Imminent invasion of the chytrid fungus threatens the last naive amphibian biodiversity hotspots

Abstract

While the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd) is driving catastrophic biodiversity loss worldwide, some amphibian communities persist seemingly unaffected despite occurring in climates conducive to pathogen establishment. These amphibian communities may remain epidemiologically naive. As mitigation of Bd is rarely successful after establishment, identifying remaining Bd-free refuges is imperative. Presently, the only known large-scale Bd-free refuge is the island of New Guinea (NG), safeguarding Australasias amphibian phylogenetic diversity otherwise devastated by Bd. Following extensive multi-year disease surveillance, we here uncover a second large-scale Bd-free refuge in the Sierra Nevada de Santa Marta (SNSM), a Neotropical biodiversity hotspot in northern Colombia. We detected no evidence of Bd in SNSM-wide screening, while we uncovered the presence of hypervirulent Bd-GPL in adjacent areas of the tropical Andes. Population genomic analyses in an SNSM-endemic anuran found no evidence for demographic bottlenecks indicative of cryptic epizootic decline. Niche modelling highlights the high risk for Bd establishment and Bd-induced declines in both the SNSM and NG, and the important role of lowland environmental barriers in restricting Bd invasion. Infection trials using three SNSM-endemic amphibians reveal varying disease susceptibility. Together, these data identify the SNSM as an epidemiologically naive refuge likely facing imminent Bd invasion, which could result in the loss of at least 25 endemic amphibian species. We highlight the urgent need for proactive conservation action and strict implementation of biosecurity to safeguard the unique and vast amphibian diversity of the worlds last major Bd-free refuges. Significance StatementAmphibian chytridiomycosis caused by Batrachochytrium dendrobatidis (Bd) has driven unprecedented global biodiversity loss. The Neotropics and Australasia comprise epicenters of declines. Identifying remaining Bd-free refuges is crucial to curb further amphibian extinctions, but so far contemporary absence of Bd has only been demonstrated for New Guinea. Here we identify the last known major Bd-free biodiversity hotspot in the Neotropics: the Sierra Nevada de Santa Marta (SNSM) in Colombia. Our results show that amphibian communities in this hotspot are immunologically naive despite occurrence of hypervirulent Bd lineages nearby and climatic conditions within the SNSM conducive to Bd-induced declines. This creates an imminent risk for Bd-driven declines and highlights the urgent need for preventive actions to avert another wave of biodiversity loss.