Interaction of diet and habitat predicts Toxoplasma gondii infection rates in wild birds at a global scale

Abstract

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License, which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made. Abstract Aim: Free-ranging wildlife are valuable sentinels for zoonotic, multi-host pathogens, and new insight into parasite transmission patterns is possible through a macroecological approach. Toxoplasma gondii is a protozoan capable of infecting all warmblooded animals, including humans, primarily through a free-living oocyst and/or tissue cyst life stage. Anthropogenic disturbance is facilitating the spread of T. gondii, making it crucial to understand the general ecological and life-history drivers of T. gondii infections in wild birds, which are important intermediate hosts. Our goal was to determine how habitat (terrestrial versus aquatic), dietary trophic level and scavenging behaviour influence the prevalence of T. gondii infection in wild birds at a global scale. Location: Global. Time period: 1952-2017. Major taxa studied: Birds.Methods: Our analysis used the serological, bioassay and molecular prevalence data of T. gondii in avian species compiled from 81 studies conducted worldwide and encompassing 24,344 individuals from 393 avian species from 84 families. Results:We showed that at a global scale, trophic level and habitat interacted significantly to influence T. gondii prevalence in avian intermediate hosts. In the terrestrial environment, T. gondii prevalence increased with trophic level, consistent with predominant tissue cyst transmission. The highest prevalence was in terrestrial omnivores, which might reflect their synanthropic foraging behaviour. In aquatic species, prevalence was more consistent across trophic levels, but high prevalence in aquatic herbivores and insectivores reflects significant waterborne exposure to oocysts.Contrary to our predictions, generalized scavenging per se was not associated with increased prevalence. Main conclusions:This study highlights the value of comparing pathogen prevalence among multiple ecological guilds and ecosystem types for a more comprehensive understanding of the epidemiology of generalist pathogens, such as T. gondii. Increased B I OS K E TCH S U PP O RTI N G I N FO R M ATI O NAdditional supporting information may be found online in the Supporting Information section.We are a group of governmental and non-governmental researchers with a research focus on anthropogenic impacts on wildlife and human health. We adopt a One Health approach to examine zoonotic diseases whose epidemiology is linked to anthropogenic activities, such as urbanization and agricultural activity.

Long-Term Determinants of the Seroprevalence of Toxoplasma gondii in a Wild Ungulate Community

“…Overall, the wild ungulate host community of DNP showed higher STG compared with those reported in the literature of the European and Iberian contexts [ 34 , 61 , 62 ]. Mechanisms determining seroprevalence in different host species of the studied community are related to the life cycle of T. gondii , which involves both an environmental and a trophic transmission route (i.e., trophic relationships among potential hosts of the community; [ 65 ]). Terrestrial herbivores should have the lowest T. gondii exposure, only through the ingestion of oocyst-contaminated vegetation, soil and/or drinking water.…”

Behavioral biology of Toxoplasma gondii infection

“…Manipulative parasites like T. gondii are likely to affect such cascades due to the creation of heterogeneity in the probability of consumption of infected versus non-infected prey. Similarly, the specificity of T. gondii behavior effects, specifically definitive versus dead-end host, might influence prey switching by generalist predators like raptors and owls [ 47 ].…”

Prevalence of Antibodies to Toxoplasma gondii in Different Wild Bird Species Admitted to Rehabilitation Centres in Portugal

“…The global decrease in the number of some avian species [ 3 ], together with the development of anthropogenic activities and the destruction of habitats, contributes to the interaction between the domestic and sylvatic cycles, reinforcing adjustments in the epidemiology of T. gondii [ 4 , 5 ]. Some species of birds develop clinical toxoplasmosis, which can be a considerable concern from the wildlife conservation perspective [ 6 ]. For instance, toxoplasmosis was reported in the Hawaiian crow or ‘alalã ( Corvus hawaiiensis ) and appears to pose a significant threat and a management challenge to the reintroduction programs of this endangered species [ 7 ].…”

“…Wild birds are particularly important intermediate hosts of T. gondii due to their high dispersal capabilities [ 6 ]. Along the flight path, migratory birds can carry infectious disease agents across oceans [ 8 ].…”

“…In addition, wild and domestic birds are excellent sentinels of environmental contamination with T. gondii oocysts, since herbivorous birds feed from the ground, and birds of prey eat intermediate hosts of T. gondii [ 9 , 10 ]. Consequently, there is a huge variety of wild bird species, with different habitats and diets, that may become infected with this parasite [ 6 , 11 ]. In the terrestrial environment, T. gondii prevalence increases with trophic level, consistent with predominant tissue cyst transmission, but in aquatic environment it reflects a considerable waterborne exposure to oocysts [ 6 ].…”