Habitat fragmentation is associated to gut microbiota diversity of an endangered primate: implications for conservation.

Claudia Barelli,Carlotta De Filippo,Claudio Donati,Kieran Michael Tuohy,Davide Albanese,Francesco Rovero,Duccio Cavalieri,Chiara Dallago,Heidi Christine Hauffe,Massimo Pindo

doi:10.1038/srep14862

Abstract

The expansion of agriculture is shrinking pristine forest areas worldwide, jeopardizing the persistence of their wild inhabitants. The Udzungwa red colobus monkey (Procolobus gordonorum) is among the most threatened primate species in Africa. Primarily arboreal and highly sensitive to hunting and habitat destruction, they provide a critical model to understanding whether anthropogenic disturbance impacts gut microbiota diversity. We sampled seven social groups inhabiting two forests (disturbed vs. undisturbed) in the Udzungwa Mountains of Tanzania. While Ruminococcaceae and Lachnospiraceae dominated in all individuals, reflecting their role in extracting energy from folivorous diets, analysis of genus composition showed a marked diversification across habitats, with gut microbiota α-diversity significantly higher in the undisturbed forest. Functional analysis suggests that such variation may be associated with food plant diversity in natural versus human-modified habitats, requiring metabolic pathways to digest xenobiotics. Thus, the effects of changes in gut microbiota should not be ignored to conserve endangered populations.

Highlights

The influence of gut microbiota homeostasis on African primate conservation is of particular interest given their threatened status
We described the gut microbiota of geographically isolated populations of red colobus monkey (n = 31) from a large pristine forest block and a remnant (Fig. 1; Supplementary Table S1 and Supplementary Fig. S2) in the Udzungwa Mountains of Tanzania, which differ in levels of human disturbance
We show that microbiota richness and diversity are reduced in Ma, likely as result of dietary changes enforced by human disturbance and habitat degradation

Summary

Introduction

The influence of gut microbiota homeostasis on African primate conservation is of particular interest given their threatened status. We analyse the phylogenetic and functional diversity of the gut microbiota in a threatened endemic primate, the Udzungwa red colobus (Procolobus gordonorum; IUCN 2014, Version 2014.3, available at www.iucnredlist.org, accessed 5 March 2015, Supplementary Fig. S1), recognized as an important flagship species[23]. This non-human primate has populations in both large intact forest blocks and forest fragments of the Udzungwa Mountains, in the Eastern Arc Mountains of Tanzania and Kenya, a global biodiversity hotspot[24,25,26]. Using barcoded 454 amplicon pyrosequencing of the 16S bacterial ribosomal RNA gene of faecal samples, 16 collected in Magombera (Ma) and 15 collected in Mwanihana (Mw), we hypothesized that gut microbiota composition and function would be altered in populations restricted to fragmented and degraded forests, and that these modifications would be associated with changes in the metabolic pathways at the level of the microbiome

Methods

Results

Conclusion