How Enemies Shape Communication Systems: Sensory Strategies of Prey to Avoid Eavesdropping Predators and Parasites

Due to human perceptional bias in favor of air-borne sounds, substrate-borne vibrational signaling has been traditionally regarded as a highly specialized, inherently short-range and, consequently, a private communication channel, free from eavesdropping by sexual competitors and predators. In this review, we synthesize current knowledge pertinent to the view that most animals live in a rich vibratory world, where vibrational information is available to unintended receivers. In recent years, we realized that vibrational signaling is one of the oldest and taxonomically most widespread forms of communication by mechanical waves and that receptors detecting substrate vibrations are ubiquitous. In nature, substrate vibrations are reliable source of information readily available to all members of the animal community able to detect them. Viewing vibrational communication in more relevant ecological context reveals that animals relying on substrate vibrations live in complex communication networks. Long evolutionary history of this communication channel is reflected in varied and sophisticated predator-prey interactions guided by substrate-borne vibrations. Eavesdropping and exploitation of vibrational signals used in sexual communication have been so far largely neglected; however, existing studies show that generalist arthropod predators can intercept such signals emitted by insects to obtain information about prey availability and use that information when making foraging decisions. Moreover, males which advertise themselves for longer periods than females and with vibrational signals of higher amplitude face higher predation risk. It is likely that eavesdropping and exploitation of vibrational signals are major drivers in the evolution taking place in the vibratory world and we believe that studies of interspecific interactions guided by substrate vibrations will, in the future, offer numerous opportunities to unravel mechanisms that are central to understanding behavior in general.

The field of predator eavesdropping concentrates on the detection by a predator or parasite of signals that prey direct at conspecifics, and the subsequent evolution by prey to avoid or lessen such detection. Here, we first point out that signaling prey species are often found in mixed-species moving groups or stationary aggregations, and ask the question of how simultaneous signaling, by members of one species or more, might affect predator eavesdropping behavior and the composition of the groups themselves. The detection risk of prey species will be affected by the other species they associate with, and prey should generally avoid joining a group with more detectable species. Yet prey may select to join other species that are preferred by predators, diluting their own risk of attack, as long as that does not lead to substantially greater detection and thereby increased predation. We next review the evidence that prey grouping and collective responses when attacked can confuse predators, leading to lower capture rates. Evidence for this confusion effect mostly involves visually orienting predators. We then ask if a similar phenomenon could occur when animals in a group simultaneously produce acoustic signals and find relevant evidence for predator confusion under such situations in the literature associated with the “cocktail party effect.” As confusion is heightened by similarities among mixed-species group members, this provides a force at ecological or evolutionary timescales to make species that associate in groups, and their signals, more similar to each other. However, heterogeneous mixed-species groups may be favored if species are differentially preferred as prey. We suggest experiments to examine whether the success rates of acoustically orienting predators depend on the group size of their mixed-species prey. More observations on the relative positions of conspecifics and heterospecifics in space, and the temporal association of their signals, will also increase our understanding of the relationship between mixed-species grouping and predator eavesdropping.