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The Gut Microbiota Appears to Compensate for Seasonal Diet Variation in the Wild Black Howler Monkey (Alouatta pigra)

  • Host Microbe Interactions
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Abstract

For most mammals, including nonhuman primates, diet composition varies temporally in response to differences in food availability. Because diet influences gut microbiota composition, it is likely that the gut microbiota of wild mammals varies in response to seasonal changes in feeding patterns. Such variation may affect host digestive efficiency and, ultimately, host nutrition. In this study, we investigate the temporal variation in diet and gut microbiota composition and function in two groups (N = 13 individuals) of wild Mexican black howler monkeys (Alouatta pigra) over a 10-month period in Palenque National Park, Mexico. Temporal changes in the relative abundances of individual bacterial taxa were strongly correlated with changes in host diet. For example, the relative abundance of Ruminococcaceae was highest during periods when energy intake was lowest, and the relative abundance of Butyricicoccus was highest when young leaves and unripe fruit accounted for 68 % of the diet. Additionally, the howlers exhibited increased microbial production of energy during periods of reduced energy intake from food sources. Because we observed few changes in howler activity and ranging patterns during the course of our study, we propose that shifts in the composition and activity of the gut microbiota provided additional energy and nutrients to compensate for changes in diet. Energy and nutrient production by the gut microbiota appears to provide an effective buffer against seasonal fluctuations in energy and nutrient intake for these primates and is likely to have a similar function in other mammal species.

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Acknowledgments

This study was funded by a National Geographic Waitt grant (W139-10) and a University of Illinois Dissertation Travel Grant to KRA, a University of Illinois Research Board Grant to PAG, and National Science Foundation grant #0935347 (HOMINID) to SRL, RMS, BAW, and KEN. KRA was also supported by a National Science Foundation Graduate Research Fellowship. We would like to thank Alejandro Estrada and the Universidad Nacional Autonoma de México for logistic support in the field, as well as Brianna Wilkinson and Sarie Van Belle. We thank Gillian Britton for her help in the lab and Manolito Torralba and Marcus Gillis for their help with sequencing at the J. Craig Venter Institute. We also thank CONANP, SEMARNAT, and SAGARPA in Mexico and the CDC in the USA for permits and logistic support. We would like to acknowledge Miguel Martínez Icó and Dave Seigler for their help with tree species identification and Alex Ulanov for his help with metabolite analyses through the Metabolomics Center at the Roy J. Carver Biotechnology Center, University of Illinois at Urbana-Champaign. PAG wishes to thank Chrissie, Sara, and Jenni for their love and support. The authors report no conflicts of interest.

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Authors and Affiliations

  1. Program in Ecology, Evolution, and Conservation Biology, University of Illinois, Urbana, IL, 61801, USA

    Katherine R. Amato

  2. Department of Anthropology, University of Colorado, Boulder, CO, 80309, USA

    Katherine R. Amato & Steven R. Leigh

  3. Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, IL, 61801, USA

    Angela Kent

  4. Department of Animal Sciences, University of Illinois, Urbana, IL, 61801, USA

    Roderick I. Mackie & Bryan A. White

  5. Institute for Genomic Biology, University of Illinois, Urbana, IL, 61801, USA

    Roderick I. Mackie, Rebecca M. Stumpf, Brenda A. Wilson & Bryan A. White

  6. Department of Animal and Range Sciences, Montana State University, Bozeman, MT, 59717, USA

    Carl J. Yeoman

  7. Department of Anthropology, University of Illinois, Urbana, IL, 80301, USA

    Rebecca M. Stumpf & Paul A. Garber

  8. Department of Microbiology, University of Illinois, Urbana, IL, 61801, USA

    Brenda A. Wilson

  9. The J. Craig Venter Institute, Rockville, MD, 20850, USA

    Karen E. Nelson

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  1. Katherine R. Amato
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  2. Steven R. Leigh
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Correspondence to Katherine R. Amato.

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Amato, K.R., Leigh, S.R., Kent, A. et al. The Gut Microbiota Appears to Compensate for Seasonal Diet Variation in the Wild Black Howler Monkey (Alouatta pigra). Microb Ecol 69, 434–443 (2015). https://doi.org/10.1007/s00248-014-0554-7

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