The Gut Microbiota Communities of Wild Arboreal and Ground-Feeding Tropical Primates Are Affected Differently by Habitat Disturbance

Abstract

Human exploitation and destruction of tropical resources are currently threatening innumerable wild animal species, altering natural ecosystems and thus, food resources, with profound effects on gut microbiota. Given their conservation status and the importance to tropical ecosystems, wild nonhuman primates make excellent models to investigate the effect of human disturbance on the diversity of host-associated microbiota. Previous investigations have revealed a loss of fecal bacterial diversity in primates living in degraded compared to intact forests. However, these data are available for a limited number of species, and very limited information is available on the fungal taxa hosted by the gut. Here, we estimated the diversity and composition of gut bacterial and fungal communities in two primates living sympatrically in both human-modified and pristine forests in the Udzungwa Mountains of Tanzania. Noninvasively collected fecal samples of 12 groups of the Udzungwa red colobus (Procolobus gordonorum) (n = 89), a native and endangered primate (arboreal and predominantly leaf-eating), and five groups of the yellow baboon (Papio cynocephalus) (n = 69), a common species of least concern (ground-feeding and omnivorous), were analyzed by the V1-V3 region of the 16S rRNA gene (bacterial) and ITS1-ITS2 (fungal) sequencing. Gut bacterial diversities were associated with habitat in both species, most likely depending on their ecological niches and associated digestive physiology, dietary strategies, and locomotor behavior. In addition, fungal communities also show distinctive traits across hosts and habitat type, highlighting the importance of investigating this relatively unexplored gut component.IMPORTANCE Gut microbiota diversity has become the subject of extensive research in human and nonhuman animals, linking diversity and composition to gut function and host health. Because wild primates are good indicators of tropical ecosystem health, we developed the idea that they are a suitable model to observe the consequences of advancing global change (e.g., habitat degradation) on gut microbiota. So far, most of the studies focus mainly on gut bacteria; however, they are not the only component of the gut: fungi also serve essential functions in gut homeostasis. Here, for the first time, we explore and measure diversity and composition of both bacterial and fungal microbiota components of two tropical primate species living in highly different habitat types (intact versus degraded forests). Results on their microbiota diversity and composition are discussed in light of conservation issues and potential applications.

Keywords: Tanzania; Udzungwa; bacteria; conservation; fungi; gut microbiota; habitat degradation; primates; red colobus; yellow baboon.