Abstract In the predator–prey arms race, survival-enhancing adaptive behaviors are essential. Prey can perceive predator presence directly from visual, auditory, or chemical cues. Non-lethal encounters with a predator may trigger prey to produce special body odors, alarm pheromones, informing conspecifics about predation risks. Recent studies suggest that parental exposure to predation risk during reproduction affects offspring behavior cross-generationally. We compared behaviors of bank vole ( Myodes glareolus ) pups produced by parents exposed to one of three treatments: predator scent from the least weasel ( Mustela nivalis nivalis ); scent from weasel-exposed voles, i.e., alarm pheromones; or a control treatment without added scents. Parents were treated in semi-natural field enclosures, but pups were born in the lab and assayed in an open-field arena. Before each behavioral test, one of the three scent treatments was spread throughout the test arena. The tests followed a full factorial design (3 parental treatments × 3 area treatments). Regardless of the parents’ treatment, pups exposed to predator odor in the arena moved more. Additionally, pups spend more time in the center of the arena when presented with predator odor or alarm pheromone compared with the control. Pups from predator odor–exposed parents avoided the center of the arena under control conditions, but they spent more time in the center when either predator odor or alarm pheromone was present. Our experiment shows that cross-generational effects are context-sensitive, depending on the perceived risk. Future studies should examine cross-generational behavioral effects in ecologically meaningful environments instead of only neutral ones. Significance statement We exposed bank voles to odors signaling predation risk to assess the effects parental predation exposure on the behavior of their offspring. Besides predator odor, we also assessed the role of a conspecific alarm cue as a novel way of spreading the predation risk information. Pup behaviors were assessed in the open-field arena, a standard way of assessing animal behavior in a wide range of contexts. We found that also alarm pheromone increased the time pups spend in the center of the arena similarly to predator odor. While previous studies suggested that offspring would be more fearful, our results indicate that the cross-generational effects are very context-dependent; i.e., they differ significantly depending on which scent cue is presented in the open-field arena. This shows the need for better tools or measurements to translate laboratory results into ecologically meaningful frameworks.

中文翻译：

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对银行田鼠幼崽捕食风险的子宫内行为印记

摘要 在捕食者-猎物军备竞赛中，增强生存的适应性行为是必不可少的。猎物可以直接从视觉、听觉或化学线索中感知捕食者的存在。与捕食者的非致命遭遇可能会触发猎物产生特殊的体味，警报信息素，告知同类捕食风险。最近的研究表明，父母在繁殖过程中暴露于捕食风险会影响后代的跨代行为。我们比较了暴露于以下三种处理之一的银行田鼠 (Myodes glareolus) 幼崽的行为： 来自最少鼬鼠 (Mustela nivalis nivalis) 的捕食者气味；暴露于黄鼠狼的田鼠的气味，即警报信息素；或不添加香味的对照处理。父母在半自然的田间围栏中接受治疗，但幼崽是在实验室出生的，并在露天场地进行分析。在每次行为测试之前，将三种气味处理中的一种散布在整个测试区域。测试遵循全因子设计（3 个亲本处理 × 3 个区域处理）。无论父母如何对待，在竞技场中暴露于捕食者气味的幼​​崽都会动得更多。此外，与对照组相比，当幼犬出现捕食者气味或警报信息素时，它们会在竞技场中心花费更多时间。在控制条件下，暴露于捕食者气味的父母的幼崽避开了竞技场的中心，但当存在捕食者气味或警报信息素时，它们会在中心呆更多的时间。我们的实验表明，跨代影响是上下文敏感的，取决于感知的风险。未来的研究应该检查具有生态意义的环境中的跨代行为影响，而不仅仅是中性环境。意义声明 我们将田鼠暴露于表明捕食风险的气味中，以评估父母捕食暴露对其后代行为的影响。除了捕食者的气味，我们还评估了同种警报线索作为传播捕食风险信息的新方法的作用。幼犬的行为是在开阔场地进行评估的，这是在各种环境中评估动物行为的标准方法。我们发现警报信息素也增加了幼崽在竞技场中心停留的时间，类似于捕食者的气味。虽然之前的研究表明后代会更害怕，但我们的结果表明，跨代影响非常依赖于环境；IE，它们的显着差异取决于在露天竞技场中呈现的气味提示。这表明需要更好的工具或测量来将实验室结果转化为具有生态意义的框架。