Gestural communication in wild spider monkeys (Ateles geoffroyi).

Gestures play a central role in the communication systems of several animal families, including primates. In this study, we provide a first assessment of the gestural systems of a Platyrrhine species, Geoffroy's spider monkeys (Ateles geoffroyi). We observed a wild group of 52 spider monkeys and assessed the distribution of visual and tactile gestures in the group, the size of individual repertoires and the intentionality and effectiveness of individuals' gestural production. Our results showed that younger spider monkeys were more likely than older ones to use tactile gestures. In contrast, we found no inter-individual differences in the probability of producing visual gestures. Repertoire size did not vary with age, but the probability of accounting for recipients' attentional state was higher for older monkeys than for younger ones, especially for gestures in the visual modality. Using vocalizations right before the gesture increased the probability of gesturing towards attentive recipients and of receiving a response, although age had no effect on the probability of gestures being responded. Overall, our study provides first evidence of gestural production in a Platyrrhine species, and confirms this taxon as a valid candidate for research on animal communication.

A first exploratory comparison of the behaviour of wolves (Canis lupus) and wolf-dog hybrids in captivity.

Extensive introgression of genes from domesticated taxa may be a serious threat for the genomic integrity and adaptability of wild populations. Grey wolves (Canis lupus) are especially vulnerable to this phenomenon, but there are no studies yet assessing the potential behavioural effects of dog-introgression in wolves. In this study, we conducted a first systematic comparison of admixed (N = 11) and non-admixed (N = 14) wolves in captivity, focusing on their reaction to unfamiliar humans and novel objects, and the cohesiveness of their social groups. When exposed to unfamiliar humans in the experimental task, wolves were more vigilant, fearful and aggressive than admixed wolves, and less likely to approach humans, but also more likely to spend time in human proximity. When exposed to novel objects, wolves were more aggressive than admixed wolves, less likely to spend time in object proximity, and more likely to interact with objects, but also less vigilant and as fearful as admixed wolves. Finally, social networks were more cohesive in wolves than in admixed wolves. Although caution is needed when comparing groups of captive individuals with different life experiences, our study suggests that dog admixture may lead to important behavioural changes in wolves, with possible implications for conservation strategies.

Perception of optical illusions in ungulates: insights from goats, sheep, guanacos and llamas.

Optical illusions have long been used in behavioural studies to investigate the perceptual mechanisms underlying vision in animals. So far, three studies have focused on ungulates, providing evidence that they may be susceptible to some optical illusions, in a way similar to humans. Here, we used two food-choice tasks to study susceptibility to the Müller-Lyer and Delboeuf illusions in 17 captive individuals belonging to four ungulate species (Lama guanicoe, Lama glama, Ovis aries, Capra hircus). At the group level, there was a significant preference for the longer/larger food over the shorter/smaller one in control trials. Additionally, the whole group significantly preferred the food stick between two inward arrowheads over an identical one between two outward arrowheads in experimental trials of the Müller-Lyer task, and also preferred the food on the smaller circle over an identical one on the larger circle in the experimental trials of the Delboeuf task. Group-level analyses further showed no significant differences across species, although at the individual level we found significant variation in performance. Our findings suggest that, in line with our predictions, ungulates are overall susceptible to the Müller-Lyer and the Delboeuf illusions, and indicate that the perceptual mechanisms underlying size estimation in artiodactyls might be similar to those of other species, including humans.

The proximate regulation of prosocial behaviour: towards a conceptual framework for comparative research.

Humans and many other animal species act in ways that benefit others. Such prosocial behaviour has been studied extensively across a range of disciplines over the last decades, but findings to date have led to conflicting conclusions about prosociality across and even within species. Here, we present a conceptual framework to study the proximate regulation of prosocial behaviour in humans, non-human primates and potentially other animals. We build on psychological definitions of prosociality and spell out three key features that need to be in place for behaviour to count as prosocial: benefitting others, intentionality, and voluntariness. We then apply this framework to review observational and experimental studies on sharing behaviour and targeted helping in human children and non-human primates. We show that behaviours that are usually subsumed under the same terminology (e.g. helping) can differ substantially across and within species and that some of them do not fulfil our criteria for prosociality. Our framework allows for precise mapping of prosocial behaviours when retrospectively evaluating studies and offers guidelines for future comparative work.

Maternal and offspring behavior in free-ranging Japanese and moor macaques: A comparative approach.

Female primates represent the most important social partner for their developing offspring. However, mothers may strongly differ in the way they relate to their offspring (e.g., in terms of two different dimensions: protectiveness and rejection). In this study, we aimed to assess how dominance style predicts (i) changes in maternal behavior through offspring development, and (ii) the link between maternal behavior and offspring behavior. We conducted behavioral observations on 34 free-ranging immatures of two species of macaques with different dominance styles: less tolerant Japanese macaques (JM; Macaca fuscata) and more tolerant moor macaques (MM; Macaca maura). Our results showed that maternal behavior differed between JM and MM: maternal proximity and grooming decreased through offspring development more quickly in MM than in JM, whereas maternal rejection and aggression, which were generally more frequent in JM, decreased with offspring age similarly in both species. In contrast, maternal restraint of offspring decreased similarly with offspring age in both species. Furthermore, dominance style was differentially associated with the link between maternal and offspring behavior: in MM only, maternal grooming predicted an increase of the probability that offspring interacted with partners other than their mothers and engaged in solitary play, whereas maternal rejection predicted a decrease in the occurrence of solitary play. Overall, these results suggest interspecific variation in maternal behavior during offspring's first years of life, and point to the possibility that these differences may have an important role in shaping their behavioral development.

Primates unleashed.

Before claiming major differences between the communication systems of humans and other species, it is necessary to (1) overcome methodological limitations in the comparative study of communicative intentions; (2) account for mechanisms other than epistemic vigilance that may also sustain complex forms of communication; and (3) better differentiate between motivational and cognitive factors potentially affecting the emergence of open-ended communication.

How primates acquire their gestures: evaluating current theories and evidence.

Mechanisms underlying gesture acquisition in primates are largely unstudied, yet heavily debated. While some studies suggest that gestural repertoires are largely innate, others emphasize that gestures emerge and are shaped in social interactions with other conspecifics. There is agreement, however, regarding the negligible role of imitation for the acquisition of gestures. The aim of this paper is to provide an overview of the current knowledge about gesture acquisition in nonhuman primates, to introduce the corresponding mechanisms suggested to be involved, and to discuss how findings from current studies support the different theories of gesture acquisition. We suggest that seemingly inconsistent findings across different research groups can be reconciled by pointing to differences between their research foci as well as methods of data collection. The additional comparison of the developmental pathways of gestural and facial communication highlights the complex interplay of genetic as well as social factors involved in shaping a species repertoire. We close by proposing that extending longitudinal studies, which capture the onset and usage of gestures in young primates, and which include the comparisons of several species and groups in different environments, will enable us to better understand developmental pathways of gestural communication in primates.

"Giving" and "responding" differences in gestural communication between nonhuman great ape mothers and infants.

In the first comparative analysis of its kind, we investigated gesture behavior and response patterns in 25 captive ape mother-infant dyads (six bonobos, eight chimpanzees, three gorillas, and eight orangutans). We examined (i) how frequently mothers and infants gestured to each other and to other group members; and (ii) to what extent infants and mothers responded to the gestural attempts of others. Our findings confirmed the hypothesis that bonobo mothers were more proactive in their gesturing to their infants than the other species. Yet mothers (from all four species) often did not respond to the gestures of their infants and other group members. In contrast, infants "pervasively" responded to gestures they received from their mothers and other group members. We propose that infants' pervasive responsiveness rather than the quality of mother investment and her responsiveness may be crucial to communication development in nonhuman great apes.

What is a gesture? A lesson from comparative gesture research.

Research into nonhuman primates' gestures is often limited by the lack of clear criteria to define a gesture and by studying gestures separately from other communicative means. Despite the fundamental differences between the gestural communication of humans and other primates, I argue that sign language research might benefit from the lessons learned from these drawbacks and the current developments in primate communication research.

A comparison of facial expression properties in five hylobatid species.

Little is known about facial communication of lesser apes (family Hylobatidae) and how their facial expressions (and use of) relate to social organization. We investigated facial expressions (defined as combinations of facial movements) in social interactions of mated pairs in five different hylobatid species belonging to three different genera using a recently developed objective coding system, the Facial Action Coding System for hylobatid species (GibbonFACS). We described three important properties of their facial expressions and compared them between genera. First, we compared the rate of facial expressions, which was defined as the number of facial expressions per units of time. Second, we compared their repertoire size, defined as the number of different types of facial expressions used, independent of their frequency. Third, we compared the diversity of expression, defined as the repertoire weighted by the rate of use for each type of facial expression. We observed a higher rate and diversity of facial expression, but no larger repertoire, in Symphalangus (siamangs) compared to Hylobates and Nomascus species. In line with previous research, these results suggest siamangs differ from other hylobatids in certain aspects of their social behavior. To investigate whether differences in facial expressions are linked to hylobatid socio-ecology, we used a Phylogenetic General Least Square (PGLS) regression analysis to correlate those properties with two social factors: group-size and level of monogamy. No relationship between the properties of facial expressions and these socio-ecological factors was found. One explanation could be that facial expressions in hylobatid species are subject to phylogenetic inertia and do not differ sufficiently between species to reveal correlations with factors such as group size and monogamy level.

A longitudinal comparison of maternal behaviour in German urban humans (Homo sapiens) and captive chimpanzees (Pan troglodytes).

Comparative perspectives are crucial in the study of human development, yet longitudinal comparisons of humans and other primates are still relatively uncommon. Here, we combined theoretical frameworks from cross-cultural and comparative psychology, to study maternal style in 10 mother-infant pairs of German urban humans (Homo sapiens) and 10 mother-infant pairs of captive chimpanzees (Pan troglodytes), during the first year of infants' development. We conducted focal observations of different behaviours (i.e. nursing, carrying, body contact, touching, grooming, restraining, approaching, leaving, rejection, aggression, mutual gaze, object stimulation), during natural interactions. Analyses revealed a more distal maternal style in WEIRD humans than in captive chimpanzees, with different behaviours being generally more common in one of the two species throughout development. For other behaviours (i.e. nursing), developmental trajectories differed between WEIRD humans and captive chimpanzees, although differences generally decreased through infants' development. Overall, our study confirms functional approaches as a valid tool for comparative longitudinal studies.

Understanding others' preferences: A comparison across primate species and human societies.

We investigated children's and non-human great apes' ability to anticipate others' choices from their evident food preferences-regardless of whether these preferences deviate or align with one's own. We assessed children from three culturally-diverse societies (Namibia, Germany, and Samoa; N = 71; age range = 5-11) and four non-human great ape species (chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla gorilla), and orangutans (Pongo abelii); N = 25; age range = 7-29) regarding their choices in a dyadic food-retrieval task. Across conditions, participants' preferences were either aligned (same preference condition) or opposed (opposite preference condition) to those of their competitors. Children across societies altered their choices based on their competitor's preferences, indicating a cross-culturally recurrent capacity to anticipate others' choices relying on preferences-based inferences. In contrast to human children, all non-human great apes chose according to their own preferences but independent of those of their competitors. In sum, these results suggest that the tendency to anticipate others' choices based on their food preferences is cross-culturally robust and, among the great apes, most likely specific to humans.

Face to face interactions in chimpanzee (Pan troglodytes) and human (Homo sapiens) mother-infant dyads.

Human mothers interact with their infants in different ways. In Western, educated, industrialized, rich and democratic (WEIRD) societies, face-to-face interactions and mutual gazes are especially frequent, yet little is known about their developmental trajectories and if they differ from those of other primates. Using a cross-species developmental approach, we compared mother-infant interactions in 10 dyads of urban humans from a WEIRD society (Homo sapiens) and 10 dyads of captive zoo-based chimpanzees (Pan troglodytes), when infants were one, six and 12 months old. Results showed that face-to-face interactions with mutual gaze events were common in both groups throughout the infant's first year of life. The developmental trajectories of maternal and infants' looks partially differed between species, but mutual gaze events were overall longer in humans than in chimpanzees. Mutual gazes were also more frequent in humans, peaking at six months in humans, while increasing with age in chimpanzees. The duration and frequency of mutual gazes varied across contexts in both groups, with mutual gazes being longer during caring/grooming and feeding contexts. These findings confirm that some aspects of early socio-cognitive development are shared by humans and other primates, and highlight the importance of combining developmental and cross-species approaches to better understand the evolutionary roots of parenting behaviour. This article is part of a discussion meeting issue 'Face2face: advancing the science of social interaction'.

Maternal Investment Fosters Male but Not Female Social Interactions with Other Group Members in Immature Wild Spider Monkeys (Ateles geoffroyi).

In several species, individuals form long-lasting social relationships with other group members, which provide them with important fitness benefits. In primates, patterns of social relationships are known to differ between sexes, but little is known about how these differences emerge through development or the role that mothers might have in this process. Here, we investigated how sex differences in social behaviour emerge during the first six years of primate life and how sex-biased maternal investment can foster immatures' social development and social interaction with other group members. For this purpose, we observed 20 males and females aged between zero and six years in a wild group of spider monkeys (Ateles geoffroyi) that was male-philopatric and, therefore, expected to show sex-biased maternal investment. Our results showed no sex difference in the social development of offspring with regards to body contact and grooming, but the probability of play was rather constant throughout age for females, whereas, for males, it became higher than females around two years of age, peaking between three and four years of age. Moreover, we found differences between female and male immatures in the importance of maternal investment (which included the time mothers spent nursing, carrying, grooming, touching and playing with their offspring) for their social integration in the natal group. In particular, maternal investment increased the probability of playing with other group members for sons, but not for daughters. Our findings suggest that mothers, through sex-biased maternal investment, might have a crucial function in the social development of spider monkeys, fostering the abilities that young offspring need to thrive as adults. By shedding light on maternal investment and social development in a still understudied primate species, these findings contribute to understanding the evolutionary roots of human maternal care and social development.

Gibbons (Hylobates pileatus, H. moloch, H. lar, Symphalangus syndactylus) follow human gaze, but do not take the visual perspective of others.

We investigated four gibbon species of two different genera (Hylobates pileatus, H. moloch, H. lar, Symphalangus syndactylus) in terms of their looking behavior in response to a human who either looked up or looked at the gibbon. Comparing those two conditions, gibbons as a group looked up more when the human was looking up, but they also performed more looks in other directions and thus generally looked more in this condition. Unlike great apes, gibbons did not respond differently between conditions when only the first look on every trial was considered. Furthermore, they did not perform double looks up to check where the human was looking and also did not habituate to the human's looks up. This suggests that gibbons co-orient with human gaze, but unlike great apes, they do not take the visual perspective of others.

Infant-directed communication in lowland gorillas (Gorilla gorilla): do older animals scaffold communicative competence in infants?

Infant-directed speech is a linguistic phenomenon in which adults adapt their language when addressing infants in order to provide them with more salient linguistic information and aid them in language acquisition. Adult-directed language differs from infant-directed language in various aspects, including speech acoustics, syntax, and semantics. The existence of a "gestural motherese" in interaction with infants, demonstrates that not only spoken language but also nonvocal modes of communication can become adapted when infants are recipients. Rhesus macaques are so far the only nonhuman primates where a similar phenomenon to "motherese" has been discovered: the acoustic spectrum of a particular vocalization of adult females may be altered when the addressees are infants. The present paper describes how gorillas adjust their communicative strategies when directing intentional, nonvocal play signals at infants in the sense of a "nonvocal motherese." Animals of ages above infancy use a higher rate of repetitions and sequences of the tactile sensory modality when negotiating play with infants. This indicates that gorillas employ a strategy of infant-specific communication.

Onset and early use of gestural communication in nonhuman great apes.

The early gesturing of six bonobos, eight chimpanzees, three gorillas, and eight orangutans was systematically documented using focal animal sampling. Apes' were observed during their first 20 months of life in an effort to investigate: (i) the onset of gesturing; (ii) the order in which signals of different sensory modalities appear; (iii) the extent to which infants make use of these modalities in their early signaling; and (iv) the behavioral contexts where signals are employed. Orangutans differed in important gestural characteristics to African ape species. Most notably, they showed the latest gestural onset and were more likely to use their early signals in food-related interactions. Tactile and visual signals appeared similarly early across all four species. In African apes, however, visual signaling gained prominence over time while tactile signaling decreased. These findings suggest that motor ability, which encourages independence from caregivers, is an important antecedent, among others, in gestural onset and development, a finding which warrants further investigation.

The social dynamics of complex gestural communication in great and lesser apes (Pan troglodytes, Pongo abelii, Symphalangus syndactylus).

Gestures play an essential role in primate communication. However, little is known about how complexity of gestural use (in terms of repertoire size, intentional use, flexibility and use of gestural sequences) relates to individual and dyadic measures of sociality and whether more complex gestural use is more effective in eliciting a response. We observed 19 captive chimpanzees (Pan troglodytes), 16 Sumatran orangutans (Pongo abelii) and 18 siamangs (Symphalangus syndactylus) to assess the complexity and effectiveness of their gestural use. We found that, beyond interspecies variation, the number of gesture types used in a dyad was higher when individuals had stronger social bonds; the probability of accounting for others' attention increased with age, especially for visual gestures; and sequences were more likely used by younger or socially less integrated individuals. In terms of effectiveness, older individuals and those using fewer sequences were more likely to be responded to, while across dyads, the probability of obtaining a response was higher when both individuals accounted for the other's attention and when they used fewer sequences. Overall, this confirms the link between sociality and complex gestural use and suggests that more complex forms of communication, at least in terms of intentional use, may be more effective at achieving communicative goals. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Great ape communication as contextual social inference: a computational modelling perspective.

Human communication has been described as a contextual social inference process. Research into great ape communication has been inspired by this view to look for the evolutionary roots of the social, cognitive and interactional processes involved in human communication. This approach has been highly productive, yet it is partly compromised by the widespread focus on how great apes use and understand individual signals. This paper introduces a computational model that formalizes great ape communication as a multi-faceted social inference process that integrates (a) information contained in the signals that make up an utterance, (b) the relationship between communicative partners and (c) the social context. This model makes accurate qualitative and quantitative predictions about real-world communicative interactions between semi-wild-living chimpanzees. When enriched with a pragmatic reasoning process, the model explains repeatedly reported differences between humans and great apes in the interpretation of ambiguous signals (e.g. pointing or iconic gestures). This approach has direct implications for observational and experimental studies of great ape communication and provides a new tool for theorizing about the evolution of uniquely human communication. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Focus on the essential: all great apes know when others are being attentive.

When begging for food, all great ape species are sensitive to a human's attention. However, studies investigating which cues are relevant for chimpanzees to assess the attentional state of others have produced highly inconsistent results. Some have suggested chimpanzees differentiate attention based on the status of the face or even the eyes, while others have indicated that body posture alone is the relevant cue. Kaminski et al. (Anim Cogn 7:216-223, 2004) compared the behaviour of chimpanzees, bonobos and orangutans while begging for food from a human experimenter who systematically varied his face and body orientation. Their results indicated that both factors, face and body orientation, affect apes' begging behaviour. The authors claimed that while body orientation provides information about the experimenter's general disposition to offer food, the visibility of the face provides information about the human's attentional state. In the current study, we tested this hypothesis with all four great apes species. However, unlike Kaminski et al. (Anim Cogn 7:216-223, 2004), the experimenter was able to hand over food regardless of body orientation. The results show that as soon as the offering of the food was no longer restricted, the orientation of the face became the key factor. Therefore, we present the first evidence that all great ape species are able to assess the attentional state of a recipient based on the orientation of the face.