Predator gaze captures both human and chimpanzee attention

Will Whitham; Bradley Karstadt; Nicola C Anderson; Walter F Bischof; Steven J Schapiro; Alan Kingstone; Richard Coss; Elina Birmingham; Jessica L Yorzinski

doi:10.1371/journal.pone.0311673

. 2024 Nov 21;19(11):e0311673. doi: 10.1371/journal.pone.0311673

Predator gaze captures both human and chimpanzee attention

Will Whitham ^1,^2,^#, Bradley Karstadt ^3,^#, Nicola C Anderson ⁴, Walter F Bischof ⁴, Steven J Schapiro ², Alan Kingstone ^4,^*, Richard Coss ⁵, Elina Birmingham ^3,^‡, Jessica L Yorzinski ^1,^‡

Editor: Nick Fogt⁶

PMCID: PMC11581262 PMID: 39570943

Abstract

Primates can rapidly detect potential predators and modify their behavior based on the level of risk. The gaze direction of predators is one feature that primates can use to assess risk levels: recognition of a predator’s direct stare indicates to prey that it has been detected and the level of risk is relatively high. Predation has likely shaped visual attention in primates to quickly assess the level of risk but we know little about the constellation of low-level (e.g., contrast, color) and higher-order (e.g., category membership, perceived threat) visual features that primates use to do so. We therefore presented human and chimpanzee (Pan troglodytes) participants with photographs of potential predators (lions) and prey (impala) while we recorded their overt attention with an eye-tracker. The gaze of the predators and prey was either directed or averted. We found that both humans and chimpanzees visually fixated the eyes of predators more than those of prey. In addition, they directed the most attention toward the eyes of directed (rather than averted) predators. Humans, but not chimpanzees, gazed at the eyes of the predators and prey more than other features. Importantly, low-level visual features of the predators and prey did not provide a good explanation of the observed gaze patterns.

1. Introduction

One of primates’ most advanced visual skills is the rapid processing of human and nonhuman animals. Because high acuity color vision, like that of most primates, transduces far more visual information than can be actively attended to, mechanisms that restrict and bias attention to those stimuli of high survival relevance can be understood as an adaptation with positive fitness consequences (e.g., [1, 2]). Indeed, adult humans are more proficient at detecting other humans and animals relative to inanimate objects (e.g., cars, trees) in complex natural scenes [1, 3, 4]. Likewise, human infants preferentially attend to animate items (e.g., police officers, lions), indicating that the prioritization of animacy emerges early on and is not learned [5]. It is even thought that this perceptual process is automatic in humans due to the tendency to look at animate objects even when they are irrelevant to the task [3, 6] and presented outside of conscious awareness [7].

These automatic attentional biases often involve stimuli of evolutionary consequence to primates. Human attention is often directed to threats, such as predators [8–10], hostile conspecifics [11], and dangerous objects [12]. Visual-search experiments have found that both human infants and adults are quicker to detect dangerous animals (e.g., snakes, spiders, lions) compared to non-dangerous animals [13–21]. Furthermore, [10] found that adults detected non-dangerous animals slower than dangerous animals because they spent more time looking at each of the dangerous (distractor) animals. Non-human primates exhibit attentional biases to animate stimuli, such as rhesus macaques’ (Macaca mulatta) and Japanese macaques’ (Macaca fuscata) vigilance to threatening versus non-threatening conspecific faces [22, 23], bonobos’ (Pan paniscus) distraction due to task-irrelevant conspecific faces and leopards [24], and several primate species’ biases to venomous animals like snakes (e.g., chimpanzees Pan troglodytes, gorillas Gorilla gorilla gorilla, and Japanese macaques: [25]; Japanese macaques: [26]; Japanese macaques: [27]). In many of these cases, the familiarity of the human participant or subject animal with any heterospecific animal stimuli was likely quite low (i.e., few encounters with real animals that would engender the attentional biases that were reported). These results have been taken to suggest that ancestral primates’ early experience with predators modified the visual system to quickly detect dangerous animals [28, 29]. Threat detection can be influenced by experience, with human participants faster to detect modern threats (e.g., guns, syringes) compared to neutral stimuli even though these threats are too recent to have impacted our evolutionary history [12, 13].

Faces are often studied for their capacity to capture and hold attention compared to other body parts. Recognition of a face-like image is indubitably innate in humans as evidenced by preterm infants orienting more toward an inverted triangular array of lights than an upright triangular array of lights [30]. Human faces are detected quicker and more accurately by human participants than nonhuman animal faces in parallel visual search tasks [31, 32]. When presented with images of human faces, people tend to fixate (look at) the internal features, with a particular focus on the eyes (e.g., [33–37]). In a similar vein, adult humans, especially those with high anxiety, are slower to disengage their attention when viewing angry faces compared to happy or neutral ones [38, 39]. This preference to fixate the eyes appears early on, often within the first fixation [40, 41]. Like humans, chimpanzees also show an initial bias to fixate the eyes of conspecifics, but spend less time looking at the eyes compared to other parts of the conspecific face and compared to humans’ gaze to eye regions [42, 43]. Bonobos, another great ape species, attend to conspecific eye regions to an even greater degree than do chimpanzees [44]. Humans and other primates may look at the eyes of others because eyes are powerful conveyors of social information, such as emotional and attentional states [45–47]. As a result gaze direction may also influence attention. Previous studies indicate that a staring gaze target was detected quicker among averted gaze distracters [48, 49], but see [50].

Proponents of a general face bias argue that it is essential for humans to prioritize animacy and faces alike given that ancestral humans had to be vigilant to both predators and other dangerous species as well as attentive to non-dangerous species, such as prey and domestic animals [1, 4, 31]. Although experimental research on the visual perception of animal faces in natural environments is limited, a handful of studies help to shed light on this area. For example, visibility of the head significantly improves the speed with which human participants detect animals in a visual search task, likely due to the expectation of a face [51]. Similarly, [52] found that forward-facing animals (i.e., animals facing towards the viewer) were more rapidly detected by adult humans than animals facing away and that forward-facing predators were more rapidly detected than forward-facing prey. These findings suggest that, as with human faces, the bias to attend to nonhuman animal faces is especially strong when direction of gaze is aimed toward the observer. Research has shown that most faces, and face-like configurations like those of pareidolia images, generally appear to capture attention in humans and other primates [53–55]. Such a bias may be understood as part of a larger system of biases to predators and prey, and conspecifics and heterospecifics, and eyes and other features; all related to discerning the relative agency and intention that motivates the behaviors of the organism to which attention is directed [56]. Only one investigation [57] provides direct experimental evidence of the shared bias to fixate eyes of humans and non-human animals alike. However, the animal images used by Yarbus were unnatural (e.g., a penciled sketch of a lion’s face, a photo of a gorilla sculpture) and it is therefore difficult to generalize the finding.

Many human studies present faces unnaturally (“passport-style”) with body features absent below the neck, precluding contextual interpretation. When presented in this manner, the eyes are a visually conspicuous part of the image with their highly contrasting colors relative to the rest of the face [58]. As a result, participants may look toward the eyes automatically because of low-level visually salient features, rather than looking toward the eyes because of high-level social meaning or scene comprehension [59–61]. To test this hypothesis, [40] presented humans with complex real-world scenes containing one to three people and compared participants’ initial fixations against the salience model using the Salience Toolbox [62]. The salience model operates by creating and combining several topographic feature maps (e.g., changes in intensity, color, and edge orientation) into one final salience map coding for conspicuous (i.e., salient) scene locations. [40] found that, even though participants’ initial fixations frequently landed on the head and eyes, salience at the head and eye regions were lower than what would be expected by chance. Using the same salience model, [51] demonstrated that pictures of animals in complex natural environments also have comparatively low salience. Thus, bottom-up processing does not appear to accurately describe eye movements in complex real-world scenes containing humans or nonhuman animals.

The present study was an initial exploration of how both humans (Experiment 1) and chimpanzees (Pan troglodytes; Experiment 2) attend to images of a species with prototypical predator features (lions) and images of a species with more prototypical prey features (impala). We did not make specific predictions about any divergent patterns of gaze behavior for humans and chimpanzees, and the two experiments are successive attempts with different species to identify the attentional biases reviewed above. Experiment 2 was not motivated by extant primate behavioral ecology per se. Mature male lions (images of which acted as the prototypical predators for these experiments) have little hunting responsibility, share little overlap with extant chimpanzee populations in either geography or habitat, and are not known to regularly interact with chimpanzees in any natural context. Likewise, chimpanzees do not hunt impala. Instead, Experiment 2 was designed as an assay of primate attentional biases to the prototypical features described above and to the social signaling of directed and averted eyes. We anticipated a degree of attention to lion images from the chimpanzees in this study, since savanna-living chimpanzees in Tanzania treat lions as a predation threat and alarm call vigorously when they see or hear them [63], but our design was not structured to assess this particular bias (e.g., of lion features versus those of other big cats). Note also that impala images, while having characteristics of many prey features, are also not necessarily “neutral” images given the entwined evolutionary histories of ancestral primates and impala. As such the impala images function in these experiments as images without characteristic predator features, and without features that should engender any conserved attentional bias related to threatening stimuli, but not as images without any evolutionary consequence.

We tested four predictions for anticipated patterns of gaze behavior of humans and chimpanzees to images of lions and impala. Three of our predictions were related to the anticipated response of humans and chimpanzees to the prototypically predatory features of the lion (e.g., forward-facing eyes, robust body) and the prototypically preyed-upon features of the impala (e.g., laterally-placed eyes). First, we predicted that participants would look at predators more than prey. Second, we predicted that the eyes of predators and prey would be the most fixated region in a natural image. Third, we predicted that fixations to the eyes will be influenced by both animal type (predator or prey) and the gaze direction of the animal. Given the importance of eyes for signifying threat for a variety of primates, including chimpanzees and humans [64–67], we expected that eyes of forward-facing predators will receive more fixations than the eyes of averted-facing predators, whereas fixations to the eyes of prey will not increase with direct gaze.

Our final prediction is related to the predictive power of visual brightness, contrast, color, and other low-level stimulus features (hereafter: salience). For our previous predictions, we assumed that any differences in patterns of gaze behavior among the predator and prey images and among the different regions of interest are due to differences in the way that the human or chimpanzee represents the content of the image. That is, we expect that gaze behaviors are caused by something about the lion being a lion, and the impala being an impala, and the orientation of the eyes. However, a more conservative hypothesis for research of this kind is always that any differences in gaze behavior are due to differences in visual salience. Effectively testing our first three predictions required testing whether our pattern of results could instead be understood as a consequence of, for example, some uniquely salient visual feature of a lion’s physiognomy, like the color and contrast introduced by a mane. We used the Salience Toolbox [62] to compute salience maps based on the low-level visual features of each image, and to test our prediction that human and chimpanzee gaze behaviors to our stimuli would not be predicted by salience information in the images alone.

To test these predictions, we presented humans (Experiment 1) and chimpanzees (Experiment 2) with 96 complex natural scenes that contained either one female impala (a prototypical prey) or one male lion (a prototypical predator). The animals in these scenes were all fully visible, doing nothing except standing in an upright posture and forward-facing (i.e., toward the observer) or averted-facing (i.e., away from the observer). Gaze behaviors were recorded as humans and chimpanzees viewed the animal images.

2. Experiment 1

2.1 Materials and methods

2.1.1 Participants

Thirty-three undergraduate students from the University of British Columbia ranging in age between 19 and 27 years (M = 19.61, SD = 1.66; 28 females) participated in this study between January and March 2020. Ethnicity was reported as 55% Chinese, 9% Caucasian, 9% Indian, 9% East Asian, 6% Arab, 6% Korean, 3% Mexican, and 3% African. All had normal or corrected-to-normal vision and were naïve to the purpose of the experiment. Each participant received course credit for participation, and written, informed consent was acquired from every participant prior to their participation in the study. This experiment was approved by the University of British Columbia’s Institutional Review Board (#H10-00527).

2.1.2 Apparatus

Eye movements were recorded at 1000Hz using a desktop mounted EyeLink 1000 Plus tracking system (SR Research, Canada). The online saccade detector of the eye tracker was set to detect saccades with an amplitude of at least 0.1°, using an acceleration threshold of 8000°/s² and a velocity threshold of 30°/s. Average accuracy of the tracker is typically within 0.25° and 0.5°.

2.1.3 Procedure

All participants completed two tasks: ’Free-view task’ and ‘Danger Rating task’. In the Free-view task, participants were instructed to simply look at the stimuli while being eye tracked. In the Danger Rating task, participants were instructed to look at and rate (see below) how dangerous the animal appeared, while being eye-tracked. Task order was counterbalanced across participants. Each block of both the Free-view task and Danger Rating task presented 96 images (24 lions with direct gaze, 24 lions with averted gaze, 24 impalas with direct gaze, 24 impalas with averted gaze) and lasted approximately 10 minutes. Images were randomised within each task without replacement. The eye tracker was recalibrated between blocks.

Participants sat in a brightly lit room and were placed in a chinrest so that they sat approximately 50 cm from the display computer screen. Before the experiment, a 9-point eye movement calibration procedure was conducted. Participants were instructed to fixate a central black dot, and to then fixate it again when it appeared at each of nine different locations on the screen. This calibration was then validated, a procedure that calculates the difference between the calibrated gaze position and target position and corrects for this error in future gaze position computations. After successful calibration and validation, the trials began.

At the beginning of each trial, a fixation point was displayed in the centre of the computer screen to correct for drift in gaze position. Participants were instructed to fixate this point and then press the spacebar to start a trial. One of 96 photographs was then shown in the centre of the screen and remained visible until 8 sec had lapsed. Note that this meant that when an image first appeared, the initial central fixation (which was discarded from analysis) landed approximately on the centre of the body of an animal. In the Free-view task, participants received no further instructions, and the image display was replaced with the drift correction screen after the 8 s. In the Danger Rating task, participants were asked to use a keyboard number pad to rate how dangerous the animal appeared (on an interval scale of 1–5 using the full range of the scale, with 1 being “Not dangerous at all” and 5 being “Extremely dangerous”). After indicating their response, the image display was then replaced with the drift correction screen. This process repeated until all images had been viewed. The participants therefore viewed each photograph twice (once in the Free-view task and once in the Danger Rating task). We found no main effects or interaction effects for task nor task order (p > .05), so we pooled the data from these two tasks to create a single data set. Because no significant differences in gaze behavior were observed between Danger Rating and Free View conditions, we did not incorporate the ratings into additional analyses. Danger Rating scores were higher for lions than impala, and higher for directed animals than averted (ps < .05).

2.1.4 Stimuli

Color digital photographs depicting lions and impala were obtained from online sources (Fig 1A). Each of the 96 photographs displayed either a male lion or a female impala. Half of the images contained animals with direct gaze and half with averted gaze. The direct-gaze images displayed animals with their eyes and heads oriented toward the camera; the averted-gaze images displayed animals with their eyes and heads looking to the side. The bodies of the animals were orientated with their sides partly or completely visible; due to limitations in available photographs, it was not possible to standardize the exact body orientation. The image backgrounds included plants, rocks, ground, or sky. In addition, in half of the averted-gaze images, the animals were facing to the left and in the other half, to the right. Regions of Interest (ROIs) were created in DataViewer (SR Research, Canada) using rectangles for the eye regions and freehand polygons for the head and body regions (Fig 1B). Photographs filled the entire screen (1024 x 768 pixels) of the eye-tracker monitor.

2.1.5 Eye-tracking analysis

We defined the following ROIs: eyes (the portion of the head around, and including, the eyes of the animal), heads (the remaining portion of the head of the animal), body (including torso and legs but excluding eyes and head), and background (everything else, see Fig 1B). These ROIs were all within the margin of error for tracker accuracy. To determine which ROIs were of most interest to participants, we computed area-normalized fixation proportions by first dividing the number of fixations for a region by the region’s area to create a normalized fixation count value; and then created a normalized fixation proportion value for each region by dividing the normalized count value for that given region by the sum of all the normalized count values across all regions [33, 34]. Use of area-normalized fixation proportions controls for potential confounds such as absolute ROI size differences or differences in the ratio of the size of one ROI to another within and across conditions, and have the advantage of incorporating gaze behaviors and ROI size into one dependent measure for further analyses.

To determine how participants first observed the visual scene, we examined the initial fixation made by participants, defined as the first fixation after making a saccade from the central fixation dot (i.e., fixation #2). Initial fixation proportions were calculated as the number of initial fixations in each region for one trial type (e.g., impala averted) divided by the total number of initial fixations for all regions in that same trial type. Initial fixation proportions were not area-normalized.

2.1.6 Salience analysis

The Salience Toolbox developed by [62] enabled the measurement of the visual salience of an image via strong changes in intensity, color and local orientation. To remain as consistent as possible with others using this toolbox, we used all default parameters. The final salience maps were scaled to the same size as the original fixation analysis (1024 x 768 pixels) using bilinear interpolation. Examples of scenes, their regions, and corresponding salience maps are shown in Fig 1. Salience values were normalized to a range of 0 (not salient) to 1 (very salient). As visual salience has been hypothesized to have its greatest impact on the first saccade [68, 69], we focused our analysis on the first fixation made by participants after making a saccade from drift correction cross. We computed the average salience of fixated scene locations and compared this value to two control values. The first control value was the average salience of random locations sampled uniformly from the image (called ‘‘uniform-random”). To control for the known bias to fixate the lower central regions of scenes [70], the second control value was the average salience of random locations sampled from the smoothed probability distribution of all first-fixation locations from participants’ eye movement data across all scenes (called ‘‘biased-random”). These comparisons allowed us to determine whether the salience model accounted for first fixation position above what would be expected by chance.

2.2 Experiment 1 results

2.2.1 Statistical analysis

First, to determine if participants displayed a general bias for fixating predators versus backgrounds, we aggregated normalized fixation proportions by region into a singular interest area for the whole animal (Section 2.2.2 Animals versus backgrounds). We performed a 2 (stimulus species: lion vs. impala) x 2 (region: animal or background) within-subjects analysis of variance (ANOVA). Second, to determine whether participants directed their gaze toward specific regions of the animals, we submitted all the normalized fixation proportion data to a 2 (stimulus species: lion vs. impala) x 2 (gaze direction: directed vs. averted) x 4 (ROI: eyes, head, body, background) within-subjects ANOVA (Section 2.2.3 Specific animal ROIs). Third, to assess whether participants directed their initial gaze toward specific regions of the animals, we performed another 2 (stimulus species: lion vs. impala) x 2 (gaze direction: directed vs. averted) x 4 (ROI: eyes, head, body, background) within-subjects ANOVA on the initial fixation proportion data (Section 2.2.4 Initial fixations on animals). We performed a comprehensive series of a priori contrasts to test our predictions–of differences between directed and averted gaze within and across each ROI and within and across each species.

2.2.2 Animals versus backgrounds

Participants rarely fixated the background, with normalized fixation proportions to lions (M = .993, SD = .011, CI = .993-.994) and impalas (M = .990, SD = .015, CI = .989-.990) greater than .99. Therefore, although the stimulus species x region interaction was significant, F_1.35,43.21 = 50.9, p < .001, the lack of variability renders interpretation inappropriate.

2.2.3 Specific animal ROIs

A significant three-way interaction among stimulus species, gaze direction, and ROI suggested that the overall effects of ROI and gaze direction on gaze behavior were affected by the stimulus species presented in the image (Fig 2, Table 1). As such, we reported and interpreted planned contrasts tailored to our specific predictions. Participants fixated the eyes of lions and impalas more than their heads (lion: p < .001; impala: p < .001) and bodies (lion: p < .001; impala: p < .001). Participants fixated lion eyes significantly more than the impala eyes (p < .001) and directed lions eyes significantly more than averted lion eyes (p < .001), but fixated directed and averted impala eyes in similar proportions (p = .021).

Fig 2 — Horizontal lines indicate statistically significant planned contrasts.

Table 1. The effect of stimulus species, gaze direction, and ROI on the normalized fixation proportions in Experiment 1.

Asterisks indicate statistically significant variables or comparisons.

Overall Model
	Factor	F _{df,df error}	p
	Stimulus species	0_1,32	>0.99
	Gaze direction	0_1,32	>0.99
	ROI	280.82_{1.08, 34.54}	< .001*
	Stimulus species* Gaze direction	0_1,32	>0.99
	Stimulus species* ROI	50.90_{1.35, 43.21}	< .001*
	Gaze direction*ROI	22.14_{1.21, 38.63}	< .001*
	Stimulus species* Gaze direction* ROI	54.19_{1.16, 37.19}	< .001*
Comparisons
	Lion
	Eyes Directed vs. Eyes Averted		< .001*
	Head Directed vs. Head Averted		< .001*
	Body Directed vs. Body Averted		.001*
	Eyes vs. Head		< .001*
	Eyes vs. Body		< .001*
	Eyes vs. Background		< .001*
	Impala
	Eyes Directed vs. Eyes Averted		.021
	Head Directed vs. Head Averted		< .001*
	Body Directed vs. Body Averted		.036
	Eyes vs. Head		< .001*
	Eyes vs. Body		< .001*
	Eyes vs. Background		< .001*
	Eyes
	Lion vs. Impala		< .001*
	Head
	Lion vs. Impala		< .001*
	Body
	Lion vs. Impala		.063

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2.2.4 Initial fixations on animals

Participants were more likely to initially fixate the eyes of lions than their heads (p < .001) but they initially fixated the eyes of impala in similar proportions as their heads (p = .44). Similar to the pattern of results for normalized fixation proportions, participants initially fixated the directed lion eyes at higher proportions than the averted lion eyes (p < .001) and they initially fixated the lion eyes more than the impala eyes (p < .001). Gaze direction had no effect on initial fixations to impala eyes, (p = .32; Table 2; Fig 3).

Table 2. The effect of stimulus species, gaze direction, and ROI on the initial fixation proportions.

Asterisks indicate statistically significant variables or comparisons.

Overall Model
	Factor	F _{df,df error}	p
	Stimulus species	0_1,32	>0.99
	Gaze direction	0_1,32	>0.99
	ROI	58.54_{1.43, 45.78}	< .001*
	Stimulus species* Gaze direction	0_1,32	>0.99
	Stimulus species* ROI	31.67_{1.98, 63.38}	< .001*
	Gaze direction*ROI	15.60_{2.33, 74.66}	< .001*
	Stimulus species* Gaze direction* ROI	19.25_{1.60, 51.09}	< .001*
Comparisons
	Lion
	Eyes Directed vs. Eyes Averted		< .001*
	Head Directed vs. Head Averted		< .001*
	Body Directed vs. Body Averted		.82
	Eyes vs. Head		< .001*
	Eyes vs. Body		< .001*
	Eyes vs. Background		< .001*
	Impala
	Eyes Directed vs. Eyes Averted		.32
	Head Directed vs. Head Averted		.002*
	Body Directed vs. Body Averted		.002*
	Eyes vs. Head		.44
	Eyes vs. Body		< .001*
	Eyes vs. Background		< .001*
	Eyes
	Lion vs. Impala		< .001*
	Head
	Lion vs. Impala		.27
	Body
	Lion vs. Impala		< .001*

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Fig 3 — Horizontal lines indicate statistically significant planned contrasts.

2.2.5 Salience analysis

The salience at the location of first fixation was compared to the two chance-based estimates described earlier (uniform-random and biased-random). To determine whether the salience model accounted for first fixation position above what would be expected by chance, non-parametric statistics (Mann–Whitney U tests) were performed to compare the medians of fixated salience and uniform-random salience as well as the medians of fixated salience and biased-random salience, with an alpha level of .05. The fixated salience was very low (0.023), as was uniform-random saliency (0.013), U-test fixation salience vs uniform-random salience: z = 1.645, p = 0.100. Fixated saliency was also no different from biased-random saliency (0.018; U-test fixation saliency vs biased-random saliency: z = 0.596, p = 0.55). Thus, the salience at fixated locations was no higher than would be expected by the random models.

2.2.6 Three-way interaction comparisons

Because the significant three-way interaction among stimulus species, gaze direction, and ROI presented in Table 1 above suggests the presence of significant effects beyond the planned contrasts that were targeted to our specific hypotheses, we conducted unplanned, exploratory, post hoc comparisons of the full matrix of three-way contrasts. Bonferroni-adjusted p values suggest significant differences in area-normalized fixation proportions between most combinations of the three factors. For example, as an extension of our third prediction regarding the joint influences of stimulus species and gaze direction towards eye ROIs, the three-way comparisons suggest that directed lion eyes are significantly greater than not only averted lion eyes, but also every other combination of the three factors (all p < .001). The complete matrix of post hoc comparisons is available in S1 Fig and S1 Table. Note that the proportional nature of this measure makes some inferences from lower priority ROIs fraught: an increase in fixations on directed lion eyes, for example, necessarily leads to a harmonic decrease in the fixation proportions to directed lion bodies, heads, and backgrounds.

2.3 Experiment 1 discussion

We aimed to test four main predictions related to how humans attend to nonhuman animals, particularly predators and prey. First, drawing from earlier research suggesting an attentional priority to threatening animals [10, 13, 15, 17], we predicted that participants would generally look at lions more than impala. Because participants gazed nearly exclusively at both lion and impala (and rarely gazed at the background), we could not examine this hypothesis.

Second, we predicted that the eyes of non-human animals would be the most fixated region in natural images. The eyes of both lions and impala were fixated by participants significantly more than the heads, bodies, and background. Initial fixation data also suggested a strong bias for gaze information by human participants: they were more likely to initially fixate the eyes and heads of animals over any other region. These results dovetail with previous literature demonstrating an early and robust preference to fixate the eyes of other people [33, 34, 57], although it should be noted that patterns of gaze behavior to conspecific and heterospecific targets may involve different attentional mechanisms [71]. Viewing patterns were also consistent with previous eye-tracking experiments using animal line illustrations as stimuli [57].

Third, we predicted that fixations of the eyes of nonhuman animals would be influenced by both stimulus species (predator or prey) and the gaze direction of the animal. In support of this prediction, we found that the eyes of lions were looked at significantly more than the eyes of impala. Moreover, we found that the eyes of forward-facing lions were fixated significantly more often (i.e., in normalized fixation proportions) and earlier (i.e., in initial fixations) than the eyes of averted-facing lions in both the humans. Previous studies have reported that forward-facing predators are detected faster relative to averted-facing predators [52]. Our results extend these findings by suggesting that it is the eyes of forward-facing predators, in particular, that may be driving this effect.

Finally, we predicted that bottom-up processing would not account for gaze patterns while viewing animals. Our results showed that the low-level markers of visual saliency we measured using the Salience Toolbox [62] offered a weak explanation for the data. Instead, it appears that attention is likely directed toward the eyes of animals as a result of their importance in assessing risk.

3. Experiment 2

3.1 Experiment 2 methods

3.1.1 Participants

Seven group-housed adult common chimpanzees (4 females and 3 males; aged 29–51 years, M = 41 years) at The University of Texas MD Anderson Cancer Center’s Michale E. Keeling Center for Comparative Medicine and Research participated in this experiment between August and October 2022. Two of the chimpanzees (Sandy, Simba) were born in the wild in regions distant from savannas or lion habitats. The other five chimpanzees (Bo, Chechekul, Lulu, Mandy, and Punch) were born in captivity.

Chimpanzees participated in the research voluntarily, choosing to interact with the experimenter and apparatus at their sole discretion. Both during experimental sessions and at all other times the chimpanzees had full access to indoor areas, outdoor areas, conspecifics (2–4 for each chimpanzee in this experiment), food (fresh fruits, vegetables, and commercial primate chow), clean water, and enrichment. These chimpanzees were highly familiar with humans and cognitive-behavioral tasks, although previous exposure to computers and eye-trackers was minimal. The chimpanzees exhibited no signs of distress during the experiment. All research was approved by the Institutional Animal Care and Use Committee of the Keeling Center (IACUC # 0894-RN01) and Texas A&M University (IACUC # 2022–0089 EX), followed the guidelines of the Institute of Medicine on the use of chimpanzees in research, complied with the Society for Neuroscience Policy on Ethics, and reported in accordance with ARRIVE guidelines.

3.1.2 Apparatus

The Tobii TX300 eye-tracker (with built-in monitor) was used for all chimpanzee testing. To properly position the eye-tracker in front of the steel mesh of the animals’ enclosures, we affixed the eye-tracker to a rolling utility cart at roughly the height of a sitting, adult chimpanzee (approximately 70 cm). To incentivize the chimpanzees to properly position themselves at the eye-tracker, we affixed a polycarbonate panel connected to a peristaltic dosing pump to the mesh to reward chimpanzees with fruit-flavored, sugar-free drink mix (hereafter: juice) for their participation in the experiment (S2 Fig). Python software was used to control stimulus presentation (via the pygame library), eye-tracker data collection (via Tobii’s Python Software Development Kit), and the juice pump (via a USB relay controlled with Python’s serial module). We applied the noise-robust fixation classification algorithm I2MC [72] to classify chimpanzee gaze data as fixations or saccades; this fixation filter is robust to noise and data loss.

3.1.3 Procedure

Chimpanzees completed this experiment in the indoor portion of their normal housing between 12:00 and 15:00. To calibrate the eye-tracker before each experimental session, we prepared a custom shaping and 2-point calibration procedure. First, chimpanzees were rewarded with juice for looking at any location on the monitor while the monitor was displaying a large (1080 x 1080 pixels) video. These were publicly available videos of monkeys feeding or playing, selected to attract chimpanzee gaze to the screen (downloaded from pixabay.com). Next, chimpanzees were rewarded only for sustaining gaze to the video for at least 400 msec, and the video incrementally decreased in size until it was sufficiently small to act as a calibration point (300 x 300 pixels). Finally, the primate video moved to the upper-right and then the lower-left quadrants of the screen (or vice versa) to calibrate the chimpanzee’s gaze at these two points according to the calibration thresholds set by Tobii’s 2-point calibration procedure. For experienced chimpanzees, this calibration process took a few minutes. Based on our validation procedure (S1 File), the accuracy of the eye-tracker using chimpanzee subjects was approximately 1.5° (this level of accuracy is similar to other eye-tracking studies using chimpanzees [42]).

After calibration, chimpanzees were presented with their first trial. A central fixation cross appeared. If the chimpanzee fixated within 100 pixels of this point for a duration of >50 ms, the software automatically presented one of the lion or impala stimuli for 3 sec. This duration was shorter than the 8 sec stimulus presentations of Experiment 1 and was instead the duration used in many previous great ape eye-tracking experiments (e.g., [44, 73–77]). While the image was onscreen, the dosing pump dispensed juice rewards continuously to the chimpanzee as long as their gaze remained onscreen. Although several reward schedules have been used in ape eye-tracking designs (e.g., every 3 seconds of activity [78]; at the start of trials, [74]), continuous juice rewards were both more appropriate for testing animals in their home enclosures (alongside conspecifics, husbandry staff, other experimenters, and a highly-enriched captive setting) and unlikely to engender specific biases of gaze behavior (e.g., to directed lion heads but averted impala backgrounds). The apes were not explicitly trained to view the stimuli in any way.

At the conclusion of the trial, the fixation screen returned to prompt the chimpanzee to begin the next trial. To minimize any biasing effects of the chimpanzees’ environment (e.g., groupmates, activity in nearby chimpanzee groups, human experimenter or caretaker vocalizations or behaviors), each of the 96 images was shown to each chimpanzee four times in randomized order (thus, each chimpanzee viewed 384 images). If the chimpanzee did not gaze onscreen for at least 10% of a trial duration, the trial was omitted from the analysis and the trial was repeated later in the session. Stimulus presentations were randomized. Because the chimpanzees were in control of each eye-tracking session’s duration, some chimpanzees finished all trials in a single day whereas other chimpanzees took as many as 4 days to complete testing.

3.1.4 Stimuli

The same set of 96 digital images of male lions and female impala were used in Experiment 2. Because of differences in screen resolution between the human (1024 x 768 pixels) and chimpanzee (1920 x 1080 pixels) eye-tracker monitors, the photographs were presented slightly differently between experiments. In particular, whereas the photographs filled the entire screen (1024 x 768 pixels) in the experiments with human subjects the photographs were centered and nearly filled the entire screen (1600 x 1080 pixels) for the experiments with the chimpanzee subjects.

3.1.5 Eye-tracking analysis

Eye-tracking analyses were the same as in Experiment 1.

3.1.6 Salience analysis

Salience analysis were the same as in Experiment 1, this time using chimpanzee fixation data to calculate median salience at fixation and the two control variables (uniform-random salience and biased-random salience).

3.2 Experiment 2 results

3.2.1 Statistical analysis

Statistical analyses were the same as in Experiment 1. All analyses were performed for the human and chimpanzee data because the experimental designs were not identical. Because fixation duration is more typically used as the dependent measure in eye-tracking designs with nonhuman primates, alternative analyses with fixation durations are presented in Supplemental Analyses S4 Fig.

3.2.2 Animals versus backgrounds

Chimpanzee gaze behaviors were biased to lions (M = .91, SD = .10; 95% CI = .84-.98) and impala (M = .84, SD = .14; 95% CI = .74-.94) versus the image backgrounds, stimulus species x region F_1,6 = 27.57, p = .002. Chimpanzees fixation proportions to the lions relative to their backgrounds were significantly higher than fixation proportions to impala relative to their backgrounds (p < .001).

3.2.3 Specific animal ROIs

Due to a significant three-way interaction among stimulus species, gaze direction, and ROI we reported and interpreted planned contrasts tailored to our specific predictions (Fig 4, Table 3). Chimpanzees fixated the eyes at similar proportions to heads and bodies of lions (eyes vs. heads: p = .95; eyes vs. bodies: p = .17) and fixated the eyes of impalas at similar proportions to their heads (p = .71), but fixated impala eyes less than their bodies (p < .001). fixated the eyes of lions and impalas more than their heads (lion: p < .001; impala: p < .001) and bodies (lion: p < .001; impala: p < .001). Chimpanzees fixated lion eyes significantly more than the impala eyes (p < .001) and directed lions eyes significantly more than averted lion eyes (p < .001), but fixated directed and averted impala eyes in similar proportions (p = .47). These effects were generally consistent across the gaze behaviors of individual chimpanzees (S3 Fig), and were maintained when area-normalized fixation duration was taken as the dependent variable instead of area-normalized fixation counts used in these results (S4 Fig).

Fig 4 — Horizontal lines indicate statistically significant planned contrasts.

Table 3. The effect of stimulus species, gaze direction, and ROI on the normalized fixation proportions in Experiment 2.

Asterisks indicate statistically significant variables or comparisons.

Overall Model
	Factor	F _{df,df error}	p
	Stimulus species	0_1,6	>0.99
	Gaze direction	0_1,6	>0.99
	ROI	6.88_{1.71, 10.25}	.02
	Stimulus species* Gaze direction	0_1,6	>0.99
	Stimulus species* ROI	25.63_{3, 18}	< .001*
	Gaze direction*ROI	16.44_{3, 18}	< .001*
	Stimulus species* Gaze direction* ROI	8.59_{3, 18}	< .001*
Comparisons
	Lion
	Eyes Directed vs. Eyes Averted		< .001*
	Head Directed vs. Head Averted		.25
	Body Directed vs. Body Averted		< .001*
	Eyes vs. Head		.95
	Eyes vs. Body		.17
	Eyes vs. Background		< .001*
	Impala
	Eyes Directed vs. Eyes Averted		.47
	Head Directed vs. Head Averted		.14
	Body Directed vs. Body Averted		.90
	Eyes vs. Head		.71
	Eyes vs. Body		< .001*
	Eyes vs. Background		.81
	Eyes
	Lion vs. Impala		< .001*
	Head
	Lion vs. Impala		< .001*
	Body
	Lion vs. Impala		< .001*

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3.2.4 Initial fixations on animals

Chimpanzees initially fixated the eyes of lions at lower proportions compared to their heads (p < .001), but also initially fixated the eyes of impala in similar proportions to their heads (p = .67). Chimpanzees initially fixated the directed lion eyes at higher proportions than the averted lion eyes (p = .002) and they initially fixated the lion eyes more than the impala eyes (chimpanzees: p = .03). Gaze direction had no effect on initial fixations to impala eyes p = .89; see Table 4; Fig 5).

Table 4. The effect of stimulus species, gaze direction, and ROI on the initial fixation proportions in Experiment 2.

Asterisks indicate statistically significant variables or comparisons.

Overall Model
	Factor	F _{df,df error}	p
	Stimulus species	0_{1, 6}	>0.99
	Gaze direction	0_{1, 6}	>0.99
	ROI	97.93_{3, 18}	< .001*
	Stimulus species* Gaze direction	0_{1, 6}	>0.99
	Stimulus species* ROI	55.93_{3, 18}	< .001*
	Gaze direction*ROI	8.95_{3, 18}	< .001*
	Stimulus species* Gaze direction* ROI	15.63_{3, 18}	< .001*
Comparisons
	Lion
	Eyes Directed vs. Eyes Averted		.002*
	Head Directed vs. Head Averted		< .001*
	Body Directed vs. Body Averted		.07
	Eyes vs. Head		< .001*
	Eyes vs. Body		< .001*
	Eyes vs. Background		< .001*
	Impala
	Eyes Directed vs. Eyes Averted		.89
	Head Directed vs. Head Averted		.64
	Body Directed vs. Body Averted		.07
	Eyes vs. Head		.67
	Eyes vs. Body		< .001*
	Eyes vs. Background		< .001*
	Eyes
	Lion vs. Impala		.03
	Head
	Lion vs. Impala		< .001*
	Body
	Lion vs. Impala		.18

Open in a new tab

Fig 5 — Horizontal lines indicate statistically significant planned contrasts.

3.2.5 Salience analysis

As in Experiment 1, fixated salience was very low (0.017), as was uniform-random saliency (0.013); U-test fixation salience vs. uniform-random salience: z = 1.788, p = 0.074. Fixated salience was also no different from biased-random saliency (0.019; U-test fixation saliency vs biased-random saliency: 0.869, z = -0.165). Thus, the salience at locations fixated by the chimpanzees was no higher than would be expected by the random models.

3.2.6 Three-way interaction comparisons

As in Experiment 1, the significant three-way interaction among stimulus species, gaze direction, and ROI suggests significant additional effects beyond those of the planned contrasts of our explicit hypotheses. Bonferroni-corrected p values over the complete matrix of post hoc comparisons again suggest that directed lion eyes were the target of greater fixation proportions than averted lion eyes (p < .001) as well as directed lion heads (p < .05), bodies (p < .001), or backgrounds (p < .001). The complete matrix of post hoc comparisons is available in S5 Fig and S2 Table.

3.3 Experiment 2 general discussion

Experiment 2 tested in chimpanzees the same four predictions for anticipated patterns of gaze behavior to lion and impala eyes and faces with directed or averted orientations as were tested in humans in Experiment 1. First, we predicted that chimpanzees would look more at lions than impala and found that they reliably looked more at lions than at impala (versus their backgrounds). This result supports our first prediction and contributes to previous work suggesting an attentional bias for dangerous animals [10, 20, 79].

Second, we predicted that chimpanzees would fixate the heterospecific eyes more than any other region. Chimpanzees did not exhibit these gaze patterns. The chimpanzees did not fixate the eyes of the lions and impalas more than their heads and bodies, nor were their initial fixations biased toward the eyes. Although this prediction was not supported, it coheres with previous research with nonhuman primates that suggests less intense bias(es) to conspecific and heterospecific eyes in great apes, especially chimpanzees [78].

Third, we predicted that fixations to the lion and impala images would be influenced by the animal type and the gaze direction of the animal. This prediction was broadly supported: lion eyes were more fixated than impala eyes, and forward-facing lion eyes were fixated at higher proportions of overall fixations and initial fixations than the averted-facing lion eyes. Although chimpanzees were not as attentive to eyes overall (prediction 2), they nevertheless attended to eyes, predators, and orientation in ways that suggest broad biases to forward-facing predators like those that have been previously reported in other eye-tracking designs with humans [52] and a special role for visible eyes in these biases. That this pattern of attention to animal eyes extended to naïve chimpanzees without prior exposure to lions, impala, or images of predators (with the possible exception of the two wild-caught chimpanzees) further emphasizes the more evolutionarily-conserved, goal-directed nature of attention to predators and prey.

Finally, salience modeling did not suggest that chimpanzee gaze behaviors can be understood as a mere recapitulation of biases to low-level stimulus features.

4. Discussion

Eyes are a rich source of information that can convey the level of threat posed by potentially dangerous predators [80, 81]. Across two designs with humans and chimpanzees, we tested several predictions about attentional biases to eyes of prototypical predators (male lions) and prototypical prey (female impala). Our predictions about the gaze patterns of the chimpanzees generally matched those of the humans in ways that replicate and extend what is currently known about the attentional priorities of primates. Chimpanzees attended more to lions than impala (supporting prediction 1) and attended to the eyes of forward-facing lions more than the eyes of averted lions (supporting prediction 3) in a way seemingly divorced from low-level stimulus information (supporting prediction 4). To our knowledge, these experiments provide some of the first evidence examining the strength of the bias towards visually fixating the eyes of heterospecific nonhuman animals in both human and chimpanzee participants.

Several design considerations complicate such direct comparison between the patterns of gaze behavior of humans and chimpanzees. Chimpanzees were exposed to multiple repetitions of the images, in shorter durations, among other typical compromises of working with the laboratory-housed population (e.g., nearby conspecifics, juice rewards, specific hardware/software). In addition, human participants were familiarized to lions by semantic learning, popular media, and lived experience (e.g., a trip to the zoo) in a way that the chimpanzees were not. For example, a major discrepancy between chimpanzee and human gaze patterns was of overall attention to eyes (prediction 2), which were the most fixated region for humans but not for chimpanzees. One possibility is that the chimpanzees disengaged attention from the eyes to explore the rest of the images more fully compared with the human participants (as in [42, 74]) or, as referenced above, it may be that humans’ prior learning and enculturation (e.g., already knowing what an impala looks like) biased their gaze behavior away from what the chimpanzees were likely attending to for the first time. Whether this sort of discrepancy should be understood as species difference, design difference, difference in enculturation, or some confluence of all of the above cannot be adequately answered using only the pair of experiments we presented and represents a target for future research.

In addition to narrowing the eye-tracking design differences between the two species, future research might measure similar attentional biases in other primate species, like bonobos, which have a similar evolutionary history to chimpanzees but have previously demonstrated divergent patterns of attention to conspecific faces [78]. Future designs may also test the prediction of attentional biases to images of dangerous animals by presenting them alongside images of less dangerous animals, using a preferential viewing design, and present a larger diversity of predator and non-predator species to better describe the features of heterospecific animals that elicit these attentional biases in primates.

In conclusion, both humans and chimpanzees exhibited a strong preference for visually fixating the eyes of forward-facing predators. Because the salience modeling predicted that low-level, visually salient features would produce very different gaze patterns than those produced by either the human or chimpanzee participants, low-level features are a weak explanation for the observed viewing patterns. Although previous learning about lions and their behaviors could have led human participants to look to the lions’ eyes and faces, the chimpanzees were naïve to images of lions, had no such learning, and nevertheless looked to lion eyes in ways that distinctly yet equivalently accorded with our predictions. Instead, a more likely explanation for our results could be that humans and chimpanzees fixate the two facing eyes of animals in ways that reflect their visual properties due to the adaptive significance of assessing the focal interests of these animals and their likelihood of posing significant threats.

Supporting information

S1 File. The procedure for validating chimpanzee eye-tracker calibrations.

(DOCX)

pone.0311673.s001.docx^{(57.4KB, docx)}

S1 Table. p values for post hoc comparison matrix for Experiment 1.

(DOCX)

pone.0311673.s002.docx^{(20.1KB, docx)}

S2 Table. p values for post hoc comparison matrix for Experiment 2.

(DOCX)

pone.0311673.s003.docx^{(20.2KB, docx)}

S1 Fig. Post hoc comparison matrix for Experiment 1.

(DOCX)

pone.0311673.s004.docx^{(105.4KB, docx)}

S2 Fig. The apparatus used for testing chimpanzee subjects.

(A) the eye-tracker and all associated hardware positioned on a rolling cart approximately 63 cm from the chimpanzee mesh, and (B) an overhead view of a chimpanzee participating in the experiment. Photograph taken by WW and printed under a CC BY license.

(DOCX)

pone.0311673.s005.docx^{(576.2KB, docx)}

S3 Fig. Area-normalized fixation proportions for individual chimpanzee subjects.

(DOCX)

pone.0311673.s006.docx^{(87.1KB, docx)}

S4 Fig. Supplemental analyses.

Fixation duration plotted as a function of stimulus species, gaze direction and ROI for chimpanzee subjects.

(DOCX)

pone.0311673.s007.docx^{(47KB, docx)}

S5 Fig. Post hoc comparison matrix for Experiment 2.

(DOCX)

pone.0311673.s008.docx^{(105.5KB, docx)}

Data Availability

All data files used in these analyses are available from the Open Science Framework database (DOI 10.17605/OSF.IO/WHSNE).

Funding Statement

This work was supported by the National Science Foundation (BCS #1926327) to W.W., S.S., and J.Y., Natural Sciences and Engineering Research Council of Canada (RGPIN-2022-03079) to B.K., N.A., and A.K the funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0311673.r001

Decision Letter 0

Nick Fogt

20 Feb 2024

PONE-D-23-40092Predator gaze captures both human and chimpanzee attentionPLOS ONE

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Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: No

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Reviewer #1: This is an interesting and well-written manuscript about a topic that has not attracted much prior research and as such is welcomed. There were however some important deficiencies in theoretical justification and experimental design (or insufficient explanation) that need to be addressed. Perhaps the authors have already thought through and solved many of these, but the reasoning should be included in the manuscript for readers to follow all points of their logic.

Major concerns:

The paper refers throughout to predator and prey gaze, but tests only lion and impala with no other species. This seriously limits the generalizability of their conclusions. This is compounded by fairly weak justification of species choice. It is true lions co-occur with eastern chimpanzees in some narrow savannah regions where chimpanzees are likely hunted to at least some extent, but most captive chimpanzees, and presumably the current population, are western chimpanzees. Beyond subspecies differences, most chimpanzees live in forest environments. For both of these reasons, leopards are much more ecologically relevant and indeed have been found to predate chimpanzees across their range more than has been reported for lions. Further, the stimuli examples appeared to show male lions, who do not typically engage in much of the hunting, and lions further are group-hunters (not solitary as are leopards) and only one individual at a time was presented. While the big cat morphology may be a form that is relatively conserved, and predates upon many primates across the world including humans and chimpanzees, the text only makes a very vague association with one species in one part of a different subspecies’ range. I recommend justifying this point in the text, that we may expect conserved attentional biases to come through across big cat morphologies including the lions used in this study. Relatedly, on the other side, chimpanzees are proficient hunters themselves but do not hunt impala. Duikers, squirrels, red colobus monkeys, would all be more species-relevant prey to a chimpanzee, why was impala chosen? This should also be mentioned when discussing why human attention may differ from other species. Chimpanzees, like humans, are both predators are prey to different animals, but the stimuli only included species that are predator and prey to humans. It is thus not really a fair species comparison. The discussion certainly should mention the lack of species diversity as a limitation on generalizability and future direction, even moreso in light of these larger concerns.

The inclusion of the saliency maps felt a little out of place and I did not find them integrated into the rest of the discussion. Some introductions of their actual use and predictive power in the introduction would be of use. As of now, they are introduced only in ways they fail to predict gaze, and then the results again fail to find them making new predictions, and the naïve reader is left wondering what these can contribute if they consistently fail to make predictions.

The hypotheses are quite vague and not well-justified, which combined with a very high number of statistical tests leads readers to wonder if this was more exploratory or hypothesis-driven. Both are welcomed, especially with new topics such as this, but perhaps the manuscript could benefit from distinguishing them and making clearer, concrete predictions associated with the actual hypotheses (ideally with citation). In particular, the first set of predictions (paragraph starting line 131) is essentially just sameness or difference, but then no statistical tests actually directly compared the two species. The lack of direct human-chimpanzee comparison is a strange choice. The reasoning of the sentence starting on line 135 is especially vague and nebulous. If these were the topics of interest wouldn’t a study comparing humans with different background knowledge and social contexts be a more salient test? The choice of a cross-species framework here could be much better-justified.

The dependent measure as proportion of fixation is very unusual compared to previous great ape work. Why was total fixation duration not included? What reasoning is there for choosing number of fixations over duration, especially considering prior work consistently showing chimpanzee gaze is likely to jump around more than humans. Could the lion have evoked more glances away (chimpanzees tend to avoid prolonged direct eye contact) while the averted gaze and impala had longer but more consistent gaze? At the very least, supplemental analysis detailing the duration should be included somewhere.

Minor concerns:

Line 87: The topic of chimpanzees seems to come out of nowhere here. As they are central to the whole paper, their introduction should be naturally connected. Perhaps a linking phrase of paragraph about the value and perspective around comparative gaze studies of chimpanzees would help improve this and address one of the major comments above?

Line 87: This finding itself also needs more rigour if chimpanzee attention to faces is a central focus of the paper. The previous studies find that chimpanzees gaze more at mouth than eyes even within faces, and this has been considered as potentially more species-relevant for social cues than eyes (Kano et al. 2018, Brooks et al 2021). Did the authors consider looking at attention to mouth by species given this finding? At the very least, the difference in the role and meaning of eye-contact across species should be mentioned. Note also that the supplemental material of some of these previous face-based studies have looked at attention to direct compared to averted gaze, which while not directly on the topic of predator/prey gaze may be useful for the authors to look at.

Line 116: This is a bit of a strange citation here, as the point of the sentence is that eyes have high saliency in the face but the cited paper is on the topic of that not being at all universal, and certainly is not a citation about them being “presented in this manner.”

Line 139: This whole paragraph does not distinguish species for the predictions. Maybe the authors intend these predictions to apply to all participants, but this should then be made explicit.

Line 161: The ethnicity states Chinese, Korean, and east Asian as distinct, please check this or clarify.

Throughout: “other part of the head” may be clearer than just head when distinguishing from eyes, since in some sentences this could easily be lost by readers.

Several times: It may be a bit inaccurate to say we couldn’t look at lion-impala differences in humans because of high attention to both. It would be more accurate to say no differences were observed because of ceiling effects, or the data was not suited for a formal model because of ceiling effects but visually appeared identical. Saying both were at ceiling is a comparison itself.

Line 430: “To our knowledge, this experiment provides some of the first evidence examining the strength of the bias towards visually fixating the eyes of nonhuman animals in both human and chimpanzee participants.” This sentence must be rephrased or removed. The prior sentence cites Kano et al. 2018, which compared several primate species including humans on social attention. Also, the nonhuman animals point is somewhat missed here if talking about nonhuman participants, maybe allospecific would be more relevant.

General: the size of the eye ROIs appears very small in the figure, especially considering the screen size used. Are these within the margin of error of accuracy? This should be mentioned.

Line 443: Chimpanzees are one of the nearest relatives, bonobos are equally closely related. Bonobos generally look much more to eyes than chimpanzees (Kano et al. 2018) and have no lions in their range (but do also face leopard predation) and are less proficient hunters. Perhaps a future comparative approach can be highlighted as a future direction?

Line 444: check divergence dates.

General: the discussion could use more interpretation and connection to the broader literature, as it stands it is hard to see what the importance beyond restatement of the results.

One point not raised anywhere in the manuscript that certainly bears discussion: predators have more forward-facing eyes than prey. Could you rule out the fact that there is a general direct eye-gaze bias, but that the lions just have more direct gaze (at least from the view of primates such as ourselves with forward-facing eyes) and it is therefore not related to predator/prey distinctions per se?

How do you account for the fact that the relative eye size between the two species is different? The eyes of the impala appear to be a much bigger proportion of the head than lions. Perhaps this strengthens the finding, but it bears discussion.

It is rare in eye-tracking with great apes to use a mesh rather than transparent barrier between eyes and screens. Can you be sure this did not affect gaze tracking when one or the other eye is blocked to the sensor?

Similarly, juice only being delivered while gaze is onscreen seems very odd. How can you be sure their behaviour was not simply shaped by perceived rewarding of certain gaze? Generally, juice is used to motivate them to join experiments, but rewards that are differentially delivered according to gaze is a slippery slope if aiming to target spontaneous gaze patterns.

How did attention change across/within trials? The trials seem longer than typical in chimpanzee research, was there any obvious effect of presentation order?

Was there consistency across individuals tested within species? This would strengthen the finding considerably given the low sample size.

There are several citation errors. Ensure the reference section matches the main text (e.g. Carter et al. wrong year, Kano et al. 2018 not in reference section).

Reviewer #2: GENERAL COMMENTS

In this study, Karstadt & Whitham et al. investigate how attentional patterns in humans and chimpanzees are influenced by predation. Utilising eye-tracking technology, they examined how features of potential predator and prey species affect attention, and how the gaze of the target animal modulates this phenomenon. This study is significant as our understanding of attentional mechanisms in response to predators and prey across different species remains limited. I would like to express my gratitude to the authors for their diligent efforts and for presenting a well-written and clear manuscript. I believe it is suitable for publication pending the below suggestions for improving the paper. Firstly, I believe that incorporating additional primate studies would complement the human research and comparative aspect of the manuscript. Secondly, I have some inquiries regarding the data processing and statistical analysis, which I will outline below. I hope these suggestions are constructive and beneficial for the authors.

ABSTRACT

L29: It is not fully clear here what you mean with 'visual features'. Does this include the gaze orientation, or the low-level features which you discuss later on.

L32: “The gaze of the predators and prey”

INTRODUCTION

- Because both human and non-human studies are addressed, it is important to mention this more explicitly. It is currently not always clear (e.g. L52)

- From the first paragraph in the introduction it should be clear to the reader that attention is a limited cognitive capacity, and that this explains why attention is selected for relevant stimuli, e.g. animate objects.

- Throughout the manuscript it is not really discussed that the prey is not necessarily a neutral animal, as (ancestral) humans hunt(ed) these species, making humans both a predator and a prey. Similar arguments can be made for chimpanzees.

- Within the introduction there is a mix between eye contact with conspecifics and heterospecifics for which we can expect different attentional and motivational systems. Barrett 2015 has written a chapter that explains this nicely: Barrett, H. C. (2015). Adaptations to predators and prey. The handbook of evolutionary psychology, 200-223. This chapter can be useful in general as they touch on the topic of forward-facing eyes of predators (p 208).

L67: You could strengthen your argument here by mentioning that it is likely that for most participants in these studies these are innate responses as they probably have never encountered such animals in real life (unless you have information about the exposure of the humans to lions).

L68-71: I think this sentence can be removed as it is focusing on conspecific interactions, which are fundamentally different from predator-prey interactions.

L73: I think there is a number of primate papers that are missing that would strengthen this argument, especially since you are comparing human and chimpanzees.

The following paper found evidence for attention biases in bonobos for leopards:

Laméris, D. W., Verspeek, J., Eens, M., & Stevens, J. M. G. (2022). Social and nonsocial stimuli alter the performance of bonobos during a pictorial emotional Stroop task. American Journal of Primatology, 84(2), e23356. https://doi.org/10.1002/ajp.23356

The following papers report attention biases for poisonous animals (e.g., snakes)

Masataka, N., Koda, H., Atsumi, T., Satoh, M., & Lipp, O. V. (2018).

Preferential attentional engagement drives attentional bias to snakes in Japanese macaques (Macaca fuscata) and humans (Homo sapiens). Scientific Reports, 8(1), 17773. https://doi.org/10.1038/s41598-018-36108-6

Hopper, L.M., Allritz, M., Egelkamp, C. L., Huskisson, S.M., Jacobson, S. L., Leinwand, J. G., & Ross, S. R. (2021). A comparative perspective on three primate species’ responses to a pictorial emotional stroop task. Animals, 11(3), 588. https://doi.org/10.3390/ani11030588

Shibasaki, M., & Kawai, N. (2009). Rapid detection of snakes by japanese monkeys (Macaca fuscata): an evolutionarily predisposed visual system. Journal of Comparative Psychology, 123(2), 131–135. https://doi.org/10.1037/a0015095

L77: Replace 'new' with 'recent'

L87-89: I feel Kano et al. (2015) is missing here. They report that bonobos, as compared to chimpanzees, pay more attention to eye regions.

Kano, F., Hirata, S., & Call, J. (2015). Social attention in the two species of pan: Bonobos make more eye contact than chimpanzees. PLoS ONE, 10(6). https://doi.org/10.1371/journal.pone.0129684

L89-91: Please highlight that this is likely more true between conspecifics, whereas the current paper is focusing on heterospecifics

L92: Please see Tomonaga & Imura (2015) DOI: 10.1038/srep11437

L97-100: I think it's debated whether the attention bias for snakes/spiders is due to their face. For example, in snakes the shape and presence of the scales drive responses (https://doi.org/10.1111/psyp.12564 and Kawai, N., & Kawai, N. (2019). Searching for the Critical Features of Snakes. The Fear of Snakes: Evolutionary and Psychobiological Perspectives on Our Innate Fear, 121-153.) Please rephrase this sentence.

L137: "or other alternative hypotheses" This is unclear, what do you exactly mean?

L138: Please elaborate on other reasons why chimpanzees would not show similar attentional biases? There is literature on pareidolia effects in primates that can be useful to discuss whether or not you would expect similar results.

METHODS

- Eye-tracking Analysis: I understand that for ape studies the trial duration is preferably shorter than for human studies. However, for a more fair comparison of the two species I would think you can make the argument to only analyse the first 3s of the human data. An extension of 5s is significantly long to capture additional attentional processes. I realise this might be a lot to request, and perhaps I am missing the rationale of why you looked at the full 8s human trials, but as you are comparing humans with chimpanzees I would expect a more similar study design.

L158: Please report whether students provided consent

L174: It is not fully clear if both the Free-view task and Danger Rating task consisted of 96 images. Please clarify. Did the two tasks use the same images?

I see now that you later discuss this at L199. Perhaps to avoid confusion you can mention this earlier?

L202-204: But did the human participants rate the lions are more dangerous than the impalas?

L212-214: Is the original range of the two wild-born chimpanzees known? Where they actually savanna dwelling chimpanzees?

L264-267: If a first trial was deemed successful, were subsequent repeated trials still included in the analysis? There could be a risk of habituation effects. This could be something you can additionally test to ensure whether or not this occurred.

L281: Please highlight that you used pictures of female impalas, as earlier mentioned in L149

L281: I appreciate the author's efforts into finding this large number of different stimuli as it can be challenging to collect sufficient suitable stimuli. I think it would increase transparency if you mention whether you aimed to control for background features, or body orientation of the animals. E.g. for directed images the animal can be approaching the camera, facing the viewer, or can walk parallel to the camera but turn its head towards the camera (e.g. the two impala images in Figure 1). I'm aware that you partially corrected for this difference in ROI area in the processing, but it would benefit the reader if this information is provided.

L300: As you are analysing initial fixations it is really important that you report how the fixation cross proceeded. For the human study this is more controlled as the participants decided themselves when they continued, but for the chimpanzees this is not clearly reported. Was this manually done, after an Xms duration or when the chimpanzee was fixating at the cross. Eye-tracker systems vary in how this can be achieved. Additionally, did you verify whether the participants were in fact focusing on the fixation cross?

Statistical analysis: I would like to ask for the rational to go for ANOVAs over mixed models. Did the data meet the assumptions for an ANOVA (homogeneity of variance, normality). I was under the impression that ANOVAs are typically not suitable for proportional data, especially when there are a lot of extreme values (0 or 100 in this case). Wouldn't a mixed model with an appropriate distribution be better? This way you would be able to control for number of trial repetitions for example.

L328: Please mention what these a priori contrasts were

RESULTS

- In my opinion, the Results section would improve by clearly mentioning the model which is being discussed. So either, label the different models (model 1, model 2, model 3) in the "statistical analysis" and present the results in this way. Or perhaps better, present the results in terms of the predictions. Because you use one model for multiple predictions, this can create some confusion of what is actually being discussed.

- My understanding is that in a significant three-way interaction, looking at significant two-way interaction effects can be misleading, or incomplete, as the three-way interaction suggests that the two-way interaction depends on the third variable. Given that you report a significant three-way interaction for both humans and chimpanzees, I'm not fully convinced that the two-way interactions you report are meaningful. I'm aware that looking at two-way interactions can be meaningful in certain cases, but if you think this applies to your results I think it would be good practice to explicitly mention this. For example, you report that there is a difference in fixation proportion for the impala and lion eyes (L355-356), however, when looking at Figure 2 there appears a modulating effect of the gaze direction for the lion stimuli that possibly explains this effect. You discuss this in the lines after, but in reporting your results you jump between mentioning the three-way and two-way effects which is confusing. Given the presence of the three-way interaction I think it is more appropriate to report the significant effects and then focus on the insignificant contrasts within that three-way interaction, rather than the significant two-way interactions.

- Is there a reason why you did not directly test if the (initial) fixation proportion was associated with the saliency of the ROI? To me this would provide more reliable evidence that gaze patterns were not influenced by such low-level features.

DISCUSSION

- Throughout the discussion I'm missing discussion that humans have arguably different relationships with lions/impalas than (captive) chimpanzees. For example, lions are typically considered charismatic species that are highly favoured to see in zoos or safaris. This is not to say that this necessarily drove your results (especially as you found very similar results between humans and chimpanzees), but I would like to see more discussion on how the difference in results between the species can be explained

- I'm missing a more detailed discussion into why the chimpanzees seemed to fixated more on the impala bodies. Could it be that you find similar results in humans when you focus on the first 3 seconds?

L415: Please highlight again that this partly supports the first prediction (which included both humans and chimpanzees) as you could only test this for the chimpanzees. Additionally, perhaps you can make suggestions as how future studies can test this in a better way (i.e., avoiding ceiling effects as found with the human participants). E.g., showing impala and leopard pictures at the same time.

L422-424: Please highlight that gaze patterns for conspecifics can be different from those for heterospecifics. Guo et al. 2019 (https://doi.org/10.1007/s00221-019-05574-3) comes to mind that reports some work on this.

L431: Please highlight that this is mostly for nonhuman heterospecific animals as there are multiple studies that report this when using conspecific stimuli.

L433: For example, this statement is based on the two-way interaction whereas Figure 2 suggests a three-way interaction. Here you would need to report if the humans and chimpanzees also fixated more on the averted lion eyes than the averted impala eyes.

L445-451: This paragraph is not very convincing in explaining why the saliency analyses show that bottom-up processing does not account for the gaze patterns. If this is mostly based on the fact that the differences in saliency do not align with the differences in gaze patterns, I do not think this is sufficient to exclude bottom-up processing

L457-459: Kano 2009 (doi:10.1098/rspb.2008.1811) and Kano 2011 (DOI 10.1007/s10071-011-0422-5) can be useful here where they report that chimpanzees after faster fixation rates than humans

L459: Please change 'is' to 'could be'

L466-468: This is just a little confusing because you look at both 3- and 2-way interactions which result in somewhat contrasting results

REFERENCES

- Kano et al. 2018 (L429) is missing from the reference list

- Please add the year in Yorzinski L669

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Reviewer #2: No

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PLoS One. 2024 Nov 21;19(11):e0311673. doi: 10.1371/journal.pone.0311673.r002

Author response to Decision Letter 0

11 Apr 2024

Note that our complete response to reviewers is both included below and uploaded as a Word document in our submission materials.

Reviewer #1 comments

R1C1 :: This is an interesting and well-written manuscript about a topic that has not attracted much prior research and as such is welcomed. There were however some important deficiencies in theoretical justification and experimental design (or insufficient explanation) that need to be addressed. Perhaps the authors have already thought through and solved many of these, but the reasoning should be included in the manuscript for readers to follow all points of their logic.

Response :: We thank the reviewer for their constructive review of the manuscript and for giving us the opportunity to present a more clearly reasoned, easier-to-follow manuscript.

Major concerns:

R1C2 :: The paper refers throughout to predator and prey gaze, but tests only lion and impala with no other species. This seriously limits the generalizability of their conclusions. This is compounded by fairly weak justification of species choice. It is true lions co-occur with eastern chimpanzees in some narrow savannah regions where chimpanzees are likely hunted to at least some extent, but most captive chimpanzees, and presumably the current population, are western chimpanzees. Beyond subspecies differences, most chimpanzees live in forest environments. For both of these reasons, leopards are much more ecologically relevant and indeed have been found to predate chimpanzees across their range more than has been reported for lions. Further, the stimuli examples appeared to show male lions, who do not typically engage in much of the hunting, and lions further are group-hunters (not solitary as are leopards) and only one individual at a time was presented. While the big cat morphology may be a form that is relatively conserved, and predates upon many primates across the world including humans and chimpanzees, the text only makes a very vague association with one species in one part of a different subspecies’ range. I recommend justifying this point in the text, that we may expect conserved attentional biases to come through across big cat morphologies including the lions used in this study. Relatedly, on the other side, chimpanzees are proficient hunters themselves but do not hunt impala. Duikers, squirrels, red colobus monkeys, would all be more species-relevant prey to a chimpanzee, why was impala chosen? This should also be mentioned when discussing why human attention may differ from other species. Chimpanzees, like humans, are both predators are prey to different animals, but the stimuli only included species that are predator and prey to humans. It is thus not really a fair species comparison. The discussion certainly should mention the lack of species diversity as a limitation on generalizability and future direction, even moreso in light of these larger concerns.

Response :: We agree that the language of our original submission both obfuscated our intent and suggested a set of ecological/evolutionary inquiries that our experiments could not effectively test. We have clarified throughout (ll 140-164; 165-171) that our questions, hypotheses, and experiments were targeted to gaze behaviors related to the prototypical features of predators (e.g., forward-facing eyes, robust body) and prey (e.g., lateral eyes) exemplified by the lion and impala. We make no claims about primate behavioral ecology except as related to any deeply conserved attentional biases that ancestral primate evolutionary history may have introduced. The lack of diversity in our sample of predator and prey images is indeed a sincere limitation (albeit an intentional one, designed to measure attentional biases in limited time with a highly unique chimpanzee population) and an appropriate target for future studies. We have added language about this limitation to the discussion (ll 474-478).

R1C3 :: The inclusion of the saliency maps felt a little out of place and I did not find them integrated into the rest of the discussion. Some introductions of their actual use and predictive power in the introduction would be of use. As of now, they are introduced only in ways they fail to predict gaze, and then the results again fail to find them making new predictions, and the naïve reader is left wondering what these can contribute if they consistently fail to make predictions.

Response :: We have added a paragraph to the introduction (ll 181-194) to justify the inclusion of salience maps to test the conservative (and arguably default) alternative hypothesis that any differences in gaze behavior can be understood, with fewer assumptions, to be the result of low-level stimulus features. We believe that such tests are a prerequisite for making more complex arguments from cognitive representation and primate evolutionary biology that our predictions require.

R1C4 :: The hypotheses are quite vague and not well-justified, which combined with a very high number of statistical tests leads readers to wonder if this was more exploratory or hypothesis-driven. Both are welcomed, especially with new topics such as this, but perhaps the manuscript could benefit from distinguishing them and making clearer, concrete predictions associated with the actual hypotheses (ideally with citation). In particular, the first set of predictions (paragraph starting line 131) is essentially just sameness or difference, but then no statistical tests actually directly compared the two species. The lack of direct human-chimpanzee comparison is a strange choice. The reasoning of the sentence starting on line 135 is especially vague and nebulous. If these were the topics of interest wouldn’t a study comparing humans with different background knowledge and social contexts be a more salient test? The choice of a cross-species framework here could be much better-justified.

Response :: We acknowledge that the original formulation of our predictions was not always clear, and we have substantially edited these sections referenced above to better convey the intent of our experiments (ll 140-164). We tested the same set of predictions – about eye direction, prototypical predator and prey features, etc – in both humans and chimpanzees with an eye towards demonstrating which primate attentional biases may have been maintained over evolutionary time. We have clarified that we do not expect differences among the humans and chimpanzees’ gaze behaviors, as these would suggest some outsized influence of background knowledge, sociocultural forces, learning, or the other enculturating forces Reviewer 2 identified (“humans have arguably different relationships with lions/impalas than (captive) chimpanzees. For example, lions are typically considered charismatic species that are highly favoured to see in zoos or safaris.”), which we did not predict nor intend to test (ll 140-152). The nature of these human-chimpanzee hypotheses is a poor fit for statistical tests since the parsimonious, literature-informed hypothesis is the null, which we cannot test, since our predictions are primarily about which species/regions are fixated most frequently (not their absolute proportion or rank order), and since any effects are nested in complex interactions with all of the other factors we tested.

R1C5 :: The dependent measure as proportion of fixation is very unusual compared to previous great ape work. Why was total fixation duration not included? What reasoning is there for choosing number of fixations over duration, especially considering prior work consistently showing chimpanzee gaze is likely to jump around more than humans. Could the lion have evoked more glances away (chimpanzees tend to avoid prolonged direct eye contact) while the averted gaze and impala had longer but more consistent gaze? At the very least, supplemental analysis detailing the duration should be included somewhere.

Response :: Our dataset is indeed well-suited to many analytical frameworks. Our choice of dependent measure, over other correlated measures, is aligned with the human work published using area-normalized fixation proportions (Birmingham et al., 2008a, 2008b). We acknowledge that fixation duration and fixation number are slightly different measures, but generally strongly correlated. No new effects emerge from our dataset when the dependent measure is changed to area normalized total fixation duration, now featured as a supplement figure 4.

Minor concerns:

R1C6 :: Line 87: The topic of chimpanzees seems to come out of nowhere here. As they are central to the whole paper, their introduction should be naturally connected. Perhaps a linking phrase of paragraph about the value and perspective around comparative gaze studies of chimpanzees would help improve this and address one of the major comments above?

Response :: The structure and language of the introduction, especially with regard to the species under study, has been updated for clarity throughout. Several additional primate eye-tracking designs have been added or elaborated upon in this revision (ll 56-57; 66-73; 91; 93-95).

R1C7 :: Line 87: This finding itself also needs more rigour if chimpanzee attention to faces is a central focus of the paper. The previous studies find that chimpanzees gaze more at mouth than eyes even within faces, and this has been considered as potentially more species-relevant for social cues than eyes (Kano et al. 2018, Brooks et al 2021). Did the authors consider looking at attention to mouth by species given this finding? At the very least, the difference in the role and meaning of eye-contact across species should be mentioned. Note also that the supplemental material of some of these previous face-based studies have looked at attention to direct compared to averted gaze, which while not directly on the topic of predator/prey gaze may be useful for the authors to look at.

Response :: We have added language on chimpanzees’ relative interest in other face regions besides eyes (ll 90-92). As emphasized by reviewer 2, we are sensitive to the idea that mechanisms of social gaze to conspecifics are distinct from mechanisms of gaze to potentially dangerous heterospecifics, with the latter the target of our research with humans and chimpanzees.

R1C8 :: Line 116: This is a bit of a strange citation here, as the point of the sentence is that eyes have high saliency in the face but the cited paper is on the topic of that not being at all universal, and certainly is not a citation about them being “presented in this manner.”

Response :: We have clarified our use of this citation.

R1C9 :: Line 139: This whole paragraph does not distinguish species for the predictions. Maybe the authors intend these predictions to apply to all participants, but this should then be made explicit.

Response :: As above, we have substantially edited the way we present our predictions to clarify what we were (and were not) testing (ll 141-169).

R1C10 :: Line 161: The ethnicity states Chinese, Korean, and east Asian as distinct, please check this or clarify.

Response :: This was the language of the demographic survey.

R1C11 :: Throughout: “other part of the head” may be clearer than just head when distinguishing from eyes, since in some sentences this could easily be lost by readers.

Response :: To avoid confusion we have language in the methods pointing the reader to Figure 1B for a visualization of what is meant by eyes, head, body, and background.

R1C12 :: Several times: It may be a bit inaccurate to say we couldn’t look at lion-impala differences in humans because of high attention to both. It would be more accurate to say no differences were observed because of ceiling effects, or the data was not suited for a formal model because of ceiling effects but visually appeared identical. Saying both were at ceiling is a comparison itself.

Response :: We thank you for this statistical point, and have corrected our language (ll 405-406).

R1C13 :: Line 430: “To our knowledge, this experiment provides some of the first evidence examining the strength of the bias towards visually fixating the eyes of nonhuman animals in both human and chimpanzee participants.” This sentence must be rephrased or removed. The prior sentence cites Kano et al. 2018, which compared several primate species including humans on social attention. Also, the nonhuman animals point is somewhat missed here if talking about nonhuman participants, maybe allospecific would be more relevant.

Response :: We have rephrased this point to make clearer that what we find novel is the measured strength of bias to lion and impala eyes, rather than the kinds of within-species / within-primate comparisons that are already part of the cited literature (ll 492-494).

R1C14 :: General: the size of the eye ROIs appears very small in the figure, especially considering the screen size used. Are these within the margin of error of accuracy? This should be mentioned.

Response :: We have now noted that all the ROIs were within the error accuracy of the trackers (ll 352-353).

R1C15 :: Line 443: Chimpanzees are one of the nearest relatives, bonobos are equally closely related. Bonobos generally look much more to eyes than chimpanzees (Kano et al. 2018) and have no lions in their range (but do also face leopard predation) and are less proficient hunters. Perhaps a future comparative approach can be highlighted as a future direction?

Response :: We have added this suggestion for a target of future research (ll 531-534).

R1C16 :: Line 444: check divergence dates.

Response :: We have removed this extraneous language.

R1C17 :: General: the discussion could use more interpretation and connection to the broader literature, as it stands it is hard to see what the importance beyond restatement of the results.

Response :: We have revised the Discussion to better highlight what is novel about our results (ll 516-517), how our results were unlikely to be the product of forces other than evolved attention biases (ll 509-511; 518-520), and how future designs could further explore this topic (ll 474-478; 531-534).

R1C18 :: One point not raised anywhere in the manuscript that certainly bears discussion: predators have more forward-facing eyes than prey. Could you rule out the fact that there is a general direct eye-gaze bias, but that the lions just have more direct gaze (at least from the view of primates such as ourselves with forward-facing eyes) and it is therefore not related to predator/prey distinctions per se?

Response :: This is an important point, and indeed something we are very interested in. We are much more explicit in the revision that exactly these differences – between a prototypical predator phenotype and a prototypical prey phenotype – are likely determinants of differences in patterns of gaze behavior across images (ll 140-142; 154-157). Future research could clarify what features of our prototypical predator and prey are most responsible for gaze behavior biases in human and nonhuman primate attention to a much more diverse set of stimuli (ll 474-478).

R1C19 :: How do you account for the fact that the relative eye size between the two species is different? The eyes of the impala appear to be a much bigger proportion of the head than lions. Perhaps this strengthens the finding, but it bears discussion.

Response :: The area-normalized fixation proportions that we used as the dependent measure in all analyses scale fixation counts to a region-of-interest by the proportion of the screen that the region-of-interest occupies. The relative size of the eye region was not necessarily larger for either or lion images or our impala images.

R1C20 :: It is rare in eye-tracking with great apes to use a mesh rather than transparent barrier between eyes and screens. Can you be sure this did not affect gaze tracking when one or the other eye is blocked to the sensor?

Response :: The mesh was an unfortunate requirement of our access to the chimpanzees. We are nevertheless confident in our

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Submitted filename: Response to Reviewers.docx

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PLoS One. doi: 10.1371/journal.pone.0311673.r003

Decision Letter 1

Nick Fogt

7 May 2024

PONE-D-23-40092R1Predator gaze captures both human and chimpanzee attentionPLOS ONE

Dear Dr. Whitham,

Please submit your revised manuscript by Jun 21 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.
A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.
An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

We look forward to receiving your revised manuscript.

Kind regards,

Nick Fogt

Academic Editor

PLOS ONE

Additional Editor Comments:

Thank you for submitting your revised manuscript.

One of the original reviewers has reviewed the revised paper. The reviewer continues to have major concerns regarding the implication in the paper that those data from the manuscript allow for a comparison between human and chimpanzee behavior. Please address to what extent such comparisons can (or cannot) be made, particularly given that the experimental procedures vary. The reviewer has offered a number of suggestions that if followed, may help to address these concerns.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: (No Response)

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2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #2: No

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: No

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4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

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6. Review Comments to the Author

Reviewer #2: I would like to thank the authors for responding to my previous comments. I appreciate some of the adjustments made by the authors which already improved the quality of the manuscript. However, there remain several points where I believe the authors' responses were not entirely adequate which I list below.

MAJOR COMMENTS

1. I continue to encounter major concerns with the difference in study designs for the human and chimpanzee study. While I acknowledge the authors’ clarification that it was not the intention to formally test species differences, many sentences throughout the manuscript suggest a comparability between the human and chimpanzee findings:

L36-38: “The striking similarities between the gaze patterns of humans and chimpanzees provide additional evidence that attentional processing of two-facing eyes is evolutionarily conserved across primates.”.

L141-144: “Attentional biases for predators over prey in modern humans were likely shaped by the same sources of natural selection as those experienced by chimpanzees and as a result patterns of chimpanzee attention should reflect the same (or similar attentional biases)”. You need to statistically test for this. Simply comparing patterns is not scientifically sound.

L486-488: “These chimpanzee results cohere with prior research suggesting that apes attend to eyes of conspecifics and heterospecifics but do so less often than human participants (Kano et al., 2018).”

L514-530: This entire paragraph compares the chimpanzee results to the human results. I don’t see how this is justified if you used a different study design and therefore potentially investigated two completely different things.

2. Linked to my previous point, the authors’ response fails to address why a similar study design wasn’t initially employed, or why they do not want to analyze only the first 3s of the human data, as previously suggested. The authors replied stating that chimpanzees saw three repetitions of each image, but the text mentions that each image was shown four times. Moreover, the argument that by repeating the trials was intended to roughly control the total screen time does not address my concern. The discrepancy between eight consecutive seconds and 3 sets of 3 seconds each is substantial, potentially leading to disparate gaze patterns and undermining the comparability of human and chimpanzee trials (e.g., it is unlikely that the chimpanzees would pick up their gaze patterns where they left in the previous trial). I strongly recommend the authors to reconsider only analyzing the first 3s of the human trials so that a comparison can actually be made. I am aware that the authors state that a human-chimpanzee comparison was not a study aim, but above I mention a couple of places in the paper where this is not clear and where readers can easily misinterpret this. In this way, the title and abstract are already not transparent as there is no mention of this difference in study design. Not even in the discussion is this limitation of the study mentioned.. Similarly for the predictions, I appreciate that the authors included the sentence stating that they did not make specific predictions about divergent patterns, but you actually ran two experiments with different study designs. This needs to be mentioned and you need to make specific predictions about this. Alternatively, the manuscript needs to be restructured in a way that it becomes clear that you tested the humans and chimpanzees on different tasks.

3. I thank the authors for their additional explanation regarding their statistical approach. I'm, however, still not convinced about including a three-way interaction but focusing on the significant two-way interactions (because these were planned contrasts). Such a selective approach may be perceived as cherry-picking, as it disregards other potential effects that may exist within the data. It also raises the question why, for example, the comparison between lion*eye*direct versus lion*body*direct is not made. From the graph it suggests that this effect is there and, to me, would give much stronger evidence for an attention bias for the eyes of a predator, incorporating your reasoning that the direction of the face is an important modulating factor. By ignoring the significant three-way interaction you're missing out on reporting results.

In L412 for example, you find a significant three-way interaction, indicating that the fixation proportion is influenced by an interplay between those three factors. But here, by looking at the two-way interaction your possibly just ignoring a possible significant effect between lion*head*direct and lion*body*direct. Alternatively, in the next sentence you focus on the significant stimulus type*ROI effect and report that humans and chimpanzees fixated more on lion eyes than the impala eyes, but from the graph it is obvious that gaze direction modulates this effect (for the lions).

4. Additionally, I find the authors' response as to why the saliency was not directly tested against the (initial) fixation proportion unsatisfactory. Mentioning that the data will be made available for alternative approaches that are outside the scope of your questions is not true, and truthfully suggests reluctance from the authors to consider changes. It’s essential to note that the current methodology precludes conclusive remarks on the impact of saliency on gaze patterns, as highlighted in specific sections of the manuscript (e.g., L504-508, L532—535). Given that the effect of saliency on AOIs is one of your main predictions, it is essential to use proper statistical methods to actually make any conclusions. I very much appreciate the inclusion of the saliency maps in this paper which is exemplary for other studies, but if the authors do not want to properly test this, I would suggest removing this component from the study. I reiterate the recommendation for using mixed models which would allow for incorporating the saliency values as a control variable or covariate.

5. I agree with Reviewer 1 that within the primate literature total fixation duration is more common. While the authors reply that proportion of fixations aligns with previous human work, this could similarly be applied to primate studies, so it is not clear why this approach was favored over the other. I appreciate the addition of figure S4 showing these data, and the authors state that no new effects emerged from the datasets with normalized total fixation duration is used as dependent variable. However, no statistics are provided or indicated in the figure. Again, simply comparing patterns between graph is not sufficient to make such conclusions. Even then, just by scanning figure S4 and comparing with figure 2B, it seems clear that the two do not follow the same pattern (but then again, we would need statistics to know this, just like with the saliency results). It is also unclear why only chimpanzee data are shown and not human data.

MINOR COMMENTS

L68-69: I would add the species for each of the references.

L71: Replace ‘lions’ with 'animals' or something alike as you don't only mention lions.

L73-75: I would move this to the next paragraph where you actually introduce that faces are relevant.

L95: You start the sentence with “One study found…” but you actually refer to multiple studies, please revise.

L115: I would add the argument of the pareidolia effect at the end of this sentence to highlight that this is such a strong tendency that it extends beyond natural faces.

L122: Senju et al. 2011 is an interesting paper here: https://doi.org/10.1080/13506280444000157

L182: Rephrase: “and the face being directed or averted”

L376: “Section 3.1.1”

L388: "stimulus species", or something to highlight it's about the lion and impala.

L410: If you used a linear mixed-effects model, I assume you included random effects. What were these?

Table 2: Having a second look at the table, the comparison Background direct vs. Background averted is missing.

L475-479: But you did not test the difference between for example impala head and body, so you cannot conclude this (or these statistics are at least not reported in the text and tables). At the same time, this was tested for in the saliency analyses. This raises concerns regarding the clarity and coherence of the testing procedures, potentially impeding readers' understanding of the tested variables and their corresponding results. Given this inconsistency, readers may find it challenging to track and interpret the outcomes of the various analyses conducted.

L484-486: Again, not listed in the tables.

**********

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Reviewer #2: No

**********

PLoS One. 2024 Nov 21;19(11):e0311673. doi: 10.1371/journal.pone.0311673.r004

Author response to Decision Letter 1

16 Aug 2024

________________________________________

Reviewer comments________________________________________

I would like to thank the authors for responding to my previous comments. I appreciate some of the adjustments made by the authors which already improved the quality of the manuscript. However, there remain several points where I believe the authors' responses were not entirely adequate which I list below.

MAJOR COMMENTS

RC1 :: I continue to encounter major concerns with the difference in study designs for the human and chimpanzee study. While I acknowledge the authors’ clarification that it was not the intention to formally test species differences, many sentences throughout the manuscript suggest a comparability between the human and chimpanzee findings:

Response :: We have removed the specific sentences of major concern. We have also, in response to several of the constructive comments below, substantially restructured the manuscript to more completely disambiguate the two experiments given the differences in design and methodology.

RC2 :: Linked to my previous point, the authors’ response fails to address why a similar study design wasn’t initially employed, or why they do not want to analyze only the first 3s of the human data, as previously suggested. The authors replied stating that chimpanzees saw three repetitions of each image, but the text mentions that each image was shown four times. Moreover, the argument that by repeating the trials was intended to roughly control the total screen time does not address my concern. The discrepancy between eight consecutive seconds and 3 sets of 3 seconds each is substantial, potentially leading to disparate gaze patterns and undermining the comparability of human and chimpanzee trials (e.g., it is unlikely that the chimpanzees would pick up their gaze patterns where they left in the previous trial). I strongly recommend the authors to reconsider only analyzing the first 3s of the human trials so that a comparison can actually be made. I am aware that the authors state that a human-chimpanzee comparison was not a study aim, but above I mention a couple of places in the paper where this is not clear and where readers can easily misinterpret this. In this way, the title and abstract are already not transparent as there is no mention of this difference in study design. Not even in the discussion is this limitation of the study mentioned.. Similarly for the predictions, I appreciate that the authors included the sentence stating that they did not make specific predictions about divergent patterns, but you actually ran two experiments with different study designs. This needs to be mentioned and you need to make specific predictions about this. Alternatively, the manuscript needs to be restructured in a way that it becomes clear that you tested the humans and chimpanzees on different tasks.

Response :: We have followed the advice to restructure the manuscript in a way that more clearly emphasizes the differences of procedure, analyses, and conclusions between the human and chimpanzee designs. In the general discussion we again emphasize these differences alongside the conservative inference that in both humans and chimpanzees we observed evidence of the biases to lions and to their directed gaze that we predicted (ln 575-590). We intended 3 repetitions of a stimulus to indicate the four total exposures described in the manuscript, but apologize for the unclear language.

RC3 :: I thank the authors for their additional explanation regarding their statistical approach. I'm, however, still not convinced about including a three-way interaction but focusing on the significant two-way interactions (because these were planned contrasts). Such a selective approach may be perceived as cherry-picking, as it disregards other potential effects that may exist within the data. It also raises the question why, for example, the comparison between lion*eye*direct versus lion*body*direct is not made. From the graph it suggests that this effect is there and, to me, would give much stronger evidence for an attention bias for the eyes of a predator, incorporating your reasoning that the direction of the face is an important modulating factor. By ignoring the significant three-way interaction you're missing out on reporting results.

Response :: We appreciate the additional notes on statistical interpretation of the results. The full matrix of three-way post hoc comparisons are briefly discussed in new sections added to the results for Experiment 1 (ll 358-370) and Experiment 2 (ll 539-545), visualized in new supplements S1 and S7, and reported explicitly in supplements S2 and S8. We attempted throughout to tailor our analyses to the specific predictions we made about anticipated patterns of gaze data. Planned contrasts were targeted to our specific statistical predictions about anticipated differences that may emerge from the hypothesized attentional biases that are the subject of the manuscript.

RC4 :: Additionally, I find the authors' response as to why the saliency was not directly tested against the (initial) fixation proportion unsatisfactory. Mentioning that the data will be made available for alternative approaches that are outside the scope of your questions is not true, and truthfully suggests reluctance from the authors to consider changes. It’s essential to note that the current methodology precludes conclusive remarks on the impact of saliency on gaze patterns, as highlighted in specific sections of the manuscript (e.g., L504-508, L532—535). Given that the effect of saliency on AOIs is one of your main predictions, it is essential to use proper statistical methods to actually make any conclusions. I very much appreciate the inclusion of the saliency maps in this paper which is exemplary for other studies, but if the authors do not want to properly test this, I would suggest removing this component from the study. I reiterate the recommendation for using mixed models which would allow for incorporating the saliency values as a control variable or covariate.

Response :: The salience analyses have been reworked to more directly test the predictive validity of salience values on initial fixation proportions using a framework that tests the salience at the fixated region to two chance-based estimates (ll 280-296; 347-356; 533-537). Salience maps do not predict the pattern of gaze behaviors that were the subject of our design, analyses, and conclusions.

RC5 :: I agree with Reviewer 1 that within the primate literature total fixation duration is more common. While the authors reply that proportion of fixations aligns with previous human work, this could similarly be applied to primate studies, so it is not clear why this approach was favored over the other. I appreciate the addition of figure S4 showing these data, and the authors state that no new effects emerged from the datasets with normalized total fixation duration is used as dependent variable. However, no statistics are provided or indicated in the figure. Again, simply comparing patterns between graph is not sufficient to make such conclusions. Even then, just by scanning figure S4 and comparing with figure 2B, it seems clear that the two do not follow the same pattern (but then again, we would need statistics to know this, just like with the saliency results). It is also unclear why only chimpanzee data are shown and not human data.

Response :: We clarify the relative merits of using area-normalized fixation proportions for designs of this kind in the Eye-tracking analysis text (ln 264-272). We have added ANOVA and planned comparisons analyses on total fixation duration to figure S4 to parallel those of the main analysis of the manuscript. Parallel analyses with the human data are unfortunately not possible using as the software did not record fixation times to background or off-screen fixations. As with the planned contrasts above, we favor a selective approach that is targeted to the specific predictions we made about anticipated patterns of gaze data using the dependent variable we intended to base our analyses on.

MINOR COMMENTS

RC6 :: L68-69: I would add the species for each of the references.

Response :: We have made this change (ln 63-67)

RC7 :: L71: Replace ‘lions’ with 'animals' or something alike as you don't only mention lions.

Response :: We have made this change (ln 67-70)

RC8 :: L73-75: I would move this to the next paragraph where you actually introduce that faces are relevant.

Response :: We have made this change (ln 79-81)

RC9 :: L95: You start the sentence with “One study found…” but you actually refer to multiple studies, please revise.

Response :: We have made this change (ln 94-96)

RC10 :: L115: I would add the argument of the pareidolia effect at the end of this sentence to highlight that this is such a strong tendency that it extends beyond natural faces.

Response :: We have made this change (ln 112-114)

RC11 :: L122: Senju et al. 2011 is an interesting paper here: https://doi.org/10.1080/13506280444000157

Response :: One of our favorites, cited ln 95-96

RC12 :: L182: Rephrase: “and the face being directed or averted”

Response :: We have made this change (ln 172-174)

RC13 :: L376: “Section 3.1.1”

Response :: We have added “Section” to each leading reference throughout the manuscript.

RC14 :: L388: "stimulus species", or something to highlight it's about the lion and impala.

Response :: We have changed stimulus type to “stimulus species” throughout the manuscript

RC15 :: L410: If you used a linear mixed-effects model, I assume you included random effects. What were these?

Response :: These salience models are no longer a part of the manuscript in favor of the new approach to salience analyses described above.

RC16 :: Table 2: Having a second look at the table, the comparison Background direct vs. Background averted is missing.

Response :: The area-normalized fixation proportions are normalized such that the proportions sum to one, allowing for only 1 unique comparison in a comparison of only animals vs backgrounds. This aside, Table 2 is omitted from the rearranged manuscript since only the chimpanzee data were interpretable.

RC17 :: L475-479: But you did not test the difference between for example impala head and body, so you cannot conclude this (or these statistics are at least not reported in the text and tables). At the same time, this was tested for in the saliency analyses. This raises concerns regarding the clarity and coherence of the testing procedures, potentially impeding readers' understanding of the tested variables and their corresponding results. Given this inconsistency, readers may find it challenging to track and interpret the outcomes of the various analyses conducted.

Response :: Table 4 is incidentally not needed in the revised manuscript due to the reconfiguration of salience analyses to use Mann-Whitney tests to more directly test the relationship between initial fixations and salience. The tests targeted to our specific hypotheses should be consistent throughout the manuscript, and all unplanned comparisons are available in supplemental materials.

RC18 :: L484-486: Again, not listed in the tables.

Response :: We would be happy to address this comment with additional context.

Attachment

Submitted filename: Response to Reviewers.docx

pone.0311673.s010.docx^{(28KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0311673.r005

Decision Letter 2

Nick Fogt

3 Sep 2024

PONE-D-23-40092R2Predator gaze captures both human and chimpanzee attentionPLOS ONE

Dear Dr. Whitham,

Please submit your revised manuscript by Oct 18 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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We look forward to receiving your revised manuscript.

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Nick Fogt

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments:

Thank you for your thorough responses to the reviewer comments. Please address the remaining reviewer comments from the latest review.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

Reviewer #2: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

Reviewer #2: Yes

**********

6. Review Comments to the Author

Reviewer #2: Dear authors,

Thank you for addressing the comments and suggestions provided in the previous round of review. I have reviewed the revised version of your manuscript and am pleased to note the improvements made.

The manuscript is now significantly clearer and more transparent, making it much easier to read and understand. The adjustments you have made have strengthened the overall quality of the paper. I appreciate the effort you have put into refining the content, particularly in the areas of data presentation, separating the two experiments and interpretation of the results.

Overall, I am satisfied with the revisions and believe the manuscript is now in a much better state for publication. I have no further major concerns, and I commend you on the work done to enhance the clarity and rigor of the research presented.

Minor comments:

L113-115: Redundant? Has been discussed earlier. Maybe can be integrated.

L327: I assume you used corrected p-values? I would suggest reported what significance values were handled to enhance transparency to the readers. Perhaps I missed it.

L354: I don’t know if the journal follows APA-style, but there the z value is reported before the p value.

L495: I know that the human participants rarely gazed at the backgrounds, but for consistency I think it'd be better to provide this information for Exp1 as well.

L575: I would be careful calling the designs similar.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

**********

PLoS One. 2024 Nov 21;19(11):e0311673. doi: 10.1371/journal.pone.0311673.r006

Author response to Decision Letter 2

16 Sep 2024

Reviewer #2: Dear authors,

RC1: Thank you for addressing the comments and suggestions provided in the previous round of review. I have reviewed the revised version of your manuscript and am pleased to note the improvements made. The manuscript is now significantly clearer and more transparent, making it much easier to read and understand. The adjustments you have made have strengthened the overall quality of the paper. I appreciate the effort you have put into refining the content, particularly in the areas of data presentation, separating the two experiments and interpretation of the results. Overall, I am satisfied with the revisions and believe the manuscript is now in a much better state for publication. I have no further major concerns, and I commend you on the work done to enhance the clarity and rigor of the research presented.

Response: We thank the reviewer for their constructive comments throughout

Minor comments:

L113-115: Redundant? Has been discussed earlier. Maybe can be integrated.

Response: We have moved these citations about human and other primates’ apparent bias to faces a few lines higher (ll 109-112) to sit after “These findings suggest that, as with human faces, the bias to attend to nonhuman animal faces is especially strong when direction of gaze is aimed toward the observer.”

L327: I assume you used corrected p-values? I would suggest reported what significance values were handled to enhance transparency to the readers. Perhaps I missed it.

Response: Bonferroni-correct p values were used for all inferences over the post hoc contrasts (ll 365, 545)

L354: I don’t know if the journal follows APA-style, but there the z value is reported before the p value.

Response: We have rearranged these reports to position z values before p (ll 357-359, ll 537-538).

L495: I know that the human participants rarely gazed at the backgrounds, but for consistency I think it'd be better to provide this information for Exp1 as well.

Response: We have added specific means, standard deviations, and confidence intervals to the Experiment 1 Animals vs Backgrounds sections as well (ll 319-321).

L575: I would be careful calling the designs similar.

Response: We have removed this language.

Attachment

Submitted filename: Response to Reviewers.docx

pone.0311673.s011.docx^{(21.7KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0311673.r007

Decision Letter 3

Nick Fogt

24 Sep 2024

Predator gaze captures both human and chimpanzee attention

PONE-D-23-40092R3

Dear Dr. Whitham,

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Kind regards,

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Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Thank you for your responses to the latest reviewer comments.

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0311673.r008

Acceptance letter

Nick Fogt

8 Oct 2024

PONE-D-23-40092R3

PLOS ONE

Dear Dr. Whitham,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

S1 File. The procedure for validating chimpanzee eye-tracker calibrations.

(DOCX)

pone.0311673.s001.docx^{(57.4KB, docx)}

S1 Table. p values for post hoc comparison matrix for Experiment 1.

(DOCX)

pone.0311673.s002.docx^{(20.1KB, docx)}

S2 Table. p values for post hoc comparison matrix for Experiment 2.

(DOCX)

pone.0311673.s003.docx^{(20.2KB, docx)}

S1 Fig. Post hoc comparison matrix for Experiment 1.

(DOCX)

pone.0311673.s004.docx^{(105.4KB, docx)}

S2 Fig. The apparatus used for testing chimpanzee subjects.

(DOCX)

pone.0311673.s005.docx^{(576.2KB, docx)}

S3 Fig. Area-normalized fixation proportions for individual chimpanzee subjects.

(DOCX)

pone.0311673.s006.docx^{(87.1KB, docx)}

S4 Fig. Supplemental analyses.

Fixation duration plotted as a function of stimulus species, gaze direction and ROI for chimpanzee subjects.

(DOCX)

pone.0311673.s007.docx^{(47KB, docx)}

S5 Fig. Post hoc comparison matrix for Experiment 2.

(DOCX)

pone.0311673.s008.docx^{(105.5KB, docx)}

Attachment

Submitted filename: Response to Reviewers.docx

pone.0311673.s009.docx^{(51.3KB, docx)}

Attachment

Submitted filename: Response to Reviewers.docx

pone.0311673.s010.docx^{(28KB, docx)}

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Submitted filename: Response to Reviewers.docx

pone.0311673.s011.docx^{(21.7KB, docx)}

Data Availability Statement

All data files used in these analyses are available from the Open Science Framework database (DOI 10.17605/OSF.IO/WHSNE).

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PERMALINK

Predator gaze captures both human and chimpanzee attention

Will Whitham

Bradley Karstadt

Nicola C Anderson

Walter F Bischof

Steven J Schapiro

Alan Kingstone

Richard Coss

Elina Birmingham

Jessica L Yorzinski

Roles

Abstract

1. Introduction

2. Experiment 1

2.1 Materials and methods

2.1.1 Participants

2.1.2 Apparatus

2.1.3 Procedure

2.1.4 Stimuli

Fig 1. Visualizations of experimental stimuli.

2.1.5 Eye-tracking analysis

2.1.6 Salience analysis

2.2 Experiment 1 results

2.2.1 Statistical analysis

2.2.2 Animals versus backgrounds

2.2.3 Specific animal ROIs

Fig 2. Normalized fixation proportions plotted as a function of stimulus species, gaze direction and ROI for Experiment 1.

Table 1. The effect of stimulus species, gaze direction, and ROI on the normalized fixation proportions in Experiment 1.

2.2.4 Initial fixations on animals

Table 2. The effect of stimulus species, gaze direction, and ROI on the initial fixation proportions.

Fig 3. Proportion of initial fixations falling on eyes, heads, bodies, or background, as a function of stimulus species and gaze direction.

2.2.5 Salience analysis

2.2.6 Three-way interaction comparisons

2.3 Experiment 1 discussion

3. Experiment 2

3.1 Experiment 2 methods

3.1.1 Participants

3.1.2 Apparatus

3.1.3 Procedure

3.1.4 Stimuli

3.1.5 Eye-tracking analysis

3.1.6 Salience analysis

3.2 Experiment 2 results

3.2.1 Statistical analysis

3.2.2 Animals versus backgrounds

3.2.3 Specific animal ROIs

Fig 4. Normalized fixation proportions plotted as a function of stimulus species, gaze direction and ROI for Experiment 2.

Table 3. The effect of stimulus species, gaze direction, and ROI on the normalized fixation proportions in Experiment 2.

3.2.4 Initial fixations on animals

Table 4. The effect of stimulus species, gaze direction, and ROI on the initial fixation proportions in Experiment 2.

Fig 5. Proportion of initial fixations falling on eyes, heads, bodies, or background, as a function of stimulus species and gaze direction for Experiment 2.

3.2.5 Salience analysis

3.2.6 Three-way interaction comparisons

3.3 Experiment 2 general discussion

4. Discussion

Supporting information

Data Availability

Funding Statement

References

Decision Letter 0

Nick Fogt

Roles

Author response to Decision Letter 0

Decision Letter 1

Nick Fogt

Roles

Author response to Decision Letter 1

Decision Letter 2

Nick Fogt

Roles

Author response to Decision Letter 2

Decision Letter 3

Nick Fogt

Roles

Acceptance letter

Nick Fogt

Roles

Associated Data

Supplementary Materials