Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression

Abstract

Emerging fungal pathogens pose a greater threat to biodiversity than any other parasitic group1, causing declines of many taxa, including bats, corals, bees, snakes and amphibians1–4. Currently, there is little evidence that wild animals can acquire resistance to these pathogens5. Batrachochytrium dendrobatidis is a pathogenic fungus implicated in the recent global decline of amphibians6. Here we demonstrate that three species of amphibians can acquire behavioural or immunological resistance to B. dendrobatidis. Frogs learned to avoid the fungus after just one B. dendrobatidis exposure and temperature-induced clearance. In subsequent experiments in which B. dendrobatidis avoidance was prevented, the number of previous exposures was a negative predictor of B. dendrobatidis burden on frogs and B. dendrobatidis-induced mortality, and was a positive predictor of lymphocyte abundance and proliferation. These results suggest that amphibians can acquire immunity to B. dendrobatidis that overcomes pathogen-induced immunosuppression7–9 and increases their survival. Importantly, exposure to dead fungus induced a similar magnitude of acquired resistance as exposure to live fungus. Exposure of frogs to B. dendrobatidis antigens might offer a practical way to protect pathogen-naive amphibians and facilitate the reintroduction of amphibians to locations in the wild where B. dendrobatidis persists. Moreover, given the conserved nature of vertebrate immune responses to fungi5 and the fact that many animals are capable of learning to avoid natural enemies10, these results offer hope that other wild animal taxa threatened by invasive fungi might be rescued by management approaches based on herd immunity.

American Bullfrogs (Lithobates catesbeianus) Resist Infection by Multiple Isolates of Batrachochytrium dendrobatidis, Including One Implicated in Wild Mass Mortality

“…The relatively thick epidermis of this species, which allows for rapid skin sloughing and thus shedding of epidermal Bd infection, may contribute to resistance (Greenspan et al 2012a, b). In addition, the complete lack of infection following our second exposure with SL Bd might be partially attributable to primed host defenses that conferred effective resistance to these individuals, all of which had been previously exposed to Bd (Shaw et al 2010;McMahon et al 2014). However, the lack of clinical signs of chytridiomycosis in the American bullfrogs that did become infected indicates tolerance mechanisms also play a role in bullfrogBd interactions, as previous work has suggested (Hanselmann et al 2004;Greenspan et al 2012b).…”

“…The distinction between infection resistance and tolerance is rarely made with respect to Bd infection in amphibians , but see Savage and Zamudio 2011;Reeder et al 2012;Gervasi et al 2013b;McMahon et al 2014), yet these host defense mechanisms have profoundly different implications for disease risk within the broader amphibian community. If American bullfrogs commonly clear themselves of Bd infection or avoid infection altogether as a result of resistance mechanisms, then bullfrogs are less likely to be important Bd carriers as is often suggested (Mazzoni et al 2003;Daszak et al 2004;Hanselmann et al 2004;Garner et al 2006;Schloegel et al 2010).…”

Large-scale recovery of an endangered amphibian despite ongoing exposure to multiple stressors

“…Second, the lower susceptibility could be the result of an acquired immune response in frogs from persistent populations after their exposure to Bd in the wild, a response that itself could be subject to natural selection. If R. sierrae are, in fact, capable of mounting such a response (as is the case in other anurans) (35,38), frogs from the persistent populations could have had at least partial immunity against Bd before the start of the experiment, and those from naïve populations would not have. A series of experiments is underway to describe adaptive immunity against Bd in R. sierrae.…”

Condition-dependent reproductive effort in frogs infected by a widespread pathogen

“…This could be because infected frogs were unable to call owing to physiological changes caused by their infections, or because frogs were adaptively adjusting their energy expenditure. For example, they may have been allocating less energy to reproduction and more to other functions required for immediate survival, such as immune responses to fight their infections [46].…”