Dataset Information

Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest.

ABSTRACT: Research on the gut microbiota of free-ranging mammals is offering new insights into dietary ecology. However, for free-ranging primates, little information is available for how microbiomes are influenced by ecological variation through time. Primates inhabiting seasonal tropical dry forests undergo seasonally specific decreases in food abundance and water availability, which have been linked to adverse health effects. Throughout the course of a seasonal transition in 2014, we collected fecal samples from three social groups of free-ranging white-faced capuchin monkeys (Cebus capucinus imitator) in Sector Santa Rosa, Área de Conservación Guanacaste, Costa Rica. 16S rRNA sequencing data reveal that unlike other primates, the white-faced capuchin monkey gut is dominated by Bifidobacterium and Streptococcus. Linear mixed effects models indicate that abundances of these genera are associated with fluctuating availability and consumption of fruit and arthropods, whereas beta diversity clusters by rainfall season. Whole shotgun metagenomics revealed that the capuchin gut is dominated by carbohydrate-binding modules associated with digestion of plant polysaccharides and chitin, matching seasonal dietary patterns. We conclude that rainfall and diet are associated with the diversity, composition, and function of the capuchin gut microbiome. Additionally, microbial fluctuations are likely contributing to nutrient uptake and the health of wild primate populations.

SUBMITTER: Orkin JD

PROVIDER: S-EPMC6298967 | biostudies-literature | 2019 Jan

REPOSITORIES: biostudies-literature

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Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest.

Orkin Joseph D JD Campos Fernando A FA Myers Monica S MS Cheves Hernandez Saul E SE Guadamuz Adrián A Melin Amanda D AD

The ISME journal 20180822 1

Research on the gut microbiota of free-ranging mammals is offering new insights into dietary ecology. However, for free-ranging primates, little information is available for how microbiomes are influenced by ecological variation through time. Primates inhabiting seasonal tropical dry forests undergo seasonally specific decreases in food abundance and water availability, which have been linked to adverse health effects. Throughout the course of a seasonal transition in 2014, we collected fecal sa ...[more]

PMID: 30135468

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Project description:BackgroundEnergy demands associated with pregnancy and lactation are significant forces in mammalian evolution. To mitigate increased energy costs associated with reproduction, female mammals have evolved behavioural and physiological responses. Some species alter activity to conserve energy during pregnancy and lactation, while others experience changes in metabolism and fat deposition. Restructuring of gut microbiota with shifting reproductive states may also help females increase the energy gained from foods, especially during pregnancy. The goal of this study was to examine the relationships among behaviour, gut microbiota composition, and reproductive state in a wild, non-human primate to better understand reproductive ecology. We combined life history data with > 13,000 behavioural scans and 298 fecal samples collected longitudinally across multiple years from 33 white-faced capuchin monkey (Cebus imitator) females. We sequenced the V4 region of the 16S rRNA gene and used the DADA2 pipeline to analyze microbial diversity. We used PICRUSt2 to assess putative functions.ResultsReproductive state explained some variation in activity, but overall resting behaviours were relatively stable across pregnancy and lactation. Foraging was less frequent among females in the early stage of nursing compared to the cycling stage, though otherwise remained at comparable levels. Maximum temperature was a strong, significantly positive predictor of resting, while social dominance had a small but significantly negative effect on resting. Ecological variables such as available fruit biomass and rainfall had a small but significantly positive effects on measures of foraging time. Gut microbial community structure, including richness, alpha diversity, and beta diversity remained stable across the reproductive cycle. In pairwise comparisons, pregnant females exhibited increased relative abundances of multiple microbial ASVs, suggesting small changes in relation to reproductive state. Reproductive state was not linked to differential abundance of putative metabolic pathways.ConclusionsPrevious data suggest that activity budget and the gut microbiome shifts considerably during reproduction. The present study finds that both activity and gut microbial communities are less associated with reproduction compared to other predictors, including ecological contexts. This suggests that behavioural flexibility and gut microbial community plasticity is contrained by ecological factors in this population. These data contribute to a broader understanding of plasticity and stability in response to physiological shifts associated with mammalian reproduction.

Project description:The extent to which interspecific niche differences structure plant communities is highly debated, with extreme viewpoints ranging from fine-scaled niche partitioning, where every species in the community is specialized to a distinct niche, to neutrality, where species have no niche or fitness differences. However, there exists a default position wherein niches of species in a community are determined by their evolutionary and biogeographic histories, irrespective of other species within the community. According to this viewpoint, a broad range of pair-wise niche overlaps-from completely overlapping to completely distinct-are expected in any community without the need to invoke interspecific interactions. We develop a method that can test for both habitat associations and niche differences along an arbitrary number of spatial and temporal niche dimensions and apply it to a 24-yr data set of the eight dominant woody-plant species (representing 84% and 76% of total community abundance and basal area, respectively) from a 50-ha permanent plot in a southern Indian tropical dry forest, using edaphic, topographic, and precipitation variables as niche axes. Species separated into two broad groups in niche space-one consisting of three canopy species and the other of a canopy species and four understory species-along axes that corresponded mainly to variation in soil P, Al and a topographic index of wetness. Species within groups tended to have significantly greater niche overlap than expected by chance. Community-wide niche overlap in spatial and temporal niche axes was never smaller than expected by chance. Species-habitat associations were neither necessary nor sufficient preconditions for niche differences to be present. Our results suggest that this tropical dry-forest community consists of several tree species with broadly overlapping niches, and where significant niche differences do exist, they are not readily interpretable as evidence for niche differentiation. We argue, based on a survey of the literature, that many of the observed niche differences in tropical forests are more parsimoniously viewed as autecological differences between species that exist independently of interspecific interactions.

Dataset Information

Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest.

Publications

Seasonality of the gut microbiota of free-ranging white-faced capuchins in a tropical dry forest.

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