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Population dynamics of snail infection by miracidia

Published online by Cambridge University Press:  06 April 2009

R. M. Anderson
Affiliation:
King's College, London University, Strand, London WC2R 2LS

Summary

The essential biological features of snail infection by miracidia are incorporated into a simple model which describes the rate of change with respect to time of the number of miracidial infections/host. The model is based on the assumption that the net rate of infection is directly proportional to the density of both miracidia and hosts. Empirical evidence is provided to support this assumption. The basic framework of the model is expanded to take into account demographic stochasticity in infection and is used to predict the percentage of snails that become infected after exposure to a known number of miracidia for a set period of time. The influence of miracidial mortalities and age-dependent infectivity are examined and theoretical predictions are compared with a range of experimental results.

Underlying heterogeneity in the distribution of the number of infections/snail is shown to generate an artifactual decrease in infection rates as exposure density rises, if rate estimation procedures are based on an assumption of randomness. Empirical evidence is presented to illustrate the generation of over-dispersion in the number of miracidial infections/snail under tightly controlled laboratory conditions, using supposedly homogeneous snail populations.

Biological causes for underlying patterns of heterogeneity are discussed in relation to snail susceptibility to infection and ‘attractiveness’ to infective stages.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1978

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References

REFERENCES

Anderson, R. M. (1976). Dynamic aspects of parasite population ecology. In Ecological Aspects of Parasitology (ed. Kennedy, C. R.). Amsterdam: North-Holland Publishing Company.Google Scholar
Anderson, R. M. & May, R. M. (1978). Regulation and stability of host–parasite population interactions. I. Regulatory processes. Journal of Animal Ecology 47, 219–48.Google Scholar
Anderson, R. M. & Whitfield, P. J. (1975). Survival characteristics of the free-living cercarial population of the ectoparasitic digenean, Transversotrema patialense. Parasitology 70, 295310.Google Scholar
Anderson, R. M., Whitfield, P. J., Dobson, A. P. & Keymer, Anne E. (1978). Concomitant predation and infection processes: an experimental study. Journal of Animal Ecology (in the Press).CrossRefGoogle Scholar
Bailey, N. T. J. (1964). The Elements of Stochastic Processes. New York: Wiley.Google Scholar
Christensen, N. O. & Nansen, P. (1976). Studies on the infectivity of Fasciola hepatica miracidia to Lymnaea truncatula. Attachment and penetration of miracidia into non-infected and infected snails. Zeitschrift für Parasitenkunde 50, 6771.Google Scholar
Chu, K. Y., Sabbaghian, H. & Massoud, J. (1966). Host–parasite relationship of Bulinus truncatus and Schistosoma haematobium in Iran. Bulletin of the World Health Organization 34, 121–30.Google Scholar
Conway, G. R., Glass, N. R. & Wilcox, J. C. (1970). Fitting non-linear models to biological data by Marquardt's algorithm. Ecology 51, 503–8.CrossRefGoogle Scholar
Free, C. A., Beddington, J. R. & Lawton, J. H. (1977). On the inadequacy of simple models of mutual interference for parasites and predators. Journal of Animal Ecology 46, 543–54.Google Scholar
Goffman, W. & Warren, K. S. (1970). An application of the Kermack–McKendrick theory to the epidemiology of Schistosomiasis. American Journal of Tropical Medicine and Hygiene 19, 278–83.CrossRefGoogle Scholar
Hairston, N. G. (1962). Population ecology and epidemiological problems. In Bilharziasis, Ciba Foundation Symposium (ed. Wolstenholme, G. E. W. and O'Connor, M.), pp. 3662. London: Churchill.Google Scholar
Hairston, N. G. (1965). An analysis of age-prevalence data by catalytic models. A contribution to the study of bilharziasis. Bulletin of the World Health Organization 33, 163–75.Google Scholar
Hassell, M. P. (1971). Mutual interference between searching insect parasites. Journal of Animal Ecology 40, 473–86.Google Scholar
Hassell, M. P. & Varley, G. C. (1969). New inductive population model for insect parasites and its bearing on biological control. Nature, London 223, 1133–7.CrossRefGoogle ScholarPubMed
Kuris, A. M. (1973). Biological control: implications of the analogy between the trophic interactions of insect pest–parasitoid and snail–trematode systems. Experimental Parasitology 33, 365–79.CrossRefGoogle ScholarPubMed
Lie, K. J., Heyneman, D. & Kostanian, N. (1975). Failure of Echinostoma lindoense to reinfect snails already harbouring that species. International Journal for Parasitology 5, 483–6.Google Scholar
Lim, H. & Heyneman, D. (1972). Intramolluscan inter-trematode antagonism: a review of factors influencing the host–parasite system and its possible role in biological control. Advances in Parasitology 10, 191268.CrossRefGoogle ScholarPubMed
Macdonald, G. (1961). Epidemiologic models in studies of vector-bourne diseases. Public Health Reports, Washington, D. C. 76, 753–64. (Reprinted as ch. 20 in Dynamics of Tropical Disease, ed. L. J. Bruce-Chwatt and V. J. Glanville.) Oxford: Oxford University Press.Google Scholar
MacInnis, A. J. (1965). Responses of Shistosoma mansoni miracidia to chemical attractants. Journal of Parasitology 51, 731–46.CrossRefGoogle Scholar
Massoud, J. (1974). The effect of variation in miracidial exposure dose on laboratory infections of Ornithobilharzia turkestanicum in Lymnaea gedrosiana. Journal of Helminthology 48, 139–44.Google Scholar
May, R. M. (1978). Host–parasite systems in patchy environments: a phenomenological model. Journal of Animal Ecology 47, (in the Press).Google Scholar
May, R. M. & Anderson, R. M. (1978). Regulation and stability of host–parasite population interactions. II. Destabilising processes. Journal of Animal Ecology 47, 249–68.Google Scholar
Nansen, P., Ornbjerg Christensen, N. O. & Frandsen, F. (1976). A technique for in vivo labelling of Faciola hepatica miracidia with radio selenium. Zeitschrift für Parasitenkunde 49, 7380.CrossRefGoogle Scholar
Newton, W. L. (1953). The inheritance of susceptibility to infection with Schistosoma mansoni in Australorbis glabratus. Experimental Parasitology 2, 242–57.Google Scholar
Oliver, J. H. & Short, R. B. (1956). Longevity of miracidia of Schistosomatium douthitti. Experimental Parasitology 5, 238–49.CrossRefGoogle ScholarPubMed
Prah, S. K. & James, C. (1977). The influence of physical factors on the survival and infectivity of miracidia of Shistosoma mansoni and S. haematobium. I. Effect of temperature and ultra violet light. Journal of Helminthology 51, 7385.CrossRefGoogle Scholar
Richards, C. S. (1973). Susceptibility of adult Biomphalaria glabrata to Shistosoma mansoni infection. American Journal of Tropical Medicine and Hygiene 22, 748–56.Google Scholar
Schreiber, F. G. & Schubert, M. (1949 a). Results of exposure of the snail Australorbis glabratus to varying numbers of miracidia of Schistosoma mansoni. Journal of Parasitology 35, 590–2.CrossRefGoogle ScholarPubMed
Schreiber, F. G. & Schubert, M. (1949 b). Experimental infection of the snail Australorbis glabratus with the trematode Schistosoma mansoni and the production of cercariae. Journal of Parasitology 35, 91100.Google Scholar
Webbe, G. (1962). Population studies on intermediate hosts in relation to transmission of bilharziasis in East Africa. In Bilharziasis, Ciba Foundation Symposium (ed. Wolstenholme, G. E. W. and O'Connor, M.), pp. 722. London: Churchill.Google Scholar
Whitfield, P. J., Anderson, R. M. & Bundy, P. A. P. (1977). Experimental investigations on the behaviour of the cercariae of an ectoparasitic digenean Transversotrema patialense: general activity patterns. Parasitology 75, 930.CrossRefGoogle ScholarPubMed
Wilson, R. A. & Denison, J. (1970). Short chain fatty acids as stimulants of turning activity by the miracidium of Fasciola hepatica. Comparative Biochemical Physiology 32, 511–17.CrossRefGoogle ScholarPubMed
Wilson, R. A. & Taylor, S. L. (1978). The effect of variations in host and parasite density on the level of parasitization of Lymnaea truncatula by Fasciola hepatica. Parasitology 76, 91–8.CrossRefGoogle ScholarPubMed