Hostname: page-component-77c89778f8-rkxrd Total loading time: 0 Render date: 2024-07-17T17:34:56.407Z Has data issue: false hasContentIssue false
  • English
  • Français

Parasite-altered behaviour: impact of infection and starvation on mating in Biomphalaria glabrata

Published online by Cambridge University Press:  06 April 2009

J. C. Rupp
J. C. Rupp
Affiliation:
Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS
Get access Rights & Permissions [Opens in a new window]

Summary

Very little is known about parasite-altered mating behaviour. This paper describes two experiments on the impact of infection and starvation on mating in Biomphalaria glabrata snails. In the first experiment, snails were infected with the parasitic trematode Schistosoma mansoni. During both the early and the late stages of infection, snails were allowed to mate with individuals of the same infection status and uninfected controls. Their mating activities were filmed and later analysed. The mating frequencies of patently infected (shedding) snails were found to be lower than those of controls. This is thought to result from stress induced by the pathology. Successfully infected snails were found to mate more often as males than as females. This is seen as a compensation for the reduced fecundity caused by trematode infection. Successfully infected snails also exhibited partner choice. More matings were found between snails of the opposite infection status than among snails of the same infection status. This may be explained by the good genes hypothesis and can be seen as a specific response to schistosome infection. In the second experiment, starved snails were allowed to mate with starved and control snails. They mated less often than controls and more often as males than as females, controls showing the opposite pattern. This may be considered to be a general stress response. No partner choice has been found with starved snails. It is suggested that partner choice in infected snails occurs in response to specific rather than general stress.

Keywords

snailsSchistosoma mansonimatechoice
Type
Research Article
Information
Parasitology , Volume 113 , Issue 4 , October 1996 , pp. 357 - 365
Copyright
Copyright © Cambridge University Press 1996

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alexander, J. & Stimson, W. H. (1988). Sexual effects on parasite infection: sex hormones and the course of parasitic infection. Parasitology Today 4, 186–189.CrossRefGoogle Scholar
Anderson, R. M. & May, R. M. (1979). Prevalence of schistosome infections within molluscan populations: observed patterns and theoretical predictions. Parasitology 79, 63–94.Google Scholar
Bayne, C. J. & Loker, E. S. (1987). Survival within the snail host. In The Biology of Schistosomes (ed. Rollinson, D. & Simpson, A. J. G.), pp. 321–346. Academic Press, London.Google Scholar
Becker, W. (1980). Microcalorimetric studies in Biomphalaria glabrata: the influence of Schistosoma mansoni on the basal metabolism. Journal of Comparative Physiology 135, 101–105.CrossRefGoogle Scholar
Berdoy, M., Webster, J. P. & Macdonald, D. W. (1995). Parasite-altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific? Parasitology 111,403–409.Google Scholar
Brandt, T. Von & Files, V. S. (1947). Chemical and histological observations on the influence of Schistosoma mansoni infection on Australorbis glabratus. Journal of Parasitology 33, 476–482.Google Scholar
Cheng, T. C. & Lee, F. O. (1971). Glucose levels in the mollusc Biomphalaria glabrata infectd with Schistosoma mansoni. Journal of Invertebrate Pathology 18, 395–399.Google Scholar
Clayton, D. (1990). Mate choice in experimentally parasitized rock doves: lousy males lose. American Zoologist,30 251–262.CrossRefGoogle Scholar
Cooper, L. A. & Lewis, F. A. (1993). Parasitic castration by Schistosoma mansoni does not prevent infected Biomphalaria glabrata snails from acting as males. Abstracts of the ASTMH/ASP Meeting, Atlanta, p. 304.Google Scholar
Crews, A. E. & Yoshino, T. P. (1989). Schistosoma mansoni: effect of infection on reproduction and gonadal growth in Biomphalaria glabrata. Experimental Parasitology 68, 326–334.CrossRefGoogle ScholarPubMed
Dazo, B. C., Hairston, N. G. & Dawood, I. K. (1966). The ecology of Bulinus truncatus and Biomphalaria alexandrina and its implications for the control of bilharziasis in the Egypt-49 project area. Bulletin of the World Health Organization 35, 339–356.Google Scholar
Dewsbury, D. A. (1992). Ejaculate cost and mate choice. American Naturalist 119, 601–610.Google Scholar
Keymer, A. E. & Read, A. F. (1991). Behavioural ecology: the impact of parasitism. In Parasite–Host Associations (ed. Toft, C. A., Aeschlimann, A. & Bolis, L.), pp. 37–61. Oxford University Press, Oxford.CrossRefGoogle Scholar
Lefcort, H. & Baynes, C. J. (1991). Thermal preferences of resistant and susceptible strains of Biomphalaria glabrata (Gastropoda) exposed to Schistosoma mansoni (Trematoda). Parasitology 103, 357–362.Google Scholar
Lodes, M. J. & Yoshino, T. P. (1990). The effects of schistosome excretory–secretory products on Biomphalaria glabrata haemocyte motility. Journal of Invertebrate Pathology 56, 75–85.CrossRefGoogle Scholar
McLennan, D. A. & Shires, V. L. (1995). Correlation between the level of infection with Bunodera inconstans and Neoechinorhynchus rutili and behavioral intensity in female brook sticklebacks. Journal of Parasitology 81, 675–682.CrossRefGoogle ScholarPubMed
Meulemann, E. A. (1972). Host–parasite interrelationships between the freshwater pulmonate Biomphalaria pfeifferi and the trematode Schistosoma mansoni. Netherlands Journal of Zoology 22, 355–427.Google Scholar
Minchella, D. J. (1985). Host life-history variation in response to parasitism. Parasitology 90, 205–216.CrossRefGoogle Scholar
Minchella, D. J. & LoVerde, P. T. (1981). Laboratory comparison of the relative success of Biomphalaria glabrata stocks which are susceptible and insusceptible to infection with Schistosoma mansoni. Parasitology 86, 335–344.Google Scholar
Moore, J. & Gotelli, N. J. (1990). A phylogenetic perspective on the evolution of altered host behavior: A critical look at the manipulation hypothesis. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.), pp. 193–229. Taylor and Francis, Ltd, London.Google Scholar
Pan, C. T. (1965). Studies on the host–parasite relationship between Schisosoma mansoni and Australorbis glabratus. American Journal of Tropical Medicine and Hygiene 14, 931–976.CrossRefGoogle Scholar
Richards, C. S. (1975). Genetic studies on variation in infectivity of Schisostoma mansoni. Journal of Parasitology 61, 233–236.Google Scholar
Richards, C. S., Knight, M. & Lewis, F. A. (1992). Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitology Today, 8 171–174.CrossRefGoogle ScholarPubMed
Rupprecht, H., Becker, W. & Schwanbek, A. (1989). Alterations of hemolymph components in Biomphalaria glabrata during long time infection with Schistosoma mansoni. Parasitology Research 75, 233–237.CrossRefGoogle Scholar
Sturrock, B. M. (1966). The influence of infection with Schistosoma mansoni on the growth rate and reproduction of Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology 60, 187–197.CrossRefGoogle ScholarPubMed
Sturrock, R. F. (1973). Field studies on the transmission of Schistosoma mansoni and on the bionomics of its intermediary host, Biomphalaria glabrata, on St Lucia, West Indies. International Journal for Parasitology 3, 175–194.Google Scholar
Sturrock, R. F. & Webb, G. (1971). The application of catalytic models to schistosomiasis in snails. Journal of Helminthology 45, 189–200.Google Scholar
Théron, A. & Gerard, C. (1994). Development of accessory sexual organs in Biomphalaria glabrata (Planorbidae) in relation to timing of infection by Schistosoma mansoni: consequences for energy utilisation patterns by the parasite. Journal of Molluscan Studies 60, 25–31.Google Scholar
Thompson, S. N. & Mejia-Scales, V. (1989). Effects of Schistosoma mansoni on the nutrition of its intermediate host, Biomphalaria glabrata. Journal of Parasitology 75, 329–332.CrossRefGoogle ScholarPubMed
Thompson, S. N., Lee, R. W.-K., Mejia-Scales, V. & shams, el-din M. (1993). Biochemical and morphological pathology of the foot of the schistosome vector Biomphalaria glabrata infected with Schistosoma mansoni. Parasitology 107, 275–285.Google Scholar
Vianey-Liaud, M. (1973). Influence du jeûne sur la production d’oeufs et la ponte chez le planorbe Australorbis glabratus (gastérpode pulmoné). Bulletin de la Societe Zoologique de France 98, 349–361.Google Scholar
Vianey-Liaud, M. (1990). Biologie de la reproduction de Biomphalaria glabrata (Say, 1818) (mollusque, gastéropode, Planorbidae). Thèse à l’ Université de Montpellier.Google Scholar
Woolhouse, M. E. J. (1989). Estimation of the effect of patent schistosome infections on the mortality rates of Bulinus globosus and Biomphalaria pfeifferi. Annals of Tropical Medicine and Parasitology 88, 137–141.CrossRefGoogle Scholar