Original Article

Subject Category: Microbe-microbe and microbe-host interactions

The ISME Journal (2013) 7, 1344–1353; doi:10.1038/ismej.2013.16; published online 14 March 2013

Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes

Katherine R Amato1,2, Carl J Yeoman3,4, Angela Kent5, Nicoletta Righini2, Franck Carbonero6, Alejandro Estrada7, H Rex Gaskins4,6, Rebecca M Stumpf2,4, Suleyman Yildirim4, Manolito Torralba8, Marcus Gillis8, Brenda A Wilson4,9, Karen E Nelson8, Bryan A White4,6 and Steven R Leigh2,4,10

  1. 1Program in Ecology, Evolution and Conservation Biology, University of Illinois, Urbana, IL, USA
  2. 2Department of Anthropology, University of Illinois, Urbana, IL, USA
  3. 3Department of Animal and Range Sciences, Montana State University, Bozeman, MT, USA
  4. 4Institute for Genomic Biology, University of Illinois, Urbana, IL, USA
  5. 5Department of Natural Resources and Environmental Sciences, University of Illinois, Urbana, IL, USA
  6. 6Department of Animal Sciences, University of Illinois, Urbana, IL, USA
  7. 7Estacion de Biologia Tropical Los Tuxtlas, Instituto de Biologia, Universidad Nacional Autonoma de Mexico, San Andrés Tuxtla, Mexico
  8. 8The J. Craig Venter Institute, Rockville, MD, USA
  9. 9Department of Microbiology, University of Illinois, Urbana, IL, USA

Correspondence: SR Leigh, Department of Anthropology, University of Illinois at Urbana-Champaign, 1206 West Gregory Drive, Urbana, IL 61801, USA. E-mail: sleigh@illinois.edu

10Present address: Department of Anthropology, University of Colorado, Boulder, CO, USA.

Received 3 July 2012; Revised 16 November 2012; Accepted 6 January 2013
Advance online publication 14 March 2013



The gastrointestinal (GI) microbiome contributes significantly to host nutrition and health. However, relationships involving GI microbes, their hosts and host macrohabitats remain to be established. Here, we define clear patterns of variation in the GI microbiomes of six groups of Mexican black howler monkeys (Alouatta pigra) occupying a gradation of habitats including a continuous evergreen rainforest, an evergreen rainforest fragment, a continuous semi-deciduous forest and captivity. High throughput microbial 16S ribosomal RNA gene sequencing indicated that diversity, richness and composition of howler GI microbiomes varied with host habitat in relation to diet. Howlers occupying suboptimal habitats consumed less diverse diets and correspondingly had less diverse gut microbiomes. Quantitative real-time PCR also revealed a reduction in the number of genes related to butyrate production and hydrogen metabolism in the microbiomes of howlers occupying suboptimal habitats, which may impact host health.


Alouatta; gut microbiome; habitat; primate