Evaluating the Relationship between the Gut Microbiome and Health Issues in Captive African and Asian Elephants

Abstract

Animals experience novel stressors inherent to captive environments. Some species are able to adapt to new environments with little consequence, while others display behavioral changes and health concerns. The gut microbiome of animals is also impacted by the captive environment. A healthy gut microbiome is important for normal immune function, metabolism, hormone regulation, and even behavior. Captive animals often have less diverse gut microbiomes than their wild counterparts. The shifting of the microbial community in captivity may be connected to prevailing health issues. Zoo managed African elephants (Loxodonta africana) and Asian elephants (Elephas maximus) experience low reproductive rates, obesity, gastrointestinal (GI) issues, and variable stress responses to external and physiological variables. This project aims to examine the relationship between health and reproductive issues in captive elephants and their gut microbiome. To assess the elephant gut microbiome, I leveraged fecal samples and health records from a large Elephant Welfare Project conducted across North American zoos in 2012. Fecal microbiomes of 69 African and 48 Asian elephants from 50 zoos were characterized using Illumina sequencing of the 16S rRNA bacterial gene. Alpha and beta diversity of gut bacterial microbiomes were assessed with respect to species, zoo, fertility status, obesity, and fecal glucocorticoid metabolite (FGM) concentrations during the study period. I further assessed the gut microbiome of African and Asian elephants to identify indicator bacterial species associated with reproductive status, and tested for correlations between bacterial abundance and reproductive and metabolic hormone concentrations. I found the gut microbiome of African and Asian elephants differed in bacterial species richness and phylogenetic diversity (alpha diversity), as well as in microbial composition (beta diversity: with host species explaining 10.2% of variation). Asian elephants had greater bacterial species richness and phylogenetic diversity than African elephants. Bacterial species richness and phylogenetic diversity also varied by zoo facility. Microbial composition was strongly influenced by zoo facility and explained 65.1% of variation. I found most health metrics were not linked to the gut microbiome in African elephants; however older elephants had higher bacterial phylogenetic diversity than younger individuals, and age was connected to differences in gut microbial composition. Similarly, in Asian elephants, most health metrics were not linked to the gut microbiome, except for age and fecal glucocorticoid metabolite (FGM) concentrations; older elephants had lower bacterial phylogenetic diversity, and changes in the gut microbiome composition were related to FGM. I found 16 and 17 indicator bacterial species associated with reproductive status in African and Asian elephants, respectively. In African elephants, three of the indicator bacterial taxa were correlated with metabolic hormones. In Asian elephants, one indicator bacterial taxa was correlated with a metabolic hormone, and one with a reproductive hormone. These bacterial species should be further studied to quantify their relationship with reproductive status, reproductive and metabolic hormones, and for potential microbial therapy applications in captive elephants. African and Asian elephants have distinct gut microbial communities and differ in how age and stress are related to their gut microbiomes. The strong influence of zoo on the gut microbiome highlights the importance of the environment in shaping the gut microbiome. My results provide insight into the relationship between captive African and Asian elephant gut microbiomes and host species, zoo institution, and health issues. These findings contribute to a better understanding of overall health and welfare of captive elephants in North America.