Costs and drivers of helminth parasite infection in wild female baboons

Abstract

Helminth parasites can have wide‐ranging, detrimental effects on host reproduction and survival. These effects are best documented in humans and domestic animals, while only a few studies in wild mammals have identified both the forces that drive helminth infection risk and their costs to individual fitness. Working in a well‐studied population of wild baboons (Papio cynocephalus) in the Amboseli ecosystem in Kenya, we pursued two goals, to (a) examine the costs of helminth infections in terms of female fertility and glucocorticoid hormone levels and (b) test how processes operating at multiple scales—from individual hosts to social groups and the population at large—work together to predict variation in female infection risk. To accomplish these goals, we measured helminth parasite burdens in 745 faecal samples collected over 5 years from 122 female baboons. We combine these data with detailed observations of host environments, social behaviours, hormone levels and interbirth intervals (IBIs). We found that helminths are costly to female fertility: females infected with more diverse parasite communities (i.e., higher parasite richness) exhibited longer IBIs than females infected by fewer parasite taxa. We also found that females exhibiting high Trichuris trichiura egg counts also had high glucocorticoid levels. Female infection risk was best predicted by factors at the host, social group and population level: females facing the highest risk were old, socially isolated, living in dry conditions and infected with other helminths. Our results provide an unusually holistic understanding of the factors that contribute to inter‐individual differences in parasite infection, and they contribute to just a handful of studies linking helminths to host fitness in wild mammals.

Noninvasive measurement of mucosal immunity in a free‐ranging baboon population

“…Using 31 fecal samples from wild baboons for which we had both parasite data and IgA concentrations (obtained with the in‐house ELISA), we tested the relationship IgA concentrations and two measures of parasitism linked to costs in female baboons: Trichuris trichiura egg counts and parasite richness (i.e., the count of distinct parasite species in the sample). T. trichiura is the most common parasite in our population, occurring in 92.5% of the female fecal samples, and in 96% of the male samples (Akinyi et al, 2019; Habig et al, 2019). Furthermore, previous research in our population has found that both T. trichiura egg counts and parasite richness are associated with reduced fertility (i.e., long interbirth intervals) in female baboons (Akinyi et al, 2019).…”

“…T. trichiura is the most common parasite in our population, occurring in 92.5% of the female fecal samples, and in 96% of the male samples (Akinyi et al, 2019; Habig et al, 2019). Furthermore, previous research in our population has found that both T. trichiura egg counts and parasite richness are associated with reduced fertility (i.e., long interbirth intervals) in female baboons (Akinyi et al, 2019). T. trichiura burdens and parasite richness were estimated by counting parasite eggs in fecal samples via fecal flotation and sedimentation (Bowman, 2014; Gillespie, 2006).…”

“…For each sample, two flotation slides were analyzed from a 4 g sample of fecal matter, and five sedimentation slides were analyzed from 2 g of fecal matter. For detailed protocols see Akinyi et al (2019).…”

“…Specifically, lactating females, who bear high energetic costs of milk production and infant carrying, heal more slowly than pregnant and cycling females (Archie, Altmann, & Alberts, 2014). However, females do not differ in helminth infection risk as a function of reproductive state, perhaps because helminth infection is predicted by exposure as well as individual traits or states (Akinyi et al, 2019). Male baboons in Amboseli exhibit little evidence for tradeoffs between reproductive effort and immunity: high‐ranking males engage in higher reproductive effort than low‐ranking males, yet they also heal faster from wounds (Archie, Altmann, & Alberts, 2012) and exhibit equivalent parasite loads to low‐ranking males (Habig et al, 2019).…”

“…Therefore, we predicted that baboons with high fecal IgA will have lower Trichuris trichiura (whipworm) egg count and lower parasite richness. We chose these measures of parasitism because in our population they are linked to reproductive costs in female baboons (Akinyi et al, 2019). Sixth and finally, we tested how IgA concentrations varied in wild baboons as a function of sex, age, and reproductive effort.…”