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Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs

  • Population Ecology
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Abstract

Many species of amphibians in the wet tropics of Australia have experienced population declines linked with the emergence of a skin-invasive chytrid fungus, Batrachochytrium dendrobatidis. An innate defense, antimicrobial peptides produced by granular glands in the skin, may protect some species from disease. Here we present evidence that supports this hypothesis. We tested ten synthesized peptides produced by Australian species, and natural peptide mixtures from five Queensland rainforest species. Natural mixtures and most peptides tested in isolation inhibited growth of B. dendrobatidis in vitro. The three most active peptides (caerin 1.9, maculatin 1.1, and caerin 1.1) were found in the secretions of non-declining species (Litoria chloris, L. caerulea, and L. genimaculata). Although the possession of a potent isolated antimicrobial peptide does not guarantee protection from infection, non-declining species (L. lesueuri and L. genimaculata) inhabiting the rainforest of Queensland possess mixtures of peptides that may be more protective than those of the species occurring in the same habitat that have recently experienced population declines associated with chytridiomycosis (L. nannotis, L. rheocola, and Nyctimystes dayi). This study demonstrates that in vitro effectiveness of skin peptides correlates with the degree of decline in the face of an emerging pathogen. Further research is needed to assess whether this non-specific immune defense may be useful in predicting disease susceptibility in other species.

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Acknowledgements

Ethical approval (A699_01) for all surveys and experiments was granted from James Cook University, and the following permits were granted: Scientific Purposes Permits and Take, Use, Keep or Interfere with Cultural or Natural Resources Permits WISP00443102, WITK00441702, F1/000375/01/SAA, Wildlife Movement Permit WIWM00525702 from the Environmental Protection Agency and Queensland Parks and Wildlife Service; and Department of Natural Resources permits to collect biological or geological material from Queensland state forest, timber reserves and other state lands #1733. This research was supported by subcontracts to L.R.-S. and R.A.A. from an NSF Integrated Research Challenges in Environmental Biology grants IBN-9977063 and DEB-0213851 (James Collins, P.I.) and NSF grant IBN-0131184 to L.R-S. D.C.W. was supported by a Doctoral Research Scholarship, Supplementary Internal Research Account Scholarship, and International Post-Graduate Research Scholarship from James Cook University, a Grant-in-Aid of Research from the National Academy of Sciences administered by Sigma-Xi, The Scientific Research Society, and the Immunobiology of Blood and Vascular Systems Training Program (NIH 5 T32 HL069765-02). We are grateful for the generous donation of peptides from Dr. John Bowie and helpful discussion about the manuscript. We thank Dr. Elizabeth Davidson and Verma Miera for isolation of the VM1 isolate of B. dendrobatidis. For field assistance, we thank Sara Townsend and volunteers: Brian Brinkman, Jasmine Cauchi, Kathryn Lewthwaite, Fiona Marshall, Esther Mitchell, Thor Sawin, and Kendall Trudgen.

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  1. Douglas C. Woodhams

    Present address: Department of Microbiology and Immunology, A-5301 Medical Center North, Vanderbilt University, Nashville, TN, 37232, USA

Authors and Affiliations

  1. School of Tropical Biology, James Cook University, 4811, Townsville, QLD, Australia

    Douglas C. Woodhams & Ross A. Alford

  2. Departments of Microbiology and Immunology and of Pediatrics, Vanderbilt University Medical Center, Nashville, TN, 37232, USA

    Louise A. Rollins-Smith & Laura Reinert

  3. Department of Integrative Physiology, University of Colorado, Boulder, CO, 80309, USA

    Cynthia Carey

  4. Department of Environmental Biology, University of Adelaide, 5005, South Australia, Australia

    Michael J. Tyler

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  1. Douglas C. Woodhams
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Correspondence to Douglas C. Woodhams.

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Communicated by Libby Marschall

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Woodhams, D.C., Rollins-Smith, L.A., Carey, C. et al. Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146, 531–540 (2006). https://doi.org/10.1007/s00442-005-0228-8

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