Phylogenetic and ecological factors impact the gut microbiota of two Neotropical primate species
- 1.2k Downloads
Recent studies suggest that variation in diet across time and space results in changes in the mammalian gut microbiota. This variation may ultimately impact host ecology by altering nutritional status and health. Wild animal populations provide an excellent opportunity for understanding these interactions. However, compared to clinical studies, microbial research targeting wild animals is currently limited, and many published studies focus only on a single population of a single host species. In this study we utilize fecal samples from two species of howler monkey (Alouatta pigra and A. palliata) collected at four sites to investigate factors influencing the gut microbiota at three scales: taxonomic (host species), ecosystemic (forest type), and local (habitat disturbance/season). The results demonstrate that the effect of host species on the gut microbiota is stronger than the effect of host forest type, which is stronger than the effect of habitat disturbance or seasonality. Nevertheless, within host species, gut microbiota composition differs in response to forest type, habitat disturbance, and season. Variations in the effect size of these factors are associated both with host species and environment. This information may be beneficial for understanding ecological and evolutionary questions associated with Mesoamerican howler monkeys, as well as determining conservation challenges facing each species. These mechanisms may also provide insight into the ecology of other species of howler monkeys, non-human primates, and mammals.
KeywordsAlouatta Microbiome Habitat Season Disturbance
We would like to thank A. Estrada and the Universidad Nacional Autónoma de México, and Alvaro Molina and the Comité de Manejo Colaborativo del Parque Nacional Volcán Maderas for logistic support in the field, as well as B. Wilkinson and S. Van Belle. Funding was provided by a National Geographic Waitt grant (W139-10), an NSF Graduate Research Fellowship, and a Univ. of IL Dissertation Travel Grant to KRA, as well as the Earth Microbiome Project and NSF grant #0935347 (HOMINID) to SRL, RMS, BAW, and KEN. Thanks to INIFAP and M.C. Antonio Sanchez for permission to work in El Tormento, Mexico. Thanks to CONANP, SEMARNAT, and SAGARPA in Mexico, MARENA in Nicaragua, the Ministerio de Salud in Costa Rica, and the CDC in the US for permits and logistic support. We also appreciate the comments of two anonymous reviewers.
Raw sequence data can be found in the European Bioinformatics Institute (EBI) nucleotide database under Accession Number ERP012937.
KRA conceived of and designed the project, provided funding, conducted fieldwork, analyzed the data and wrote the manuscript. RMM, NR, and MRS conducted fieldwork and wrote the manuscript. FBC conducted fieldwork. GH, GG, JG, EL, LW, and AL conducted laboratory analyses of samples. EM, MGDB, RMS, BW, KN, RK, and SRL provided funding, logistical support and manuscript revisions.
- Altmann SA (1998) Foraging for survival: yearling baboons in Africa. University of Chicago Press, ChicagoGoogle Scholar
- Arroyo-Rodriguez V, Dias PAD (2009) Effects of habitat fragmentation and disturbance on howler monkeys: a review. Am J Primatol 71:1–16Google Scholar
- Campbell C, Fuentes A, MacKinnon KC, Bearder SK, Stumpf RM (2011) Primates in perspective, second edn. Oxford University Press, New YorkGoogle Scholar
- Cuaron AD et al (2008) Alouatta palliata. The IUCN red list of threatened species, version 2014.3 ednGoogle Scholar
- Di Fiore A, Link A, Campbell C (2011) The Atelines: behavioral and socioecological diversity in a New World monkey radiation. In: Campbell C, Fuentes A, MacKinnon KC, Panger M, Bearder SK (eds) Primates in perspective, 2nd edn. Oxford University Press, Oxford, pp 390–416Google Scholar
- Dias PAD, Rangel-Negrin A (2015) Diets of howler monkeys. In: Kowalewski MM, Garber PA, Cortes-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology, and conservation. Springer, New York, pp 21–56Google Scholar
- Foster JA, McVey Neufeld KA (2013) Gut-brain axis: how the microbiome influences anxiety and depression. Cell 36:305–312Google Scholar
- Garber PA, Righini N, Kowalewski MM (2015) Evidence of alternative dietary syndromes and nutritional goals in the Genus Alouatta. In: Kowalewski MM, Garber PA, Cortes-Ortiz L, Urbani B, Youlatos D (eds) Howler monkeys: behavior, ecology and conservation. Springer, Berlin, pp 85–109Google Scholar
- Marsh LK, Cuaron AD, Cortes-Ortiz L, Shedden A, Rodriguez Luna E, de Grammont PC (2008) Alouatta pigra. The IUCN Red List of Threatened Species., Version 2014.3 ednGoogle Scholar
- Martinez-Mota R (2015) The effects of habitat disturbance, host traits, and host physiology on patterns of gastrointestinal parasite infection in black howler monkeys (Alouatta pigra). PhD dissertation, Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, IL, USAGoogle Scholar
- Norconk MA, Wright BW, Conklin-Brittain NL, Vinyard CJ (2009) Mechanical and nutritional properties of food as factors in platyrrhine dietary adaptations. In: Garber PA, Bicca-Marques JC, Estrada AE, Heymann EW, Strier KB (eds) South American primates, developments in primatology: progress and prospects. Springer, New York, pp 279–319CrossRefGoogle Scholar
- Pozo-Montuy G, Serio-Silva JC (2006) Comportamiento alimentario de monos aulladores negros (Alouatta pigra Lawrence, Cebidae) en habitat fragmentado en Balancan, Tabasco, Mexico. Acta Zool Mex 22:53–66Google Scholar
- Raguet-Schofield ML (2010) The ontogeny of feeding behavior of Nicaraguan mantled howler monkeys (Alouatta palliata). PhD dissertation, Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, IL, USAGoogle Scholar
- Rey-Benayas JM et al. (2007) Plant diversity in highly fragmented forest landscapes in Mexico and Chile: Implications for conservation. In: Newton AC (ed) Biodiversity Loss and Conservation in Fragmented Forest Landscapes: the Forests of Montane Mexico and Temperate South America. CAB International, Oxfordshire, pp 43–68Google Scholar
- Righini N (2014) Primate nutritional ecology: the role of food selection, energy intake, and nutrient balancing in Mexican black howler monkey (Alouatta pigra) foraging strategies. PhD dissertation, Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, IL, USAGoogle Scholar
- Rylands AB, Groves CP, Mittermeier RA, Cortes-Ortiz L, Hins JJH (2006) Taxonomy and distributions of Mesoamerican primates. In: Estrada AE, Garber PA, Pavelka MS, Luecke L (eds) New perspectives in the study of Mesoamerican primates: distribution, ecology, behavior, and conservation. Springer, New York, pp 29–79CrossRefGoogle Scholar
- Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon HA (2009) The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1:6ra14Google Scholar
- Urbani B (2009) Spatial mapping in wild white-faced capuchin monkeys (Cebus capucinus). PhD dissertation, Department of Anthropology, University of Illinois at Urbana-Champaign, Urbana, IL, USAGoogle Scholar
- Van Schaik CP, Brockman DK (eds) (2005) Seasonality in primate ecology, reproduction, and life history: an overview. Cambridge University Press, New YorkGoogle Scholar
- Villalobos F, Valerio AA, Retana AP (2004) A phylogeny of howler monkeys (Cebidae: Alouatta) based on mitochondrial, chromosomal and morphological data. Rev Biol Trop 52:671–677Google Scholar