Do American Crows Pay Attention to Human Gaze and Facial Expressions?

Abstract

Interactions between species can lead to the evolution of interspecific communication. Non‐verbal communication by humans, both intentional and unintentional, can be interpreted by other species. We tested whether American crows (Corvus brachyrhynchos) were sensitive to human facial features under field conditions by comparing flight initiation distances and urgency of escape behavior to human approaches varying in eye contact and facial expression. We first examined whether crows distinguish between an approaching human who is directly gazing at them and a human approaching them with an averted gaze. In a second experiment, we tested whether crows differentiate a smiling from scowling human approaching them with direct or averted gaze. In the first experiment, we found that crows fled sooner and more urgently when humans were directly gazing at them. Similarly, in the second experiment, crows responded sooner to a direct vs. averted gaze; however, they did not react differently to varying human facial expressions. We suggest that crows use human gaze as a reliable visual cue compared with facial expressions when making decisions about responding to approaching humans. This is the first study to show that a wild corvid species changes its behavior based on human gaze, possibly representing an adaptation to living in human‐dominated urban areas and suggesting crows might perceive human intention by this visual cue.

New perspectives in gaze sensitivity research

“…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.…”

“…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.…”

“…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).…”

“…A recent study looked at whether American crows responded to human gaze direction and facial expression. Birds had a shorter flight initiation distance when an approaching human was looking directly at the crow, rather than away, regardless of the facial expression (scowling vs. smiling) (Clucas et al, 2013). Captive jackdaws showed adverse responses to direct gaze if the human was unfamiliar, but not when they were a familiar caretaker (von Bayern & Emery, 2009).…”

Titmouse calling and foraging are affected by head and body orientation of cat predator models and possible experience with real cats

“…Calling patterns of songbirds can also change when individuals detect predators (Templeton et al 2005), and variation in predator hunting behavior (Griesser 2008) or the movement trajectory of a predator can alter these vocalizations (Burger and Gochfeld 1981;Leavesley and Magrath 2005). Prey behavior is sensitive to the turning direction, speed of approach, facial orientation, and specific identity and facial expressions of potentially threatening individuals such as predators (Clucas et al 2013;Burger et al 1992;Cooper 1998Cooper , 2003Lee et al 2011;Marzluff et al 2010). As a final example, and one central to the present study, tufted titmice, Baeolophus bicolor, called more and foraged less when a masked human observer faced a highly preferred food source as opposed to faced away from that food source (Freeberg et al 2014).…”