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Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes

Published online by Cambridge University Press:  07 April 2017

C. Combes ,
A. Fournier ,
H. Moné  and
A. Théron
C. Combes
Affiliation:
Laboratoire de Biologie Animate (URA CNRS 698), Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France
A. Fournier
Affiliation:
Laboratoire de Biologie Animate (URA CNRS 698), Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France
H. Moné
Affiliation:
Laboratoire de Biologie Animate (URA CNRS 698), Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France
A. Théron
Affiliation:
Laboratoire de Biologie Animate (URA CNRS 698), Centre de Biologie et d'Ecologie Tropicale et Méditerranéenne, Université, Avenue de Villeneuve, 66860 Perpignan Cedex, France
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Extract

Cercariae, like miracidia, are non-parasitic larval stages implicated in the life cycle of all trematodes for the host-to-host parasite transmission. Almost all cercariae are free-living in the external environment. With a few exceptions (cercariae of Halipegus occidualis (Halipegidae) can live several months, Shostak & Esch, 1990a), cercariae have a short active life during which they do not feed, living on accumulated reserves. Most cercariae encyst as metacercariae in second intermediate hosts which are prey of the definitive host; in certain species, the interruption of the active life is achieved by an encystment in the external environment (or a simple immobile waiting strategy in a few species). In some two-host life cycles, the cercariae develop into adults after penetration (this is the case for various species causing human schistosomiasis). Some cercariae do not leave the mollusc which must then be ingested by the definitive host.

Keywords

Host-locationtrematodecercariabehaviourtransmissionecology
Type
Research Article
Information
Parasitology , Volume 109 , supplement S1: Parasites and behaviour , 1994 , pp. S3 - S13
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Anderson, R. M. & May, R. M. (1978). Regulation and stability of host-parasite population interactions. 1. Regulatory processes. Journal of Animal Ecology 47, 219–47..CrossRefGoogle Scholar
Anderson, R. M. & Whitfield, P. J. (1975). Survival characteristics of the free-living cercarial population of the ectoparasitic digenean Transversotrema patialensis (Soparker, 1924). Parasitology 70, 295–310.CrossRefGoogle Scholar
Asch, H. L. (1972). Rhythmic emergence of Schistosoma mansoni cercariae from Biomphalaria glabrata: control by illumination. Experimental Parasitology 31, 189–98.CrossRefGoogle ScholarPubMed
Bartoli, P. & Combes, C. (1986). Strategies de dissemination des cercaires de trematodes dans un ecosysteme marin littoral. Acta Œcologica Œcologia Generalis 7, 101–14.Google Scholar
Beuret, J. & Pearson, J. C. (1994). Description of a new zygocercous cercaria (Opisthorchioidea: Hecterophyidae) from prosobranch gastropods collected at Heron Island (Great Barrier Reef, Australia) and a review of zygocercariae. Systematic Parasitology 27, 105–25.CrossRefGoogle Scholar
Bouix-Busson, D., Rondelaud, D. & Combes, C. (1985). L'infestation de Lymnaea glabra Muller par Fasciola hepatica L. Les caracteristiques des émissions cercariennes. Annales de Parasitologie Humaine et Comparee 60, 11–21.Google Scholar
Cable, R. M. (1972). Behaviour of digenetic trematodes. In Behavioural Aspects of Parasite Transmission, (ed. Canning, E. U. & Wright, C. A.), pp.1–18. London: Academic Press.Google Scholar
Chapman, H. D. (1974). The behaviour of the cercaria Cryptocotyle lingua. Zeitschrift fur Parasitenkunde 44, 211–26.Google Scholar
Chassé, J. L. & Théron, 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.Google Scholar
Cheng, T. C. (1986). General Parasitology, 2nd edn. Orlando: Academic Press College Division.Google Scholar
Christensen, N. O. (1979). Schistosoma mansoni: interference with cercarial host-finding by various aquatic organisms. Journal of Helminthology S3, 7–14.Google Scholar
Christensen, N. O., Frandsen, F. & Nansen, P. (1980). The interaction of some environmental factors influencing Schistosoma mansoni cercarial host-finding. Journal of Helminthology 54, 203–5.Google Scholar
Combes, C. (1971). Uber die Rolle des Verhaltens des Zweiten Zwischenwirtes im biologischen Zyklus der Gorgoderiden. Parasitologische Schriftenreike 21, 183–5.Google Scholar
Combes, C. (1980). Les mécanismes de recrutements chez les métazoaires parasites et leur interprétation en termes de stratégies démographiques. Vie et Milieu 30, 55–63.Google Scholar
Combes, C. (1991). Ethological aspects of parasite transmission. The American Naturalist 138, 866–80.Google Scholar
Curtis, L. A. (1987). Vertical distribution of an estuarine snail altered by parasite. Science 235, 1509–11.CrossRefGoogle ScholarPubMed
Curtis, L. A. (1990). Parasitism and the movements of intertidal gastropod individuals. Biological Bulletin 179, 105–12.CrossRefGoogle ScholarPubMed
Dönges, J. (1964). Der lebenszyklus von Posthodiplostomum cuticola (v. Nordmann 1832) Dubois 1936 (Trematoda, Diplostomatidae). Zeitschrift fur Parasitenkunde 24, 169–248.CrossRefGoogle Scholar
Erasmus, D. A. (1972). The Biology of Trematodes, London: Edward Arnold Ltd.Google Scholar
Evans, N. A. & Gordon, D. M. (1983). Experimental observations on the specificity of Echinoparyphium recurvatum toward second intermediate hosts. Zeitschrift fur Parasitenkunde 69, 217–22.CrossRefGoogle Scholar
Evans, N. A., Whitfield, P. J. & Dobson, A. P. (1981). Parasite utilization of a host community: the distribution and occurrence of metacercarial cysts of Echinoparyphium recurvatum (Digenea: Echinostomatidae) in seven species of mollusc at Harting Pond, Sussex. Parasitology 83, 1–12.Google Scholar
Feiler, W. & Haas, W. (1988). Host-finding in Trichobilharzia ocellata cercariae: swimming and attachment to the host. Parasitology 96, 493–505.Google Scholar
Fournier, A. (1984). Photoreceptors and photosensitivity in Platyhelminthes. In Photoreception and Vision in Invertebrates. (Ed. Ali, M. A.) pp. 217–239, New York and London: Plenum Press.CrossRefGoogle Scholar
Fried, B. & King, B. W. (1989). Attraction of Echinostoma revolutum cercariae to Biomphalaria glabrata dialysate. Journal of Parasitology 75, 55–7.Google Scholar
Giovannola, A. (1936). Some observations on the emission of cercariae of Schistosoma mansoni (Trematoda: Schistosomatidae) from Australorbis glabratus. Proceedings of the Helminthological Society of Washington. 3, 60–1.Google Scholar
Glaudel, R. J. & Etges, F. G. (1973). The effect of photoperiod inversion upon Schistosoma mansoni cercarial emergence from Biomphalaria glabrata. International Journal for Parasitology 3, 619–21.Google Scholar
Haas, W. (1969). Reizphysiologische Untersuchungen an cercarien von Diplostomum spathaceum. Zeitschrift für vergleichende Physiologie 64, 254–87.Google Scholar
Haas, W., Granzer, M. & Brockelman, C. R. (1990). Finding and recognition of the bovine host by the cercariae of Schistosoma spindale. Parasitology Research 76, 343–50.CrossRefGoogle ScholarPubMed
Hendrickson, G. L. & Kingston, N. (1974) Cercaria laramiensis sp. n., a freshwater zygocercous cercaria from Physa gyrina Say, with a discussion of cercarial aggregation. Journal of Parasitology 60, 777–81.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.Google Scholar
Kuntz, R. E. (1947). Effect on light and temperature on emergence of Schistosoma mansoni cercariae. Transactions of the American Microscopical Society 66, 37–49.CrossRefGoogle ScholarPubMed
Ladle, R. J. (1992). Parasites and sex: catching the red queen. Trends in Ecology and Evolution 7, 405–8.CrossRefGoogle ScholarPubMed
Lewis, M. C., Welsford, I. G. & Uglem, G. L. (1989). Cercarial emergence of Proterometra macrostoma and P. edneyi (Digenea: Azygiidae): contrasting responses to light:dark cycling. Parasitology 99, 215–23.Google Scholar
Luttermoser, G. (1955) Studies on the chemotherapy of experimental schistosomiasis: III. Harvest of Schistosoma mansoni cercariae by forced nocturnal emergence from Australorbis glabratus. Journal of Parasitology 41, 201–8.Google Scholar
Maillard, C. (1971). Cycle évolutif de Cainocreadium labracis (Dujardin, 1845) (Trematoda, Allocreadiidae). Comptes Rendus de l'Académie des Sciences, Paris 272, 3303–6.Google Scholar
May, R. M. & Anderson, R. M. (1978). Regulation and stability of host-parasite population interactions. 2. Destabilizing processes. Journal of Animal Ecology 47, 249–267.CrossRefGoogle Scholar
Meyrowitsch, D., Christensen, N. O. & Hindsbo, O. (1991). Effects of temperature and host-density on the snail-finding capacity of cercariae of Echinostoma caproni (Digenea: Echinostomatidae). Parasitology 102, 391–5.Google Scholar
Mouchet, F., Théron, A., Brémond, P., Sellin, E. & Sellin, B. (1992). Pattern of cercarial emergence of Schistosoma curassoni from Niger and comparison with three sympatric species of schistosomes. Journal of Parasitology 78, 61–3.Google Scholar
Nojima, H., Sato, A. & Matsunaga, K. (1981). The emergence of Schistosome cercariae from the snails. 3. Combined effect of light and temperature on the emergence of Schistosoma mansoni and S. haematobium cercariae. Japanese Journal of Parasitology 30, 405–15.Google Scholar
Nolf, L. O. & Cort, W. W. (1933). On immunity reactions of snails to the penetration of the cercariae of the strigeid trematode, Cotylurus flabelliformis (Faust). Journal of Parasitology 20, 38–48.CrossRefGoogle Scholar
Pagès, J. R. & Théron, A. (1990a) Analysis and comparison of cercarial emergence rhythms of Schistosoma haematobium, S. intercalatum and S. bovis and their hybrid progeny. International Journal for Parasitology 20, 193–7.CrossRefGoogle ScholarPubMed
Pagès, J. R. & Theron, A. (1990b). Schistosoma intercalatum from Cameroon and Zaïre: chronobiological differenciation of cercarial emergence. Journal of Parasitology 76, 743–5.Google Scholar
Raymond, K. & Probert, A. J. (1991). The daily cercarial emission rhythm of Schistosoma margrebowiei with particular reference to dark period stimuli. Journal of Helminthology 65, 159–68.Google Scholar
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. (1992a). 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.Google Scholar
Rea, J. G. & Irwin, W. B. (1992b). The effects of computer-controlled shadow stimuli on the success of cercarial transmission by Cryptocotyle lingua (Digenea: Heterophidae). Parasitology 105, 243–6.Google Scholar
Saladin, K. S. (1980). Behavioral manifestations of photosensitivity in cercariae of Schistosoma mansoni (Digenea: Schistosomatidae). Ph. D. Florida State University, 216pp. Diss. Abstr. Intern., 40, 7.Google Scholar
Saladin, K. S. (1982). Schistosoma mansoni: cercarial responses to irradiance changes. Journal of Parasitology 68, 120–4.CrossRefGoogle ScholarPubMed
Shostak, A. W. & Esch, G. W. (1990a). Temperature effects on survival and encystment of cercariae of Halipegus occidualis (Trematoda). International Journal for Parasitology 20, 95–9.CrossRefGoogle Scholar
Shostak, A. W. & Esch, G. W. (1990b). Photocycle-dependent emergence by cercariae of Halipegus occidualis from Helisoma anceps, with special reference to cercarial emergence patterns as adaptations for transmission. Journal of Parasitology 76, 790–5.CrossRefGoogle Scholar
Théron, A. (1975). Chronobiologie des cercaires de Ribeiroia marini (Faust et Hoffman, 1934) parasite de Biomphalaria glabrata: action de la photopériode sur le rythme d'émission. Ada tropica 32, 309–16.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.Google Scholar
Théron, A. (1985). Le polymorphisme du rythme d'émission des cercaires de Schistosoma mansoni et ses relations avec l'éecologie de la transmission du parasite. Vie et Milieu 35, 23–31.Google Scholar
Théron, A. (1989). Hybrids between Schistosoma mansoni and S. rodhaini: characterization by cercarial emergence rhythms. Parasitology 99, 225–8.Google Scholar
Théron, A. & Combes, C. (1988). Genetic analysis of cercarial emergence rhythms of Schistosoma mansoni. Behavior Genetics 18, 201–9.Google Scholar
Uglem, G. L. & Prior, D. J. (1983). Control of swimming in cercariae of Proterotrema macrostoma (Digenea). Journal of Parasitology 69, 866–70.CrossRefGoogle ScholarPubMed
Valle, C., Pellegrino, J. & Alvarenga, N. (1973). Rhythmic emergence of Schistosoma mansoni cercariae from Biomphalaria glabrata: influence of temperature. Revista del Instituto de Medicine Tropical, Sao Paolo 15, 195–201.Google Scholar
Whitfield, P. J., Anderson, R. M. & Bundy, D. A. P. (1977). Experimental investigations of the behaviour of the cercariae of an ectoparasitic digenean, Transversotrema patialense: general activity patterns. Parasitology 75, 9–30.Google Scholar
Winfield, G. F. (1932). On the immunity of snails infested with the sporocysts of the strigeid, Cotylurus flabelliformis, to the penetration of its cercaria. Journal of Parasitology 19, 130–3.CrossRefGoogle Scholar
Wright, D. G. S. (1974). Responses of cercariae of Trichobilharzia ocellata to white light, monochromatic light and irradiance reduction. Canadian Journal of Zoology 52, 575–579.Google Scholar
Yamaguti, S. (1975). A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates with Special Reference to the Morphology of their Larval Forms. Keigaku Publishing Co., Ltd, Japan, 590p.Google Scholar