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Population-Level Resistance to Chytridiomycosis is Life-Stage Dependent in an Imperiled Anuran

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Abstract

Amphibian declines caused by chytridiomycosis have been severe, but some susceptible populations have persisted or even recovered. Resistance to the causal agent Batrachochytrium dendrobatidis (Bd) could result from alleles of the adaptive immune system. During metamorphosis, however, immune systems may not be fully functional, implying that an effective immune response to Bd may be life-stage dependent. We evaluated the susceptibility of the relict leopard frog (Rana onca) sourced from two areas where Bd was present or absent, and where the populations appeared to show differences in pathogen resistance. We evaluated whether population-level resistance manifested across life stages using challenge experiments with late-stage tadpoles (Gosner stage 31–38), metamorphs (stage 45–46), and juvenile frogs. We used three different Bd isolates including one from wild R. onca to challenge juvenile frogs and focused on the isolate from R. onca to challenge tadpoles and resulting metamorphs. We found that juveniles from the Bd exposed population were 5.5 times more likely to survive Bd infection and 10 times more likely to clear infections than those from the area without Bd. In contrast, and regardless of the source area, we observed 98% survivorship of tadpoles, but only 19% survivorship of resulting metamorphs following re-exposure. Given the low survivorship of exposed metamorphs in the laboratory, we speculate on how resistance characteristics, whether adaptive or innate, that do not manifest at each life stage could develop in the wild. We suggest that seasonal high temperatures during times when metamorphosis appears common may modulate the effects of the pathogen during this most susceptible life stage.

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Acknowledgements

This research was predominately supported by the Bureau of Land Management under agreement with the University of Nevada, Las Vegas (UNLV), and we thank Mark Slaughter for his interest in our research questions and for his efforts in gaining support. Additional support was provided by the UNLV Graduate and Professional Student Association. We recognize the following individuals for their laboratory or field assistance: Marlai Sai, Ghazal Rezaei, Audrey Bischoff, Nikhil Pattni, Jason Burgins, Shaylene Scarlett, Alexandra Zmuda, David Miller, Jessica Hill, Yesenia Vasquez, Alexa Krauss, Lori Scholer, Brandon Barrett, Ally Rezazadeh, Briana Miskey-Patterson, Charles Ronkon, Claudia Silva Rubio, Kevin Guadalupe, and Daniel Villanueva. Laura Brannelly provided statistical advice. All applicable institutional and national guidelines for the care and use of animals were followed. Protocols involving live animals were approved by the UNLV Institutional Care and Use Committee. Field efforts were conducted under permits from the Nevada Department of Wildlife, Spring Mountain Ranch State Park, and the National Park Service, Lake Mead National Recreation Area.

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Funding was provided by US Bureau of Land Management (Agreement # L16AC00149).

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Correspondence to Anthony W. Waddle.

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Waddle, A.W., Levy, J.E., Rivera, R. et al. Population-Level Resistance to Chytridiomycosis is Life-Stage Dependent in an Imperiled Anuran. EcoHealth 16, 701–711 (2019). https://doi.org/10.1007/s10393-019-01446-y

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  • DOI: https://doi.org/10.1007/s10393-019-01446-y

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