Gaze tracking of large-billed crows (Corvus macrorhynchos) in a motion capture system.

Previous studies often inferred the focus of a bird's attention from its head movements because it provides important clues about their perception and cognition. However, it remains challenging to do so accurately, as the details of how they orient their visual field toward the visual targets remain largely unclear. We thus examined visual field configurations and the visual field use of large-billed crows (Corvus macrorhynchos Wagler 1827). We used an established ophthalmoscopic reflex technique to identify the visual field configuration, including the binocular width and optical axes, as well as the degree of eye movement. A newly established motion capture system was then used to track the head movements of freely moving crows to examine how they oriented their reconstructed visual fields toward attention-getting objects. When visual targets were moving, the crows frequently used their binocular visual fields, particularly around the projection of the beak-tip. When the visual targets stopped moving, crows frequently used non-binocular visual fields, particularly around the regions where their optical axes were found. On such occasions, the crows slightly preferred the right eye. Overall, the visual field use of crows is clearly predictable. Thus, while the untracked eye movements could introduce some level of uncertainty (typically within 15 deg), we demonstrated the feasibility of inferring a crow's attentional focus by 3D tracking of their heads. Our system represents a promising initial step towards establishing gaze tracking methods for studying corvid behavior and cognition.

Bonobos and chimpanzees remember familiar conspecifics for decades.

Recognition and memory of familiar conspecifics provides the foundation for complex sociality and is vital to navigating an unpredictable social world [Tibbetts and Dale, Trends Ecol. Evol. 22, 529-537 (2007)]. Human social memory incorporates content about interactions and relationships and can last for decades [Sherry and Schacter, Psychol. Rev. 94, 439-454 (1987)]. Long-term social memory likely played a key role throughout human evolution, as our ancestors increasingly built relationships that operated across distant space and time [Malone et al., Int. J. Primatol. 33, 1251-1277 (2012)]. Although individual recognition is widespread among animals and sometimes lasts for years, little is known about social memory in nonhuman apes and the shared evolutionary foundations of human social memory. In a preferential-looking eye-tracking task, we presented chimpanzees and bonobos (N = 26) with side-by-side images of a previous groupmate and a conspecific stranger of the same sex. Apes' attention was biased toward former groupmates, indicating long-term memory for past social partners. The strength of biases toward former groupmates was not impacted by the duration apart, and our results suggest that recognition may persist for at least 26 y beyond separation. We also found significant but weak evidence that, like humans, apes may remember the quality or content of these past relationships: apes' looking biases were stronger for individuals with whom they had more positive histories of social interaction. Long-lasting social memory likely provided key foundations for the evolution of human culture and sociality as they extended across time, space, and group boundaries.

SMART-BARN: Scalable multimodal arena for real-time tracking behavior of animals in large numbers.

The SMART-BARN (scalable multimodal arena for real-time tracking behavior of animals in large numbers) achieves fast, robust acquisition of movement, behavior, communication, and interactions of animals in groups, within a large (14.7 meters by 6.6 meters by 3.8 meters), three-dimensional environment using multiple information channels. Behavior is measured from a wide range of taxa (insects, birds, mammals, etc.) and body size (from moths to humans) simultaneously. This system integrates multiple, concurrent measurement techniques including submillimeter precision and high-speed (300 hertz) motion capture, acoustic recording and localization, automated behavioral recognition (computer vision), and remote computer-controlled interactive units (e.g., automated feeders and animal-borne devices). The data streams are available in real time allowing highly controlled and behavior-dependent closed-loop experiments, while producing comprehensive datasets for offline analysis. The diverse capabilities of SMART-BARN are demonstrated through three challenging avian case studies, while highlighting its broad applicability to the fine-scale analysis of collective animal behavior across species.

Disgust in animals and the application of disease avoidance to wildlife management and conservation.

Disgust is an adaptive system hypothesized to have evolved to reduce the risk of becoming sick. It is associated with behavioural, cognitive and physiological responses tuned to allow animals to avoid and/or get rid of parasites, pathogens and toxins. Little is known about the mechanisms and outcomes of disease avoidance in wild animals. Furthermore, given the escalation of negative human-wildlife interactions, the translation of such knowledge into the design of evolutionarily relevant conservation and wildlife management strategies is becoming urgent. Contemporary methods in animal ecology and related fields, using direct (sensory cues) or indirect (remote sensing technologies and machine learning) means, provide a flexible toolbox for testing and applying disgust at individual and collective levels. In this review/perspective paper, we provide an empirical framework for testing the adaptive function of disgust and its associated disease avoidance behaviours across species, from the least to the most social, in different habitats. We predict various trade-offs to be at play depending on the social system and ecology of the species. We propose five contexts in which disgust-related avoidance behaviours could be applied, including endangered species rehabilitation, invasive species, crop-raiding, urban pests and animal tourism. We highlight some of the perspectives and current challenges of testing disgust in the wild. In particular, we recommend future studies to consider together disease, predation and competition risks. We discuss the ethics associated with disgust experiments in the above contexts. Finally, we promote the creation of a database gathering disease avoidance evidence in animals and its applications.

Le dégoût est un système adaptatif supposé avoir évolué afin de réduire le risque de tomber malade. Il est associé à des réponses comportementales, cognitives et physiologiques adaptées pour permettre aux animaux d'éviter et/ou de se débarrasser des parasites, pathogènes et toxines. On sait peu de choses sur les mécanismes et les conséquences de l'évitement des maladies chez les animaux sauvages. Étant donné l'escalade des interactions négatives entre humains et faune, la traduction de ces connaissances dans la conception de stratégies de conservation et de gestion de la faune - prenant en considération l'évolution des espèces - devient urgente. Les méthodes contemporaines en écologie animale et dans les domaines connexes, utilisant des moyens directs (indices sensoriels) ou indirects (technologies de télédétection et apprentissage automatique), fournissent une boîte à outils flexible pour tester et appliquer le dégoût aux niveaux individuel et collectif. Dans cet article de revue/perspective, nous fournissons un cadre empirique pour tester la fonction adaptative du dégoût et les comportements associés d'évitement des maladies chez différentes espèces - des moins sociales aux plus sociales, et dans différents habitats. Nous prédisons divers compromis en fonction du système social et de l'écologie de l'espèce. Nous proposons cinq contextes dans lesquels les comportements d'évitement liés au dégoût pourraient être appliqués: la réhabilitation d'espèces menacées; les espèces envahissantes; les dommages aux cultures; les nuisibles urbains; et le tourisme animalier. Nous mettons en avant certaines perspectives et défis actuels de l'expérimentation sur le dégoût en milieu naturel. En particulier, nous recommandons la considération de plusieurs risques ensemble: maladie, prédation et compétition. Nous discutons également de l'éthique associée aux expériences sur le dégoût dans les contextes ci-dessus. Enfin, nous promouvons la création d'une base de données rassemblant les stratégies d'évitement des maladies chez les animaux et leurs applications.

Evolution of the uniformly white sclera in humans: critical updates.

The human eye characteristically has exposed and uniformly white sclera, which is hypothesized to have evolved to enhance eye-gaze signaling for conspecific communication. Although recent studies have put this hypothesis into question, current morphological and experimental evidence supports its key premise, albeit with recommendations for critical updates.

Head-tracking of freely-behaving pigeons in a motion-capture system reveals the selective use of visual field regions.

Using a motion-capture system and custom head-calibration methods, we reconstructed the head-centric view of freely behaving pigeons and examined how they orient their head when presented with various types of attention-getting objects at various relative locations. Pigeons predominantly employed their retinal specializations to view a visual target, namely their foveas projecting laterally (at an azimuth of ± 75°) into the horizon, and their visually-sensitive "red areas" projecting broadly into the lower-frontal visual field. Pigeons used their foveas to view any distant object while they used their red areas to view a nearby object on the ground (< 50 cm). Pigeons "fixated" a visual target with their foveas; the intervals between head-saccades were longer when the visual target was viewed by birds' foveas compared to when it was viewed by any other region. Furthermore, pigeons showed a weak preference to use their right eye to examine small objects distinctive in detailed features and their left eye to view threat-related or social stimuli. Despite the known difficulty in identifying where a bird is attending, we show that it is possible to estimate the visual attention of freely-behaving birds by tracking the projections of their retinal specializations in their visual field with cutting-edge methods.

Oxytocin and social gaze during a dominance categorization task in tufted capuchin monkeys.

Visual attention to facial features is an important way that group-living primate species gain knowledge about others. However, where this attention is focused on the face is influenced by contextual and social features, and emerging evidence in Pan species suggests that oxytocin, a hormone involved in forming and maintaining affiliative bonds among members of the same group, influences social attention as measured by eye gaze. Specifically, bonobos tend to focus on conspecifics' eyes when viewing two-dimensional images, whereas chimpanzees focus more on the edges of the face. Moreover, exogenous oxytocin, which was hypothesized to increase eye contact in both species, instead enhanced this existing difference. We follow up on this to (1) determine the degree to which this Pan pattern generalizes across highly social, cooperative non-ape primates and (2) explore the impact of exogenously administered vs. endogenously released oxytocin in impacting this behavior. To do so, we tracked gaze direction on a computerized social categorization task using conspecific faces in tufted capuchin monkeys (Sapajus [Cebus] apella) after (1) exogenously administering intranasal oxytocin using a nebulizer or (2) inducing an endogenous increase in oxytocin using fur-rubbing, previously validated to increase oxytocin in capuchins. Overall, we did not find a general tendency in the capuchins to look toward the eyes or mouth, but we found that oxytocin was related to looking behavior toward these regions, albeit not in a straightforward way. Considering frequency of looking per trial, monkeys were more likely to look at the eye region in the fur-rubbing condition as compared to either the saline or exogenous oxytocin conditions. However, in terms of duration of looking during trials in which they did look at the eye region, monkeys spent significantly less time looking at the eyes in both oxytocin conditions as compared to the saline condition. These results suggest that oxytocin did not necessarily enhance eye looking in capuchins, which is consistent with the results from Pan species, and that endogenous and exogenous oxytocin may behave differently in their effect on how social attention is allocated.

Testing the effect of oxytocin on social grooming in bonobos.

Oxytocin has attracted research attention due to its role in promoting social bonding. In bonobos and chimpanzees, the two species most closely related to humans, urinary oxytocin is known to correlate with key behaviours related to social bonding such as social grooming in chimpanzees and female-female sexual behaviour in bonobos. However, no study has demonstrated that the administration of oxytocin promotes real-life social interactions in Pan, leaving it unclear whether oxytocin is merely correlated with social behaviors or does affect them in these species. To test this, we administered nebulized oxytocin or saline placebo to a group of female bonobos and subsequently observed changes in their gross behavior during free interaction. We found an overall effect of more frequent grooming in the oxytocin condition. However, on the individual level this effect remained significant for only one participant in our follow-up models, suggesting future work should explore interindividual variation. Our results provide some experimental support for the biobehavioural feedback loop hypothesis, which posits that some functions of the oxytocin system support the formation and maintenance of social bonds through a positive feedback loop; however, further tests with a larger number of individuals are required. Our results, at a minimum, demonstrated that oxytocin affects spontaneous, naturalistic social interactions of at least some female bonobos, adding to accumulating evidence that oxytocin modulates complex social behaviors of Pan.

Oxytocin promotes species-relevant outgroup attention in bonobos and chimpanzees.

Previous research has found that oxytocin (OT) is associated with intergroup behaviour in humans as well as wild chimpanzees, and that exogenous OT affects Pan social attention. The two Pan species, bonobos and chimpanzees, differ drastically from one another in their intensity of intergroup competition, with lethal intergroup aggression often led by males in chimpanzees and more tolerant associations often centered around females in bonobos. However, it remains unclear how exogenous OT changes the two species' responses to ingroup and outgroup individuals. In this study, after intranasal administration of nebulized OT or placebo control, chimpanzees and bonobos viewed image pairs of ingroup and outgroup conspecifics while their eye movements were tracked with an eye-tracker. Although the overall effect of OT was small, we found that OT shifted bonobos' and chimpanzees' attention to outgroup images of the sex primarily involved in intergroup encounters in each species. Specifically, OT selectively shifted attention towards outgroup photos of female conspecifics in bonobos, and those of outgroup male conspecifics in chimpanzees. This suggests that OT generally promotes outgroup attention in both bonobos and chimpanzees but this effect is restricted to the sex most relevant in intergroup relations. These results suggest that, although OT may have a generally conserved role in hominid intergroup behaviour, it may act in species-relevant ways under the influence of their socio-ecological backgrounds.

Experimental evidence that uniformly white sclera enhances the visibility of eye-gaze direction in humans and chimpanzees.

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.

Do chimpanzees enjoy a virtual forest? A pilot investigation of the use of interactive art as a form of environmental enrichment for zoo-housed chimpanzees.

Environmental enrichment is essential for the well-being of zoo animals. Recent advances in sensor and video technologies may contribute to improvements in enrichment in terms of their flexibilities and time constraints. The purpose of this study was to investigate whether interactive movie art can be used as a form of environmental enrichment. We implemented interactive movies designed by a professional artist, a visual art aiming to reflect naturalistic forest habitat, in an indoor chimpanzee enclosure at Kyoto City Zoo in Japan. Motion-tracking sensors embedded in buoys were installed at several locations around the indoor enclosure; the chimpanzees could change the movie contents by physically interacting with these objects. We recorded behaviors by observing entire troop of chimpanzees (six) between March 16 and 20, 2020 (control condition), then recorded behaviors when the interactive movie was presented (experimental condition) between March 21 and 29, 2020. Behaviors were recorded via direct observations and video recordings to examine any changes after the installation of interactive art. The chimpanzees spent more time in the indoor enclosures during the experimental condition than during the control condition. Activity budgets did not change substantially during the study period. There was no evidence of habituation to the movie during the study period. Three chimpanzees, including two young chimpanzees, interacted with the movie more frequently than the others; these young chimpanzees occasionally showed playful expressions when interacting with the movie and exhibited different reactivities to the movie scenes. These results demonstrate, first, that the interactive art did not negatively affect chimpanzee behavior, and second, that some of the chimpanzees indeed showed positive responses to the art. This study, therefore, introduces a novel possibility for environmental enrichment in zoos, involving a collaboration between science and art.

Chimpanzees (Pan troglodytes) exhibit gaze bias for snakes upon hearing alarm calls.

Calls of several species of nonhuman animals are considered to be functionally referential. However, the cognitive mechanisms underlying audience behaviors remain unclear. This study used an audiovisual cross-modal preferential-looking paradigm to examine whether captive chimpanzees spontaneously associated a conspecific call with images of a corresponding item. Chimpanzees were presented with videos of snakes and fruit side-by-side while hearing playbacks of alarm calls, food-associated calls, or no sound (as a baseline condition). Chimpanzees looked at videos of snakes for longer when hearing alarm calls compared with food calls or baseline. However, chimpanzees did not look at videos of fruit for longer when hearing food calls compared with baseline. An additional experiment tested whether chimpanzees' gaze bias to the snake videos was driven by negative affective states in general via affect-driven attention biases. When chimpanzees were presented with the same snake and fruit videos while hearing playbacks of conspecific screams or no sound, they exhibited no gaze bias for snake videos. These results suggest that chimpanzees spontaneously associated alarm calls with images of a potential threat in a preferential-looking experiment and that this response was not simply driven by an affective state matching process. These findings should be interpreted in consideration of a procedural limitation related to pseudoreplication in the experimental stimuli. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Evolutionary foundations of knowledge and belief attribution in nonhuman primates.

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.

Erratum to "Bonobos and chimpanzees preferentially attend to familiar members of the dominant sex" [Animal Behaviour 177 (2021) 193-206].

[This corrects the article DOI: 10.1016/j.anbehav.2021.04.027.].

Divergent effects of oxytocin on eye contact in bonobos and chimpanzees.

Oxytocin has drawn significant research attention for its role in modulating mammalian social behavior. Despite generally conserved roles, oxytocin can function differently even in closely related species. Previous studies have shown that bonobos and chimpanzees, humans' two closest relatives, demonstrate considerable behavioral differences, including that bonobos look more at others' eyes than chimpanzees. Oxytocin is known to increase attention to another's eyes in many mammalian species (e.g. dogs, monkeys, and humans), yet this effect has not been tested in any nonhuman great ape species. This study examined how intranasally-administered oxytocin affects eye contact in bonobos and chimpanzees using eye tracking. Following administration of either oxytocin or saline control with a nebulizer, chimpanzees (n = 6) and bonobos (n = 5) were shown images of conspecific faces while their eye movement was recorded. Oxytocin changed the eye-looking behavior of bonobos and chimpanzees differently. We found that oxytocin increased eye contact in bonobos but not chimpanzees; while one chimpanzee showed an increase, interestingly, 5 out of 6 chimpanzees showed decreased looking to the eyes compared to the mouth, suggesting moderate eye avoidance. Given the importance of eye contact in their social interactions, our results suggest that oxytocin may play modulatory roles in bonobos' and chimpanzees' species-specific social behavior and underscore the importance of oxytocin in hominid social evolution.

The application of noninvasive, restraint-free eye-tracking methods for use with nonhuman primates.

Over the past 50 years there has been a strong interest in applying eye-tracking techniques to study a myriad of questions related to human and nonhuman primate psychological processes. Eye movements and fixations can provide qualitative and quantitative insights into cognitive processes of nonverbal populations such as nonhuman primates, clarifying the evolutionary, physiological, and representational underpinnings of human cognition. While early attempts at nonhuman primate eye tracking were relatively crude, later, more sophisticated and sensitive techniques required invasive protocols and the use of restraint. In the past decade, technology has advanced to a point where noninvasive eye-tracking techniques, developed for use with human participants, can be applied for use with nonhuman primates in a restraint-free manner. Here we review the corpus of recent studies (N=32) that take such an approach. Despite the growing interest in eye-tracking research, there is still little consensus on "best practices," both in terms of deploying test protocols or reporting methods and results. Therefore, we look to advances made in the field of developmental psychology, as well as our own collective experiences using eye trackers with nonhuman primates, to highlight key elements that researchers should consider when designing noninvasive restraint-free eye-tracking research protocols for use with nonhuman primates. Beyond promoting best practices for research protocols, we also outline an ideal approach for reporting such research and highlight future directions for the field.

Chimpanzees' (Pan troglodytes) internal arousal remains elevated if they cannot themselves help a conspecific.

Chimpanzees help conspecifics achieve their goals in instrumental situations, but neither their immediate motivation nor the evolutionary basis of their motivation is clear. In the current study, we gave chimpanzees the opportunity to instrumentally help a conspecific to obtain food. Following recent studies with human children, we measured their pupil diameter at various points in the process. Like young children, chimpanzees' pupil diameter decreased soon after they had helped. However, unlike children, chimpanzees' pupils remained more dilated upon watching a third party provide the needed help instead of them. Our interpretation is that chimpanzees are motivated to help others, and the evolutionary basis is direct or indirect reciprocity, as providing help oneself sets the conditions for a payback. This is in contrast to young children whose goal is to see others being helped-by whomever-presumably because their helping is not based on reciprocity. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Establishing an infrastructure for collaboration in primate cognition research.

Inferring the evolutionary history of cognitive abilities requires large and diverse samples. However, such samples are often beyond the reach of individual researchers or institutions, and studies are often limited to small numbers of species. Consequently, methodological and site-specific-differences across studies can limit comparisons between species. Here we introduce the ManyPrimates project, which addresses these challenges by providing a large-scale collaborative framework for comparative studies in primate cognition. To demonstrate the viability of the project we conducted a case study of short-term memory. In this initial study, we were able to include 176 individuals from 12 primate species housed at 11 sites across Africa, Asia, North America and Europe. All subjects were tested in a delayed-response task using consistent methodology across sites. Individuals could access food rewards by remembering the position of the hidden reward after a 0, 15, or 30-second delay. Overall, individuals performed better with shorter delays, as predicted by previous studies. Phylogenetic analysis revealed a strong phylogenetic signal for short-term memory. Although, with only 12 species, the validity of this analysis is limited, our initial results demonstrate the feasibility of a large, collaborative open-science project. We present the ManyPrimates project as an exciting opportunity to address open questions in primate cognition and behaviour with large, diverse datasets.

Great apes use self-experience to anticipate an agent's action in a false-belief test.

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.