The Effects of Captivity on the Mammalian Gut Microbiome

Abstract

SynopsisRecent studies increasingly note the effect of captivity or the built environment on the microbiome of humans and other animals. As symbiotic microbes are essential to many aspects of biology (e.g., digestive and immune functions), it is important to understand how lifestyle differences can impact the microbiome, and, consequently, the health of hosts. Animals living in captivity experience a range of changes that may influence the gut bacteria, such as diet changes, treatments, and reduced contact with other individuals, species and variable environmental substrates that act as sources of bacterial diversity. Thus far, initial results from previous studies point to a pattern of decreased bacterial diversity in captive animals. However, these studies are relatively limited in the scope of species that have been examined. Here we present a dataset that includes paired wild and captive samples from mammalian taxa across six Orders to investigate generalizable patterns of the effects captivity on mammalian gut bacteria. In comparing the wild to the captive condition, our results indicate that alpha diversity of the gut bacteria remains consistent in some mammalian hosts (bovids, giraffes, anteaters, and aardvarks), declines in the captive condition in some hosts (canids, primates, and equids), and increases in the captive condition in one host taxon (rhinoceros). Differences in gut bacterial beta diversity between the captive and wild state were observed for most of the taxa surveyed, except the even-toed ungulates (bovids and giraffes). Additionally, beta diversity variation was also strongly influenced by host taxonomic group, diet type, and gut fermentation physiology. Bacterial taxa that demonstrated larger shifts in relative abundance between the captive and wild states included members of the Firmicutes and Bacteroidetes. Overall, the patterns that we observe will inform a range of disciplines from veterinary practice to captive breeding efforts for biological conservation. Furthermore, bacterial taxa that persist in the captive state provide unique insight into symbiotic relationships with the host.

Introduction: The host‐associated microbiome: Pattern, process and function

“…Somewhat surprisingly, microbiota divergence rates were not greatly accelerated in groups with higher numbers of dietary shifts. This work reinforces the importance of the environment in structuring the microbiota in humans (Rothschild et al., ) and other mammals (McKenzie et al., ), although it is unclear just how, and how fast, major lifestyle transitions drove natural shifts in whale and bat microbiomes. This work also highlights the nuanced insights that can be gained by probing individual lineages, showing that lineages at a detailed taxonomic scale (OTU or genus level) strongly reflect host phylogenetic signal, while broad taxonomic categories are associated with lifestyle or dietary transitions (Groussin et al., ; Nishida & Ochman, ).…”

Evolutionary signal in the gut microbiomes of 74 bird species from Equatorial Guinea

“…While many of these taxa were low abundance, and there is the risk of false positives in any data set, this is a high level of raw richness. Alpha diversity patterns were consistent across the four data sets; the Shannon diversity of many of the birds was lower than the average Shannon diversity of both wild and captive mammals (McKenzie et al, ). Again, this may be due to a high level of low‐abundance taxa.…”

Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats

“…Similarly, administration of probiotic bacteria to brown trout (Salmo trutta) increases the activity of the complement system, also suggesting links between the microbiota and innate immune function in animals (Balcázar et al, 2007). Compared to studies of laboratory animals and humans, interactions between endosymbiotic microbial communities and the host immune system are less well understood for wildlife (Evans, Buchanan, Griffith, Klasing, & Addison, 2017;Pedersen & Babayan, 2011), which are regularly exposed to pathogens and to environmental variation (McKenzie et al, 2017).…”