Abstract
Macroecological approaches can provide valuable insight into the epidemiology of globally distributed, multi-host pathogens. Toxoplasma gondii is a zoonotic protozoan that infects any warm-blooded animal, including humans, in almost every ecosystem worldwide. There is substantial geographical variation in T. gondii prevalence in wildlife populations and the mechanisms driving this variation are poorly understood. We implemented Bayesian phylogenetic mixed models to determine the association between species’ ecology, phylogeny and climatic and anthropogenic factors on T. gondii prevalence. Toxoplasma gondii prevalence data were compiled for free-ranging wild mammal species from 202 published studies, encompassing 45 079 individuals from 54 taxonomic families and 238 species. We found that T. gondii prevalence was positively associated with human population density and warmer temperatures at the sampling location. Terrestrial species had a lower overall prevalence, but there were no consistent patterns between trophic level and prevalence. The relationship between human density and T. gondii prevalence is probably mediated by higher domestic cat abundance and landscape degradation leading to increased environmental oocyst contamination. Landscape restoration and limiting free-roaming in domestic cats could synergistically increase the resiliency of wildlife populations and reduce wildlife and human infection risks from one of the world's most common parasitic infections.
Highlights
Anthropogenic pressures can promote the emergence of novel pathogens or worsen the disease burden of endemic pathogens [1,2]
The inclusion of human density resulted in the greatest improvement in model support (ΔDIC = 23.97), followed by the inclusion of human footprint index (HFI) (ΔDIC = 17.73)
We found a significant phylogenetic signal for T. gondii prevalence, where phylogenetic variation (λ) accounted for 48% of the random variation, while the variation attributed to species as a random variable accounted for approximately 3.9% of total variation
Summary
Anthropogenic pressures can promote the emergence of novel pathogens or worsen the disease burden of endemic pathogens [1,2]. Latent T. gondii infections in wildlife have been associated with reduced population fitness through altered fetal development [20] and increased mortality due to automobile collisions [21], cold weather [22] and concurrent parasitic infections [23] Given these acute and chronic health impacts of T. gondii for such large numbers of individuals, identifying specific environmental risk factors that are amenable to mitigation, such as anthropogenic landscape changes and domestic animal management, would benefit public and wildlife health initiatives. Mammals in more anthropized locations may have a higher T. gondii prevalence because of land conversion (e.g. impervious surfaces and losses of wetlands [5,29]) effects on oocyst transport and survival and increased exposure to higher densities of free-roaming domestic cats [30], which are the most consequential definitive host species compared to wild felids [28]. We predicted a positive relationship between T. gondii prevalence and these three measures of human impact
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