The development of alarm-call responses in free-living and captive Belding's ground squirrels, Spermophilus beldingi.

Abstract

Responding appropriately to alarm calls may be especially important to immature animals, since they are generally more susceptible to predators than adults, yet little is known about alarm-call response development. Responses of free-living and captive Belding's ground squirrels (Spermophilus beldingi) to playbacks of conspecific (three classes of alarm calls and juvenile squeals) and heterospecific (wren-song) vocalizations were observed from natal emergence until dispersal. Cardiac responses revealed that pre-emergent pups can discriminate between whistle alarm calls, indicative of fast-moving predators, and trill alarm calls (slow-moving predator calls). Behavioral discrimination of the five auditory stimuli was not detected at emergence, but appeared within the next five days, with responsivity to whistles developing earlier than to trills. Development of post-emergent discrimination was dependent on experience with hearing calls and possibly with responding behaviorally to calls. Response patterns (initial responses, duration, vigilant postures) changed throughout the following four weeks, and approximated adult responses before juveniles dispersed. These patterns were largely mediated by maturation of sensory-perceptual and motor systems. Juveniles' responses were indirectly influenced by conspecifics' responses. Dams were not necessary for juvenile response-pattern development but facilitated the development of discrimination among alarm and non-alarm calls. Pre-emergent experiences, including exposure to auditory, visual and tactile stimulation, had a prolonged effect on juveniles' post-emergent responses to playbacks, with captive juveniles more responsive to calls and exhibiting heightened responses compared with free-living juveniles. Manipulations of post-emergent rearing histories had no effect on response development. Finally, animals were conditioned to exhibit escape responses to a previously neutral vocalization, indicating that juvenile and adult repertoires are modifiable through experience. Alarm-call responses appear to be adapted to the current stage of juvenile development, with younger juveniles making a trade-off between information gathering and escape responses. Despite their vulnerability, juveniles may not emerge with fully formed associations between alarm calls and appropriate responses because local predator contexts change over time, favoring developmental plasticity in response repertoires. In summary, alarm-call responses of S. beldingi develop epigenetically during their first summer above ground, through a combination of experience with calls and maturation of physical systems, and is in part socially facilitated by adult conspecifics.