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Physiological analyses of host-finding behaviour in trematode cercariae: adaptations for transmission success

Published online by Cambridge University Press:  07 April 2017

W. Haas
W. Haas
Affiliation:
Institut für Zoologie I, Universität Erlangen-Nürnberg, Staudtstrasse 5, D-91058 Erlangen, Germany
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Summary

Physiological analyses of the behaviour of several cercarial species which actively find and invade their hosts have revealed very complex sequences of behaviour patterns and responses to very different stimuli from the environment and the host. A result of these physiological studies is that the behaviour patterns of each of the species investigated are surprisingly individual. The behavioural patterns of host-finding of those species analysed in some detail reveal profound adaptations to maximize transmission success. This can be demonstrated for movement patterns during swimming, for responses to environmental conditions such as gravity, light and temperature, for responses to stimuli emanating from the host such as shadows, water turbulence and chemical compounds and especially for the responses after contact with the host. The behaviour patterns can be interpreted as adaptations to: (1) dispersal by leaving the habitat of the snail intermediate host and distribution within the area; (2) long survival by energy saving swimming behaviour, by avoiding responses to inappropriate stimuli, by selecting favourable microhabitats and probably by avoiding predation; (3) finding and invading particular host types by selecting microhabitats frequented by the hosts and responding to sequences of specific stimuli emanating from the hosts.

Type
Research Article
Information
Parasitology , Volume 109 , supplement S1: Parasites and behaviour , 1994 , pp. S15 - S29
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Austin, F. G., Frappaolo, P., Gilbert, B., Landis, W., Rosa, D A, , M. N. & Stirewalt, M. A. (1974). Further studies of Schistosoma mansoni cercarial stimulation by crude egg lecithin and other lipids. Parasitology 69, 455–63.CrossRefGoogle ScholarPubMed
Austin, F. G., Stirewalt, M. A. & Danzinger, R. E. (1972). Schistosoma mansoni: Stimulatory effect of rat skin lipid fractions on cercarial penetration behavior. Experimental Parasitology 31, 217–24.CrossRefGoogle ScholarPubMed
Bundy, D. A. P. (1981). Swimming behaviour of the cercaria of Transversotrema patialense. Parasitology 82, 319–34.CrossRefGoogle Scholar
Cable, R. M. (1972). Behaviour of digenetic trematodes. Zoological Journal of the Linnean Society 51, 1–18.Google Scholar
Chapman, H. D. (1974). The behaviour of the cercaria of Cryptocotyle lingua. Zeitschrift für Parasitenkunde 44, 211–26.CrossRefGoogle ScholarPubMed
Chapman, H. D. & Wilson, R. A. (1973). The propulsion of the cercariae of Himasthla secunda (Nicoll) and Cryptocotyle lingua. Parasitology 67, 1–15.CrossRefGoogle ScholarPubMed
Chasse, J.-L. & Theron, A. (1988). An example of circular statistics in chronobiological studies: Analysis of polymorphism in the emergence rhythms of Schistosoma mansoni cercariae. Chronobiology International 5, 433–9.CrossRefGoogle ScholarPubMed
Christensen, N. O. (1979). Schistosoma mansoni: interference with cercarial host-finding by various aquatic organisms. Journal of Helminthology 53, 7–14.CrossRefGoogle ScholarPubMed
Christensen, N. O. & Frandsen, F. (1980). The interaction of some environmental factors influencing Schistosoma mansoni cercarial host-finding. Journal of Helminthology 54, 203–5.CrossRefGoogle ScholarPubMed
Clegg, J. A. (1969). Skin penetration by cercariae of the bird schistosome Austrobilharzia terrigalensis: The stimulatory effect of cholesterol. Parasitology 59, 973–89.CrossRefGoogle ScholarPubMed
Coil, W. H. (1984). An analysis of swimming by the cercariae of Fasciola hepatica using high speed cinematography. Proceedings of the Helminthological Society of Washington 51, 293—6.Google Scholar
Combes, C, Fournier, A., Moné, H. & Théron, A. (1994). Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology 109, S3–13.CrossRefGoogle ScholarPubMed
Dönges, J. (1964). Der Lebenscyklus von Posthodiplostomum cuticola (v. Nordmann 1832) Dubois 1936 (Trematoda, Diplostomatidae). Zeitschrift fiir Parasitenkunde 24, 169–248.Google Scholar
Erasmus, D. A. (1972). The Biology of Trematodes. London: Edward Arnold Limited.Google Scholar
Evans, N. A. & Gordon, D. M. (1983). Experimental studies on the transmission dynamics of the cercariae of Echinoparyphium recurvatum (Digenea: Echinostomatidae). Parasitology 87, 167–74.CrossRefGoogle Scholar
Feiler, W. & Haas, W. (1988 a). Host-finding in Trichobilharzia ocellata cercariae: swimming and attachment to the host. Parasitology 96, 493–505.CrossRefGoogle ScholarPubMed
Feiler, W. & Haas, W. (1988 b). Trichobilharzia ocellata: chemical stimuli of duck skin for cercarial attachment. Parasitology 96, 507–17.CrossRefGoogle ScholarPubMed
Fried, B. & King, W. (1989). Attraction of Echinostoma revolutum cercariae to Biomphalaria glabrata dialysate. Journal of Parasitology 75: 55–7.CrossRefGoogle Scholar
Fusco, A. C, Salafsky, B., & Delbrook, K. (1986). Schistosoma mansoni: Production of cercarial eicosanoids as correlates of penetration and transformation. Journal of Parasitology 72, 397—404.CrossRefGoogle ScholarPubMed
Fusco, A.C, Salafsky, B. & Kevin, M. B. (1985). Schistosoma mansoni: Eicosanoid production by cercariae. Experimental Parasitology 59, 44—50.CrossRefGoogle ScholarPubMed
Graefe, G. W. & Burkert, D. G. (1972). Zur Lokomotionsmechanik von Diplostomatiden- und Echinostomatiden-Cercarien (Trematoda). Zoologischer A.nzeiger, Leipzig 188, 366—9.Google Scholar
Graefe, G. W., Hohorst, W. & Dräger, H. (1967). Forked tail of the cercaria of Schistosoma mansoni — a rowing device. Nature 215, 207–8.CrossRefGoogle ScholarPubMed
Granzer, M. & Haas, W. (1986). The chemical stimuli of human skin surface for the attachment response of Schistosoma mansoni cercariae. International Journal for Parasitology 16, 575–9.CrossRefGoogle ScholarPubMed
Haas, W. (1969). Reizphysiologische Untersuchungen an Cercarien von Diplostomum spathaceum. Zeitschrift fur vergleichende Physiologie 64, 254—87.CrossRefGoogle Scholar
Haas, W. (1974 a). Analyse der Invasionsmechanismen der Cercarie von Diplostomum spathaceum—I. Fixation und Penetration. International Journal for Parasitology 4, 311–9.CrossRefGoogle ScholarPubMed
Haas, W. (1974 b). Analyse der Invasionsmechanismen der Cercarie von Diplostomum spathaceum-II. Chemische Invasionsstimuli. International Journal for Parasitology 4, 321–30.CrossRefGoogle Scholar
Haas, W. (1975). Einfluß von CO2 und pH auf das Fixationsverhalten der Cercarie von Diplostomum spathaceum (Trematoda). Zeitschrift für Parasitenkunde 46, 53–60.CrossRefGoogle ScholarPubMed
Haas, W. (1976). Die Anheftung (Fixation) der Cercarie von Schistosoma mansoni. Einfluß natürlicher Substrate und der Temperatur. Zeitschrift für Parasitenkunde 49, 63–72.CrossRefGoogle Scholar
Haas, W. (1984). Schistosoma mansoni: Cercaricidal effect of 2-tetradecenoic acid, a penetration stimulant. Experimental Parasitology 58, 215–22.CrossRefGoogle ScholarPubMed
Haas, W. (1988). Host finding–;a physiological effect. In Parasitology in Focus, (ed. Mehlhorn, H.), pp. 454—64. Berlin, Heidelberg, New York, Tokyo: Springer Verlag.CrossRefGoogle Scholar
Haas, W. (1992). Physiological analysis of cercarial behavior. Journal of Parasitology 78, 243–55.CrossRefGoogle ScholarPubMed
Haas, W., Granzer, M. & Brockelman, C. (1990 a). Finding and recognition of the bovine host by the cercariae of Schistosoma spindale. Parasitology Research 76, 343–50.CrossRefGoogle ScholarPubMed
Haas, W., Granzer, M. & Brockelman, C. (1990 b). Opisthorchis viverrini: Finding and recognition of the fish host by the cercariae. Experimental Parasitology 71, 422–31.CrossRefGoogle ScholarPubMed
Haas, W., Cranzer, M. & Garcia, E. G. (1987 ). Host identification by Schistosoma japonicum cercariae. Journal of Parasitology 73, 568–77.CrossRefGoogle ScholarPubMed
Haas, W., Granzer, M. & Hannappel, E. (1989). Ein Funktionswandel des Signals Arginin bei der Wirtsfindung von Schistosoma-Cerc&nen. Verhandlungen der Deutschen Zoologischen Gesellschaft 82, 241.Google Scholar
Haas, W., Gui, M., Haberl, B. & Ströbel, M. (1991). Miracidia of Schistosoma japonicum: approach and attachment to the snail host. Journal of Parasitology 77, 509–13.CrossRefGoogle Scholar
Haas, W., Haberl, B., Schmalfuss, G. & Khayyal, M. T. (1994). Schistosoma haematobium cercarial host-finding and host-recognition differs from that of Schistosoma mansoni. Journal of Parasitology 80, 345–53.CrossRefGoogle Scholar
Haas, W. & Ostrowsky, D ENuñez, M. (1988). Chemical signals of fish skin for the attachment response of Acanthostomum brauni cercariae. Parasitology Research 74, 552–7.CrossRefGoogle ScholarPubMed
Haas, W. & Schmitt, R. (1982 a). Characterization of chemical stimuli for the penetration of Schistosoma mansoni cercariae. I. Effective substances, host specificity. Zeitschrift für Parasitenkunde 66, 293–307.CrossRefGoogle ScholarPubMed
Haas, W. & Schmitt, R. (1982 b). Characterization of chemical stimuli for the penetration of Schistosoma mansoni cercariae. II. Conditions and mode of action. Zeitschrift für Parasitenkunde 66, 309–19.CrossRefGoogle ScholarPubMed
Haberl, B. & Haas, W. (1992). Miracidium of Schistosoma mansoni: a macromolecular glycoconjugate as signal for the behaviour after contact with the snail host. Comparative Biochemistry and Physiology 101A, 329–33.CrossRefGoogle Scholar
Haberl, B., Ströbel, M., Gui, M. & Haas, W. (1992). Miracidial host-finding: a new approach to an old problem. Zentralblatt für Bakteriologie, Abstracts 325, 34.Google Scholar
Heiss, C. & Haas, W. (1990). Life cycle and host-finding of the cercaria of Apatemon (Australapatemon) minor. Zentralblatt für Bakteriologie und Hygiene, Abstracts 317, 43.Google Scholar
Hutterer, E., Kläver, S., Wegner, M. & Haas, W. (1992). Snails as intermediate hosts: mechanisms of hostfinding in cercariae. Zentralblatt für Bakteriologie, Abstracts 325, 43.Google Scholar
Jourdane, J. & Théron, A. (1987). Larval development: eggs to cercariae. In The Biology of Schistosomes. From Genes to Latrines, (ed. Rollinson, D. & Simpson, A. J. G.), pp. 83–113. London, San Diego: Academic Press.Google Scholar
Kennedy, M. J. (1979). The responses of miracidia and cercariae of Bunodera mediovitellata (Trematoda: Allocreadiidae) to light and gravity. Canadian Journal of Zoology 57, 603–9.CrossRefGoogle Scholar
Knight, W. B., Ritchie, L. S., Liard, F. & Chiriboga, J. (1970). Cercariophagic activity of guppy fish (Lebistes reticulatus) detected by cercariae labeled with radioselenium (75Se). American Journal of Tropical Medicine and Hygiene 19, 620–5.CrossRefGoogle ScholarPubMed
Lee, H.-F. (1962). Life history of Heterobilharzia americana Price 1929, a schistosome of the racoon and other mammals in southeastern United States. Journal of Parasitology 48, 728–39.CrossRefGoogle Scholar
Macinnis, A. J. (1969). Identification of chemicals triggering cercarial penetration responses of Schistosoma mansoni. Nature 224, 1221–2.CrossRefGoogle ScholarPubMed
Macinnis, A. J. (1976). How parasites find hosts: Some thoughts on the inception of host-parasite integration. In Ecological Aspects of Parasitology, (ed. Kennedy, C. R.), pp. 3–20. Amsterdam: North-Holland Publications.Google Scholar
Mccarthy, A. M. & Kanev, I. (1990 ). Pseudechinoparyphium echinatum (Digenea: Echinostomatidae): experimental observations on cercarial specificity toward second intermediate hosts. Parasitology 100, 423–8.CrossRefGoogle ScholarPubMed
Miller, H. M., & Mahaffy, E. E. (1930). Reactions of Cercaria hamata to light and to mechanical stimuli. Biological Bulletin 59, 95–103.CrossRefGoogle Scholar
Miller, H. M. & Mccoy, O. R. (1930). An experimental study of the behavior of Cercaria floridensis in relation to its fish intermediate host. Journal of Parasitology 16, 185–97.CrossRefGoogle Scholar
Motzel, W. & Haas, W. (1985). Studies on the attachment response of Isthmiophora melis cercariae (Trematoda: Echinostomatidae). Zeitschrift für Parasitenkunde 71, 519–26.CrossRefGoogle ScholarPubMed
Nevhutalu, P. A., Salafsky, B., Haas, W. & Conway, T. (1993). Schistosoma mansoni and Trichobilharzia ocellata: comparison of secreted cercarial eicosanoids. Journal of Parasitology 79, 130–3.CrossRefGoogle ScholarPubMed
Ostrowski, D ENunez, M. & Haas, W. (1991). Penetration stimuli of fish skin for Acanthostomum brauni cercariae. Parasitology 102, 101–104.CrossRefGoogle Scholar
Pellegrino, J., De Maria, M. & De Moura, M. F. (1966). Observations on the predatory activity of Lebistes reticulatus (Peters, 1859) on cercariae of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 15, 337–341.CrossRefGoogle ScholarPubMed
Pike, A. W. (1990). Interpreting parasite host location behaviour. Parasitology Today 6, 343–4.CrossRefGoogle ScholarPubMed
Prior, D. J. & Uglem, G. L. (1979). Behavioural and physiological aspects of swimming in cercariae of the digenetic trematode, Proterometra macrostoma. Journal of Experimental Biology 83, 239–47.CrossRefGoogle ScholarPubMed
Rea, J. G. & Irwin, S. W. B. (1991). Behavioural responses of the cercariae of Cryptocotyle lingua (Digenea: Heterophyidae) to computer-controlled shadow sequences. Parasitology 103, 471–7.CrossRefGoogle ScholarPubMed
Rea, J. G. & Irwin, S. W. B. (1992 a). The effects of age, temperature, light quantity and wavelength on the swimming behaviour of the cercariae of Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 105, 131–7.CrossRefGoogle ScholarPubMed
Rea, J. G. & Irwin, S. W. B. (1992 b). The effects of computer-controlled shadow stimuli on the success of cercarial transmission by Cryptocotyle lingua (Digenea: Heterophyidae). Parasitology 105, 243–6.CrossRefGoogle ScholarPubMed
Rees, G. (1971). Locomotion of the cercaria of Parorchis acanthus, Nicoll and the ultrastructure of the tail. Parasitology 62, 489–503.CrossRefGoogle ScholarPubMed
Rogers, W. P. (1962). The Nature of Parasitism, New York: Academic Press.Google Scholar
Saladin, K. S. (1979 b). Behavioral parasitology and perspectives on miracidial host-finding. Zeitschrift fur Parasitenkunde 60, 197–210.CrossRefGoogle ScholarPubMed
Saladin, K. S. (1979 b). Behavioral manifestation of photosensitivity in cercariae of Schistosoma mansoni (Digenea; Schistosomatidae). Dissertation, Ph.D., The Florida State University, Tallahassee, Florida. Saladin, K. S. (1982). Schistosoma mansoni: cercarial responses to irradiance changes. Journal of Parasitology 68, 120–4.CrossRefGoogle Scholar
Salafsky, B. & Fusco, A. (1987). Eicosanoids as immunomodulators of penetration by schistosome cercariae. Parasitology Today 3: 279–81.CrossRefGoogle ScholarPubMed
Schauer, R. (1982). Sialic Acids: Chemistry, Metabolism and Function, Cell Biology Monographs, Volume 10. New York: Springer-Verlag.CrossRefGoogle Scholar
Shiff, C. J., Cmelik, S. H., Ley, H. E. & Kriel, R. L. (1972). The influence of human skin lipids on the cercarial penetration responses of Schistosoma haematobium and Schistosoma mansoni. Journal of Parasitology 58, 476–80.CrossRefGoogle ScholarPubMed
Smyth, J. D. & Halton, D. W. (1983). The Physiology of Trematodes. 2nd edn. Cambridge: Cambridge University Press.Google Scholar
Sommerville, R. I. & Rogers, W. P. (1987). The nature and action of host signals. Advances in Parasitology 26, 239–93.CrossRefGoogle ScholarPubMed
Standen, O. D. & Fuller, K. A. (1959). Ultraviolet irradiation of the cercariae of Schistosoma mansoni. Inhibition of development to adult stage. Transactions of the Royal Society of Tropical Medicine and Hygiene 53, 372–9.CrossRefGoogle ScholarPubMed
Stirewalt, M. A. (1971). Penetration stimuli for schistosome cercariae. In Aspects of the Biology of Symbiosis, (ed. Cheng, T.C.), pp. 1–23. Baltimore: University Park Press, Baltimore.Google Scholar
Stirewalt, M. A. & Evans, A. S. (1960). Chromatographic analysis of secretions of acetabular glands of cercariae of Schistosoma mansoni. Experimental Parasitology 10, 75–80.CrossRefGoogle Scholar
Stirewalt, M. A. & Walters, M. (1973). Schistosoma mansoni: histochemical analysis of the postacetabular gland secretion of cercariae. Experimental Parasitology 33, 56–72.CrossRefGoogle ScholarPubMed
Styczynska-Jurewicz, E. (1961). On the geotaxis, invasivity and span of life of Opisthioglyphe ranae Duj. cercariae. Bulletin de l'Academie Polonaise des Sciences, Classe II. Série des Sciences Biologiques 9, 31–5.Google Scholar
Sukhdeo, M. V. K. & Mettrick, D. F. (1987). Parasite behaviour: understanding platyhelminth responses. Advances in Parasitology 26, 73–144.CrossRefGoogle ScholarPubMed
Takahashi, T., Mori, K & Shigeta, Y. (1961). PhotOtaCtlC, thermotactic and geotactic responses of miracidia of Schistosoma japonicum. Japanese Journal of Parasitology 10, 686–91.Google Scholar
Théron, A. (1984). Early and late shedding patterns of Schistosoma mansoni cercariae: ecological significance in transmission to human and murine hosts. Journal of Parasitology 70, 652–5.CrossRefGoogle ScholarPubMed
Tomberg, V. & Lagrange, E. (1952). Étude de l'action de quelques agents physiques sur les planorbes et les cercaires de Bilharzia mansoni. Annales de la Société Beige de Médécine Tropicale 32, 501–11.Google Scholar
Ulmer, M. J. 1971. Site-finding behaviour in helminths in intermediate and definitive hosts. In Ecology and Physiology of Parasites, (ed. Fallis, A. M.), pp. 123–60. Toronto: University of Toronto Press.CrossRefGoogle Scholar
Valle, C., Pellegrino, J. & Gazzinelli, G. (1974). Influence of temperature on the backward propulsion speed of Schistosoma mansoni cercariae. Journal of Parasitology 60, 372–3.CrossRefGoogle ScholarPubMed
Whitfield, P. J., Anderson, R. M. & Bundy, D. A. P. (1977). Experimental investigations on the behaviour of the cercariae of an ectoparasitic digenean Transversotrema patialense: general activity patterns. Parasitology 75, 9–30.CrossRefGoogle ScholarPubMed
Wilson, R. A. (1987). Cercariae to liver worms: development and migration in the mammalian host. In The Biology of Schistosomes. From Genes to Latrines, (ed. Rollinson, D. & Simpson, A. J. G.), pp. 115—46. London, San Diego: Academic Press.Google Scholar
Woicke, E. & Haas, W. (1989). Schistosoma mansoni: Stimuli der menschlichen Haut fur die Verbleibreaktion der Cercarie. Verhandlungen der Deutschen Zoologischen Gesellschaft 82, 250.Google Scholar
Wright, D. G. S. (1974). Responses of the cercariae of Trichobilharzia ocellata to white light, monochromatic light, and irradiance reduction. Canadian Journal of Zoology 52, 575–9.CrossRefGoogle ScholarPubMed
Zibulewsky, J., Fried, B. & Bacha, W. J. (1982). Skin surface lipids of the domestic chicken, and neutral lipid standards as stimuli for the penetration response of Austrobilharzia variglandis cercariae. Journal of Parasitology 68, 905–8.CrossRefGoogle ScholarPubMed