Introduction

The capacity for trichromatic colour vision has evolved in many primates, including humans. Catarrhines (Old World monkeys and apes) are routine trichromats [1, 2], while most platyrrhines and some strepsirrhines also have a capacity for trichromatic colour vision in that some individuals are trichromats (polymorphic trichromats) [3–6]. Two hypothesized functions for the evolution of trichromatic colour vision are that this capability provided advantages in detecting ripe fruits and in detecting young leaves [2, 7]. In this context, it is assumed to have provided advantages for diurnal species [5]. However, there does not seem to be a consistent difference between fruit predominantly consumed by dichromats and that predominantly consumed by trichromats [2, 8]. Another hypothesized function of trichromatic colour vision is the advantage of being able to discriminate modulations in the skin colour of conspecifics for extracting information about emotional states, socio-sexual signals and threat displays [9]. In addition, functions of colour preferences have been widely discussed in relation to mate choice, both in humans and other primates [10–12], and also in relation to crypsis, communication and physiological functions [10]. Furthermore, as Humphrey [13] pointed out, “signal colours commonly have three functions: they catch attention, they transmit information and they directly affect the emotions of the viewer”. Hence, sensitivity to signal colours probably also influences preferences for specific colours. This raises the question, in regard to humans and non-human great apes, whether shared colour biases could have evolved together with the evolution of colour vision. Moreover, Osorio and Vorobyev [8] noted that there are different perspectives regarding the evolution of sensory systems: “One is that communication signals evolve in response to a fixed sensory system [14], the other is that senses and signals co-evolve as a specialised communication system.” If senses and signals co-evolved, it could be that biases for specific colours are linked to this communication system.

Various studies have examined colour preferences in primates other than great apes, mostly in relation to sexual contexts [15–20], but also in relation to object preferences [21]. Studies on the colour preferences of non-human great apes which are not related to mate information but rather to food and object choice have shown that zoo-housed orangutans (Pongo pygmaeus) prefer coloured to non-coloured monkey chow [22] and that gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes) both have a preference for blue and green objects over red ones [23]. Wells et al. [23] therefore concluded that the colour preferences of gorillas and chimpanzees resemble those of humans, suggesting that for the three species, there is a common innate relationship between colours and behavioural reactions, that is, the approach or avoidance behaviour that is provoked. However, the use of specific contexts to study colour preferences (such as reproductive contexts or contexts involving objects or food) gives rise to biases, because each species has adapted differently to different contexts. Hence, in comparisons between different species, the correct analysis of context-related preferences may be difficult. Studies that focus on species comparisons should therefore use colour stimuli that are not related to a specific context.

The extensive body of research on colour preferences in humans (for a review, see [24]) has found that blue is always most preferred and yellow is always least preferred [25–29]. The findings differ only in regard to preferences for the colours purple, red and green. Furthermore, research on the influence of colours on human emotions has suggested that a participant’s age [30] as well as saturation and brightness of the colour [31] play an important role in the association of a colour with an emotion. Brighter colours are judged more pleasant, and saturated, darker colours are judged more arousing, while hue plays only a minor role in the influence on mood [24]. However, despite the extensive body of research on human colour preferences, there is no consistent pattern in the conclusions which have been drawn from findings about the association between emotions and colours. Aesthetic perceptions are guided by different overlapping influences, such as person–situation interactions, the domain in which a specific colour occurs [32] and the interaction of biological factors with social processes, and as a result researchers give rather inconsistent reasons for human colour biases. Similarly, and relevant for the present comparative study, primate colour signals also occur in different contexts, such as mate choice (reproductive context) and threat displays (competitive context).

In the acoustic domain, a variety of experimental studies have also been conducted on the perception of consonant and dissonant sounds and their influence on human emotions (for reviews, see [33] and [34]). Functional imaging studies have suggested that consonant and dissonant sounds activate the same brain regions as other pleasant and unpleasant stimuli, respectively [35, 36]. Moreover, consonant sequences of sounds are perceived as pleasant and dissonant sequences as unpleasant when heard in isolation, but dissonant sequences can disperse and become harmonious and pleasant when they are integrated in a composition [37]. The few studies that have investigated the perception of consonant and dissonant sounds across cultures [38, 39] have found similar perceptions in humans regardless of their cultural background, suggesting that human sound biases in terms of being pleasant or unpleasant are most likely innate. This is supported by developmental studies conducted by Zentner and Kagan [40, 41] and Trainor et al. [42], who found that 4-month-old infants already preferred consonant over dissonant sounds—which led McDermott and Hauser to conclude that the preference for consonant sounds is innate and emerges independently of experience [34]. If the preference for consonant sounds is innate in humans, it most likely evolved in the primate lineage and should thus be shared by other primates. However, apart from another study by McDermott and Hauser [43], which did not find similar approach–avoidance reactions to consonant or dissonant sounds in tamarins (a species of New World monkeys), virtually nothing is known about the biases of non-human primates in the auditory domain regarding sounds which are detached from vocal information. Thus, it remains an open question whether great apes, which are more closely related to humans than are New World monkeys, share the bias for consonant sounds with humans.

Furthermore, if colours provoke a psychological reaction (bias for or against) or a behavioural reaction (approach or avoidance), the question arises whether a consonant or dissonant sound can amplify the reactions associated with specific colours. Multimodal signalling has been examined in many studies in an evolutionary context [44, 45]. One of the functions of multimodal signalling could be that the psychological effects of visual cues can be enhanced by non-visual cues (for a review, see [45]). Multimodal signalling occurs in very different combinations of modal domains, such as coloration and odours, but also gestures and vocalizations [46–48]. As most primate vocalizations are species-specific, we needed to find a different acoustic stimulus that could be used across species and that was also known to provoke approach–avoidance reactions. Therefore, we used consonant and dissonant sounds and conducted a non-invasive comparative eye-tracking study of orangutans—a species of non-human great apes—and humans, to test the duration of their fixations on different colours with and without simultaneous auditory stimuli.

The non-invasive eye-tracking technique has been successfully applied by Kano and colleagues [49–51] to investigate the gazing patterns of great apes, including orangutans. These previous studies mostly focused on how great apes process visual information such as facial and bodily expressions when they look at pictures of conspecifics or humans. In contrast to these studies, we used colours, which are also visual stimuli, but without any relation to objects or persons. Despite the complexity that arises in the domains of both colour and sound biases due to the influence of human participants’ cultural and personal backgrounds, and also despite humans being more familiar with certain colours than orangutans, we combined a basic visual stimulus with a basic auditory stimulus because we needed stimuli that could be used across different primate species, free of any biases that might be caused by the colours being combined with objects or other types of stimuli. Thus, although presenting colours and sounds detached from any related information, such as mate information or objects (for colours) and vocalizations (for sounds), could be viewed as having low ecological validity, it reduces the biases associated with such related information.

Our aim was to investigate 1) whether there is a similar pattern of gaze duration biases and avoidances related to different colours in the two species and 2) whether humans and orangutans associate specific colours with auditory information—specifically, whether the approach or avoidance of a colour cumulates with the approach or avoidance of an auditory stimulus. We examined gaze fixation durations for the four colours blue, red, yellow and green, both separately and in combination with an auditory stimulus comprising a consonant or dissonant triad and chord (a triad is a set of three tones played one after another and the chord was the same set of three tones played simultaneously, directly after the triad). If colour biases are innate, they should be similar across humans. If they are shared with other species and thus represent an evolutionarily older trait, the gaze duration biases for specific colours should be similar in humans and orangutans. The gaze duration biases in combination with auditory information should also be similar.

Methods

Results

The likelihood ratio test between model 1 and model 2 showed no effect of Sex, and the likelihood ratio test between model 1 and model 3 showed no effect of Age. As Sex and Age showed no effect, they were excluded from the subsequent analyses. The likelihood ratio test between model 3 and model 4 indicated that including the factor Colour in model 4 improved the fit of the model to the data, but not significantly (p-value = 0.062; Table 1). The likelihood ratio test between model 4 and model 5 indicated that including the cross-level interaction between Colour and Group in model 5 significantly improved the fit of the model to the data (p-value = 0.015), which means that species-specific differences existed in relation to the factor Colour. Table 1 shows the results of the likelihood ratio tests for all generated models for colours only.

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Table 1. Likelihood-ratio tests of model comparisons for colours only.

The table shows the results of the model comparisons for colours only. All models had mean fixation duration as the dependent variable and Subject as random effects.

https://doi.org/10.1371/journal.pone.0139894.t001

The likelihood ratio test for the comparison of models 5 and 6 found no effect of Sound. The likelihood ratio test for models 6 and 7 showed no effect of Sound on the effect of Colour (cross-level interaction between Colour and Sound). The likelihood ratio test of the comparison between models 6 and 8 showed no species-specific effects of Sound. Table 2 shows the results of the likelihood ratio tests for all models generated to test the effects of Sound.

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Table 2. Likelihood-ratio tests of model comparisons for colours and sounds.

The table shows the results of the model comparisons for colours and sound. All models had mean fixation duration as the dependent variable and Subject as random effects. Model 4 and model 5 were built like the models 4 and 5 for colours only (Table 1). Models 7 and 8 were both extensions of model 6 and hence were both compared to model 6.

https://doi.org/10.1371/journal.pone.0139894.t002

Since Sound showed no effects (see Table 2), model 5 (with mean fixation duration as the dependent variable, the cross-level interaction of the factors Colour and Group as fixed effects and Subject as random effects) was the only model that showed a significant effect. Model 5 revealed that species-specific differences arose in the mean fixation duration for the four colours, in that the human group observed yellow for significantly shorter durations than the colours red (Estimate: 0.257; t-value: 3.36; p = 0.001) and green (Estimate: 0.244; t-value: 3.20; p = 0.001). For the colour blue, again in the human group, there was no visible effect indicating that it was observed for significantly longer durations than yellow (blue: Estimate: 0.140; t-value: 1.83; p = 0.068). Using the Šidák correction, the critical p-value for the tests of the regression weights is 0.007. We calculated the p-values from the t-values of the colours red, green and blue with respect to yellow in the intercept, with df for level-1 regression, since Colour is a characteristic of the stimulus and not of the subject. This works for models with fewer than 40 level-2 entities ([68], p. 95). (A detailed list of all calculated Estimates, t-values and p-values for all colours can be found in S2 Table). In the orangutan group, there were no such effects visible in the mean fixation duration, which indicates that the humans avoided yellow (and as a trend also blue, as blue was not observed significantly differently than yellow), while the orangutans did not (please see also Fig 1). When combined with the four sounds, the fixation durations remained almost the same as they were for the colour-only condition (please see Table 2 and also Fig 2). Fig 1 shows the mean fixation duration for the four colours in the two groups for the colour-only condition, here represented with the non-log-transformed dependent variable. As described above, it is clear that yellow was observed for shorter durations than the other colours in the human group, but not in the orangutan group. Fig 2 shows the mean fixation durations in the two groups for the four colours together with the different sounds. The mean fixation duration remained almost the same in both groups, which indicates that the sounds did not have a significant influence on the fixation duration.

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Fig 1. Predicted mean fixation duration in ms for the four colours.

Fig 1 represents the predicted mean fixation duration in the two groups for the four colours. Values were calculated with a non-log-transformed dependent variable and represent the fixation duration in milliseconds. The left box shows the values for the human participants, the right box those for the orangutans.

https://doi.org/10.1371/journal.pone.0139894.g001

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Fig 2. Predicted mean fixation duration in ms for the four colours and sounds.

Fig 2 represents the predicted mean fixation duration in the two groups for the four colours together with the four sounds. Values were calculated with a non-log-transformed dependent variable and represent the fixation duration in milliseconds. The four boxes represent the four types of sound, and the two groups are represented by the different shapes of the dots.

https://doi.org/10.1371/journal.pone.0139894.g002

Discussion

Our finding that humans avoided yellow confirms findings of the previous studies with humans [25–29] mentioned in the introduction. However, in contrast to these studies, we did not find evidence for a clear bias for blue in humans, because the mean fixation durations for yellow vs. blue, and also for blue vs. green and blue vs. red, did not differ significantly. This can be seen in the fact that the Estimates for red (Estimate: 0.257; t-value: 3.36; p = 0.001) and green (Estimate: 0.244; t-value: 3.20; p = 0.001) are very similar, and blue lies between those values for yellow and red/green. The orangutans did not show any bias for or avoidance of specific colours, which seems to support a study by Barbiers [22], who also found no overall preference for a specific colour. In Barbiers’ study, when orangutans were confronted with differently coloured food items (monkey chow in red, blue, green and orange), only one of the five orangutans showed a clear preference for red monkey chow [22]. This also seems to indicate that orangutans are different from gorillas and chimpanzees, since Wells et al. [23] concluded that these species, which are more closely related to humans, show a colour preference for blue and green, similar to humans. However, based on these very few studies with non-human great apes, it is not yet possible to determine whether this is evidence for a difference between humans, chimpanzees and gorillas on the one hand and the more distantly related orangutans on the other, or whether the different findings of the present study and of Wells et al. [23] are due to differences in the methodology used. Still, the differences suggest that the capacity for trichromatic colour vision did not evolve together with a shared bias for specific colours. The advantages of trichromatic colour vision discussed in the studies described in the introduction to this paper were advantages for detecting ripe fruits and young leaves [2, 7] and for discriminating skin colour modulations [9]. The present study’s findings neither support nor disagree with the suggested reasons for the evolution of trichromatic colour vision, because a clear shared bias for one colour was not found in the two groups and hence cannot be used to speculate about a shared evolutionary reason for trichromatic colour vision. The results of this study show differences between humans’ and orangutans’ relative gaze fixation durations when confronted with these colours, which suggests that the two groups react differently to the colours when confronted with them.

Regarding the combination of colours with an auditory stimulus, we found no influence of either consonant or dissonant sounds on colour biases. However, contrary to our predictions, human avoidance of the colour yellow was not modified when this colour was combined with sound. Since previous studies have found that isolated dissonant sounds provoke an avoidance reaction [37], we expected that this reaction would cumulate with an avoidance reaction for a specific colour. The avoidance of dissonant sounds has been supported by different studies, including comparative studies which have investigated the perception of consonant and dissonant chords in non-human primates (for a review, see [69]). For example, rhesus monkeys are able to clearly discriminate between consonant and dissonant chords, with activation of similar brain regions to those in humans [34]. However, it remains an open question whether the monkeys’ activated brain regions and the ability to discriminate between consonant and dissonant sounds reflect the same pleasurable or aversive reactions found in humans [34]. At the age of 16 weeks, human infants already show these reactions and will turn away from dissonant sounds, even crying, but will turn towards consonant sounds, often smiling [40, 41, 70]. Our study’s finding of the absence of a cumulative effect from avoidance of dissonant sounds therefore suggests that perceptions of visual stimuli are not influenced by auditory stimuli.

While several studies [23, 24] have suggested similarities in colour preferences across different species and cultures, other studies have proposed, with regard to cross-cultural variations in colour meaning, that any effects of colour upon behaviour are learned [71, 72]. Thus, studies investigating the perception of colours and their representation in cultural usages and the corresponding languages have shown that across cultures, the meanings of colours are not independent of the syntax and semantics with which the colour names are used [72]. In this regard, the mere-exposure effect plays an important role: based on their degree of familiarity, spectators develop different attitudes towards observed objects in general and, more specifically, towards colours. This means that the contexts in which different colours have been used influence spectators’ attitudes and hence the approach or avoidance reactions they exhibited. This is also supported by Whitfield’s observation that “colours vary in regard to the extent in which they correspond with the learned specifications of different object categories” [73]. Similarly, Davidoff et al.’s [74] findings did not support the idea that colour categories are universal, though they admitted that neurons are selective toward wavelength, brightness and colour constancy, as discovered in monkeys [75, 76]. They concluded that a cultural group’s environment and language influence colour categorization. The differences in colour categorizations among languages show that language, culture and colour perception are interlinked. In addition to environment and language, there are other influences on individuals’ colour biases, such as world knowledge, education, historical change and individual- and group-specific leitmotifs, as Jacobsen [77] made clear. However, Crozier [24] and Adams and Osgood [25] conclude that despite obvious cultural differences, there are also many similarities between cultures in regard to the usage and meanings of specific colours. For example, the association of red with fire or blood is widely shared across cultures. But the importance of the context in which colours occur applies not only to humans, but also to other primates, as noted in the introduction. For example, red as a signal can be linked to a reproductive context, like the red swellings in female baboons [78], but also to a competitive context for social status among males, as in the scrotal colour of adult vervet monkeys [79]. Because of these different types of biological information that can be linked to colours, we conducted our study with colour stimuli that were designed to have a most basic form. Our stimuli contain the risk of low ecological validity, but they hold the advantage of minimizing any asymmetry in possible biases.

Since we did not find a shared colour bias between the two species, we cannot, in particular, support the idea that the association of red with a potential hazard (such as fire or blood; see above) has a biological root, as suggested by the different cross-cultural and primate studies mentioned above. We did not find any evidence for an avoidance of—or bias for—the colour red in humans and orangutans. We only found a clear avoidance of yellow in the human group, while red and green were fixated upon for equal durations. In addition, we cannot support previous findings that blue is the most preferred colour for humans [24, 25], as humans observed it only slightly longer than yellow in our study. Regarding the avoidance of the colour yellow, we can only speculate why humans but not orangutans avoid this colour. Since several cross-cultural studies covering a wide age range across childhood and adolescence [80–83] have found that the avoidance of yellow is present in both children and adolescents independent of their cultural background, a possible explanation which has been offered for this avoidance reaction is based on the perceived hue and brightness of the colours. Katz and Breed reported that “there was a distinct rise in the preference values of colours of short wave length and a corresponding decline in the values of colours of long wave length, as the children advanced in age” ([83], p. 255). While infants younger than three months preferred colours with longer wavelengths (red and yellow), after the age of three months [84] infants showed a preference for colours with shorter wavelengths (blue and green). However, why the preference for shorter wavelengths evolved and why it only emerges later in ontogeny is not clear. To summarize, on the one hand, approach or avoidance reactions to specific colours are strongly influenced by different cultural, group-specific and individual characteristics, as argued above; but on the other hand, studies with infants have seemed to consistently show that prior to cultural learning, there are approach reactions to specific colours. Finally, regarding cultural influences, one would expect that individual differences in colour approach or avoidance reactions would be stronger, which was not the case in our study.

Conclusions

Our findings confirm previous findings that humans avoid yellow, but do not provide any evidence confirming a clear bias for blue. Unlike humans, orangutans showed neither biases for nor avoidance of specific colours. Hence, we conclude that the evolution of trichromatic colour vision does not eventually have to be accompanied by biases for specific colours. Furthermore, when we combined colours with different consonant or dissonant auditory stimuli, we found that the latter had no influence on the approach or avoidance reactions to the visual stimuli and hence conclude, within the restricted parameters of this study, that the bias for or avoidance of a specific colour seems to be independent of the perception of an auditory stimulus.

Supporting Information

Acknowledgments

We thank the participants from Freie Universität Berlin for their participation in this study. Many thanks also to Josep Call from the Max Planck Institute for Evolutionary Anthropology, Leipzig and the Wolfgang Köhler Primate Research Centre at Leipzig Zoo for permission to test their orangutans. Special thanks to Martin Schultze and Albrecht Stark for their advice regarding the analysis of the data and to Merrie Bergmann and an anonymous reviewer for their helpful comments on the manuscript.