Ecology, Evolution and Marine Biology, University of California, Santa Barbara, Santa Barbara, CA, USA.
Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA.
J Anim Ecol. 2020 Dec;89(12):2876-2887. doi: 10.1111/1365-2656.13343. Epub 2020 Sep 28.
World-wide, infectious diseases represent a major source of mortality in humans and livestock. For wildlife populations, disease-induced mortality is likely even greater, but remains notoriously difficult to estimate-especially for endemic infections. Approaches for quantifying wildlife mortality due to endemic infections have historically been limited by an inability to directly observe wildlife mortality in nature. Here we address a question that can rarely be answered for endemic pathogens of wildlife: what are the population- and landscape-level effects of infection on host mortality? We combined laboratory experiments, extensive field data and novel mathematical models to indirectly estimate the magnitude of mortality induced by an endemic, virulent trematode parasite (Ribeiroia ondatrae) on hundreds of amphibian populations spanning four native species. We developed a flexible statistical model that uses patterns of aggregation in parasite abundance to infer host mortality. Our model improves on previous approaches for inferring host mortality from parasite abundance data by (i) relaxing restrictive assumptions on the timing of host mortality and sampling, (ii) placing all mortality inference within a Bayesian framework to better quantify uncertainty and (iii) accommodating data from laboratory experiments and field sampling to allow for estimates and comparisons of mortality within and among host populations. Applying our approach to 301 amphibian populations, we found that trematode infection was associated with an average of between 13% and 40% population-level mortality. For three of the four amphibian species, our models predicted that some populations experienced >90% mortality due to infection, leading to mortality of thousands of amphibian larvae within a pond. At the landscape scale, the total number of amphibians predicted to succumb to infection was driven by a few high mortality sites, with fewer than 20% of sites contributing to greater than 80% of amphibian mortality on the landscape. The mortality estimates in this study provide a rare glimpse into the magnitude of effects that endemic parasites can have on wildlife populations and our theoretical framework for indirectly inferring parasite-induced mortality can be applied to other host-parasite systems to help reveal the hidden death toll of pathogens on wildlife hosts.
在全球范围内，传染病是人类和家畜死亡的主要原因。对于野生动物种群来说，疾病导致的死亡率可能更高，但由于地方性感染，这种死亡率很难估计——这是出了名的。评估由于地方性感染导致的野生动物死亡率的方法在历史上受到限制，因为无法直接在自然界中观察野生动物的死亡率。在这里，我们解决了一个对于野生动物的地方性病原体很少能回答的问题：感染对宿主死亡率的种群和景观水平的影响是什么？我们结合实验室实验、广泛的野外数据和新颖的数学模型，间接估计了一种地方性、高毒力的吸虫寄生虫（Ribeiroia ondatrae）对跨越四个本地物种的数百个两栖动物种群的宿主死亡率的影响。我们开发了一种灵活的统计模型，该模型利用寄生虫丰度的聚集模式来推断宿主死亡率。我们的模型通过（i）放宽对宿主死亡和采样时间的限制性假设，（ii）将所有死亡率推断置于贝叶斯框架内，以更好地量化不确定性，以及（iii）容纳实验室实验和野外采样的数据，从而允许在宿主种群内和种群间进行死亡率的估计和比较，从而改进了从寄生虫丰度数据推断宿主死亡率的先前方法。我们将该方法应用于 301 个两栖动物种群，发现吸虫感染与平均 13%至 40%的种群水平死亡率有关。对于四个两栖物种中的三个，我们的模型预测，一些种群由于感染而经历了超过 90%的死亡率，导致池塘内数千只两栖幼虫死亡。在景观尺度上，预测由于感染而屈服的两栖动物总数是由少数高死亡率地点驱动的，不到 20%的地点对景观上超过 80%的两栖动物死亡率有贡献。本研究中的死亡率估计值提供了一个罕见的视角，了解地方性寄生虫对野生动物种群的影响程度，我们用于间接推断寄生虫引起的死亡率的理论框架可应用于其他宿主-寄生虫系统，以帮助揭示病原体对野生动物宿主的隐性死亡人数。
