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

SIMPLE SUMMARY: Toxoplasma gondii is a zoonotic intracellular parasite which infects a wide range of warm-blooded animals. Long-term studies provide the necessary perspective required to understand those processes which took place over many years in order to address epidemiology and ecology in complex host communities. This study is focused on evaluating what the main long-term determinants of the seroprevalence of T. gondii are in the wild ungulate community from Doñana National Park (southwestern Spain). With this purpose, we assayed sera from 1573 wild ungulates (wild boar, red deer, and fallow deer), collected for 13 years (from 2005 to 2018). We found high seroprevalence values of T. gondii (% ± CI 95%; wild boar 39 ± 3.3; red deer 30.7 ± 4.4; and fallow deer 29.7 ± 4.2. Several factors operating in the medium and long-term (individual, environmental, population and stochastic) explained the risk of T. gondii in wild boar and deer, some of them operating at the community level. ABSTRACT: Toxoplasma gondii is an obligate intracellular protozoan which infects warm-blooded vertebrates, including humans, worldwide. In the present study, the epidemiology of T. gondii was studied in the wild ungulate host community (wild boar, red deer, and fallow deer) of Doñana National Park (DNP, south-western Spain) for 13 years (2005–2018). We assessed several variables which potentially operate in the medium and long-term (environmental features, population, and stochastic factors). Overall, the wild ungulate host community of DNP had high seroprevalence values of T. gondii (STG; % ± confidence interval (CI) 95%; wild boar (Sus scrofa) 39 ± 3.3, n = 698; red deer (Cervus elaphus) 30.7 ± 4.4, n = 423; fallow deer (Dama dama) 29.7 ± 4.2, n = 452). The complex interplay of hosts and ecological/epidemiological niches, together with the optimal climatic conditions for the survival of oocysts that converge in this area may favor the spread of the parasite in its host community. The temporal evolution of STG oscillated considerably, mostly in deer species. The relationships shown by statistical models indicated that several factors determined species patterns. Concomitance of effects among species, indicated that relevant drivers of risk operated at the community level. Our focus, addressing factors operating at broad temporal scale, allows showing their impacts on the epidemiology of T. gondii and its trends. This approach is key to understanding the epidemiology and ecology to T. gondii infection in wild host communities in a context where the decline in seroprevalence leads to loss of immunity in humans.