Ex-situ and in-situ conservation in practice: effects of species-management strategies on the behavior and microbiota of amphibians

Abstract

In the midst of the current biodiversity crisis, amphibians are the most endangered vertebrate class, with over a third of species globally threatened with extinction. Given the urgency of the situation and the impossibility to rapidly impede all threats putting them at risk, conservation instances recommend, among possible actions, to move amphibians from threatened locations to safer sites in the wild (in-situ translocations) or into captivity to build “survival assurance populations” that could prevent the extinction of threatened species and enable their latter reintroduction in the wild (ex-situ collections). While such human-driven interventions have undoubtedly contributed to the survival of several amphibian taxa, their success is still rather limited, and they often fail to ensure the persistence of sustainable populations. Management protocols are now adapted to overcome long-known limitations associated with translocations and captive breeding (e.g., increased risks of disease spread, genetic bottlenecks, etc.) but many other, unexplored, aspects of the biology of amphibians may be affected by these conservation strategies, and could thus explain their mixed results. For example, several authors recently recommended to incorporate behavior and microbiota to amphibian conservation research since their consideration gave very promising results in other taxa. Indeed, the bacterial communities that reside on the skin of amphibians play a crucial role in their resistance to deadly pathogens and are strongly influenced by environmental factors. Therefore, the displacement of amphibians and their ex-situ management under husbandry protocols (which typically involve artificial cycles of temperature and habitat-shifts to induce breeding) could restructure their skin microbiota and deplete it from protective symbionts, thus increasing their vulnerability to disease. Moreover, amphibians could behaviorally adapt to the inherent homogeneity and predictability of captive environments; consequently, behavioral variation among- (personality) and within- (plasticity) individuals may decrease ex-situ. These dimensions of behavior have major ecological implications, and the potential behavioral uniformization of captive amphibians and reduction of their behavioral plasticity could thus jeopardize reintroduction efforts. In this context, my objectives were to determine whether common amphibian conservation practices such as in-situ translocation and ex-situ husbandry affected their skin microbiota, and to investigate whether long-term captivity had consequences on their personality and behavioral plasticity. I hypothesized that any displacements, whether into captivity or between wild sites, would disrupt the skin bacterial communities of amphibians. Moreover, I predicted that their behavioral variability would decrease ex-situ. To test these hypotheses, I established an ex-situ collection of newts managed under typical protocols for survival assurance populations and monitored their activity, exploration and boldness for 10 months; I also repeatedly sampled their skin microbiota to characterize the effect of husbandry protocols on its structure using high-throughput sequencing. Moreover, I translocated salamander larvae between similar wild sites, using mesocosms to keep track of each individual; I sampled their skin microbiota before and 15 days after moving them to determine how in-situ translocations may affect their skin bacterial communities. The results of my research suggest that ex-situ conservation is associated with a loss of diversity in both individual behavior and in amphibian skin microbiota, and that artificial habitat-shifts implemented as part of husbandry protocols strongly restructure their skin microbial communities. Indeed, among- and within-individual variation in behavior decreased throughout time in captivity, suggesting that the newts became more similar in their personalities and more predictable in their behavioral responses. Moreover, the richness and diversity of their skin bacterial communities decreased rapidly and lastingly after their displacement from the wild into captivity. While habitat-shift protocols caused strong species-turnovers in the microbiota of the newts, they did not bring it back to its initial, wild structure. Such diversity loss ex-situ could have detrimental implications for reintroduced individuals as they may not behaviorally and microbially readapt fast enough to survive in the wild. Conversely, I found that in-situ translocations have little effect on the amphibian microbiota, suggesting a strong resilience of skin bacterial communities to environmental change. Interestingly, the development of the experimental larvae strongly affected the composition and diversity of their skin microbiota, indicating that ontogeny can be a much stronger driver of its structure than the environment – at least in young life stages. Therefore, in-situ translocations may be a softer conservation approach for amphibians and their microbiota, but more research is needed to determine whether this is also the case with animals in other developmental stages. Taken together, my results suggest that species-management strategies for conservation have differential effects on many aspects of the biology of amphibians, and that their implications on the fitness of animals and the long-term success of conservation efforts should be investigated further. In conclusion, this work demonstrates the pertinence of integrating behavior and microbiota to amphibian conservation, and more generally, of adopting a comprehensive approach when evaluating species-management strategies. I hope my thesis underlines the necessity to develop protocols for maintaining diversity ex-situ and opens new avenues for applied research in this field. Ultimately, expending our understanding of the impacts of conservation methods on amphibians’ biology will likely provide key information to improve future management strategies and thus ensure the persistence of viable amphibian populations.