Fecal avoidance and gastrointestinal parasitism in semi-free ranging woolly monkeys ( Lagothrix lagotricha poeppigii )

Epidemiological studies have identified numerous environmental and individual characteristics underlying the heterogeneity of gastrointestinal parasitism within host populations. However, the contribution of anti-parasite behaviors remains understudied, although recent studies revealed individual variation in their expression. Here, we explored the relationship between individual tendency to exhibit fecal avoidance during feeding tests and gastrointestinal nematode infections in 17 semi-free ranging female woolly monkeys ( Lagothrix lagotricha poeppigii ). We also investigated how parasitism varied with individual age, social connectedness and level of terrestriality, and across seasons. We focused on Strongyloides sp. and Trichuris sp., the two main nematode taxa observed in the population. We found that individual tendency to avoid fecally contaminated food was negatively correlated with Strongyloides sp. infection only. Individual social connectedness was also related to infection status, but while Strongyloides sp. infection increased with the level of spatial proximity, Trichuris sp. infection increased with the rate of body contacts. Furthermore, Strongyloides sp. and Trichuris sp. infections both increased with individual frequency of ground use and decreased with age. Finally, Strongyloides sp. infection showed a seasonal pattern, with females being more parasitized during the dry than the humid season. Differences in parasite life cycles and transmission strategies may have generated the contrasted patterns of infection between Strongyloides sp. and Trichuris sp. We argue that considering individual tendency to avoid parasites among the potential determinants of gastrointestinal parasitism within populations could help to better understand disease dynamics and improve parasite control strategies, which has become a major concern for animal conservation. Significance statement Hosts have evolved behavioral strategies to avoid gastrointestinal parasites, such as fecal avoidance, and their expression varies among individuals. We studied the relationship between nematode infections and individual tendency to avoid feces in a feeding context, social connectedness, level of terrestriality, age and season in female woolly monkeys. Our results revealed that the more females avoided feces, the less they were parasitized, suggesting the efficiency of anti-parasite behavioral strategies. We further found that high social connectedness, intense ground use, young age and dry season were associated with increased parasitism. This study highlights the importance of considering host behaviors in epidemiological models and suggests that hosts can actively mitigate parasite risk by adopting specific anti-parasite behaviors.