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Eye gaze is an important source of information for animals, implicated in communication, cooperation, hunting and antipredator behaviour. Gaze perception and its cognitive underpinnings are much studied in primates, but the specific features that are used to estimate gaze can be difficult to isolate behaviourally. We photographed 13 laboratory-housed tufted capuchin monkeys ( Sapajus [Cebus] apella ) to quantify chromatic and achromatic contrasts between their iris, pupil, sclera and skin. We used colour vision models to quantify the degree to which capuchin eye gaze is discriminable to capuchins, their predators and their prey. We found that capuchins, regardless of their colour vision phenotype, as well as their predators, were capable of effectively discriminating capuchin gaze across ecologically relevant distances. Their prey, in contrast, were not capable of discriminating capuchin gaze, even under relatively ideal conditions. These results suggest that specific features of primate eyes can influence gaze perception, both within and across species.
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Chimpanzee (Pan troglodytes) gaze is conspicuous at ecologically-relevant distances
Abstract Chimpanzee ( Pan troglodytes ) sclera appear much darker than the white sclera of human eyes, to such a degree that the direction of chimpanzee gaze may be concealed from conspecifics. Recent debate surrounding this topic has produced mixed results, with some evidence suggesting that (1) primate gaze is indeed concealed from their conspecifics, and (2) gaze colouration is among the suite of traits that distinguish uniquely social and cooperative humans from other primates (the cooperative eye hypothesis). Using a visual modelling approach that properly accounts for specific-specific vision, we reexamined this topic to estimate the extent to which chimpanzee eye coloration is discriminable. We photographed the faces of captive chimpanzees and quantified the discriminability of their pupil, iris, sclera, and surrounding skin. We considered biases of cameras, lighting conditions, and commercial photography software along with primate visual acuity, colour sensitivity, and discrimination ability. Our visual modeling of chimpanzee eye coloration suggests that chimpanzee gaze is visible to conspecifics at a range of distances (within approximately 10 m) appropriate for many species-typical behaviours. We also found that chimpanzee gaze is discriminable to the visual system of primates that chimpanzees prey upon, Colobus monkeys. Chimpanzee sclera colour does not effectively conceal gaze, and we discuss this result with regard to the cooperative eye hypothesis, the evolution of primate eye colouration, and methodological best practices for future primate visual ecology research.
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- Award ID(s):
- 1926327
- PAR ID:
- 10339118
- Date Published:
- Journal Name:
- Scientific Reports
- Volume:
- 12
- Issue:
- 1
- ISSN:
- 2045-2322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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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.more » « less
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null (Ed.)The white sclera is important in facilitating gaze perception in humans. Iris color may likewise influence gaze perception but no previous studies have directly assessed its effect. We therefore examined how the interaction between sclera and iris color influences human gaze perception. We recorded the eye movements of human participants as they performed a visual search task with human faces exhibiting directed or averted gaze. The faces either exhibited light or dark irises. In addition, the faces had sclera that were depigmented (white) or pigmented (matched the color of the iris). We found that participants were quick and accurate in evaluating gaze regardless of iris color in faces with depigmented sclera. When the sclera were pigmented, participants were slower to evaluate the gaze of faces with both light and dark irises but these effects were most pronounced in the faces with dark irises. Furthermore, participants were generally less accurate in assessing faces with pigmented sclera when the irises were dark rather than light. Our results suggest that depigmented sclera are especially important for gaze perception in faces with dark irises. Because depigmented sclera likely evolved at a time when ancestral humans exhibited dark irises, the depigmented sclera may have been crucial for efficient and accurate gaze perception in ancestral humans.more » « less
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TBD (Ed.)Animal colouration is fundamentally important for social communication within conspecifics to advertising threat to competitors or fitness to possible mates. Social status and animal colouration are covarying traits that are plastic in response to dynamic environments. In the African cichlid,Astatotilapia burtoni, body colouration and behaviour have been extensively reported to vary with social rank. However, the nature of the interaction between these two traits is poorly understood. We hypothesise that pigmentation patterns could be linked to the behavioural repertoires underlying social status and can be resolved to regions on the cichlid body plan. To test this hypothesis, we generated Territorial (T) and Non-territorial (NT) males and employed computer vision tools to quantify and visualise patterns/colour enrichment associated with stereotyped T/NT male behaviour. We report colour-behaviour interactions localised in specific areas of the body and face for two colour morphs illustrating a more nuanced view of social behaviour and pigmentation. Since behavioural and morphological variation are key drivers of selection in the East African Great Rift Lakes, we surmise our data may be translatable to other cichlid lineages and underline the importance of trait covariance in sexual selection and male competition.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s41598-022-13273-3
