Humans but Not Chimpanzees Vary Face-Scanning Patterns Depending on Contexts during Action Observation

Human and nonhuman primates comprehend the actions of other individuals by detecting social cues, including others’ goal-directed motor actions and faces. However, little is known about how this information is integrated with action understanding. Here, we present the ontogenetic and evolutionary foundations of this capacity by comparing face-scanning patterns of chimpanzees and humans as they viewed goal-directed human actions within contexts that differ in whether or not the predicted goal is achieved. Human adults and children attend to the actor’s face during action sequences, and this tendency is particularly pronounced in adults when observing that the predicted goal is not achieved. Chimpanzees rarely attend to the actor’s face during the goal-directed action, regardless of whether the predicted action goal is achieved or not. These results suggest that in humans, but not chimpanzees, attention to actor’s faces conveying referential information toward the target object indicates the process of observers making inferences about the intentionality of an action. Furthermore, this remarkable predisposition to observe others’ actions by integrating the prediction of action goals and the actor’s intention is developmentally acquired.     

Dogs Evaluate Threatening Facial Expressions by Their Biological Validity – Evidence from Gazing Patterns

Appropriate response to companions’ emotional signals is important for all social creatures. The emotional expressions of humans and non-human animals have analogies in their form and function, suggesting shared evolutionary roots, but very little is known about how animals other than primates view and process facial expressions. In primates, threat-related facial expressions evoke exceptional viewing patterns compared with neutral or positive stimuli. Here, we explore if domestic dogs (Canis familiaris) have such an attentional bias toward threatening social stimuli and whether observed emotional expressions affect dogs’ gaze fixation distribution among the facial features (eyes, midface and mouth). We recorded the voluntary eye gaze of 31 domestic dogs during viewing of facial photographs of humans and dogs with three emotional expressions (threatening, pleasant and neutral). We found that dogs’ gaze fixations spread systematically among facial features. The distribution of fixations was altered by the seen expression, but eyes were the most probable targets of the first fixations and gathered longer looking durations than mouth regardless of the viewed expression. The examination of the inner facial features as a whole revealed more pronounced scanning differences among expressions. This suggests that dogs do not base their perception of facial expressions on the viewing of single structures, but the interpretation of the composition formed by eyes, midface and mouth. Dogs evaluated social threat rapidly and this evaluation led to attentional bias, which was dependent on the depicted species: threatening conspecifics’ faces evoked heightened attention but threatening human faces instead an avoidance response. We propose that threatening signals carrying differential biological validity are processed via distinctive neurocognitive pathways. Both of these mechanisms may have an adaptive significance for domestic dogs. The findings provide a novel perspective on understanding the processing of emotional expressions and sensitivity to social threat in non-primates.     

Sex Differences in Object Manipulation in Wild Immature Chimpanzees (Pan troglodytes schweinfurthii) and Bonobos (Pan paniscus): Preparation for Tool Use?

Sex differences in immatures predict behavioural differences in adulthood in many mammal species. Because most studies have focused on sex differences in social interactions, little is known about possible sex differences in ‘preparation’ for adult life with regards to tool use skills. We investigated sex and age differences in object manipulation in immature apes. Chimpanzees use a variety of tools across numerous contexts, whereas bonobos use few tools and none in foraging. In both species, a female bias in adult tool use has been reported. We studied object manipulation in immature chimpanzees at Kalinzu (Uganda) and bonobos at Wamba (Democratic Republic of Congo). We tested predictions of the ‘preparation for tool use’ hypothesis. We confirmed that chimpanzees showed higher rates and more diverse types of object manipulation than bonobos. Against expectation, male chimpanzees showed higher object manipulation rates than females, whereas in bonobos no sex difference was found. However, object manipulation by male chimpanzees was play-dominated, whereas manipulation types of female chimpanzees were more diverse (e.g., bite, break, carry). Manipulation by young immatures of both species was similarly dominated by play, but only in chimpanzees did it become more diverse with age. Moreover, in chimpanzees, object types became more tool-like (i.e., sticks) with age, further suggesting preparation for tool use in adulthood. The male bias in object manipulation in immature chimpanzees, along with the late onset of tool-like object manipulation, indicates that not all (early) object manipulation (i.e., object play) in immatures prepares for subsistence tool use. Instead, given the similarity with gender differences in human children, object play may also function in motor skill practice for male-specific behaviours (e.g., dominance displays). In conclusion, even though immature behaviours almost certainly reflect preparation for adult roles, more detailed future work is needed to disentangle possible functions of object manipulation during development.     

The Right Time to Happen: Play Developmental Divergence in the Two Pan Species

Bonobos, compared to chimpanzees, are highly motivated to play as adults. Therefore, it is interesting to compare the two species at earlier developmental stages to determine how and when these differences arise. We measured and compared some play parameters between the two species including frequency, number of partners (solitary, dyadic, and polyadic play), session length, and escalation into overt aggression. Since solitary play has a role in developing cognitive and physical skills, it is not surprising that chimpanzees and bonobos share similar developmental trajectories in the motivation to engage in this activity. The striking divergence in play developmental pathways emerged for social play. Infants of the two species showed comparable social play levels, which began to diverge during the juvenile period, a ‘timing hotspot’ for play development. Compared to chimpanzees, social play sessions in juvenile bonobos escalated less frequently into overt aggression, lasted longer, and frequently involved more than two partners concurrently (polyadic play). In this view, play fighting in juvenile bonobos seems to maintain a cooperative mood, whereas in juvenile chimpanzees it acquires more competitive elements. The retention of juvenile traits into adulthood typical of bonobos can be due to a developmental delay in social inhibition. Our findings show that the divergence of play ontogenetic pathways between the two Pan species and the relative emergence of play neotenic traits in bonobos can be detected before individuals reach sexual maturity. The high play motivation showed by adult bonobos compared to chimpanzees is probably the result of a long developmental process, rooted in the delicate transitional phase, which leads subjects from infancy to juvenility.     

Differences in the Cognitive Skills of Bonobos and Chimpanzees

While bonobos and chimpanzees are both genetically and behaviorally very similar, they also differ in significant ways. Bonobos are more cautious and socially tolerant while chimpanzees are more dependent on extractive foraging, which requires tools. The similarities suggest the two species should be cognitively similar while the behavioral differences predict where the two species should differ cognitively. We compared both species on a wide range of cognitive problems testing their understanding of the physical and social world. Bonobos were more skilled at solving tasks related to theory of mind or an understanding of social causality, while chimpanzees were more skilled at tasks requiring the use of tools and an understanding of physical causality. These species differences support the role of ecological and socio-ecological pressures in shaping cognitive skills over relatively short periods of evolutionary time.     

Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): Implications for natural social systems and interindividual relationships

This study compares adult play behavior in the two Pan species in order to test the effects of phylogenetic closeness and the nature of social systems on play distribution. The social play (both with fertile and immature subjects) performed by adults did not differ between the two species. In contrast, in bonobos, play levels among fertile subjects were higher than in chimpanzees. Findings regarding levels of undecided conflicts (more frequent in bonobos) and formal submission displays (lacking in bonobos) confirm, in the two colonies under study, that bonobos exhibit "egalitarianism" more than chimpanzees. Some authors emphasized the importance of play-fighting for social assessment when relationships among individuals are not codified and structured according to rank-rules. Indeed, adult bonobos played more roughly than chimpanzees. Moreover, adult bonobos displayed the full play-face at a high frequency especially during rough play sessions, whereas in chimpanzees, the frequency of play signals was not affected by roughness of play. The frequency of social play among bonobo females was higher than in any other sex combinations, whereas no difference was found for chimpanzees. As a matter of fact, social play can be viewed as a balance between cooperation and competition. Among bonobo females, characterized by social competence and affiliation, social play might enhance their behavioral flexibility and increase their socially symmetrical relationships which, after all, are the basis for their egalitarian society.     

Salient eyes deter conspecific nest intruders in wild jackdaws (Corvus monedula)

Animals often respond fearfully when encountering eyes or eye-like shapes. Although gaze aversion has been documented in mammals when avoiding group-member conflict, the importance of eye coloration during interactions between conspecifics has yet to be examined in non-primate species. Jackdaws (Corvus monedula) have near-white irides, which are conspicuous against their dark feathers and visible when seen from outside the cavities where they nest. Because jackdaws compete for nest sites, their conspicuous eyes may act as a warning signal to indicate that a nest is occupied and deter intrusions by conspecifics. We tested whether jackdaws’ pale irides serve as a deterrent to prospecting conspecifics by comparing prospectors’ behaviour towards nest-boxes displaying images with bright eyes (BEs) only, a jackdaw face with natural BEs, or a jackdaw face with dark eyes. The jackdaw face with BEs was most effective in deterring birds from making contact with nest-boxes, whereas both BE conditions reduced the amount of time jackdaws spent in proximity to the image. We suggest BEs in jackdaws may function to prevent conspecific competitors from approaching occupied nest sites.     

Preference for Orientations Commonly Viewed for One’s Own Hand in the Anterior Intraparietal Cortex

Brain regions in the intraparietal and the premotor cortices selectively process visual and multisensory events near the hands (peri-hand space). Visual information from the hand itself modulates this processing potentially because it is used to estimate the location of one’s own body and the surrounding space. In humans specific occipitotemporal areas process visual information of specific body parts such as hands. Here we used an fMRI block-design to investigate if anterior intraparietal and ventral premotor ‘peri-hand areas’ exhibit selective responses to viewing images of hands and viewing specific hand orientations. Furthermore, we investigated if the occipitotemporal ‘hand area’ is sensitive to viewed hand orientation. Our findings demonstrate increased BOLD responses in the left anterior intraparietal area when participants viewed hands and feet as compared to faces and objects. Anterior intraparietal and also occipitotemporal areas in the left hemisphere exhibited response preferences for viewing right hands with orientations commonly viewed for one’s own hand as compared to uncommon own hand orientations. Our results indicate that both anterior intraparietal and occipitotemporal areas encode visual limb-specific shape and orientation information.     

Putting Culture Under the ‘Spotlight’ Reveals Universal Information Use for Face Recognition

Background

Eye movement strategies employed by humans to identify conspecifics are not universal. Westerners predominantly fixate the eyes during face recognition, whereas Easterners more the nose region, yet recognition accuracy is comparable. However, natural fixations do not unequivocally represent information extraction. So the question of whether humans universally use identical facial information to recognize faces remains unresolved.

Methodology/Principal Findings

We monitored eye movements during face recognition of Western Caucasian (WC) and East Asian (EA) observers with a novel technique in face recognition that parametrically restricts information outside central vision. We used ‘Spotlights’ with Gaussian apertures of 2°, 5° or 8° dynamically centered on observers'' fixations. Strikingly, in constrained Spotlight conditions (2° and 5°) observers of both cultures actively fixated the same facial information: the eyes and mouth. When information from both eyes and mouth was simultaneously available when fixating the nose (8°), as expected EA observers shifted their fixations towards this region.

Conclusions/Significance

Social experience and cultural factors shape the strategies used to extract information from faces, but these results suggest that external forces do not modulate information use. Human beings rely on identical facial information to recognize conspecifics, a universal law that might be dictated by the evolutionary constraints of nature and not nurture.     

Social orienting in gaze leading: a mechanism for shared attention

Here, we report a novel social orienting response that occurs after viewing averted gaze. We show, in three experiments, that when a person looks from one location to an object, attention then shifts towards the face of an individual who has subsequently followed the person''s gaze to that same object. That is, contrary to ‘gaze following’, attention instead orients in the opposite direction to observed gaze and towards the gazing face. The magnitude of attentional orienting towards a face that ‘follows’ the participant''s gaze is also associated with self-reported autism-like traits. We propose that this gaze leading phenomenon implies the existence of a mechanism in the human social cognitive system for detecting when one''s gaze has been followed, in order to establish ‘shared attention’ and maintain the ongoing interaction.     

Social Interactions through the Eyes of Macaques and Humans

Group-living primates frequently interact with each other to maintain social bonds as well as to compete for valuable resources. Observing such social interactions between group members provides individuals with essential information (e.g. on the fighting ability or altruistic attitude of group companions) to guide their social tactics and choice of social partners. This process requires individuals to selectively attend to the most informative content within a social scene. It is unclear how non-human primates allocate attention to social interactions in different contexts, and whether they share similar patterns of social attention to humans. Here we compared the gaze behaviour of rhesus macaques and humans when free-viewing the same set of naturalistic images. The images contained positive or negative social interactions between two conspecifics of different phylogenetic distance from the observer; i.e. affiliation or aggression exchanged by two humans, rhesus macaques, Barbary macaques, baboons or lions. Monkeys directed a variable amount of gaze at the two conspecific individuals in the images according to their roles in the interaction (i.e. giver or receiver of affiliation/aggression). Their gaze distribution to non-conspecific individuals was systematically varied according to the viewed species and the nature of interactions, suggesting a contribution of both prior experience and innate bias in guiding social attention. Furthermore, the monkeys’ gaze behavior was qualitatively similar to that of humans, especially when viewing negative interactions. Detailed analysis revealed that both species directed more gaze at the face than the body region when inspecting individuals, and attended more to the body region in negative than in positive social interactions. Our study suggests that monkeys and humans share a similar pattern of role-sensitive, species- and context-dependent social attention, implying a homologous cognitive mechanism of social attention between rhesus macaques and humans.     

Oxytocin and Vasopressin Receptor Gene Variation as a Proximate Base for Inter- and Intraspecific Behavioral Differences in Bonobos and Chimpanzees

Recent literature has revealed the importance of variation in neuropeptide receptor gene sequences in the regulation of behavioral phenotypic variation. Here we focus on polymorphisms in the oxytocin receptor gene (OXTR) and vasopressin receptor gene 1a (Avpr1a) in chimpanzees and bonobos. In humans, a single nucleotide polymorphism (SNP) in the third intron of OXTR (rs53576 SNP (A/G)) is linked with social behavior, with the risk allele (A) carriers showing reduced levels of empathy and prosociality. Bonobos and chimpanzees differ in these same traits, therefore we hypothesized that these differences might be reflected in variation at the rs53576 position. We sequenced a 320 bp region surrounding rs53576 but found no indications of this SNP in the genus Pan. However, we identified previously unreported SNP variation in the chimpanzee OXTR sequence that differs from both humans and bonobos. Humans and bonobos have previously been shown to have a more similar 5′ promoter region of Avpr1a when compared to chimpanzees, who are polymorphic for the deletion of ∼360 bp in this region (+/− DupB) which includes a microsatellite (RS3). RS3 has been linked with variation in levels of social bonding, potentially explaining part of the interspecies behavioral differences found in bonobos, chimpanzees and humans. To date, results for bonobos have been based on small sample sizes. Our results confirmed that there is no DupB deletion in bonobos with a sample size comprising approximately 90% of the captive founder population, whereas in chimpanzees the deletion of DupB had the highest frequency. Because of the higher frequency of DupB alleles in our bonobo population, we suggest that the presence of this microsatellite may partly reflect documented differences in levels of sociability found in bonobos and chimpanzees.     

Tolerance and Social Facilitation in the Foraging Behaviour of Free‐Ranging Crows (Corvus corone corone; C. c. cornix)

Social foraging provides animals with opportunities to gain knowledge about available food. Studies indicate that animals are influenced by social context during exploration and are able to learn socially. Carrion and hooded crows, which are opportunistic generalists with flexible social systems, have so far received little focus in this area. We combined observational and experimental approaches to investigate social interactions during foraging and social influences on crow behaviour within a free‐ranging population at Vienna Zoo, which included 115 individually marked crows. We expected the crows to be tolerant of conspecifics during foraging due to high food abundance. We predicted that social context would enhance familiar object exploration, as well as a specific foraging strategy: predation by crows on other species. We found that crows were highly tolerant of one another, as reflected by their high rates of cofeeding – where they fed directly beside conspecific(s) – relative to affiliative or agonistic interactions. Evidence for social facilitation – when the observer's behaviour is affected by the mere presence of a model – was found in both object exploration and predation behaviour. Specifically, crows touched the objects more frequently when others were present (whilst only approaching the objects when alone), and conspecifics were present more frequently during predation events involving the high‐risk target species. Evidence for enhancement during object exploration – where the observer's attention is drawn to a place or object by a model's actions – was not confirmed in this context. Our results highlight the role played by the presence of conspecifics across different contexts: natural foraging behaviour, familiar object exploration and a specific foraging strategy. To our knowledge, this is one of the first corvid studies aimed at teasing apart specific social influence and learning mechanisms in the field. These crows therefore make promising candidates for studying social learning and its consequences under naturalistic conditions.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

It’s All in the Eyes: Subcortical and Cortical Activation during Grotesqueness Perception in Autism

Atypical face processing plays a key role in social interaction difficulties encountered by individuals with autism. In the current fMRI study, the Thatcher illusion was used to investigate several aspects of face processing in 20 young adults with high-functioning autism spectrum disorder (ASD) and 20 matched neurotypical controls. “Thatcherized” stimuli were modified at either the eyes or the mouth and participants discriminated between pairs of faces while cued to attend to either of these features in upright and inverted orientation. Behavioral data confirmed sensitivity to the illusion and intact configural processing in ASD. Directing attention towards the eyes vs. the mouth in upright faces in ASD led to (1) improved discrimination accuracy; (2) increased activation in areas involved in social and emotional processing; (3) increased activation in subcortical face-processing areas. Our findings show that when explicitly cued to attend to the eyes, activation of cortical areas involved in face processing, including its social and emotional aspects, can be enhanced in autism. This suggests that impairments in face processing in autism may be caused by a deficit in social attention, and that giving specific cues to attend to the eye-region when performing behavioral therapies aimed at improving social skills may result in a better outcome.     

Co–Residence between Males and Their Mothers and Grandmothers Is More Frequent in Bonobos Than Chimpanzees

In long–lived social mammals such as primates, individuals can benefit from social bonds with close kin, including their mothers. In the patrilocal chimpanzee (Pan troglodytes spp.) and bonobo (Pan paniscus), sexually mature males reside and reproduce in their natal groups and can retain post-dependency bonds with their mothers, while immatures of both sexes might also have their paternal grandmothers available. However, quantitative information on the proportion of males and immatures that co-reside with both types of these close female relatives is limited for both species. Combining genetic parentage determination and group composition data from five communities of wild chimpanzees and three communities of wild bonobos, we estimated the frequency of co-residence between (1) mature males and their mothers, and (2) immature males and females and their paternal grandmothers. We found that adult males resided twice as frequently with their mothers in bonobos than in chimpanzees, and that immature bonobos were three times more likely to possess a living paternal grandmother than were immature chimpanzees. Patterns of female and male survivorship from studbook records of captive individuals of both species suggest that mature bonobo females survive longer than their chimpanzee counterparts, possibly contributing to the differences observed in mother–son and grandmother–immature co-residency levels. Taking into account reports of bonobo mothers supporting their sons'' mating efforts and females sharing food with immatures other than their own offspring, our findings suggest that life history traits may facilitate maternal and grandmaternal support more in bonobos than in chimpanzees.     

Differential sensitivity to conspecific and allospecific cues in chimpanzees and humans: a comparative eye-tracking study

Previous studies have shown that a variety of animals including humans are sensitive to social cues from others and shift their attention to the same objects attended to by others. However, little is known about how animals process conspecifics'' and another species'' actions, although primates recognize conspecific faces better than those of another species. In this study, using unrestrained eye-tracking techniques, we first demonstrated that conspecific social cues modulated looking behaviours of chimpanzees more than human cues, whereas human observers were equally sensitive to both species. Additionally, first pass gaze duration at the face indicates that chimpanzees looked at the chimpanzees'' face longer than the human face, suggesting that chimpanzees might extract more referential information from a conspecific face. These results also imply that a unique ability for extracting referential information from a variety of social objects has emerged during human evolution.     

Female Genito-genital Rubbing in a Group of Captive Chimpanzees

Wild and captive female bonobos exhibit a form of noncopulatory sexual behavior—genito-genital (GG) rubbing—in which 2 individuals rub their genital regions together. GG-rubbing in bonobos occurs in several contexts and may serve several functions, including tension reduction and reconciliation. It has not been reported for chimpanzees. In a study of captive, adolescent chimpanzees at the New Iberia Research Center, I observed that females rubbed genital regions at rates equivalent to those of bonobos, though the form of the behavior differed in significant ways from classic bonobo GG-rubbing. I describe the pattern of GG-rubbing in the chimpanzees and provide preliminary tests of 5 hypotheses for why the behavior occurs. All 4 females in the study group participated in GG-rubbing, though the frequency with which they initiated and participated varied. Females that GG-rubbed the most also groomed each other the most, supporting the hypothesis that GG-rubbing reinforces or at least reflects social bonds. The data do not support the hypothesis that females GG-rub to reconcile conflicts, to reduce tension during feeding, to signal social status, or to attract mates.     

The Influence of Shyness on the Scanning of Own- and Other-Race Faces in Adults

The current study explored the relationship between shyness and face scanning patterns for own- and other-race faces in adults. Participants completed a shyness inventory and a face recognition task in which their eye movements were recorded by a Tobii 1750 eye tracker. We found that: (1) Participants’ shyness scores were negatively correlated with the fixation proportion on the eyes, regardless of the race of face they viewed. The shyer the participants were, the less time they spent fixating on the eye region; (2) High shyness participants tended to fixate significantly more than low shyness participants on the regions just below the eyes as if to avoid direct eye contact; (3) When participants were recognizing own-race faces, their shyness scores were positively correlated with the normalized criterion. The shyer they were, the more apt they were to judge the faces as novel, regardless of whether they were target or foil faces. The present results support an avoidance hypothesis of shyness, suggesting that shy individuals tend to avoid directly fixating on others’ eyes, regardless of face race.     

Chimpanzees Show a Developmental Increase in Susceptibility to Contagious Yawning: A Test of the Effect of Ontogeny and Emotional Closeness on Yawn Contagion

Contagious yawning has been reported for humans, dogs and several non-human primate species, and associated with empathy in humans and other primates. Still, the function, development and underlying mechanisms of contagious yawning remain unclear. Humans and dogs show a developmental increase in susceptibility to yawn contagion, with children showing an increase around the age of four, when also empathy-related behaviours and accurate identification of others’ emotions begin to clearly evince. Explicit tests of yawn contagion in non-human apes have only involved adult individuals and examined the existence of conspecific yawn contagion. Here we report the first study of heterospecific contagious yawning in primates, and the ontogeny of susceptibility thereto in chimpanzees, Pan troglodytes verus. We examined whether emotional closeness, defined as attachment history with the yawning model, affected the strength of contagion, and compared the contagiousness of yawning to nose-wiping. Thirty-three orphaned chimpanzees observed an unfamiliar and familiar human (their surrogate human mother) yawn, gape and nose-wipe. Yawning, but not nose-wiping, was contagious for juvenile chimpanzees, while infants were immune to contagion. Like humans and dogs, chimpanzees are subject to a developmental trend in susceptibility to contagious yawning, and respond to heterospecific yawn stimuli. Emotional closeness with the model did not affect contagion. The familiarity-biased social modulatory effect on yawn contagion previously found among some adult primates, seem to only emerge later in development, or be limited to interactions with conspecifics. The influence of the ‘chameleon effect’, targeted vs. generalised empathy, perspective-taking and visual attention on contagious yawning is discussed.