High prevalence rates of Toxoplasma gondii in cat-hunted small mammals - Evidence for parasite induced behavioural manipulation in the natural environment?

Abstract

Toxoplasma gondii causes one of the most frequent parasitic infections in vertebrates on earth. The present study aimed to assess the occurrence of T. gondii infection in cat-hunted wild small mammals, and to determine the circulating T. gondii genotypes in cat prey. There is evidence suggesting that T. gondii may manipulate rodents' behaviour enhancing transmission to their definitive feline host by facilitating predation. Given that most studies focusing on rodent behavior have been performed under laboratory conditions, we tested this hypothesis in the natural environment. We analysed 157 cat-hunted wild small mammals of six different species from Switzerland. Brain and skeletal muscle samples from each animal were tested for T. gondii DNA by PCR, and positive samples were genotyped using a multilocus sequence typing approach, including 10 genetic markers. Additionally, to evaluate exposure to cat faeces, the presence of Taenia taeniaeformis metacestodes was investigated at necropsy. The prevalence of T. gondii in cat-hunted Arvicola amphibius s.l. was 11.1% (7/63), 14.6% (7/48) in Apodemus spp., 13.6% (3/22) in Myodes glareolus, 6.7% (1/15) in Crocidura russula, and 0% in Microtus arvalis (0/8) and Sorex sp. (0/1). All completely genotyped T. gondii parasites, exhibited the ToxoDB #3 genotype, a Type II variant. We additionally analysed 48 trap-captured A. amphibius s.l., which all tested negative for T. gondii infection, contrasting with the higher prevalence in cat-hunted A. amphibius s.l. (0% vs. 11.1%; p = 0.0176). Furthermore, T. taeniaeformis was detected in both groups, indicating widespread contamination with cat faeces in the sampled areas. These results provide evidence that T. gondii infected rodents are at higher risk to be predated by cats and therewith support the behaviour manipulation hypothesis.