Integrating Gut Bacterial Diversity and Captive Husbandry to Optimize Vulture Conservation

Abstract

Endangered species recovery plans often include captive breeding and reintroduction, but success remains rare. Critical for effective recovery is an assessment of captivity-induced changes in adaptive traits of reintroduction candidates. The gut microbiota is one such trait and is particularly important for scavengers exposed to carcass microbiomes. We investigated husbandry-associated differences in the gut microbiota of two Old World vulture species using 16S RNA gene amplicon sequencing. Increased abundance of Actinobacteria occurred when vultures were fed quail but not rat or chicken. Conversely, diet preparation (sanitization) had no effect, although bacterial diversity differed significantly between vulture species, likely reflective of evolved feeding ecologies. Whilst the relative lack of influence of a sanitized diet is encouraging, changes in bacterial abundance associated with the type of prey occurred, representing a dietary influence on host-microbiome condition warranting consideration in ex situ species recovery plans. Incorporation of microbiome research in endangered species management, therefore, provides an opportunity to refine conservation practice.

Keywords: ex situ conservation; feeding ecology; gut microbiome; husbandry; old world vultures; prey diet; species recovery.

FIGURE 1

Variation in gut bacterial diversity between Egyptian and Griffon vultures. Alpha diversity based on rarefied data, measured by observed species and Shannon diversity Index, plotted for 52 fecal samples of two Old World vulture species (EV = Egyptian vulture, six individuals, n = 22 samples; GY = Griffon vulture, seven individuals, n = 30 samples). Statistical testing showed significant difference in observed species (Wilcoxon, P < 0.05) and Shannon diversity (Wilcoxon, P < 0.05) between both vulture species. Vultures were fed either a sanitized diet (SD) consisting of skinned, de-gutted and washed rats, chicken and quail, or un-sanitized diet (UD) consisting of intact whole rats, chicken and quail. No significant difference were observed between diets.

FIGURE 2

Gut bacterial composition of Egyptian and Griffon vultures. Taxonomic bacterial profile of 52 fecal samples from Egyptian (EV; six individuals, n = 22 samples) and Griffon vultures (GY; seven individuals, n = 30 samples) at phylum (A; left) and family (B; right) level. Of 75 families classified, only 14 with an abundance >1% of total reads are displayed.

FIGURE 3

Egyptian and Griffon vultures exhibit different bacterial communities. Beta diversity; principal coordinate analysis visualizing the clustering of bacterial communities of 52 fecal samples from Egyptian (six individuals, n = 22 samples; red) and Griffon vultures (seven individuals, n = 30 samples; blue) based on unweighted UniFrac dissimilarity matrix. Vulture species exhibited minor overlap (ANOSIM; R = 0.545, P = 0.001).

FIGURE 4

Relative abundance of Actinobacteria in the fecal bacterial community of vultures varied according to prey type. Boxplots showing the relative abundance of Actinobacteria in fecal samples from Griffon vultures (seven individuals, n = 30 samples) fed either rat (n = 12 samples) or quail (n = 18 samples), and Egyptian vultures (six individuals, n = 22 samples) fed either quail (n = 2 samples), rat (n = 5 samples), or chicken (n = 12 samples), or following a ‘fasted’ day (n = 3 samples). For quail and rat prey types, fecal Actinobacteria abundance data from both vulture species were combined, but differences between prey type were only statistically significant for Griffon vultures (P = 0.02). No statistical differences were detected between the four prey types fed to Egyptian vultures.