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Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression

2014; Nature Portfolio; Volume: 511; Issue: 7508 Linguagem: Inglês

10.1038/nature13491

1476-4687

Taegan A. McMahon, Brittany Sears, Matthew D. Venesky, Scott Bessler, Jenise M. Brown, Kaitlin R. Deutsch, Neal T. Halstead, Garrett Lentz, Nadia Tenouri, S. M. M. Young, David J. Civitello, Nicole Ortega, J. Scott Fites, Laura K. Reinert, Louise A. Rollins‐Smith, Thomas R. Raffel, Jason R. Rohr,

Species Distribution and Climate Change

The fungal pathogen Batrachochytrium dendrobatidis has been implicated in the decline of a large number of amphibian species; here it is shown that frogs can learn to avoid the pathogen, acquire resistance to it and be immunized against it using dead pathogen, findings that potentially offer a way in which resistant populations could be reintroduced into areas that have seen catastrophic declines. The fungal pathogen Batrachochytrium dendrobatidis, or Bd, has been implicated in the declines of many amphibian species worldwide. There has been little evidence that amphibians can acquire resistance to this pathogen, but now Jason Rohr and colleagues present experiments on several amphibian species, including the Cuban tree frog Osteopilus septentrionalis, shown here, that demonstrate that frogs can learn to avoid the pathogen, can overcome Bd-induced immunosuppression after repeated exposure, and can be immunized against it using dead pathogen. Conservation projects have removed threatened amphibian species from Bd-positive habitats and are breeding them in captivity. Using vaccines to induce resistance in captive-bred amphibians prior to a return to the wild could make it possible in the future to repopulate areas that have seen catastrophic declines. 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 amphibians1,2,3,4. 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 immunosuppression7,8,9 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.