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Gaze sensitivity: function and mechanisms from sensory and cognitive perspectives
Abstract and Figures
Sensitivity to the gaze of other individuals has long been a primary focus in sociocognitive research on humans and other animals. Information about where others are looking may often be of adaptive value in social interactions and predator avoidance, but studies across a range of taxa indicate there are substantial differences in the extent to which animals obtain and use information about other individuals' gaze direction. As the literature expands, it is becoming increasingly difficult to make comparisons across taxa as experiments adopt and adjust different methodologies to account for differences between species in their socioecology, sensory systems and possibly also their underlying cognitive mechanisms. Furthermore, as more species are found to exhibit gaze sensitivity, more terminology arises to describe the behaviours. To clarify the field, we propose a restricted nomenclature that defines gaze sensitivity in terms of observable behaviour, independent of the underlying mechanisms. This is particularly useful in nonhuman animal studies where cognitive interpretations are ambiguous. We then describe how socioecological factors may influence whether species will attend to gaze cues, and suggest links between ultimate factors and proximate mechanisms such as cognition and perception. In particular, we argue that variation in sensory systems, such as retinal specializations and the position of the eyes, will determine whether gaze cues (e.g. head movement) are perceivable during visual fixation. We end by making methodological recommendations on how to apply these variations in socioecology and visual systems to advance the field of gaze research.
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... The sensitivity to subtle indicators could also be affected by other risks, including predator and social information (Davidson and Clayton 2016). There is often interplay between multiple predator information and the features of the gaze cues available (Davidson et al. 2014). As reviewed by Davidson and Clayton (2016), predator identity, facial expression, approach direction and other predator information had significant effects on gaze sensitivity. ...
... This aversion to human gaze has been reported not only in birds but also in ungulates and lizards (Sreekar and Quader 2013;Stankowich and Coss 2006). A predator gaze may provide accurate information for prey to decide when to flee (Davidson et al. 2014). Prey may eventually benefit from more foraging opportunities or more frequent nest visits by precisely perceiving a predator's direct gaze (Carter et al. 2008;Davidson et al. 2015). ...
In predator–prey interactions, various factors affect the prey’s perception of risk and decision to flee. Gaze sensitivity, the ability to react to the presence, direction, or movement of the head and eyes, has been reported in many birds. However, few studies have focussed on variation in sensitivity to human gaze in relation to other risks and potential breeding costs. Here, we studied the influence of human gaze on the escape behaviour of Azure-winged magpies (Cyanopica cyanus) and investigated the effects of breeding state (breeding season and nonbreeding season) and approach direction on gaze sensitivity. In Experiment 1, we tested whether magpies showed different sensitivities to human gaze according to age class and breeding state when approached directly. The results showed that the breeding state could affect the flight initiation distance (FID), with adults in the breeding season having a shorter FID compared to those in the nonbreeding season. Meanwhile, only adults were found to be averse to direct human gaze and juveniles showed no sensitivity. In Experiment 2, we conducted three different gaze treatments on adult magpies in the breeding season under three bypass distances (0 m, 2.5 m, 5 m). The results showed that approach direction had no effect on FID, while the sensitivity to human gaze differed under three bypass distances. Adults could clearly recognise human head and eye direction at a certain bypass distance (2.5 m). Our study reveals the cognitive ability of Azure-winged magpies to human head and eye direction and the effects of age, breeding state and approach direction, which may provide further insights into human–wildlife interactions, especially for birds in urban habitats.
... This probably favored the evolution of stalking behavior by making the presence of predators less obvious for their prey. Still, even if these predators managed to occlude parts of their bodies, they must have needed to visually monitor prey to carry out an attack, leaving their gaze available as an environmental cue (Coss, Ramakrishnan, and Schank 2005;Davidson et al. 2014). We expected that lateral posture would require shorter detection latency and result in higher detection accuracy than the other postures because laterally positioned models are the largest stimuli (i.e., they activate a larger retinal area) (Smith and Pokorny 1977;Gomes et al. 2005). ...
The success of a predatory attack is related to how much a predator manages to approach a prey without being detected. Some carnivore mammals use environmental objects (e.g., leaves and branches) as visual obstacles during stalking behavior, allowing them to expose only parts of their bodies while approaching and visual monitoring their prey. Here, we investigate the influence of carnivores’ body postures, gaze direction, and camouflage pattern on their detection by prey. To do so, we photographed taxidermized carnivore models (cougar, ocelot, and lesser grison) in their preserved natural habitats and presented these images to human dichromats (i.e., colourblinds) and trichromats (i.e., normal color vision). Our findings highlight the importance of body outline and gaze as search images during predator detection tasks. We also demonstrate that coat and facial color patterns can camouflage predator's body outline and gaze. This is the first behavioral evidence that the facial coloration of natural predators might mask their gaze to potential prey. Furthermore, we observed that carnivore coat color patterns may serve as an additional cue for trichromats, particularly in hidden carnivore detection tasks that proved to be more challenging for dichromats. Our results show possible strategies that evolved between predator and preys, in which prey make use of body outlines, gaze direction, and coat color to improve predator detection, while predators potentially evolved stalking behavior and body/gaze camouflage as counter strategies to cope with the improvements in prey's perception and conceal their presence.
... Alternatively, a possible reason for the shorter looking durations at the human stimuli might be due to avoidance of the human face images, as the presented humans might be perceived as possible predators (Davidson et al., 2014). This might have led to behavioural responses aimed at reducing the time the human images can be observed, e.g. by moving away from the experimental apparatus. ...
... One study found that individuals in pairs of captive birds synchronized their head turns but it did not examine gaze direction [20]. Gaze synchronization could arise from gaze following as one individual follows the gaze of another to look at the same thing [36]. Florida scrub jays have lateral eyes and probably a wide field of view [28]. ...
Sentinels can detect predators and rivals early by monitoring their surroundings from vantage points. Multiple sentinels in a group may reduce the perceived predation risk by diluting the risk and increasing collective detection, especially if sentinels monitor different areas at the same time. We investigated sentinel behavior in groups of the Florida scrub jay (Aphelocoma caerulescens). Sentinels in this species turn their heads frequently to monitor different areas for threats. As predicted, we found that sentinels turned their heads less frequently in the presence of other sentinels. Multiple sentinels, however, tended to gaze in the same direction at the same time more often than predicted by chance alone. Gaze synchronization reduces the efficiency of collective detection by reducing visual coverage at any one time at the group level. Despite the benefits of the presence of other sentinels, our results highlight the limits to collective detection when multiple individuals are vigilant at the same time.
This handbook lays out the science behind how animals think, remember, create, calculate, and remember. It provides concise overviews on major areas of study such as animal communication and language, memory and recall, social cognition, social learning and teaching, numerical and quantitative abilities, as well as innovation and problem solving. The chapters also explore more nuanced topics in greater detail, showing how the research was conducted and how it can be used for further study. The authors range from academics working in renowned university departments to those from research institutions and practitioners in zoos. The volume encompasses a wide variety of species, ensuring the breadth of the field is explored.
Many primate species reliably track and follow the visual gaze of conspecifics and humans, even to locations above and behind the subject. However, it is not clear whether primates follow a human's gaze to find hidden food under one of two containers in an object-choice task. In a series of experiments six adult female chimpanzees followed a human's gaze (head and eye direction) to a distal location in space above and behind them, and checked back to the human's face when they did not find anything interesting or unusual. This study also assessed whether these same subjects would also use the human's gaze in an object-choice task with three types of occluders: barriers, tubes, and bowls. Barriers and tubes permitted the experimenter to see their contents (i.e., food) whereas bowls did not. Chimpanzees used the human's gaze direction to choose the tube or barrier containing food but they did not use the human's gaze to decide between bowls. Our findings allowed us to discard both simple orientation and understanding seeing-knowing in others as the explanations for gaze following in chimpanzees. However, they did not allow us to conclusively choose between orientation combined with foraging tendencies and understanding seeing in others. One interesting possibility raised by these results is that studies in which the human cannot see the reward at the time of subject choice may potentially be underestimating chimpanzees' social knowledge.
The avian eye is considered to be “supreme amongst all living creatures” and capable of attaining “an order of excellence unmatched in any other species not excepting man” (Duke-Elder, 1958). Many structural and functional adaptations have become involved in the perfection of visual processes in birds which, according to Pumphrey (1948a) represent the culmination of phylogenetic development toward diurnal vision. This chapter is concerned with several of these adaptations, the most obvious of which are the oil droplet inclusions and glycogen deposits within their photoreceptors, the well-developed areae and foveae within their retina and the highly vascularized pecten within their vitreous body. A detailed description of the avian eye is not intended; excellent sources are available on this subject: Wood (1914), Slonaker (1918), Franz (1934), Walls (1942), Rochon-Duvigneaud (1943), Polyak (1957), Duke-Elder (1958), and Hodges (1974)
The vertebrate retina is an extension of the brain, a hemisphere of neural tissue upon which is mapped an image of a particular species visual environment. Each point in visual space is subtended by a corresponding point on the neural retina which in turn is retinotopically mapped onto the visual centres of the brain. Light energy or the ‘optical image’ is transformed into electrical energy or a ‘neural image’ by the photoreceptors and, via a number of interneurons (bipolar, amacrine and horizontal cells), these signals reach the ganglion cells each of which possess an axon carrying information to the central nervous system via the optic nerve. Although processing at the level of the photoreceptors may not necessarily change the neural image, due to the over abundance of photoreceptors relative to the number of ganglion cells, it is the ganglion cells which ultimately define the perception of a species’ environment received by the central nervous system.
Black iguanas (Ctenosaura similis) are eaten by humans and other predators throughout Central America. The importance of a human face to the avoidance and fleeing behavior of black iguanas was examined using an approaching person as the stimulus. Iguanas were exposed to an approaching person either with an exposed face or with the face covered with hair. In the latter case the iguanas received the conflicting stimuli of a person both approaching, yet appearing to retreat. Iguanas moved earlier, ran earlier, and ran farther when the approaching person had an exposed face compared to a face hidden by hair. For iguanas exposed to a face there were significant correlations between the escape behaviors; iguanas that moved and ran earlier also ran farther. However, for iguanas exposed to the hair there were no significant correlations among escape behaviors.
Food caching is accompanied by a risk of theft, especially when observers remember cache locations and pilfer them later. This is the case in some corvids, in which cachers have been shown to change their behaviour flexibly to prevent and reduce the quality of information available to observers who might steal their caches, and invalidate information those observers have already obtained. In this 'war of information', strategies that observers use to increase the amount and validity of information about caches have been studied much less. A first step in exploring pilferer strategies is to determine what individuals prefer to watch when observing others. To that end, we allowed western scrub-jays, Aphelocoma californica, to observe either of two cages through peepholes, varying the information available in them in four experimental conditions. We later extracted the number and duration of looks into each peephole and the behaviour of the individuals that were observed through them. Jays spent much more time looking at caching individuals than either at noncaching individuals or at a cage with only a food bowl and caching trays, suggesting the birds prefer to watch caching and cache-related behaviours. Moreover, when we analysed the attention-getting and attention-holding aspects separately, our results suggested that jays are specifically tuned to looking at locations where there is high potential for caching. Improved pilfering success associated with such active information seeking by observers may have forced cachers to evolve better strategies for concealing or invalidating caching information, in a coevolutionary process resulting in the sophisticated strategies some corvids use.
Corvids such as jays and ravens cache food for future consumption and can remember the location of caches that they have seen others make. Given the risk of caches being pilfered by observers, corvids limit opportunities for conspecifics to witness caching events. Faced with cache protection tactics, pilferers should also utilize tactics to maximize their success. Cacher-pilferer interactions and their underlying cognition have largely been investigated in semisocial ravens, Corvus corax, and western scrub-jays, Aphelocoma californica. However to understand the factors influencing the development of these abilities, data are required from species that differ in their socioecology from ravens and western scrub-jays. In the current study, we tested the caching and pilfering behaviour of territorial Eurasian jays in two social contexts. In one context, subjects competed with a dominant conspecific, while in the other the same individuals interacted with a subordinate competitor. When subordinate, birds initially suppressed caching, before caching more in less exposed locations. In contrast, when socially dominant, birds cached more and moved items multiple times. As subordinate pilferers, birds took longer to approach cache sites and approached when the cacher was at a distance, while when dominant, birds rapidly approached the conspecifics' cache sites, frequently when the cacher was still in the process of caching. Individual jays therefore flexibly switched caching and pilfering tactics in response to the relative dominance of their competitor. We discuss the implications of our results for competing theories on the origin of behavioural flexibility and its underlying complex cognition in the corvid lineage.
A surprising finding in comparative social cognition is that great apes seem to have difficulties understanding others' communicative behaviour. In no other paradigm is this more evident than in the object-choice task in which subjects use a human cue, such as pointing, to infer the correct choice of a reward hidden in one of a number of containers. Apes often perform poorly in the task whereas many other species succeed. One popular explanation for this finding is that apes have not evolved the propensity to understand others' communicative behaviour because their social systems are based predominantly on competitive relationships. We caution against this hypothesis by highlighting recent experimental evidence that suggests methodological factors are responsible for the apes' poor performance in object-choice studies. Furthermore, we compared the methodology and results of 63 published object-choice studies in a range of animal taxa. We found that the central object-choice method that is only used with apes and other primates typically results in failure. When, however, modifications are made to this method or apes are tested with a peripheral method that is similar to the one used with many other species, their performance vastly improves. We discuss the significance of this in relation to past object-choice research and make several recommendations as to how future research can be improved upon so that apes are tested in a manner comparable to the testing of other animal species.