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Disease and thermal acclimation in a more variable and unpredictable climate

Abstract

Global climate change is shifting the distribution of infectious diseases of humans and wildlife with potential adverse consequences for disease control1,2,3,4. As well as increasing mean temperatures, climate change is expected to increase climate variability5,6, making climate less predictable. However, few empirical or theoretical studies have considered the effects of climate variability or predictability on disease, despite it being likely that hosts and parasites will have differential responses to climatic shifts6,7. Here we present a theoretical framework for how temperature variation and its predictability influence disease risk by affecting host and parasite acclimation responses. Laboratory experiments conducted in 80 independent incubators, and field data on disease-associated frog declines in Latin America6, support the framework and provide evidence that unpredictable temperature fluctuations, on both monthly and diurnal timescales, decrease frog resistance to the pathogenic chytrid fungus Batrachochytrium dendrobatidis. Furthermore, the pattern of temperature-dependent growth of the fungus on frogs was opposite to the pattern of growth in culture, emphasizing the importance of accounting for the host–parasite interaction when predicting climate-dependent disease dynamics. If similar acclimation responses influence other host–parasite systems, as seems likely, then present models, which generally ignore small-scale temporal variability in climate7, might provide poor predictions for climate effects on disease.

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Figure 1: Graphical representation of the temperature variability hypothesis.
Figure 2: Evidence for increased susceptibility to infection following a shift in temperature.
Figure 3: Effects of random and diurnal temperature variation on B. dendrobatidis growth and frog mortality in the diurnal temperature experiment.

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Acknowledgements

Thanks to A. Blaustein, P. Hudson and members of the Rohr lab for thoughts on this paper, M. McGarrity for assisting with frog collections, V. Vasquez for providing the B. dendrobatidis isolate, M. McCoy for suggesting zero-inflated negative binomial regression, C. Steffan for technical assistance and undergraduate assistants for assisting with experiments: J. Guirguis, L. Garibova, C. Hall, D. Marante, L. Caicedo, D. Bradberry, M. Chawdry, C. Kobasa, J. Hudson, P. Michel, J. Heet, A. Makhijani, L. Domaradzki, S. Agaj, H. Dorling, E. Esterrich, J. Waldman, D. Litowchak, M. Derakhshan, R. Rai, A. Drennen, T. Pham, P. Michel, D. Litowchak, A. Congelosi, N. Donn, M. Mancao and E. Sites. Financial support came from the National Science Foundation (NSF; DEB-0809487) and US Department of Agriculture (NRI 2008-00622 and 2008-01785) grants to J.R.R., a US Environmental Protection Agency STAR (R83-3835) grant to J.R.R. and T.R.R, an EPA CAREER (no. 83518801) grant to J.R.R. and a NSF grant to T.R.R. and P. T. Johnson (IOS-1121529). This work has not been subjected to review by these agencies providing financial support and therefore does not necessarily reflect the views of, or official endorsement by, these agencies.

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T.R.R. and J.R.R. should be considered joint first authors of this work. T.R.R. conducted mathematical modelling and statistical analyses. T.R.R. and J.R.R. conceived the experiments and obtained financial support. J.R.R. compiled field data. All authors assisted with writing the manuscript and with design and execution of the experiments.

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Correspondence to Thomas R. Raffel.

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Raffel, T., Romansic, J., Halstead, N. et al. Disease and thermal acclimation in a more variable and unpredictable climate. Nature Clim Change 3, 146–151 (2013). https://doi.org/10.1038/nclimate1659

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