Department of Biology, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.
Marine Biology and Aquaculture & ARC Centre of Excellence for Coral Reef Studies, James Cook University, Qld, Australia.
J Anim Ecol. 2019 Sep;88(9):1281-1290. doi: 10.1111/1365-2656.12986. Epub 2019 Apr 17.
Animal signalling systems outside the realm of human perception remain largely understudied. These systems consist of four main components: a signalling context, a voluntary signal, receiver responses and resulting fitness benefits to both the signaller and receiver(s). It is often most difficult to determine incidental cues from voluntary signals. One example is chemical disturbance cues released by aquatic prey during predator encounters that may serve to alert conspecifics of nearby risk and initiate tighter shoaling. We aimed to test whether disturbance cues are released incidentally (i.e. as a cue) or are produced voluntarily depending on a specific signalling context such as the audience surrounding the individual, and thus constitute a signal. We hypothesized that if receivers use disturbance cues to communicate risk among themselves, they would produce more (or more potent) disturbance cues when present in a group of conspecifics rather than when they are isolated (presence/absence of an audience) and use disturbance cues more when present alongside familiar rather than unfamiliar conspecifics (audience composition effect). We placed fathead minnows (Pimephales promelas) in groups with familiar fish, unfamiliar fish or as isolated individuals with no audience present, and then simulated a predator chase to evoke disturbance cues. We used bioassays with independent receivers to assess whether the disturbance cues produced differed depending on the signallers' audience. We found evidence of voluntary signalling, as minnows responded to disturbance cues from groups of fish with tighter shoaling while disturbance cues from isolated minnows did not evoke a significant shoaling response (presence/absence audience effect). Receivers also increased shoaling, freezing and dashing more in response to disturbance cues from familiar groups compared to disturbance cues from unfamiliar groups or isolated minnows (audience composition effect). Together, these findings support our hypothesis that disturbance cues are used as an antipredator signal to initiate coordinated group defences among familiar conspecifics involving shoaling, freezing and dashing. This study represents the strongest evidence to date that chemicals released by aquatic prey upon disturbance by predators serve as voluntary signals rather than simply cues that prey have evolved to detect when assessing their risk of predation.
动物在人类感知范围之外的信号系统在很大程度上仍未得到充分研究。这些系统由四个主要组成部分组成：信号环境、自愿信号、接收者的反应以及信号发送者和接收者（多个）的适应度收益。通常，从自愿信号中确定偶然线索是最困难的。一个例子是水生猎物在遇到捕食者时释放的化学干扰线索，这些线索可能用于警告附近的同类存在风险，并促使它们更紧密地聚集在一起。我们旨在测试干扰线索是否是偶然释放的（即作为线索），还是根据特定的信号环境（例如个体周围的观众）自愿产生的，从而构成信号。我们假设，如果接收者使用干扰线索在彼此之间传达风险，那么当它们处于同类群体中时，它们会产生更多（或更有效）的干扰线索，而不是当它们孤立无援时（有/无观众），并且当它们与熟悉的而不是陌生的同类在一起时，它们会更多地使用干扰线索（观众组成效应）。我们将胖头鱼（Pimephales promelas）放在有熟悉鱼类、陌生鱼类的群体中或没有观众的孤立个体中，然后模拟捕食者追逐以引发干扰线索。我们使用独立接收者的生物测定法来评估产生的干扰线索是否因信号发送者的观众而异。我们发现了自愿信号的证据，因为胖头鱼对来自鱼类群体的干扰线索做出了更紧密的聚集反应，而来自孤立的胖头鱼的干扰线索并没有引起明显的聚集反应（有/无观众效应）。与来自陌生鱼类群体或孤立的胖头鱼的干扰线索相比，接收者对来自熟悉鱼类群体的干扰线索做出了更多的聚集、冻结和冲刺反应（观众组成效应）。总的来说，这些发现支持了我们的假设，即干扰线索被用作一种抗捕食者信号，以在熟悉的同类中启动协调一致的群体防御，包括聚集、冻结和冲刺。这项研究代表了迄今为止最强有力的证据，表明水生猎物在受到捕食者干扰时释放的化学物质是自愿信号，而不仅仅是猎物在评估捕食风险时进化出来的线索。
