Amphibian species traits, evolutionary history and environment predict Batrachochytrium dendrobatidis infection patterns, but not extinction risk

Abstract

The fungal pathogen Batrachochytrium dendrobatidis (B. dendrobatidis) has emerged as a major agent of amphibian extinction, requiring conservation intervention for many susceptible species. Identifying susceptible species is challenging, but many aspects of species biology are predicted to influence the evolution of host resistance, tolerance, or avoidance strategies towards disease. In turn, we may expect species exhibiting these distinct strategies to differ in their ability to survive epizootic disease outbreaks. Here, we test for phylogenetic and trait‐based patterns of B. dendrobatidis infection risk and infection intensity among 302 amphibian species by compiling a global data set of B. dendrobatidis infection surveys across 95 sites. We then use best‐fit models that associate traits, taxonomy and environment with B. dendrobatidis infection risk and intensity to predict host disease mitigation strategies (tolerance, resistance, avoidance) for 122 Neotropical amphibian species that experienced epizootic B. dendrobatidis outbreaks, and noted species persistence or extinction from these events. Aspects of amphibian species life history, habitat use and climatic niche were consistently linked to variation in B. dendrobatidis infection patterns across sites around the world. However, predicted B. dendrobatidis infection risk and intensity based on site environment and species traits did not reveal a consistent pattern between the predicted host disease mitigation strategy and extinction outcome. This suggests that either tolerant or resistant species may have no advantage in ameliorating disease during epizootic events, or that other factors drive the persistence of amphibian populations during chytridiomycosis outbreaks. These results suggest that using a trait‐based approach may allow us to identify species with resistance or tolerance to endemic B. dendrobatidis infections, but that this approach may be insufficient to ultimately identify species at risk of extinction from epizootics.

Longitudinal study of Amphibiocystidium sp. infection in a natural population of the Italian stream frog (Rana italica)

“…In those cases, the disease incidence increased and the infected frogs eliminated the infection after a longer time than previously. A disease triangle (host–pathogen–environment interactions) has often been considered the key for explaining disease outcome (Scholthof, 2007; James et al ., 2015; Lips, 2016; Greenberg et al ., 2017; Scheele et al ., 2017). The trend observed in this study could have been promoted by changes in the environmental context in which host–parasite interaction favoured both the rate of infection transmission and the spread of the parasite, increasing its ability to reproduce, but without causing the loss of individuals.…”

“…Some amphibian populations showed stability and disease recovery (Retallick et al ., 2004; Puschendorf et al ., 2011; Tobler et al ., 2012; Newell et al ., 2013), while others continued to be threatened by endemic chytridiomycosis despite host–pathogen coexistence for multiple host generations (Murray et al ., 2009; Pilliod et al ., 2010; Phillott et al ., 2013; Scheele et al ., 2015). Several authors have argued that infection outcome, including chytridiomycosis, depends on physiological responses that must be considered within the context of host-specific factors, including life history, ecology, behaviour and physiology, and environmental conditions in which host and pathogen interact (Råberg et al ., 2009; Blaustein et al ., 2012; Murone et al ., 2016; Greenberg et al ., 2017).…”

Deeply conserved susceptibility in a multi‐host, multi‐parasite system

“…; plant pathogens – Gilbert & Parker ; amphibian fungal pathogens – Greenberg et al . ). If susceptibility is conserved, it would indicate that real‐time ecological interactions are partly contingent on deep‐time evolutionary history.…”

Low-load pathogen spillover predicts shifts in skin microbiome and survival of a terrestrial-breeding amphibian

“…We selected four aquatic-breeding amphibian species with varying life histories (stream and pond breeders; tree frogs and frogs), and one focal terrestrial-breeding species: the pumpkin toadlet Brachycephalus pitanga. Terrestrial-breeding amphibians tend to be less exposed to waterborne Bd throughout their ontogeny [23] and thus show lower acquired immunity and resistance to the pathogen than aquatic-breeding species [24]. To maximize ecological realism, we conducted an experiment using wild-collected hosts harbouring natural symbiotic microbiomes and Bd infection loads.…”