Vocal functional flexibility in the grunts of young chimpanzees.

All living things communicate yet only humans can be said to communicate using language. How this came to be the case is a fundamental mystery unsolved by contemporary science. Within a human lifetime, language emerges from a complex developmental process. As such, understanding chimpanzee vocal development is essential to understanding the evolutionary roots of language. In human development, language is directly built upon the early capacity for "vocal functional flexibility"-the ability to flexibly express the same vocalizations in different ways to achieve different functions. Primate vocalizations, by contrast, have long been believed to be relatively inflexible regarding both production and function. In this paper, we break new ground by providing evidence for vocal functional flexibility in one of the first systematic studies of early chimpanzee vocal production and function. This finding implies the developmental foundations for language are rooted in our primate evolutionary heritage.

Object use in communication of semi-wild chimpanzees.

Object interactions play an important role in human communication but the extent to which nonhuman primates incorporate objects in their social interactions remains unknown. To better understand the evolution of object use, this study explored how objects are used in social interactions in semi-wild chimpanzees (Pan troglodytes). We used an observational approach focusing on naturally occurring object actions where we examined their use and tested whether the production of object actions was influenced by the recipients' visual attention as well as by colony membership. The results show that chimpanzees adjusted both the type of object used, and the modality of object actions to match the visual attention of the recipient, as well as colony differences in the use of targeted object actions. These results provide empirical evidence highlighting that chimpanzees use objects in diverse ways to communicate with conspecifics and that their use may be shaped by social factors, contributing to our understanding of the evolution of human nonverbal communication, language, and tool use.

Preverbal infants produce more protophones with artificial objects compared to natural objects.

Protophones are considered to be precursors of speech. These vocalizations have been notably discussed in relation to toys and their importance for developing language skills. However, little is known about how natural objects, compared to artificial objects, may affect protophone production, an approach that could additionally help reconstruct how language evolved. In the current study, we examined protophone production in 58 infants (4-18 months) while interacting with their caregivers when using natural objects, household items, and toys. The infants were recorded in their home environment, in a rural area in Zambia. The results showed that the infants produced significantly fewer protophones when using natural objects than when using household items or toys. Importantly, this pattern was found only for the younger preverbal infants, and there was no indication in the data that the level of caregiver responsiveness differed with regard to the object type. Furthermore, the infants of the present work selected primarily the household items when exposed to both natural objects and household items. These findings suggest that natural objects are less likely to promote protophone production and, consequently, language skill development than artificial objects in preverbal infants, who seem to favor the latter, perhaps due to their features designed for specific functional purposes. Furthermore, these findings provide empirical evidence that the use of complex tools in social interactions may have helped to promote the evolution of language among hominins.

Chimpanzee communities differ in their inter- and intrasexual social relationships.

Male and female human social bonding strategies are culturally shaped, in addition to being genetically rooted. Investigating nonhuman primate bonding strategies across sex groups allows researchers to assess whether, as with humans, they are shaped by the social environment or whether they are genetically predisposed. Studies of wild chimpanzees show that in some communities males have strong bonds with other males, whereas in others, females form particularly strong intrasex bonds, potentially indicative of cultural differences across populations. However, excluding genetic or ecological explanations when comparing different wild populations is difficult. Here, we applied social network analysis to examine male and female social bonds in two neighbouring semiwild chimpanzee groups of comparable ecological conditions and subspecies compositions, but that differ in demographic makeup. Results showed differences in bonding strategies across the two groups. While female-female party co-residence patterns were significantly stronger in Group 1 (which had an even distribution of males and females) than in Group 2 (which had a higher proportion of females than males), there were no such differences for male-male or male-female associations. Conversely, female-female grooming bonds were stronger in Group 2 than in Group 1. We also found that, in line with captive studies but contrasting research with wild chimpanzees, maternal kinship strongly predicted proximity and grooming patterns across the groups. Our findings suggest that, as with humans, male and female chimpanzee social bonds are influenced by the specific social group they live in, rather than predisposed sex-based bonding strategies.

Directedness and engagement in chimpanzee vocal ontogeny.

Directedness and engagement during pre-verbal vocal communication play a major role in language development. What was their role in the evolution of language? This question invites us to examine these behaviours in chimpanzee vocal ontogeny. We collected observational data on infant (N = 15) and juvenile (N = 13) chimpanzees at Chimfunshi Wildlife Orphanage, Zambia. We examined the impact of age and vocalization type (grunts, whimpers, laughs and screams) on directed cues (gaze directedness and face directedness) and engagement (mutual face directedness) during vocal communication. We also assessed the impact of directed cues and engagement on social interactions by coding the behaviour of social partners before, during and after a vocalisation, and examining whether they contingently changed their behaviour in response to the vocalisation if it was directed or if engagement occurred. We found that face directed vocalisations showed a general increase during ontogeny and we observed call-type dependent effects of age for mutual face directedness. Only face directed vocalisations were significantly predictive of behavioural responses in social partners. We conclude that like young humans, young chimpanzees routinely exhibit directed behaviours and engagement during vocal communication. This social competency improves during ontogeny and benefits individuals by increasing the chances of eliciting behavioural responses from social partners. Directedness and engagement likely provide a foundation for language phylogenetically, as well as ontogenetically. RESEARCH HIGHLIGHTS: We show that directedness and engagement routinely occur during early chimpanzee vocalisations. Directedness increases throughout chimpanzee vocal ontogeny, similar to human infants. Directedness enhances social partner responsiveness, demonstrating a direct benefit to this style of communication. Directedness and engagement could provide a route towards language phylogenetically as well as ontogenetically.

Testing for personality consistency across naturally occurring behavioral contexts in sanctuary chimpanzees (Pan troglodytes).

Personality is both a reflection of the bio-behavioral profile of individuals and a summary of how they typically interact with their physical and social world. Personality is usually defined as having distinct behavioral characteristics, which are assumed to be consistent over time and across contexts. Like other mammals, primates have individual differences in personality. Although temporal consistency is sometimes measured in primates, and contextual consistency is sometimes measured across experimental contexts, it is rare to measure both in the same individuals and outside of experimental settings. Here, we aim to measure both temporal and contextual consistency in chimpanzees, assessing their personality with behavioral observations from naturally occurring contexts (i.e., real-life settings). We measured personality-based behaviors in 22 sanctuary chimpanzees, in the contexts of feeding, affiliation, resting, and solitude, across two time periods, spanning 4 years. Of the 22 behaviors recorded, about 64% were consistent across two to four contexts and 50% were consistent over time. Ten behaviors loaded significantly onto three trait components: explorativeness, boldness-sociability, and anxiety-sociability, as revealed by factor analysis. Like others, we documented individual differences in the personality of chimpanzees based on reliably measured observations in real-life contexts. Furthermore, we demonstrated relatively strong, but not absolute, temporal, and contextual consistency in personality-based behaviors. We also found another aspect of individual differences in personality, specifically, the extent to which individual chimpanzees show consistency. Some individuals showed contextual and temporal consistency, whereas others show significant variation across behaviors, contexts, and/or time. We speculate that the relative degree of consistency in personality may vary within chimpanzees. It may be that different primate species vary in the extent to which individuals show consistency of personality traits. Our behavioral-based assessment can be used with wild populations, increasing the validity of personality studies, facilitating comparative studies and potentially being applicable to conservation efforts.

Laughter, play faces and mimicry in animals: evolution and social functions.

Human laughter and laugh faces show similarities in morphology and function with animal playful expressions. To better understand primordial uses and effects of human laughter and laugh faces, it is important to examine these positive expressions in animals from both homologous and analogous systems. Phylogenetic research on hominids provided empirical evidence on shared ancestry across these emotional expressions, including human laughter and laugh faces. In addition, playful expressions of animals, in general, arguably have a key role in the development of social cognitive skills, a role that may help explain their polyphyletic history. The present work examines the evolution and function of playful expressions in primates and other animals. As part of this effort, we also coded for muscle activations of six carnivore taxa with regard to their open-mouth faces of play; our findings provide evidence that these carnivore expressions are homologues of primate open-mouth faces of play. Furthermore, our work discusses how the expressions of animal play may communicate positive emotions to conspecifics and how the motor resonance of these expressions increases affiliation and bonding between the subjects, resembling in a number of ways the important social-emotional effects that laughter and laugh faces have in humans. This article is part of the theme issue 'Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience'.

The Complexity and Phylogenetic Continuity of Laughter and Smiles in Hominids.

Laughter and smiles are often, but not always, associated with positive affect. These expressions of humans help to promote social relationships as well as the development of cognitive and socio-emotional skills and they may have a positive impact on health and well-being, hereby covering a selection of fitness-relevant benefits. Both laughter and smiles of positive affect also occur early in human development and across cultures, suggesting deep roots in human biology. The present work provides an evolutionary reconstruction of the evolution of human laughter and smiles of positive affect in form and function, based on the principle of maximum parsimony. According to the Complexity and Continuity Hypothesis, human laughter and smiles of positive affect must have evolved within the context of play from ancestral species. Furthermore, ancestral ape laughter and their open-mouth faces must already have been complex in form and function and changed over time via categorically different phylogenetic pathways to become characteristic, effective, and pervasive behaviors of everyday social interactions in humans.

Filling in the gaps: Acoustic gradation increases in the vocal ontogeny of chimpanzees (Pan troglodytes).

Human vocal ontogeny is considered to be a process whereby a large repertoire of discrete sounds seemingly emerges from a smaller number of acoustically graded vocalizations. While adult chimpanzee vocal behavior is highly graded, its developmental trajectory is poorly understood. In the present study, we therefore examined the size and structure of the chimpanzee vocal repertoire at different stages of ontogeny. Audio recordings were collected on infant (N = 13) and juvenile (N = 13) semi-wild chimpanzees at Chimfunshi Wildlife Orphanage, Zambia, using focal and ad libitum sampling. All observed call types were acoustically measured. These were predominantly grunts, whimpers, laughs, screams, hoos, and barks and squeaks. A range of spectral and temporal acoustic parameters were extracted, and fuzzy c-means clustering was used to quantify the size and structure of the repertoire. The infant and juvenile vocal repertoires were both best described with the same number of clusters. However, compared to infants, juvenile call clusters were less distinct from one another and could be extracted only when a low level of overlap between call clusters was permitted. Moreover, the acoustic overlap between call clusters was significantly higher for juveniles. Overall, this pattern shows greater acoustic overlap in juvenile vocalizations compared to infants, suggesting a trend toward increased acoustic gradation in chimpanzee vocal ontogeny. This may imply in contrast to humans, chimpanzees become increasingly proficient in using graded signals effectively rather than developing a larger repertoire of more discrete sounds in ontogeny.

A machine learning approach to infant distress calls and maternal behaviour of wild chimpanzees.

Distress calls are an acoustically variable group of vocalizations ubiquitous in mammals and other animals. Their presumed function is to recruit help, but there has been much debate on whether the nature of the disturbance can be inferred from the acoustics of distress calls. We used machine learning to analyse episodes of distress calls of wild infant chimpanzees. We extracted exemplars from those distress call episodes and examined them in relation to the external event triggering them and the distance to the mother. In further steps, we tested whether the acoustic variants were associated with particular maternal responses. Our results suggest that, although infant chimpanzee distress calls are highly graded, they can convey information about discrete problems experienced by the infant and about distance to the mother, which in turn may help guide maternal parenting decisions. The extent to which mothers rely on acoustic cues alone (versus integrate other contextual-visual information) to decide upon intervening should be the focus of future research.

Facial Complexity in Sun Bears: Exact Facial Mimicry and Social Sensitivity.

Facial mimicry is a central feature of human social interactions. Although it has been evidenced in other mammals, no study has yet shown that this phenomenon can reach the level of precision seem in humans and gorillas. Here, we studied the facial complexity of group-housed sun bears, a typically solitary species, with special focus on testing for exact facial mimicry. Our results provided evidence that the bears have the ability to mimic the expressions of their conspecifics and that they do so by matching the exact facial variants they interact with. In addition, the data showed the bears produced the open-mouth faces predominantly when they received the recipient's attention, suggesting a degree of social sensitivity. Our finding questions the relationship between communicative complexity and social complexity, and suggests the possibility that the capacity for complex facial communication is phylogenetically more widespread than previously thought.

Infrared thermal imaging: Positive and negative emotions modify the skin temperatures of monkey and ape faces.

Facial thermography has enabled researchers to noninvasively and continuously measure the changes of a range of emotional states in humans. The present work used this novel technology to study the effect of positive and negative emotions in nonhuman primates by focusing on four facial areas (the peri-orbital area, the nose bridge, the nose tip, and the upper lip). Monkeys and apes were examined for positive emotions (during interactions with toys and during tickling) and for negative emotions (during food delay and teasing). For the combined toy and tickling condition, the results indicated a drop in the nose tip temperature and a tendency of an increase in the peri-orbital temperature. For the combined food delay and teasing condition, the results also revealed a rise in the upper lip temperature of the subjects. These different effects on the facial temperatures in monkeys and apes most likely reflect distinctive physiological reactions of a primordial primate emotion system. We conclude that facial thermal imaging represents a promising physiologically grounded technology to noninvasively and continuously obtain reliable data on emotional states in nonhuman primates, which may help modernize research on emotions in nonhuman primates and enhance our understanding of the evolution of human emotions.

Morphometric, Behavioral, and Genomic Evidence for a New Orangutan Species.

Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P. pygmaeus (Linnaeus 1760) and P. abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual and other extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepest split in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba, whereas both currently recognized species separated much later, about 674 kya. Our combined analyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.

Spatial transposition tasks in Indian sloth bears (Melursus ursinus) and Bornean sun bears (Helarctos malayanus euryspilus).

Spatial transposition tasks assess individuals' ability to represent nonvisible spatial object displacements. Several nonhuman mammal species have been tested on this task including primates, cats, and dogs, but to date, great apes seem the only taxon that has repeatedly and consistently solved spatial transposition tasks. The authors investigated the ability of captive sloth and sun bears to solve spatial transposition tasks. Both species belong to the same taxonomic group as cats and dogs, but unlike them and similar to apes, they have an omnivorous diet that requires them to keep track of fruit sources in space and time. The bears were first tested on a visible displacement task and those that succeeded were further tested on a spatial transposition task that involved a 180° transposition, followed by 2 tasks with two 360° transpositions. All 7 sloth bears and 7 out of 9 sun bears solved the visible displacement task. The 180° transposition task was solved by 6 out of 7 sloth bears and 1 out of the 5 tested sun bears. Three sloth bears were tested on all 4 experiments and even solved 2-chained 360° transpositions. Control conditions were conducted showing that the bears' performance did not rely on olfactory or auditory cues. The results provide the first indication that bears might be able to track invisible objects. Further studies will be necessary to confirm these results and to control the influence of associative learning. The present study emphasizes the importance of including different animal species in the investigation of what underlies the evolution of different cognitive skills. (PsycINFO Database Record

Skin temperature changes in wild chimpanzees upon hearing vocalizations of conspecifics.

A growing trend of research using infrared thermography (IRT) has shown that changes in skin temperature, associated with activity of the autonomic nervous system, can be reliably detected in human and non-human animals. A contact-free method, IRT provides the opportunity to uncover emotional states in free-ranging animals during social interactions. Here, we measured nose and ear temperatures of wild chimpanzees of Budongo Forest, Uganda, when exposed to naturally occurring vocalizations of conspecifics. We found a significant temperature decrease over the nose after exposure to conspecifics' vocalizations, whereas we found a corresponding increase for ear temperature. Our study suggests that IRT can be used in wild animals to quantify changes in emotional states in response to the diversity of vocalizations, their functional significance and acoustical characteristics. We hope that it will contribute to more research on physiological changes associated with social interactions in wild animals.

An analysis of bimanual actions in natural feeding of semi-wild chimpanzees.

OBJECTIVE: The objective of the current study was to investigate the lateral dominance for a bimanually coordinated natural feeding behavior in semi-wild chimpanzees. METHODS: Strychnos spp. fruit consumption behaviors in semi-wild chimpanzees as an ecologically comparable feeding behavior to those found in cerebral lateralization studies of non-primate species was investigated. Video recordings of 33 chimpanzees were assessed while they consumed hard-shelled strychnos fruits. Statistical and descriptive measures of hand dominance to highlight lateralized patterns were explored. RESULTS: Statistical evaluation of feeding bouts revealed a group-level right-handed bias for bimanual coordinated feeding actions, however, few individuals were statistically lateralized. Descriptive analyses revealed that the majority of individuals were lateralized and possessed a right-handed bias for strychnos feeding behavior. CONCLUSIONS: The results provided empirical evidence in support of an early evolutionary delineation of function for the right and left hemispheres. The present findings suggest that great apes express an intermediate stage along the phylogenetic trajectory of human manual lateralization.

No strings attached: physiological monitoring of rhesus monkeys (Macaca mulatta) with thermal imaging.

Methodological challenges make physiological affective observations very restrictive as in many cases they take place in a laboratory setting rather than the animals' natural habitat. In the current study using Infrared Thermal Imaging we examine the physiological thermal imprints of five macaques. The monkeys were exposed in three different experimental scenarios. Playing with a toy, food teasing as well as feeding. It was observed that during teasing the temperature of the region surrounding the eyes was higher than play as a result of rapid saccades directed at the food. Compared to play and teasing, a lower temperature accompanied feeding on the upper lip, nose and orbital region suggesting elevated levels of distress. These findings prove that thermal imaging is a reliable method of physiological monitoring the subject at a distance while preserving a semi-experimental setting.

Chimpanzees (Pan troglodytes) Produce the Same Types of 'Laugh Faces' when They Emit Laughter and when They Are Silent.

The ability to flexibly produce facial expressions and vocalizations has a strong impact on the way humans communicate, as it promotes more explicit and versatile forms of communication. Whereas facial expressions and vocalizations are unarguably closely linked in primates, the extent to which these expressions can be produced independently in nonhuman primates is unknown. The present work, thus, examined if chimpanzees produce the same types of facial expressions with and without accompanying vocalizations, as do humans. Forty-six chimpanzees (Pan troglodytes) were video-recorded during spontaneous play with conspecifics at the Chimfunshi Wildlife Orphanage. ChimpFACS was applied, a standardized coding system to measure chimpanzee facial movements, based on FACS developed for humans. Data showed that the chimpanzees produced the same 14 configurations of open-mouth faces when laugh sounds were present and when they were absent. Chimpanzees, thus, produce these facial expressions flexibly without being morphologically constrained by the accompanying vocalizations. Furthermore, the data indicated that the facial expression plus vocalization and the facial expression alone were used differently in social play, i.e., when in physical contact with the playmates and when matching the playmates' open-mouth faces. These findings provide empirical evidence that chimpanzees produce distinctive facial expressions independently from a vocalization, and that their multimodal use affects communicative meaning, important traits for a more explicit and versatile way of communication. As it is still uncertain how human laugh faces evolved, the ChimpFACS data were also used to empirically examine the evolutionary relation between open-mouth faces with laugh sounds of chimpanzees and laugh faces of humans. The ChimpFACS results revealed that laugh faces of humans must have gradually emerged from laughing open-mouth faces of ancestral apes. This work examines the main evolutionary changes of laugh faces since the last common ancestor of chimpanzees and humans.

Orangutans modify facial displays depending on recipient attention.

Primate facial expressions are widely accepted as underpinned by reflexive emotional processes and not under voluntary control. In contrast, other modes of primate communication, especially gestures, are widely accepted as underpinned by intentional, goal-driven cognitive processes. One reason for this distinction is that production of primate gestures is often sensitive to the attentional state of the recipient, a phenomenon used as one of the key behavioural criteria for identifying intentionality in signal production. The reasoning is that modifying/producing a signal when a potential recipient is looking could demonstrate that the sender intends to communicate with them. Here, we show that the production of a primate facial expression can also be sensitive to the attention of the play partner. Using the orangutan (Pongo pygmaeus) Facial Action Coding System (OrangFACS), we demonstrate that facial movements are more intense and more complex when recipient attention is directed towards the sender. Therefore, production of the playface is not an automated response to play (or simply a play behaviour itself) and is instead produced flexibly depending on the context. If sensitivity to attentional stance is a good indicator of intentionality, we must also conclude that the orangutan playface is intentionally produced. However, a number of alternative, lower level interpretations for flexible production of signals in response to the attention of another are discussed. As intentionality is a key feature of human language, claims of intentional communication in related primate species are powerful drivers in language evolution debates, and thus caution in identifying intentionality is important.