Alarm calls of a cooperative bird are referential and elicit context-specific antipredator behavior

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Abstract
Although functionally referential signals have been extensively studied, largely in mammals (e.g., nonhuman primates, see Cheney and Seyfarth (1988); mongooses, see Manser et al. (2002); and other ground-dwelling species, see Blumstein and Armitage (1997), other social taxa such as birds would similarly benefit from the use of referential signals. We therefore investigated alarm calling in the cooperative noisy miner (Manorina melanocephala), a species that has been anecdotally recorded producing aerial alarms to flying predators and empirically recorded generating terrestrial alarms to ground-based threats. For these signals to be truly referential however, they must meet 3 criteria. First, calls must be structurally distinct, a requirement that these 2 call types meet. Second, calls must be stimulus-specific and reliably associated with a given stimulus. We tested this on free-living birds by exposing them to a simulated aerial predator that was either in flight or subsequently perched and thus presented one of the first studies on functionally referential alarm systems where both aerial and terrestrial alarm calls have been tested. Miners only produced aerial alarms while the stimulus was in flight, switching to terrestrial alarms once it landed. Third, referential signals must elicit different escape responses that are “appropriate” to the associated threat. Under field conditions, aerial alarm playback alone provoked an almost instantaneous response of fleeing to vegetation cover, whereas terrestrial alarm playback elicited significantly slower responses by receivers and an increase in scanning behavior. During laboratory experiments, aerial alarms stimulated birds to spend more time looking upwards, whereas terrestrial alarm calls stimulated individuals to scan perpendicularly, as expected if these stimuli provided information on likely predator location. Although other avian taxa have been shown to use referential alarm signals, this system provides novel evidence of referential calls based on the behavior rather than the type of predator, providing a highly adaptive means of communicating risk to other members of the social group in this cooperative species.

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