More people, more cats, more parasites: Human population density and temperature variation predict prevalence of Toxoplasma gondii oocyst shedding in free-ranging domestic and wild felids

Abstract

Toxoplasma gondii is a ubiquitous zoonotic parasite that can infect warm-blooded vertebrates, including humans. Felids, the definitive hosts, drive T. gondii infections by shedding the environmentally resistant stage of the parasite (oocysts) in their feces. Few studies characterize the role of climate and anthropogenic factors in oocyst shedding among free-ranging felids, which are responsible for the majority of environmental contamination. We determined how climate and anthropogenic factors influence oocyst shedding in free-ranging domestic cats and wild felids using generalized linear mixed models. T. gondii oocyst shedding data from 47 studies were systematically reviewed and compiled for domestic cats and six wild felid species, encompassing 256 positives out of 9,635 total fecal samples. Shedding prevalence in domestic cats and wild felids was positively associated with human population density at the sampling location. Larger mean diurnal temperature range was associated with more shedding among domestic cats and warmer temperature in the driest quarter was associated with lower oocyst shedding in wild felids. Increasing human population density and temperature fluctuation can exacerbate environmental contamination with the protozoan parasite T. gondii. Management of free-ranging domestic cats could lower the burden of environmental oocysts due to their large population sizes and affinity with human settlements.

The role of species ecology in predicting Toxoplasma gondii prevalence in wild and domesticated mammals globally

“…Species with higher vagility may have an increased prevalence due to the increased probability of travelling through an area with a high T. gondii infection risk. Factors that are associated with increased T. gondii prevalence in wildlife are exposure to urbanization [31,[48][49][50], agriculture [51], sewage [52,53], anthropogenic food provisioning [54] and domestic cat abundance [29][30][31]. Synanthropic wildlife often suffer from higher pathogen loads [55], but as we were unaware of any indices of synanthropism for wildlife taxa, we could not test that explicitly.…”

“…Our final objective compared prevalence patterns between domestic animals (cattle, sheep, pigs) and free-ranging wildlife from the same taxonomic family. We predicted domestic animals would have higher infection rates due to previously demonstrated associations between anthropogenic disturbance and T. gondii [29][30][31].…”

“…Carnivores that scavenge may have an even higher risk of T. gondii infection because scavengers that consume higher trophic levels have increased potential for bioaccumulation. Scavenging taxa also often have a predilection for using anthropogenic subsidies, a known risk factor for T. gondii [30,31]. Therefore, we predicted that globally, T. gondii prevalence would increase with carnivory and scavenging.…”

“…Scavenging taxa also often have a predilection for using anthropogenic subsidies, a known risk factor for T . gondii [ 30 , 31 ]. Therefore, we predicted that globally, T .…”

“…There are strong geographic determinants of T . gondii infection risk, such as human density [ 30 , 31 ], landscape conversion [ 35 ] and free-roaming cat density [ 29 , 31 ]. Therefore, we predicted that highly vagile species would have an increased probability of infection due to the increased probability of travelling through these high-risk locations.…”