The effect of captivity on the skin microbial symbionts in three Atelopus species from the lowlands of Colombia and Ecuador

PeerJ. 2017 Jul 31:5:e3594. doi: 10.7717/peerj.3594. eCollection 2017.

Abstract

Many amphibian species are at risk of extinction in their natural habitats due to the presence of the fungal pathogen Batrachochytrium dendrobatidis (Bd). For the most highly endangered species, captive assurance colonies have been established as an emergency measure to avoid extinction. Experimental research has suggested that symbiotic microorganisms in the skin of amphibians play a key role against Bd. While previous studies have addressed the effects of captivity on the cutaneous bacterial community, it remains poorly studied whether and how captive conditions affect the proportion of beneficial bacteria or their anti-Bd performance on amphibian hosts. In this study we sampled three amphibian species of the highly threatened genus, Atelopus, that remain in the wild but are also part of ex situ breeding programs in Colombia and Ecuador. Our goals were to (1) estimate the diversity of culturable bacterial assemblages in these three species of Atelopus, (2) describe the effect of captivity on the composition of skin microbiota, and (3) examine how captivity affects the bacterial ability to inhibit Bd growth. Using challenge assays we tested each bacterial isolate against Bd, and through sequencing of the 16S rRNA gene, we identified species from thirteen genera of bacteria that inhibited Bd growth. Surprisingly, we did not detect a reduction in skin bacteria diversity in captive frogs. Moreover, we found that frogs in captivity still harbor bacteria with anti-Bd activity. Although the scope of our study is limited to a few species and to the culturable portion of the bacterial community, our results indicate that captive programs do not necessarily change bacterial communities of the toad skins in a way that impedes the control of Bd in case of an eventual reintroduction.

Keywords: Atelopus; Bacterial communities; Batrachochytrium dendrobatidis; Beneficial bacteria; Culturable bacteria; Ex situ conservation; Growth inhibition.

Grants and funding

This work was supported by the Association of Zoos and Aquariums Conservation Endowment Fund (08-836), the Facultad de Ciencias at Universidad de los Andes, and the Dirección General Académica of the Pontificia Universidad Católica del Ecuador. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.