ABSTRACT
Ground squirrels (Spermophilus spp.) have evolved a battery of defences against the rattlesnakes (Crotalus spp.) that have preyed on them for millions of years. The distinctive behavioural reactions by these squirrels to rattlesnakes have recently been shown to include self-application of rattlesnake scent-squirrels apply scent by vigorously licking their fur after chewing on shed rattlesnake skins. Here, we present evidence that this behaviour is a novel antipredator defence founded on exploitation of a foreign scent. We tested three functional hypotheses for snake scent application--antipredator, conspecific deterrence and ectoparasite defence--by examining reactions to rattlesnake scent by rattlesnakes, ground squirrels and ectoparasites (fleas). Rattlesnakes were more attracted to ground squirrel scent than to ground squirrel scent mixed with rattlesnake scent or rattlesnake scent alone. However, ground squirrel behaviour and flea host choice were not affected by rattlesnake scent. Thus, ground squirrels can reduce the risk of rattlesnake predation by applying rattlesnake scent to their bodies, potentially as a form of olfactory camouflage. Opportunistic exploitation of heterospecific scents may be widespread; many species self-apply foreign odours, but few such cases have been demonstrated to serve in antipredator defence.
Subject(s)
Crotalus/physiology , Odorants , Predatory Behavior/physiology , Sciuridae/physiology , Adaptation, Physiological , Animal Communication , Animals , Ectoparasitic Infestations/parasitology , Female , Male , Rodent Diseases , Siphonaptera/physiologyABSTRACT
Animal communication involves very dynamic processes that can generate new uses and functions for established communicative activities. In this article, the authors describe how an aposematic signal, the rattling sound of rattlesnakes (Crotalus viridis), has been exploited by 2 ecological associates of rattlesnakes: (a) California ground squirrels (Spermophilus beecheyi) use incidental acoustic cues in rattling sounds to assess the danger posed by the rattling snake, and (b) burrowing owls (Athene cunicularia) defend themselves against mammalian predators by mimicking the sound of rattling. The remarkable similarity between the burrowing owl's defensive hiss and the rattlesnake's rattling reflects both exaptation and adaptation. Such exploitation of the rattling sound has favored alternations in both the structure and the deployment of rattling by rattlesnakes.
Subject(s)
Animal Communication , Crotalus , Environment , Imitative Behavior , Sciuridae , Strigiformes , Vocalization, Animal , Animals , Biological Evolution , Fear , Female , Male , Sound SpectrographyABSTRACT
The evolution of communicative signals involves a major hurdle; signals need to effectively stimulate the sensory systems of their targets. Therefore, sensory specializations of target animals are important sources of selection on signal structure. Here we report the discovery of an animal signal that uses a previously unknown communicative modality, infrared radiation or "radiant heat," which capitalizes on the infrared sensory capabilities of the signal's target. California ground squirrels (Spermophilus beecheyi) add an infrared component to their snake-directed tail-flagging signals when confronting infrared-sensitive rattlesnakes (Crotalus oreganus), but tail flag without augmenting infrared emission when confronting infrared-insensitive gopher snakes (Pituophis melanoleucus). Experimental playbacks with a biorobotic squirrel model reveal this signal's communicative function. When the infrared component was added to the tail flagging display of the robotic models, rattlesnakes exhibited a greater shift from predatory to defensive behavior than during control trials in which tail flagging included no infrared component. These findings provide exceptionally strong support for the hypothesis that the sensory systems of signal targets should, in general, channel the evolution of signal structure. Furthermore, the discovery of previously undescribed signaling modalities such as infrared radiation should encourage us to overcome our own human-centered sensory biases and more fully examine the form and diversity of signals in the repertoires of many animal species.