Abstract

Understanding how pathogens respond to changing environmental conditions is a central challenge in disease ecology. The environmentally sensitive fungal pathogen Batrachochytrium dendrobatidis (Bd), which causes the amphibian disease chytridiomycosis, has spread globally causing amphibian extirpations in a wide variety of climatic regions. To gain an in-depth understanding of Bd's responses to temperature, we used an integrative approach, combining empirical laboratory experiments with mathematical modeling. First, we selected a single Bd isolate and serially propagated two lineages of the isolate for multiple generations in two stable thermal conditions: 4°C (cold-adapted lineage) and 23°C (warm-adapted lineage). We quantified the production of infectious zoospores (fecundity), the timing of zoospore release, and zoospore activity in reciprocal temperature transplant experiments in which both Bd lineages were grown in either high or low temperature conditions. We then developed population growth models for the Bd lineages under each set of temperature conditions. We found that Bd had lower population growth rates, but longer periods of zoospore activity in the low temperature treatment (4°C) compared to the high temperature treatment (23°C). This effect was more pronounced in Bd lineages that were propagated in the low temperature treatment (4°C), suggesting a shift in Bd's response to low temperature conditions. Our results provide novel insights into the mechanisms by which Bd can thrive in a wide variety of temperature conditions, potentially altering the dynamics of chytridiomycosis and thus, the propensity for Bd to cause amphibian population collapse. We also suggest that the adaptive responses of Bd to thermal conditions warrant further investigation, especially in the face of global climate change.

Highlights

  • In many disease systems, the manifestations of disease exhibit patterns that can be attributed to changes in environmental factors, such as temperature (Altizer et al 2006)

  • We were interested in temperature-mediated shifts in the Batrachochytrium dendrobatidis (Bd) reproductive life cycle because the density of Bd on an amphibian host is associated with the development of lethal chytridiomycosis (Voyles et al 2009; Vredenburg et al 2010)

  • We found that Bd had lower population growth rates, but longer periods of zoospore activity, in the low temperature treatment (4°C) compared to the high temperature treatment (23°C)

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Summary

Introduction

The manifestations of disease (e.g., morbidity and mortality) exhibit patterns that can be attributed to changes in environmental factors, such as temperature (Altizer et al 2006). Pathogen Responses to Temperature Treatments understanding disease dynamics. This is true in disease systems where environmental temperatures have strong effects on pathogen abundance, distribution, and life history patterns (Harvell et al 2002; Lafferty 2009). One such disease is chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd). Genetic studies suggest that Bd is a recently emerged pathogen that has spread around the world rapidly (James et al 2009; Farrer et al 2011), on all continents where amphibians occur

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