Subtle cues of predation risk: starlings respond to a predator's direction of eye-gaze

Abstract

For prey animals to negotiate successfully the fundamental trade-off between predation and starvation, a realistic assessment of predation risk is vital. Prey responses to conspicuous indicators of risk (such as looming predators or fleeing conspecifics) are well documented, but there should also be strong selection for the detection of more subtle cues. A predator's head orientation and eye-gaze direction are good candidates for subtle but useful indicators of risk, since many predators orient their head and eyes towards their prey as they attack. We describe the first explicit demonstration of a bird responding to a live predator's eye-gaze direction. We present wild-caught European starlings (Sturnus vulgaris) with human 'predators' whose frontal appearance and gaze direction are manipulated independently, and show that starlings are sensitive to the predator's orientation, the presence of eyes and the direction of eye-gaze. Starlings respond in a functionally significant manner: when the predator's gaze was averted, starlings resumed feeding earlier, at a higher rate and consumed more food overall. By correctly assessing lower risk and returning to feeding activity earlier (as in this study), the animal gains a competitive advantage over conspecifics that do not respond to the subtle predator cue in this way.

New perspectives in gaze sensitivity research

“…Gaze following (co-orienting gaze with a conspecific or human experimenter) has been reported in apes (e.g., Bräuer, Call, & Tomasello, 2005), monkeys (e.g., Emery, Lorincz, Perrett, Oram, & Baker, 1997), ungulates (e.g., Kaminski, Riedel, Call, & Tomasello, 2005), dogs (e.g., Bräuer, Call, & Tomasello, 2004), birds (e.g., ravens (Corvus corax), Bugnyar, Stowe, & Heinrich, 2004), and reptiles (red-footed tortoise (Geochelone carbonaria), Wilkinson, Mandl, Bugnyar, & Huber, 2010). Moreover, gaze aversion, in which animals respond fearfully to direct gaze, presumably because forward facing eyes are associated with predator attacks, has been reported in a similar breath of taxa including mammals (e.g., Coss, 1978b), birds (e.g., Carter, Lyons, Cole, & Goldsmith, 2008;von Bayern & Emery, 2009), reptiles (basking black iguana (Ctenosaura similis), Burger, Gochefeld, & Murray Jr, 1991), and fish (African jewel fish (Hemichromis bimaculatus), Coss, 1979) (see Davidson, Butler, Fernández-Juricic, Thornton, & Clayton, 2013, for review). Comparative psychologists have used gaze sensitivity as a paradigm to test whether animal responses to gaze are due to an understanding of the attention and perspective of others, or whether they are responding to physical features of gaze direction as salient cues (e.g., movement, shape, conspicuousness) (e.g., Povinelli & Eddy, 1996;von Bayern & Emery, 2009).…”

“…This is because they do not perceive eye direction as a meaningful cue to indicate gaze direction. Gaze aversion tasks have also tested whether birds can distinguish between subtle eye gaze cues (Hampton, 1994;Carter et al, 2008;Clucas, Marzluff, Mackovjak, & Palmquist, 2013;Garland, Low, Armstrong, & Burns, 2014;von Bayern & Emery, 2009). Predators with gaze facing towards prey rather than away may predict a predator's attack; therefore prey should respond more aversively to eyes that are direct rather than averted.…”

“…Birds that have been reported to discriminate between human eye directions have had extensive experience with humans. This is because they have either been raised by humans (jackdaws, von Bayern & Emery, 2009), tested within in the confines of an experimental arena with the human (starlings, Carter et al, 2008;jackdaws, von Bayern & Emery, 2009) or habituated to close observation (American crows, Clucas et al, 2013;New Zealand robins, Garland et al, 2014). Similarly, the type of predator may determine whether gaze direction is considered valued information (sensu Stephens, 1989).…”

“…Predators with gaze facing towards prey rather than away may predict a predator's attack; therefore prey should respond more aversively to eyes that are direct rather than averted. Jackdaws (von Bayern & Emery, 2009), New Zealand robins (Petroica australis) (Garland et al, 2014), American crows (Corvus brachyrhynchos) (Clucas et al, 2013), and starlings (Sturnus vulgaris) (Carter et al, 2008), but not house sparrows (Passer domesticus) (Hampton, 1994), are sensitive to subtle differences in eye direction. Although in principle it may seem reasonable to assume that the capacity to differentiate between very subtle eye orientations would be an indication of where another individual is looking, it remains plausible that birds have evolved predispositions to respond fearfully to forwardfacing eyes, or individuals may have learned which cue was more likely to predict the actions of humans or natural predators.…”

Salient eyes deter conspecific nest intruders in wild jackdaws ( Corvus monedula )

“…For example, basking black iguanas (Ctenosaura similis) [1] and jewel fish (Hemichromis bimaculatus) [2] respond to eye shapes by fleeing rapidly. Birds, including house sparrows (Passer domesticus) [3], starlings (Sturnus vulgaris) [4] and jackdaws (Corvus monedula) [5], also exhibit fearful responses when presented with heterospecific eyes. These responses have been attributed to an instinctive tendency to avoid stimuli that resemble predator eyes [3].…”