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Studies on the biosystematics and biology of strigeids (Digenea) parasitic in freshwater fish

This study is concerned with two strigeid genera which utilise fish as their second intermediate host and piscivorous birds as a definitive host, i.e. Apatemon (Apatemon) Sudarikov, 1959 and Ichthyocotylurus Odening, 1969. Although the lifecycle has been ascertained for most Ichthyocotylurus spp., confusion and disagreement still exist as to the constituent species, while all of the life-stages have been described for only a single member of the subgenus Apatemon (Apatemon). In order to clarify species membership to these taxa and indeed the taxonomic position of the subgenus Apatemon (Apatemon) further information was required on the life-cycles and life-stages of these strigeids. Although, metacercariae from this family have been recorded from a variety of British fishes, confirmed records, i.e. those supported with life-cycle data, are limited to a single species. It was this lack of confidence in identifying metacercariae recovered from fishes and the lack of known good criteria for distinguishing the adults that prompted the present study. Collections of metacercariae from a variety of hosts and locations were made, from which all subsequent life-cycle stages were obtained. The project aims were to establish the identity of the forms occurring in British fishes, by applying discriminatory techniques to the experimentally reared life-stages. In addition to traditional methods, techniques with little previous application to these genera were used and included, scanning electron microscopy (SEM), chaetotaxy, principal components analysis (PCA), and karyology. Furthermore, behavioural aspects such as the release patterns of cercariae from their molluscan hosts were studied to investigate whether they would prove to be of diagnostic value. Metacercariae obtained from the sampling survey were tentatively identified, using all currently employed methods for their determination, i.e. morphology, nature of cyst, host and site specificities, as Ichthyocotylurus erraticus (Rudolphi, 1809), I. variegatus (Creplin, 1825), Apatemon gracilis (Rudolphi, 1819) and A. annuligerum (Nordmann, 1832). Material collected from Finland was considered to contain both Ichthyocotylurus spp. recovered in the U.K., as well as I. platycephalus (Creplin, 1825) and I. pileatus (Rudolphi, 1802). The Ichthyocotylurus spp. were found to be more host specific than A. gracilis, although A. annuligerum was considered oioxenic to perch Perea fluiatilis L. Records of I. erraticus from gwyniad Coregonus lavaretus (L.) and grayling Thymallus thymallus (L.), and A. gracilis from arctic charr Salvelinus alpinus (L.) constitute first listings from Britain. The large number of sensilla present on the body surface of these metacercariae, observed by SEM and chaetotaxy, precluded their diagnostic use. PCA was, however, found to be of value for distinguishing between species and determining morphological variation within a species. I. erraticus, I. variegatus and A. gracilis adults were successfully reared in experimental hosts using metacercariae from a variety of fish hosts, sites within a single fish host and geographical sites. The adults obtained enabled clarification of the identities assigned to the metacercariae. Those metacercariae believed to represent I. pileatus and A. annuligerum failed to establish in experimental hosts. Herring gulls and lesser black-backed gulls proved to be extremely good experimental hosts for both Ichthyocotylurus spp., with the vast majority of infections establishing and providing high yields of eggs and adults. These infections yielded information on the establishment, development, fecundity, site specificity, longevity and morphological variability of the adults. Aspects of the morphology and biology of I. variegatus adults recorded were found to support its validity as a species discrete from I. platycephalus which was in some doubt. The experimental hosts used for A. gracilis infections, domestic and mallard ducklings, were found to be less satisfactory. Challenges were performed with A. gracilis metacercariae from three sources, rainbow trout, salmon parr and stone loach. The latter source was the only one to result in egg producing adults, with specimens exhibiting normal morphology and demonstrating an increased longevity over adults raised from salmonid metacercariae. These findings suggest that the metacercarial host may affect the successful completion of the life-cycle. Eggs of known origin were collected for all three cultured strigeid species, enabling further life-cycle studies, these were incubated and miracidia successfully raised. Developmental periods were found to be temperature dependent and differed for the three species at 20°C: A. gracilis < I. erraticus < I. variegatus. Light microscopy revealed the morphology of all three species to be identical, as were the epidermal plate formulae and chaetotaxy, indicated by silver-staining. The nomenclature for the distribution of miracidial sensilla derived by Dimitrov et al. (1989) was amended to enable a full description of these species. Osmotic shock resulted in an improved deciliation of the miracidia compared to sonication and subsequent SEM observation confirmed the arrangement of body surface structures, while revealing sensilla forms. Behavioural aspects of I. variegatus miracidia were examined, with a maximum longevity (< 11 hours) recorded at the lowest temperature studied (l0 degrees C), and host finding demonstrated to occur by an increased turning response in the presence of substances emitted from the susceptible snail host, following an initial unresponsive dispersal phase. Ichthyocotylurus cercariae were found in naturally infected Valvata piscinalis which constitutes the first record in Britain of cercariae of this genus. Cercariae of I. erraticus and I. variegatus were successfully raised experimentally from miracidia of known identity and origin within naive, experimentally raised V. piscinalis hosts, while A. gracilis cercariae were obtained from laboratory reared Lymnaea peregra. Cercarial developmental periods within the molluscan host were found to be temperature dependent and markedly different for the strigeid genera investigated, as were their behaviour and morphology. The Ichthyocotylurus spp. exhibit a distinct diurnal emergence rhythm from their molluscan host, being shed during the hours of daylight, while A. gracilis cercariae demonstrate a reciprocal pattern, emerging during the hours of darkness. Behavioural contrasts were also observed in longevities, emergence strategies (route of exit) and swimming behaviour. The two Ichthyocotylurus spp. were extremely similar, the only cercarial features found to be of diagnostic use were: the presence or absence of eye-spots; their differing developmental periods from miracidium to cercaria; the number and distribution of sensilla when compared by PCA; and their differing longevities at 20 degrees C. Characters considered to be of value in differentiating between strigeid cercariae at the species level, including the armature, chaetotaxy pattern and resting posture, did not differ between these two species. SEM observations enabled descriptions of the variety and structure of sensilla present on different life-stages, while transmission electron microscopy revealed the internal structure of cercarial sensory structures. Experimentally raised cercariae were found to be infective and the life-cycle was completed for the three strigeid species. Host specificities were observed for I. erraticus and A. gracilis, being particularly stringent for the latter species, while site specificities recorded were as observed in natural infections. Metacercarial maturation periods (for encystment) were highly temperature dependent, being comparable for the two Ichthyocotylurus spp. and more rapid than for A. gracilis specimens.

Identiferoai:union.ndltd.org:bl.uk/oai:ethos.bl.uk:295846
Date January 1995
CreatorsBell, Andrew Stuart
PublisherUniversity of Stirling
Source SetsEthos UK
Detected LanguageEnglish
TypeElectronic Thesis or Dissertation
Sourcehttp://hdl.handle.net/1893/3383

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