Emerging infectious diseases are responsible for declines in wildlife populations around the globe. Mass mortality events associated with emerging infectious diseases are often associated with high number of infected individuals (prevalence) and high pathogen loads within individuals (intensity). At the landscape scale spatial and temporal variation in environmental conditions can alter the relationship between these infection parameters and blur the overall picture of disease dynamics. Quantitative estimates of how infection parameters covary with environmental heterogeneity at the landscape scale are scarce. Predicting rates of pathogen transmission and identifying wild populations at risk of disease epidemics requires that we elucidate the factors that shape, and potentially decouple, the link between pathogen prevalence and intensity of infection over complex ecological landscapes. Using a network of 41 populations of the amphibian host Rana pipiens in Ontario, Canada, we present the spatial and temporal heterogeneity in pathogen prevalence and intensity of infection of the chytrid fungus Batrachochytrium dendrobatidis (Bd), across a 3-year period. We then quantify how covariation between both infection parameters measured during late summer, are modified by previously experienced spatiotemporal environmental heterogeneity across 14 repeat sampled populations. Late summer Bd infection parameters are governed, at least in part, by different environmental factors operating during separate host life history events. Our results provide evidence for a relationship between Bd prevalence and thermal regimes prior to host breeding at the site level, and a relationship between intensity of infection and aquatic conditions (precipitation, hydroshed size and river density) throughout host breeding period at the site level. This demonstrates that microclimatic variation within temporal windows, can drive divergent patterns of pathogen dynamics within and across years, by effecting changes in host behaviour which interfere with the pathogen's ability to infect and re-infect hosts. A clearer understanding of the role that spatiotemporal heterogeneity has upon infection parameters will provide valuable insights into host-pathogen epidemiology, as well as more fundamental aspects of the ecology and evolution of interspecific interactions.

中文翻译：

---

时空异质性使两栖类壶菌病的感染参数解耦

新出现的传染病是全球野生动物种群减少的原因。与新发传染病相关的大规模死亡事件通常与大量感染个体（流行率）和个体内高病原体载量（强度）有关。在景观尺度上，环境条件的空间和时间变化可以改变这些感染参数之间的关系，并模糊疾病动态的整体图景。关于感染参数如何与景观尺度的环境异质性共变的定量估计很少。预测病原体传播率和识别有疾病流行风险的野生种群需要我们阐明形成和潜在脱钩的因素，复杂生态景观中病原体流行与感染强度之间的联系。使用加拿大安大略省 41 个两栖动物寄主 Rana pipiens 的网络，我们展示了 3 年间壶菌属真菌 Batrachochytrium dendrobatidis (Bd) 的病原体流行率和感染强度的时空异质性。然后，我们量化了夏末测量的两种感染参数之间的协变如何被先前经历的 14 个重复采样种群的时空环境异质性所修改。夏末 Bd 感染参数至少部分受不同宿主生活史事件中不同环境因素的控制。我们的研究结果提供了证据，证明了在场地水平的寄主繁殖之前 Bd 流行率与热状况之间的关系，以及在场地水平的整个寄主繁殖期间感染强度与水生条件（降水、分水岭大小和河流密度）之间的关系。这表明，时间窗口内的小气候变化可以通过影响宿主行为的变化，从而干扰病原体感染和重新感染宿主的能力，从而在年内和跨年内驱动病原体动态的不同模式。更清楚地了解时空异质性对感染参数的作用，将为宿主 - 病原体流行病学以及生态学和种间相互作用进化的更基本方面提供有价值的见解。感染强度和水生条件（降水、分水岭大小和河流密度）之间的关系在整个寄主繁殖期间现场水平。这表明，时间窗口内的小气候变化可以通过影响宿主行为的变化，从而干扰病原体感染和重新感染宿主的能力，从而在年内和跨年内驱动病原体动态的不同模式。更清楚地了解时空异质性对感染参数的作用，将为宿主 - 病原体流行病学以及生态学和种间相互作用进化的更基本方面提供有价值的见解。感染强度和水生条件（降水、分水岭大小和河流密度）之间的关系在整个寄主繁殖期间现场水平。这表明，时间窗口内的小气候变化可以通过影响宿主行为的变化，从而干扰病原体感染和重新感染宿主的能力，从而在年内和跨年内驱动病原体动态的不同模式。更清楚地了解时空异质性对感染参数的作用，将为宿主 - 病原体流行病学以及生态学和种间相互作用进化的更基本方面提供有价值的见解。这表明，时间窗口内的小气候变化可以通过影响宿主行为的变化，从而干扰病原体感染和重新感染宿主的能力，从而在年内和跨年内驱动病原体动态的不同模式。更清楚地了解时空异质性对感染参数的作用，将为宿主-病原体流行病学以及生态学和种间相互作用进化的更基本方面提供有价值的见解。这表明，时间窗口内的小气候变化可以通过影响宿主行为的变化，从而干扰病原体感染和重新感染宿主的能力，从而在年内和跨年内驱动病原体动态的不同模式。更清楚地了解时空异质性对感染参数的作用，将为宿主 - 病原体流行病学以及生态学和种间相互作用进化的更基本方面提供有价值的见解。