The effective detection of both prey and predators is pivotal for the survival of mesopredators. However, the condition of being a mesopredator is strongly context dependent. Here we focus on two aquatic caudate species that have colonised caves: the Pyrenean newt (Calotriton asper) and the olm (Proteus anguinus). The former maintains both surface and subterranean populations, while only cave-adapted populations of the latter exist. Both species are apex predators in underground waterbodies, while the Pyrenean newt is a mesopredator in surface waterbodies. Shifting to a higher level of the trophic web through colonising caves may promote the loss of anti-predator response against surface apex predators, and an increase in the ability to detect prey. To test these two non-exclusive hypotheses, we integrated classical behavioural characterisations with a novel approach: the assessment of lateralisation (i.e. preference for one body side exposure). Behavioural experiments were performed using laboratory-reared individuals. We performed 684 trials on 39 Pyrenean newts and eight olms. Under darkness and light conditions, we tested how exposure to different chemical cues (predatory fish, prey and unknown scent) affected individuals’ activity and lateralisation. Both cave and surface Pyrenean newts responded to predator cues, while olms did not. In Pyrenean newts, predator cues reduced the time spent in movement and time spent in lateralisation associated with hunting. Our results show that predator recognition is maintained in a species where recently separated populations inhabit environments lacking of higher predators, while such behaviour tends to be lost in populations with longer history of adaptation. Predator recognition can be maintained in animals adapted to predator free habitats, but varies with their history of adaptation. Species that are not at the apex of the food web can become top predators if they colonise subterranean environments. We compared the behavioural responses of the olm, a strictly cave species with a long underground evolutionary history, and of the Pyrenean newt, a facultative cave species that also has stream-dwelling populations. Moreover, we integrated a classical behavioural characterisation, such as movement detection, with a novel approach: the assessment of lateralisation. While olms do not respond to external predators scent, cave-dwelling newts still recognise it. This clearly indicates that predator recognition is still maintained in species that have colonised predator-free environments more recently.

中文翻译：

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从中掠食者转变为顶级捕食者：适应洞穴生活的两栖动物的反应有何不同？

对猎物和捕食者的有效探测对于食肉动物的生存至关重要。然而，成为 mesopredator 的条件强烈依赖于上下文。在这里，我们专注于在洞穴中定居的两种水生尾状体物种：比利牛斯蝾螈（Calotriton asper）和蝾螈（Proteus anguinus）。前者维持地表和地下种群，而后者只有适应洞穴的种群存在。这两个物种都是地下水体中的顶级捕食者，而比利牛斯蝾螈是地表水体中的中掠食者。通过殖民洞穴转移到更高层次的营养网可能会促进对表面顶级捕食者的反捕食者反应的丧失，并增加探测猎物的能力。为了检验这两个非排他性假设，我们将经典的行为特征与一种新颖的方法相结合：侧化评估（即偏向于身体一侧的暴露）。使用实验室饲养的个体进行行为实验。我们对 39 条比利牛斯蝾螈和 8 条蝾螈进行了 684 次试验。在黑暗和光照条件下，我们测试了接触不同化学线索（掠食性鱼类、猎物和未知气味）如何影响个体的活动和偏侧化。洞穴蝾螈和地表比利牛斯蝾螈都会对捕食者的线索做出反应，而奥尔姆斯则没有。在比利牛斯蝾螈中，捕食者的线索减少了与狩猎相关的运动时间和侧向化时间。我们的结果表明，在最近分离的种群居住在缺乏高级捕食者的环境中的物种中，捕食者识别得以维持，而这种行为往往在适应历史较长的人群中消失。捕食者识别可以在适应无捕食者栖息地的动物中保持，但随着它们的适应历史而变化。不在食物网顶端的物种如果在地下环境中定居，就可能成为顶级捕食者。我们比较了 olm（一种具有悠久地下进化历史的严格洞穴物种）和比利牛斯蝾螈（一种也有溪流栖息种群的兼性洞穴物种）的行为反应。此外，我们将经典的行为特征（例如运动检测）与一种新颖的方法相结合：侧化评估。虽然 olms 对外部捕食者的气味没有反应，但穴居蝾螈仍然能识别它。