The effect of captivity on the primate gut microbiome varies with host dietary niche

Abstract

Despite careful attention to animal nutrition and wellbeing, gastrointestinal distress remains relatively common in captive non-human primates (NHPs), particularly dietary specialists such as folivores. These patterns may be a result of marked dietary differences between captive and wild settings and associated impacts on the gut microbiome. However, given that most existing studies target NHP dietary specialists, it is unclear if captive environments have distinct impacts on the gut microbiome of NHPs with different dietary niches. To begin to examine this question, we used 16S ribosomal RNA gene amplicon sequences to compare the gut microbiomes of five NHP genera categorized either as folivores (Alouatta, Colobus) or non-folivores (Cercopithecus, Gorilla, Pan) sampled both in captivity and in the wild. Though captivity affected the gut microbiomes of all NHPs in this study, the effects were largest in folivorous NHPs. Shifts in gut microbial diversity and in the relative abundances of fiber-degrading microbial taxa suggest that these findings are driven by marked dietary shifts for folivorous NHPs in captive settings. We propose that zoos and other captive care institutions consider including more natural browse in folivorous NHP diets and regularly bank fecal samples to further explore the relationship between NHP diet, the gut microbiome, and health outcomes.

Effects of captivity, diet, and relocation on the gut bacterial communities of white‐footed mice

“…However, the diversity was not in terms of total phylotype richness but in terms of common bacterial groups with the wild “original” state of the microbiota. The generalization that captivity induces an imbalanced microbiota linked to negative effects on the host should be considered with caution, because it can depend on the taxonomy and ecology of the host, as demonstrated by Greene et al (2019) and Frankel et al (2019).…”

“…The majority of the studies show similar trends: a decrease in bacterial phylotype richness (or α‐diversity) among captive individuals compared to their wild conspecifics, as well as differences in community composition (or β‐diversity) between the groups. However, some host species show an opposite pattern (Frankel, Mallott, Hopper, Ross, & Amato, 2019; Greene et al, 2019; McKenzie et al, 2017), postulating that the gut microbiota of group taxa respond differently to captivity, mainly through their feeding strategy and gut physiology. Differences observed in gut microbial communities have largely been attributed to altered diets in captivity that can also lead to the extinction of microbial niches and functions in the host's gut over multiple generations in captivity (Sonnenburg et al, 2016).…”

The Gut Microbiome of Exudivorous Marmosets in the Wild and Captivity

“…Gut microbiome studies of captive and wild mammals show that non-human primates (NHPs) experience relatively large losses of native gut microbiome diversity in captivity compared to the wild [6,11]. Additionally, folivorous NHPs are especially prone to GI problems in captivity [15], and among humans and non-human primates (NHPs) dysbiosis in GMC has been tied to gastrointestinal (GI) diseases [7,15,16].…”

Primate phageomes are structured by superhost phylogeny and environment

“…This pattern of transmission may be facilitated by the tendency for primates to live in stable social groups (11), creating opportunities for bacterial transmission to conspecifics (12,13). When removed from their natural social and ecological environments in captivity, primates quickly develop humanized bacterial microbiomes (14,15); this apparent plasticity makes the long-term associations of primates with particular bacterial lineages all the more striking (8,9).…”