Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, Boulder, CO, USA.
J Anim Ecol. 2022 Jan;91(1):35-45. doi: 10.1111/1365-2656.13591. Epub 2021 Sep 24.
Predation on parasites is a common interaction with multiple, concurrent outcomes. Free-living stages of parasites can comprise a large portion of some predators' diets and may be important resources for population growth. Predation can also reduce the density of infectious agents in an ecosystem, with resultant decreases in infection rates. While predator-parasite interactions likely vary with parasite transmission strategy, few studies have examined how variation in transmission mode influences contact rates with predators and the associated changes in consumption risk. To understand how transmission mode mediates predator-parasite interactions, we examined associations between an oligochaete predator Chaetogaster limnaei that lives commensally on freshwater snails and nine trematode taxa that infect snails. Chaetogaster is hypothesized to consume active (i.e. mobile), free-living stages of trematodes that infect snails (miracidia), but not the passive infectious stages (eggs); it could thus differentially affect transmission and infection prevalence of parasites, including those with medical or veterinary importance. Alternatively, when infection does occur, Chaetogaster can consume and respond numerically to free-living trematode stages released from infected snails (cercariae). These two processes lead to contrasting predictions about whether Chaetogaster and trematode infection of snails correlate negatively ('protective predation') or positively ('predator augmentation'). Here, we tested how parasite transmission mode affected Chaetogaster-trematode relationships using data from 20,759 snails collected across 4 years from natural ponds in California. Based on generalized linear mixed modelling, snails with more Chaetogaster were less likely to be infected by trematodes that rely on active transmission. Conversely, infections by trematodes with passive infectious stages were positively associated with per-snail Chaetogaster abundance. Our results suggest that trematode transmission mode mediates the net outcome of predation on parasites. For trematodes with active infectious stages, predatory Chaetogaster limited the risk of snail infection and its subsequent pathology (i.e. castration). For taxa with passive infectious stages, no such protective effect was observed. Rather, infected snails were associated with higher Chaetogaster abundance, likely owing to the resource subsidy provided by cercariae. These findings highlight the ecological and epidemiological importance of predation on free-living stages while underscoring the influence of parasite life history in shaping such interactions.
捕食寄生虫是一种常见的相互作用，具有多种并发结果。寄生虫的自由生活阶段可能构成某些捕食者饮食的很大一部分，并且可能是种群增长的重要资源。捕食还可以降低生态系统中感染因子的密度，从而降低感染率。虽然捕食者-寄生虫相互作用可能因寄生虫传播策略而异，但很少有研究检查传播模式的变化如何影响与捕食者的接触率以及相关的消耗风险变化。为了了解传播模式如何介导捕食者-寄生虫相互作用，我们研究了生活在淡水蜗牛上的寡毛纲捕食者 Chaetogaster limnaei 与感染蜗牛的九种吸虫类寄生虫之间的关联。推测 Chaetogaster 会消耗感染蜗牛的活动（即移动）自由生活阶段的吸虫（尾蚴），而不会消耗被动感染阶段（卵）；因此，它可以对包括具有医学或兽医学重要性的寄生虫的传播和感染流行率产生不同的影响。或者，当感染确实发生时，Chaetogaster 可以从受感染的蜗牛中消耗并在数量上响应释放的自由生活的吸虫阶段（尾蚴）。这两个过程导致了关于 Chaetogaster 和蜗牛感染吸虫是否呈负相关（“保护性捕食”）或正相关（“捕食者增强”）的相反预测。在这里，我们使用来自加利福尼亚州自然池塘的 4 年时间内收集的 20,759 只蜗牛的数据，测试了寄生虫传播模式如何影响 Chaetogaster-吸虫关系。基于广义线性混合模型，带有更多 Chaetogaster 的蜗牛不太可能被依赖主动传播的吸虫感染。相反，具有被动感染阶段的吸虫感染与每只蜗牛的 Chaetogaster 丰度呈正相关。我们的结果表明，吸虫传播模式介导了捕食寄生虫的净结果。对于具有主动感染阶段的吸虫，捕食性 Chaetogaster 限制了蜗牛感染及其随后的病理学（即去势）的风险。对于具有被动感染阶段的分类单元，没有观察到这种保护作用。相反，受感染的蜗牛与更高的 Chaetogaster 丰度相关，这可能是由于尾蚴提供的资源补贴。这些发现强调了捕食自由生活阶段的生态和流行病学重要性，同时强调了寄生虫生活史在塑造这种相互作用中的影响。
