Captivity Shapes the Gut Microbiota of Andean Bears: Insights into Health Surveillance

Abstract

The Andean bear is an endemic species of the tropical Andes who has an almost exclusively plant-based diet. Since herbivorous mammals do not carry enzymes for fiber degradation, the establishment of symbiosis with cellulolytic microorganisms in their gastrointestinal (GI) tract is necessary to help them fulfill their nutritional needs. Furthermore, as described for other mammals, a stable, diverse, and balanced gut microbial composition is an indicator of a healthy status of the host; under disturbances this balance can be lost, leading to potential diseases of the host. The goal of this study was to describe the gut microbiota of wild and captive Andean bears and determine how habitat status influences the composition and diversity of the gut symbiotic community. Fecal samples from wild (n = 28) and captive (n = 8) Andean bears were collected in “Reserva Pantano de Martos” and “Fundación Bioandina”, Colombia. Composition and diversity analyses were performed using amplicons from the V4 region of the 16S rDNA gene sequenced using the Ion PGM platform. PICRUSt algorithm was applied to predict the gene content of the gut microbiome of wild and captive Andean bears. A total of 5,411 and 838 OTUs were identified for wild and captive bears, respectively. Captive bears contained a lower number of bacterial phyla (n = 7) compared to wild individuals (n = 9). Proteobacteria (59.03%) and Firmicutes (14.03%) were the phyla that contributed the most to differences between wild and captive bears (overall dissimilarity = 87.72%). At family level, Enterobacteriaceae drove the main differences between the two groups (13.7%). PICRUSt metagenomics predictions suggested a similar pattern of relative abundance of gene families associated with the metabolism of carbohydrates across samples in wild individuals, despite the taxonomic differences of their gut microbiota. Captivity alters the availability and diversity of food resources, which likely reduces microbiota richness and diversity compared to wild individuals. Further considerations should be taken into account for nutritional schemes improving ex-situ conservation and its potential as a surveillance tool of endangered populations of wild Andean bears.

Conservation Implications of Shifting Gut Microbiomes in Captive-Reared Endangered Voles Intended for Reintroduction into the Wild

“…Bray-Curtis distances showed that wild-captured samples clustered on their own while colony and colony-transitional samples clustered together ( Figure 4 a). This is in line with previous studies that show different microbial diversity and community structure in captive vs wild conspecifics [ 28 , 48 , 68 , 69 ]. PLS-DA analysis also indicated separation of wild-captured samples ( Figure 2 a).…”

Conserving the holobiont

“…The current evidence confirms that captivity alters the community structure, and in many cases, the diversity of animal gut microbiota (e.g. Borbon‐Garcia, Reyes, Vives‐Florez, & Caballero, ; Cheng et al, ; Delport, Power, Harcourt, Webster, & Tetu, ; McKenzie et al, ; Wasimuddin et al, ), although there is little evidence to date equating these changes with harm.…”

“…(e.g Borbon-Garcia, Reyes, Vives-Florez, & Caballero, 2017;Cheng et al, 2015;Delport, Power, Harcourt, Webster, & Tetu, 2016;McKenzie et al, 2017;Wasimuddin et al, 2017),. although there is little evidence to date equating these changes with harm.…”

First report of foregut microbial community in proboscis monkeys: are diverse forests a reservoir for diverse microbiomes?

“…Our results may not be representative of the entire proboscis monkey population due to the small sample size (N = 6) with high individual variation within the same environmental condition. Effects of diet on both foregut and hindgut microbial patterns have previously been shown in various free-ranging and captive animals (Dill-McFarland et al, 2016;Borbon-Garcia et al, 2017;Hale et al, 2018), although these results are rarely shown together with information on the living environment of the animals. The geographic region Sundaland, which includes our study sites, is a large reservoir of endemic tropical plant and animal species such as the proboscis monkey (Myers et al, 2000).…”