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Specificity of the Toxoplasma gondii-altered behaviour to definitive versus non-definitive host predation risk

  • P. H. L. LAMBERTON (a1), C. A. DONNELLY (a2) and J. P. WEBSTER (a1)
Summary
SUMMARY

The hypothesis that the parasite Toxoplasma gondii manipulates the behaviour of its intermediate rat host in order to increase its chance of being predated specifically by its feline definitive host, rather than a non-definitive host predator species, was tested. The impact of a range of therapeutic drugs, previously demonstrated to be effective in preventing the development of T. gondii-associated behavioural and cognitive alterations in rats, on definitive-host predator specificity was also tested. Using a Y-shaped maze design, we demonstrated that T. gondii-associated behavioural changes, apparently aimed to increase predation rate, do appear to be specific to that of the feline definitive host – there were significant and consistent differences between the (untreated) infected and uninfected rats groups where T. gondii-infected rats tended to choose the definitive host feline-predator-associated maze arm and nest-box significantly more often than a maze arm or nest-box treated with non-definitive host predator (mink) odour. Drug treatment of infected rats prevented any such host-specificity from being displayed. We discuss our results in terms of their potential implications both for T. gondii epidemiology and the evolution of parasite-altered behaviour.

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Corresponding author
*Corresponding author and address for request for materials: Department of Infectious Disease Epidemiology, Faculty of Medicine, Imperial College, Norfolk Place, London W2 1PG, UK. E-mail: joanne.webster@imperial.ac.uk
References
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Adamec R. E., Blundell J. and Burton P. (2005). Neural circuit changes mediating lasting brain and behavioral response to predator stress. Neuroscience and Biobehavioural Reviews 29, 12251241.
Adamec R. E., Blundell J. and Burton P. (2006). Relationship of the predatory attack experience to neural plasticity, pCREB expression and neuroendocrine response. Neuroscience and Biobehavioural Reviews 30, 356375.
Adamec R. E., Burton P., Shallow T. and Budgell J. (1999). NMDA receptors mediate lasting increases in anxiety-like behaviour produced by the stress of predator exposure – implications for anxiety associated with post-traumatic stress disorder. Physiology and Behaviour 65, 723737.
Barnard C. J. (1990). Parasitic relationships. In Parasitism and Host Behaviour (ed. Barnard C. J. and Behnke J. M.), pp. 133. Taylor and Francis, London.
Berdoy M., Webster J. P. and Macdonald D. W. (1995). Parasite altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific? Parasitology 111, 403409.
Berdoy M., Webster J. P. and Macdonald D. W. (2000). Fatal attraction in Toxoplasma-infected rats: a case of parasite manipulation of its mammalian host. Proceedings of the Royal Society of London, B 267, 267.
Blanchard R. J., Blanchard D. C., Rodgers J. and Weiss S. M. (1990). The characterisation and modelling of antipredator defensive behavior. Neuroscience and Biochemical Reviews 14, 463472.
Blanchard R. J., Yang M., Li C. I., Gervacio A. and Blanchard D. C. (2001). Cue and context conditioning of defensive behaviors to cat odor stimuli. Neuroscience and Biobehavioural Reviews 25, 587595.
Brun-Pascaud M., Chau F., Garry L., Jacobus D., Derouin F. and Girard P. M. (1996). Combination of PS-15, epiroprim, or pyrimethamine with dapsone in prophylaxis of Toxoplasma gondii and Pneumocystis carinii dual infection in a rat model. Antimicrobial Agents and Chemotherapy 40, 20672070.
Buck L. and Axel R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175187.
Derouin F., Piketty C., Chastang C., Chau F., Rouviex B. and Pocidalo J. J. (1991). Anti-Toxoplasma effects of dapsone alone and combined with pyrimethamine. Antimicrobial Agents and Chemotherapy 35, 252255.
Flecknell P. A., Roughan J. V. and Stewart R. (1999). Use of oral buprenorphine (‘buprenorphine jello’) for postoperative analgesia in rats–a clinical trial. Laboratory Animal 33, 169174.
Girard P. M., Landman R., Gaudebout C., Olivares R., Saimot A. G., Jelazko P., Gaudebout C., Certain A., Boue F., Bouvet E., Lecompte T. and Jean-Coulaud P. (1993). Dapsone-pyrimethamine compared with aerosolized pentamidine as primary prophylaxis against Pneumocystis carinii pneumonia and toxoplasmosis in HIV infection. The New England Journal of Medicine 328, 15141520.
Grostal P. and Dicke M. (1999). Direct and indirect cues of predation risk influence behavior and reproduction of prey: a case for acarine interactions. Behavioural Ecology 10, 422427.
Hendrie C. A., Weiss S. M. and Eilam D. (1996). Exploration and predation models of anxiety: evidence from laboratory and wild species. Pharmacology, Biochemistry and Behavior 54, 1320.
HMSO. (1989). Home Office: Code of Practice for the Housing and Care of Animals used in Scientific Procedures. HMSO, London.
Holmes J. C. and Bethel W. M. (1972). Modification of intermediate behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning E. U. and Wright C. A.), pp. 123149. Academic Press, New York.
Hrda S., Votypka J. and Kodym P. (2000). Transient nature of Toxoplasma gondii-induced behavioural changes in mice. Journal of Parasitology 86, 657663.
Hutchison W. M., Dunachie J. F., Siim J. and Work K. (1969). The life cycle of Toxoplasma gondii. British Medical Journal 94, 806812.
Kapur S., VanderSpek S. C., Brownlee B. A. and Nobrega J. N. (2003). Antipsychotic dosing in preclinical models is often unrepresentative of the clinical condition – a suggested solution based on in vivo occupancy. Journal of Pharmacology and Experimental Therapeutics 305, 625631.
Kemble E. D. (1994). Novel odors increase defensiveness and inhibit attack behaviour in mice. In Ethology and Psychopharmacology (ed. Cooper S. J. and Hendrie C. A.), pp. 191204. John Wiley, Chichester.
Kobayakawa K., Kobayakawa R., Matsumoto H., Oka Y., Imai T., Ikawa M., Okabe M., Ikeda T., Itohara S., Kikusui T., Mori K. and Sakano H. (2007). Innate versus learned odour processing in the mouse olfactory bulb. Nature, London 450, 503510.
LeDoux J. (2003). The emotional brain, fear, and the amygdala. Cellular and Molecular Neurobiology 23, 727738.
Linscombe C., Kinler N. and Aukrich R. J. (1982). Mink. In Wild Mammals of North America: Biology, Management, and Economics (ed. Chapman J. A. and Feldhamer G. A.), pp. 629643. Baltimore, Maryland: The Johns Hopkins University Press.
Mouritsen K. N. and Poulin R. (2003). The mud flat anemone-cockle association: mutualism in the intertidal zone? Oecologia 135, 131137.
Remington J. S. and Krahenbuhl J. L. (1982). Immunology of Toxoplasma gondii. In Immunology of Human Infection Part II. (ed. Nahmias A. J. and O'Reilly J.), pp. 327371. Plenum Publishing Corporation, New York.
Staples L. G., Hunt G. E., Cornish J. L. and McGregor I. S. (2005). Neural activation during cat odor-induced conditioned fear and ‘trial 2’ fear in rats. Neuroscience and Biobehavioural Reviews 29, 12651277.
Torrey E. F. and Yolken R. H. (2003). Toxoplasma gondii and schizophrenia. Emerging Infectious Diseases 9, 13751380.
Vervaeke M., Davis S., Leirs H. and Verhagen R. (2006). Implications of increased susceptibility to predation for managing the sylvatic cycle of Echinococcus multilocularis. Parasitology 132, 893901.
Vyas A., Seon-Kyeong K., Giacomini N., Boothroyd J. C. and Sapolsky R. M. (2007 a). Behavioural changes induced by Toxoplasma infection of rodents are highly specific to aversion of cat odours. Proceedings of the National Academy of Sciences, USA 104, 64426447.
Vyas A., Kim S. K. and Sapolsky R. M. (2007 b). The effects of Toxoplasma infection on rodent behavior are dependent on dose of the stimulus. Neuroscience 148, 342348.
Webster J. P. (1994). The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology 109, 583589.
Webster J. P. (2001). Rats, cats, people and parasites: the impact of latent toxoplasmosis on behaviour. Microbes and Infection 3, 19.
Webster J. P. (2007). The impact of Toxoplasma gondii on animal behaviour: playing cat and mouse. Schizophrenia Bulletin 33, 752756.
Webster J. P., Brunton C. F. A. and Macdonald D. W. (1994). Effect of Toxoplasma gondii on neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology 109, 3743.
Webster J. P., Lamberton P. H. L., Donnelly C. A. and Torrey E. F. (2006). Parasites as causative agents of human affective disorders? The impact of anti-psychotic and anti-protozoan medication on Toxoplasma gondii's ability to alter host behaviour. Proceedings of the Royal Society of London, B 273, 10231030.
Werner H., Masihi K. N. and Senk U. (1981). Latent Toxoplasma infection as a possible risk factor for CNS disorders. Zentralblatt für Bakteriologie Mikrobiologie und Hygiene, I. Abteilung Originale A 250, 368375.
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Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
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