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.

Figure 1

(a) Side and (b) plan views of experimental situation. In experiment 1, the predator faced directly towards the aviary unit (predator A) or directly away. In experiment 2, the predator faced directly towards the aviary (predator A) with eyes showing or eyes covered. In experiment 3, the predator faced directly towards the aviary with eye-gaze directed either laterally towards the food source (predator B) or laterally away from the food source (predator C). The experimenter (E), sitting behind the predator, recorded the starlings' responses to the human predator without providing face cues (head is obscured by a fine-mesh stocking hood). A starling was considered near to the food in zone N (forward and below the lowest perch) and within bird's reach of the food source in region F.

Figure 2

Starlings were slower to (a) approach and (b) feed from a food source if a nearby (human) predator's eyes were visible rather than covered: mean difference in latency (eyes showing minus eyes covered) was positive for approach and feeding in both sexes. Starlings also (c) fed at a slower rate and (d) ate fewer mealworms (mw) in total from a food source if a nearby (human) predator's eyes were visible rather than covered: mean difference in latency (eyes showing minus eyes covered) was negative in both sexes. Values represent mean difference ±1 s.e.

Figure 3

Starlings were slower to (a) approach and (b) feed from a food source if a nearby (human) predator's eye-gaze was directed towards the food source rather than away from the food source: mean difference in latency (gaze towards minus gaze averted) was positive for approach and feeding in both sexes. Starlings also (c) fed at a slower rate and (d) ate fewer mealworms (mw) in total from a food source if a nearby (human) predator's eye-gaze was directed towards the food source rather than away from the food source: mean difference (gaze towards minus gaze averted) was negative in both sexes. Values represent mean difference ±1 s.e.