Hanningfield Reservoir (Wootten, 1973b), August in Lake Seliger (Lyaiman, 1940), Lake Druino (Kozicka, 1959), a lake near Oslo (Skorping, 1976) and the River Yenisei (Androsova and Bauer, 1947) and not until September in the River Glomma (Halvorsen, 1972) and Lake Konche (Malakhova, 1963). However, by contrast to the above, at Llyn Tegid, juvenile trematodes recently excysted from metacercariae were found throughout the year, although most commonly from July onwards (Andrews, 1977). Habitat Lake Opeongo, Canada Lake Seliger, U S S R Lake Ontario, Conada Lake VGrtsprv, U S S R L l y n Tegid , Wales Loch Leven, Scotland River Glornma, Norway Lake Druzno, Poland Shropshire Union Canal, England Rostherne Mere, England Lake,Oslo, Norway

Juvenile

1-

Gravid

-

Lake Dargin, Poland ~

Honningfield Reservoir, England River Dnepr, U S S R River Yenisei, U S S R Lake Konche,

U SSR

FIG.6 . The occurrence of juvenile and gravid Bunoderu hrciopevcue in fishes during May to October in 16 habitats in four climate zones. See text p. 241 for full explanation.

Cannon (1971) found the juvenile B. luciopevcae in the gall bladder of Perca flavescetzs in late June, although they subsequently migrated to the intestine. In Llyn Tegid, Andrews (1977) searched for B. luciopercae in the gall bladders of Percafluviati/is but only found the trematodes in this organ in one heavily infected fish.

244

J A M E S C. CHUBB

The juvenile B. luciopercae matured during autumn and winter t o produce the first eggs by November in Lake Seliger (Lyaiman, 1940), by December in Lake Opeongo (Cannon, 197 l), at Hanningfield Reservoir (Wootten, 1973b) and in Loch Leven (Campbell, 1974), by January in the River Dnepr (Komarova, M. S., 1941), by February in Lake Konche (Malakhova, 1963), in Rostherne Mere (Rizvi, 1964) and in Llyn Tegid (Andrews, 1977) but not until March in the Shropshire Union Canal (Mishra, 1966). The majority of eggs accumulated during March and April in most habitats, although a little later in Lake Konche (Malakhova, 1963). Egg release by B. luciopercae was shown by Cannon (1972) to occur over a short period when the water temperature rose to 20°C. He considered that the retention of eggs until gravid adults were dropped from the fishes as lakes warmed up ensured release of miracidia over a short period. It appeared to be an adaptation to a short summer season. Most authors reported gravid adults from March/April onward until the trematodes disappeared from the intestines of the definitive host later in the summer. Lavrov (1955) found sexually mature B. luciopercae in Lucioperca lucioperca in the River Volga at the end of June, and Bauer (1959a) attributed this delay of development in rivers to their more severe hydrothermal conditions. However, it is likely that the final disappearance of gravid B. luciopercae from fishes during the summer is related t o the water temperature rising to about 20°C. The maturation of the adult B. luciopercae described above takes I year. Andrews (1977), as a result of some experimental studies, has postulated that an extended period of vernalization is necessary for normal development and maturation of B. luciopercae. The life cycle of B. luciopercae has been studied by WiSniewski (1958b), Frolova (l958), Moravec (19691, Cannon (1971) and Andrews (1977). A 2-year life cycle was postulated by Malakhova (1963), 1 year in the molluscan host and 1 year in the definitive host, and the studies of Moravec (1969), Cannon (1971) and Andrews (1977) confirmed this. As the Pisidium species may live for only 1 year, Cannon (1972) has emphasized that the molluscs must be infected when young. The incidence and intensity of infection of the fish hosts reported by the various workers rose during late summer and autumn, remained high over the winter and fell sharply when the gravid worms were lost in spring and early summer. The incidences for Lucioperca Zucioperca in Lake Seliger, U.S.S.R., were: June and July, 0, August 32%, September 88%, October 88 %, November through February 100 %, March 64 %, April 48 % and May 8 % (Lyaiman, 1940). Andrews (1977) has emphasized the dynamic nature of the relationship between invasion of the host by B. luciopercrre metacercariae, the population of trematodes in the intestine and the loss of worms from the fishes. His observations at Llyn Tegid suggested the following patterns of gain and loss of B. luciopercae from adult Percajuviatilis. During July the incidence and intensity of infection rose after a seasonal minimum, as a result of acquisition of juvenile wornis from infected zooplankton. At this time there may have been little loss of juveniles. As a result of extensive plankton feeding by P.fluviati1i.s both incidence and intensity of infection was

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

245

high in August and September. During this period both gain and loss were relatively high and resulted in a constant intensity of infection. In October. owing to a decrease in plankton feeding, gain fell but loss continued. to produce a marked fall in intensity. Between November and February gain and loss continued at a reduced level and maintained a fairly constant winter population. The loss increased during April to July as a result of the passing of the gravid worms. During these months incidence and intensity fell as a result of a very low gain of juvenile B. Iuciopercae (Andrews, 1977). The variations in gain reported by Andrews (1977) were attributed to seasonal changes in feeding of the Perca fluviatilis on zooplankton containing metacercariae, the loss in August and September to some density-dependent process, and that of the spring to the passing of the adult worms. This latter phase was probably affected by temperature (see Cannon, 1972). It is clear that water temperature is a major factor in the processes of establishment. maturation and release of gravid worms from the fish hosts. It is also highly probable that the variations reported in different habitats, geographic regions and from year to year reflect the importance of temperature for synchronized development and life processes of the parasite and its molluscan, crustacean and fish hosts. Wierzbicki (1971), Cannon (1972) and Andrews (1977) did not find any change in incidence of Bunodera luciopercae with depth of capture of the fish host. Bwiodera sacculata Van Cleave and Mueller, 1932 Cannon (1971, 1972, 1973) has studied the seasonal occurrence of B. saccuhta in Perca flavescens at Lake Opeongo, Ontario, Canada. He also investigated the life cycle, which probably required 2 years for completion (Cannon, 1971). A clear seasonality was seen in 1967, but less so in 1968. It was deduced that the infective metacercariae were most abundant in July and August, and P . ,flavesceiis fed more extensively on the crustaceans a t that time. Maturation of B. sacculata occurred within 3 weeks of establishment In the fish. Gravid worms were passed when the water temperature rose in the summer. Cannon (1971) demonstrated experimentally that B. sacculata left or were expelled from the fishes after I1 t o 20 days at 25°C. Thus seasonal fluctuations in Lake Opeongo could be explained in terms of response of the worms t o increased temperature, and the clear seasonality i n the summer of I967 was caused by the more rapid rise in water temperature of that year compared with the slower rise in 1968. Incidence during the year from 1967 to 1968 was minimal in July (about 473, rising t o about 48% in November. Ice covered the lake from midNovember to mid-April, and no results were obtained from December to February. In March incidence was still about 48 %, and it fluctuated between 34 and 50% through April to June. Incidence decreased in the summer of 1968 but as the lake temperature rose more slowly, B. sacculata did not almost disappear as it had done in the summer of 1967. Crepidostomum cooperi Hopkins, 1931 The nietacercariae of C. cooperi were collected by Hopkins (1934) from Hesageilia nymphs in Illinois, U.S.A. The lowest incidence was of 61 % in 1

246

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

July/August 1931 and the highest, 95% in July 1932. During the winter months the incidence was between 61 and 95 %. Noble, R. L. (1970) studied PercaJlavescens in Lake Oneida, New York, U.S.A., from April through November, but no seasonal trends in occurrence of C. cooperi were apparent. However, Cannon (1972) did find seasonal trends in Lake Opeongo, Ontario, Canada. The maximum incidence was in midsummer of both 1967 and 1968. He showed by experiment that C. cooperi was the least temperature-sensitive of the species he examined ( B . luciopercae, B. sacculata and C. cooperi). The trematodes matured within 3 weeks of invading the host. Maximum invasion was deduced to be June to August, but insects showed a steady increase in importance in the diet of P. flnvescens from spring to summer (Cannon, 1973). No mortality of C. cooperi was seen in relation to increased summer water temperatures, but a loss of worms occurred in autumn and early winter. McDaniel and Bailey (1974) reported on the occurrence of C. cooperi in Lepomis cyanellus and L. megalotis in the Little River, Oklahoma, U.S.A. In this habitat incidence was about 44% in January, 90% in February, 26% in March, falling to a minimum of about 6 % in July, to ascend again to around 26 % by September. The trematodes overwintered as adults, matured and passed eggs in the spring after which they disappeared. The next generation of adults appeared in the autumn. McDaniel and Bailey (1974) speculated that a state of equilibrium between seasonal recruitment and degeneration of established infections was soon reached because incidence did not increase greatly with time. It is noteworthy that the observations of Cannon (1972) and McDaniel and Bailey (1974) on C. cooperi appear contradictory; summer incidence was highest in Lake Opeongo, but lowest in Little River. Temperature may be involved in this apparent disparity. In Little River, summer water temperatures may be sufficiently high to cause significant loss of worms. Crepidostomum cornutum (Osborn, 1903) Cloutman (1975) tabulated data for the seasonal occurrence of C. cornutum in Lepomis gulosus, L. macrochirus and Micropterus salmoides from Lake Fort Smith, Arkansas, U.S.A. The information expressed as average number per fish showed that the trematode was present in fishes all year. Maximal numbers were in August (32.7), January (10.4), March (10.8), April (15.7) and May (9.7). Crepidostomum farionis (Muller, 1780) Awachie (1963, 1968) studied the seasonal dynamics of C. .farionis in Salmo trutta in a small stream, the Afon Terrig, Wales. The mollusc intermediate host was Pisidium casertanum and the metacercariae were encysted in Gammarus pulex. Incidence rose from August to a peak in December (14.3%), and remained high through the winter until May. No C. farionis were found in the fishes during June and July. Maturation occurred during the winter, most worms contained eggs by February and egg release was during the spring. The incidence was related to temperature. Awachie (1963, 1968) found that establishment of the juvenile worms took place when the water temperature fell to below 10°C in late autumn, and in May or June a rapid rise in water temperature to 11°C coincided with a steep fall in

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incidence and intensity of infection of S. trutta. Awachie (1968) suggested that C. farionis was unable to establish in fishes at temperatures above 10°C. Other seasonal records of C. farionis from the British Isles are Brown (1927) from Salmo trutta and Thymallus thymallus in the Rivers Wharfe and Yore, Yorkshire, England, Chubb (1961) from T. thymallus in Llyn Tegid, Wales, and Robertson (1953) from S. trutta in Dunalastair Reservoir, Scotland. Brown (1927) found the rediae in Pisidium amnicum and Sphaerium corneum, and the cercariae were released in abundance from April through to June, and in gradually decreasing numbers until October. Brown (1927) obtained S. trutta only during April to September, and T. thymallus in November, and his mention of worms from the pyloric caeca suggests that he had mixed infections of C. farionis and C. metoecus. The pattern of incidence and maturation observed by Robertson (1953) closely agreed with that seen by Awachie (1963), with maximum infections during the cold months. Thomas (1958a, 1964) also reported maximum infections of S. salar parr and S. trutta during the winter months at the River Teify, Wales. However, his data do not separate C. farionis from C. metoecus. Dyk (1957, 1958) and Dyk et al. (1954) reported the seasonal dynamics of C. farionis from some lakes in the High Tatra Mountains, Czechoslovakia. These lakes were covered with ice for between 54 to 7 months of the year, and the waters warmed slowly so that the incidence of C. farionis in Salmo trutta and Salvelinus fontinalis was high even during the summer months, June to August, to fall in September in some lakes (Strbsky) to zero. The maturation stages reported by Dyk (1958) showed that mature worms with eggs were present in July, but that juveniles appeared from August. The importance of water temperature was shown by the absence of C. farionis from fishes in September in Strbsky Lake after a long, warm summer. Voth et al. (1974) found a maximum incidence of C. farionis in Salmo trutta in the South Platte River, Colorado, U.S.A., during the winter months. However, they attributed the low summer incidences to the effect of increased water flow from the Roberts’ Tunnel, as the annual pattern of incidence of the trematode was inversely proportional to the volume of water flow. They did not consider the possibility of the seasonal cycle of incidence being related to the biological requirements of C. farionis. Crepidostomum ictaluri (Surber, 1928) Spa11 and Summerfelt (1969) found C. ictaluri in Zctalurus punctatus from Lake Carl Blackwell, Oklahoma, U.S.A., with no apparent variation between seasons. Crepidostomum isostomum Hopkins, 1931 Elkins and Corkum (1976) reported the seasonal dynamics of C. isostomum from Aphredoderus sayanus from Whisky Bay, Louisiana, U.S.A. A periodicity of incidence, intensity and maturation of infection was found. Incidence was almost 100% April to July, to fall from August (85%) to December (38 %). In January it was 80 % and in February 0 %, but small samples made these data unreliable. Intensity followed incidence, being maximal (mean about 25 per infected fish) during April and May, to fall to about 5 in June and July and decline gradually from then to January (2.5). The maturation

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was assessed by four phases. Phase A, March to July, had slight genital development with testes not clearly defined and the ovarian complex undifferentiated. Phase B, March to November, had functional testes. but no vitelline products or eggs. Phase C, April to January, had functional male and female genitalia with five or fewer eggs, which were not released in saline. Phase D, September to May, had more than five eggs, which were shed when the worms were placed in saline. Thus the annual cycle was invasion of fishes in March to July, maximum April-May, with all worms gravid from November to January. Crepidostomum metoecus (Braun, 1900) The most comprehensive seasonal study is that of Awachie (1963, 1968) in Salmo trutta from the Afon Terrig, Wales. The mollusc intermediate host was Lymnaea peregra and the metacercariae occurred in Gammarus pules. The incidence of C. metoecus in S. trutta was minimal in September (4.8%), rose through October and November to reach 90.5% in December, and remained about that level through the cold months until April. to fall progressively through May (82.6 %), June (68.2 %), July (45.5 %) and August (14.4%) to the minimal level in September. Intensity of infection was high during the autumn months (mean of 40 per infected fish in November), level (about 30) during the winter months, to fall from spring onwards (May, 24) to a minimum during the summer (August, 3). The maturation was studied. The autumn was the period of recruitment and initial genital development. By December a few worms had produced eggs, but by February most contained eggs. Eggs were released during spring, so that by June remaining worms had fewer eggs. Summer adult worms were dying. with disintegration of internal organs. Awachie (1963) concluded that the infection of S. trutta commenced when the water temperature fell below 10°C. A rapid rise in water temperature to 11.2"C in May/June coincided with the sharp fall in incidence and intensity of infection by the gravid worms. The dynamics of all stages of the life cycle were assessed by Awachie ( 1963). Two generations of rediae were seen in Lymnaea peregra, with cercarial liberation commencing in June, maximal i l i July to October. Recently established metacercariae were seen in G. pulex as follows ( % incidence): June, 7.75; July, 21; August, 70.75; September, 57.75; October, 20; November. 14; December, 2%. The swarming of the cercariae corresponded to the peak incidence of young G. pulex. The overall occurrence of metacercariae in G. pulex (Awachie, 1968) showed a well-defined seasonal periodicity. Incidence and intensity rose from July, and remained high until January. to fall thereafter. The peak occurrence of metacercariae in G. pules (AugustOctober) Corresponded to the lowest occurrence of worms in S. trutta. Although large numbers of metacercariae were present in G. pule.\- from July onwards, newly established juvenile worms did not occur in S. t r u t t n until water temperatures were less than 10°C. Awachie (1968) considered that the environmental temperature was the main factor synchronizing the life cycle of C. metoecus (also C. ,furionis, see above) with that of its three host species. It determined the time of estab-

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lishment of worms in the fish host, and thereafter it determined the time of development in the other hosts. Most other workers in the British lsles have found an essentially similar pattern t o that reported by Awachie (1968), for instance: Aderounmu (personal communication) in Salmo trutta at Chirk Fish Hatchery, Llyn Celyn and Llyn Tegid, Wales: Bwathondi (1976) in S. trutta at Loch Strathbeg, Scotland; Chubb (1961) in Tliymallus tl~prnallusat Llyn Tegid, Wales; Davies, E. H. (1967) in T. thyrnallus at the River Lugg, Herefordshire, England; and Thomas (1958a) in S. trutta in some Welsh rivers As noted under C. fbrionis, Thomas (1958a) presented combined data for C. ,briouis and C. inetoecus. However, Campbell (1974) in S. trutta at Loch Leven, Scotland, did not find clear periodicity because C. i?ietoecus occurred infrequently in the loch. It usually occurred in young fishes from the tributary streams. Also John (1973) was reported (see Britain, 1971) as finding S. trutta in Dowles Brook, Worcestershire, England, that had become infected in June after intensive feeding on emerging mayflies. 5. Fainily Crypt ogoti itnidae Acrtodpxtra arniuri (Stafford, 1900) Over 2000 of these trematodes were recovered from the ovary of a single host individual, and almost every female fish, Ictalurus punctatus, was infected (Perkins. 1950, 1951, 1956). Eggs accumulated in the worms’ uterus and these were not discharged until the gravid worms were expelled with the host eggs during spawning. The gravid A . aniiuri then ruptured explosively to release the eggs (Perkins, 1956). Very young worms predominated among parasites seen in the ovaries o f the fishes after spawning; however, there were also many that contained eggs. The fate of these gravid worms was not determined, but encapsulated parasite egg masses suggested that gravid worms not expelled when the fishes spawned died and degenerated (Perkins, 1956). It is assumed that A . ainiuri was present in the fishes all year. Perkins (1956) was unable to determine the details of the life cycle.

6. Family Fellodistomidae Orieiitophorus breviclirus Srivastava, 1935 Srivastava (1935b) studied this species in HilAa ilisl7a in the Allahabad region of Northern India. During the winter months nearly every fish was infected by 10 to 80 trematodes. As summer approached, however. the occurrence declined to reach an incidence of below 10~(1in mid-summer. Pal (1963) examined H . ilisha from the Nabadwip to Kakdwip region of the River Hooghly, India, over an I8 month period. Orietitopliorus h r r i ~ i c ~ l ~ r u s was rarely seen during the monsoon months (July and August), but 12-67):; incidences were found during November to January. with 1 0 0 ~incidences o during February and March. The coolest and driest time of the year in this area is November to February, the period of peak occurrence of the parasite.

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7. Family Gorgoderidae

Phyllodistomurn angulaturn Linstow, 1907 Dubinina (1949) found P. angulaturn i n Lucioperca luciopevca from the Volga Delta, U.S.S.R. in spring (13-3%), but not during summer and winter. Contrary to this, Izyumova (1958, 1959b) found a more or less constant incidence (92-96 %) in L. lucioperca in all seasons. Phyllodistomum conostomun~(Olsson, 1876) The parasite fauna of Coregonus lavaretus baeri natio ladogae was studied in Lake Ladoga, U.S.S.R., from July to November by Bauer and Nikol'skaya (1957). Phyllodistomum conostomurn was found in August (33 %), October (13 %) and November (27 %). Phyllodistomum elongaturn Nybelin, 1926 This species has been reported from fishes during all seasons of the year. It was found in Abramis brama in the Volga Delta, U.S.S.R., in spring (47.6% and 60%), summer (100%) and winter (21.4%) (Dubinina, 1949). Izyumova (1958) reported a lower but consistent incidence in A . brama at the Rybinsk Reservoir, U.S.S.R., January-April 6.6 %, May-August 4.9 % and October-November 6.6 %. A higher but also relatively constant incidence was found by Vojtkova (1959) in the River Svratka, Czechoslovakia, May incidence 38 %, intensity 1-4, July 33 %, 3, August 33 %, 1-4 and October 40%, 1-6. A more detailed analyis of seasonal occurrence in relation to age class of A. brama was provided by Titova (1957) from Lake Ubinsk, Siberia, U.S.S.R. The incidence in summer, autumn and winter increased with age through the age classes of fishes, for example in the autumn samples percentage incidences were: 3 + fishes 52.5, 4 + 60, 5 + 77 and 7 + and 8 + 85.2. The overall incidences for all A . bramae were summer 50.6%, autumn 58.8 % and winter 40.8 %. Sporadic incidences of Phyllodistomum elongaturn through the seasons have been noted by other authors. Bogdanova (1958) found a 6.6% incidence in A . brama in the River Volga, U.S.S.R. in July/August, but the trematode was not seen in February/March or May. Izyumova (1959a), at the Rybinsk Reservoir, U.S.S.R., found P. elongaturn in the winter (1.6%) and summer (3.8%), but not in spring and autumn. At the same locality, Izyumova (1960) found incidences in Abramis ballerus in the autumn (5.8%) and in Blicca bjoerkna in summer (3.579, but not in either host at other seasons. In the Dnepr Delta, U.S.S.R., Komarova, T. I. (1964) noted P. elongaturn in four species of fishes examined from February to October: in A. brama July/August only (7.1 %), in B. bjoerkna April only (13.2%), in Rutilus rutilus heckeli May, July/August and October (all 6.6% incidences) and in Vimba virnba vimba natio carinata in June/July only (13.2%). At the Dubossary Reservoir, Moldavia, U.S.S.R., Marits and Vladimirov (1969) found low incidences in V. v. vimba natio carinata in summer (8.5%) and autumn (2.5 %)>,but not in spring. Phyllodistomurn folium (Olfers, 1816) Chappell (1969) studied P. folium in Gasterosteus aculeatus at a pond on Baildon Moor, Yorkshire, England. Samples were collected at 2-monthly

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25 1

intervals and during the period of investigation, September 1966 to August 1967, both the incidence and intensity of infection increased slightly. A seasonal pattern with regard t o size and degree of maturity of the trematodes was seen. The smallest were found in August when the fish population was composed of mostly newly hatched fishes, but an increasing percentage of P. folium contained over 300 eggs in the uterus from September (0 %) through to May/June (61 %), to fall by August to 17%. Chappell (1969) considered that invasions of the fishes took place throughout the entire year as incidence and intensity of infection increased over the period of investigation. Two routes of invasion were postulated, either by the ingestion of the mollusc hosts containing metacercariae during the winter [Anodonta sp. (Bykhovskaya-Pavlovskaya et al., 1962) or Dressenia polymorpha (Sinitzin, 1901)], or by metacercariae encysted in insect larvae eaten by the fishes during the spring, summer or autumn. Chappell(1969) found that cercariae were released from Sphaerium sp. in the laboratory only between spring and autumn. Tell (1971) at Lake VGrtsjarv, Estonia, U.S.S.R., found a similar pattern of incidence and intensity in Esox lucius and Percajuviarilis. In this locality the P. folium were of maximum size and gravid at the end of April and the beginning of May, with a high incidence and intensity of infection. By the end of May and the beginning of June the trematodes were absent from the fishes, but by the end of June to early July reinvasion occurred with a low incidence and intensity of small immature parasites. Thereafter there was a gradual increase in the size of the worm population to the following spring. An apparently active reproductive cycle throughout the year was seen by Chappell (1969). He postulated that the duration of the lower winter temperatures was more important in this context than the absolute minimum temperature, in which case the specific geographical locality from which the fishes were sampled might be of extreme importance in an examination of the seasonal variations of fish parasite fauna. Johnston, J. M. (1967) investigated the number of eggs released every 24 h over 14-day periods at various temperatures by Phyllodistomum .folium inhabiting the urinary system of Gasterosteus aculeatus. She found that the ovarian activity was a rhythmic process of alternating production and rest. The length of the rest period was progressively reduced with trematode age. In any 14-day period there were at least two resting sequences. In a population of the trematodes each individual retained its own production rate so that even where small numbers of P. folium were involved eggs were continuously released from the host. The egg production rhythms were not directly affected by crowding, long association nor the hormonal condition of the host. However, summer egg-laying rates were in excess of those of the winter months. Other authors have also provided seasonal data for Phyllodistomum folium. Bogdanova (1958) found incidences of 19.8 % in Abramis brama in the River Volga, U.S.S.R., in May and July/August, but not at all in February/March. However, in Esos lucius it occurred in February/March (6.6%) but not in May or August. Izyumova (1960) at the Rybinsk Reservoir, U.S.S.R., observed an incidence of 13.3% in E. lucius in summer only. Komarova, T. I. (1964) at the Dnepr Delta, U.S.S.R., found P. folium in E. Iucius in

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February only (6.6 :h) and in Pelecus cultratus in July/August only (6.62,). In A . brama at the Kuybyshev Reservoir, U.S.S.R., Lyubarskaya (1970) noted incidences in A . brama in spring (5.1 7;) and autumn (9.5%), but not in winter or summer. Markova (1958) at the River Oka, U.S.S.R.. saw the trematode in E. lucius all year around. but Rautskis (1970b) did not find it in this fish species at Lake Dusia, Lithuania, in January-March. but it was present in April-May (37.5 ",;,), June-July (33.3 7")and October-November (6.6:4). Davies, E. H. (1967) at the River Lugg, Herefordshire, England, found P.,folium in E. lucius in June (75%) and July (14%), but not otherwise. and in Thymallus thymallus in July (0.576) only. These sporadic incidences over the year are an indication of low levels of infection of the host fishes in particular habitats and d o not contradict the observations of Chappell(1969), Markova (1958) o r Tell (l97l), which indicate an annual cycle for P.,foliuni. Phyllotiistornuni lacustri (Loewen, 1929) Sexually mature worms of this species were found in Ictaluvus punctntus at Lake Carl Blackwell, Oklahoma. U.S.A., throughout the period June 1967 to September 1968 by Spall and Summerfelt (1969). lmmature P. lacustri were seen in February to May 1968 and June 1967. There was no significant difference in infection rate with season. except that higher values in spring were concurrent with the period when immature worms were present in greatest numbers. Phyllodistomunz pearsei Holl, 1929 Holl (1932) found P. yearsei in Eiineachanthus gloriosus in an artificial lake at Lakeview, North Carolina, U.S.A., in February, March, July, November and December. However, detailed investigation of seasonal occurrence has recently been provided by Elkins and Corkum (1976) from Aphredoderzcs sayanus from Whisky Bay, Louisiana, U.S.A. In summary, there was no seasonal periodicity of incidence or intensity o f infection at this habitat; however, a marked maturation cycle was apparent. Six maturation stages were separated: Phase A, no genital development, seen March to July; Phase B, paired vitellaria and rudimentary testes visible, seen June to August; Phase C, fully differentiated male and female genitalia, but n o eggs in uterus, seen June to August; Phase D, tanned eggs in uterus, but none in region anterior to ventral sucker, seen JUIYt o November; Phase E, eggs filled uterus in hind body also anterior to ventral sucker, worms shedding eggs, seen September to November; and Phase F, with regression of testes, seen October t o June. The annual maturation pattern was: March, immature worms appeared; April-May, all worms phases A and B ; June t o August, worms began t o mature, phases C to F; September to January, all mature, phases C t o F. Elkins and Corkum (1976) noted the interesting fact that immature and mature trematodes were never collected from the same host. Thus in Phyllodistom~cni pearsei the population was stable through the year, recruitment occurred only in the spring (March t o May), maturation in the summer (from June through August) and the worms were gravid from September to January. Phyllodistomum psrudqfoliuti I N y be I i n 1926 Izyumova (1959a) found this species in G~~mnocephalusceriiua at the

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253

Rybinsk Reservoir, U.S.S.R., during all seasons of the year: winter, incidence 15.5% intensity 2-16, spring 16.7%,, 1-2, summer 28.6%, 1-3 and autumn 13.3 1-6. Phyllodistomtim simile Nybelin. 1926 This species was reported by Thomas (1958b. 1964) i n Salriio tl'uttir from the River Teify, Wales. It was found throughout the year and there were no significant seasonal changes in either incidence or intensity of infection. Pliyllodistomum staforrli Pearse, 1 924 Holl (1932) found this trematode (as P. c~aroliiii,a synonym of P . stqflbrtli) at the Ern0 River and a nearby settling basin, North Carolina, U.S.A.. in Ictnlurus rzatalis. At these localities it was present in October and November. but not from May to September. However, in a lake near Gibsonville, North Carolina, Holl (1932) found that it occurred in March but not in November and December. Pliyllodistomiini sp. Pigulevskii { 1953) suggested that the representatives of the genus Piijsllodistomum had a 1 year cycle from egg to death. The time spent in the fish was more than half that required for the complete cycle and it occurred i n the cold part of the year, autumn through winter to spring. However, in most species for which seasonal data are reviewed (see above), it seems probable that the life cycle could take up to 2 years, 1 year for development in the intermediate hosts and 1 year in the fish host. Banina and lsakov (1972) noted occurrence of Phyllodistoniuu~ sp. in Gastrrosteiis aculeatus and Purigitius yuiigitius from the River Neva Delta, U.S.S.R., in FebruaryjMarch, April, June and September.

x,

8. Family Halipegidae Buiiocotyle ciiigulata Odhner, 1928 Dubinina (1949) observed this trematode i n Silurus glanis from the Volga Delta, U.S.S.R., 1940 summer. 6.7 9', incidence, 1941 winter, 0";. spring, 53.3 ",. 9. Family Hen1 iuviclae Aplinnurus rnotiolecitlius (Srivastava, 1941)

Reported from Hilsa ilisha in the marine (66.6",/,), gradient ( 5 6 " , ) and freshwater zones (10% incidence) of the River Hooghly, Lndia. by Pal (1963). Infection occurred in the marine zone, but the seasonal fluctuations were more or less common to all zones of the river. Pal (1963) observed peak incidence (100 %) during September. and the other months with heavy incidences were November (1971, SO%, 1972. 66"/,) to March (3473 (winter). The trematode was not found during July and August, the monsoon period. 10. Family Lecithasteridae

Lecithaster extralobus Srivastava, 1935 The remarks reported below (Srivastava, 193%) probably applied to both L. extralobus and L. indicus.

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JAMES C. CHUBB

Lecithaster indicus Srivastava, 1935 Srivastava (1935a) described L. extralobus and L. indicus from Hilsa ilisha in the Allahabad region of India. The fish species occurred in large numbers in local rivers for about 8 months of the year, became rare toward the end of summer and almost totally disappeared during the rainy season. Srivastava observed that the rate of incidence of L. indicus in winter was nearly loo%, with 8-20 worms per host. In summer, however, the worms had gone. 11. Family Lissorchiidae Lissorchis fairporti Magath, 1918 L. fairporti was studied in Zctiobus bubalus and I. cyprinellus at the Fairport Biological Station, Iowa, U.S.A., by Magath (1918). In infected fishes it was noted that as summer advanced the average size of the trematodes increased and more eggs accumulated in the uterus of each worm. Eggs were expelled in great numbers towards the end of summer. Some other stages of the life cycle of Lissorchis fairporti were found by Magath (1918). Sporocysts were seen in larger numbers in HeZisoma trivolvis in early summer rather than later. Magath (1918) concluded from observations and experiment that the miracidia hatched out from eggs laid by the adult fluke in late summer and penetrated the mollusc, to develop in it during winter and spring. The following early summer xiphidiocercariae left the snails, infected chironomids to form metacercariae, to be eaten by the fishes during the later part of the summer. Magath (1918) speculated that it was barely possible that some of the first metacercariae to infect fishes might mature before autumn, but considered it more likely that the young trematodes overwintered in the fishes to mature the following summer. However, Cort er al. (1950) reviewed the evidence presented by Magath (1918) about the life cycle of L. fairporti and were forced to conclude that he was mistaken and that the xiphidiocercariae from H. trivolvis were of another species of trematode. 12. Family Monorchiidae Asymphylodora demeli Markowski, 1935 The seasonal occurrence of A . demeli was reported by Komarova, T. I. (1964) from Rutilus rutilus heckeli in the Dnepr Delta, U.S.S.R. Samples were taken from February to October. The incidence was fairly uniform throughout, except for March: February 20%, March OX, April, May, June, July/ August all 26.6 %, October 13.2 %. Intensity of infection showed no pattern but was maximal in April, 6-90, and minimal in October, 2-3. Asymphylodora imitans (Muhling, 1898) Several authors have studied A . imitans, which was present in fishes throughout the year, except possibly winter. Dubinina (1949) found it in Abramis brama at the Volga Delta, U.S.S.R., in spring (1940, 58.8 %; 1941, 66.7 %) and summer (25 but not in winter. In the same host, A . brama, Marits and Tomnatik (1971) at Dubossary Reservoir, Moldavia, U.S.S.R., observed it in spring (6 %), summer (41 %) but not autumn. Komarova, T. I.

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(1964), at the Dnepr Delta, U.S.S.R., noted it in A . brama from March to October, but not in February. She also found it in Blicca bjoerkna, Pelecus cultratus, Rutilus rutilus heckeli and Vimba vimba vimba natio carinata. Peak incidence in most species tended t o be early summer: A . brama, April and June, 26.6%; B. bjoerkna, June 68.7%; R. rutilus heckeli, May 46.6%; and V. vimba vimba natio carinata, April/May 98 %. It was found in at least one fish species during all months investigated, February to October. Peak intensity of occurrence also tended to be early summer. lzyumova (1960) investigated B. bjoerkna at the Rybinsk Reservoir, U.S.S.R., but found a low incidence (3.5%) in summer only, whereas Marits and Vladimirov (1969) saw A. imitans in spring (15.9%), summer (25%) and autumn (10.2%) in V. vimba vimba natio carinafa at Dubossary Reservoir, Moldavia, U.S.S.R. Asymphylodora kubanicum (Issaitschkoff, 1923) Mishra (1966) studied A. kubanicum in Rutilus rutilus through the year at the Shropshire Union Canal, Cheshire, England. N o worms were seen January, but they were found in all other months. The incidence rose from February 6 % , March 9% , April 17%, May 44%, June 45% to a peak in July (62%). It varied thereafter, August 39%, September 33%, October 41 %, November 22 % and December, 23 %. Intensity was low from February to April (maximum 2), high in May, June and July (maximum 165, 22 and 102 respectively) and varied thereafter, August 5, September 17, October 18, November 2 and December 15. Mishra (1966) found that the worms were juvenile in August and September, genitalia developed through the winter, but eggs were seen only in May, June and July (in 45%, 80% and 100% respectively). Accordingly, an annual cycle of development was postulated. Evans, N. A. (1977b, 1978) investigated A. kubanicum in Rutilus rutilus from the Worcester-Birmingham Canal, England. He found a marked cycle of occurrence and maturation. Low incidences and intensities in winter preceded a dramatic increase in infection during spring and summer. The worms matured rapidly during spring and summer and laid their eggs and died in late summer and early autumn (Evans, N. A., 1978). The observations from other localities and host fishes tend to conform to the pattern found by Evans, N. A. (1978) and Mishra (1966). In particular, Komarova, T. I. (1964) studied A. kubanicum in Abramis brama, Blicca bjoerkna, Rutilus rutilus heckeli and Vimba viniba vimba natio carinata in the Dnepr Delta, U.S.S.R. The trematode was found in all months from February to October, although not in every fish species in each instance. Peak incidences and intensities of occurrence were: A . brama incidence in May 40%, intensity in March 185; B. bjoerkna May 20%, June 30; R. rutilus heckeli April 40%, May 90; and V. vimba vimba natio carinata June/July 13.2%, April/May 19. Komarova, M. S. (1957) at the Donets River, U.S.S.R., located A. kubanicum in Tinca tinca in July only, usually A . tincae (see below) was found. At the Volga Delta, U.S.S.R., Dubinina (1949) found A. kubanicum in A . brama and Cyprinus carpi0 in spring only. Asymphylodora markewitschi Kulakovskaya, 1947 Kozicka (1959) was unable to ascertain the seasonal occurrence of A. markewitschi in Afburnus alburnus and Scardinius erythrophthalmus in Lake

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Maniry Polnocne, Poland. Mature individuals with eggs were seen in July, August and September. Asyrnphylodora tincae (Modeer, 1790) Details of the seasonal development of A . tincae in Tinca tinca were provided by Komarova, M. S. (1951b) from the middle reaches of the River Dnepr, U.S.S.R. The maximum life of the trematodes in the fish host was 1 year. Invasion of the fishes occurred during the end of autumn, through winter and spring, eggs were produced in summer, to be deposited during autumn, winter and spring after which the worms died. The incidence of fishes with sexually mature rather than immature A. tiricae was given by Komarova, M. S. (1951b) for two groups of 15 fishes for each of four months as follows: October, mature 46.6 and 33.3 %, immature 0 and 0 % ; January, mature 60 and SO%, immature, 33.3 and 2004; April, mature 80 and 93.3 %. immature 53.3 and 66.6 %; July, mature 100 and 100 %, immature 0 and 0 %. Accordingly, young immature trematodes occurred in January and April. but mature individuals were present all year, and at a maximum in July. In the River Donets, U.S.S.R., Komarova, M. S. (1957) found A. iincae in T. tiiwa to have the following incidences during a 2 year period: 1952, spring 80%;. summer loox, autumn 53.3% and winter 73.3%; 1953, spring 86.6%. summer 100 %, autumn 46.6 % and winter 80 ”/,. The pattern of incidence was similar during each year, Komarova, M. S. (1957) noted that during the winter A . titicae was hardly mobile and maturation was slowed down. Wierzbicka (1964, 1970) also found A. tincae in Tinca tinca in lakes in the Olsztyn region of Poland. Trematodes at all stages of maturity were found all the year round, and adult worms occurred in fry as early as October. Wierzbicka concluded that there was no clear seasonal cycle of development, but that in Poland climatic conditions allowed many successive development cycles. Youngest and gravid A . tincae occurred at all seasons, although there was an increase in juveniles, that is worms without eggs, during autumn to spring, perhaps because of lowered wzter temperatures. The occurrence of adults in fry in October was considered by Wierzbicka (1970) to be evidence of rapid maturation of A . tincae in the definitive host. Other authors, Hausmann (1897) in Switzerland, Kozicka (1959) in Poland, Lyubina (1970) in U.S.S.R., Ruszkowski (1926) in Poland and Yoshino (1940) in Japan have provided less complete data about seasonal occurrence of A . tincae; their findings fit the observed patterns of occurrence. Palaeorchis incognitus Szidat, 1943 According to Bauer (1959a), Kulakovskaya (1955) found this species of trematode in Rutilus rutilus in the upper Dneister Basin, U.S.S.R. Invasion of the fishes occurred in March, April and rarely May. The R. rutilus were free of infection from December to February. This pattern of seasonal occurrence was attributed by Bauer (1959a) to the southern origin of P. incognitus. Komarova, T. I. (1964) found P. incognitus in Blicca bjoerkria in February (6.673, May (20%) and June (6,2%) and in Rutilus rutilus heckeli in July/August (6.6 %) in the Dnepr Delta, U.S.S.R. Palaeorchis unicus Szidat, 1943 Komarova, T. I. (1964) reported P. unicus from Blicca bjoerktia in the

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Dnepr Delta, U.S.S.R., in March (6.6%), May (13.2%) and June (18.7%), but not in February, April or October. 13. Family Opecoelidae Nicolla gallica (Dollfus, 1941) Metacercariae were found in Gammarus pulex and G. pungens in France (Grizel and Vianey-Liaud, 1973) and G. pulex in the River Avon, Hampshire, England (Rumpus, 1975). At this latter locality the seasonal dynamics of N . gallica in Cottus gobio were studied. Rumpus (1975) observed that the incidence rose from about 45% in July t o almost 70% in August. declined then through September t o November (about 30%) and thereafter rose again from December to a peak in February of 100%. The incidence remained high in March and April, t o fall to around 20% in May and June. Intensity of infection closely followed the pattern for incidence. The highest period of recruitment of N . gallica was probably July through September, and the proportion of small trematodes was low from January t o May. The egg production of N . gallica occurred all year. The incidence of egg-producing worms was between 33 and 90% each month, except January when it was 0%. This latter level was attributed t o a sampling deficiency. Rumpus (1975) suggested that the low spring level of incidence and the summer (August) peak of N. gallica in Cottus gobio were related to the availability of metacercariae in G. pules, but that the peak in winter (February), which occurred when larval incidence was falling, was influenced by some other factor, possibly either increased feeding on G. pu1e.u or the presence of mature female fishes in the host population during the winter. Maturing and gravid C. gobio had a higher level of infection by N . gallica. Nicolla skrjabini (Iwanitzky, 1928) According t o Dollfus (1958), Crowcrocaec~mis a synonym of Nicolla. Almost all the authors quoted below referred to this species as Croiiwocaecu/?i sk rjabini. Komarova, M. S. (1951a) studied N . skrjabini in Gyn~tiocephalusaceriiia in the middle reaches of the River Dnepr? U.S.S.R. Incidence of infection was high throughout the year. In summer the percentage of fishes infected with mature trematodes was 944-100 %, and with immature individuals 20.8-42.1%. In the autumn the percentages were, mature 73.3%, and immature 33 %. During the winter, only mature N . skrjabini were found, some with fully developed genitalia but no eggs, and some with a few eggs. Komarova, M. S. (1951a) concluded that the trematodes that invaded the fishes in summer matured during summer, autumn and winter. In spring they laid their eggs and the larvae developed in the intermediate hosts and invaded fishes during the summer. Trematodes that invaded fishes in the autumn matured through autumn, winter and spring to deposit eggs and die during the summer. The larval development occurred in the summer to give invasion of fishes during autumn. Koval’ (1952, quoted from Bauer. 1959a) reported that fishes in the River Dnepr were invaded in March and early April, and that development of the trematode was completed after about

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2 months. Eggs were then accumulated in the uterus, with gradual oviposition. The fishes were free of infection in winter, from December to February. The data from Komarova, T. I. (1964) for the River Dnepr Delta, U.S.S.R., show zero incidence in Abramis brama and Pelecus cultratus for February, but there was an incidence of 6.6% in Esox lucius in February. In the four fishes examined, A . brama, E. lucius, Lucioperca lucioperca and P. cultratus, highest incidences were, respectively, April 20 %, March 40 %, April 26.6 % and April/May 27.7 %, followed by a decline in incidence thereafter through to October when incidence was 6.6 % in all four fish species. Results were not available for November to January. At the Dubossary Reservoir, Moldavia, U.S.S.R., Marits and Vladimirov (1969) found a low incidence (2%) of N . skrjabini in Vimba vimba vimba natio carinata in spring and summer, but none in the autumn. In Lake Balaton, Hungary, Molnar (1966) found an incidence of N . skrjabini i n Gymnocephahis cernuu during all months (no samples November, December, March or April). At this locality the highest incidences were in January (80 %), February (81.2 %) and May (80 %). Ponyi et a/. (1972) found increased incidences at the same habitat and in the same host compared with Molnir (1966); they were May 92.3 % (intensity 1-33), July 81.2 % (3-29), September 75 % (2-21) and October 100 % (2-51). A small June sample of fishes was uninfected. At Lake Balaton Molnar (1966) found that Lucioperca lucioperca fry were invaded from the end of May onwards. Sten’ko (1976a) found cercariae of N . skrjabini in the mollusc Lithoglyphus naticoides in Crimea, U.S.S.R. The incidence was 43.88% in summer and 28.57 % in the winter. Metacercariae were experimentaily obtained in Gammarus (Rivulogammarus) balcanicus, but natural hosts were Pontogammarus crassus and Dikerogammarus haemobaphes. The metacercariae were infective after 1 month in the gammarids. Carassius auratus gibelio were experimentally infected to give mature N . skrjabini in 1 to 2 weeks. Nicolla csisniewskii (Slusarski, 1958) Koval’ et a/. (1973) found N. wisnieki,skii (also N . skrjabini) in Salmo trutta and Thymallus thymallus in breeding ponds and reservoirs in the Transcarpathian area of the U.S.S.R. In July/August young and mature trematodes, the latter containing eggs, were seen. Sphaerostoma bramae (Miiller, 1776) S . bramae has been studied fairly extensively so that its seasonal dynamics are relatively clear. Malakhova (1961, 1963) established a well-defined seasonal pattern for it in Rutilus rutilus from Lake Konche, Karelia, U.S.S.R. Incidence was zero in July and August; from September (6.7 %) it rose through to February (66.6%) and remained about this level during March and April, to fall in May (43.3 %) and June (40 %) and disappear by July. Intensity followed a similar pattern; from September (range 1-5) it rose through to January (1-150), to remain high in April, peak in May (1-431), stay high in June (1-228) before the trematodes disappeared in July (Malakhova, 1961). Six stages of maturation were recognized by Malakhova (1963), Stage I juvenile, testes and ovary rudimentary, Stage I1 testes and ovary developed, vitellaria rudimentary, Stage 111 vitellaria functional,

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Stage IV genitalia functional, first eggs, Stage V eggs more numerous, and Stage VI gravid, with many eggs. Measurements of the genitalia were also made. The juvenile worms (Stage I) were found in September and October, and during these months were the only stage of development. Stage I worms were found until May. From January Stage I1 and 111 worms were seen, Stage IV and V worms first appeared in February, and Stage VI in April. The level of maturation increased during the spring (March to May) warming period, and the eggs ripened and the adults died during June (maximum occurrence of Stage Vl). Essentially similar seasonal cycles were found by Rizvi (1964), Davies, E. H. (1967) and Evans, N. A. (1977a) in the British Isles. Rizvi (1964), at Rostherne Mere, Cheshire, England, did not find a complete absence of s. bramae during some of the summer months. In Rutilus rutilus young trematodes occurred from mid-July, concurrent with the gravid worms which persisted until September in small numbers. Eggs were first seen in March. Invasion of the fishes took place over at least a 2 to 3 month period. Davies, E. H. (1967) found S. bramae in Leuciscus cephalus, L. leuciscus and R. rutilus at the River Lugg, Herefordshire, England. S. bramae was found all year in R. rutilus, but not from June through October in L. cephalus or from June through September in L. leuciscus. The trematode was most common, with higher incidences, in R. rutilus. In R . rutilus the lowest incidence was August, rising from then over the winter to reach a peak of 50 % by April, which was maintained through June, to fall from July. The intensity of infection was never high, but tended to follow the pattern of incidence. A similar flow of incidence was seen in L. cephalus, except that the infection was first found in November (7 %), rose to 42 % by February and 47 % by April, to fall in May (19%) and disappear that month. The incidence of S. bramae in L . leuciscus was more sporadic but rather similar to L. cephalus. The maturation was studied as four stages. Worms equivalent to Malakhova’s (1961) Stages I and It were found in R . rutilus from October to July, but predominated in October and December. They were most common in L. cephalus in November and December. Eggs were first seen in January in both fish species, and the main egg production was February to May in L. cephalus, but March to July in R. rutilus. Worms with eggs were last seen in L. cephalus in May, but persisted until September in R . rutilus. Evans, N. A. (1977a) studied S. braniae in R. rutilus from the Worcester-Birmingham Canal, England. Incidence was low from June to October, but increased sharply from October to November. During March and April the incidence fell to the low summer level. Intensity followed this overall pattern. From August to February the trematodes were largely immature (equivalent to Malakhova’s (1961) Stages I and 11) and the most rapid development occurred in April and May so that by June and July most parasites were gravid. The gravid worms died in July and August. The following authors have also provided data about the seasonal occurrence of S. bramae: Ruszkowski (1926), Koval’ (1952), Kulakovskaya (1955), Bogdanova (1958), Izyumova (1958, 1959a,b, 1960), Vojtkova (1959), Kozicka (1959), Komarova, T. I. (1964), Lyubarskaya (1970), Raut-

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skis (1970a, b), Marits and Tomnatik (1971) and Kennedy (1972). Localities and species of fishes studied are given in Table 3. In each instance the findings conformed to the concept of an annual pattern of development, commencing late summer or autumn and terminating in the fish host the following summer. Evans. N. A. (1977b) studied site-preference o f S. hramae within the intestines of Rutilus rutilus. In summary, he concluded that once the worms were established in the intestine there was little migration. The larval stages of S. hrarnne were studied by Chernogorenko-Bidulina and Bliznyuk (1960). Bithytiia leachi were infected by sporocysts. Cercariae of three types, short-tailed, tailless and encysted, were within the liver of one of the snails. Sporocysts with only encysted cercariae were in the liver of the same snail, and in many others. Encysted cercariae were also seen outside the sporocysts. One snail contained a sporocyst having two tailless cercariae, two metacercariae, one sexually mature S. hramae and numerous eggs with developed miracidia. The authors concluded that the larval development could involve a mollusc only, o r a mollusc and a leech, or perhaps a situation where two mollusc individuals of the same species were utilized. Spliaerostoma globiporum ( Rudolphi. 1802) This species is sometimes regarded as a synonym of S. bramae. Hausrnann (1897) recorded it from five species of fishes a t Basel, Switzerland. from March to September and in November. It was not found i n January or February. and fishes were not examined in October and December. Kozicka (1959) was unable to establish a clear periodicity in Misguriius fossilis and Scardinius eryt~iroplit~ialt~ius from Lake Druino, o r Rutilus rtitilus and S. erythroplithalmus from Lake Mamry Polnocne, Poland. However. she did find more S. g/obir,oruin in autumn and winter than in summer. None were seen in Lake Mamry Polnocne in summer in older fishes, but I-year-old fry were heavily infected by the trematode a t that time. Milicer (1938) reported . S. brarnae in Lake Wigry, Poland, in July and August. Shul'man et a/. (1974) found S. glohiporurn in Rutilus rutilus from the Karelian Lakes, U.S.S.R. The cycle of occurrence was very similar to that of S. bramae. In 1957 no worms were found in August, the incidence rose from 13% in September up to 100% by January 1958 and remained about 60% from March to June, to fall to 6 % in July when the last trematodes were recovered. A reinvasion occurred in October (6'%;), 1 month later than the previous year, to rise to 6 6 % by April 1959. the last worms being found in June 1959 (l2%), 1 month earlier than 1958. The month difference either way between the start of invasion and the loss of the gravid worms probably reflected different weather conditions in these years, which would have influenced water temperatures. 1 4. Familv Orientocreadiidae

Orientocreadiurn siluri (Dubinina and Bykhovskii, 1954) Dubinina ( I 949) reported this species, as Paratormopsolus siluri, in Silurus glanis from the Volga Delta, U.S.S.R. The incidences were: summer 1940, 26.7%; winter 1941, 6.7%; spring 1941, 33.3%.

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15. Familj~Paranrphistoniidae

Pisciamphisromrr stunkardi ( Holl, 1929) Holl (1932) observed P. stunkardi in Lepotnis gihhosus and L. gulosus from a settling pond, near Durham, North Carolina, U.S.A. In L. gihhosus the highest incidence was autumn (October, 48 %) and it occurred from September to April, but not in June and July. Highest intensity (average number per fish) was also in October (4.7). In L . gulosus an incidence was found in A.ugust (33 %) and from October to May, excluding January. Peak incidences were May and December (both 40%) and peak intensity was in August (1.5). Cloutman (1975) reported the average number per fish for L . p i l o s ~ i r . L. macrochirus and Micropterus salmoides from Lake Fort Smith, Arkansas, U.S.A. P. sturikardi was present in L. gulosus during all months of the year. except for August. It did not occur in L. rnacrocliirus or M . salmoirles during this month. Maximal occurrence was in October ( L . gulosus. 3.1) through to June (4.2). with a peak in March (16.0). 16. Faniily Plagiorchidae Alloglossidium corti ( Lamont, I92 I ) Holl (1932) found A . corti in a settling basin near the Ern0 River. North Carolina. U.S.A. The incidence in Ictalurus natalis was: May 103, June 0,

J u l y 40, August 28.6. September 60, October 44.4 and November ?3.3".;,. Specimens were also obtained in bullheads. presumably I. natalis, from a lake near Gibsonville, North Carolina, in November and December 1927 and March 1928. Large numbers of A . corti were found during the spring (Holl, 1932). Experimental infections of Ictalurus. iinralis by A . corti from Ramona Lake, Missouri, U.S.A., were made by McCoy (1928a). i n March (aquarium water temperature about 18°C) compared with July (water temperature about 27"C), the worms recovered in July 6 days after feeding were at about the same stage of development as those recovered 12 days after feeding i n March. Thus development was more rapid at the higher water temperatures.

I 7. Family Saiiguirzicolidae Sanguiiiicola armata Plehn, 1905 Reported from Aristiclitliys nobilis, Cypriiius carpio, Hy~~o~~litlinliiiic~litli~~s niolitrix and Mylopliaryngodoii piceus from Taihu, China, by Cheng-Yen et a/. (1965), this species seemed to increase gradually in occurrence with the advance of the season. Sanguinicola inermis Plehn, 1905 S. inermis is a potential danger to the rearing of Cyprinus carpio i n ponds in the southern areas of the U.S.S.R. (Bauer, 1959a, 1968; Bauer ct d.. 1969). The epizootiology, pathology and treatment in fish-breeding farms in the U.S.S.R. was considered by Naumova (1961a). Smith (1972) has reviewed the seasonal dynamics of infection of S . iiiernzis and other sanguinicolids.

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Lucky (1964) has shown that seasonal variations were temperaturedependent. In spring and early summer the trematodes occurred mostly in the heart and ascending aorta of Cyprinus carpio (80% in heart, conus arteriosus and aorta ascendens, 20% in gill arteries). During egg release of S. inermis, July and August, 95% of the worms were in the gill arteries and the gill arches were filled with eggs. Scheuring (1923), in Germany, had earlier shown that sexual development, with optimum temperatures for egg development, occurred in summer, and was slowed down by decreasing temperatures. There is general agreement that the development was facilitated by warm water temperatures (Chechina, 1959; Lucky, 1964; Naumova, 1961b; Scheuring, 1923). The development in the mollusc hosts also occurred in summer. Lymnaea auricularia, L. stagnalis and Radix ovata were infected (Chechina, 1959; Naumova, 1961b; Sapozhnikov, 1976; Scheuring, 1923), as well as a number of other species of molluscs (see Scheuring, 1923). Cercariae were released at 12°C and above, and survived for 48 h at 13"C, and 22-29 h at 20°C (Naumova, 1961b). Specificity of infection of fish hosts was demonstrated by Naumova (1961b). She achieved successful experimental establishment of cercariae in Cyprinus carpio, but not in Carassius auratus or Tinca tinca. Cercariae killed C. carpio; Sapozhnikov (1976) found that 8-day-old fish were killed by 10 cercariae, but at the age of 3 months, the lethal level to kill all the fishes had risen to between 2 and 2.5 thousand cercariae. Invasion of the fishes occurred at an early age. Indeed Scheuring (1923) found most S. inermis in young rather than old Cyprinus carpio. The softer skin tissues of young fishes facilitated penetration. During May to July in the Ukraine, U.S.S.R., Sapozhnikov (1976) observed that in the worst affected pond, all the young C. carpio were infected, at least half the Lymnaea auricularia were also infected and 1 ml could contain 5 or 6 cercariae. Naumova (1961~)reported infections in 1-month-old C. carpio fry. Highest incidence and intensity of infection by S. inermis were reported during the summer months (Chechina, 1959; Lyaiman, 1951; Lucky, 1964; Naumova, 1961~).However, high incidences in winter were found by Ivasik (1953, 1957) and Ivasik and Svirepo (1971). The latter authors found that 14% of young Cyprinus carpio on a fish farm in the Lvov area, U.S.S.R., died in wintering ponds owing to S. inermis infections. Thus worms were present throughout the year (Bauer, 1959a) and the levels of infection in particular circumstances were determined by the time of invasion of the fishes and their ages. Worms of spring-summer invasions died by autumn, but those of autumn invasions overwintered to die after reproduction the following summer (Ivasik, 1957; Naumova, 1961~).Although Scheuring (1923) had found most S. inermis in young C. carpio, and Bauer et al. (1969) agreed, Ivasik (1957) reported increased infections with age. Sanguinicola magnus Cheng-Yen Hu, So Long and Wei-Chu Lee, 1965 Described from Ctenopharyngodon idella Cheng-Yen et al. (1965) found that in Taihu, China, there seemed to be a tendency for infection to increase gradually with the season. Sanguiiiicola volgensis Raiin, 1929

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Izyumova (1960) found this species in Esos lucius from the Rybinsk Reservoir, U.S.S.R. Incidence and intensity of occurrence were: winter 9.9 %, 1; spring 13.3 %, 1-2; summer and autumn, 0. 18. Family Transversotrematidae Transversotrema patialense (Soparkar, 1924) T. patialense was studied at Batalogoda, Ceylon, by Crusz and Sathananthan (1960) and Crusz et a/. (1964). The snail host was Melanoides tuberculata, and the fish hosts Macropodus cupanus, Ophiocephalus putictatus and Tilapia mossambica. The worms were found established under the fish scales, with a 40% incidence. Specimens in November had abundant spermatozoa, but no eggs in the uterus (Crusz and Sathananthan, 1960). Crusz et a/. (1964) experimentally demonstrated the life cycle. Trematodes became established on the fishes 1-22 days post-exposure to infection. Small trematodes without vitellaria were recovered a day after exposure, and egg-laden individuals were obtained at least 8 days post-infection. T. patialense was collected in the field in March, April, May and November. This trematode was utilized as an experimental laboratory model by Anderson, R. M. (1976), Anderson, R. M. and Whitfield (1975), Anderson, R. M. et al. (1977) and Mills (1976). The worms were maintained as a selfsustaining natural population in aquaria at 24-26"C, using Melanoides tuberculata as the intermediate and Brachydanio rerio as the definitive host. Anderson, R. M. and Whitfield (1975) provided a flow chart of the life cycle. The water temperature of 2426° C was selected as corresponding to the May water temperature (23-25°C) in Penang, Malaysia, where a natural population of T , patialense occurred (Anderson, R. M. et al., 1977). A number of parameters, including survival and fecundity in relation to water temperature, have been, and are, in process of study. Anderson, R. M. et al. (1977) showed that the adult population on a single host was controlled by two processes, immigration and death rates. The maximum life span on a fish was about 10 weeks. Death of the T. patialerise may be from senescence, immune responses or density-dependent effects. However, immune responses of the host were not important in the parasite population levels used in the experiment, and density-dependent survival was not demonstrated for infections of up to 40 worms per host. At constant temperature and light (12 h light, 12 h dark), the survival of the adult parasites on the fishes remained constant in form in parasite populations subject to temporally overlapping infections. The results of these population experiments showed that the observed mean number of parasites per host closely followed the predictions of a theoretical model (equation 14) defined by Anderson, R. M. (1976). The relationship between adult and larval survival of T. patialense and water temperature will be considered in a later publication, according to Anderson, R. M. et al. (1977). The results of this study may be of considerable significance in explaining seasonal dynamics of trematodes in tropical and other conditions.

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

19. F m i i l v Walliniidae Macrolecithus papilliger Rees, 1968 This species was studied in Phoxinus yho.\-inus from Frongoch Lake, Wales, by Bibby (1972). Incidence occurred throughout the year and varied from 14”/, ( J L I ~ Yup) to 56% (April). There were two peaks, in spring (April) and autumn (November). The seasonal variations in incidence were related to several factors, including “hibernation” of the host in low winter temperatures. and an increase of activity in summer a t high temperatures. No significant correlation was found between season and incidence and intensity of infection. Maturity of the trematodes was assessed in three stages: inimature. no sperm present, eyespot remains visible; mature, with sperm in the seminal receptable; gravid, with eggs in the uterus. There was a percentage increase in all three stages in spring and autumn. Fishes appeared t o become invaded i n summer, early autumn and early spring. Peak incidence of immature worms was in September 1967 and August 1968, followed by increased numbers of mature worms from October 1967 t o February 1968 and May to September 1968. Gravid worms increased from February to May 1968. with none present during late summer. Bibby (1972) postulated that egg release occurred during early summer.

SEASONAL STUDIES OF ADULTTREMATODES I N WORLDCLIMATIC ZONES The reasons for considering seasonal studies of helminth parasites in relation to world climate zones have been discussed fully by Chubb ( I 977) and earlier in this review (Section IV). A map showing climate zones was provided in Chubb (1977). Table 3 lists adult trematodes studied for seasonal occurrence in their appropriate climate zones. V11.

A.

TROPICAL (CLIMATE ZONE

I)

1 . Rain)! (Climate zone 1 a)

Few seasonal studies have been attempted in tropical conditions. The studies of Crusz and Sathananthan (1960) and Crusz et al. (1964) on Transvzrsotrema patialense in Sri Lanka are within this zone. The trematodes were present in fishes in the field in March to May and November, but an attempt to assess incidence during all months was not made. The experimental studies of Anderson, R. M. and Whitfield (1975) showed that the life cycle was continuous and self-sustaining in laboratory conditions at 24-26°C so that it seems likely that the worms will be present in wild fishes during all months of the year. However, Crusz and Sathananthan (1960) did not find eggs in the worms recovered in November, 1959, thus further field investigation is needed.

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265

2. Sai~aniia(Climate zone I b) Three species have been investigated in this climate zone. Pal (1963) provided some information for Aphanurus monolecitlius and Orien~opliorus hrevichrus for the migratory fish Hilsa ilisha from the River Hooghly, India. Seasonality occurred in both species of trematodes, which showed maximum incidences during the coolest time of the year, November to February, and were not found, o r rarely so, during the monsoon months (July and August). The seasonal changes in these species may be related to the invasion of fishes by the trematodes in the marine zone of the river and the migratory movements of H. ilisha. A clear demonstration of seasonal occurrence in tropical freshwater conditions was provided by Madhavi (1979) for Allocrea~Iiuiii.fasciatusi at Waltair. India. Although cercariae were released from the snail host all year. there was a maximum transmission of nietacercariae via several copepod intermediate hosts in September, following the monsoon rains of JUIYand August. This peak transmission established peak periods of growth, maturation and egg release in succession during the following months, so that the maximum eggs were released from January t o April. However, immature and niatiire A . jasciatusi were present all year. In this locality and circumstance temperature was not a limiting factor in determining seasonality. 3. Highland (Climate zone 1 c), Semi-desert (Climate zone 1 d ) atid Desert (Climate zone 1 e) N o seasonal studies of adult trematodes are known to the author from these climate zones. B.

SUBTROPICAL (CLIMATE ZONE

2)

1. Mediterranean (Climate zone 2 a) N o seasonal studies of adult trematodes are known to the author from this climate zone.

2. Humid (Climate zone 2 b) Some information is available for 10 species of trematodes that have been investigated in this climate zone. Annual fluctuations of Asymphylodora tincae in Carassius auratus from Okayama Province, Japan, were related to temperature (Yoshino, 1940). Lecithaster indicus and L. extralobus were found by Srivastava (1935a) in Hilsa ilisha at Allahabad, India, in the winter, but not during the rainy season (July and August). A similar pattern of occurrence at the same locality was reported for Orientophorus breviclirus in H . ilisha (Srivastava, 193513). Almost every fish was infected in winter, but in

266

JAMES C . C H U B B

summer incidence rapidly declined to below 10 %. The migratory life pattern of H . ilisha may be an important factor (see also Section VII A 2). Cheng-Yen et a/. (1965) have reported that the incidences of Sanguinicola armata and S. magnus in cyprinids at Taihu, China, seemed to have a tendency to increase gradually with the season. A clear seasonal pattern was seen for Crepidostomum cooperi. At Little River, Oklahoma, U.S.A., McDaniel and Bailey (1974) found a high incidence during winter (90% in February) and a low incidence in summer (6 % in July) which ascended to about 26 % by September. The worms overwintered as adults, matured to pass eggs in spring, after which they were lost. Recruitment occurred in the autumn. Crepidostomum isostomum in Aphredoderus sayanus at Whisky Bay, Louisiana, U.S.A., also demonstrated seasonality (Elkins and Corkum, 1976). Invasion of fishes occurred from March to July (maximum in April and May) at which time incidence and intensity of occurrence were also at peaks. From June onwards the numbers declined, maturation occurred, to reach a 100% level by November through to January. Eggs were shed from September to May. Phyllodistomum pearsei, also from Aphredoderus sayanus from Louisiana, U.S.A., did not show seasonal periodicity of incidence or intensity of occurrence (Elkins and Corkum, 1976). However, seasonal maturation was evident. Immature worms appeared in March, and in April and May all were juvenile. Maturation occurred from June to August, to give worms shedding eggs from September onward. There was a complete change of populations, gravid to juvenile worms in March/April. The seasonal cycle of the didymozoidean trematode Ovarionematobothrium texomensis from the ovaries of Zctiobus species in Lake Texoma, Oklahoma, U.S.A., was related to the ovarian development and spawning cycle of the host fishes (Self et a]., 1961, 1963). C.

MID-LATITUDE (CLIMATE ZONE

3)

1. Humid warm summers (Climate zone 3 a i) The following species of adult trematodes have been studied in this climate zone, although not in great detail, none the less the data conform to patterns of seasonality studied in more depth in other mid-latitude zones: Allocreadium isoporum, Hausmann (1 897) ; Aspidogaster limacoides, Marits and Tomnatik (1971), Marits and Vladimirov (1969) ; Asymphylodora imitans, Marits and Tomnatik (1971), Marits and Vladimirov (1969); A . tincae, Hausmann (1897), Ruszkowski (1926); Azygia lucii, Hausmann (1897), Ruszkowski (1926) ; Buceplzalus polymorphus, Hausmann (1897), Molnhr (1966) ; Bunodera luciopercae, Dyk et al. (1954), Hausmann (1897), Milicer (1938), Ruszkowski (1926), Sramek (1901), Vojtkova (1959); Nicolla skrjabini, Marits and Vladimirov (1969); Phyllodistomum elongatum, Marits and Vladimirov (1969), Vojtkova (1959) ; Phyllodistomum pearsei, Holl (1932); Rhipidocotyle illense, Molnhr (1966) ; Sanguinicola inermis, Ivasik (1953,

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

267

1957), Ivasik and Svirepo (1971), Sapozhnikov (1976); Sphaerostoma bramae, Marits and Tomnatik (1971), Ruszkowski (1926), Vojtkova (1959); and S. globiporum, Hausmann (1897), Seasonal studies of nine species of trematodes have been carried out in this zone and no other. The incidence and maturation of Acetodextra amiuri, which occurred in the ovaries of Ictalurus species in the River Wabash, Indiana, U.S.A., was tied to the maturation cycle of the host (Perkins, 1950, 1951, 1956). Crepidostomum ictaluri from Ictalurus punctatus in Lake Carl Blackwell, Oklahoma, U.S.A., was present in all seasons, with no apparent variation (Spall and Summerfelt, 1969). Phyllodistomum lacustri, from the same host and habitat, also showed little seasonal difference in incidence and intensity of occurrence, but the presence of immature worms in February to May or June revealed the seasonal turnover of population. Lissorchis fairporti, from Ictiobus bubalus and I. cyprinellus in Iowa, U.S.A., increased in size during summer, to expel eggs in great numbers in late summer (Magath, 1918). However, for five of the species, Alloglossidium corti, Crepidostomum cornutum, Nicolla wisniewskii, Phillodistomum staffordi and Pisciamphistoma stunkardi the data are incomplete. Seasonal changes were shown, but cannot be evaluated fully without further information. The studies of Nicolla skrjabini in Lake Balaton, Hungary (Molnar, 1966), and of Sanguinicola inermis in Germany by Scheuring (1923) and in Czechoslovakia by Lucky (1964) are important contributions to our knowledge of seasonal aspects of the biology of these species. Dyk (1957, 1958) and Dyk et al. (1954) have shown how the altitude of habitat can influence the seasonal periodicity of adult trematodes. Crepidostomum farionis matured earlier or later in the summer as the water temperature was influenced by lake altitude and the warmth of the particular year. In summary, all the species studied i n this zone probably show seasonal changes, most in incidence and intensity of occurrence, and all in patterns of maturation. 2. Humid cool summers (Climate zone 3 a ii) Twenty-three species have been studied, and all show evidence of seasonal variations. The following species need further investigation, in order to clarify detail : Asymphylodora imitans, A. kubanicum, Bucephalus polymorphus, Phyllodistomum conostomum, Phyllodistomum sp. from Gasterosteus aculeatus and Pungitius pungitius (Banina and Isakov, 1972), Rhipidocotyle illense and Sanguinicola volgensis. Evidence from other mid-latitude climate zones for some of these species confirms that the observations made in this zone conform to overall seasonal patterns determined elsewhere. The remaining sixteen species have been investigated in some detail and all have seasonal patterns of occurrence and maturation. Details can be found as follows: Allocreadium isoporum (Koval’, 1952), A. lobatum (De Giusti, 1962), A. markewitschi (Koval’, 1952), Asymphylodora tincae (Komarova, M. S., 1951b), Azygia lucii (Markova, 1958; Tell, 1971), Bunodera luciopercae (Cannon, 1972; Komarova, M. S., 1941; Lyaiman, 1940), B. sacculala

268

JAMES C . CHUBB

(Cannon, 1972), Crepidostornuvri cooperi (Cannon, 1972), Nicolla s k r p b i i i i (Komarova, M. S., 1951a; Koval', 1952), Palueorcliis incognitis (Kulakovskaya, 1955j, Pliyllorlistornun~ aiigulatun? (Izyuniova, 1958, I959bj, P . elongaturn (Izyumova, 1958), P. fbliutn (Tell, 197 I), P . pseudofolium (Izyumova, 1959a), Sunguinicola iiiermis (Nauinova. 1961~)and Splinerosronin hramae (Kulakovskaya, 1955). There are contradictions that need to be resolved; two examples are quoted here. Markova ( 1958) found clear seasonality of invasion, incidence and maturation of Azygia lucii in the River Oka, U.S.S.R. She concluded that invasion occurred from January to March, with the concurrent loss during these months of the previous generation of worms. However, Tell (1971) reported that the population of A . lucii in Lake VGrtsjarv, Estonia, started to increase from the end of June or early July, and that these worms disappeared from the fishes the end of May or early June the following year. A similar apparent contradiction applies to Nicolla skrjabini. Both Koniarova, M . S. (1951a) and Koval' (1952) investigated its occurrence in the River Dnepr, U.S.S.R., but Koniarova found N . skrjabini all year, whereas Koval' observed that the fishes were free of the trematode from December to February. These examples show clearly how variation in the same or different habitats can occur, but unfortunately. with our present knowledge. it is not always possible to explain them. 3. Enst coasi (Cliniate m i e 3 a

iii)

The study of Noble, R. L. (1970) on Perca flnvescetis at Oneida Lake. New York, U.S.A., suggested that Bunorleva luciopercae followed its usual seasonal incidence pattern, but no seasonal trends were noted for Crepitlostonium cooperi between 31 March and 1 December 1966. Krull ( I934b) experimentally observed that Rhipidocotyle septpripillata from the Potomac River, Virginia, U.S.A.. invaded fishes both during winter and summer. I n winter, maturity was achieved after 10-15 days, in summer after 5-7. The trematodes lived in the host for a further 18 days in winter and produced eggs containing miracidia. but in summer were expelled on reaching maturity . 4. Marine west coasi (Cliniute zone 3 b) Seventeen species have been investigated in this climate zone. and all show evidence of seasonal changes of status. Three species, A s ~ n i j ~ l i ~ ~ l o r l ~ ~ r a niarkewitschi, Buceplialus polymorplius and Spliaerostorna glohiporuni. have not been studied in detail, thus further examination is needed. A . niarkeii-itsclii has not been investigated in any other climate zone. The other fourteen species have been examined in considerable detail, so that the seasonal incidence. intensity and maturation patterns are clear. The most detailed studies are: Allocreadium isoporum (Davies, E. H., 1966, 1967; Halvorsen, 1972; Kennedy, 1972). A. trnnsversale (Davies, E. H., 1967), Asymnpliylodora kubanicuni (Evans, N. A., 1978; Mishra, 1966), A. fiiicae (Wierzbicka, 1964, 1970), Azygia lucii (Halvorsen, 1968, 1972; Odening

HELMINTHS I N FRESHWATER FISHES

269

and Bockhardt, 1976); Bunoclera luciopercae (Andrews. 1977: Mishra. 1966; Rizvi, 1964: Wierzbicki, 1970: Wootten. 1973b). Crepiclostomuni ,farionis (Awachie. 1963. 1968). C . rnetoecus (Awachie. 1963, 1968). Macrolecitlius papilliger (Bibby, 1972). Nicolla gallica (Rumpus. 1975). PliyllocjistoiiiiuiiJolium (Chappell, 1969). P. simile (Thomas, 1958b. 1964). Rhipiclocotjllr illense (Halvorsen, 1972) and Spliaerostotna hraniae (Davies. E. H.. 1967: Evans, N. A., 1977a: Rizvi. 1964). Differences between localities within the climate zone occur. At the River Lugg. Herefordshire, England, Davies. E. H. ( 1967) found A1locreadiur)i isoporuni i n its principal hosts Leuciscus ceplialus and L. Ieuciscus during all months of the year, but Kennedy (1972) reported it from the River Avon. Hampshire. England, in L . leuciscus from November to June only. Halvorsen (1972) in the River Glomma, Norway, found an even more restricted occurrence of A . isoporuni, in Abraniis bratiin May and June only. and in Rutilus rutilus from May to July. Davies. E. H. (1967) at the River Lugg, observed A . isoporutn in R . rutilus during all months from October to August, but not in September. Halvorsen ( 1972) speculated that low water temperatures in the River Glomma prevented establishment of A . isoporum in fishes in October and November. I t is interesting to see that differences in incidence of Sphaerostoma bratnae also occur. At the River Lugg it was found in R. rutilus in all months of the year, but in L. ceplialus from November to May only and in L. leuciscus during October, December and in March to May only (Davies, E. H., 1967). At the River Avon, Kennedy (1972) recorded S. branine in L. leuciscus from January to June. In these instances it appeared to be some aspect of the biology of the host fishes that determined incidence of the parasite. 5 . Semi-desert (Climate zone 3 c)

In this zone seventeen species have been examined, and in all instances there is evidence of seaonal changes. Reasonable detail is available for Aspidogaster

limacoides, Bunodera luciopercae, Asympliylodora demeli, A . iinitans, A . kubanicurn, Bucephalus polyrnorphus and Nicolla skrjabini as a result of the work of Koniarova, T. I. (1964). Crepidostonium,farionis was investigated by Voth et a/. (1974) and Phyllodistomum elongatuni by Dubinina (1949) and Komarova, T. 1. (1964). The remaining species, Azygia Iucii, Bunocotyle cingulata, Orientocreadiuni siluvi, Palaeorchis incognitus. P . unicus, Phyllodistomuni angulatum, P. foliuni and Sphaeroston?a brainae require further investigation to clarify the

details of their seasonal biology in climate zone 3 c. It is noteworthy that Lavrov (1955) found Bunodera luciopercae in Lucioperca lucioperca in the River Volga, near Saratov, U.S.S.R., on 26 June. The waters of the Volga were near zero in winter, and Lavrov (1955) attributed the delayed development to more severe hydrothermal conditions in rivers conipared with lakes, where winter temperatures were higher. 6. Desert (Climate zone 3 d ) No seasonal studies from this climate zone are known to the author.

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

7. Sub-polar (Climate zone 3 e) Six species have been studied in this zone and detailed seasonal information is available for Allocreadium isoporum (Malakhova, 1961), Azygia Iucii (Malakhova, 1961), Bunodera luciopercae (Androsova and Bauer, 1947; Malakhova, 1961, 1963), Phyllodistomum elongatum (Titova, 1957), Sphaerostoma bramae (Malakhova, 1961, 1963) and S. globiporum (Shul'nian et al., 1974). 4 a and 4 b) The polar climates are probably unsuitable habitats for trematodes in freshwaters. Crepidostomum farionis has been reported from Iceland by Brinckmann (1956) from Myvatn, which falls within climate zone 4 a. It must be assumed, therefore, that at least some life cycles can be completed under these climatic conditions. Brinckmann's (1956) specimens were collected in July and contained eggs. Blair (1973) found that Lymnaea peregra was infected by larval stages of a number of trematodes in southern Iceland (climate zone 3 b). D.

POLAR (CLIMATE ZONES

5) The work of Dyk (1957, 1958) on the seasonal dynamics of Crepidostomum farionis in lakes in the High Tatra Mountains, Czechoslovakia, has already been mentioned in climate zone 3 a i (Section VII C 1). It suggests that the cooler water temperatures of high altitudes can delay maturation of the adult worms. No work on seasonal occurrence of adult trematodes in mountain country falling within this zone are known to the author. E.

F.

MOUNTAIN (CLIMATE ZONE

SPECIES STUDIED IN MORE THAN ONE CLIMATE ZONE

A number of species of adult trematodes have been studied in sufficient detail in more than one climate zone so that an interesting comparison on an intra- and inter-zone basis can be made. All the trematodes investigated in more than one climate zone are shown in Table 4. The following species have not been examined in sufficient detail to make it possible to give more than the generalization that the basic patterns of seasonality appear the same from zone to zone: Aspidogaster limacoides, Asymphylodora imitans, Bucephalus polymorphus, Palaeorcliis incognitus, Phyllodistomum angulatum, P. elongatum, P. pearsei, Rhipidocotyle illense and Sphaerostoma globiporum. The other species, discussed in more detail below, also conform to this generalization, although with some variations of timing of events, which are noted. Only one species, Crepidostomum cooperi, appears as a possible exception t o the generalization. Cannon (1972) observed maximum incidence of Crepidostomum cooperi during the summer in Lake Opeongo, Canada (climate zone 3 a ii), and

TABLE4 Species of adult trematodes studied ( S )for seasonal occiirrence in more than one climate zone The species are in alphabetical order Climate zone

Trematode species Allocreadium isoporum Aspidogaster limacoides Asymphylodora imitans Asymphylodora kubanicum Asymphylodora tincae Azygia Iucii Bucephalus polymorphus Bunodera luciopercae Crepidostomum cooperi Crepidostomum farionis Nicolla skrjabini Orientophorus brevichrus Palaeorchis incognitus Phyllodistomum angulatum Phyllodistomum elongatum Phyllodistomum folium Phyllodistomum pearsei Rhipidocotyle illense Sanguinicola inermis Sphaerostoma bramae Sphaerostoma globiporum

1

2

b

b

S

S S

S

3

ai

aii

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

aiii

S S

b

S

S

C

S S S S S S

e S

S

S

S S S S S S

S

S S S

S

S S

272

JAMES C. C H U B B

stated that it was the least temperature-sensitive of the three species he investigated. Noble, R. I-. (1970) also found high incidences of C. cooperi during the summer months in Lake Oneida, New York, U.S.A. (climate zone 3 a iii). In contrast to these occurrences, McDaniel and Bailey (1974) noted incidences of 9076 in February, falling to a minimum of about 6 % in July in Little River, Oklahoma, U.S.A. (climate zone 2 b). The worms passed their eggs in spring in the Little River after which they disappeared. The next generation was established in the autumn. It is possible to speculate, without detriment to Cannon's (1972) observation that C. coopevi was the least temperature-sensitive of his species, that the higher summer water temperatures of the most southern habitat, Little River, were high enough to cause loss of the adult worms during this season. However, the hypothesis that water temperature is the factor causing this relatively major change in pattern of seasonality of C. cooperi between southern and northern habitats reniains to be tested. lntrazone differences of timing of events i n the annual patterns of occurrence can be seen in Allocreadium isoporuni, Azygia lucii, Buiiodem luciopercae, Nicolla skrjabitii and Splinerosronia branine. The differences for Allocreadiuni isoporuni within climate zone 3 b have already been discussed in Section VII C 4. Halvorseii (1972) speculated that low water temperatures i n the River Glomma, Norway, may have prevented establishment of this species in fishes in October and November. Similar variations for Spliaerosrot~iahraimw i n England between the River Lugg, Herefordshire (Davies, E. H., 1967), and the River Avon (Kennedy. 1972), were also considered in Section VII C 4. It was suggested that the explanation should be sought in some aspect of the biology of the host species in the two habitats. However, other investigations of S. hratnar within climate zone 3 b (Evans, N . A., 1977a: Rizvi. 1964) have shown the pattern described by Davies, E. H. (1967) so that the situation in the River Avon (Kennedy. 1972) may be the atypical one. The marked intrazonal differences in the annual patterns of occurrence of Azygia lucii and Nicolla skyjahitii have been considered in Section VII C 2. It should be noted with A . lucii that most workers have not found such clear seasonal variations as those described by Markova (1958) or Tell (1971) but this will be referred to later under interzonal variations. Butiodera luciopercae is one of the most investigated of the adult fish trematodes. It has been examined by nine authors in climate zone 3 b. A number of intrazonal differences and similarities can be seen (see Fig. 6). Invasion of the host fishes commenced in July at Loch Leven. Scotland (Campbell. 1974), the Shropshire Union Canal, Cheshire, England (Mishra, 1966), Rostherne Mere, Cheshire, England (Rizvi, 1964), Lake Dargin, Poland (Wierzbicki, 1970), and Hanningfield Reservoir, Essex. England (Wootten, 1973b). However, invasion occurred from August at Lake Druino, Poland (Kozicka, 1959), and at a lake near Oslo, Norway (Skorping. 1976), but not until September at the River Glomma, Norway (Halvorsen. 1972). Andrews (1977), a t Llyn Tegid. Wales, found that invasion could occur in all months. but the annual period of peak invasion commenced in July. In all

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273

habitats, maturation of the adults occurred through the winter. The gravid adults disappeared from the fishes during May at the Shropshire Union Canal, Cheshire, England (Mishra, 1966), and Lake Dargin, Poland (Wierzbicka, 1970), June at the River Glomma, Norway (Halvorsen, 1972), a t a lake near Oslo, Norway (Skorping, 1976). and at Hanningfield Reservoir, Essex, England (Wootten, 1973b), and in July at Llyn Tegid, Wales (Andrews. 1977). Loch Leven, Scotland (Campbell. 1974), and Rostherne Mere, Cheshire, England (Rizvi, 1964). Thus there is an overall similarity of annual pattern of biology of B. luciopercae within the climate zone, but with something of a 3 month variation in time of commencement of peak invasion and loss of adult worms. If Cannon (1972) is correct, loss of gravid adult worms can be correlated with an increase in water temperature above 20'C. and it is likely that these variations of timing of both invasion of the fishes and loss of the gravid worms could be correlated with temperature regimes in the particular habitats as well as the changes in weather patterns from year to year. in a s much as weather affects the rate of warming o r cooling of water in the environment. It is appropriate, in the light of the intrazonal variations reported for Bunodeva luciopercae above, t o discuss the interzonal variations. B. Iuciopercae has also been studied in detail in climate zones 3 a ii, 3 c and 3 e. In climate zone 3 a i i , invasion of the fishes commenced in late June at Lake Opeongo, Ontario, Canada (Cannon, 1972), and Lake VBrtsjarv, Estonia (Tell, 1971). in August at Lake Seliger, U.S.S.R. (Lyaiman, 1940). but not until late October and November a t Bay of Quinte, Lake Ontario, Canada (Tedla and Fernando, 1969). In climate zone 3 c. Komarova. M. S. (1941) found invasion in the River Dnepr, U.S.S.R., to start from June. I n climate zone 3 e, invasion commenced in mid-August at the River Yenisei. U.S.S.R. (Androsova and Bauer, 1947), and in September a t Lake Konche. Karelia. U.S.S.R. (Malakhova, 1963). Loss of the gravid adult worms occurred in climate zone 3 a ii in May at Lake Opeongo, Canada (Cannon, 1972). Lake Seliger, U.S.S.R. (Lyaiman, 1940), Bay of Quinte, Lake Ontario. Canada (Tedla and Fernando, 1969), and in early June a t Lake VBrtsjarv. Estonia. U.S.S.R. (Tell, 1971), i n climate zone 3 c in June at the River Dnepr. U.S.S.R. (Komarova, M . S., 1941), and in climate zone 3 e in June a t the River Yenisei, U.S.S.R. (Androsova and Bauer, 1947), and in July a t Lake Konche. Karelia, U.S.S.R. (Malakhova, 1963). The times of invasion of the fishes by Bunodera luciopercae. zone to zone, are rather similar, the commonest months are: 3 a ii. end June, two of four investigations; 3 b, July, six of nine; 3 c, June, one; and 3 e, August. one and September, one. These data suggest a later commencement of invasion in the colder conditions of the sub-polar climate zone 3 e, and overall a range from the end of June through to October. The loss of gravid worms occurred: 3 a ii, May, three of four investigations: 3 b, very varied, May, June. July, three each of nine investigations; 3 c, June, one; and 3 e, June. one and July, one. It is clear that in the more continental conditions of climate zones 3 a ii and 3 c the timing of loss of gravid worms has minimal variation. May/June, in sub-polar zone 3 e it is a month later, June/July, but that in

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JAMES C. CHUBB

the more oceanic conditions of zone 3 b it has maximum variation, May through July. If temperature is the controlling factor, then the effect of a cool spring is likely to delay loss of worms most in the sub-polar 3 e and oceanic 3 b zones, where warming of the water above the critical 20°C will be slower. I n all the habitats in zones 3 a ii (four) and 3 e (two) there was a period of 1 or 2 months, usually June and July, when no fishes were infected by Bunodera luciopercae. This phenomenon was also seen in some habitats (five) in climate zone 3 b, but not in others (four), nor in the one habitat investigated in climate zone 3 c. The absence of B. luciopercae during these summer months may reflect a temperature effect, or be due to the absence of metacercariae in the second intermediate host, or a combination of these factors. It is clear that if the details of intra- and inter-zonal variation are to be understood fully, more precise observations of, for example, water temperature, must be recorded during each investigation and published as part of the results. An ideal arrangement, unlikely to be achieved unfortunately, would be to have investigations carried out on one trematode species, at three or four selected habitats within each climate zone where it occurs, and during the same 2 or 3 year period. In this way it is likely that compatible and comparable data would be obtained which would allow an understanding of the significance of year to year and habitat to habitat seasonal variations. Some other interzonal observations show similarity in seasonal details, for instance: Asymphylodora tincae, 3 a ii Komarova, M. S. (1951b, 1957) compared with 3 b Wierzbicka (1964, 1970); Crepidostomum farionis, 3 b Awachie (1968) compared with 3 c Voth et al. (1974); Nicolla skrjabini, 3 a i Molnar (1966) compared with 3 a i i Komarova, M. S. (1951a); Orientophorus brevichrus, 1 b Pal (1963) compared with 2 b Srivastava (1935b); and Sanguinicola inermis, 3 a i Lucky (1964)compared with 3 a ii Naumova (1961~). In other interzonal studies differences in timing are apparent. With Allocreadium isoporum, Koval' (1952) found that Cyprinus carpio in the River Dnepr, U.S.S.R. (climate zone 3 a ii), were invaded July/August and the gravid adults were lost the following May/June. By contrast, Davies, E. H. (1967) at the River Lugg, Herefordshire, England (climate zone 3 b), observed that Leuciscus cephalus and L. leuciscus were invaded from August to November, Rutilus rutilus from October, and the gravid adults were lost July/August in all three fishes. With Sphaerostoma bramae, Malakhova (1963) observed that invasion of Rutilus rutilus in Lake Konche, Karelia, U.S.S.R. (climate zone 3 e), was during September and October and the gravid adults were all gone by the end of June the following year. Again, the comparison is with S. bramae at the River Lugg (Davies, E. H., 1967) where invasion of R . rutilus occurred from October, but the gravid adults persisted until September the following year. It is suggested, as earlier for Bunodera luciopercae, that the continental conditions of climate zones 3 a ii and 3 e tend to limit the period of invasion and the loss of gravid adults into shorter periods than those seen in the oceanic conditions of climate zone 3 b. With Asymphylodora kubanicum in the River Dnepr Delta, U.S.S.R. (climate zone 3 c), Komarova, T. 1. (1964) found maximum incidence and

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275

intensities of infection as follows: Abramis brama, incidence April, intensity March; Blicca bjoerkna, incidence May, intensity June; Rutilus rutilus heckeli, incidence April, intensity May; and Vimba vimba ilimba natio carinata, incidence June/July, intensity April/May. At the Shropshire Union Canal, Cheshire, England (climate zone 3 b), Mishra (1966) found maximum incidence in July and maximum intensity in May in Rutilus rutilus. There is a tendency for the maxima t o be earlier in the continental conditions of climate zone 3 a ii compared with the oceanic zone 3 b. As noted above, this could be due to water temperatures increasing more rapidly in the spring in the continental conditions. In contrast t o the maximal occurrences of A . kuhanicum, it is noteworthy that the worms were not present in B. bjoerkna, R . rutilus Iieckeli or V. vimba vimba natio carinata at all during February and March in the River Dnepr Delta, and had low incidences in A . brama during these months. In the Shropshire Union Canal, A . kubanicum had low incidences in R. rutilus during February and March. In this respect, there seems to be a similarity in the biology of A . kubanicum between the two climate zones. In the examples quoted so far in this section the differences, intra- and inter-zone, have been of timing. Two species appear to show more radical variations. In climate zone 3 a ii, both Markova (1958) at the River Oka and Tell (1971) in Lake Vortsjarv, Estonia, U.S.S.R., found the Azygia lucii had clear periods when gravid adults were present and subsequently lost. In the River Oka, the gravid generation was lost in January to March, in Lake Vortsjarv at the end of May, beginning of June. I t will be noted that these two timings are different. In climate zone 3 b, however, Halvorsen (1968) at Bogstad Lake and (1972) the River Glomma, Norway, and Odening and Bockhardt (1976) at Beetzsee, near Brandenberg, Germany, did not find this pronounced seasonality. Large gravid worms with eggs in the uterus were seen all year, although in the River Glomma their number decreased after June. No doubt the explanation for these differences will be shown by further study. A second example on maturation of the adult worms is found in Phyllodistomum folium. At Lake Vortsjarv, Estonia (climate zone 3 a ii), Tell (1971) found that the parasites were of maximum size and gravid at the end of April and beginning of May. They disappeared from the fishes at the end of May and beginning of June, and reinvasion occurred from the end of July and then there was a gradual population increase to the following spring. As a contrast to this well-defined cycle, Chappell (1969) observed that Gasterosteus aculeatus in a pond on Baildon Moor, Yorkshire, England (climate zone 3 b), contained P . folium in an apparently active reproductive state and containing eggs throughout the year. Chappell (1969) speculated that it might be the duration of the lower winter water temperatures, rather than the absolute minimum, which was the most important factor. Thus, if so, the more severe winters of climate zone 3 a ii may create the distinct pattern of occurrence and maturation seen by Tell (1971), and the mild winters of climate zone 3 b allow the continuous invasion and maturation through the year noted by Chappell (1969). Such an explanation might also apply to Azygia lucii (see above).

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JAMES C. CHUBB

V111: A.

GENERAL CONCLUSIONS, ADULTTREMATODES INCIDENCE A N D INTENSITY OF OCCURKENCE

It was seen in Section V A that there were problems assessing the significance of data on incidence and intensity of occurrence of metacercariae, owing to the longevity of the metacercariae and the high probability of superimposed infections over a number of years. I t was suggested that the age of the fish was the relevant parameter for comparison with metacercarial occurrence. This situation does not apply to the adult trematodes of fishes, for as can be seen from the information in Section V1 the majority if not all of the adult worms have an annual turnover of occurrence in their hosts where invasion, establishme~t,growth, maturation of genitalia, egg accumulation and loss of gravid worms are all achieved within a maximum period of 12 months. I f an overlap of generations occurs, as for example in Azygia lucii (Markova, 1958), and some other species, there is no problem in separating the two generations, as the new one is of juvenile worms and the old one of gravid worms. The majority of the species of trematodes, 44 of those considered here. invade the fishes by means of metacercariae ingested with food organisms. Only five species, Sanguinicola armaia, S. inermis, S. magnus, S. volgensis and Transi~ersoirernapatialense normally achieve invasion by direct penetration of the fish by the cercariae. In Azygia Iucii, and possibly other species, small Es0.1- Iurius can be invaded by direct penetration of cercariae but larger E. lucius are invaded secondarily by feeding on smaller fishes. The two facts. the annual generation pattern of the adult trematodes and the route of invasion with food seen in the majority of species, suggest that the most meaningful comparison of data for incidence and intensity of occurrence will be with the length of the fishes, rather than age. It is clear in the study of most species of fishes that any diet changes, and the quantities of food eaten, are related to increasing size which can be conveniently expressed by length. Chubb (1961), for instance, found such a relationship for a number of fish species at Llyn Tegid, Wales, and it is a very general phenomenon. Length of the fish is only a valid parameter of comparison for species of parasites whose numbers are maintained in dynamic balance within the host, by the processes of invasion and elimination of worms. The annual pattern of occurrence, in theoretical terms, is of a gradual increase in incidence and intensity to a peak, followed by a decline to a minimum, after which the generation of worms is completed. The pattern includes phases of invasion (Section VIII C) and growth and maturation (Section V l l l D). In fact, the clear pattern may be hidden as far as incidence and intensity of occurrence are concerned by an overlap of generations, especially if invasion of the fish host is possible over a long period, but the stages of maturation present normally reveal the successive generations. In

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some species of adult trematodes, invasion of the fishes occurs over very long periods, and in others, during the whole year. In these instances the patterns may in practice disappear. Table 5 provides a calendar of seasonal events for 25 species of trematodes for which a reasonable amount of information is available. These species will be used to demonstrate the annual patterns of incidence and intensity of occurrence. Maturation will be mentioned here, but is discussed more fully in Section VIII D. Eight species show an annual pattern of incidence and occurrence, and in addition of maturation. These species are : Allocreadium isoporum (Davies, E. H., 1967), Asymphylodora kubanicum (Mishra, 1966; Evans, N. A., 1978), Bunodera luciopercae (Lyaiman, 1940; Komarova, M. S., 1941; Androsova and Bauer, 1947; Malakhova, 1961; Rizvi, 1964; Mishra, 1966; Cannon, 1972; Wootten, 1973b; Andrews, 1977), B. sacculata (Cannon, 1972), Crepidostomum farionis (Awachie, 1968), C. isostomum (Elkins and Corkum, 1976), C. metoecus ( Davies, E. H., 1967; Awachie, 1968) and Sphaerostoma bramae (Malakhova, 1961; Rizvi, 1964; Davies, E. H., 1967). The pattern of occurrence has four recognizable components, which can overlap in time to a considerable extent: invasion (see Section VIII C), growth and maturation (see Section VIII D), accumulation of eggs and loss of gravid worms (also see Section VIIl D). The overall annual pattern of incidence and intensity is a dynamic process, which involves gain of worms from the intermediate host, maintenance of a population of worms in the definitive fish host and loss of both partially developed and gravid worms from the fishes. The dynamic aspects of these phases have been recognized especially well by Andrews (1977) for Bumdera luciopercae. The main invasion of Percafluviatilis commenced in July, when the incidence and intensity increased after the annual minimum. In this month there was little loss of juveniles. In August and September, incidence and intensity were high, and Andrews (1977) suggested that both gain of worms from the zooplankton intermediate hosts and loss of juvenile worms from the fishes intestines were high, which were made manifest as a constant intensity of infection. In October, plankton feeding decreased so that gain of worms fell, but the loss from the fishes continued, thus there was a marked fall in intensity. This level of intensity was maintained from November to February, and a reduced gain and loss was postulated. However, the loss of worms increased during April to July because of passing of gravid worms, so that both incidence and intensity declined even though there was a low gain of juvenile B. luciopercae (Andrews, 1977). Similar patterns of incidence and intensity are reported for some other species, and usually correlations have been noted between presence of the metacercariae in the intermediate host, feeding of the fishes on the intermediate host and the levels of incidence and intensity of occurrence in the fishes (see e.g. Awachie, 1968; Rumpus, 1975; Evans, N. A., 1978). Allocreadium fasciatusi was shown by Madhavi (1979) to have a main annual pattern of incidence and intensity of occurrence, even though smaller numbers of worms invaded and matured in the fish host without regard to K

TABLE5 A calendar of seasonaI events for some adult trematodes of freshwater fishes The species are in alphabetical order. The site of occurrence in the host and the last larval stage are shown. The periods of invasion of the fishes, of growth and maturation and presence of gravid worms are also given. The time of ending of a generation of worms is the point at which the last gravid worms were seen. The seasons listed are all for the northern hemisphere, but where possible months are used. Species

Site in host

Invasion

Growth and maturation

Acetodextra amiuri

Ovary

Metacercariae ? Time not known

During growth of host ovary

A Ilocreadium fasciatusi

Intestine

A Ilocreadium isoporum

Intestine

Metacercariae All year, with peak September Metacercariae September onwards May July-August Metacercariae March onwards

All year, but peak November to April

A Ilocreadium lobatum

Intestine

A Ilocreadium markewitschi Allocreadium transversale Asymphylodora kubanicum

Intestine Intestine Intestine

Metacercariae ? March-May Metacercariae September onwards Metacercariae From autumn, but especially spring and summer August-September

January to May

End of generation

Gravid

References

Eggs accumulated At time of host Perkins (1950, 1951, before host spawning 1956) spawning All year, but peak All year, but end Madhavi (1979) of main January to April generation April Dawes (1946) March to July June to August Davies, E. H. (1967)

May onwards June During winter Spring Progenetic development in amphipods November to February

June-July May-June

Halvorsen (1972) Koval’ (1952)

July

De Giusti (1962)

During summer

Autumn

November

Spring and summer Late summer and early autumn

Early autumn

Koval’ (1952) Dawes (1946) Davies, E. H. (1967) Evans, N. A. (1978) Evans, N. A. (1978)

February-April

July ?

July?

October-April

July

Mishra (1966)

May-July

Species Asymphylodora tincae

Azygia lucii

Bunodera luciopercae

Site in host

Invasion

Intestinal Metacercariae Autumn to spring

Stomach

Intestine

Growth and maturation Summer

End of generation

Gravid Autumn to spring

All year, but Rapid, occurred all All year increased autumn year to spring Cercariae, or via other fishes All year All year All year, peak May-June January-March March onwards October onwards Secondary invasion All year All year all year End June onward End June onward April-May Metacercariae During autumn Spring-summer All year, peak and winter July-October Spring-early During autumn August onward summer and winter Spring-early During autumn July-Augus t summer maximum and winter May-June September onward During autumn and winter March-June June onward During autumn and winter March-May August onward During autumn and winter

Spring All year

All year December-March All year May-June May-Jul y June

References Szidat (1943) Komarova, M. S. (1951b) Wierzbicka (1970) Odening and Bockhardt (1976) Halvorsen (1968, 1972) Markova (1958) Odening and Bockhardt (1976) Tell (1971) Wiiniewski (1958b) Andrews (1977)

June

Androsova and Bauer (1947) Cannon (1 972)

June

Halvorsen (1972)

June

Komarova, M. S. (1941) Kozicka (1959)

Probably May

TABLE 5 (continued) Species

Site in host

Invasion August onward

During autumn and winter September onward During autumn and winter July onward During autumn and winter July onward During autumn and winter August-March During autumn and winter November onward During winter

B. luciopercae (continued)

End June-July onward Late summer onward July onward Bunodera sacculata

Intestine

Metacercariae July-AuguSt

Crepidostomum cooperi

Intestine

Metacercariae Peak June to August August onward

Crepidostomum farionis

Growth and maturation

Intestine

Metacercariae August onward

End of generation

Gravid

d

References

March-May

May

Lyaiman (1940)

February-Jul y

June-Jul y

Malakhova (1963)

May

May

Mishra (1966)

March-June

June-July

Rizvi (1964)

Late spring-June

June

Skorping (1976)

July

During autumn and winter During autumn and winter During autumn and winter

April-May

May-June

Tedla and Fernando (1969) Tell (1971)

Spring

May-June

Wierzbicki (1970)

January-June

June

Wootten (1973b)

Within 3 weeks

Spring

May-Jul y

Within 3 weeks

No defined limit

No defined limit

During autumn and winter

Spring

Spring-Summer

During autumn and winter

March-May

May

~

Cannon (1 971, 1972) Hopkins (1934) Cannon (1972) McDaniel and Bailey (1974) Awachie (1968) Awachie (1968)

Species

Site in host

Invasion

Growth and maturation

September-May

March-May

August

Hoffman (1967) Elkins and Corkum (1976) Awachie (1968) Awachie (1968)

March-May

July

Davies, E. H. (1967)

Peak OctoberFebruary

Peak FebruaryMay

July

Bibby (1972)

July onward

All year, with peak April-May

June

Rumpus (1 975) Rumpus (1 975)

Summer-winter March onward

Spring-summer Grad ua1 oviposition to November

Summer November

Sten’ko (1976a,b) Komarova (195 1 a) Koval’ (1952)

Mature worms in November onward

February-June

At time of host spawning, February-June

All year

October-August

N o defined host

Sinitzin (1901) Chappell (1969)

June onward

Peak April-May

May-June

Tell (1 97 1)

Intestine

Metacercariae March-July

Crepidostomum metoecus

Intestine

Metacercariae November onwards NovemberFebruary October onwards NovemberFebruary

Intestine

Nicolla gallica

Intestine

Nicolla skrjabini

Intestine

Ovarionematobothrium texomensis

Ovary

Phyllodistomum folium

Urinary system

?

Summer, early autumn, early spring Metacercariae June onward Metacercariae Summer-autumn March-April ? ?

Metacercariae August peak, but all year June onward

References

March-January

Crepidostomum isostomum

Macrolecithus papilliger

End of generation

Gravid

March-July

Self et al. (1961, 1963)

TABLE 5 (continued) Species

Site in host

Invasion

Growth and maturation

Gravid

End of generation

References

Phy llodistomum lacustri

Urinary system

Metacercariae ? February-June

All year

All year

No defined limit

Phyllodistomum pearsei

Urinary system

Metacercariae? March-July

Spa11 and Summerfelt (1969)

June-November

October-June

Sanguinicola inermis

Blood vessels

Cercariae, 12°C and above Spring-au tumn

SeptemberNovember

Elkins and Corkum (1976) Naumova (1961b)

September

Luck9 (1964)

Sphaerostoma bramae

Intestine

Metacercariae October onward October onward

Overwinter to July-August following summer October-April Oct ober-M ay

September July-August

Szidat (1944) Davies, E. H. (1967) Evans, N. A. (1977a)

Transversotrema patialense

Under scales

February-July June-Jul y

September onward Overwinter April-June July onward December onward April-May Cercariae

June September

All year in experimental tanks at 2426°C

10 week maximum life span Anderson, R. M. et al. (1977)

Not given

Not given

Malakhova (1963) Rizvi (1964) Anderson, R. M. e f al. (1977)

HELMINTHS IN FRESHWATER FISHES

283

season. This main annual cycle was initiated by peak occurrence of the infected intermediate copepod hosts in September. An annual pattern of occurrence for Azygia lucii was found by Markova (1958) and Tell (1971), but the absence of an obvious pattern was reported by Halvorsen (1968, 1972) and Odening and Bockhardt (1976). Tell (1971) also found an annual pattern for Phyllodistomum folium, whereas Chappell(l969) did not. With Crepidostomum cooperi, Cannon (1972) observed peak occurrence during midsummer, but McDaniel and Bailey (1974) noted a pattern with peak incidence in February and minimal incidence in July. These observations show that patterns of occurrence and their timing can change within a species from one locality to another (see Section VlI). The species of host can also influence these patterns (see Section VIII B). Macrolecithus papilliger (Bibby, 1972) and Phyllodistomum pearsei (Elkins and Corkum, 1976) lacked clear seasonal patterns of incidence and intensity of occurrence, but had seasonal periodicity of maturation, which showed that in fact there were annual patterns of population turnover. In M.papi1liger invasion of fishes probably occurred in summer, early autumn and early spring (Bibby, 1972) and in P. pearsei from March to July (Elkins and Corkum, 1976). Some species not only lack clear seasonal patterns of incidence and intensity of occurrence, but also showed the presence of maturing and eggcontaining worms during the whole year. These include Asymphylodora tincae (Komarova, 1951b; Wierzbicka, 1970), Nicolla gallica (Rumpus, 1975), N . skrjabini (Komarova, M. S., 1951a), Phyllodistomum folium (Chappell, 1969) and P. lacustri (Spa11 and Summerfelt, 1969). It is evident, therefore, that there is a range of seasonal patterns of incidence and intensity of occurrence of trematodes in freshwater fishes. Each pattern reflects the synthesis of the requirements of the biology of the habitat, the intermediate and definitive hosts and the species of parasite. These patterns are dynamic in quality, and involve an equilibrium between gain of invasive larvae from the intermediate host and the loss of adults, gravid or not, from the fishes. Some studies of certain species of trematodes clearly reveal the dynamic relationships, whereas others do not. B.

PRINCIPAL AND AUXILIARY HOSTS

Davies, E. H. (1967) has observed some seasonal differences between hosts in the occurrence of infections of Allocreadium isoporum and Sphaerostoma bramae in the River Lugg, Herefordshire, England, during the same period of time. The principal hosts for A . isoporum were Leuciscus cephalus and L. leuciscus. In the auxiliary host, Rutilus rutilus, the worms were smaller. Incidence and intensity followed essentially similar patterns in the three hosts. However, there were differences in the times of maturation of the worms. Davies, E. H. (1967) recognized four stages of development, Stage I, parasites small, gonad rudiments present, without vitellaria, Stage 11, gonads well developed, vitellaria present, Stage 111, gonads and vitellaria well developed, eggs in uterus, and Stage IV, regression of gonads, but eggs still present.

284

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

I n L. cephalus and L. leuciscus (compared with R. rutilus, in parentheses) the main period of occurrence of each stage was; Stage I, August to November, predominant (October onwards), followed by loss of many in NovemberDecember (no loss of worms); Stage TI, predominant L. cephalus JanuaryFebruary and L. leuciscus January-April (January-May) ; Stage 111, MarchJune and July (May only); and Stage IV, L. cephalus June-August, L. leuciscus June-July (June-August). Thus in R. rutilus, Stage I did not appear until October, 2 months later than L. cephalus and L. leuciscus, Stage I1 persisted 1 month later, Stage I11 occurred in May only and Stage IV was more or less the only stage present from June to August, whereas Stage 111 persisted to July in L. leuciscus and August in L. cephalus. Further, there was no loss of worms in R . rutilus between November and December, when many were lost from L. cephalus and L. leuciscus. The difference in time of invasion of R. rutilus compared with L. cephalus or L. Ieuciscus could reflect either different feeding habits or a physiological barrier to worm establishment. The later occurrence of Stage I1 in R. rutilus could also be attributed to a physiological deficiency, as could the short time of occurrence (1 month) when Stage 111 worms were predominant. The principal host for Sphaerostoma bramae in the River Lugg was Rutilus rutilus, with Leuciscus cephalus and L. leuciscus as auxiliary hosts (Davies, E. H., 1967). Incidences and intensities of S. bramae were normally higher in R. rutilus than in the other two fishes. Some R . rutilus were infected every month of the year, whereas L. cephalus was not infected from June to October and L. leuciscus not infected in January, February, June-September, nor November. To assess maturation of S. bramae, Davies, E. H. (1967) used the same stages as those described above for Allocreadium isoporum. Stage I and I1 reappeared in October in R. rutilus, Stage I in November and December in L. cephalus, but Stage I1 not until January. Stage I l l predominated in April and May, and Stage IV from June to September in R. rutilus, but in L. cephalus Stage I11 predominated from February to May, with Stage IV in March; however, S. bramae was absent from this species of fish from June until November. As with A . isoporum in these hosts, ecological or physiological reasons for the differences can be postulated. This study by Davies, E. H. (1977) on the two species of trematodes in the three species of fishes at the same time and place, shows that differences of incidence and intensity of occurrence and of maturation of the worms occurred between the principal and axiliary hosts. The principal hosts had higher incidences for longer times, with higher intensities of worms and probably also provided more favourable conditions for maturation of these worms. C. INVASION OF FISHES Entry into the fish host can be achieved by direct penetration of cercariae or oral ingestion of metacercariae. Relatively few of the species discussed here (only six) invaded by means of cercariae, whereas 41 species have been recorded as having metacercariae.

HELMINTHS IN FRESHWATER FISHES

285

The species with cercariae are Azygia lucii, Sanguinicola armata, S. inermis, S. magnus, S. volgensis and Transversotrema patialense. A . lucii is interesting in that Esox lucius can become invaded either directly, as small fish up t o 3 cm long, by penetration of cercariae, or indirectly as larger fish, by eating infected fishes of the same or a different species. These alternative methods were designated primary and secondary by Odening and Bockhardt (1976), and only the first was seasonally limited as it affected fishes in their first year of life, because penetration by cercariae was possible only in these small E. lucius. The cercariae of Sanguinicola inermis are released from the mollusc host at temperatures above 12"C, and survive 48 h at 13"C, but only 22-29 h at 20°C (Naumova, 1976b). Invasion of Cyprinus carpio is thus limited to the time of the year when water temperatures are above 12"C, and is especially intense at the warmest periods (Scheuring, 1923; Bauer, 1959a; Chechina, 1959; Naumova, 1 9 6 1 ~Lucky, ; 1964; Sapozhnikov, 1976). Cercarial production by Transversotrema patialense under conditions of constant temperature and dark-light regimes has been studied by Anderson e f a/. (1977). There was a remarkable temporal constancy in daily cercarial emission by infected Melanoides tuberculata, the most important factor affecting output appeared to be the nutritional state of the snails, starvation causing cessation of production, although this was resumed once conditions were improved. The invasion of the fishes Brachydanio rerio was proportional to the density of cercariae present in the habitat and was a matter of chance contact between cercariae and fishes. Anderson et a/. (1977) considered that the life cycle of T. patialense contained many density-dependent population processes. The details of survival of the free-living cercariae were studied by Anderson and Whitfield (1975). The seasonal changes in cercarial production by T. patialense in the natural tropical conditions where it occurs have not been studied, so that it is not known whether or not there are variations. As noted above, the majority of species of trematodes considered here have metacercariae, therefore invasion of fishes is normally achieved by ingestion of these with food. It is noteworthy that in Sphaerostoma bratnae Chernogorenko-Bidulina and Bliznyuk (1960) found a variety of larval forms in the snail host, including short-tailed, tailless and encysted cercariae, as well as in one snail a sexually mature form of S. bramae and numerous eggs containing developed miracidia. They postulated that the life cycle of S. bramae could involve alternative pathways, via only an intermediate mollusc host, or a first intermediate mollusc and a second intermediate leech host, or a first and second intermediate mollusc host of the same species. Progenesis is reported for a number of species, S. bramae above, but also Allocreadium lobatum (De Giusti, 1962), a species of Alloglossidium (Beckerdite, 1974), Asymphylodoru demeli (Vaes, 1974), and others (see Erasmus, 1972). The significance of progenesis for the phylogeny of the digeneans has been discussed by Stunkard (1959). In the context of seasonal occurrence of trematodes in fishes, these variations may provide alternative pathways, thereby increasing the possibility or prolonging the season of invasion (see also Section V C, Diplostomum spathaceum precocious meta-

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cercariae). The complex variations possible in the Iife cycles of the digenean trematodes have been reviewed by Heyneman (1960). The times of acquisition by fishes of metacercariae are summarized in Table 5. It is apparent that if metacercariae are present in the intermediate host, and that host is available to the fishes, then an infection can occur at any time of the year. Such a situation has been seen in Allocreadium fasciatusi by Madhavi (1979) and in Bunodera luciopercae by Andrews (1977). However, most of the species shown in Table 5 have a more limited, although often lengthy, season of invasion. It is noteworthy that the presence of metacercariae in a life cycle frequently allows the process of invasion of the fishes to continue through the cold seasons of the year, when cercariae are not normally liberated. The metacercariae may themselves have a seasonal pattern of development and occurrence. These patterns have been reported for Allocreadium lobatum (De Giusti, 1962), Asymphylodora kubanicum (Evans, N. A., 1978), Crepidostomum cooperi (Hopkins, 1934), C . farionis, C . metoecus (Awachie, 1963, 1968) and Nicolla gallica (Rumpus, 1973). A number of authors have attempted to relate the annual feeding habits of the host fishes to invasion by the trematode metacercariae. Examples are Andrews (1977) for Bunodera luciopercae in Perca JEuviatilis, Cannon (1973) for B. sacculata and Crepidostomum cooperi in P . JEavescens and Evans, N. A. (1978) for Asymphylodora kubanicum in Rutilus rutilus. Such studies can be extremely informative with respect to the distribution of the trematodes through the host population. Evans, N. A. (1978), for instance, showed that R. rutilus were infected by A . kubanicum from their third year onward, when the infected molluscs became a dominant item of diet, and older fishes were more heavily infected because of their greater consumption of molluscs per individual. D.

MATURATION OF TREMATODES

It is clear from the observations reported in Section VI that frequently seasonal maturation of the adult trematodes occurs in fishes. A summary is provided for some of these species in Table 5. Once invasion of the host is achieved, it is followed by growth, development of the genital organs, spermatogenesis, oogenesis, fertilization and egg production and liberation, or accumulation until gravid, according to species. The details of gametogenesis have been studied by Perkins (1956) for Acetodextra amiuri. The stages were : spermatogenesis-primary spermatogonia, secondary spermatogonia, tertiary spermatogonia, primary spermatocytes, secondary spermatocytes, spermatids, spermatozoa; oogenesisoogonia, primary oocytes, secondary oocytes, pronuclei and fertilization. In order to relate the stage of development of the worms to the time of the year, a number of authors have differentiated stages suitable for the particular species they studied. These stages serve to describe, as a series of discrete steps, the status achieved in the continuous process of development at a particular time. These stages in some instances may be no more than

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a division of the worms found into those without compared with those with eggs, but associated with measurement of worm length (Rizvi, 1964Sphaerostoma brarnae), or a count of the number of eggs carried in the uterus (Lyaiman, 1940-Bunodera Zuciopercae). Bibby (1972) recognized three stages for Macrolecithus papilliger, immature, no spermatozoa present; mature, spermatozoa in seminal receptacle; and gravid, with eggs in the uterus, and Evans, N. A. (1977a, 1978) three similar stages for Sphaerostoma brarnae and Asyrnphylodora kubanicum, immature, vitellaria absent, no eggs in the uterus; mature, vitellaria present, no eggs in the uterus; gravid, vitellaria present, eggs in the uterus. Davies, E. H. (1967) separated four stages for studies of Allocreadium isoporum, A. transversale, Crepidostomum metoecus and Sphaerostoma bramae. They were Stage I, parasites small, with gonad rudiments, vitellaria absent; Stage 11, gonads well developed, vitellaria present; Stage 111, gonads and vitellaria functional, eggs in uterus; and Stage IV, regression of gonads, eggs still in uterus. A similar number of stages was used by Elkins and Corkum (1976) for Crepidostomum isostornum, Phase A, slight genital development, testes not clearly defined, ovarian complex undifferentiated; Phase B, genitalia well-stained structures, spermatozoa present, but no vitelline function or eggs; Phase C, male and female genitalia functional, five or fewer eggs in uterus, none liberated when living worms placed in saline; and Phase D, more than five eggs in uterus, eggs shed when worms placed in saline. Wootten (1973b) used a five-stage scheme for Bunodera luciopercae, Stage I, juvenile worms, vitellaria not developed; Stage 11, immature worms, gonads full size, vitellaria starting to develop; Stage 111, maturing worms, vitellaria developing; Stage IV, mature worms, gonads and vitellaria fully developed; and Stage V, gravid worms, eggs in uterus. A modified version of this scheme was also used by Andrews (1977) for Bunodera luciopercae. The most complex assessments of developmental stages are those of Elkins and Corkum (1976) and Malakhova (1963) which recognize six stages of development. Elkins and Corkum (1976) studied Phyllodistomurn pearsei; the stages were: Phase A, no genital development; Phase B, testis rudiments and paired vitellaria visible; Phase C, fully differentiated male and female genitalia, no eggs in uterus; Phase D, tanned eggs in uterus, but none anterior to ventral sucker; Phase E, eggs fill uterus in hind body and anterior to ventral sucker, shed eggs readily; and Phase F, regression of testes, failure to stain and smaller in size. Malakhova (1963) studied Bunodera Iuciopercae (see Fig. 5 ) and Sphaerostoma bramae, and her stages were: Stage I, juvenile, with ovary and testis rudiments; Stage 11, cirrus and vitellaria appear; Stage 111, genitalia fully developed, vitellaria functional ; Stage IV, a small number of eggs present; Stage V, eggs numerous; and Stage VI, gravid, eggs fill uterus. It can be seen that these two systems have similar Stages I-IV, but vary somewhat in Stages V and VI, owing to differences in the mode of egg liberation. P. pearsei probably releases its egg from the uterus when they are mature over a period of time, whereas gravid B. luciopercae probably are passed whole into the habitat still packed with eggs where the worms disintegrate to release the eggs. In addition to using the stages described above

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Malakhova (1963) also provided measurements of the worms and their genitalia, month by month. These attempts to relate the sexual maturation of the worms to the time of the year have been described in some detail because if used more widely they would provide much useful additional information. The six-stage schemes of Malakhova (1963) and Elkins and Corkum (1976) are the best, and can probably be applied to the development of the majority of fish trematodes. If one of the stages cannot be separated from the next with a particular species of worm, then rather than applying a scheme with fewer stages, it would assist comparability of data if these combined stages were expressed as, for example, Stage V-VI. It is relevant to note at this point that in some species of trematodes, for instance Phyllodistomum pearsei (Elkins and Corkum, 1976), immature and mature worms were never collected from the same host individual. A mixture of immature, mature and gravid worms are normally together at the appropriate season in one host individual in most species of fish trematodes. The times of maturation where determined have been given in Section VI and are summarized for some species in Table 5. The species can be divided into three broad divisions : those maturing over the winter in mid-latitude climates, or at the coolest time of the year in subtropical and tropical conditions, and liberating their eggs spring and early summer; those maturing in summer, or the warm season, and liberating their eggs in summer and autumn; and those that appear to be capable of maturation, and perhaps egg liberation, without regard to season. The intraspecific and specific variations possible have already been considered in relation to world climate zones in Section VII, especially Section VII F. However, three species will be taken here as examples of the divisions stated above, Bunodera luciopercae, Asymphylodora kubanicum and A . tincae. Bunodera luciopercae (see Section VI C) matures during the winter months, is gravid by spring, and releases its eggs in the early summer. It is important to note that growth in size, maturation of genitalia and the commencement of egg accumulation all occur during the cold months of the year. The reasons have not been determined. Andrews (1977) attempted some experiments using Perca Jluviatilis maintained in the following conditions: all had 16 hours light, 8 hours dark each day. Four groups of fishes previously unexposed to B. luciopercae were infected by transplant of worms from naturally infected P.Jluviatilis to the experimental fishes. The temperature conditions used were: constant cool 6"C, constant warm 16-20°C, the natural environmental range as a control, and finally, constant cool for 43 days at 6"C, followed by constant warm at 20°C for the remainder of the experiment. At the natural environmental range of temperatures, representing normal overwinter conditions in the British Isles, Stage V (gravid) worms were recovered. on examination of the fishes on day 165 (5t months, normal development). In the constant cool conditions Stages IV and V were recovered on day 158; in the constant warm conditions on day 83 Stage I1 and I11 worms were found, but on days 130 and 165 no worms were recovered. In the constant cool followed by constant warm conditions on day 100 (43 days cool,

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57 warm) Stage I1 and IT1 worms were found, but on days 135 and 170 no worms were recovered. These interesting and timely experiments carried out by Andrews (1977) show that in constant low temperatures normal gravid worms were produced in the same time as that found in natural environmental conditions. However, in warm conditions, or cold of short duration followed by warm, the B. luciopercae only reached Stages I1 and 111 (vitellaria developing, but no egg formation), and then apparently were lost from the host. Andrews (1977) postulated that an extended period of vernalization was necessary for normal development and maturation to occur. Asymphylodora kubanicum is a species in which the majority of the population invades, grows and matures during spring and summer, to release eggs during late summer and early autumn. The majority of the worms are lost from the host fish, Rutilus rutilus, by early autumn (Evans, N. A., 1978). It would be interesting to conduct a series of experiments on this parasite to determine its precise temperature requirements. Asymphylodora tincae is present in its host, Tinca tinca, during all times of the year, and gravid worms are also seen throughout (Wierzbicka, 1970). It is clear that rapid growth and maturation of A . tincae is possible, as Wierzbicka (1970) observed fully adult parasites in fry in the autumn. Despite its occurrence as gravid worms during winter, Komarova, M. S. (1957) stated that they were hardly mobile during the winter and that maturation was slowed down. Again, it would be extremely interesting to carry out experiments to determine the precise temperature requirements of this species. It is clear that temperature has a marked relationship with the growth, maturation and loss of gravid worms from the host fishes. Three more experimental examples are quoted: the establishment of Rhipidocotyle septpapillata in Lepomis gibbosus at low and high temperatures, where at 7°C they matured in 10-12 days, remained in the fishes for 30 days to produce eggs containing miracidia, but at summer temperatures (up to 37°C) they matured in 5-7 days and were then eliminated (Krull, 1934b); the egg release by Phyllodistomum folium in Gasterosteus aculeatus, where summer laying rates exceeded those of the winter (Johnston, J. M., 1967); and the rapid elimination of Bunodera luciopercae from Perca jlavescens during a period of 11-20 days at both 20" and 25°C (Cannon, 1972). Cannon (1972) speculated that the correlation between temperature and incidence of gravid adult Bunodera species presumably allowed egg dispersion at a time most favourable for a continuation of the cycle. Moravec (1969) and Cannon (1971) demonstrated that the parasite development in the pisidia took 1 year, and as the mollusc host lived for only 1 year, such a coordination was necessary to ensure infection of the pisidia shortly after birth. As Cannon (1971) also showed that B. luciupercae did not lay eggs but had them ruptured from its body after it left the fish, a temperature stimulus was the simplest explanation, although it was possible that the gravid worms disappeared in relation to thermal summation above some threshold. However, high temperatures per se were not detrimental to the species, as juveniles invaded P . jlavescens in July and August, the warmest time of the year (Cannon, 1972).

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E.

ABIOTIC FACTORS

Although abiotic factors clearly influence the distribution of fish trematodes, factors such as the amount of light entering the water, the depth, hydrogen ion concentration (pH), oxygen content and salinity (see Bauer, 1959a for discussion) do not appear to influence the seasonal occurrence or development of these parasites. Voth et al. (1974) related seasonal incidence of Crepidostomum farionis to water flow in the South Platte River, Colorado, U.S.A., but in fact the pattern shown was as normally found elsewhere, and probably the low summer incidence was attributable to high temperatures rather than high water flow. As has been discussed at length in Section VIII D and elsewhere, water temperature is clearly very important in the maturation of adult trematodes. It is also a vital factor in the development of trematodes in the molluscan host and for the release of cercariae (Section V C ) . Both field and experimental observations suggest that each species of trematode has an optimum temperature range at which the life processes occur with maximal efficiency for survival and reproduction of the species. It is also clear that certain vital stages of transmission may be activated by some form of temperature control. Such control by temperature is likely to provide the vital synchronization of the life cycles of parasite, definitive and intermediate hosts. F.

BIOTIC FACTORS

Biotic factors must influence the life of any species, and the effects of host feeding patterns in relation to seasonal occurrence of trematodes have been noted in Section VIII C . Other factors of fish biology must also be considered. The densities of the fish populations will affect numerical occurrence of the parasites, but have not been reported as causing modification of the maturation cycles of the trematodes. Reproductive behaviour of the fishes is of vital importance for the distribution of trematodes living in the host ovarian tissues. The life cycles of Acetodextra amiuri and Ovarionematobothrium taxomensis are closely bound to the ovarian cycle of the host, and rely on the spawning of the fishes for the liberation and dispersal of their eggs (Perkins, 1956; Self et al., 1963). Although the details are not available, the migratory movements of the fish Hilsa ilisha are likely to be significant in the seasonal patterns of occurrence of Aphanurus monolecithus, Lecithaster extralobus, L. indicus and Orientophorus brevichrus. Pal (1963) stated that invasion of H. ilisha by A . monlecithus occurred in the marine zone of the River Hooghly, India, and 0. brevichrus had the highest incidences in the marine (59 %) and gradient (92 %) zones of the river, rather than the freshwater zone (25 %). Rumpus (1975) observed that maturing and gravid female hosts, Cottus gobio, showed a higher level of infection by Nicolla gallica. The evidence suggested that this was due to the retention of worms already established for a longer period than by fishes in a non-reproductive condition. A similar

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29 1

occurrence was seen by Thomas (1964) for Phyllodistomum simile in SaZmo trutta, and he considered that this retention was an effect of the overall physiological condition of the host, rather than a direct hormonal response. Rumpus (1975) was unable to explain the precise manner in which the reproductive condition of C. gobio affected the population of N . gallica. However, other authors, for instance Evans, N. A. (1978) for Asymphylodora kubanicum in Rutilus rutilus, have specifically noted that the sex of the fish made no difference to the occurrence of the parasites. Szidat (1956, 1958) has suggested that a host hormonal effect influenced the development of the trematode Genarchella genarchella. The whole life cycle can be completed in the snail Littoridina australis, and the passage through the definitive fish host, Salminus maxillosus, was no longer obligatory. Szidat (1956, 1958) postulated that the shortened life cycle was due to the effect of thyroid and hypophysis hormones produced in excess by cypriniform fishes when they adapted from sea to freshwater in an earlier geological era. However, Bauer (1959a) has noted that although the hormonal state of the fish may be a highly significant factor in fish parasite biology, it has been studied very little. More recently, Kennedy (1975b) has discussed hormonal control of parasite life cycles in general. As far as the author is aware, no immunological responses of fishes affecting the seasonal occurrence of trematodes have been reported. Anderson, D. P. (1974) has presented an extensive account of fish immunology but makes no reference to adult trematodes in fishes. Vernberg (1961) and Vernberg and Vernberg (1966, 1974) investigated thermal and other metabolic parameters of marine trematodes and their hosts. They reviewed (Vernberg and Vernberg, 1974) the physiological adaptations to the various environmental conditions encountered at each stage in the life history, and suggested that the thermal tolerances of the adult trematodes agreed very closely with the respective hosts. That such is true for adult freshwater trematodes and their respective hosts is perhaps shown by the essentially similar thermal preferences of Crepidosromum farionis and C. metoecus, as postulated by Awachie (1963, 1968) and those of Salmo trutta, as discussed by Varley (1967). The general topics of the dynamic aspects of parasite population biology (see Anderson, R. M., 1976) and of the regulation of fish parasite populations (see Kennedy, 1977) must of course always be kept in mind with respect to seasonal occurrence of parasites, because it is only one aspect of the biology of the host-parasite relationship as a whole. G.

LONG-TERM POPULATION CHANGES

It is unusual for an investigation of seasonal occurrence of parasites to be continued for more than 2 years or so. Hence, longer-term variations of seasonality are rarely reported. However, Campbell (1974) has studied Bunodera luciopercae in PercaJEuviatilis in Loch Leven, Scotland, from April 1967 through to March 1972. Campbell (1974) provided data (his Textfigure 5) for incidence for these years, with the exception of 1968. Several

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facts are apparent. An increasing incidence was found during the following months of each year: 1967, July to December; 1969, July to December and through to April 1970, and July to October 1970; and 1971, July to October. A 100% incidence of occurrence was seen: 1967, May-June, December; i969, March-May; 1970, April, October-December; 1971, FebruaryMay, October-December and through to March 1972 (end of study). A decline in incidence was seen: 1967, May-July; 1969, May-July; 1970, MayJune; and 1971, May-July. The minimum incidences each year, estimated from Text-figure 5 (Campbell, 1974, p. 358), were: 1967, July 38%, 1969, July 5 %; 1970 June-July 0; and 1971 July 10%. Thus small changes of timing of the periods of increasing incidence, representing rate of invasion, of maximum incidence, showing peak population levels, and of decreasing incidence, representing rate of loss of the gravid worms, were seen from year to year. In addition, the summer minimal population levels varied quite markedly, from 37 % to 0 %. These variations are of course consistent within the range reported for the species (see Section VI C ) , but show clearly that some year to year modifications do occur as would be expected from a response to variable weather conditions. H.

SEASONAL STUDIES I N WORLD CLIMATIC ZONES

Seasonal studies in relation to world climatic zones were discussed at length in Section VII. It was seen that there were very few studies in tropical conditions, but the interesting investigation of Allocreadium fasciatusi at Waltair, India, by Madhavi (1979) most clearly demonstrated that seasonal variation of fish trematodes parasites is not confined to the mid-latitude climates. I t is to be hoped that many more investigations of this nature will be undertaken in tropical climates. In the tropics, four species have been investigated, in the subtropics 10 species and in mid-latitude climates about 46 species. I.

AN HYPOTHESIS FOR SEASONAL OCCURRENCE

Owing to the great variation of patterns of seasonal occurrence of adult trematodes in freshwater fishes, it is difficult to produce a simple hypothesis that will be applicable to all, none the less it is possible to identify some of the component factors involved. This is attempted by reference to the one species, Crepidostomum metoecus, which was studied in a small river, the Afon Terrig, Wales, by Awachie (1963, 1968). Owing to the smallness of the habitat, which facilitated sampling, Awachie was able to study the dynamics of the interrelationships between the water temperature, occurrence of the parasite in the snail first intermediate host Lymnaea peregra, the shrimp second intermediate host Gammarus pulex and the fish definitive host Salmo trutta. It is noteworthy that these studies in the three hosts were carried out concurrently in the field, and were supported by experimental work in the laboratory. A seasonal flow diagram (Fig. 7) represents the annual progression of the life cycle in the stream in the three host species. I t should be stated that the

-

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kite diagrams attempt to show relative abundance within each stage, month by month, but for precise figures, where available, the original works of Awachie (1963, 1968) must be consulted. Host species Free - l i v i n g

Stage of parasite development Eggs of trematode in river

Invasion of snails. establishment

Intermediate

LvmnQeo p e r e w

Development of cercariae Emerqsnce of cercarioe

Free - l i v i n g

,,

A

-

+

+

*

3

8 - 17 OC

Cercariae in river Invasion of shrimps, establishment

nd intermediate

3

7

Grawth of rediae

Month

*

3

Miracidia in river

Is'

A

-

c

Growth of metocercarroe

Garnrnarus pulex

Definitive

Safmo lrulfa

FIG. 7. A seasonal calendar for the life cycle of Crepidustomcim metuecw in the Afon Terrig, Wales. [The data are reproduced from Awachie (1963, 1968).] See pp. 292-294 for a full explanation. The kite diagrams show relative abundance within the stage.

It is convenient to start with the eggs passed from the worms into the river. Egg release was estimated to occur mainly from April to July, but a few probably persisted a little longer. Thus it can be assumed that eggs were present in the river during this period, and that miracidia hatched and invaded the snail host Lymnaea peregra. The optimum conditions for this process have not been determined, but it is likely that the higher water temperatures of the summer months were significant. These same higher temperatures were also likely to favour the establishment of the infection, and the growth of the readiae in the snails. The details and duration of growth of the rediae have not been determined. However, cercarial formation probably commenced before May, when the snails harboured rediae containing cercariae

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in all stages of development. By June, only a few cercariae were being shed, whereas in July to October, snails kept at stream temperature in the laboratory liberated hundreds, but by December again only a few cercariae were released. Cercariae emerged at 8 to 17"C, but most left the snails at the higher temperatures. The cercariae survived for 4, maximum 5 days at 8°C. It is clear that the optimum conditions for cercarial production and release occurred during the warmer months of the summer. The invasion and establishment of the cercariae can be predicted to have occurred from June to December with a peak in August and September, as shown by the liberation of cercariae and the increasing incidence of metacercariae in shrimps during this time. The period of swarming of the cercariae corresponded with the presence in the stream of the largest possible population of young G. pulex (Hynes, 1955), which showed the correlation of life cycles of parasite and second intermediate host. The metacercariae showed increasing incidence in G. pulex from July to September, the incidence then gradually declined to January, to fall dramatically in February and then it declined to its lowest level in May to June. The metacercariae required some 2-3 months to become invasive to the fishes, although Awachie (1963) did not confirm this experimentally. Gammarus pulex in the Afon Terrig formed an important component of the food of Salmo trutta all the year round (Awachie, 1963), but it was observed that metacercariae appeared to be unable to establish in the fishes in a water temperature above 10°C. Thus newly established worms were not recovered until about November. Growth and maturation followed, the first eggs within the uterus were seen in December, but by February most worms contained eggs. In June the eggs were seen to be fewer and disintegration of the internal organs of the remaining C. metoecus had started. From then to October, worms were either not found, or if present, appeared to be empty and dying. The major drop in intensity of occurrence of the worms in S. trutta was in May when water temperature reached 10°C once more. The main period of egg release was estimated as April to July, which completed the cycle. The death of the generation of adult worms reach a peak in May, despite a few persisting through the summer to the autumn. It can be seen from the above account that different parameters apply at each stage in the life cycle. It was also evident that temperature can operate in different ways throughout the life cycle. In the instance of Crepidostomum metoecus the optimum conditions for larval development in the intermediate hosts were at higher temperatures, 10-17"C, but for establishment, growth, maturation and egg production in the fish definitive host below 10°C. The exact mechanism of temperature control remains to be determined, but the causal relationship is clear. The overall effect of environmental temperature was that of the synchronization of the life cycles of the intermediate and definitive hosts with that of the parasite. Thus a cold spring will delay all, or a warm spring speed, the progress of all the cycles. If temperature optima are used to explain, in part, the phenomena of seasonal occurrence of adult trematodes in fishes in mid-latitude climates, then of the three examples discussed in Section VIII D, Bunodera luciopercae

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has a low temperature optimum, Asymphylodora kubanicum a high temperature optimum and A . tincae will develop over a wide range of temperatures. The experiments of Andrews (1977) discussed in Section VIII D go some way towards confirming a low temperature requirement for B. luciopercae. However, temperature requirements are only part of the story, for, as Madhavi (1979) has shown for Allocreadium fasciatusi, temperature was not a significant factor. Never the less, a peak seasonal pattern of incidence, growth, maturation and egg production was found in the fishes, initiated by a peak seasonal incidence of metacercariae in the copepod second intermediate hosts. In this example, it appears to be the interaction of the life cycles of the mollusc, copepod and fish hosts with the life cycle of the parasite that determined the major seasonal pattern of occurrence of the adult worms. These ideas of interaction of life cycles and water temperature are not new. Ginetsinskaya (1958) wrote: “In fish helminths with annual life cycles the period of intensive reproduction frequently coincides with the seasons during which great numbers of planktonic and benthic invertebrates appear in the water. This enhances the chances of contact between the eggs and larvae of parasites with their intermediate hosts and the infestation of the latter. Such coincidence is well noticeable in the life cycles of the trematodes: Coitocoecum skrjabini,” Bunodera luciopercae, etc. (Komarova, 1951 ;t Lyaiman, 1940). The temperature of the water is a major determining factor in this context, since it regulates both the period of the peak reproduction of plankton and benthos and the development of the parasites within their intermediate hosts. The times of the reproductive seasons of parasites may vary, depending on the annual fluctuations of temperature and the seasons of greatest development of the vertebrate fauna. This has been demonstrated for Bunodera luciopercae by Bauer and Androsova (1947).” (Ginetsinskaya, 1958.) J.

EXPERIMENTAL STUDIES IN CONTROLLED CONDITIONS

A number of experimental observations have been described in the body of this review. However, more are urgently needed in carefully controlled conditions in order to identify the exact factors responsible for the various phenomena which are observed. The recent studies on the biology of Transrersotrema patialense by Anderson, R. M. and Whitfield (1975), Anderson, R. M. et al. (1977) and Mills (1976) serve to emphasize this point. These authors have examined the effect of age and density-dependence and water temperature on the survival and fecundity of the adult parasites. This trematode is a species that can be maintained easily in the laboratory through all stages of its life cycle and it is therefore an ideal laboratory model. Most other species are perhaps less convenient to work with, but nevertheless experimental work is possible. For instance, Andrews (1977) was able to utilize Bunodera luciopercae. In order to start with known intensities of infection in the experimental fishes,

* Nicolla skrjabini in this review. t Komarova (1951a) in the references in this review.

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he used the technique of transplantation of juvenile adult worms from fishes obtained from natural populations. The utilization of this technique should greatly facilitate experimentation on the factors involved in the seasonal patterns of occurrence of adult trematodes in fishes. ACKNOWLEDGEMENTS

I am grateful to Professor 0. N. Bauer, Zoological Institute, Academy of Sciences, Leningrad for his continued assistance in recommending relevant Russian literature. D r C. R. Andrews, Scientific Service, Yorkshire Water Authority, Leeds and D r R. Madhavi, Department of Zoology, Andhra University, Waltair, India have kindly allowed me t o quote from their recent studies which were in process of publication. I also wish t o thank Miss S. Tysoe, Harold Cohen Library, University of Liverpool who went t o great trouble t o assist with my very large number of inter-library loan applications. Mrs Helen J. Hart, Librarian, Commonwealth Institute of Helminthology, St Albans also provided invaluable assistance with the literature. I a m pleased to acknowledge the speed and efficiency of Miss D. S. Paterson and Miss A. Callaghan of the Department of Zoology, University of Liverpool who typed the manuscript. Three figures are reproduced from other sources, by kind permission of the authors and publishers: Fig. 1, D r R. A. Sweeting, Thames Water Authority, Reading and Cambridge University Press, London; Fig. 4, D r E. H. Davies, North East London Polytechnic, London; and Fig. 5 , D r R. P. Malakhova, Karelian Branch of the Academy of Sciences of the U.S.S.R., Petrozavodsk and Izdatel’stvo “Nauka”, Moscow. REFERENCES Anderson, D. P. (1974). “Diseases of fishes. Book 4: Fish immunology” (S. F. Snieszko and H. R. Axelrod, eds.), pp. 1-239. T. F. H. Publications, Neptune. Anderson, R. M. (1976). Dynamic aspects of parasite population ecology. In “Ecological aspects of parasitology” (C. R. Kennedy, ed.), pp. 43 1462. NorthHolland, Amsterdam. Anderson, R. M. and Whitfield, P. J. (1975). Survival characteristics of the freeliving cercarial population of the ectoparasitic digenean Transversotrema patialensis (Soparkar, 1924). Parasitology 70, 295-310. Anderson, R. M., Whitfield, P. J. and Mills, C. A. (1977). An experimental study of the population dynamics of an ectoparasitic digenean, Transversotremapatialense: the cercarial and adult stages. Journal of Animal Ecology 46, 555-580. Andrews, C. R. (1977). “The biology of the parasite fauna of perch (Percafluviatilis L.) from Llyn Tegid, North Wales.” Ph.D. thesis, University of Liverpool. Androsova, E. I. and Bauer, 0. N. (1947). (Developmental characteristics of Bunodeva luciopercae in the far north.) TrudJ Instituta Zoologii, Akademiya Nairk Ukrainskoi SSR Zbirnik Prats’ z Parazitologii No. 1, 149-151. (In Russian). Aristanov, E. (1970). (The effect of ecological factors on infestation of molluscs with trematode larvae in waters of the Amu-Darya delta.) Parazitologiya 4, 210-218. (In Russian.)

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