Hostname: page-component-f7d5f74f5-qtg9w Total loading time: 0 Render date: 2023-10-03T12:13:57.652Z Has data issue: false Feature Flags: { "corePageComponentGetUserInfoFromSharedSession": true, "coreDisableEcommerce": false, "coreDisableSocialShare": false, "coreDisableEcommerceForArticlePurchase": false, "coreDisableEcommerceForBookPurchase": false, "coreDisableEcommerceForElementPurchase": false, "coreUseNewShare": true, "useRatesEcommerce": true } hasContentIssue false

Decreased predator avoidance in parasitized mice: neuromodulatory correlates

Published online by Cambridge University Press:  06 April 2009

M. Kavaliers
Division of Oral Biology, Faculty of Dentistry and Neuroscience Program, University of Western Ontario, London, Ontario, CanadaN6A 5C1
D. D. Colwell
Agriculture and Agri-Food Canada Box 3000, Main, Lethbridge, Alberta, CanadaT1J 4B1


Although parasites are reported to alter host responses to predators, little is known about the neurochemical mechanisms involved. Using an odour preference test, we examined the effects of an acute, subclinical infection with the naturally occurring, single host, enteric protozoan parasite, Eimeria vermiformis, on the responses of male laboratory mice, Mus musculus, to a predator. Uninfected mice avoided the odour of a predatory cat, spending a minimal amount of time in a Y-maze in the vicinity of the cat odour. In contrast, mice infected with E. vermiformis, spent a significantly greater amount of time in the proximity of the cat odour, showing a reduced avoidance of the cat odour and a reduction in predator-induced fear or anxiety. This was not related to augmented opioid activity and decreased pain sensitivity in the infected mice, as neither treatment with the exogenous opiate, morphine, nor restraint stress-induced augmentation of endogenous opioid activity, had any significant effects on the responses of uninfected mice to cat odour. The altered responses of the infected mice to the cat odour were reduced by peripheral administration of the gamma-aminobutyric A (GABAA) antagonists, bicuculline and picrotoxin, but were not significantly affected by either the benzodiazepine antagonist, Ro 15–1788, the opiate antagonist, naloxone, or the excitatory amino acid, N-methyl-D-aspartate (NMDA) antagonist, MK-801. These results indicate that infection with E. vermiformis in mice reduces the avoidance of predator odour through neurochemical systems associated with anxiety involving, at least in part, GABAA receptor mechanisms.

Research Article
Copyright © Cambridge University Press 1995

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.)



Andrews, N., Hogg, S. & Gonzalez, S. E. (1994). 5-HT1A receptors in the median raphe nucleus and dorsal hippocampus may mediate anxiolytic and anxiogenic behaviours respectively. Brain Research 264, 259–64.Google ScholarPubMed
Blagburn, B. L., Adams, J. H. & Todd, S. D. Jr., (1982). First asexual generation of Eimeria vermiformis Ernst, Chobotar and Hammond, 1971, in Mus musculus. Journal of Parasitology 68, 1178–80.CrossRefGoogle ScholarPubMed
Blanchard, D. C., Blanchard, R. J., Rodgers, R. J. & Weiss, S. M. (1990). The characterization and modelling of antipredator defensive behavior. Neuroscience and Biobehavioral Reviews 14, 463–72.CrossRefGoogle ScholarPubMed
Blanchard, D. C., Weatherspoon, A., Shepherd, J., Rodgers, R. J., Weiss, S. M. & Blanchard, R. J. (1991). ‘Paradoxical’ effects of morphine on antipredator defense reactions in wild and laboratory rats. Pharmacology, Biochemistry and Behavior 40, 819–28.CrossRefGoogle ScholarPubMed
Colwell, D. D. & Kavaliers, M. (1993). Altered nociceptive responses of mice infected with Eimeria vermiformis: evidence for involvement of endogenous opioid systems. Journal of Parasitology 79, 751–6.CrossRefGoogle Scholar
Coopersmith, C. B. & Lenington, S. (1992). Female preferences based on male quality in house mice: interaction between male dominance and t-complex genotype. Ethology 90, 116.CrossRefGoogle Scholar
Dobson, A. P. (1988). The population biology of parasite-induced changes in host behavior. Quarterly Review of Biology 63, 149–65.CrossRefGoogle ScholarPubMed
File, S. E. (1991). The biological basis of anxiety. In Current Practices and Future Developments in the Pharmacotherapy of Mental Disorders (ed. Meltzer, H. Y. & Nerozzi, D.) pp. 159165, Amsterdam, Elsevier.Google Scholar
File, S. E., Zangrossi, H. Jr. & Andrews, N. (1993). Novel environment and cat odor change GABA and 5-HT release and uptake in the rat. Pharmacology Biochemistry and Behavior 45, 931–4.CrossRefGoogle ScholarPubMed
Giles, N. (1987). Predation risk and reduced foraging activity in fish: experiments with parasitized and non-parasitized three-spined sticklebacks, Gasterosteus aculeatus L. Journal of Fish Biology 31, 3744.CrossRefGoogle Scholar
Godin, J.-G. J. & Sproul, C. D. (1988). Risk taking in parasitized sticklebacks under threat of predation: effects of energetic need and food availability. Canadian Journal of Zoology 66, 2360–7.CrossRefGoogle Scholar
Heiligenberg, W. (1991). The neural basis of behavior: a neuroethological view. Annual Review of Neuroscience 14, 247–67.CrossRefGoogle ScholarPubMed
Holmes, J. C. & Bethel, W. M. (1972). Modification of intermediate host behaviour by parasites. In Behavioural Aspects of Parasite Transmission (ed. Canning, E. U. & Wright, C. A.) pp. 123149, London: Academic Press.Google Scholar
Holmes, J. C. & Zohar, S. (1990). Pathology and host behaviour. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.) pp. 3463, London: Taylor and Francis.Google Scholar
Hoogenboom, I. & Dijkstra, C. (1987). Sarcocystis cernae: a parasite increasing the risk of predation of its intermediate host, Microtus arvalis. Oceologia 74, 8692.CrossRefGoogle ScholarPubMed
Hudson, P. D., Dobson, A. P. & Newborn, D. (1992). Do parasites make prey vulnerable to predation? Red grouse and parasites. Journal of Animal Ecology 61, 681–92.CrossRefGoogle Scholar
Kavaliers, M. (1988). Evolutionary and comparative aspects of nociception. Brain Research Bulletin 21, 923–31.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Colwell, D. D. (1991). Sex differences in opioid and nonopioid mediated predator-induced analgesia in mice. Brain Research 568, 173–7.CrossRefGoogle Scholar
Kavaliers, M. & Colwell, D. D. (1992). Parasitism, opioid systems and host behaviour. Advances in Neuroimmunology 2, 287–95.CrossRefGoogle Scholar
Kavaliers, M. & Colwell, D. D. (1993). Multiple opioid system involvement in the mediation of parasitic-infection induced analgesia. Brain Research 623, 316–20.CrossRefGoogle ScholarPubMed
Kavaliers, M. & Colwell, D. D. (1994). Parasite infection attenuates nonopioid mediated predator-induced analgesia in mice. Physiology and Behavior 55, 505–10.CrossRefGoogle ScholarPubMed
Kavaliers, M., Wiebe, J. P. & Galea, L. A. M. (1994 a). Reduction of predator odor-induced anxiety in mice by the neurosteroid 3α-hydroxy-4-pregnen-20-one (3αHP). Brain Research 645, 325–9.CrossRefGoogle Scholar
Kavaliers, M., Wiebe, J. P. & Galea, L. A. M. (1994 b). Male preference for the odors of estrous female mice is enhanced by the neurosteroid 3a-hydroxy-4-pregnene-20-one (3aHP). Brain Research 646, 140–140.CrossRefGoogle Scholar
Majewska, M. D. (1992). Neurosteroids: endogenous bimodal modulation of the GABAA receptor: mechanism of action and physiological significance. Progress in Neurobiology 38, 379–85.CrossRefGoogle ScholarPubMed
Martin, W. R. (1984). Pharmacology of opioids. Pharmacological Reviews 5, 283323.Google Scholar
Milinski, M. (1984). Parasites determine a predators optimal feeding strategy. Behavioral Ecology and Sociobiology 15, 35–7.CrossRefGoogle Scholar
Milinski, M. (1985). Risk of predation of parasitized sticklebacks (Gasterosteus aculeatus L.) under competition for food. Behaviour 93, 203–16.CrossRefGoogle Scholar
Milinski, M. (1990). Parasites and host decision making. In Parasitism and Host Behaviour (ed. Barnard, C. J. & Behnke, J. M.) pp. 95116, London: Taylor and Francis.Google Scholar
Moller, A. P., Dufva, R. & Allander, K. (1993). Parasites and the evolution of host social behavior. Advances in the Study of Behaviour 23, 65102.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. 193223, London: Taylor and Francis.Google Scholar
Porro, C. A. & Carli, G. (1988). Immobilization and restraint effects on pain reactions in animals. Pain 32, 289307.CrossRefGoogle ScholarPubMed
Poulin, R. (1993). Age-dependent effects of parasites on anti-predator responses in two New Zealand freshwater fish. Oceologia 96, 431–8.CrossRefGoogle ScholarPubMed
Poulin, R. (1994). Meta-analysis of parasite-induced behavioural changes. Animal Behaviour 48, 137–46.CrossRefGoogle Scholar
Purdy, R. H., Morrow, A. L., Moore, P. & Paul, S. M. (1991). Stress-induced elevations of gamma-aminobutyric acid type A receptor active steroids in the rat brain. Proceedings of the National Academy of Sciences, USA 88, 4553–7.CrossRefGoogle ScholarPubMed
Rose, M. E. & Hesketh, P. (1976). Immunity to coccidiosis: stages of the life-cycle of Eimeria vermiformis which induce and are affected by the response of the host. Parasitology 73, 2537.CrossRefGoogle Scholar
Rose, M. E., Owen, D. G. & Hesketh, P. (1984). Susceptibility to coccidiosis: effect of strain of mouse on reproduction of Eimeria vermiformis. Parasitology 88, 45–45.CrossRefGoogle ScholarPubMed
Thompson, S. N. & Kavaliers, M. (1994). Physiological bases for parasite-induced alterations of host behaviour. Parasitology 109, S119S138.CrossRefGoogle ScholarPubMed
Temple, S. E. (1987). Do predators always capture substandard individuals disproportionately from prey populations? Ecology 68, 669–669.CrossRefGoogle Scholar
Zangrossi, H. Jr. & File, S. E. (1992). Behavioral consequences in animal tests of anxiety and exploration of exposure to cat odor. Brain Research Bulletin 29, 381–8.CrossRefGoogle ScholarPubMed