Intrinsic and extrinsic determinants of parasite infections in spotted hyenas in the Serengeti National Park

Abstract

Parasite infections have been examined in a limited number of wild mammalian species. These studies have revealed substantial heterogeneity between individuals within a population. Currently little is known about the Darwinian fitness consequences of parasite infections and the factors determining the observed heterogeneity. Key determinants expected to affect individual differences in the infection load of different parasite taxa are host environmental factors, including the social environment, that influence exposure to parasites, and phenotypic characteristics and life-history stages of individual hosts that may be linked to susceptibility to parasite infections. The biotic environment of gastrointestinal parasites, i.e., the assemblage of organisms found in the gastrointestinal tract of the host, collectively called intestinal biome, is also expected to be a key determinant of infection load. Knowledge is limited on the composition, diversity and richness of the intestinal biomes of wild mammals. In this thesis I aimed to investigate determinants of gastrointestinal parasite infections and their fitness consequences in a free-ranging population of a highly social large mammal, the spotted hyena (Crocuta crocuta), in three social groups termed clans in the Serengeti National Park, Tanzania. I hypothesised that individual variation in parasite infections is determined by 1) life-history traits; 2) social, ecological and abiotic environmental factors; 3) host immuno-competence and 4) the gastrointestinal biome community. In chapter 2, I conducted the first metabarcoding (amplicon sequencing) study of the intestinal biome of female spotted hyenas, including both the eukaryome and bacterial microbiome. Consistent with my predictions, juveniles differed in the composition of their bacterial microbiomes from adults, and overall showed a low richness and diversity. The composition, richness and diversity of the eukaryome of females varied with their social status, with high-ranking individuals having a higher richness and diversity than low-ranking individuals. In chapter 3, I investigated the ubiquitous intracellular parasite of warm blooded animals Toxoplasma gondii. I analysed sera from spotted hyenas and sympatric carnivores, including mostly adult lions (Pathera leo), the most abundant large felid in the Serengeti, and also a striped hyena (Hyaena hyaena) and four bat-eared foxes (Otocyon megalotis), an insectivore. This study revealed high seropositivity of adult spotted hyenas and lions. Juvenile spotted hyenas had significantly lower seropositivity than adults, suggesting exposure is primarily caused by the consumption of infected carcasses rather than environmental contamination with T. gondii oocysts. In line with the likely importance of a carnivorous diet for exposure to T.gondii in the Serengeti ecosystem, none of the four analysed bat-eared foxes were positive. In chapter 4, I explored a range of factors likely to determine gastrointestinal parasite infection in individually known juvenile spotted hyenas. In this study I focused on two energetically costly and common parasites, to investigate determinants of infection loads: the intracellular apicomplexan Cystoisospora and the blood feeding, extracellular hookworm (nematode) Ancylostoma. I also assessed the fitness consequences of individual infection load in terms of juvenile survival to adulthood. The results indicate that (1) high hookworm infection load decreased fitness, as the chance of juvenile survival significantly declined as Ancylostoma infection load increased; (2) infection loads of both parasites decreased with age, most likely because immunocompetence in juvenile mammals increases with age; (3) high infection loads were associated with an increase in the number of co-infecting taxa, suggesting a downregulation of immune responses and increased susceptibility to other co-infecting gastrointestinal parasites; (4) hookworm infection load decreased as the number of adult hyenas per clan increased, suggesting an encounter-reduction effect, and (5) Cystoisospora infection load increased as the number of juveniles in the clan increased, suggesting that both transmission during social interactions between juveniles at communal dens and environmental contamination with oocysts at den sites contributed to infection. Overall, the findings presented in my thesis highlight the complex range of factors that affect parasite infections in wild mammal populations and contribute to the considerable heterogeneity between individuals in terms of parasite infection load, parasite community composition and parasite exposure. I found that age (and its effect on both the development of immune processes and diet), social status, the number of juveniles and the number of adults at clan communal dens were key drivers of parasite infection in spotted hyenas. My research revealed that high infection loads with an energetically costly parasite had a negative effect on an important fitness component in juveniles, i.e., survival to adulthood. This finding highlights the ecological and evolutionary importance of such energetically costly parasites in wild mammal populations. Together, the findings in my thesis contribute to the body of knowledge on parasite – host interactions and parasite communities in wild mammalian populations.