Intentional gestural communication amongst red-capped mangabeys (Cercocebus torquatus).

Apes, human's closest living relatives, are renowned for their intentional and highly flexible use of gestural communication. In stark contrast, evidence for flexible and intentional gestural communication in monkeys is scarce. Here, we investigated the intentionality and flexibility of spontaneous gesture use in red-capped mangabeys (Cercocebus torquatus). We applied established methods used in ape gesture research to analyse whether the body acts produced by a total of 17 individuals living in three different groups in captivity qualified as intentionally produced gesture instances. Results showed that signallers showed all hallmarks of intentionality during the production of 20 out of a total of 21 different types of body acts. These were only produced in the presence of other individuals, and the monkeys showed audience checking, sensitivity to the attentional states of recipients, adjustment of signal modality, and response waiting relative to their production. Moreover, in case of communication failure, the monkeys showed goal persistence, and regarding the production contexts they showed some signs of means-ends dissociation. Therefore, these monkeys are capable of flexible and intentional gestural communication and use this to communicate with conspecifics. Our results corroborate recent findings showing that intentional gestural communication was already present in the monkey lineage of catarrhine primates. We discuss our results in light of the comparative approach towards human language evolution and highlight our finding that these monkeys also showed flexible and intentional use of four 'free' manual gesture types.

Joint attention skills in wild Arabian babblers ( Turdoides squamiceps): a consequence of cooperative breeding?

Human cooperation strongly relies on the ability of interlocutors to coordinate each other's attentional state: joint attention. One predominant hypothesis postulates that this hallmark of the unique cognitive system of humans evolved due to the combination of an ape-like cognitive system and the prosocial motives that facilitate cooperative breeding. Here, we tested this hypothesis by investigating communicative interactions of a cooperatively breeding bird species, the Arabian babbler ( Turdoides squamiceps). The behaviour of 12 wild social groups was observed focusing on two distinct communicative behaviours: object presentation and babbler walk. The results showed that both behaviours fulfilled the criteria for first-order intentional communication and involved co-orientation of recipients' attention. In turn, recipients responded with cooperative and communicative acts that resulted in coordinated joint travel between interlocutors. These findings provide the first evidence that another animal species shows several key criteria traditionally used to infer joint attention in prelinguistic human infants. Furthermore, they emphasize the influence of cooperative breeding on sophisticated socio-cognitive performances, while questioning the necessity of an ape-like cognitive system underlying joint attentional behaviour.

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.

How many fingers am I holding up? The answer depends on children's language background.

Monolingual English-speaking preschool children tend to process number gestures as unanalyzed wholes rather than use the one-to-one (finger-to-quantity) correspondence. By school age, however, children can use the one-to-one correspondence. The purpose of the present studies was to test whether children learn one-to-one correspondence through exposure to a variety of finger configurations to convey a single quantity. In Study 1, we compared children with exposure to multiple one-to-one configurations, that is, French-English and German-English bilingual children, to English monolingual children who see consistent representations. As predicted, the bilingual children performed better in interpreting unconventional number gestures. In Study 2, we compared Chinese-English bilingual children who knew arbitrary one-handed Chinese numbers gestures for quantities 6-10 to Chinese-English bilingual children who did not know these gestures, as well as to monolingual English speakers. Chinese-English bilinguals who knew the arbitrary gestures were more likely to interpret unconventional gestures arbitrarily (i.e., influenced by the written and/or Chinese gesture forms). These children did not differ from English monolinguals in the interpretation of unconventional gestures. These results are consistent with the argument that children can become sensitive to the one-to-one correspondence in number gestures with exposure to multiple configurations for the same quantity.

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.

Taking turns: bridging the gap between human and animal communication.

Language, humans' most distinctive trait, still remains a 'mystery' for evolutionary theory. It is underpinned by a universal infrastructure-cooperative turn-taking-which has been suggested as an ancient mechanism bridging the existing gap between the articulate human species and their inarticulate primate cousins. However, we know remarkably little about turn-taking systems of non-human animals, and methodological confounds have often prevented meaningful cross-species comparisons. Thus, the extent to which cooperative turn-taking is uniquely human or represents a homologous and/or analogous trait is currently unknown. The present paper draws attention to this promising research avenue by providing an overview of the state of the art of turn-taking in four animal taxa-birds, mammals, insects and anurans. It concludes with a new comparative framework to spur more research into this research domain and to test which elements of the human turn-taking system are shared across species and taxa.

A multifactorial investigation of captive gorillas' intraspecific gestural laterality.

Multifactorial investigations of intraspecific laterality of primates' gestural communication aim to shed light on factors that underlie the evolutionary origins of human handedness and language. This study assesses gorillas' intraspecific gestural laterality considering the effect of various factors related to gestural characteristics, interactional context and sociodemographic characteristics of signaller and recipient. Our question was: which factors influence gorillas' gestural laterality? We studied laterality in three captive groups of gorillas (N = 35) focusing on their most frequent gesture types (N = 16). We show that signallers used predominantly their hand ipsilateral to the recipient for tactile and visual gestures, whatever the emotional context, gesture duration, recipient's sex or the kin relationship between both interactants, and whether or not a communication tool was used. Signallers' contralateral hand was not preferentially used in any situation. Signallers' right-hand use was more pronounced in negative contexts, in short gestures, when signallers were females and its use increased with age. Our findings showed that gorillas' gestural laterality could be influenced by different types of social pressures thus supporting the theory of the evolution of laterality at the population level. Our study also evidenced that some particular gesture categories are better markers than others of the left-hemisphere language specialization.

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.

Bodies at play: the role of intercorporeality and bodily affordances in coordinating social play in chimpanzees in the wild.

The comparative approach is a crucial method to gain a better understanding of the behavior of living human and nonhuman animals to then draw informed inferences about the behavior of extinct ancestors. One focus has been on disentangling the puzzle of language evolution. Traditionally, studies have predominantly focused on intentionally produced signals in communicative interactions. However, in collaborative and highly dynamic interactions such as play, underlying intentionality is difficult to assess and often interactions are negotiated via body movements rather than signals. This "lack" of signals has led to this dynamic context being widely ignored in comparative studies. The aim of this paper is threefold: First, we will show how comparative research into communication can benefit from taking the intentionality-agnostic standpoint used in conversation analysis. Second, we will introduce the concepts of 'intercorporeality' and 'bodily affordance', and show how they can be applied to the analysis of communicative interactions of nonhuman animals. Third, we will use these concepts to investigate how chimpanzees (Pan troglodytes) initiate, end, and maintain 'contact social play'. Our results showed that bodily affordances are able to capture elements of interactions that more traditional approaches failed to describe. Participants made use of bodily affordances to achieve coordinated engagement in contact social play. Additionally, these interactions could display a sequential organization by which one 'move' by a chimpanzee was responded to with an aligning 'move', which allowed for the co-construction of the activity underway. Overall, the present approach innovates on three fronts: First, it allows for the analysis of interactions that are often ignored because they do not fulfil criteria of intentionality, and/or consist of purely body movements. Second, adopting concepts from research on human interaction enables a better comparison of communicative interactions in other animal species without a too narrow focus on intentional signaling only. Third, adopting a stance from interaction research that highlights how practical action can also be communicative, our results show that chimpanzees can communicate through their embodied actions as well as through signaling. With this first step, we hope to inspire new research into dynamic day-to-day interactions involving both "traditional" signals and embodied actions, which, in turn, can provide insights into evolutionary precursors of human language.

Application of insects to wounds of self and others by chimpanzees in the wild.

Self-medication refers to the process by which a host suppresses or prevents the deleterious effects of parasitism and other causes of illness via behavioural means1. It has been observed across multiple animal taxa (e.g. bears, elephants, moths, starlings)2, with many case studies in great apes1,3. Although the majority of studies on self-medication in non-human primates concern the ingestion of plant parts or non-nutritional substances to combat or control intestinal parasites4, more recent examples also report topical applications of leaves or other materials (including arthropods) to skin integuments3. Thus far, however, the application of insects or insect parts to an individual's own wound or the wound of a conspecific has never been reported. Here, we report the first observations of chimpanzees applying insects to their own wounds (n = 19) and to the wounds of conspecifics (n = 3).

Female bonobos use copulation calls as social signals.

During mating events, females of many primate species produce loud and distinct vocalizations known as 'copulation calls'. The adaptive significance of these signals is considered to be in promoting the caller's direct reproductive success. Here, we investigated copulation calling in bonobos (Pan paniscus), a species in which females produce these vocalizations during sexual interactions with partners of both sexes. Females were more likely to call when mating with males than with females. We also observed a positive relationship between the likelihood of calling and partner rank, regardless of partner sex. Sexual activity generally increased with swelling size (an indicator of reproductive state) and, during their peak swelling, females called more with male than with female partners. Female bonobos are unusual among the non-human primates in terms of their heightened socio-sexuality. Our results suggest that in this species, copulation calls have undergone an evolutionary transition from a purely reproductive to a more general social function, reflecting the intrinsic evolutionary links between vocal behaviour and social cognition.

Lethal coalitionary attacks of chimpanzees (Pan troglodytes troglodytes) on gorillas (Gorilla gorilla gorilla) in the wild.

Intraspecies violence, including lethal interactions, is a relatively common phenomenon in mammals. Contrarily, interspecies violence has mainly been investigated in the context of predation and received most research attention in carnivores. Here, we provide the first information of two lethal coalitionary attacks of chimpanzees (Pan troglodytes troglodytes) on another hominid species, western lowland gorillas (Gorilla gorilla gorilla), that occur sympatrically in the Loango National Park in Gabon. In both events, the chimpanzees significantly outnumbered the gorillas and victims were infant gorillas. We discuss these observations in light of the two most widely accepted theoretical explanations for interspecific lethal violence, predation and competition, and combinations of the two-intraguild predation and interspecific killing. Given these events meet conditions proposed to trigger coalitional killing of neighbours in chimpanzees, we also discuss them in light of chimpanzees' intraspecific interactions and territorial nature. Our findings may spur further research into the complexity of interspecies interactions. In addition, they may aid in combining field data from extant models with the Pliocene hominid fossil record to better understand behavioural adaptations and interspecific killing in the hominin lineage.

Intercommunity interactions and killings in central chimpanzees (Pan troglodytes troglodytes) from Loango National Park, Gabon.

Intercommunity competition in chimpanzees (Pan troglodytes) has been widely studied in eastern (P. t. schweinfurthii) and western (P. t. verus) communities. Both subspecies show hostility towards neighboring communities but differ in rates of lethal attacks and female involvement. However, relatively little is known about the territorial behavior of the two other subspecies, central (P. t. troglodytes) and Nigeria-Cameroon chimpanzees (P. t. ellioti). Here, we present the first insights into intercommunity interactions of individuals of a community of central chimpanzees living in the Loango National Park in Gabon. The presence of individuals of neighboring communities in the Rekambo home range was assessed using 27 camera traps. Information was compiled on intergroup interactions recorded before (2005-2016) and after (January 2017-June 2019) the habituation of the community. Individuals from neighboring communities entered the core area, where nine out of 16 recorded intercommunity encounters occurred. Males were the main participants in territorial patrols and intercommunity aggressions. Females were part of all six territorial patrols recorded and dependent offspring participated in five patrols. Females were involved in intercommunity aggression in five out of twelve recorded encounters in which there was visual contact between communities. While the intercommunity encounter rate was lower than that reported across most other long-term chimpanzee sites, the annual intercommunity killing rate was among the highest. These results suggest that the frequency of lethal attacks at Loango is comparable to that reported for the eastern subspecies. In contrast, female involvement in intercommunity interactions mirrors that of the western subspecies.

Home range size in central chimpanzees (Pan troglodytes troglodytes) from Loango National Park, Gabon.

Ranging behavior has been studied extensively in eastern (Pan troglodytes schweinfurthii) and western (P. t. verus) chimpanzees, but relatively little is known regarding home ranges of the other two subspecies (P. t. ellioti; P. t. troglodytes). In this study, we determined the home range size and space use of a habituated community (Rekambo) of central chimpanzees living in a habitat mosaic in Loango National Park, Gabon. Data on travel routes were collected during follows between January 2017 and April 2019 (N = 670,616 relocations, collected over 640 days and 5690 h of observation). We used three methods for calculating home range size (minimum convex polygon, kernel density estimation, and biased random bridges). We compare our estimates to those obtained from prior genetic and camera trap studies of the Rekambo community and contrast them with estimates from other chimpanzee communities of the four chimpanzee subspecies. Depending on the methodology used, the home range size of the Rekambo community ranged between 27.64 and 59.03 km2. The location of the center of the home range remained relatively stable over the last decade, while the overall size decreased. The Rekambo home range is, therefore, one of the largest documented so far for chimpanzees outside savannah-woodland habitats. We discuss several explanations, including the presence of savannah, interspecies competition, and intercommunity interactions.

Hunting of mammals by central chimpanzees (Pan troglodytes troglodytes) in the Loango National Park, Gabon.

The predation and consumption of animals are common behaviours in chimpanzees across tropical Africa. To date, however, relatively little is known concerning the hunting behaviour of central chimpanzees (Pan troglodytes troglodytes). Here, we provide the first direct observations of hunting behaviour by individuals of the newly habituated Rekambo community in the Loango National Park, Gabon. Over a period of 23 months (May 2017 to March 2019), we observed a total of 61 predation attempts on eight mammal species, including four monkey species. The two most frequently hunted species were two monkey species (Cercocebus torquatus, Cercopithecus nictitans), which are not hunted at other long-term field sites. The majority of predation events observed involved parties of an average of eight individuals, mainly adult males, with hunting success being higher with increasing numbers of participants. Hunting occurred all year round, but hunting rates increased in the dry season, the period of high fruit availability in the Loango National Park. These results are in line with the nutrient surplus hypothesis which explains seasonal variation in hunting behaviour in several populations of eastern chimpanzees (Pan troglodytes schweinfurthii: e.g., Mahale, Tanzania; Ngogo, Uganda). Finally, with a hunting frequency of 2.65 hunts per month, the Rekambo community had higher hunting rates than other sites (Bossou, Republic of Guinea; Kahuzi-Biega, Democratic Republic of Congo; Budongo, Uganda) where red colobus monkeys are also absent. We discuss these results and compare them to patterns at other long-term sites.

Gorillas' (Gorilla g. gorilla) knowledge of conspecifics' affordances: intraspecific social tool use for food acquisition.

The use of tools, long thought to be uniquely human, has now been observed in other animal taxa including several species of birds, non-primate mammals as well as some non-human primate species. Chimpanzees, one of humankind's closest living relatives, exceed all other non-human animal species as they have been reported to use an exceptionally large toolkit. However, relatively little is known about the tool-use skills of the other great ape species. While the majority of tools described are inanimate objects, the use of social tools has received relatively little attention. Here we provide the first evidence of naturally occurring spontaneous exploitative behaviour of a conspecific as a social tool for food acquisition in non-human animals. We observed gorillas in captivity utilising a conspecific as a ladder to gain access to unreachable food. We discuss our findings in the light of other studies on social tool use and suggest the need for more nuanced interpretations of gorillas' cognitive skills.

Old and New Approaches to Animal Cognition: There Is Not "One Cognition".

Using the comparative approach, researchers draw inferences about the evolution of cognition. Psychologists have postulated several hypotheses to explain why certain species are cognitively more flexible than others, and these hypotheses assume that certain cognitive skills are linked together to create a generally "smart" species. However, empirical findings suggest that several animal species are highly specialized, showing exceptional skills in single cognitive domains while performing poorly in others. Although some cognitive skills may indeed overlap, we cannot a priori assume that they do across species. We argue that the term "cognition" has often been used by applying an anthropocentric viewpoint rather than a biocentric one. As a result, researchers tend to overrate cognitive skills that are human-like and assume that certain skills cluster together in other animals as they do in our own species. In this paper, we emphasize that specific physical and social environments create selection pressures that lead to the evolution of certain cognitive adaptations. Skills such as following the pointing gesture, tool-use, perspective-taking, or the ability to cooperate evolve independently from each other as a concrete result of specific selection pressures, and thus have appeared in distantly related species. Thus, there is not "one cognition". Our argument is founded upon traditional Darwinian thinking, which-although always at the forefront of biology-has sometimes been neglected in animal cognition research. In accordance with the biocentric approach, we advocate a broader empirical perspective as we are convinced that to better understand animal minds, comparative researchers should focus much more on questions and experiments that are ecologically valid. We should investigate nonhuman cognition for its own sake, not only in comparison to the human model.

Ravens parallel great apes in physical and social cognitive skills.

Human children show unique cognitive skills for dealing with the social world but their cognitive performance is paralleled by great apes in many tasks dealing with the physical world. Recent studies suggested that members of a songbird family-corvids-also evolved complex cognitive skills but a detailed understanding of the full scope of their cognition was, until now, not existent. Furthermore, relatively little is known about their cognitive development. Here, we conducted the first systematic, quantitative large-scale assessment of physical and social cognitive performance of common ravens with a special focus on development. To do so, we fine-tuned one of the most comprehensive experimental test-batteries, the Primate Cognition Test Battery (PCTB), to raven features enabling also a direct, quantitative comparison with the cognitive performance of two great ape species. Full-blown cognitive skills were already present at the age of four months with subadult ravens' cognitive performance appearing very similar to that of adult apes in tasks of physical (quantities, and causality) and social cognition (social learning, communication, and theory of mind). These unprecedented findings strengthen recent assessments of ravens' general intelligence, and aid to the growing evidence that the lack of a specific cortical architecture does not hinder advanced cognitive skills. Difficulties in certain cognitive scales further emphasize the quest to develop comparative test batteries that tap into true species rather than human specific cognitive skills, and suggest that socialization of test individuals may play a crucial role. We conclude to pay more attention to the impact of personality on cognitive output, and a currently neglected topic in Animal Cognition-the linkage between ontogeny and cognitive performance.

Chimpanzee ethnography reveals unexpected cultural diversity.

Human ethnographic knowledge covers hundreds of societies, whereas chimpanzee ethnography encompasses at most 15 communities. Using termite fishing as a window into the richness of chimpanzee cultural diversity, we address a potential sampling bias with 39 additional communities across Africa. Previously, termite fishing was known from eight locations with two distinguishable techniques observed in only two communities. Here, we add nine termite-fishing communities not studied before, revealing 38 different technical elements, as well as community-specific combinations of three to seven elements. Thirty of those were not ecologically constrained, permitting the investigation of chimpanzee termite-fishing culture. The number and combination of elements shared among individuals were more similar within communities than between them, thus supporting community-majority conformity via social imitation. The variation in community-specific combinations of elements parallels cultural diversity in human greeting norms or chopstick etiquette. We suggest that termite fishing in wild chimpanzees shows some elements of cumulative cultural diversity.

Author Correction: Chimpanzee ethnography reveals unexpected cultural diversity.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.