Thirty years of conservation breeding: Assessing the genetic diversity of captive Livingstone's fruit bats.

Fruit bats (genus Pteropus) are typically island-endemic species important in seed dispersal and reforestation that are vulnerable to increased extinction risk. An effective method of reducing extinction risk in vulnerable species that cannot be conserved in their native habitat is establishing an ex-situ captive breeding programme. Due to anthropogenic threats and low population numbers, in the early 1990s, a captive breeding programme was established at Jersey Zoo, British Isles, for Critically Endangered Livingstone's fruit bats (Pteropus livingstonii). Here we use six polymorphic microsatellite loci to assess genetic diversity in the captive breeding population of Livingstone's fruit bats (P. livingstonii), 30 years after the programme's establishment, investigating change over generations and comparing our findings with published data from the wild population. We found no significant difference between the genetic diversity in the captive and wild populations of Livingstone's fruit bats (P. livingstonii), in both expected heterozygosity and allelic richness. The captive population has retained a comparable level of genetic diversity to that documented in the wild, and there has been no significant decline in genetic diversity over the last 30 years. We advise that a full pedigree of the paternal lineage is created to improve the management of the captive breeding programme and further reduce the possibility of inbreeding. However, it appears that the captive breeding programme is currently effective at maintaining genetic diversity at levels comparable to those seen in the wild population, which suggests reintroductions could be viable if genetic diversity remains stable in captivity.

Predictors of dominance rank and agonistic interactions in captive Livingstone's fruit bats.

Male dominance hierarchies have been studied in many animals but rarely in bats (Chiroptera). The dominance rank of social animals may dictate access to resources and mates; therefore, it has important implications for an individual's fitness and is crucial for successful captive management. Between January and December 2018, at both Bristol Zoo Gardens (Bristol, UK) and Jersey Zoo (Jersey, British Isles), we observed 19 male Livingstone's fruit bats Pteropus livingstonii using focal follows for 345 h overall, noting the outcome of all agonistic interactions. We recorded instigators of interactions, along with winners and losers, and analyzed these data using the R-package "EloRating" to create Elo-rating temporal plots of dominance ranks. We used generalized linear mixed models and multiple linear regression to analyze interaction data and test hypotheses regarding predictors of dominance rank, frequency of agonistic interaction, and choice of interaction partner. Age was positively correlated with dominance rank up to around year 9, when an asymptote was attained. Highly ranked bats instigated the most agonistic interactions, and largely directed these interactions at bats with much lower rankings than themselves. Hierarchies were extremely stable throughout the data collection period at both sites. We conclude that Livingstone's fruit bats have a stable linear dominance hierarchy, with high-ranking, typically older males instigating the most interactions with lowest ranking males to secure dominance rank. This study adds to the limited discourse on Pteropus social behaviors, indicating that some bat species may have social systems similar in complexity to some nonhuman primates.

Social roles influence cortisol levels in captive Livingstone's fruit bats (Pteropus livingstonii).

A critical component of conserving and housing species ex situ is an explicit scientific understanding of the physiological underpinnings of their welfare. Cortisol has been repeatedly linked to stress, and therefore used as an indicator of welfare for many species. In order to measure cortisol in the Livingstone's fruit bat (Pteropus livingstonii; a critically endangered keystone species) without disturbing the captive population, we have developed and validated a non-invasive, novel hormone extraction procedure and faecal glucocorticoid assay. A total of 92 faecal samples, 73 from the P. livingstonii breeding colony at Jersey Zoo, Channel Islands and 19 samples from P. livingstonii housed at Bristol Zoological Gardens, UK, have been collected and analyzed. Mixed-effect modelling of the influence of physiological state variables on cortisol concentration revealed that lactating females had higher cortisol levels than non-lactating females, indicating that our assay is measuring biologically relevant hormone concentrations. Males and older bats also had higher cortisol than non-lactating females and younger individuals. Further analysis applied social network methodology to compare the cortisol levels of bats with different social roles. We found that individuals that linked social groups possessed higher than average cortisol levels and conversely, individuals with high-quality, positive relationships had lower cortisol levels. These results demonstrate, for the first time in a bat species, social mediation of stress hormones. Lastly, the frequency of vocalisation was found to positively correlate with cortisol concentration in males, suggesting that this behaviour may be used by animal management as a visual indicator of a bat's hormonal status. Hence, this research has provided unique insights and empirical scientific knowledge regarding the relationship between the physiology and social behaviour of P. livingstonii, therefore allowing for recommendations to be made to optimise bat welfare at the individual level.