Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Hotspot shelters stimulate frog resistance to chytridiomycosis

Abstract

Many threats to biodiversity cannot be eliminated; for example, invasive pathogens may be ubiquitous. Chytridiomycosis is a fungal disease that has spread worldwide, driving at least 90 amphibian species to extinction, and severely affecting hundreds of others1,2,3,4. Once the disease spreads to a new environment, it is likely to become a permanent part of that ecosystem. To enable coexistence with chytridiomycosis in the field, we devised an intervention that exploits host defences and pathogen vulnerabilities. Here we show that sunlight-heated artificial refugia attract endangered frogs and enable body temperatures high enough to clear infections, and that having recovered in this way, frogs are subsequently resistant to chytridiomycosis even under cool conditions that are optimal for fungal growth. Our results provide a simple, inexpensive and widely applicable strategy to buffer frogs against chytridiomycosis in nature. The refugia are immediately useful for the endangered species we tested and will have broader utility for amphibian species with similar ecologies. Furthermore, our concept could be applied to other wildlife diseases in which differences in host and pathogen physiologies can be exploited. The refugia are made from cheap and readily available materials and therefore could be rapidly adopted by wildlife managers and the public. In summary, habitat protection alone cannot protect species that are affected by invasive diseases, but simple manipulations to microhabitat structure could spell the difference between the extinction and the persistence of endangered amphibians.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Effects of various thermal treatments on chytrid infection.
Fig. 2: Effects of prior pathogen exposure on chytrid infection and survivorship.
Fig. 3: Effects of higher operative temperatures and prior pathogen exposure on frog body temperature and chytrid infection.

Similar content being viewed by others

Data availability

Our data are available through figshare at https://doi.org/10.6084/m9.figshare.23672805 (ref. 46). Source data are provided with this paper.

Code availability

The R code used for our GAMMs is available through GitHub: https://github.com/erinsauer/Waddle-et-al.-Hotspot-shelters.

References

  1. Wake, D. B. & Vredenburg, V. T. Are we in the midst of the sixth mass extinction? A view from the world of amphibians. Proc. Natl Acad. Sci. USA 105, 11466–11473 (2008).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  2. Berger, L. et al. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proc. Natl Acad. Sci. USA 95, 9031–9036 (1998).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  3. Longcore, J. E., Pessier, A. P. & Nichols, D. K. Batrachochytrium dendrobatidis gen. et sp. nov., a chytrid pathogenic to amphibians. Mycologia 91, 219–227 (1999).

    Article  Google Scholar 

  4. Scheele, B. C. et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363, 1459–1463 (2019).

    Article  ADS  CAS  PubMed  Google Scholar 

  5. Stockwell, M., Clulow, S., Clulow, J. & Mahony, M. The impact of the amphibian chytrid fungus Batrachochytrium dendrobatidis on a green and golden bell frog Litoria aurea reintroduction program at the Hunter Wetlands Centre Australia in the Hunter Region of NSW. Aust. Zool. 34, 379–386 (2008).

    Article  Google Scholar 

  6. Brannelly, L. A. et al. Chytrid infection and post‐release fitness in the reintroduction of an endangered alpine tree frog. Anim. Conserv. 19, 153–162 (2016).

    Article  Google Scholar 

  7. Berger, L. et al. Effect of season and temperature on mortality in amphibians due to chytridiomycosis. Aust. Vet. J. 82, 434–439 (2004).

    Article  CAS  PubMed  Google Scholar 

  8. Waddle, A. W. et al. Amphibian resistance to chytridiomycosis increases following low‐virulence chytrid fungal infection or drug‐mediated clearance. J. Appl. Ecol. 58, 2053–2064 (2021).

    Article  CAS  Google Scholar 

  9. Piotrowski, J. S., Annis, S. L. & Longcore, J. E. Physiology of Batrachochytrium dendrobatidis, a chytrid pathogen of amphibians. Mycologia 96, 9–15 (2004).

    Article  PubMed  Google Scholar 

  10. Voyles, J. et al. Diversity in growth patterns among strains of the lethal fungal pathogen Batrachochytrium dendrobatidis across extended thermal optima. Oecologia 184, 363–373 (2017).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  11. Andre, S. E., Parker, J. & Briggs, C. J. Effect of temperature on host response to Batrachochytrium dendrobatidis infection in the mountain yellow-legged frog (Rana muscosa). J. Wildl. Dis. 44, 716–720 (2008).

    Article  PubMed  Google Scholar 

  12. Greenspan, S. E. et al. Realistic heat pulses protect frogs from disease under simulated rainforest frog thermal regimes. Funct. Ecol. 31, 2274–2286 (2017).

    Article  Google Scholar 

  13. Cohen, J. M. et al. The thermal mismatch hypothesis explains host susceptibility to an emerging infectious disease. Ecol. Lett. 20, 184–193 (2017).

    Article  PubMed  Google Scholar 

  14. Bustamante, H. M., Livo, L. J. & Carey, C. Effects of temperature and hydric environment on survival of the Panamanian Golden Frog infected with a pathogenic chytrid fungus. Integr. Zool. 5, 143–153 (2010).

    Article  PubMed  Google Scholar 

  15. Savage, A. E., Sredl, M. J. & Zamudio, K. R. Disease dynamics vary spatially and temporally in a North American amphibian. Biol. Conserv. 144, 1910–1915 (2011).

    Article  Google Scholar 

  16. Bell, S. C., Heard, G. W., Berger, L. & Skerratt, L. F. Connectivity over a disease risk gradient enables recovery of rainforest frogs. Ecol. Appl. 30, e02152 (2020).

    Article  PubMed  Google Scholar 

  17. Heard, G. W. et al. Refugia and connectivity sustain amphibian metapopulations afflicted by disease. Ecol. Lett. 18, 853–863 (2015).

    Article  ADS  PubMed  Google Scholar 

  18. Hettyey, A. et al. Mitigating disease impacts in amphibian populations: capitalizing on the thermal optimum mismatch between a pathogen and its host. Front. Ecol. Evol. 7, 254 (2019).

    Article  Google Scholar 

  19. Sauer, E. L., Sperry, J. H. & Rohr, J. R. An efficient and inexpensive method for measuring long-term thermoregulatory behavior. J. Therm. Biol. 60, 231–236 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Sauer, E. L. et al. Variation in individual temperature preferences, not behavioural fever, affects susceptibility to chytridiomycosis in amphibians. Proc. R. Soc. B 285, 20181111 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  21. Hamer, A. J., Lane, S. J. & Mahony, M. J. Retreat site selection during winter in the green and golden bell frog, Litoria aurea Lesson. J. Herpetol. 37, 541–545 (2003).

    Article  Google Scholar 

  22. Abu Bakar, A. et al. Susceptibility to disease varies with ontogeny and immunocompetence in a threatened amphibian. Oecologia 181, 997–1009 (2016).

    Article  ADS  PubMed  Google Scholar 

  23. Hammond, T. T. et al. Overwinter behavior, movement, and survival in a recently reintroduced, endangered amphibian, Rana muscosa. J. Nat. Conserv. 64, 126086 (2021).

    Article  Google Scholar 

  24. McMahon, T. A. et al. Amphibians acquire resistance to live and dead fungus overcoming fungal immunosuppression. Nature 511, 224–227 (2014).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  25. Bakewell, L., Kelehear, C. & Graham, S. P. Impacts of temperature on immune performance in a desert anuran (Anaxyrus punctatus). J. Zool. 315, 49–57 (2021).

    Article  Google Scholar 

  26. Valdez, J. et al. Microhabitat selection varies by sex and age class in the endangered green and golden bell frog Litoria aurea. Aust. Zool. 38, 223–234 (2016).

    Article  Google Scholar 

  27. Sauer, E. L., Trejo, N., Hoverman, J. T. & Rohr, J. R. Behavioural fever reduces ranaviral infection in toads. Funct. Ecol. 33, 2172–2179 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  28. Richards-Zawacki, C. L. Thermoregulatory behaviour affects prevalence of chytrid fungal infection in a wild population of Panamanian golden frogs. Proc. R. Soc. B 277, 519–528 (2010).

    Article  PubMed  Google Scholar 

  29. Puschendorf, R. et al. Environmental refuge from disease‐driven amphibian extinction. Conserv. Biol. 25, 956–964 (2011).

    Article  PubMed  Google Scholar 

  30. McCoy, C. M., Lind, C. M. & Farrell, T. M. Environmental and physiological correlates of the severity of clinical signs of snake fungal disease in a population of pigmy rattlesnakes, Sistrurus miliarius. Conserv. Physiol. 5, cow077 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Hopkins, S. R. et al. Continued preference for suboptimal habitat reduces bat survival with white-nose syndrome. Nat. Commun. 12, 166 (2021).

    Article  MathSciNet  CAS  PubMed  PubMed Central  Google Scholar 

  32. Berger, L. et al. Advances in managing chytridiomycosis for Australian frogs: Gradarius Firmus Victoria. Annu. Rev. Anim. Biosci. 12, 113–133 (2024).

    Article  PubMed  Google Scholar 

  33. Kosch, T. A. et al. Genetic approaches for increasing fitness in endangered species. Trends Ecol. Evol. 37, 332–225 (2022).

    Article  CAS  PubMed  Google Scholar 

  34. Heard, G. W. et al. Can habitat management mitigate disease impacts on threatened amphibians? Conserv. Lett. 11, e12375 (2018).

    Article  Google Scholar 

  35. Rhoo, K. H. et al. Distinct host–mycobacterial pathogen interactions between resistant adult and tolerant tadpole life stages of Xenopus laevis. J. Immunol. 203, 2679–2688 (2019).

    Article  CAS  PubMed  Google Scholar 

  36. Clulow, S. et al. Elevated salinity blocks pathogen transmission and improves host survival from the global amphibian chytrid pandemic: Implications for translocations. J. Appl. Ecol. 55, 830–840 (2018).

    Article  CAS  Google Scholar 

  37. Murray, K. et al. The distribution and host range of the pandemic disease chytridiomycosis in Australia, spanning surveys from 1956–2007. Ecology 91, 1557–1558 (2010).

    Article  Google Scholar 

  38. O’hanlon, S. J. et al. Recent Asian origin of chytrid fungi causing global amphibian declines. Science 360, 621–627 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  39. Fisher, M. C. et al. Development and worldwide use of non-lethal, and minimal population-level impact, protocols for the isolation of amphibian chytrid fungi. Sci. Rep. 8, 7772 (2018).

    Article  ADS  PubMed  PubMed Central  Google Scholar 

  40. Waddle, A. W. et al. Systematic approach to isolating Batrachochytrium dendrobatidis. Dis. Aquat. Organ. 127, 243–247 (2018).

    Article  CAS  PubMed  Google Scholar 

  41. Jaeger, J. R. et al. Batrachochytrium dendrobatidis and the decline and survival of the relict leopard frog. EcoHealth 14, 285–295 (2017).

    Article  PubMed  Google Scholar 

  42. Waddle, A. W. et al. Population-level resistance to chytridiomycosis is life-stage dependent in an imperiled anuran. EcoHealth 16, 701–711 (2019).

    Article  PubMed  Google Scholar 

  43. Boyle, D. G., Boyle, D. B., Olsen, V., Morgan, J. A. T. & Hyatt, A. D. Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay. Dis. Aquat. Organ. 60, 141–148 (2004).

    Article  CAS  PubMed  Google Scholar 

  44. Brannelly, L. A., Wetzel, D. P., West, M. & Richards-Zawacki, C. L. Optimized Batrachochytrium dendrobatidis DNA extraction of swab samples results in imperfect detection particularly when infection intensities are low. Dis. Aquat. Organ. 139, 233–243 (2020).

    Article  PubMed  Google Scholar 

  45. R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org/ (R Foundation for Statistical Computing, 2020).

  46. Waddle, A. et al. Data for reinfection study, thermal preference study, behavioural fever study, and mesocosm study. Figshare https://doi.org/10.6084/m9.figshare.23672805 (2024).

Download references

Acknowledgements

We thank M. Elphick, B. Ashton, R. Miller, C. Wilson, K. Pasfield and H. Malouf for their assistance with setting up mesocosms; M. Whiting for lending us laboratory space for disease testing; M. Elphick for assistance with data entry and management; V. Russell and S. Deering for their assistance with data collection; and M. Holmes for assistance with visuals. A.W.W. was supported by a Melbourne Research Scholarship, a Graduate Education Scholarship from the American Australian Association, and also supported by the Schmidt Science Fellows, in partnership with the Rhodes Trust; L.F.S. was supported by ARC FT190100462; S.C. was supported by a Macquarie University Research Fellowship; and J.A.F. was supported by ARC DP200100747 and ARC FT210100034. Research funding was provided by Macquarie University. Additional funding was provided by the Frog and Tadpole Study Group of New South Wales, a Royal Zoological Society of New South Wales Ethel Mary Read Student Grant and a Holsworth Wildlife Research Endowment Student Grant.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: A.W.W., S.C., E.L.S. and R.S. Methodology: A.W.W., S.C., R.S. and E.L.S. Investigation: A.W.W., A.A., H.G., I.D., R.S. and S.W.K. Validation: A.W.W., Y.L., E.L.S. and R.S. Visualization: A.W.W., E.L.S. and Y.L. Funding acquisition: A.W.W., R.S. and S.C. Data curation: A.W.W., C.M., J.A.F., P.T.C., R.S., Y.L. and E.L.S. Writing (original draft): A.W.W. Writing (review and editing): A.W.W., L.F.S., L.B., R.S. and Y.L.

Corresponding author

Correspondence to Anthony W. Waddle.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Peer review

Peer review information

Nature thanks Ross Alford, Brian Gratwicke and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data figures and tables

Extended Data Fig. 1 Effects of various preferred temperature regimes on chytrid infection.

Infection intensity data for green and golden bell frogs (L. aurea) that were exposed to Bd. Frogs were infected with Bd, held at 19.0 °C for 14 days and then placed at one of three temperatures (26.4 °C, 29.1 °C or 31.0 °C), on the basis of the temperatures selected by those individuals in a previous study.

Extended Data Fig. 2 Effects of heat treatments on chytrid infection intensity and survivorship.

a,b, Infection intensity (a) and survivorship data (b) for green and golden bell frogs (L. aurea) that were exposed to Bd. Heat control frogs (n = 23) were treated with heat and then exposed to Bd, whereas Bd control frogs (n = 23) had no heat treatment before Bd exposure.

Extended Data Fig. 3 Experimental treatments and design of hothouse thermal shelters for the mesocosm study.

a,b, Mesocosm set-up for unshaded greenhouse (a) and shaded greenhouse (b) treatments. c, Brick configuration inside greenhouses. Photo credit A.W.W.

Extended Data Fig. 4 Design of thermal gradients for thermal selection experiments.

Green and golden bell frogs (L. aurea) in thermal gradients. Photo credit A.W.W.

Extended Data Table 1 Daily temperature extremes in thermal shelters and the surrounding environment

Supplementary information

Supplementary Information

This file contains Supplementary Results and Supplementary Table 1

Reporting Summary

Source data

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Waddle, A.W., Clulow, S., Aquilina, A. et al. Hotspot shelters stimulate frog resistance to chytridiomycosis. Nature 631, 344–349 (2024). https://doi.org/10.1038/s41586-024-07582-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41586-024-07582-y

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing Microbiology

Sign up for the Nature Briefing: Microbiology newsletter — what matters in microbiology research, free to your inbox weekly.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing: Microbiology