Evidence of high exposure to Toxoplasma gondii in free-ranging and captive African carnivores

Abstract

Toxoplasma gondii is an ubiquitous intracellular protozoan parasite. Mammals and birds are intermediate hosts and felid species are definitive hosts. In most human altered habitats the domestic cat is the predominant definitive host. Current knowledge of T. gondii infection in African ecosystems is limited. This study aimed to assess exposure to T. gondii in wild carnivores in the Serengeti ecosystem in East Africa. Carnivores can be infected by the consumption of tissue cysts when feeding on infected animals and by incidental ingestion of oocysts from environmental contamination. Incidental ingestion should occur regardless of a species’ diet whereas the consumption of cysts should increase the chance of infection in carnivorous species. This predicts higher seropositivity in carnivorous than in insectivorous carnivores and lower seropositivity in juvenile carnivores with a long dependency on milk than in adults. We found high seropositivity in carnivorous species: 100% (15 of 15 samples) in adult African lions, 93% (38 of 41 samples) in adult spotted hyenas and one striped hyena sample was positive, whereas all four samples from the insectivorous bat-eared fox were negative. Juvenile hyenas (11 of 19 sera) had significantly lower seropositivity than adults (38 of 41 sera). Long-term monitoring of spotted hyenas revealed no significant difference in seropositivity between two periods (1988–1992 and 2000 to 2016). Identical results were produced in lion and hyena samples by a commercial multi-species ELISA (at serum dilution 1:10) and an in-house ELISA based on a recombinant T. gondii protein (at serum dilution 1:100), making the latter a useful alternative for small amounts of serum. We suggest that diet, age and lifetime range are factors determining seropositivity in carnivores in the Serengeti ecosystem and suggest that the role of small wild felids in the spread of T. gondii in the African ecosystem warrants investigation.

Species-specific differences in Toxoplasma gondii, Neospora caninum and Besnoitia besnoiti seroprevalence in Namibian wildlife

“…A more recent study from South Africa detected also antibodies against T. gondii in honey badgers, and also confirmed the presence of the parasite [58]. Insectivorous species seem to be more protected from infection with this parasite, as bat-eared foxes showed no antibodies in our study and in a previous study from Tanzania [56]. In herbivores the seroprevalence is low, but varies between species, which might be partially associated with their feeding strategy (e.g.…”

“…Similar to our study, free-ranging African lions, spotted hyenas and caracals had high seropositivity to T. gondii in other studies. African lions had values between 92% and 100% in Botswana, Namibia, South Africa, Tanzania and Zimbabwe [25,55,56], spotted hyenas had values of 93% in Tanzania [56] and caracals of 83% in an urban environment in South Africa [57]. However, in these studies IFAT or ELISAs without confirmatory immunoblot tests were used, thus the prevalences may be in general higher than in our study.…”

“…A cumulative effect of age on the likelihood of T. gondii infection has been previously suggested for many free-ranging species, e.g. spotted hyenas in Tanzania [56], feral cats in South Africa [65] and Iberian lynx (Lynx pardinus) in Spain [66].…”

Parasite infections in a social carnivore: Evidence of their fitness consequences and factors modulating infection load

“…For example, during early life, juveniles are generally more susceptible to infection by pathogens than adults, partly because of their limited capacity to mount an effective immune responses due to qualitative differences in the T‐cell populations of juveniles and adults (Ramsburg et al, ), and naïve, mostly young animals that lack exposure to pathogen antigens have not developed the acquired immune responses that develop as a result of exposure (Cattadori et al, ; Koudela & Kučerová, ). The decrease in Ancylostoma and Cystoisospora infection loads in juvenile hyenas with age may be the combined outcome of increased immunocompetence due to active immune responses induced by parasite exposure, which is likely to increase with age (East et al, ; Ferreira, Torelli, et al, ) and the general maturation of the mammalian immune system in juvenile hyenas with increasing age. Currently, little is known about factors that affect immunocompetence in juvenile hyenas, so in addition to age, factors such as genotype and gene expression (Gulland, Albon, Pemberton, Moorcroft, & Clutton‐Brock, ; Jackson et al, ), allostatic load, physiological processes, behavior, and diet may be relevant (Ardia et al, ; VanderWaal & Ezenwa, ).…”

“…In mammals, age is one intrinsic factor that can alter resistance to infection, because immune processes generally improve from early life to adulthood and then decline in old age (Simon, Hollander, & McMichael, 2015). When young, the cellular immune responses of juveniles typically differ both qualitatively and quantitatively from those of adults (Ramsburg, Tigelaar, Craft, & Hayday, 2003;Watson et al, 2016) and juveniles are less likely to have the acquired immunity that develops following exposure to pathogen antigen than adults, (Cattadori, Boag, Bjørnstad, Cornell, & Hudson, 2005;Ferreira, Torelli, et al, 2019), and thus, juveniles are generally more vulnerable to infection than adults.…”