Abstract

Captive breeding has been used as an effective approach to protecting endangered animals but its effect on the gut microbiome and the conservation status of these species is largely unknown. The giant panda is a flagship species for the conservation of wildlife. With integrated efforts including captive breeding, this species has been recently upgraded from “endangered” to “vulnerable” (IUCN 2016). Since a large proportion (21.8%) of their global population is still captive, it is critical to understand how captivity changes the gut microbiome of these pandas and how such alterations to the microbiome might affect their future fitness and potential impact on the ecosystem after release into the wild. Here, we use 16S rRNA (ribosomal RNA) marker gene sequencing and shotgun metagenomics sequencing to demonstrate that the fecal microbiomes differ substantially between wild and captive giant pandas. Fecal microbiome diversity was significantly lower in captive pandas, as was the diversity of functional genes. Additionally, captive pandas have reduced functional potential for cellulose degradation but enriched metabolic pathways for starch metabolism, indicating that they may not adapt to a wild diet after being released into the wild since a major component of their diet in the wild will be bamboo. Most significantly, we observed a significantly higher level of amylase activity but a lower level of cellulase activity in captive giant panda feces than those of wild giant pandas, shown by an in vitro experimental assay. Furthermore, antibiotic resistance genes and virulence factors, as well as heavy metal tolerance genes were enriched in the microbiomes of captive pandas, which raises a great concern of spreading these genes to other wild animals and ecosystems when they are released into a wild environment. Our results clearly show that captivity has altered the giant panda microbiome, which could have unintended negative consequences on their adaptability and the ecosystem during the reintroduction of giant pandas into the wild.

Highlights

  • The giant panda (Ailuropoda melanoleuca) has been listed as an endangered animal species for decades (The IUCN Red List of Threatened Species, 2016) but concerted, integrated efforts to protect the species has led to a 31.7% population increase and a recent upgrade in conservation status from “endangered” to “vulnerable” (The IUCN Red List of Threatened Species, 2016)

  • We characterized the fecal microbiomes from 49 healthy captive pandas raised at the CCRC for the

  • We demonstrate that the diversity, composition, functional potential, enzyme activity, and presence of antibiotic resistance genes (ARGs), mobile genetic elements (MGEs), metal resistance genes (MRGs), and virulence factors in the fecal microbiomes of wild and captive giant pandas differ significantly

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Summary

Introduction

The giant panda (Ailuropoda melanoleuca) has been listed as an endangered animal species for decades (The IUCN Red List of Threatened Species, 2016) but concerted, integrated efforts to protect the species has led to a 31.7% population increase and a recent upgrade in conservation status from “endangered” to “vulnerable” (The IUCN Red List of Threatened Species, 2016). Captive breeding has been one of the main integrated approaches used towards protecting the giant panda and increasing their population size. There are 21.8% of giant pandas living in zoos worldwide The gut microbiome of giant pandas has been implicated in their health and disease status [1]. Gastrointestinal diseases have been reported to be a primary cause of death in giant pandas [2,3]. We hypothesized that captivity alters the gut microbiome of giant pandas

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