Environmental Stress and the Primate Microbiome: Glucocorticoids Contribute to Structure Gut Bacterial Communities of Black Howler Monkeys in Anthropogenically Disturbed Forest Fragments

Abstract

Animals living in anthropogenically disturbed habitats are exposed to environmental stressors which can trigger physiological reactions, such as chronic elevations of glucocorticoid hormones. Physiological responses to stressors may induce changes in the gut microbiome, most likely, facilitated by the gut–brain communication. Although these effects have been observed in humans and animal models, elucidating gut bacterial changes in wild animals under natural stressful conditions is still an ongoing task. Here we analyzed the association between physiological stress related to anthropogenic forest disturbance and changes in gut bacterial communities of black howler monkeys (Alouatta pigra) living in forest fragments in Mexico. We measured individuals’ fecal glucocorticoid metabolites (fGCMs) as an index of physiological stress and created inventories of fecal bacterial communities sequencing the 16S rRNA gene to assess gut microbiome change. We evaluated environmental stress by estimating differences in food availability – feeding tree diversity and biomass – in each group’s habitat. We found that both fGCMs and food availability indices were related to gut bacterial community shifts in black howler monkeys. Furthermore, using structural equation modeling, we found that a decrease in food availability, estimated through reductions in feeding tree basal area, increased fGCMs, which in turn induced increases in bacterial richness. Our findings show that the activation of the hypothalamic–pituitary–adrenal (HPA)-axis, which is a physiological response sensitive to environmental stressors such as the ecological disturbance of a habitat, contributes to structure the gut microbiome of arboreal primates in disturbed forests.

Gut microbiota variations in wild yellow baboons (Papio cynocephalus) are associated with sex and habitat disturbance

“…However, although longitudinal data are currently unavailable to test this hypothesis, the greater challenges between the two habitats (including vast monocultures and frequent clusters of human habitation) may act as deterrent to dispersal, especially considering that safer alternatives are available on both sites (e.g., east of Magombera or along the edge of the Mwanihana forest where forest connectivity is greater). In addition, the release of stressors (such as glucocorticoid) has already been associated with gut microbiota variation in both black howler monkey 61 and eastern lowland gorilla ( G. beringei graueri ) 62 , respectively, and could also be a contributing factor. In any case, additional surveys would be useful for the Udzungwa populations to obtain more information about genetic and ecological dissimilarities between the two habitats (e.g., in diet, stressors, male dispersal) and those associated with age and sex-related physiology (e.g., hormone production, metabolism).…”