Primate socio-ecology shapes the evolution of distinctive facial repertoires.

Primate facial musculature enables a wide variety of movements during bouts of communication, but how these movements contribute to signal construction and repertoire size is unclear. The facial mobility hypothesis suggests that morphological constraints shape the evolution of facial repertoires: species with higher facial mobility will produce larger and more complex repertoires. In contrast, the socio-ecological complexity hypothesis suggests that social needs shape the evolution of facial repertoires: as social complexity increases, so does communicative repertoire size. We tested these two hypotheses by comparing chimpanzees (Pan troglodytes) and gibbons (family Hylobatidae), two distantly related apes who vary in their facial mobility and social organization. While gibbons have higher facial mobility than chimpanzees, chimpanzees live in more complex social groups than gibbons. We compared the morphology and complexity of facial repertoires for both apes using Facial Action Coding Systems designed for chimpanzees and gibbons. Our comparisons were made at the level of individual muscle movements (action units [AUs]) and the level of muscle movement combinations (AU combinations). Our results show that the chimpanzee facial signaling repertoire was larger and more complex than gibbons, consistent with the socio-ecological complexity hypothesis. On average, chimpanzees produced AU combinations consisting of more morphologically distinct AUs than gibbons. Moreover, chimpanzees also produced more morphologically distinct AU combinations than gibbons, even when focusing exclusively on AUs present in both apes. Therefore, our results suggest that socio-ecological factors were more important than anatomical ones to the evolution of facial signaling repertoires in chimpanzees and gibbons. (PsycInfo Database Record (c) 2024 APA, all rights reserved).

A Comparison of Focal and Opportunistic Sampling Methods when Studying Chimpanzee Facial and Gestural Communication.

Researchers frequently use focal individual sampling to study primate communication. Recent studies of primate gestures have shown that opportunistic sampling offers benefits not found in focal individual sampling, such as the collection of larger sample sizes. What is not known is whether the opportunistic method is biased towards certain signal types or signalers. Our goal was to assess the validity of the opportunistic method by comparing focal individual sampling to opportunistic sampling of facial and gestural communication in a group of captive chimpanzees (Pan troglodytes). We compared: (1) the number of observed facial and gestural signals per signal type and (2) the number of observed facial and gestural signals produced by each signaler. Both methods identified facial signals, gesture signals, and gesture signalers at similar relative rates, but the opportunistic sampling method yielded a more even distribution of signalers and signal types than the focal individual sampling method. In addition, the opportunistic sampling method resulted in larger sample sizes for both facial and gestural communication. However, the opportunistic method did not allow us to calculate the signals per time for each individual, which is easily done with the focal individual method. These results suggest that the opportunistic sampling method is (1) comparable to the focal individual sampling method in multiple important measures, (2) associated with additional sampling benefits, and (3) limited in measuring some variables. Thus, we recommend that future studies use a mixed-methods approach, as focal individual and opportunistic sampling have distinct strengths that complement each other's limitations.

Chimpanzees (Pan troglodytes) tolerate some degree of inequity while cooperating but refuse to donate effort for nothing.

In cooperative hunting, a carcass cannot be divided equally, and hunts may be unsuccessful. We studied how chimpanzees respond to these two variables, working for unequal rewards and no rewards, which have been rarely included in experimental cooperative tasks. We presented chimpanzees with a task requiring three chimpanzees to work together and varied the reward structure in two separate experiments. In Experiment 1, two individuals received more rewards than the third, making the outcome unequal. We wanted to know if cooperation would continue or break down, and what mechanisms might maintain performance. Experiment 2 used equal rewards, but this time one or more locations were left unbaited on a proportion of trials. Thus, there was a chance of individuals working to receive nothing. In Experiment 1, the chimpanzees worked at a high rate, tolerating the unequal outcomes, with rank appearing to determine who got access to the higher-value locations. However, equal outcomes (used as a control) enhanced cooperative performance, most likely through motivational processes rather than the absence of inequity aversion. In Experiment 2, performance dropped off dramatically when the chimpanzees were not rewarded on every trial. Their strategy was irrational as donating effort would have led to more rewards in the long run for each individual. Our results lead to a hierarchy of performances by condition with equity > inequity > donating effort. Chimpanzees therefore tolerate mild inequity, but cannot tolerate receiving nothing when others are rewarded.

Observational data reveal evidence and parameters of contagious yawning in the behavioral repertoire of captive-reared chimpanzees (Pan troglodytes).

There is robust experimental evidence for contagious yawning, yet observational studies of naturalistic behavior have been fewer. Without data from real-world behavior, researchers have questioned the existence of contagious yawning and made assumptions about some parameters (e.g., the duration of the effect). We observed contagious yawning in chimpanzees to confirm/disconfirm its existence in the behavioral repertoire of this species, and if present, provide some of the missing descriptives. We recorded yawns on an all-occurrence basis from 18 captive-reared chimpanzees at the Los Angeles Zoo. We recorded identity, time, and individuals who could have been affected. We calculated a threshold for contagion by taking the mean and adding 1.96 standard deviations, constructing a response curve. Across multiple measures we see a consistent pattern in which there is a strong effect of contagion for 1.5 minutes, a less strong but still significant effect lasting up to 3.5 minutes in some measures, and no evidence of contagion beyond 3.5 minutes. From the time stamp on each yawn we were able to rule out temporal synchrony as an alternative hypothesis. Thus, contagious yawning appears to be a natural phenomenon in chimpanzees lending support to the myriad experimental and observational studies to date.

Chimpanzee uses manipulative gaze cues to conceal and reveal information to foraging competitor.

Tactical deception has been widely reported in primates on a functional basis, but details of behavioral mechanisms are usually unspecified. We tested a pair of chimpanzees (Pan troglodytes) in the informed forager paradigm, in which the subordinate saw the location of hidden food and the dominant did not. We employed cross-correlations to examine temporal contingencies between chimpanzees' behavior: specifically how the direction of the subordinate's gaze and movement functioned to manipulate the dominant's searching behavior through two tactics, withholding, and misleading information. In Experiment 1, not only did the informed subordinate tend to stop walking toward a single high value food, but she also refrained from gazing toward it, thus, withholding potentially revealing cues from her searching competitor. In a second experiment, in which a moderate value food was hidden in addition to the high value food, whenever the subordinate alternated her gaze between the dominant and the moderate value food, she often paused walking for 5 s; this frequently recruited the dominant to the inferior food, functioning as a "decoy." The subordinate flexibly concealed and revealed gaze toward a goal, which suggests that not only can chimpanzees use visual cues to make predictions about behavior, but also that chimpanzees may understand that other individuals can exploit their gaze direction. These results substantiate descriptive reports of how chimpanzees use gaze to manipulate others, and to our knowledge are the first quantitative data to identify behavioral mechanisms of tactical deception. RESEARCH HIGHLIGHTS: Cross correlations show a subordinate chimpanzee tactically deceived a dominant by not gazing toward a valuable food (withholding), and recruiting to a "decoy" food (misleading). Chimpanzees understand that others can exploit their gaze direction.

How chimpanzees cooperate in a competitive world.

Our species is routinely depicted as unique in its ability to achieve cooperation, whereas our closest relative, the chimpanzee (Pan troglodytes), is often characterized as overly competitive. Human cooperation is assisted by the cost attached to competitive tendencies through enforcement mechanisms, such as punishment and partner choice. To examine if chimpanzees possess the same ability to mitigate competition, we set up a cooperative task in the presence of the entire group of 11 adults, which required two or three individuals to pull jointly to receive rewards. This open-group set-up provided ample opportunity for competition (e.g., freeloading, displacements) and aggression. Despite this unique set-up and initial competitiveness, cooperation prevailed in the end, being at least five times as common as competition. The chimpanzees performed 3,565 cooperative acts while using a variety of enforcement mechanisms to overcome competition and freeloading, as measured by (attempted) thefts of rewards. These mechanisms included direct protest by the target, third-party punishment in which dominant individuals intervened against freeloaders, and partner choice. There was a marked difference between freeloading and displacement; freeloading tended to elicit withdrawal and third-party interventions, whereas displacements were met with a higher rate of direct retaliation. Humans have shown similar responses in controlled experiments, suggesting shared mechanisms across the primates to mitigate competition for the sake of cooperation.

Chimpanzees prefer African and Indian music over silence.

[Correction Notice: An Erratum for this article was reported in Vol 40(4) of Journal of Experimental Psychology: Animal Learning and Cognition (see record 2014-35305-001). For the article, the below files were used to create the audio used in this study. The original West African akan and North Indian raga pieces were used in their entirety and the Japanese taiko piece was used from the 0:19 second mark through the end. The tempo of each piece was adjusted so that they maintained an identical base tempo of 90 beats per minute, then looped to create 40 minutes of continuous music. Additionally, the volume of the music was standardized at 50 dB so that the all music maintained the same average amplitude. All audio manipulations were completed using GarageBand © (Apple Inc.).] All primates have an ability to distinguish between temporal and melodic features of music, but unlike humans, in previous studies, nonhuman primates have not demonstrated a preference for music. However, previous research has not tested the wide range of acoustic parameters present in many different types of world music. The purpose of the present study is to determine the spontaneous preference of common chimpanzees (Pan troglodytes) for 3 acoustically contrasting types of world music: West African akan, North Indian raga, and Japanese taiko. Sixteen chimpanzees housed in 2 groups were exposed to 40 min of music from a speaker placed 1.5 m outside the fence of their outdoor enclosure; the proximity of each subject to the acoustic stimulus was recorded every 2 min. When compared with controls, subjects spent significantly more time in areas where the acoustic stimulus was loudest in African and Indian music conditions. This preference for African and Indian music could indicate homologies in acoustic preferences between nonhuman and human primates. .

Ape duos and trios: spontaneous cooperation with free partner choice in chimpanzees.

The purpose of the present study was to push the boundaries of cooperation among captive chimpanzees (Pan troglodytes). There has been doubt about the level of cooperation that chimpanzees are able to spontaneously achieve or understand. Would they, without any pre-training or restrictions in partner choice, be able to develop successful joint action? And would they be able to extend cooperation to more than two partners, as they do in nature? Chimpanzees were given a chance to cooperate with multiple partners of their own choosing. All members of the group (N = 11) had simultaneous access to an apparatus that required two (dyadic condition) or three (triadic condition) individuals to pull in a tray baited with food. Without any training, the chimpanzees spontaneously solved the task a total of 3,565 times in both dyadic and triadic combinations. Their success rate and efficiency increased over time, whereas the amount of pulling in the absence of a partner decreased, demonstrating that they had learned the task contingencies. They preferentially approached the apparatus when kin or nonkin of similar rank were present, showing a preference for socially tolerant partners. The forced partner combinations typical of cooperation experiments cannot reveal these abilities, which demonstrate that in the midst of a complex social environment, chimpanzees spontaneously initiate and maintain a high level of cooperative behavior.

Using cross correlations to investigate how chimpanzees (Pan troglodytes) use conspecific gaze cues to extract and exploit information in a foraging competition.

In a dyadic informed forager task, chimpanzees (Pan troglodytes) are known to exploit the knowledge of informed subordinates; however, the behavioral mechanisms they employ are unknown. It is tempting to interpret outcome measures, such as which individual obtained the food, in a cognitively richer way than the outcomes may justify. We employed a different approach from prior research, asking how chimpanzees compete by maneuvering around each other, whether they use gaze cues to acquire information from others, and what information they use in moment-to-moment decision-making. We used cross correlations, which plot the correlation between two variables as a function of time, systematically to examine chimpanzee interactions in a series of dyadic informed forager contests. We used cross correlations as a "proof of concept" so as to determine whether the target actions were contingent on, or occurred in a time-locked pattern relative to, the referent actions. A subordinate individual was given privileged knowledge of food location. As expected, an ignorant dominant followed the informed subordinate's movement in the enclosure. The dominant also followed the subordinate's gaze direction: after she looked at the subordinate, she was more likely to gaze toward this same direction within one second. In contrast, the subordinate only occasionally followed the dominant's movement and gaze. The dominant also changed her own direction of movement to converge on the location to which the subordinate directed her gaze and movement. Cross correlation proves an effective technique for charting contingencies in social interactions, an important step in understanding the use of cognition in natural situations.

Chimpanzees empathize with group mates and humans, but not with baboons or unfamiliar chimpanzees.

Human empathy can extend to strangers and even other species, but it is unknown whether non-humans are similarly broad in their empathic responses. We explored the breadth and flexibility of empathy in chimpanzees, a close relative of humans. We used contagious yawning to measure involuntary empathy and showed chimpanzees videos of familiar humans, unfamiliar humans and gelada baboons (an unfamiliar species). We tested whether each class of stimuli elicited contagion by comparing the effect of yawn and control videos. After including previous data on the response to ingroup and outgroup chimpanzees, we found that familiar and unfamiliar humans elicited contagion equal to that of ingroup chimpanzees. Gelada baboons did not elicit contagion, and the response to them was equal to that of outgroup chimpanzees. However, the chimpanzees watched the outgroup chimpanzee videos more than any other. The combination of high interest and low contagion may stem from hostility towards unfamiliar chimpanzees, which may interfere with an empathic response. Overall, chimpanzees showed flexibility in that they formed an empathic connection with a different species, including unknown members of that species. These results imply that human empathic flexibility is shared with related species.

Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy.

Humans favor others seen as similar to themselves (ingroup) over people seen as different (outgroup), even without explicitly stated bias. Ingroup-outgroup bias extends to involuntary responses, such as empathy for pain. However, empathy biases have not been tested in our close primate relatives. Contagious yawning has been theoretically and empirically linked to empathy. If empathy underlies contagious yawning, we predict that subjects should show an ingroup-outgroup bias by yawning more in response to watching ingroup members yawn than outgroup. Twenty-three chimpanzees (Pan troglodytes) from two separate groups watched videos of familiar and unfamiliar individuals yawning or at rest (control). The chimpanzees yawned more when watching the familiar yawns than the familiar control or the unfamiliar yawns, demonstrating an ingroup-outgroup bias in contagious yawning. These results provide further empirical support that contagious yawning is a measure of empathy, which may be useful for evolutionary biology and mental health.

Methodological problems in the study of contagious yawning.

The recent interest in contagious yawning has raised several challenges as the varied methods of testing have left some unresolved issues. We do not know how differences in key variables affect the observed rates of yawning, and we highlight these as being in need of direct testing. Different researchers analyze their results differently, and we make some recommendations for more rigorous, thorough and informative analyses. Ultimately, problems arise when authors compare studies that used different methods and different analyses without acknowledging how these differences may have affected the results. In these cases, authors make inappropriate comparisons, which lead to conclusions that add confusion to the literature. Our goal in raising awareness of these issues is to generate new experiments and improve the discussion of existing research. With its link to empathy, a more standardized study of contagious yawning may be a useful tool for a variety of disciplines.

Computer animations stimulate contagious yawning in chimpanzees.

People empathize with fictional displays of behaviour, including those of cartoons and computer animations, even though the stimuli are obviously artificial. However, the extent to which other animals also may respond empathetically to animations has yet to be determined. Animations provide a potentially useful tool for exploring non-human behaviour, cognition and empathy because computer-generated stimuli offer complete control over variables and the ability to program stimuli that could not be captured on video. Establishing computer animations as a viable tool requires that non-human subjects identify with and respond to animations in a way similar to the way they do to images of actual conspecifics. Contagious yawning has been linked to empathy and poses a good test of involuntary identification and motor mimicry. We presented 24 chimpanzees with three-dimensional computer-animated chimpanzees yawning or displaying control mouth movements. The apes yawned significantly more in response to the yawn animations than to the controls, implying identification with the animations. These results support the phenomenon of contagious yawning in chimpanzees and suggest an empathic response to animations. Understanding how chimpanzees connect with animations, to both empathize and imitate, may help us to understand how humans do the same.

Captive-born cotton-top tamarins (Saguinus oedipus) respond similarly to vocalizations of predators and sympatric nonpredators.

What types of cues do callitrichid primates use to detect and respond to predators? Do they respond to predator-specific cues or to more general cues? The evidence for these questions remains conflicting. We presented captive-born and reared cotton-top tamarins with no previous exposure to predators (or predator cues) with vocalizations from three potential predators of cotton-top tamarin in the wild (white hawk, jaguar, and tayra) and with vocalizations from sympatric nonpredators (black-faced antthrush and red howler monkey). Vocalizations from predators and from nonpredator mammals elicited equivalent arousal, fear, and vocal responses. Howler monkey roars produced the strongest responses. The results suggest that predator-naïve cotton-top tamarins do not recognize specific predator vocalizations, but may respond to vocal qualities (low-frequency, noisy sounds) that indicate large body size, threat, or aggression. On the other hand, tamarins responded much more strongly to the higher frequency calls from the hawk than the antthrush, suggesting another mechanism must also be involved. The failure of captive-reared tamarins to distinguish between vocalizations of predators and nonpredator mammals has important implications for reintroduction studies.

Racial bias in decisions made by mock jurors evaluating a case of sexual harassment.

White (N = 161) and Black (N = 152) college students served as mock jurors in a simulated civil case in which a female plaintiff accused a male defendant of sexual harassment. The authors experimentally manipulated the race (Black or White) of the litigants and asked the mock jurors to decide whether the defendant was guilty; to rate the certainty of their belief in the defendant's guilt; and, when they judged the defendant guilty, to recommend an award to the plaintiff. Mock jurors of both races tended to favor litigants of their own race and their own gender. Racial bias was highest among White male jurors and lowest among White female jurors.