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

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.

尽管功能参照信号（functionally referential signals）已得到广泛研究，且主要集中于哺乳类（如非人灵长类，参见Cheney与Seyfarth 1988；獴类，参见Manser等人2002年研究；其他陆栖物种，参见Blumstein与Armitage 1997年研究），但鸟类等其他社会类群同样可从功能参照信号的使用中获益。为此，我们对群居性黑头矿吸蜜鸟（Manorina melanocephala）的报警鸣叫行为展开研究。该物种此前有轶事记录显示其会针对飞行中的捕食者发出空中报警信号，且已有实验记录表明其会针对地面威胁发出地面报警信号。但要让这些信号具备真正的参照性，需满足三项标准。其一，鸣叫需具备结构差异性，该物种的两类鸣叫均满足此项要求。其二，鸣叫需具备刺激特异性，并与特定刺激建立可靠关联。我们通过让自由活动的野生鸟类接触处于飞行状态或后续停栖状态的模拟空中捕食者，对该项标准进行了检验——本研究也是首批同时检验空中与地面报警鸣叫功能参照性的研究之一。黑头矿吸蜜鸟仅在捕食者处于飞行状态时发出空中报警信号，一旦捕食者降落，则会切换为地面报警信号。其三，参照信号需引发与对应威胁相适配的不同逃避反应。在野外环境中，仅播放空中报警鸣叫便会引发接收者几乎瞬时的逃避反应——逃至植被遮蔽处；而播放地面报警鸣叫则会引发接收者明显更迟缓的反应，并伴随警戒行为的增加。在实验室实验中，空中报警鸣叫会促使鸟类花费更多时间向上观察，而地面报警鸣叫则会促使个体进行垂直方向的警戒扫描，这与“此类信号可提供捕食者可能位置的相关信息”的预期相符。尽管已有研究表明其他鸟类类群会使用参照性报警信号，但本研究系统首次提供了基于捕食者行为而非捕食者类型的参照性鸣叫的新证据，为这类群居物种向社会群体内其他成员传递风险信息提供了一种高度适应性的途径。