Gestural communication in young gorillas (Gorilla gorilla): gestural repertoire,learning, and use

In the present study we investigated the gestural communication of gorillas (Gorilla gorilla). The subjects were 13 gorillas (1-6 years old) living in two different groups in captivity. Our goal was to compile the gestural repertoire of subadult gorillas, with a special focus on processes of social cognition, including attention to individual and developmental variability, group variability, and flexibility of use. Thirty-three different gestures (six auditory, 11 tactile, and 16 visual gestures) were recorded. We found idiosyncratic gestures, individual differences, and similar degrees of concordance between and within groups, as well as some group-specific gestures. These results provide evidence that ontogenetic ritualization is the main learning process involved, but some form of social learning may also be responsible for the acquisition of special gestures. The present study establishes that gorillas have a multifaceted gestural repertoire, characterized by a great deal of flexibility with accommodations to various communicative circumstances, including the attentional state of the recipient. The possibility of assigning Seyfarth and Cheney's [1997] model for nonhuman primate vocal development to the development of nonhuman primate gestural communication is discussed.     

The learning and use of gestural signals by young chimpanzees: A trans-generational study

Observations of chimpanzee gestural communication are reported. The observations represent the third longitudinal time point of an ongoing study of the Yerkes Primate Center Field Station chimpanzee group. In contrast to observations at the first two time points, the current observations are of a new generation of infants and juveniles. There were two questions. The first concerned how young chimpanzees used their gestures, with special focus on the flexibility or intentionality displayed. It was found that youngsters quite often used the same gesture in different contexts, and different gestures in the same context. In addition, they sometimes used gestures in combinations in a single social encounter, these combinations did not convey intentions that could not be conveyed by the component gestures, however. It was also found that individuals adjusted their choice of signals depending on the attentional state of the recipient. The second question was how chimpanzees acquired their gestural signals. In general, it was found that there was little consistency in the use of gestures among individuals, especially for non-play gestures, with much individual variability both within and across generations. There were also a number of idiosyncratic gestures used by single individuals at each time point. It was concluded from these results that youngsters were not imitatively learning their communicatory gestures from conspecifics, but rather that they were individually conventionalizing them with each other. Implications of these findings for the understanding of chimpanzee communication and social learning are discussed.     

To Beg,or Not to Beg? That Is the Question: Mangabeys Modify Their Production of Requesting Gestures in Response to Human’s Attentional States

Background

Although gestural communication is widespread in primates, few studies focused on the cognitive processes underlying gestures produced by monkeys.

Methodology/Principal Findings

The present study asked whether red-capped mangabeys (Cercocebus torquatus) trained to produce visually based requesting gestures modify their gestural behavior in response to human’s attentional states. The experimenter held a food item and displayed five different attentional states that differed on the basis of body, head and gaze orientation; mangabeys had to request food by extending an arm toward the food item (begging gesture). Mangabeys were sensitive, at least to some extent, to the human’s attentional state. They reacted to some postural cues of a human recipient: they gestured more and faster when both the body and the head of the experimenter were oriented toward them than when they were oriented away. However, they did not seem to use gaze cues to recognize an attentive human: monkeys begged at similar levels regardless of the experimenter’s eyes state.

Conclusions/Significance

These results indicate that mangabeys lowered their production of begging gestures when these could not be perceived by the human who had to respond to it. This finding provides important evidence that acquired begging gestures of monkeys might be used intentionally.     

What Role Do Mothers Play in the Gestural Acquisition of Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)?

Contemporary research hypothesizes that biological inheritance and ontogenetic factors shape the development of gestural communication in nonhuman great apes. However, little is known about the specific role that mothers play in the acquisition of their infants’ gestures. We observed 6 bonobo (Pan paniscus) and 4 chimpanzee (Pan troglodytes) mother–infant dyads and recorded their gesture types and frequency. We analyzed all behavioral contexts in which gestures occurred as well as the play context alone. Infants of both species were unlikely to share gestures with their mother or unrelated adult females. However, gestural sharing was prevalent within age groups. Within and across species, infant–infant and mother–mother groups were homogeneous regarding the types of gestures they shared, although there was individual variation in the frequency of gesture use. Our findings provide limited evidence that infants learned their gestures by imitating their mothers. Phylogenetic influences seem to be vital in gestural acquisition but, we suggest, repertoire development cannot be disentangled from individual social encounters during life.     

Multi-Modal Use of a Socially Directed Call in Bonobos

‘Contest hoots’ are acoustically complex vocalisations produced by adult and subadult male bonobos (Pan paniscus). These calls are often directed at specific individuals and regularly combined with gestures and other body signals. The aim of our study was to describe the multi-modal use of this call type and to clarify its communicative and social function. To this end, we observed two large groups of bonobos, which generated a sample of 585 communicative interactions initiated by 10 different males. We found that contest hooting, with or without other associated signals, was produced to challenge and provoke a social reaction in the targeted individual, usually agonistic chase. Interestingly, ‘contest hoots’ were sometimes also used during friendly play. In both contexts, males were highly selective in whom they targeted by preferentially choosing individuals of equal or higher social rank, suggesting that the calls functioned to assert social status. Multi-modal sequences were not more successful in eliciting reactions than contest hoots given alone, but we found a significant difference in the choice of associated gestures between playful and agonistic contexts. During friendly play, contest hoots were significantly more often combined with soft than rough gestures compared to agonistic challenges, while the calls'' acoustic structure remained the same. We conclude that contest hoots indicate the signaller''s intention to interact socially with important group members, while the gestures provide additional cues concerning the nature of the desired interaction.     

The origins of gestures and language: history,current advances and proposed theories

Investigating in depth the mechanisms underlying human and non‐human primate intentional communication systems (involving gestures, vocalisations, facial expressions and eye behaviours) can shed light on the evolutionary roots of language. Reports on non‐human primates, particularly great apes, suggest that gestural communication would have been a crucial prerequisite for the emergence of language, mainly based on the evidence of large communication repertoires and their associated multifaceted nature of intentionality that are key properties of language. Such research fuels important debates on the origins of gestures and language. We review here three non‐mutually exclusive processes that can explain mainly great apes' gestural acquisition and development: phylogenetic ritualisation, ontogenetic ritualisation, and learning via social negotiation. We hypothesise the following scenario for the evolutionary origins of gestures: gestures would have appeared gradually through evolution via signal ritualisation following the principle of derived activities, with the key involvement of emotional expression and processing. The increasing level of complexity of socioecological lifestyles and associated daily manipulative activities might then have enabled the acquisition and development of different interactional strategies throughout the life cycle. Many studies support a multimodal origin of language. However, we stress that the origins of language are not only multimodal, but more broadly multicausal. We propose a multicausal theory of language origins which better explains current findings. It postulates that primates' communicative signalling is a complex trait continually shaped by a cost–benefit trade‐off of signal production and processing of interactants in relation to four closely interlinked categories of evolutionary and life cycle factors: species, individual and context‐related characteristics as well as behaviour and its characteristics. We conclude by suggesting directions for future research to improve our understanding of the evolutionary roots of gestures and language.     

Social games between bonobos and humans: evidence for shared intentionality?

Triadic social games are interesting from a cognitive perspective because they require a high degree of mutual social awareness. They consist of two agents incorporating an object in turn-taking sequences and require individuals to coordinate their attention to the task, the object, and to one another. Social games are observed commonly in domesticated dogs interacting with humans, but they have received only little empirical attention in nonhuman primates. Here, we report observations of bonobos (Pan paniscus) engaging in social games with a human playmate. Our behavioral analyses revealed that the bonobos behaved in many ways similar to human children during these games. They were interested in the joint activity, rather than the play objects themselves, and used communicative gestures to encourage reluctant partners to perform their role, suggesting rudimentary understanding of others' intentions. Our observations thus may imply that shared intentionality, the ability to understand and shares intention with other individuals, has emerged in the primate lineage before the origins of hominids.     

Social communication in siamangs (<Emphasis Type="Italic">Symphalangus syndactylus</Emphasis>): use of gestures and facial expressions

The current study represents the first systematic investigation of the social communication of captive siamangs (Symphalangus syndactylus). The focus was on intentional signals, including tactile and visual gestures, as well as facial expressions and actions. Fourteen individuals from different groups were observed and the signals used by individuals were recorded. Thirty-one different signals, consisting of 12 tactile gestures, 8 visual gestures, 7 actions, and 4 facial expressions, were observed, with tactile gestures and facial expressions appearing most frequently. The range of the signal repertoire increased steadily until the age of six, but declined afterwards in adults. The proportions of the different signal categories used within communicative interactions, in particular actions and facial expressions, also varied depending on age. Group differences could be traced back mainly to social factors or housing conditions. Differences in the repertoire of males and females were most obvious in the sexual context. Overall, most signals were used flexibly, with the majority performed in three or more social contexts and almost one-third of signals used in combination with other signals. Siamangs also adjusted their signals appropriately for the recipient, for example, using visual signals most often when the recipient was already attending (audience effects). These observations are discussed in the context of siamang ecology, social structure, and cognition.To see video sequences of signals described here, please go to     

Do Mechanical Effectiveness and Recipient Species Influence Intentional Signal Laterality in Captive Chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>)?

Studying the relationships between the directions of brain lateralization for handedness and language can shed light on mechanisms underlying hemispheric specialization for manipulation and signalling functions. We investigated the influence of manipulation and communication functions and of recipient species (conspecific- versus human-directed communication) on manual laterality in signalling context, taking several factors into account simultaneously. We assessed laterality in 39 chimpanzees (Pan troglodytes), including 4 manipulators (mechanically effective social actions used to get things done) and 18 gestures (mechanically ineffective social actions implying that the signaller takes the recipient’s response into account). We focused on the following factors: interactional context components (e.g., visual fields of both interactants), degree of use of signals (“rare” for signals performed by only a few subjects in the population or “common” for signals performed by many subjects), mechanical effectiveness, subjects’ sociodemographic characteristics (e.g., age and hierarchy), and recipient species. We found a significant population-level right-hand bias for one type of human-directed gesture (slap hand). Mechanical effectiveness influenced laterality: right-hand use was more pronounced for conspecific-directed gestures than for conspecific-directed manipulators. The laterality of conspecific-directed gestures overall did not differ from that of human-directed gestures. However, we found an indirect influence of recipient species on laterality as conspecific- and human-directed gestural lateralities were modulated differently by the position of the recipient in the signaller’s visual field and by signaller’s age. We hypothesize that the communication nature of gestures might have developed from manipulators. Manipulators may have contributed to the emergence and the evolution of the left-lateralized communication system in primates.     

Chimpanzee vocal signaling points to a multimodal origin of human language

The evolutionary origin of human language and its neurobiological foundations has long been the object of intense scientific debate. Although a number of theories have been proposed, one particularly contentious model suggests that human language evolved from a manual gestural communication system in a common ape-human ancestor. Consistent with a gestural origins theory are data indicating that chimpanzees intentionally and referentially communicate via manual gestures, and the production of manual gestures, in conjunction with vocalizations, activates the chimpanzee Broca's area homologue--a region in the human brain that is critical for the planning and execution of language. However, it is not known if this activity observed in the chimpanzee Broca's area is the result of the chimpanzees producing manual communicative gestures, communicative sounds, or both. This information is critical for evaluating the theory that human language evolved from a strictly manual gestural system. To this end, we used positron emission tomography (PET) to examine the neural metabolic activity in the chimpanzee brain. We collected PET data in 4 subjects, all of whom produced manual communicative gestures. However, 2 of these subjects also produced so-called attention-getting vocalizations directed towards a human experimenter. Interestingly, only the two subjects that produced these attention-getting sounds showed greater mean metabolic activity in the Broca's area homologue as compared to a baseline scan. The two subjects that did not produce attention-getting sounds did not. These data contradict an exclusive "gestural origins" theory for they suggest that it is vocal signaling that selectively activates the Broca's area homologue in chimpanzees. In other words, the activity observed in the Broca's area homologue reflects the production of vocal signals by the chimpanzees, suggesting that this critical human language region was involved in vocal signaling in the common ancestor of both modern humans and chimpanzees.     

Neural Dynamics of Learning Sound—Action Associations

A motor component is pre-requisite to any communicative act as one must inherently move to communicate. To learn to make a communicative act, the brain must be able to dynamically associate arbitrary percepts to the neural substrate underlying the pre-requisite motor activity. We aimed to investigate whether brain regions involved in complex gestures (ventral pre-motor cortex, Brodmann Area 44) were involved in mediating association between novel abstract auditory stimuli and novel gestural movements. In a functional resonance imaging (fMRI) study we asked participants to learn associations between previously unrelated novel sounds and meaningless gestures inside the scanner. We use functional connectivity analysis to eliminate the often present confound of ‘strategic covert naming’ when dealing with BA44 and to rule out effects of non-specific reductions in signal. Brodmann Area 44, a region incorporating Broca''s region showed strong, bilateral, negative correlation of BOLD (blood oxygen level dependent) response with learning of sound-action associations during data acquisition. Left-inferior-parietal-lobule (l-IPL) and bilateral loci in and around visual area V5, right-orbital-frontal-gyrus, right-hippocampus, left-para-hippocampus, right-head-of-caudate, right-insula and left-lingual-gyrus also showed decreases in BOLD response with learning. Concurrent with these decreases in BOLD response, an increasing connectivity between areas of the imaged network as well as the right-middle-frontal-gyrus with rising learning performance was revealed by a psychophysiological interaction (PPI) analysis. The increasing connectivity therefore occurs within an increasingly energy efficient network as learning proceeds. Strongest learning related connectivity between regions was found when analysing BA44 and l-IPL seeds. The results clearly show that BA44 and l-IPL is dynamically involved in linking gesture and sound and therefore provides evidence that one of the mechanisms required for the evolution of human communication is found within these motor regions.     

Use of gesture sequences in chimpanzees

Gestural communication in a group of 19 captive chimpanzees (Pan troglodytes) was observed, with particular attention paid to gesture sequences (combinations). A complete inventory of gesture sequences is reported. The majority of these sequences were repetitions of the same gestures, which were often tactile gestures and often occurred in play contexts. Other sequences combined gestures within a modality (visual, auditory, or tactile) or across modalities. The emergence of gesture sequences was ascribed to a recipient's lack of responsiveness rather than a premeditated combination of gestures to increase the efficiency of particular gestures. In terms of audience effects, the chimpanzees were sensitive to the attentional state of the recipient, and therefore used visually-based gestures mostly when others were already attending, as opposed to tactile gestures, which were used regardless of whether the recipient was attending or not. However, the chimpanzees did not use gesture sequences in which the first gesture served to attract the recipient's visual attention before they produced a second gesture that was visually-based. Instead, they used other strategies, such as locomoting in front of the recipient, before they produced a visually-based gesture.     

Social Use of Facial Expressions in Hylobatids

Non-human primates use various communicative means in interactions with others. While primate gestures are commonly considered to be intentionally and flexibly used signals, facial expressions are often referred to as inflexible, automatic expressions of affective internal states. To explore whether and how non-human primates use facial expressions in specific communicative interactions, we studied five species of small apes (gibbons) by employing a newly established Facial Action Coding System for hylobatid species (GibbonFACS). We found that, despite individuals often being in close proximity to each other, in social (as opposed to non-social contexts) the duration of facial expressions was significantly longer when gibbons were facing another individual compared to non-facing situations. Social contexts included grooming, agonistic interactions and play, whereas non-social contexts included resting and self-grooming. Additionally, gibbons used facial expressions while facing another individual more often in social contexts than non-social contexts where facial expressions were produced regardless of the attentional state of the partner. Also, facial expressions were more likely ‘responded to’ by the partner’s facial expressions when facing another individual than non-facing. Taken together, our results indicate that gibbons use their facial expressions differentially depending on the social context and are able to use them in a directed way in communicative interactions with other conspecifics.     

Is birth attendance a uniquely human feature? New evidence suggests that Bonobo females protect and support the parturient

Birth attendance has been proposed as a distinguishing feature of humans (Homo sapiens) and it has been linked to the difficulty of the delivery process in our species. Here, we provide the first quantitative study based on video-recordings of the social dynamics around three births in captive bonobos (Pan paniscus), human closest living relative along with the chimpanzee. We show that the general features defining traditional birth attendance in humans can also be identified in bonobos. As in humans, birth in bonobos was a social event, where female attendants provided protection and support to the parturient until the infant was born. Moreover, bystander females helped the parturient during the expulsive phase by performing manual gestures aimed at holding the infant. Our results on bonobos question the traditional view that the “obligatory” need for assistance was the main driving force leading to sociality around birth in our species. Indeed, birth in bonobos is not hindered by physical constraints and the mother is self-sufficient in accomplishing the delivery. Although further studies are needed both in captivity and in the wild, we suggest that the similarities observed between birth attendance in bonobos and humans might be related to the high level of female gregariousness in these species. In our view, the capacity of unrelated females to form strong social bonds and cooperate could have represented the evolutionary pre-requisite for the emergence of human midwifery.     

A longitudinal investigation of gestural communication in young chimpanzees

A longitudinal study of chimpanzee gestural communication is reported. Subjects were seven 5- to 8-year-old members of a semi-natural group at the Yerkes Field Station. These were the same individuals observed byTomasello et al. (1985) four years previously. Nearly identical operational definitions and observational procedures were used in the two studies. Longitudinal comparisons between the two observation periods revealed that the development of chimpanzee gestural communication is best characterized as a series of ontogenetic adaptations: as particular social functions (e.g., nursing, playing, grooming, etc.) arise, decline, or change, gestural communication follows suit. Most gestures seem to be conventionalized by individuals in direct social interaction with conspecifics. Some gestures may be learned by “second-person imitation”—an individual copying a behavior directed to it by another individual. No evidence was found for “third-person imitation”—an individual copying a gesture used between two other individuals. Implications for the concept of chimpanzee “culture” are discussed. This research was supported in part by NIH Grant RR-00165 from the Division of Research Resources to the Yerkes Regional Primate Research Center. The Yerkes Center is fully accredited by the American Association for the Accreditation of Laboratory Animal Care.     

Human infants and baboons show the same pattern of handedness for a communicative gesture

To test the role of gestures in the origin of language, we studied hand preferences for grasping or pointing to objects at several spatial positions in human infants and adult baboons. If the roots of language are indeed in gestural communication, we expect that human infants and baboons will present a comparable difference in their pattern of laterality according to task: both should be more right-hand/left-hemisphere specialized when communicating by pointing than when simply grasping objects. Our study is the first to test both human infants and baboons on the same communicative task. Our results show remarkable convergence in the distribution of the two species' hand biases on the two kinds of tasks: In both human infants and baboons, right-hand preference was significantly stronger for the communicative task than for grasping objects. Our findings support the hypothesis that left-lateralized language may be derived from a gestural communication system that was present in the common ancestor of baboons and humans.     

Multimodal communication and language origins: integrating gestures and vocalizations

The presence of divergent and independent research traditions in the gestural and vocal domains of primate communication has resulted in major discrepancies in the definition and operationalization of cognitive concepts. However, in recent years, accumulating evidence from behavioural and neurobiological research has shown that both human and non‐human primate communication is inherently multimodal. It is therefore timely to integrate the study of gestural and vocal communication. Herein, we review evidence demonstrating that there is no clear difference between primate gestures and vocalizations in the extent to which they show evidence for the presence of key language properties: intentionality, reference, iconicity and turn‐taking. We also find high overlap in the neurobiological mechanisms producing primate gestures and vocalizations, as well as in ontogenetic flexibility. These findings confirm that human language had multimodal origins. Nonetheless, we note that in great apes, gestures seem to fulfil a carrying (i.e. predominantly informative) role in close‐range communication, whereas the opposite holds for face‐to‐face interactions of humans. This suggests an evolutionary shift in the carrying role from the gestural to the vocal stream, and we explore this transition in the carrying modality. Finally, we suggest that future studies should focus on the links between complex communication, sociality and cooperative tendency to strengthen the study of language origins.     

Do bonobos say NO by shaking their head?

Head-shaking gestures are commonly used by African great apes to solicit activities such as play. Here, we report observations of head shaking in four bonobos apparently aimed at preventing the recipient from doing something. This may reflect a primitive precursor of the negatively connoted head-shaking behavior in humans. Further investigations are needed to clarify the preventive function of head shakes and their evolutionary role in the evolution of negation in humans.     

Behavioral laterality in captive bonobos (Pan paniscus): Replication and extension

We report observational data on behavioral laterality in 10 captive bonobos (Pan paniscus)at the San Diego Zoo. The unimanual measures include carrying, leading limb in locomotion, self-touching, face-touching, reaching, and gestures. We also recorded bimanual feeding in these subjects. A significant population level left-hand bias exists for carrying. Right-hand biases occur for leading limb in locomotion and gestures. During bimanual feeding, the bonobos hold food items with the left hand while feeding with the right hand. Overall, bonobos exhibit behavioral asymmetries that are similar to previous findings in other pongid ape species. The asymmetries in gestures and bimanual feeding represent novel findings with theoretical implications for the origins of tool use and language.     

Behavioral laterality in captive bonobos (Pan paniscus): Replication and extension

We report observational data on behavioral laterality in 10 captive bonobos (Pan paniscus)at the San Diego Zoo. The unimanual measures include carrying, leading limb in locomotion, self-touching, face-touching, reaching, and gestures. We also recorded bimanual feeding in these subjects. A significant population level left-hand bias exists for carrying. Right-hand biases occur for leading limb in locomotion and gestures. During bimanual feeding, the bonobos hold food items with the left hand while feeding with the right hand. Overall, bonobos exhibit behavioral asymmetries that are similar to previous findings in other pongid ape species. The asymmetries in gestures and bimanual feeding represent novel findings with theoretical implications for the origins of tool use and language.