Differential patterns of Batrachochytrium dendrobatidis infection in relict amphibian populations following severe disease-associated declines

Abstract

Global amphibian biodiversity has declined dramatically in the past 4 decades, and many amphibian species have declined to near extinction as a result of emergence of the amphibian chytrid fungus, Batrachochytrium dendrobatidis (Bd). However, persistent or recovering populations of several amphibian species have recently been rediscovered, and such populations may illustrate how amphibian species that are highly susceptible to chytridiomycosis may survive in the presence of Bd. We conducted field surveys for Bd infection in 7 species of Costa Rican amphibians (all species that have declined to near extinction but for which isolated populations persist) to characterize infection profiles in highly Bd-susceptible amphibians post-decline. We found highly variable patterns in infection, with some species showing low prevalence (~10%) and low infection intensity and others showing high infection prevalence (>80%) and either low or high infection intensity. Across sites, infection rates were negatively associated with mean annual precipitation, and infection intensity across sites was negatively associated with mean average temperatures. Our results illustrate that even the most Bd-susceptible amphibians can persist in Bd-enzootic ecosystems, and that multiple ecological or evolutionary mechanisms likely exist for host-pathogen co-existence between Bd and the most Bd-susceptible amphibian species. Continued monitoring of these populations is necessary to evaluate population trends (continuing decline, stability, or population growth). These results should inform efforts to mitigate impacts of Bd on amphibians in the field.

Infection with Batrachochytrium dendrobatidis is common in tropical lowland habitats: Implications for amphibian conservation

“…However, the extirpation of the Golfito robber frog in this area, where it was abundant before the 1980s and 1990s (Chaves et al, ), suggests this may not be the case. We also found the highest levels of Bd prevalence in the Caribbean sites which coincide with studies conducted in the nearby locations within the same geographic zone (Whitfield et al, , , ). Thus, even within lowland zones, there is large variation in Bd prevalence across zones and sites.…”

“…The populations of C. taurus and A. lemur that we surveyed also tested positive in past surveys (Briggs et al, ; Whitfield et al, ). The continuous occurrence of these endangered species and the lack of clinical signs of chytridiomycosis in Bd‐infected individuals (Berger et al, ; Voyles et al, ) suggest these populations are capable of surviving with enzootic Bd dynamics (Whitfield et al, ). Remarkably, infection levels in several individuals of the robber frog ( C. taurus ) were above 10,000 Bd genomic equivalents, a theoretical threshold that has been linked to epizootic outbreaks, population die‐offs, and local extinctions (Vredenburg et al, ).…”

“…The three endangered species sampled (Craugastor taurus, Agalychnis lemur, and Oophaga granulifera) tested positive for Bd (Table 2). The populations of C. taurus and A. lemur that we surveyed also tested positive in past surveys Whitfield et al, 2017). The continuous occurrence of these endangered species and the lack of clinical signs of chytridiomycosis in Bd-infected individuals (Berger et al, 1998;Voyles et al, 2009) suggest these populations are capable of surviving with enzootic Bd dynamics .…”

“…Low sample sizes were caused by low detectability during the survey period for some of the common species (e.g., Rhinella horribilis, Smilisca sordida, Lithobates vaillanti, Leptodactylus savagei ) or due to the low year‐round detectability for the more cryptic and rare species (e.g., fossorial and canopy dwellers like Oedipina gracilis, Bolitoglossa colonnea, Cruziohyla calcarifer ). To increase species detectability and/or sample size, future studies in lowlands and neglected sites should conduct surveys restricting or focusing the sampling on threatened species (Thorpe et al, ; Whitfield et al, ), to describe host–pathogen population dynamics, or preferably survey multiple species across seasons to obtain more accurate estimates of prevalence and infection intensity for all species within the amphibian community (Brannelly et al, ; Kinney et al, ; Vredenburg et al, ).…”

“…Similar studies conducted in lowlands of Costa Rica also suggest seasonal dynamics. For example, remnant populations of the lowland robber frog C. ranoides in the tropical dry forest of Costa Rica exhibited infection prevalence values that varied from <1 to 60% across a dry season (December to May) (Whitfield et al, ; Zumbado‐Ulate et al, ). Similarly, prevalence of Bd varied from <5% to around 35% in an amphibian assemblage in tropical lowland forest across 1‐year period (Whitfield et al, ).…”