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The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus

Published online by Cambridge University Press:  06 April 2009

J. P. Webster
J. P. Webster
Affiliation:
Wildlife Conservation Research Unit, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS
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Extract

Using both correlational and experimental evidence, the relationship between parasite load and host activity was assessed in brown rats, Rattus norvegicus. Two hypotheses were tested – (1) that parasites with indirect life-cycles, involving transmission between a prey and its predator, will alter the activity of the intermediate host so as to increase its susceptibility to predation by the definitive host and (2) that activity levels in parasitized rats would be increased rather than decreased. Four groups of rats (n = 140) were examined. One group (n = 50) were wild brown rats trapped from 3 UK farmsteads, with naturally occurring parasites. The others were purpose-bred wild/laboratory hybrid rats with experimentally induced parasitic infections of either (n = 15) adult-acquired or (n = 15) congenitally-acquired Toxoplasma gondii (an indirect life-cycle parasite), or (n = 15) Syphacia muris (a direct life-cycle parasite). Uninfected hybrid rats (n = 45), matched for sex, age and weight, served as controls. Rats were housed individually in outdoor cages, and their activities were recorded on video-tapes for 6 non-consecutive 10 h nights. Exercise wheels were also available for the hybrid rats. Out of 6 parasite species detected in the wild rats, T. gondii was the only one which required predation by a definitive host to complete its life-cycle, and was also the only parasite to be associated with higher activity levels in infected than uninfected rats. Hybrid rats infected with T. gondii were also more active than those uninfected, whereas there were no differences in activity levels between S. muris infected and uninfected rats. This study shows that the indirect life-cycle parasite T. gondii can influence the activity of its intermediate host the rat. I suggest that this may facilitate its transmission to the cat definitive host.

Keywords

parasite-altered host behaviourRattus norvegicusToxoplasma gondiiSyphacia murisactivity
Type
Research Article
Information
Parasitology , Volume 109 , Issue 5 , December 1994 , pp. 583 - 589
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

Agriculture Canada (1979). Control of rats and mice. Publication 1370. Information Services, Ottawa, K1A OC97.Google Scholar
Baumans, V., Havenaar, R. ↦ Herck, H Van (1988). The use of repeated treatment with Ivomec and Neguvon spray in the control of murine fur mites and oxyurid worms, Laboratory Animals 22, 246–9.CrossRefGoogle ScholarPubMed
Berdoy, M. (1994). Making decisions in the wild: constraints, conflicts and communication in foraging wild rats. In Behavioural Aspects of Feeding (ed. Galef, B. G. Jr, Mainardi, M. & Valsechi, P.), pp. 289–313. Ettore Majorana International Life Science Series. London: Harwood Academic Publishers.Google Scholar
Berdoy, M. & Macdonald, D. W. (1991). Factors affecting feeding in wild rats. Acta Oecologica 12, 261–79.Google Scholar
Berdoy, M. & Smith, P. (1993). Arms race and rat race: adaptations against poisoning in the brown rat. Review Ecologica 48, 215–28.Google Scholar
Beverley, J. K. A. (1959). Congenital transmission of toxoplasmosis through successive generations of mice. Nature, London 183, 1348–9.CrossRefGoogle ScholarPubMed
Beverley, J. K. A. (1976). Toxoplasmosis in animals. Veterinary Record 99, 123–7.CrossRefGoogle ScholarPubMed
Blackwell, J. M., Roberts, C. W. & Alexander, J. (1994). Influences of genes within the MHC on mortality and brain cyst development in mice infected with Toxoplasma gondii: Kinetics of immune regulation in BALB H-2 congenic mice. Parasite Immunology (in the Press).Google Scholar
Fitzgerald, B. M. & Karl, B. J. (1979). Food of feral house cats (Felis catus L.) in forests of the Orongorongo Valley, Wellington. New Zealand Journal of Zoology 6, 107–26.CrossRefGoogle Scholar
Frenkel, J. K. (1972). Toxoplasmosis. In Pathology of the Nervous System, Vol. 3, (ed. Minckler, J.), pp. 2521–2538. New York: McGraw Hill.Google Scholar
Frenkel, J. K. (1974). Pathology and pathogenesis of congenital toxoplasmosis. Bulletin of the New York Academy of Medicine 50, 182–91.Google ScholarPubMed
Hart, J. A. (1988). Rust fungi and host parasite coevolution – do primitive hosts harbour primitive parasites? Cladistics. The International Journal of the Will Henning Society 4, 339–66.Google Scholar
Hay, J., Hutchison, W. M., Aitken, P. P. & Graham, D. I. (1983 a). The effect of congenital and adult-acquired Toxoplasma infections on the motor performance of mice. Annals of Tropical Medicine and Parasitology 77, 261–77.CrossRefGoogle ScholarPubMed
Hay, J., Aitken, P. P., Hutchison, W. M. & Graham, D. I. (1983 b). The effect of congenital and adult-acquired Toxoplasma infections on activity and responsiveness to novel stimulation in mice. Annals of Tropical Medicine and Parasitology 77, 483–95.CrossRefGoogle ScholarPubMed
Hubel, D. H. & Wiesel, T. N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–54.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Dunachie, J. F., Slim, J. Chr. & Work, K. (1969). The life cycle of Toxoplasma gondii. British Medical Journal 4, 806.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Bradley, M., Cheyne, W. M., Wells, B. W. P. & Hay, J. (1980). Behavioural abnormalities in Toxoplasma-infected mice. Annals of Tropical Medicine and Parasitology 74, 507–10.CrossRefGoogle Scholar
Jackson, M. H., Hutchison, W. M. & Slim, J. Chr. (1986). Toxoplasmosis in a wild rodent population of central Scotland and a possible explanation of the mode of transmission. Journal of Zoology 209, 549–57.CrossRefGoogle Scholar
Kobyashi, T. (1963). Brain-to-body ratios and time of maturation of the mouse brain. American Journal of Physiology 204, 343–6.CrossRefGoogle Scholar
Lewis, J. W. & D'Silva, J. (1986). The life-cycle of Syphacia muris Yamaguti (Nematoda: Oxyuroidea) in the laboratory rat. Journal of Helminthology 60, 39–46.CrossRefGoogle ScholarPubMed
Leyhausen, p. (1979). Cat Behaviour: The Predatory and Social Behaviour of Domestic and Wild Cats. Garland Series in Ethology. New York, London: Garland S. T. P. M. Press.Google Scholar
Martin, P. & Bateson, p. (1988). Measuring Behaviour, an Introductory Guide. Cambridge: Cambridge University Press.Google Scholar
Mitchell, D. (1976). Experiments of neophobia in wild and laboratory rats: a revaluation. Journal of Comparative Physiological Psychology 90, 190–7.CrossRefGoogle Scholar
Moore, J. & Gotelli, N. J. (1990). A phylogenetic perspective on the evolution of altered host behaviours: a critical look at the manipulation hypothesis. In Parasitism and Host Behaviour, (ed. Barnard, C. J. & Behnke, J. M), pp. 193–223. London: Taylor & Francis.Google Scholar
Ostlind, D. A., Nartowicz, M. A. & Mickle, W. G. (1985). Efficacy of ivermectin against Syphacia obvelata (Nematoda) in mice. Journal of Helminthology 59, 257–61.CrossRefGoogle ScholarPubMed
Owen, D. G. (1992). Parasites of laboratory animals. Laboratory Animals Handbook, no. 12. London.Google Scholar
Rau, M. E. (1983). The open-field behaviour of mice infected with Trichinella spiralis. Parasitology 86, 311–18.CrossRefGoogle ScholarPubMed
Rau, M. E. & Putter, L. (1984). Running responses of Trichinella spiralis-infected CD-1 mice. Parasitology 89, 579–83.CrossRefGoogle ScholarPubMed
Sas (1988). SAS Institute Incorporated. Box 8000. Cary, North Carolina, 27511.Google Scholar
Smart, J. L. & Dobbing, J. (1971 a). Vulnerability of the developing brain: II. Effects of ontogeny and development of behaviour in the rat. Brain Research 28, 85–95.CrossRefGoogle ScholarPubMed
Smart, J. L. & Dobbing, J. (1971 b). Vulnerability of the developing brain: VI. Relative effects of fetal and early post-natal undernutrition on reflex ontogeny and development of behaviour in the rat. Brain Research 32, 303–14.CrossRefGoogle Scholar
Smart, J. L., Dobbing, J., Adlar, B. P. F., Lynch, A. & Sands, J. (1973). Vulnerability of the developing brain: relative effects of growth restriction during fetal and suckling periods on behaviour and composition in adult rats. Journal of Nutrition 103, 1327–8.CrossRefGoogle ScholarPubMed
Stretch, R. G. A., Leytham, G. W. H. & Kershaw, W. E. (1960 a). The effect of acute Schistosomiasis upon discrimination learning and activity in mice. Annals of Tropical Medicine and Parasitology 54, 476–86.Google Scholar
Stretch, R. G. A., Leytham, G. W. H. & Kershaw, W. E. (1960 b). The effect of acute Schistosomiasis upon learning in rats under different levels of motivation. Annals of Tropical Medicine and Parasitology 54, 487–92.CrossRefGoogle Scholar
Tsubota, N., Hiraoka, K., Sawada, Y., Ohshima, S. & Ohshima, M. (1977). Studies on latex agglutination test for toxoplasmosis; Evaluation of the microtiter test as a serologic test for toxoplasmosis in some animals. Japanese Journal of Parasitology 26, 291.Google Scholar
Turk, W. P. G. (1981). Q fever. In Medical Microbiology and Infectious Diseases (ed. Braude, A. J., Davis, C. E. & Fierer, J.), pp. 932–948. Toronto: WB Saunders.Google Scholar
Voller, A., Bidwell, D. E. & Bartlett, A. (1976). Enzyme immunosorbent assay in diagnostic medicine; theory and practice. Bulletin of the World Health Organization 53, 55–65.Google Scholar
Waitkins, S. A. (1985). Leptospires and leptospirosis. In Isolation and Identification of Micro-organisms of Medical and Veterinary Importance, (ed. Collins, C. H. & Grange, J. M.), pp. 251–273. London: Academic Press.Google Scholar
Webster, J. P. (1994). Prevalence and transmission of Toxoplasma gondii in wild brown rats, Rattus norvegicus. Parasitology 108, 407–11.CrossRefGoogle ScholarPubMed
Webster, J. P., Brunton, C. F. A. & Macdonald, D. W. (1994). Effect of Toxoplasma gondii on neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology 109, 37–43.CrossRefGoogle ScholarPubMed