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Susceptibility to disease varies with ontogeny and immunocompetence in a threatened amphibian

  • Physiological ecology - original research
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Abstract

Ontogenetic changes in disease susceptibility have been demonstrated in many vertebrate taxa, as immature immune systems and limited prior exposure to pathogens can place less developed juveniles at a greater disease risk. By causing the disease chytridiomycosis, Batrachochytrium dendrobatidis (Bd) infection has led to the decline of many amphibian species. Despite increasing knowledge on how Bd varies in its effects among species, little is known on the interaction between susceptibility and development within host species. We compared the ontogenetic susceptibility of post-metamorphic green and golden bell frogs Litoria aurea to chytridiomycosis by simultaneously measuring three host-pathogen responses as indicators of the development of the fungus—infection load, survival rate, and host immunocompetence—following Bd exposure in three life stages (recently metamorphosed juveniles, subadults, adults) over 95 days. Frogs exposed to Bd as recently metamorphosed juveniles acquired higher infection loads and experienced lower immune function and lower survivorship than subadults and adults, indicating an ontogenetic decline in chytridiomycosis susceptibility. By corresponding with an intrinsic developmental maturation in immunocompetence seen in uninfected frogs, we suggest these developmental changes in host susceptibility in L. aurea may be immune mediated. Consequently, the physiological relationship between ontogeny and immunity may affect host population structure and demography through variation in life stage survival, and understanding this can shape management targets for effective amphibian conservation.

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Acknowledgments

We would like to thank John Gould and Lachlan Campbell for animal husbandry assistance, James Garnham and Carla Pollard for qPCR assistance, and Kim Colyvas for statistical advice. This study was funded by ARC Linkage grant LP0989459 (industry partners—Australian Research Council, Sydney Olympic Park Authority, Strathfield Council, South Australian Museum, NSW Roads and Traffic Authority, NSW Department of Environment and Climate Change). The authors declare that they have no conflict of interest. All applicable institutional and/or national guidelines for the care and use of animals were followed, with approvals granted by the University of Newcastle Animal Care and Ethics Committee (A-2008-165) and NSW National Parks scientific licence (SL100190).

Author contribution statement

M. M. and J. C. obtained the funding; A. A. and M. S. performed the laboratory work; D. B. and S. C. provided the training and logistical support; all the authors contributed significantly to the experimental design; and A. A. wrote the manuscript.

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  1. School of Environmental and Life Science, University of Newcastle, Callaghan, NSW, 2300, Australia

    Amalina Abu Bakar, Deborah S. Bower, Michelle P. Stockwell, Simon Clulow, John Clulow & Michael J. Mahony

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  1. Amalina Abu Bakar
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  2. Deborah S. Bower
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  3. Michelle P. Stockwell
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  4. Simon Clulow
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Correspondence to Amalina Abu Bakar.

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Communicated by Raoul Van Damme.

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Abu Bakar, A., Bower, D.S., Stockwell, M.P. et al. Susceptibility to disease varies with ontogeny and immunocompetence in a threatened amphibian. Oecologia 181, 997–1009 (2016). https://doi.org/10.1007/s00442-016-3607-4

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