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

While functionally referential signals have been extensively studied, largely in mammals (e.g. non-human primates, see Cheney & Seyfarth; mongooses, see Manser et al. and other ground-dwelling species, see Blumstein et al.), 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 three criteria. Firstly, calls must be structurally distinct, a requirement that these two call types meet. Secondly, 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 whilst the stimulus was in flight, switching to terrestrial alarms once it landed. Thirdly, 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. While 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.尽管功能指涉信号（functionally referential signals）已得到广泛研究，且研究对象多集中于哺乳类（例如非人灵长类，参见Cheney与Seyfarth的研究；獴类，参见Manser等人的研究；以及其他陆生穴居物种，参见Blumstein等人的研究），但诸如鸟类在内的其他社会性类群，同样可从指涉信号的使用中获益。为此，我们针对群居性黑额矿吸蜜鸟（Manorina melanocephala）的报警鸣叫（alarm calling）展开了研究。该物种曾有轶事记录显示其会针对飞行捕食者发出空中报警叫声，且经实证记录可针对地面威胁产生地面报警叫声。然而，若要认定这些信号属于真正的指涉信号，则需满足三项标准：其一，两类叫声需具备结构上的差异性，该物种的这两种报警叫声恰好符合此项要求；其二，叫声需具备刺激特异性（stimulus-specific），且与特定刺激建立可靠关联。我们通过向野外自由生活的鸟类个体展示处于飞行状态或后续停落的模拟空中捕食者，对该标准进行了检验，本研究也是首批同时针对空中与地面报警叫声开展测试的功能指涉报警通讯系统研究之一。结果显示，黑额矿吸蜜鸟仅在模拟捕食者处于飞行状态时发出空中报警叫声，而当捕食者降落之后，则会切换为地面报警叫声。其三，指涉信号必须引发与对应威胁相适配的差异化逃逸反应。在野外条件下，仅对空中报警叫声进行回放播放（playback）便会引发受试个体几乎瞬间逃往植被遮蔽处的反应，而对地面报警叫声进行回放播放则会引发接收者明显更迟缓的反应，同时伴随警戒行为的增加。在实验室实验中，空中报警叫声会刺激个体花费更多时间向上观察，而地面报警叫声则会促使个体进行垂直方向的警戒扫描，这一结果与"这些叫声可传递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也会使用指涉报警信号，但本研究系统为基于捕食者行为而非捕食者种类的指涉叫声提供了全新证据，为该群居物种向社群其他成员传递风险信息提供了一种高度适应性的通讯方式。