Are sleeping site ecology and season linked to intestinal helminth prevalence and diversity in two sympatric, nocturnal and arboreal primate hosts (Lepilemur edwardsi and Avahi occidentalis)?

BACKGROUND: Various factors, such as climate, body size and sociality are often linked to parasitism. This constrains the identification of other determinants driving parasite infections. Here, we investigate for the first time intestinal parasites in two sympatric arboreal primate species, which share similar activity patterns, feeding ecology, body size and sociality, and cope with the same climate conditions, but differ in sleeping site ecology: the Milne-Edward's sportive lemur (Lepilemur edwardsi) and the Western woolly lemur (Avahi occidentalis). Comparison of these two species aimed to test whether differences in sleeping sites are related to differences in parasite infection patterns. Additionally, gender and seasonal factors were taken into account. Animals were radio-collared to record their sleeping site dynamics and to collect fecal samples to assess intestinal parasitism during both the dry and the rainy season. RESULTS: Only low parasite diversity was detected, which is attributable to the strict arboreal lifestyle of these lemurs, limiting their contact with infective parasite stages. L. edwardsi, which sleeps in tree holes and repeatedly uses the same sleeping site, excreted eggs of strongyle and oxyurid nematodes, whereby strongyles always occurred in coinfection with oxyurids. In contrast, A. occidentalis, which sleeps on open branches and frequently changes sleeping sites, only excreted eggs of strongyle nematodes. This difference can be attributed to a potential favorable environment presented by tree holes for infective stages, facilitating parasitic transmission. Additionally, Strongylida in A. occidentalis were only observed in the rainy season, suggesting an arrested development during the dry season in the nematodes' life cycle. Males and females of both lemur species showed the same frequency of parasitism. No differences in body mass of infected and non-infected individuals were observed, indicating that the animals' body condition remains unaffected by the detected gastrointestinal parasites. CONCLUSIONS: The comparison of two primate hosts with a very similar lifestyle suggests an influence of the sleeping site ecology on intestinal parasites. In A. occidentalis there was a clear seasonal difference in strongyle egg excretion. These results improve our understanding of the parasite ecology in these endangered primate species, which may be critical in the light of species conservation.

Sleeping site ecology, but not sex, affect ecto- and hemoparasite risk, in sympatric, arboreal primates (Avahi occidentalis and Lepilemur edwardsi).

BACKGROUND: A central question in evolutionary parasitology is to what extent ecology impacts patterns of parasitism in wild host populations. In this study, we aim to disentangle factors influencing the risk of parasite exposure by exploring the impact of sleeping site ecology on infection with ectoparasites and vector-borne hemoparasites in two sympatric primates endemic to Madagascar. Both species live in the same dry deciduous forest of northwestern Madagascar and cope with the same climatic constraints, they are arboreal, nocturnal, cat-sized and pair-living but differ prominently in sleeping site ecology. The Western woolly lemur (Avahi occidentalis) sleeps on open branches and frequently changes sleeping sites, whereas the Milne-Edward's sportive lemur (Lepilemur edwardsi) uses tree holes, displaying strong sleeping site fidelity. Sleeping in tree holes should confer protection from mosquito-borne hemoparasites, but should enhance the risk for ectoparasite infestation with mites and nest-adapted ticks. Sex may affect parasite risk in both species comparably, with males bearing a higher risk than females due to an immunosuppressive effect of higher testosterone levels in males or to sex-specific behavior. To explore these hypotheses, ectoparasites and blood samples were collected from 22 individuals of A. occidentalis and 26 individuals of L. edwardsi during the dry and rainy season. RESULTS: L. edwardsi, but not A. occidentalis, harbored ectoparasites, namely ticks (Haemaphysalis lemuris [Ixodidae], Ornithodoros sp. [Argasidae]) and mites (Aetholaelaps trilyssa, [Laelapidae]), suggesting that sleeping in tree holes promotes infestation with ectoparasites. Interestingly, ectoparasites were found solely in the hot, rainy season with a prevalence of 75% (N = 16 animals). Blood smears were screened for the presence and infection intensity of hemoparasites. Microfilariae were detected in both species. Morphological characteristics suggested that each lemur species harbored two different filarial species. Prevalence of microfilarial infection was significantly lower in L. edwardsi than in A. occidentalis. No significant difference in infection intensity between the two host species, and no effect of season, daytime of sampling or sex on prevalence or infection intensity was found. In neither host species, parasite infection showed an influence on body weight as an indicator for body condition. CONCLUSIONS: Our findings support that sleeping site ecology affects ectoparasite infestation in nocturnal, arboreal mammalian hosts in the tropics, whereas there is no significant effect of host sex. The influence of sleeping site ecology to vector-borne hemoparasite risk is less pronounced. The observed parasite infections did not affect body condition and thus may be of minor importance for shaping reproductive fitness. Findings provide first evidence for the specific relevance of sleeping site ecology on parasitism in arboreal and social mammals. Further, our results increase the sparse knowledge on ecological drivers of primate host-parasite interactions and transmission pathways in natural tropical environments.