Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research

Abstract

The amphibian fungal disease chytridiomycosis, which affects species across all continents, recently emerged as one of the greatest threats to biodiversity. Yet, many aspects of the basic biology and epidemiology of the pathogen, Batrachochytrium dendrobatidis (Bd), are still unknown, such as when and from where did Bd emerge and what is its true ecological niche? Here, we review the ecology and evolution of Bd in the Americas and highlight controversies that make this disease so enigmatic. We explore factors associated with variance in severity of epizootics focusing on the disease triangle of host susceptibility, pathogen virulence, and environment. Reevaluating the causes of the panzootic is timely given the wealth of data on Bd prevalence across hosts and communities and the recent discoveries suggesting co‐evolutionary potential of hosts and Bd. We generate a new species distribution model for Bd in the Americas based on over 30,000 records and suggest a novel future research agenda. Instead of focusing on pathogen “hot spots,” we need to identify pathogen “cold spots” so that we can better understand what limits the pathogen's distribution. Finally, we introduce the concept of “the Ghost of Epizootics Past” to discuss expected patterns in postepizootic host communities.

Spatial distribution of Batrachochytrium dendrobatidis in South American caecilians

“…These results, combined with a recent report of lethal chytridiomycosis in wild-caught caecilians (Gower et al 2013), indicate that Gymno phiona are potentially experiencing silent population declines in the wild due to Bd. Spatial regressions are also consistent with the observed associations between macroclimate and Bd infection in anuran species (Becker & Zamudio 2011, James et al 2015, Becker et al 2016. Specifically, we detected a positive effect of precipitation and a negative effect of temperature variables on the likelihood of Bd infection in caecilian hosts.…”

“…Because Bd is a waterborne fungus (Longcore et al 1999, Kilpatrick et al 2010, we also expect fully aquatic caecilians to be exposed to the pathogen not only during their early life stages. Therefore, fossorial and aquatic life styles observed in caecilians are life history traits that likely make an efficient host reservoir, espe- James et al 2015, Becker et al 2016, we detected an infection prevalence of 16%, which is surprisingly high compared to the observed ~3% in museum-preserved anurans in this region (Becker et al 2016). In contrast, the proportion of infected caecilians in the Atlantic Forest was slightly lower than what has been observed for preserved anurans (~23%) in this ecoregion (Rodriguez et al 2014).…”

“…Service layer source: US National Park Service (Rödder et al 2009, Liu et al 2012, James et al 2015, Becker et al 2016. Although most of the Bdpositive records overlapped with reported areas of high climatic suitability for the fungus in the Neotropics (Rödder et al 2009, Liu et al 2012, James et al 2015, Becker et al 2016, several Bd-positive records extend far into areas of poor suitability for Bd in anurans (e.g. central Amazon: see Becker et al 2016).…”

“…Furthermore, conspicuous die-offs due to chytridiomycosis, such as those observed in anurans, are relatively unlikely to be observed in caecilians (Gower et al 2013) due to their fossorial or fully aquatic life styles (Wells 2007, Vitt & Caldwell 2014. Caecilians are broadly distributed in the tropics (Taylor 1968, Frost 2016, often co-occurring with anuran populations heavily impac ted by chytridiomycosis (Seimon et al 2007, Gower et al 2012, Bataille et al 2013, James et al 2015 and inhabiting microhabitats within Bd's optimal growth conditions of temperature and humidity (Piotrowski et al 2004). Determining whether caecilians are af fected by chytridiomycosis as much as anurans and salamanders are, and whether caecilians are serving as pathogen reservoirs, is relevant for amphibian conservation (Gower & Wilkinson 2005).…”

Jumping into a trap: high prevalence of chytrid fungus in the preferred microhabitats of a bromeliad-specialist frog

“…The pathogenic chytrid fungus Batrachochytrium dendrobatidis (hereafter Bd) has now been detected in over 500 amphibian species worldwide (Olson et al 2013, James et al 2015. Despite its documented role in amphibian population declines (e.g.…”