The amphibian‐killing fungus in a biodiversity hotspot: identifying and validating high‐risk areas and refugia

Abstract

Amphibian chytridiomycosis, due to infection with the fungus Batrachochytrium dendrobatidis (Bd), has been associated with the alarming decline and extinction crisis of amphibians worldwide. It is essential for conservation management to identify regions with high or low suitability for Bd. We use a species distribution model to estimate the environmental suitability of Bd in the Chilean Winter Rainfall–Valdivian Forest biodiversity hotspot. Fourteen environmental variables were used as predictors in the statistical modeling (Maxent, generalized linear models, random forest) which also included 56 independent Bd+ localities. High‐risk areas (i.e., suitability above a defined threshold) were validated through prospective field surveys conducted in 2017. As results from Maxent, which only uses presence data, were the only results retained, refugia (i.e., suitability below a defined threshold) were validated with the Bd absences (N = 12) used in the GLM and RF modeling. Our results showed that (1) suitability for Bd increased with human footprint and with shorter distances to urban centers and water bodies and decreased with elevation; (2) climate was not a major factor shaping the current distribution of Bd; and (3) the model predicted high‐risk and refugia areas fairly well. Surveys of 24 new localities in high‐risk areas confirmed that 23 were Bd+; hence, these areas warrant consideration for long‐term Bd surveillance, population monitoring, and disease mitigation. In addition, five localities with apparent Bd absence were found in the predicted high‐risk areas. Our models showed that refugia can exist near high‐risk areas and Bd+ sites. Four localities with apparent Bd absence were located within the refugia predicted by the model. Preventing Bd transmission to such refugia is of paramount importance for persistence of Bd‐susceptible amphibian populations. The identification and validation through prospective field surveys of high‐risk areas and refugia are imperative to develop strategies to prevent further arrival and establishment of Bd and also, by identifying amphibian species or populations of conservation concern in such areas, will help to guide specific actions to reduce the biodiversity loss caused by chytridiomycosis.

Species distribution models predict the geographic expansion of an enzootic amphibian pathogen

“…The increased suitability for Bd in lowlands of Costa Rica may explain the enigmatic declines experienced by several amphibian species in regions that were thought to be unsuitable for Bd (below 1,000 m elevation; Bolaños, 2009; Chaves et al., 2014; Zumbado‐Ulate, Bolaños, Willink, & Soley‐Guardia, 2011). The suitable elevational range predicted for enzootic Bd in Costa Rica matched with the elevational range reported for enzootic Bd in Panama, Mexico, Colombia, and Chile (Bacigalupe et al., 2019; Bolom‐Huet, Pineda, Díaz‐Fleischer, Muñoz‐Alonso, & Galindo‐González, 2019; Flechas et al., 2017; Kilburn et al., 2010; Woodhams et al., 2008). The climatic variable contributions in our model (Table S1) also suggested that habitat suitability for enzootic Bd in Costa Rica is associated with seasonal climatic interactions across the year that favor or constrain Bd occurrence.…”

“…The bars under each map show suitability by elevation with black indicating the predicted percentage of climatic suitability for Bd. Altitudinal bars display belts of 500 m except the seventh bar that shows all elevations above 3,000 m (1 = 0-500 m; 2 = 500-1,000 m; 3 = 1,000-1,500 m, 4 = 1,500-2,000 m; 5 = 2,000-2,500 m; 6 = 2,500-3,000 m; 7 = 3,000-3,820 m) the elevational range reported for enzootic Bd in Panama, Mexico, Colombia, and Chile (Bacigalupe et al, 2019;Bolom-Huet, Pineda, Díaz-Fleischer, Muñoz-Alonso, & Galindo-González, 2019;Flechas et al, 2017;Kilburn et al, 2010;Woodhams et al, 2008). The climatic variable contributions in our model (Table S1) confirmed that enzootic Bd is currently infecting species that exhibit multiple life-history traits across all elevations.…”

“…In our study, the use of the combined dataset increased the power to detect hotspots and cold spots (e.g., Puschendorf et al., 2011). Our findings suggest that other suitability maps for Bd in the Americas (at the continental and regional level) that were generated datasets derived from only one method of detection (e.g., Bacigalupe et al., 2019; Bolom‐Huet et al., 2019; James et al., 2015; Ron, 2005) could be reanalyzed in follow‐up studies with combined datasets and interpolation methods to revalidate high‐risk areas, Bd hotspots and cold spots.…”

A flagship for Austral temperate forest conservation: an action plan for Darwin's frogs brings key stakeholders together

“…Once signed by the environment authorities of both countries, the strategy will facilitate interdisciplinary and international working amongst public agencies. Another area in which both countries can take action involves animal health departments, with the enforcement of amphibian import regulations and the implementation of biosecurity protocols aimed at limiting the spread of B. dendrobatidis (and other invasive species) both at national and local levels (Valenzuela-Sánchez et al, 2018; Bacigalupe et al, 2019). Official recognition of the strategy is also relevant for establishing nation-wide conservation education programmes.…”

Urban growth threatens the lowland Amazonian Manaus harlequin frog which represents an evolutionarily significant unit within the genus Atelopus (Amphibia: Anura: Bufonidae)

“…However, most of the more than 96 species of Atelopus are now extinct or in decline, mainly because of infection by the pathogenic fungus Batrachochytrium dendrobatidis ( Bd ) for those inhabiting mid to high elevations and due to habitat loss for lowland species (La Marca et al., 2005). Despite Bd being generally less severe in warmer lowland areas (Bacigalupe et al., 2019), these portions of the landscape in Amazonia are often deforested for human use and disturbed areas seem to be suitable for Bd invasion in central Amazonia (Becker, Rodriguez, Lambertini, Toledo, & Haddad, 2015), and other tropical regions (Bolom‐Huet, Pineda, Días‐Fleischer, Muñoz‐Alonso, & Galindo‐González, 2019).…”