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.

Full text

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Chimpanzee (Pan troglodytes)
gaze is conspicuous
at ecologically‑relevant distances
Will Whitham1,2*, Steven J. Schapiro2, Jolyon Troscianko3 & Jessica L. Yorzinski1
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 conspecics. Recent debate
surrounding this topic has produced mixed results, with some evidence suggesting that (1) primate
gaze is indeed concealed from their conspecics, 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 specic‑specic vision, we
reexamined this topic to estimate the extent to which chimpanzee eye coloration is discriminable. We
photographed the faces of captive chimpanzees and quantied 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
conspecics 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 eectively 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.
e colours and patterns of primate faces are remarkably diverse, and are related to primate social ecology in
ways that suggest adaptive, communicative functions1. For example, more varied, complex, and colourful facial
patterning is most common in Old World primates that live in larger social groups2. Eye colours appear exemplary
of this relationship between morphology and social ecology. e sizes, shapes, and colours of primate eyes are
highly variable across species in ways that potentially aect their perceptibility and utility for communication3.
e cooperative eye hypothesis suggests that primate eyes are adapted to reveal or conceal gaze information4.
According to this hypothesis, lighter primate sclera, like those of humans, are discriminable, conspicuous, and
useful for gaze perception whereas darker primate sclera, like those of chimpanzees, are dark, obscured, and
camouaged in ways that impede gaze perception. e hypothesis suggests that these divergent phenotypes are
the product of evolutionary pressures to cooperate and communicate prosocially (with highly discriminable
gaze) or to avoid doing so (with eye colouration that conceals intraspecic cues), and that eye colouration thus
provides a window into the evolutionary history of primate social ecology. In support of this hypothesis, natural
human sclera colours are indeed highly perceptible, communicative cues. Newborn infants attend preferen-
tially to individuals who gaze directly at them5, and exhibit rudimentary gaze following6. By 18-months-of-age,
humans infants use gaze cues functionally to nd hidden items7. Human adults detect gaze information more
easily when sclera are naturally coloured, rather than darker or the same colour as the iris, across multiple light
environments8–10. e extent to which dark sclera in nonhuman primates are cryptic is less clear. Chimpanzees
have relatively dark sclera and follow the gaze of conspecics in their social group11 as well as the gaze of a com-
puterized conspecic on a computer monitor12. However, it is unclear in both of these cases whether chimpanzees
use conspecic eyes specically, rather than the head or body, to guide gaze following. More recent experimenta-
tion suggests that experimentally-enculturated chimpanzees are capable of discriminating computerized images
of averted chimpanzee eyes from images of chimpanzee eyes directed forward, albeit with less success than
when making the same discrimination of human eye images or chimpanzee eye images with reversed polarity13.
e cooperative eye hypothesis makes predictions about both primate eye colours and primate perception.
One approach to studying the cooperative eye hypothesis measures primate eye colours, then estimates whether
OPEN
1Department of Ecology and Conservation Biology, Texas A&M University, College Station, TX, USA. 2Department
of Comparative Medicine, UT MD Anderson Cancer Center, Bastrop, TX, USA. 3Centre for Ecology and
Conservation, University of Exeter, Exeter, UK. *email: wwhitham@tamu.edu
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primates are likely to distinguish among those colours. For example, evidence that a species’ iris colors are
highly discriminable from its sclera colors would suggest that the species is capable of using conspecic eyes as
an informative cue in its social ecology. To this end, recent research has sought to quantify ape eye morphology
using commercial photo-editing soware and archival or publicly available photographs to estimate the relative
conspicuousness of ape eye colours. Perea-García and colleagues reported that chimpanzee sclera are conspicu-
ous, counter to the predictions of the cooperative eye hypothesis14. Mearing and Koops failed to replicate this
result using the same method, reporting that chimpanzee and bonobo sclera are indeed cryptic15. Mearing and
colleagues went on to report that phylogenetic analyses of 15 primate species suggested that patterns of scleral
pigmentation (e.g., in chimpanzees) and depigmentation (e.g., in humans) were fundamentally related to spe-
cies sociality, and were most likely to be functional adaptations for social cooperation or competition16. Other
researchers have included the relative degree of scleral exposure, the width/height ratio of the eye, and other
morphological measurements into such analyses. Mayhew & Gómez reported that the averted gaze of gorillas
(Gorilla gorilla) reveals similar amounts of visible sclera as a human’s averted gaze, and is not heavily pigmented in
many individuals17. Caspar and colleagues quantied ocular pigmentation and eye morphology across 15 homi-
noid and reported three unique phenotypic clusters: one that was uniquely human (bright, exposed sclera), one
that included gibbons, siamangs, and chimpanzees (cryptic, hidden sclera), and one that included the remaining
apes (variable pigmentation and morphology with brighter, more exposed sclera than the second cluster)18. Kano
etal. performed sophisticated image analyses on images of seven great ape species and reported that whereas
human eye outlines and iris colours were much more visually distinct in humans than other apes, ape eyes are
broadly conspicuous rather than cryptic19.
Taken together, these studies demonstrate wide variability in eye morphology of primates, with uncertain
functional signicance. A key limitation of these studies (noted by19) is their omission of several key dimensions
of animal perception. In particular, dierent species have dierent capacities to discriminate colour (e.g., sclera
colours that are discriminable to human perception are not necessarily discriminable to other species) and to
resolve ne detail (e.g., a given sclera may be conspicuous up to 5m in one species but only up to 2m in another
species). And, all species’ ability to resolve ne detail decreases with increasing distance (e.g., sclera that are
conspicuous at 5m may be cryptic at 10m within a given species)20,21. Furthermore, photographs of unknown
origin and uncontrolled lighting conditions, and soware that are tuned for human perception, are poor ts
for empirical modeling of nonhuman animal perception22,23. Because any hypothesized relationship between
ape eye morphology and social cognition depends on a conspecic observer’s ability to perceive and act on any
cues the eye morphology produces, analyses that account for the unique perception of the observer species are a
necessary part of understanding any hypothetical selection pressures for primate gaze colouration. For example,
species-specic visual modeling reveals that the gaze colouration of a New World monkey species, Sapajus apella,
is uniquely suited for signaling to conspecics and prospective predators, but not to prey24.
We tested the cooperative eye hypothesis using modern tools for modeling the species-specic and distance-
dependent determinants of animal perception with colour calibrated photographs of chimpanzee faces. Speci-
cally, we tested whether a perceptual model based on the chimpanzee visual system can discriminate among the
colours of four regions of interest (ROIs) involved in perceiving gaze—chimpanzee iris, pupil, sclera, and skin
(Fig.1)—at simulated distances up to 16m. Because the relative perceptibility of chimpanzee gaze may also aect
chimpanzees’ facility in interspecic interactions, we also tested whether the visual phenotype of chimpanzees’
primate prey, the colobus monkey (genus Colobus), can perceive chimpanzee gaze information. In doing so, we
oer a more complete account of how chimpanzee eye colour is perceived by chimpanzees and other primates.
Results
Perceptual modeling suggests that the chromatic (color) information of chimpanzee iris, sclera, and pupil are
not discriminable from each other at any distance (∆S discriminability measure values at all distances < thresh-
old value 3), nor are they discriminable from chimpanzee face skin, for either species (Fig.2). e achromatic
(luminance) information of these same regions are discriminable from each other (∆S discriminability measure
values > threshold value 3) by both species. Using the lower-bound of the highest posterior density interval as
criteria for discrimination (see “Methods”), chimpanzees and colobus can discriminate the iris from the pupil
using achromatic information when they are less than approximately 7m and 6m away, respectively. Similarly,
chimpanzees can discriminate the sclera from the pupil, iris, or skin when they are approximately 20m, 24m,
and 29m away, respectively. And, colobus can discriminate the sclera from the pupil, iris, or hair when they are
approximately 21m, 16m, and 21m away, respectively. e ability of chimpanzees and colobus to discriminate
ROIs is similar because they have similar color sensitivities and acuity (see “Methods”).
Discussion
Using a visual modelling approach, regions of chimpanzee eyes relevant to gaze perception are discriminable
from each other and from surrounding skin to both chimpanzees and colobus. Some discriminations (iris versus
skin, and pupil versus skin) are dicult at any distance, while any discrimination involving chimpanzee sclera
is likely possible at distances of 10m or greater. While we do not know the specic facial regions that chimpan-
zees and colobus rely on to inform their gaze discriminations, our analyses suggest that they can use contrasts
between the sclera and pupil, iris or surrounding skin to evaluate gaze. is result conforms to previous research
in which human experimenters reliably identied chimpanzee gaze direction when they were within 10m of
the chimpanzees25. A 10–20m distance at which chimpanzee sclera are conspicuous is likely to have many con-
sequences for chimpanzee ecology. Many chimpanzee social behaviours—mating, ghting, grooming, feeding,
play—necessarily occur within this distance. Outside this distance, it may be adaptive for gaze information to be
more cryptic. Similarly, predators benet by having their gaze cues hidden as they approach prey, as many prey
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Figure1. Chimpanzee face. (a) A sample photograph of a chimpanzee. (b) Enlarged view of the regions of the
chimpanzee’s eye region. (c) Example ROIs for this photograph with pupil outlined in red, iris in blue, sclera in
green, and skin in yellow. We omitted highlights in the ocular media, like the visible reection of the sky, from
all ROIs.
Figure2. Chromatic and achromatic ∆S values for contrasts among the eye regions shaded in the top-right
inset. A ∆S value greater than 3 at some distance suggest that the two ROI can be discriminated from each other.
Shaded regions around lines are Bayesian 94% Highest Posterior Density intervals around ∆S estimates. Tick
intervals on the x-axis are log-scaled.
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species decide whether to remain in place or ee on the basis of predator gaze26–28. It would be adaptive for chim-
panzee gaze cues to remain indiscriminable to Colobus monkeys as the apes approach, but the 10–20m distance
at which Colobus may discriminate chimpanzee gaze is likely benecial to the monkeys. is dynamic perhaps
underpins chimpanzee strategies for hunting Colobus that rely on coordinated pursuit rather than ambush29.
It is also probable that other determinants, aside from gaze perception, contribute to the evolution of facial
colouration. e colours of primate hair and skin demonstrably vary with a primate’s native geography, cli-
mate, and diurnality; the relationship between these determinants and social ecology is inconsistent1,2,30. ese
non-social determinants of primate colour extend even to the regions immediately surrounding the eyes, with
some Neotropical primates exhibiting dark eye masks that likely function as defense from UV radiation1. A
phylogenetically-controlled analysis of eye colour across the primate order that uses proper animal colouration
techniques could provide evidence that primate eye colour is broadly adapted to its social ecology. e coopera-
tive eye hypothesis would be supported if lighter sclera colours were visible to conspecics or predators at greater
distances than darker sclera. Absent such evidence, hypotheses that lighter sclera colours are of great functional
signicance in intraspecic signaling, or that the evolution of human sclera suggests a uniquely hyper-cooperative
evolutionary trajectory relative to other primates, are unsupported by data from primate eye colours.
Primate eyes vary along several morphological continua, and this extensive variability accordingly yields
high variability in the contexts in which primate eyes and gaze directions are discriminable. Our study mod-
eled and emphasized the distance-dependent and species-specic nature of visual perception. Future research
may extend these techniques with additional context—of how perception of chimpanzee eye colours changes in
dierent lighting environments, or of how discriminable the amount of visible sclera available during species-
typical social interactions is likely to be. e cooperative eye hypothesis regards chimpanzee sclera as exemplary
of cryptic eye colouration. Our analyses, along with recent work on the topic13,14,19 conrm that this is not so to
the chimpanzee visual system, and oer substantive context using established tools for studying animal sensory
ecology. Additional studies will be necessary to experimentally determine whether chimpanzees can discriminate
gaze and at what distance they can make these discriminations, while accounting for their specic visual system.
Methods
Photograph collection. We photographed captive chimpanzees housed at e University of Texas’ MD
Anderson Cancer Center’s Michale E. Keeling Center for Comparative Medicine and Research in April and
May of 2021. All work was approved by the Institutional Animal Care and Use Committee at the Keeling Center
(IACUC approval number 0894-RN01), followed the guidelines of the Institute of Medicine on the use of chim-
panzees in research, complied with the Society for Neuroscience Policy on Ethics, and reported in accordance
with ARRIVE guidelines31. We used a Sony α7 II (ILCEm2) mirrorless digital camera (24 megapixel sensor) and
Sony lens with 70–350mm focal length for all photography. To standardize lighting as much as possible across
photographs we photographed animals outside at a distance of approximately 10m, in articial shade, only on
clear, sunny days (between 10:27 and 15:16) using the same aperture (f/6.3) and focal length (350mm) for all
photography. Because it was not feasible to place a photography reectance standard in the same lighting con-
ditions as unrestrained chimpanzees, we photographed a grey concrete region of the animals’ enclosure in the
same lighting as the animal moments aer taking each photograph of an animal (i.e., the sequential method32,33.
To identify the grey value appropriate for each concrete region of the animals’ enclosure, we took additional
photographs of the concrete alongside a 20% grey reectance standard (Spectralon). A total of 76 photos (11
chimpanzees, 1–23 photos per chimpanzee) were used for all analyses. Skin and iris ROIs were identiable in
every photograph, sclera ROIs were identiable in 73 photographs, and pupil ROIs were identiable in 23 pho-
tographs (due primarily to highlights in the ocular media masking pupil colouration).
Cone catch conversion and acuity correction. We used the micaToolbox (v.2.2.2) plugin for ImageJ
(v.1.53e) to transform the colour and luminance data of the RAW photographs (.ARW format) into forms rep-
resentative of chimpanzee and colobus colour vision22. Briey, a linearized set of pixel values was extracted
from each RAW photograph and normalized for dierences in lighting using the concrete grey standard photo-
graph taken immediately aer each chimpanzee photograph. en, the RGB sensitivities of our camera sensor
(included in a stock version of micaToolbox) were mapped to chimpanzee and colobus monkey colour sensitivi-
ties using a linear regression, resulting in pixel values representative of the animals’ colour vision phenotype.
We used the micaToolbox instantiation of AcuityView to transform photographs in ways representative of these
species’ vision at distances of 0.25, 0.5, 1, 2, 4, 8, and 16 m20,34; Fig.3). e parameters of chimpanzee and colobus
vision on which these operations are based, and relevant citations, are listed in Table1.
Receptor noise limited modeling. We used chromatic41 and achromatic42 receptor noise limited (RNL)
modeling procedures to estimate the discriminability of eye and face colours of the transformed chimpanzee
photographs. is modeling yields psychometric distances (∆S) among regions of interest (ROI) that predict
whether or not ROI are likely discriminable from each other. We used a conservative criterion of 3 ∆S through-
out, such that ∆S > 3 are likely discriminable. Additional parameters of chimpanzee and colobus vision on which
RNL depends are listed in Table1.
Statistical modeling. In order to quantify uncertainty around ∆S values, we used ∆S values to estimate
94% Highest Posterior Density intervals (HPD) using a Bayesian logistic regression with parameter estimates for
each ROI contrast, vision phenotype, and distance. ese HPD intervals estimate the likeliest 94% of values for
an ROI contrast, and act as an easily interpreted decision criteria: if an HPD estimate for an ROI contrast is less
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than or includes 3 ∆S, the ROI are plausibly not discriminable from each other. e regression also allowed for
inferences about the eect of distance beyond the range of values that were explicitly modeled using AcuityView.
Data availability
All data that were used as regression model input are publicly available in an OSF repository at https:// osf. io/
ap74f/? view_ only= 3da59 b82af 3d4a9 e9e4c 200b9 58c53 be.
Received: 17 February 2022; Accepted: 23 May 2022
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Acknowledgements
e research was supported by National Science Foundation (BCS #1926327), the College of Agriculture and
Life Sciences at Texas A&M University, and Texas A&M AgriLife Research funding to J.Y. and W.W.; and S.S.
were supported by the National Science Foundation funding (BCS #1926327).
Content courtesy of Springer Nature, terms of use apply. Rights reserved

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Vol.:(0123456789)
Scientic Reports | (2022) 12:9249 | https://doi.org/10.1038/s41598-022-13273-3
www.nature.com/scientificreports/
Author contributions
W.W.: data curation, formal analysis, investigation, methodology, soware, visualization, writing—original dra;
S.S.: funding acquisition, project administration, resources, supervision, writing—review and editing; J.T.: fund-
ing acquisition, methodology, soware, supervision, writing—review and editing; J.Y.: conceptualization, funding
acquisition, methodology, project administration, resources, supervision, writing—review and editing.
Competing interests
e authors declare no competing interests.
Additional information
Correspondence and requests for materials should be addressed to W.W.
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