Abstract
We tested the hypothesis that the parasite Toxoplasma gondii manipulates the behaviour of its intermediate rat host in order to increase its chance of being predated by cats, its feline definitive host, thereby ensuring the completion of its life cycle. Here we report that, although rats have evolved anti-predator avoidance of areas with signs of cat presence, T. gondii's manipulation appears to alter the rat's perception of cat predation risk, in some cases turning their innate aversion into an imprudent attraction. The selectivity of such behavioural changes suggests that this ubiquitous parasite subtly alters the brain of its intermediate host to enhance predation rate whilst leaving other behavioural categories and general health intact. This is in contrast to the gross impediments frequently characteristic of many other host parasite systems. We discuss our results in terms of their potential implications both for the epidemiology of toxoplasmosis and the neurological basis of anxiety and cognitive processes in humans and other mammals.
Full Text
The Full Text of this article is available as a PDF (172.8 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Adamec R. E., Burton P., Shallow T., Budgell J. NMDA receptors mediate lasting increases in anxiety-like behavior produced by the stress of predator exposure--implications for anxiety associated with posttraumatic stress disorder. Physiol Behav. 1999 Jan 1;65(4-5):723–737. doi: 10.1016/s0031-9384(98)00226-1. [DOI] [PubMed] [Google Scholar]
- BURKINSHAW J., KIRMAN B. H., SORSBY A. Toxoplasmosis in relation to mental deficiency. Br Med J. 1953 Mar 28;1(4812):702–704. doi: 10.1136/bmj.1.4812.702. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berdoy M., Webster J. P., Macdonald D. W. Parasite-altered behaviour: is the effect of Toxoplasma gondii on Rattus norvegicus specific? Parasitology. 1995 Nov;111(Pt 4):403–409. doi: 10.1017/s0031182000065902. [DOI] [PubMed] [Google Scholar]
- Beverley J. K. Toxoplasmosis in animals. Vet Rec. 1976 Aug 14;99(7):123–127. doi: 10.1136/vr.99.7.123. [DOI] [PubMed] [Google Scholar]
- Blanchard R. J., Blanchard D. C., Rodgers J., Weiss S. M. The characterization and modelling of antipredator defensive behavior. Neurosci Biobehav Rev. 1990 Winter;14(4):463–472. doi: 10.1016/s0149-7634(05)80069-7. [DOI] [PubMed] [Google Scholar]
- Desmonts G., Couvreur J. Congenital toxoplasmosis. A prospective study of 378 pregnancies. N Engl J Med. 1974 May 16;290(20):1110–1116. doi: 10.1056/NEJM197405162902003. [DOI] [PubMed] [Google Scholar]
- File S. E., Zangrossi H., Jr, Andrews N. Novel environment and cat odor change GABA and 5-HT release and uptake in the rat. Pharmacol Biochem Behav. 1993 Aug;45(4):931–934. doi: 10.1016/0091-3057(93)90142-g. [DOI] [PubMed] [Google Scholar]
- Flegr J., Hrdý I. Influence of chronic toxoplasmosis on some human personality factors. Folia Parasitol (Praha) 1994;41(2):122–126. [PubMed] [Google Scholar]
- Hogg S., File S. E. Regional differences in rat benzodiazepine binding in response to novelty and cat odour. Neuropharmacology. 1994 Jul;33(7):865–868. doi: 10.1016/0028-3908(94)90183-x. [DOI] [PubMed] [Google Scholar]
- Hutchison W. M., Dunachie J. F., Siim J. C., Work K. Life cycle of toxoplasma gondii. Br Med J. 1969 Dec 27;4(5686):806–806. doi: 10.1136/bmj.4.5686.806-b. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kavaliers M., Colwell D. D. Parasite infection attenuates nonopioid mediated predator-induced analgesia in mice. Physiol Behav. 1994 Mar;55(3):505–510. doi: 10.1016/0031-9384(94)90108-2. [DOI] [PubMed] [Google Scholar]
- Kavaliers M., Colwell D. D. Sex differences in opioid and non-opioid mediated predator-induced analgesia in mice. Brain Res. 1991 Dec 24;568(1-2):173–177. doi: 10.1016/0006-8993(91)91394-g. [DOI] [PubMed] [Google Scholar]
- Klein S. L., Lambert K. G., Durr D., Schaefer T., Waring R. E. Influence of environmental enrichment and sex on predator stress response in rats. Physiol Behav. 1994 Aug;56(2):291–297. doi: 10.1016/0031-9384(94)90197-x. [DOI] [PubMed] [Google Scholar]
- Mitchell D. Experiments on neophobia in wild and laboratory rats: a reevaluation. J Comp Physiol Psychol. 1976 Feb;90(2):190–197. doi: 10.1037/h0077196. [DOI] [PubMed] [Google Scholar]
- Nokes C., Grantham-McGregor S. M., Sawyer A. W., Cooper E. S., Bundy D. A. Parasitic helminth infection and cognitive function in school children. Proc Biol Sci. 1992 Feb 22;247(1319):77–81. doi: 10.1098/rspb.1992.0011. [DOI] [PubMed] [Google Scholar]
- Ostlind D. A., Nartowicz M. A., Mickle W. G. Efficacy of ivermectin against Syphacia obvelata (Nematoda) in mice. J Helminthol. 1985 Sep;59(3):257–261. doi: 10.1017/s0022149x00008051. [DOI] [PubMed] [Google Scholar]
- Poulin R. The evolution of parasite manipulation of host behaviour: a theoretical analysis. Parasitology. 1994;109 (Suppl):S109–S118. doi: 10.1017/s0031182000085127. [DOI] [PubMed] [Google Scholar]
- Rau M. E. Establishment and maintenance of behavioural dominance in male mice infected with Trichinella spiralis. Parasitology. 1983 Apr;86(Pt 2):319–322. doi: 10.1017/s0031182000050484. [DOI] [PubMed] [Google Scholar]
- Rau M. E. Loss of behavioural dominance in male mice infected with Trichinella spiralis. Parasitology. 1984 Apr;88(Pt 2):371–373. [PubMed] [Google Scholar]
- Thompson S. N., Kavaliers M. Physiological bases for parasite-induced alterations of host behaviour. Parasitology. 1994;109 (Suppl):S119–S138. doi: 10.1017/s0031182000085139. [DOI] [PubMed] [Google Scholar]
- Webster J. P., Brunton C. F., MacDonald D. W. Effect of Toxoplasma gondii upon neophobic behaviour in wild brown rats, Rattus norvegicus. Parasitology. 1994 Jul;109(Pt 1):37–43. doi: 10.1017/s003118200007774x. [DOI] [PubMed] [Google Scholar]
- Webster J. P., Gowtage-Sequeira S., Berdoy M., Hurd H. Predation of beetles (Tenebrio molitor) infected with tapeworms (Hymenolepis diminuta): a note of caution for the manipulation hypothesis. Parasitology. 2000 Mar;120(Pt 3):313–318. doi: 10.1017/s003118209900548x. [DOI] [PubMed] [Google Scholar]
- Webster J. P. Prevalence and transmission of Toxoplasma gondii in wild brown rats, Rattus norvegicus. Parasitology. 1994 May;108(Pt 4):407–411. doi: 10.1017/s0031182000075958. [DOI] [PubMed] [Google Scholar]
- Webster J. P. The effect of Toxoplasma gondii and other parasites on activity levels in wild and hybrid Rattus norvegicus. Parasitology. 1994 Dec;109(Pt 5):583–589. doi: 10.1017/s0031182000076460. [DOI] [PubMed] [Google Scholar]
- Werner H., Masihi K. N., Senk U. Latent toxoplasma-infection as a possible risk factor for CNS-disorders. Zentralbl Bakteriol Mikrobiol Hyg A. 1981 Sep;250(3):368–375. [PubMed] [Google Scholar]