Spatial and temporal variation in the gut microbiome of wild, black howler monkeys (Alouatta pigra).

Background/Question/Methods

All mammals rely on mutualistic microbial communities in the gut to provide them with energy via the fermentation of otherwise indigestible material. Laboratory studies have linked differences in host physiology and diet to differences in gut microbial community composition and also suggest that gut microbial community composition influences host immune function and stress response. However, studies of mammals in their natural habitats are needed to more fully understand the mechanisms underlying these relationships. This study investigates the influence of spatial and temporal differences in diet on the gut microbiome of the wild black howler monkey (Alouatta pigra), and the consequences of those differences on host nutrition and health. Because howler monkeys are one of the most folivorous Neotropical primates, they can persist in habitats with limited resource availability and can endure seasonal variation in resource availability, but they rely heavily on the gut microbiome for energy acquisition.

Results/Conclusions

We used molecular methods (ARISA, pyrosequencing) to analyze fecal samples from ten groups of black howlers across three seasons in four habitats (continuous evergreen rainforest, fragmented evergreen rainforest, continuous semi-deciduous forest, captivity) in southeastern Mexico. Gut microbiome composition clustered by howler habitat, and gut microbiome richness and diversity was lower in howlers outside of the continuous evergreen rainforest (F_{3, 31} = 28.91, p < 0.0001). These patterns were correlated with differences in diet diversity and composition across habitats (Spearman’s ρ = 0.820, p < 0.01). Differences in the relative abundance of butyrate producers and hydrogenotrophs, as well as mortality of the eight individuals with the lowest gut microbiome richness suggest health consequences. Across seasons, differences in gut microbiome composition between the evergreen continuous and fragmented forests were maintained. However, gut microbiome richness was higher in the continuous forest only during the dry season, when fruit availability is highest in the region. This pattern was driven by reductions in gut microbiome richness in fragment howlers. Quantitative analyses of diet from fecal samples are underway to confirm that these patterns are associated with changes in diet. Estimates of energy production associated with each gut microbiome are being produced to describe the influence of these changes on host nutrition. This study suggests that the gut microbiome plays an important role in determining howler monkey nutrition and health in response to spatial and temporal variation in food availability. Understanding this role is crucial to our knowledge of primate, and likely mammalian, ecology, evolution, and conservation.