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Hallmark social activities of humans, such as cooperation and cultural learning, involve eye-gaze signaling through joint attentional interaction and ostensive communication. The gaze-signaling and related cooperative-eye hypotheses posit that humans evolved unique external eye morphologies, including uniformly white sclera (the whites of the eye), to enhance the visibility of eye-gaze for conspecifics. However, experimental evidence is still lacking. This study tested the ability of human and chimpanzee participants to discriminate the eye-gaze directions of human and chimpanzee images in computerized tasks. We varied the level of brightness and size in the stimulus images to examine the robustness of the eye-gaze directional signal against simulated shading and distancing. We found that both humans and chimpanzees discriminated eye-gaze directions of humans better than those of chimpanzees, particularly in visually challenging conditions. Also, participants of both species discriminated the eye-gaze directions of chimpanzees better when the contrast polarity of the chimpanzee eye was reversed compared to when it was normal; namely, when the chimpanzee eye has human-like white sclera and a darker iris. Uniform whiteness in the sclera thus facilitates the visibility of eye-gaze direction even across species. Our findings thus support but also critically update the central premises of the gaze-signaling hypothesis. From an early age, we are able to detect the direction others are looking in (known as eye-gaze) and make eye contact with each other to communicate. The front of the human eye has a large white area known as the sclera that surrounds the darker colored iris and pupil in the center. Compared to us, chimpanzees and other nonhuman great apes have sclerae that are much darker in color or at least not as uniformly white as human eyes. Some researchers believe that the white sclera of the human eye may have evolved to make it easier for other individuals to detect the direction of our gaze. However, there is a lack of experimental evidence as to whether white sclerae actually helps humans to distinguish the direction of eye-gaze. Here, Kano, Kawaguchi and Yeow presented human and chimpanzee participants with images of other humans and chimpanzees on a computer screen and asked them to indicate the direction of eye-gaze in each image. The experiments found that both humans and chimpanzees were better able to discriminate the directions of eye-gaze from the images of humans than those of chimpanzees, particularly when the images were smaller or more shaded. Moreover, artificially altering the eyes in the chimpanzee images so that they were more human-like – that is, had a light-colored sclera and a darker iris – enabled both humans and chimpanzees to better discriminate the eye-gaze directions of the chimpanzees. Kano, Kawaguchi and Yeow’s findings indicate that white sclerae do indeed help both humans and chimpanzees to discriminate the direction of eye-gaze, even though only humans have white sclerae. This is likely because humans use eye-gaze in key social activities (including learning languages, coordinating to complete complex tasks and transmitting cultural information), indicating that white sclerae may have evolved to enhance human-specific communication. To learn more about this type of communication, future research could focus on finding out when white sclerae first evolved.

Humans operate with a \"theory of mind\" with which they are able to understand that others' actions are driven not by reality but by beliefs about reality, even when those beliefs are false. Although great apes share with humans many social-cognitive skills, they have repeatedly failed experimental tests of such false-belief understanding. We use an anticipatory looking test (originally developed for human infants) to show that three species of great apes reliably look in anticipation of an agent acting on a location where he falsely believes an object to be, even though the apes themselves know that the object is no longer there. Our results suggest that great apes also operate, at least on an implicit level, with an understanding of false beliefs.

During collective vigilance, it is commonly assumed that individual animals compromise their feeding time to be vigilant against predators, benefiting the entire group. One notable issue with this assumption concerns the unclear nature of predator ‘detection’, particularly in terms of vision. It remains uncertain how a vigilant individual utilizes its high-acuity vision (such as the fovea) to detect a predator cue and subsequently guide individual and collective escape responses. Using fine-scale motion-capture technologies, we tracked the head and body orientations of pigeons (hence reconstructed their visual fields and foveal projections) foraging in a flock during simulated predator attacks. Pigeons used their fovea to inspect predator cues. Earlier foveation on a predator cue was linked to preceding behaviors related to vigilance and feeding, such as head-up or down positions, head-scanning, and food-pecking. Moreover, earlier foveation predicted earlier evasion flights at both the individual and collective levels. However, we also found that relatively long delay between their foveation and escape responses in individuals obscured the relationship between these two responses. While our results largely support the existing assumptions about vigilance, they also underscore the importance of considering vision and addressing the disparity between detection and escape responses in future research. Most animals have to compromise between spending time foraging for food and other resources and keeping careful watch for approaching predators or other threats. Many are thought to address this trade-off by living in a group where they rely on the vigilance of others to free up more time for foraging. If one individual animal detects a threat, they alert the whole group so that every individual can respond. However, it remains unclear how individuals use vision to detect a threat and how they communicate the threat to the rest of the group. Pigeons are a useful animal model to address this question because they tend to live in groups and their vision is well understood. A pit at the back of their eye called the fovea is responsible for building clear, detailed images of the centre of the field of vision. When pigeons attend to something of interest, they typically direct their gaze by moving their whole head instead of moving their eyes, making head orientation a good proxy for researchers to track where they are looking. To better understand how pigeons detect potential threats and communicate them to the rest of the flock, Delacoux and Kano used motion capture technology to track the head movements of groups of pigeons. To encourage the pigeons to forage, grain was scattered in the centre of an enclosed room. A plastic sparrowhawk (representing a potential predator) would then emerge and move across the room before disappearing again. Analysis of the imaging data revealed that pigeons use their fovea to spot predators. Individuals that were looking around before the potential predator emerged directed their fovea towards it more quickly than pigeons that were eating. These pigeons also took flight more quickly, and this likely triggered the rest of the group to follow. Due to improvements in the tracking technologies, these findings may help scientists understand in finer detail how animals in a group detect and respond to threats and other cues in their environment. Therefore, the experimental approach used by Delacoux and Kano could also be used to investigate how information is passed among groups of other animal species.

Human social life depends on theory of mind, the ability to attribute mental states to oneself and others. A signature of theory of mind, false belief understanding, requires representing others’ views of the world, even when they conflict with one’s own. After decades of research, it remains controversial whether any nonhuman species possess a theory of mind. One challenge to positive evidence of animal theory of mind, the behavior-rule account, holds that animals solve such tasks by responding to others’ behavioral cues rather than their mental states. We distinguish these hypotheses by implementing a version of the “goggles” test, which asks whether, in the absence of any additional behavioral cues, animals can use their own self-experience of a novel barrier being translucent or opaque to determine whether another agent can see through the same barrier. We incorporated this paradigm into an established anticipatory-looking false-belief test for great apes. In a between-subjects design, apes experienced a novel barrier as either translucent or opaque, although both looked identical from afar. While being eye tracked, all apes then watched a video in which an actor saw an object hidden under 1 of 2 identical boxes. The actor then scuttled behind the novel barrier, at which point the object was relocated and then removed. Only apes who experienced the barrier as opaque visually anticipated that the actor would mistakenly search for the object in its previous location. Great apes, therefore, appeared to attribute differential visual access based specifically on their own past perceptual experience to anticipate an agent’s actions in a false-belief test.

Surprisingly little is known about the eye movements of chimpanzees, despite the potential contribution of such knowledge to comparative cognition studies. Here, we present the first examination of eye tracking in chimpanzees. We recorded the eye movements of chimpanzees as they viewed naturalistic pictures containing a full-body image of a chimpanzee, a human or another mammal; results were compared with those from humans. We found a striking similarity in viewing patterns between the two species. Both chimpanzees and humans looked at the animal figures for longer than at the background and at the face region for longer than at other parts of the body. The face region was detected at first sight by both species when they were shown pictures of chimpanzees and of humans. However, the eye movements of chimpanzees also exhibited distinct differences from those of humans; the former shifted the fixation location more quickly and more broadly than the latter. In addition, the average duration of fixation on the face region was shorter in chimpanzees than in humans. Overall, our results clearly demonstrate the eye-movement strategies common to the two primate species and also suggest several notable differences manifested during the observation of pictures of scenes and body forms.

Humans' two closest primate living relatives, bonobos and chimpanzees, differ behaviorally, cognitively, and emotionally in several ways despite their general similarities. While bonobos show more affiliative behaviors towards conspecifics, chimpanzees display more overt and severe aggression against conspecifics. From a cognitive standpoint, bonobos perform better in social coordination, gaze-following and food-related cooperation, while chimpanzees excel in tasks requiring extractive foraging skills. We hypothesized that attention and motivation play an important role in shaping the species differences in behavior, cognition, and emotion. Thus, we predicted that bonobos would pay more attention to the other individuals' face and eyes, as those are related to social affiliation and social coordination, while chimpanzees would pay more attention to the action target objects, as they are related to foraging. Using eye-tracking we examined the bonobos' and chimpanzees' spontaneous scanning of pictures that included eyes, mouth, face, genitals, and action target objects of conspecifics. Although bonobos and chimpanzees viewed those elements overall similarly, bonobos viewed the face and eyes longer than chimpanzees, whereas chimpanzees viewed the other elements, the mouth, action target objects and genitals, longer than bonobos. In a discriminant analysis, the individual variation in viewing patterns robustly predicted the species of individuals, thus clearly demonstrating species-specific viewing patterns. We suggest that such attentional and motivational differences between bonobos and chimpanzees could have partly contributed to shaping the species-specific behaviors, cognition, and emotion of these species, even in a relatively short period of evolutionary time.

Recent findings from anticipatory-looking false-belief tests have shown that nonhuman great apes and macaques anticipate that an agent will go to the location where the agent falsely believed an object to be. Phillips et al.'s claim that nonhuman primates attribute knowledge but not belief should thus be reconsidered. We propose that both knowledge and belief attributions are evolutionary old.

Collection of large behavioural data‐sets on wild animals in natural habitats is vital in ecology and evolution studies. Recent progress in machine learning and computer vision, combined with inexpensive microcomputers, has unlocked a new frontier of fine‐scale markerless measurements. Here, we leverage these advancements to develop a 3D Synchronized Outdoor Camera System (3D‐SOCS): an inexpensive, mobile and automated method for collecting behavioural data on wild animals using synchronized video frames from Raspberry Pi controlled cameras. Accuracy tests demonstrate 3D‐SOCS' markerless tracking can estimate postures with a 3 mm tolerance. To illustrate its research potential, we place 3D‐SOCS in the field and conduct a stimulus presentation experiment. We estimate 3D postures and trajectories for multiple individuals of different bird species, and use this data to characterize the visual field configuration of wild great tits (Parus major), a model species in behavioural ecology. We find their optic axes at ~±60° azimuth and −5° elevation. Furthermore, birds exhibit functional lateralization in their use of the right eye with conspecific stimulus, and show individual differences in lateralization. We also show that birds' convex hulls predicts body weight, highlighting 3D‐SOCS' potential for non‐invasive population monitoring. 3D‐SOCS is a first‐of‐its‐kind camera system for wild research, presenting exciting potential to measure fine‐scaled behaviour and morphology in wild birds. Zusammenfassung Die Erhebung umfangreicher Verhaltensdatensätze von Wildtieren in natürlichen Lebensräumen ist von zentraler Bedeutung für die Ökologie und Evolutionsforschung. Fortschritte im Bereich des maschinellen Lernens und der Computer Vision, kombiniert mit kostengünstigen Mikrocomputern, haben eine neue Ära der feinmaßstäblichen, markierungsfreien Messungen eröffnet. Wir nutzen diese Entwicklungen, um ein 3D‐Synchronisiertes Outdoor‐Kamerasystem (3D‐SOKS) zu entwickeln: eine kostengünstige, mobile und automatisierte Methode zur Erhebung von Verhaltensdaten bei Wildtieren anhand synchronisierter Videoaufnahmen von mit Raspberry Pis gesteuerten Kameras. Genauigkeitstests zeigen, dass die markierungsfreie Verfolgung durch 3D‐SOKS Körperhaltungen mit einer Toleranz von 3 mm schätzen kann. Zur Demonstration des wissenschaftlichen Potenzials setzen wir 3D‐SOKS im Feld ein und führen ein Stimulus‐Präsentationsexperiment durch. Wir schätzen 3D‐Körperhaltungen und ‐Trajektorien mehrerer Individuen verschiedener Vogelarten und nutzen diese Daten, um die Konfiguration des Gesichtsfelds von wildlebenden Kohlmeisen (Parus major), einer Modellspezies in der Verhaltensökologie, zu charakterisieren. Wir finden deren optische Achsen bei etwa ±60° Azimut und −5° Elevation. Zudem zeigen die Vögel eine funktionelle Lateralisation in der Nutzung des rechten Auges bei der Wahrnehmung von Artgenossen und individuelle Unterschiede in dieser Lateralisation. Wir zeigen außerdem, dass der konvexe Hüllenbereich der Vögel das Körpergewicht vorhersagt, was das Potenzial von 3D‐SOKS für nichtinvasives Populationsmonitoring unterstreicht. 3D‐SOKS ist das erste Kamerasystem seiner Art für die Wildtierforschung und eröffnet neue Möglichkeiten zur Erfassung feinmaßstäblicher Verhaltens‐ und Morphologiedaten bei wildlebenden Vögeln.

When viewing social scenes, humans and nonhuman primates focus on particular features, such as the models' eyes, mouth, and action targets. Previous studies reported that such viewing patterns vary significantly across individuals in humans, and also across closely-related primate species. However, the nature of these individual and species differences remains unclear, particularly among nonhuman primates. In large samples of human and nonhuman primates, we examined species differences and the effects of experience on patterns of gaze toward social movies. Experiment 1 examined the species differences across rhesus macaques, nonhuman apes (bonobos, chimpanzees, and orangutans), and humans while they viewed movies of various animals' species-typical behaviors. We found that each species had distinct viewing patterns of the models' faces, eyes, mouths, and action targets. Experiment 2 tested the effect of individuals' experience on chimpanzee and human viewing patterns. We presented movies depicting natural behaviors of chimpanzees to three groups of chimpanzees (individuals from a zoo, a sanctuary, and a research institute) differing in their early social and physical experiences. We also presented the same movies to human adults and children differing in their expertise with chimpanzees (experts vs. novices) or movie-viewing generally (adults vs. preschoolers). Individuals varied within each species in their patterns of gaze toward models' faces, eyes, mouths, and action targets depending on their unique individual experiences. We thus found that the viewing patterns for social stimuli are both individual- and species-specific in these closely-related primates. Such individual/species-specificities are likely related to both individual experience and species-typical temperament, suggesting that primate individuals acquire their unique attentional biases through both ontogeny and evolution. Such unique attentional biases may help them learn efficiently about their particular social environments.

This study offers a new method for examining the bodily, manual, and eye movements of a chimpanzee at the micro-level. A female chimpanzee wore a lightweight head-mounted eye tracker (60 Hz) on her head while engaging in daily interactions with the human experimenter. The eye tracker recorded her eye movements accurately while the chimpanzee freely moved her head, hands, and body. Three video cameras recorded the bodily and manual movements of the chimpanzee from multiple angles. We examined how the chimpanzee viewed the experimenter in this interactive setting and how the eye movements were related to the ongoing interactive contexts and actions. We prepared two experimentally defined contexts in each session: a face-to-face greeting phase upon the appearance of the experimenter in the experimental room, and a subsequent face-to-face task phase that included manual gestures and fruit rewards. Overall, the general viewing pattern of the chimpanzee, measured in terms of duration of individual fixations, length of individual saccades, and total viewing duration of the experimenter's face/body, was very similar to that observed in previous eye-tracking studies that used non-interactive situations, despite the differences in the experimental settings. However, the chimpanzee viewed the experimenter and the scene objects differently depending on the ongoing context and actions. The chimpanzee viewed the experimenter's face and body during the greeting phase, but viewed the experimenter's face and hands as well as the fruit reward during the task phase. These differences can be explained by the differential bodily/manual actions produced by the chimpanzee and the experimenter during each experimental phase (i.e., greeting gestures, task cueing). Additionally, the chimpanzee's viewing pattern varied depending on the identity of the experimenter (i.e., the chimpanzee's prior experience with the experimenter). These methods and results offer new possibilities for examining the natural gaze behavior of chimpanzees.