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

The ISME Journalvolume 13pages183196 (2019) | Download Citation

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.

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Acknowledgements

For assistance and advice, we thank Guatam Dantas, Mrinalini Watsa, Matt Workentine, PJ Perry, Emily Davenport, Urs Kalbitzer, Jeremy Hogan, Xiaoqing Sun, and Emily Walco. Research was supported by The Eppley Foundation for Research, The International Center for Advanced Renewable Energy and Sustainability (I-CARES), Washington University in St. Louis, and the Alberta Children’s Hospital Research Institute (ACHRI). Research protocols were approved by the Animal Studies Committee of Washington University in St. Louis, Approval No. 20140017, and the Animal Care Committee of the University of Calgary, Approval No. AC15-0161. Capuchin feces were collected in Costa Rica under permission from CONEGABIO, Approval No. R-025-2014-OT-CONEGABIO and exported under Área de Conservación Guanacaste permit number DSVS-029-2014-ACG-PI-060-2014. Feces were imported to Washington University in St. Louis under Center for Disease Control (CDC) permit number 2014-03-093, and transferred to the University of Calgary with permission from the Public Health Agency of Canada (PHAC), Permit No. P-15-6481. Raw sequencing reads are available at the NCBI Sequence Read Archive (SRA) under the accession number SRP156892 and the BioProject PRJNA485217.

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Affiliations

  1. Department of Anthropology & Archaeology, University of Calgary, Calgary, AB, Canada

    • Joseph D. Orkin
    • , Monica S. Myers
    • , Saul E. Cheves Hernandez
    •  & Amanda D. Melin
  2. Alberta Children’s Hospital Research Institute, University of Calgary, Calgary, AB, Canada

    • Joseph D. Orkin
    •  & Amanda D. Melin
  3. Department of Anthropology, Washington University in St. Louis, St. Louis, MO, USA

    • Joseph D. Orkin
    •  & Amanda D. Melin
  4. Department of Anthropology, University of Texas at San Antonio, San Antonio, TX, USA

    • Fernando A. Campos
  5. Department of Biology, Duke University, Durham, NC, USA

    • Fernando A. Campos
  6. Área de Conservación Guanacaste, Guanacaste, Costa Rica

    • Monica S. Myers
    • , Saul E. Cheves Hernandez
    •  & Adrián Guadamuz

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The authors declare that they have no conflict of interest.

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Correspondence to Joseph D. Orkin or Amanda D. Melin.

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https://doi.org/10.1038/s41396-018-0256-0