Wild and captive immature orangutans differ in their non-vocal communication with others, but not with their mothers.

Abstract: In many group-living species, individuals are required to flexibly modify their communicative behaviour in response to current social challenges. To unravel whether sociality and communication systems co-evolve, research efforts have often targeted the links between social organisation and communicative repertoires. However, it is still unclear which social or interactional factors directly predict communicative complexity. To address this issue, we studied wild and zoo-housed immature orangutans of two species to assess the impact of the socio-ecological setting on the production of non-vocal signal repertoires. Specifically, we compared repertoire size, dyadic repertoire similarity, and number of social goals (i.e. observer's estimate of the signaller's intended interaction outcome) for communicative interactions with mothers versus other conspecifics, controlling for critical individual and environmental factors. In this small sample of immature orangutans, wild-captive contrasts were statistically significant only for other-directed repertoires, but not for mother-directed repertoires, and not for the number of social goals that immatures communicated towards. While the repertoires of individuals living in the same research setting were more similar than those living in contrasting settings, this difference was most pronounced for other-directed repertoires of the less socially tolerant orangutan species. These results suggest that the boosted interactional opportunities in captivity rather than mere differences in environmental affordances or communicative needs drive the wild-captive contrast in orangutan communicative repertoires. Overall, this fine-grained analysis of repertoires further underscores that not only a species' social organisation but also the targeted audience may have a profound impact on communicative behaviour. Significance statement: Navigating a dynamic social environment often requires flexible signal use. While it has repeatedly been shown that the social organisation and structure of species predict the complexity of their communication systems, the mechanisms underlying these relationships are largely unknown. Because targeted studies to assess this issue in great apes are difficult, we take an alternative approach here: we compare the same species living in the wild and in artificial habitats in captivity. This contrast allows a direct test of how repertoires respond to the relevant difference in socio-ecological conditions. Our results show that the diversity of interaction partners (i.e. social opportunities), but not the diversity of social goals (i.e. possible interaction outcomes) or the broader physical opportunities (i.e. safe ground use), predict the size and consistency of wild and captive signalling repertoires. Supplementary Information: The online version contains supplementary material available at 10.1007/s00265-023-03426-3.

Social tolerance and interactional opportunities as drivers of gestural redoings in orang-utans.

Communicative repair is a fundamental and universal element of interactive language use. It has been suggested that the persistence and elaboration after communicative breakdown in nonhuman primates constitute two evolutionary building blocks of this capacity, but the conditions favouring it are poorly understood. Because zoo-housed individuals of some species are more social and more terrestrial than in the wild, they should be more likely to show gestural redoings (i.e. both repetition and elaboration) after communicative failure in the coordination of their joint activities. Using a large comparative sample of wild and zoo-housed orang-utans of two different species, we could confirm this prediction for elaboration, the more flexible form of redoings. Specifically, results showed that gestural redoings in general were best predicted by the specific social action context (i.e. social play) and interaction dyad (i.e. beyond mother-offspring), although they were least frequent in captive Bornean orang-utans. For gestural elaboration, we found the expected differences between captive and wild research settings in Borneans, but not in Sumatrans (the more socially tolerant species). Moreover, we found that the effectiveness of elaboration in eliciting responses was higher in Sumatrans, especially the captive ones, whereas effectiveness of mere repetition was influenced by neither species nor setting. We conclude that the socio-ecological environment plays a central role in the emergence of communicative repair strategies in great apes. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Coordinating social action: a primer for the cross-species investigation of communicative repair.

Human joint action is inherently cooperative, manifested in the collaborative efforts of participants to minimize communicative trouble through interactive repair. Although interactive repair requires sophisticated cognitive abilities, it can be dissected into basic building blocks shared with non-human animal species. A review of the primate literature shows that interactionally contingent signal sequences are at least common among species of non-human great apes, suggesting a gradual evolution of repair. To pioneer a cross-species assessment of repair this paper aims at (i) identifying necessary precursors of human interactive repair; (ii) proposing a coding framework for its comparative study in humans and non-human species; and (iii) using this framework to analyse examples of interactions of humans (adults/children) and non-human great apes. We hope this paper will serve as a primer for cross-species comparisons of communicative breakdowns and how they are repaired. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Revisiting the human 'interaction engine': comparative approaches to social action coordination.

The evolution of language was likely facilitated by a special predisposition for social interaction, involving a set of communicative and cognitive skills summarized as the 'interaction engine'. This assemblage seems to emerge early in development, to be found universally across cultures, and to enable participation in sophisticated joint action through the addition of spoken language. Yet, new evidence on social action coordination and communication in nonhuman primates warrants an update of the interaction engine hypothesis, particularly with respect to the evolutionary origins of its specific ingredients. However, one enduring problem for comparative research results from a conceptual gulf between disciplines, rendering it difficult to test concepts derived from human interaction research in nonhuman animals. The goal of this theme issue is to make such concepts accessible for comparative research, to promote a fruitful interdisciplinary debate on social action coordination as a new arena of research, and to enable mutual fertilization between human and nonhuman interaction research. In consequence, we here consider relevant theoretical and empirical research within and beyond this theme issue to revisit the interaction engine's shared, convergently derived and uniquely derived ingredients preceding (or perhaps in the last case, succeeding) human language. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Individual variation and plasticity in the infant-directed communication of orang-utan mothers.

Between-individual variation in behavioural expression, such as social responsiveness, has been shown to have important eco-evolutionary consequences. However, most comparative research on non-human primate communication has focused on species- or population-level variation, while among- and within-individual variation has been largely ignored or considered as noise. Here, we apply a behavioural reaction norm framework to repeated observations of mother-offspring interactions in wild and zoo-housed orang-utans (Pongo abelii, P. pygmaeus) to tease apart variation on the individual level from population-level and species-level differences. Our results showed that mothers not only differed in the composition of their infant-directed gestural repertoires, but also in communicative tactics, such as gestural redoings (i.e. persistence) and responsiveness to infants' requests. These differences remained after controlling for essential moderators, including species, setting, parity and infant age. Importantly, mothers differed in how they adjusted their behaviour across social contexts, making a strong case for investigating within-individual variation. Our findings highlight that partitioning behavioural variation into its within-individual, between-individual and environmental sources allows us to estimate the extent of plastic responses to the immediate environment in great ape communication.

Orangutans have larger gestural repertoires in captivity than in the wild-A case of weak innovation?

Whether nonhuman species can change their communicative repertoire in response to socio-ecological environments has critical implications for communicative innovativeness prior to the emergence of human language, with its unparalleled productivity. Here, we use a comparative sample of wild and zoo-housed orangutans of two species (Pongo abelii, Pongo pygmaeus) to assess the effect of the wild-captive contrast on repertoires of gestures and facial expressions. We find that repertoires on both the individual and population levels are larger in captive than in wild settings, regardless of species, age class, or sampling effort. In the more sociable Sumatran species, dominant use of signals toward single outcomes was also higher in captive settings. We thus conclude that orangutans exposed to more sociable and terrestrial conditions evince behavioral plasticity, in that they produce additional innate or innovated signals that are highly functionally specific. These findings suggest a latent capacity for innovativeness in these apes' communicative repertoires.

Multicomponent and multisensory communicative acts in orang-utans may serve different functions.

From early infancy, human face-to-face communication is multimodal, comprising a plethora of interlinked communicative and sensory modalities. Although there is also growing evidence for this in nonhuman primates, previous research rarely disentangled production from perception of signals. Consequently, the functions of integrating articulators (i.e. production organs involved in multicomponent acts) and sensory channels (i.e. modalities involved in multisensory acts) remain poorly understood. Here, we studied close-range social interactions within and beyond mother-infant pairs of Bornean and Sumatran orang-utans living in wild and captive settings, to examine use of and responses to multicomponent and multisensory communication. From the perspective of production, results showed that multicomponent acts were used more than the respective unicomponent acts when the presumed goal did not match the dominant outcome for a specific communicative act, and were more common among non-mother-infant dyads and Sumatran orang-utans. From the perception perspective, we found that multisensory acts were more effective than the respective unisensory acts, and were used more in wild compared to captive populations. We argue that multisensory acts primarily facilitate effectiveness, whereas multicomponent acts become relevant when interaction outcomes are less predictable. These different functions underscore the importance of distinguishing between production and perception in studies of communication.

Must all signals be evolved? A proposal for a new classification of communicative acts.

While signals in evolutionary biology are usually defined as "acts or traits that have evolved because of their effect on others", work on gestures and vocalizations in various animal taxa have revealed population- or even individual-specific meanings of social signals. These results strongly suggest that communicative acts that are like signals with regard to both form and function (meaning) can also be acquired ontogenetically, and we discuss direct evidence for such plasticity in captive settings with rich opportunities for repeated social interactions with the same individuals. Therefore, in addition to evolved signals, we can recognize invented signals that are acquired during ontogeny (either through ontogenetic ritualization or social transmission). Thus, both gestures and vocalizations can be inventions or innate adaptations. We therefore propose to introduce innate versus invented signals as major distinct categories, with invented signals subdivided into dyad-specific and cultural signals. We suggest that elements of some signals may have mixed origins, and propose criteria to recognize acquired features of signals. We also suggest that invented signals may be most common in species with intentional communication, consistent with their ubiquity in humans, and that the ability to produce them was a necessary condition for the evolution of language. This article is categorized under: Cognitive Biology > Evolutionary Roots of Cognition Linguistics > Evolution of Language Psychology > Comparative Psychology.

The loud scratch: a newly identified gesture of Sumatran orangutan mothers in the wild.

The communicative function of primates' self-directed behaviours like scratching has gained increasing attention in recent years, but their intentional use is still debated. Here, we addressed this issue by exploring the communicative function of 'loud scratches' in wild Sumatran orangutans. Building on previous studies in chimpanzees, we examined the prediction that audio-visual loud scratches are used communicatively in mother-infant travel coordination. Specifically, we examined whether individual, social and scratch features affected the use of pre-move scratches, markers of intentional signal use and approach responses. We analysed a total of 1457 scratching bouts, produced by 17 individuals (including four mothers and their dependent offspring) observed during 305 h of focal follows. Overall, we found that scratching bouts preceded departure mainly when these were produced by mothers and showed features of exaggeration. If the scratching individual was a mother, associates were more likely to be visually attentive during pre-move scratches than in other contexts. Approach or follow responses to scratches by individuals in association were predicted by context, the relationship with the scratcher (i.e. offspring) and the associate's attentional state. We conclude that orangutan mothers use loud scratches as communicative strategies to coordinate joint travel with their infants.

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.

Gestural acquisition in great apes: the Social Negotiation Hypothesis.

Scientific interest in the acquisition of gestural signalling dates back to the heroic figure of Charles Darwin. More than a hundred years later, we still know relatively little about the underlying evolutionary and developmental pathways involved. Here, we shed new light on this topic by providing the first systematic, quantitative comparison of gestural development in two different chimpanzee (Pan troglodytes verus and Pan troglodytes schweinfurthii) subspecies and communities living in their natural environments. We conclude that the three most predominant perspectives on gestural acquisition-Phylogenetic Ritualization, Social Transmission via Imitation, and Ontogenetic Ritualization-do not satisfactorily explain our current findings on gestural interactions in chimpanzees in the wild. In contrast, we argue that the role of interactional experience and social exposure on gestural acquisition and communicative development has been strongly underestimated. We introduce the revised Social Negotiation Hypothesis and conclude with a brief set of empirical desiderata for instigating more research into this intriguing research domain.

The ontogeny of intentional communication in chimpanzees in the wild.

The onset of intentional communication in children's first year of life represents a major milestone in human cognitive development. Similarly, it is well established that our closest living relatives, the great apes, communicate with signals characterized by at least first-order intentionality. Despite the well-documented influence of developmental experiences on socio-cognitive abilities in apes, the developmental trajectory of intentional signal use as well as effects of social exposure remain poorly understood under naturalistic conditions. Here, we addressed these issues by studying the ontogeny of intentional communication in chimpanzee infants of two subspecies (Pan troglodytes schweinfurthii/verus) and communities living in their natural environments. Overall, we found that gestures and bimodal signal combinations were most commonly accompanied by markers of intentional communication: audience checking, persistence to the goal, and sensitivity to recipient's attentional state. Within individuals, the proportion of communicative behaviours associated with goal persistence and sensitivity to attention increased with age. Cross-sectional comparisons between infants revealed an age effect on the use of audience checking. Context, interaction partner and site affiliation affected the production of specific markers irrespective of infants' age. The present study provided hitherto undocumented evidence for the development of three important markers of intentional communication in great apes. Moreover, our results suggest that social exposure impacts early intentional signal use.

The function of primate multimodal communication.

Language is commonly narrowed down to speech, but human face-to-face communication is in fact an intrinsically multimodal phenomenon. Despite growing evidence that the communication of non-human primates, our main model for the evolution of language, is also inherently multimodal, most studies on primate communication have focused on either gestures or vocalizations in isolation. Accordingly, the biological function of multimodal signalling remains poorly understood. In this paper, we aim to merge the perspectives of comparative psychology and behavioural ecology on multimodal communication, and review existing studies in great apes for evidence of multimodal signal function based on content-based, efficacy-based and inter-signal interaction hypotheses. We suggest that cross-species comparisons of great ape interactions in both captive and wild settings will allow us to test the conditions in which these hypotheses apply. We expect such studies to provide novel insights into the function of speech-accompanying signals and cues, such as gestures, facial expressions, and eye gaze.

Taking turns across channels: Conversation-analytic tools in animal communication.

In the quest to bridge the gulf between the fields of linguistics and animal communication, interest has recently been drawn to turn-taking behavior in social interaction. Vocal turn-taking is the core form of language usage in humans, and has been examined in numerous species of birds and primates. Recent studies on great apes have shown that they engage in a bodily form, gestural turn-taking, to achieve mutual communicative goals. However, most studies on turn-taking neglected the fact that signals are prevalently perceived and produced in a multimodal format. Here, I propose that research on animal communication may benefit a more holistic and dynamic approach: studying turn-taking using a multimodal, conservation-analytic framework. I will discuss recent comparative research that implemented this approach via a specific set of parameters. In sum, I argue that a conversation-analytic framework might help substantially to pinpoint the ways in which crucial components of language are embodied in the 'human interaction engine'.

Play-solicitation gestures in chimpanzees in the wild: flexible adjustment to social circumstances and individual matrices.

Social play is a frequent behaviour in great apes and involves sophisticated forms of communicative exchange. While it is well established that great apes test and practise the majority of their gestural signals during play interactions, the influence of demographic factors and kin relationships between the interactants on the form and variability of gestures are relatively little understood. We thus carried out the first systematic study on the exchange of play-soliciting gestures in two chimpanzee (Pan troglodytes) communities of different subspecies. We examined the influence of age, sex and kin relationships of the play partners on gestural play solicitations, including object-associated and self-handicapping gestures. Our results demonstrated that the usage of (i) audible and visual gestures increased significantly with infant age, (ii) tactile gestures differed between the sexes, and (iii) audible and visual gestures were higher in interactions with conspecifics than with mothers. Object-associated and self-handicapping gestures were frequently used to initiate play with same-aged and younger play partners, respectively. Our study thus strengthens the view that gestures are mutually constructed communicative means, which are flexibly adjusted to social circumstances and individual matrices of interactants.

Unpeeling the layers of language: Bonobos and chimpanzees engage in cooperative turn-taking sequences.

Human language is a fundamentally cooperative enterprise, embodying fast-paced and extended social interactions. It has been suggested that it evolved as part of a larger adaptation of humans' species-unique forms of cooperation. Although our closest living relatives, bonobos and chimpanzees, show general cooperative abilities, their communicative interactions seem to lack the cooperative nature of human conversation. Here, we revisited this claim by conducting the first systematic comparison of communicative interactions in mother-infant dyads living in two different communities of bonobos (LuiKotale, DRC; Wamba, DRC) and chimpanzees (Taï South, Côte d'Ivoire; Kanyawara, Uganda) in the wild. Focusing on the communicative function of joint-travel-initiation, we applied parameters of conversation analysis to gestural exchanges between mothers and infants. Results showed that communicative exchanges in both species resemble cooperative turn-taking sequences in human conversation. While bonobos consistently addressed the recipient via gaze before signal initiation and used so-called overlapping responses, chimpanzees engaged in more extended negotiations, involving frequent response waiting and gestural sequences. Our results thus strengthen the hypothesis that interactional intelligence paved the way to the cooperative endeavour of human language and suggest that social matrices highly impact upon communication styles.

Should I stay or should I go? Initiation of joint travel in mother-infant dyads of two chimpanzee communities in the wild.

It is well established that great apes communicate via intentionally produced, elaborate and flexible gestural means. Yet relatively little is known about the most fundamental steps into this communicative endeavour-communicative exchanges of mother-infant dyads and gestural acquisition; perhaps because the majority of studies concerned captive groups and single communities in the wild only. Here, we report the first systematic, quantitative comparison of communicative interactions of mother-infant dyads in two communities of wild chimpanzees by focusing on a single communicative function: initiation of carries for joint travel. Over 156 days of observation, we recorded 442 actions, 599 cases of intentional gesture production, 51 multi-modal combinations and 80 vocalisations in the Kanyawara community, Kibale National Park, Uganda, and the Taï South community, Taï National Park, Côte d'Ivoire. Our results showed that (1) mothers and infants differed concerning the signal frequency and modality employed to initiate joint travel, (2) concordance rates of mothers' gestural production were relatively low within but also between communities, (3) infant communicative development is characterised by a shift from mainly vocal to gestural means, and (4) chimpanzee mothers adjusted their signals to the communicative level of their infants. Since neither genetic channelling nor ontogenetic ritualization explains our results satisfactorily, we propose a revised theory of gestural acquisition, social negotiation, in which gestures are the output of social shaping, shared understanding and mutual construction in real time by both interactants.

Mechanics of fresh, frozen-thawed and heated porcine liver tissue.

PURPOSE: For a better understanding of the effects of thermally altered soft tissue, the biothermomechanics of these tissues need to be studied. Without the knowledge of the underlying physical processes and the parameters that can be controlled clinically, thermal treatment of cancerous hepatic tissue or the preservation of liver grafts are based primarily on trial and error. MATERIALS AND METHODS: Thus, this study is concerned with the investigation of the influence of temperature on the rheological properties and the histological properties of porcine liver. RESULTS: Heating previously cooled porcine liver tissue above 40 °C leads to significant, irreversible stiffness changes observed in the amplitude sweep. The increase of the complex shear module of healthy porcine liver from room temperature to 70 °C is approximately 9-fold. Comparing the temperatures -20 °C and 20 °C, no significant difference of the mechanical properties was observed. Furthermore, there is a strong relation between the mechanical and histological properties of the porcine liver. Temperatures above 40 °C destroy the collagen matrix within the liver tissue. This results in the alteration of the biomechanical properties. The time-temperature superposition principle is applied to generate temperature-dependent shift factors that can be described by a two-part exponential function model with an inflection temperature of 45 °C. CONCLUSIONS: Tumor ablation techniques such as heating or freezing have a significant influence on the histology of liver tissue. However, only for temperatures above body temperature an influence on the mechanical properties of hepatic tissues was noticeable. Freezing up to -20 °C did not affect the liver mechanics.