Many morphs: Parsing gesture signals from the noise.

Parsing signals from noise is a general problem for signallers and recipients, and for researchers studying communicative systems. Substantial efforts have been invested in comparing how other species encode information and meaning, and how signalling is structured. However, research depends on identifying and discriminating signals that represent meaningful units of analysis. Early approaches to defining signal repertoires applied top-down approaches, classifying cases into predefined signal types. Recently, more labour-intensive methods have taken a bottom-up approach describing detailed features of each signal and clustering cases based on patterns of similarity in multi-dimensional feature-space that were previously undetectable. Nevertheless, it remains essential to assess whether the resulting repertoires are composed of relevant units from the perspective of the species using them, and redefining repertoires when additional data become available. In this paper we provide a framework that takes data from the largest set of wild chimpanzee (Pan troglodytes) gestures currently available, splitting gesture types at a fine scale based on modifying features of gesture expression using latent class analysis (a model-based cluster detection algorithm for categorical variables), and then determining whether this splitting process reduces uncertainty about the goal or community of the gesture. Our method allows different features of interest to be incorporated into the splitting process, providing substantial future flexibility across, for example, species, populations, and levels of signal granularity. Doing so, we provide a powerful tool allowing researchers interested in gestural communication to establish repertoires of relevant units for subsequent analyses within and between systems of communication.

Call combinations and compositional processing in wild chimpanzees.

Through syntax, i.e., the combination of words into larger phrases, language can express a limitless number of messages. Data in great apes, our closest-living relatives, are central to the reconstruction of syntax's phylogenetic origins, yet are currently lacking. Here, we provide evidence for syntactic-like structuring in chimpanzee communication. Chimpanzees produce "alarm-huus" when surprised and "waa-barks" when potentially recruiting conspecifics during aggression or hunting. Anecdotal data suggested chimpanzees combine these calls specifically when encountering snakes. Using snake presentations, we confirm call combinations are produced when individuals encounter snakes and find that more individuals join the caller after hearing the combination. To test the meaning-bearing nature of the call combination, we use playbacks of artificially-constructed call combinations and both independent calls. Chimpanzees react most strongly to call combinations, showing longer looking responses, compared with both independent calls. We propose the "alarm-huu + waa-bark" represents a compositional syntactic-like structure, where the meaning of the call combination is derived from the meaning of its parts. Our work suggests that compositional structures may not have evolved de novo in the human lineage, but that the cognitive building-blocks facilitating syntax may have been present in our last common ancestor with chimpanzees.

Maternal attitudes and behaviours differentially shape infant early life experience: A cross cultural study.

Early life environments afford infants a variety of learning opportunities, and caregivers play a fundamental role in shaping infant early life experience. Variation in maternal attitudes and parenting practices is likely to be greater between than within cultures. However, there is limited cross-cultural work characterising how early life environment differs across populations. We examined the early life environment of infants from two cultural contexts where attitudes towards parenting and infant development were expected to differ: in a group of 53 mother-infant dyads in the UK and 44 mother-infant dyads in Uganda. Participants were studied longitudinally from when infants were 3- to 15-months-old. Questionnaire data revealed the Ugandan mothers had more relational attitudes towards parenting than the mothers from the UK, who had more autonomous parenting attitudes. Using questionnaires and observational methods, we examined whether infant development and experience aligned with maternal attitudes. We found the Ugandan infants experienced a more relational upbringing than the UK infants, with Ugandan infants receiving more distributed caregiving, more body contact with their mothers, and more proximity to mothers at night. Ugandan infants also showed earlier physical development compared to UK infants. Contrary to our expectations, however, Ugandan infants were not in closer proximity to their mothers during the day, did not have more people in proximity or more partners for social interaction compared to UK infants. In addition, when we examined attitudes towards specific behaviours, mothers' attitudes rarely predicted infant experience in related contexts. Taken together our findings highlight the importance of measuring behaviour, rather than extrapolating expected behaviour based on attitudes alone. We found infants' early life environment varies cross-culturally in many important ways and future research should investigate the consequences of these differences for later development.

Declarative referential gesturing in a wild chimpanzee (Pan troglodytes).

Humans are argued to be unique in their ability and motivation to share attention with others about external entities-sharing attention for sharing's sake. Indeed, in humans, using referential gestures declaratively to direct the attention of others toward external objects and events emerges in the first year of life. In contrast, wild great apes seldom use referential gestures, and when they do, it seems to be exclusively for imperative purposes. This apparent species difference has fueled the argument that the motivation and ability to share attention with others is a human-specific trait with important downstream consequences for the evolution of our complex cognition [M. Tomasello, Becoming Human (2019)]. Here, we report evidence of a wild ape showing a conspecific an item of interest. We provide video evidence of an adult female chimpanzee, Fiona, showing a leaf to her mother, Sutherland, in the context of leaf grooming in Kibale Forest, Uganda. We use a dataset of 84 similar leaf-grooming events to explore alternative explanations for the behavior, including food sharing and initiating dyadic grooming or playing. Our observations suggest that in highly specific social conditions, wild chimpanzees, like humans, may use referential showing gestures to direct others' attention to objects simply for the sake of sharing. The difference between humans and our closest living relatives in this regard may be quantitative rather than qualitative, with ramifications for our understanding of the evolution of human social cognition.

Chimpanzee pant-hoots encode individual information more reliably than group differences.

Vocal learning, the ability to modify the acoustic structure of vocalizations based on social experience, is a fundamental feature of speech in humans (Homo sapiens). While vocal learning is common in taxa such as songbirds and whales, the vocal learning capacities of nonhuman primates appear more limited. Intriguingly, evidence for vocal learning has been reported in chimpanzees (Pan troglodytes), for example, in the form of regional variation ("dialects") in the "pant-hoot" calls. This suggests that some capacity for vocal learning may be an ancient feature of the Pan-Homo clade. Nonetheless, reported differences have been subtle, with intercommunity variation representing only a small portion of the total acoustic variation. To gain further insights into the extent of regional variation in chimpanzee vocalizations, we performed an analysis of pant-hoots from chimpanzees in the neighboring Kasekela and Mitumba communities at Gombe National Park, Tanzania, and the geographically distant Kanyawara community at Kibale National Park, Uganda. We did not find any statistically significant differences between the neighboring communities at Gombe or among geographically distant communities. Furthermore, we found differences among individuals in all communities. Hence, the variation in chimpanzee pant-hoots reflected individual differences, rather than group differences. Thus, we did not find evidence of dialects in this population, suggesting that extensive vocal learning emerged only after the lineages of Homo and Pan diverged.

Vocal signals facilitate cooperative hunting in wild chimpanzees.

Cooperation and communication likely coevolved in humans. However, the evolutionary roots of this interdependence remain unclear. We address this issue by investigating the role of vocal signals in facilitating a group cooperative behavior in an ape species: hunting in wild chimpanzees. First, we show that bark vocalizations produced before hunt initiation are reliable signals of behavioral motivation, with barkers being most likely to participate in the hunt. Next, we find that barks are associated with greater hunter recruitment and more effective hunting, with shorter latencies to hunting initiation and prey capture. Our results indicate that the coevolutionary relationship between vocal communication and group-level cooperation is not unique to humans in the ape lineage and is likely to have been present in our last common ancestor with chimpanzees.

Degraded and computer-generated speech processing in a bonobo.

The human auditory system is capable of processing human speech even in situations when it has been heavily degraded, such as during noise-vocoding, when frequency domain-based cues to phonetic content are strongly reduced. This has contributed to arguments that speech processing is highly specialized and likely a de novo evolved trait in humans. Previous comparative research has demonstrated that a language competent chimpanzee was also capable of recognizing degraded speech, and therefore that the mechanisms underlying speech processing may not be uniquely human. However, to form a robust reconstruction of the evolutionary origins of speech processing, additional data from other closely related ape species is needed. Specifically, such data can help disentangle whether these capabilities evolved independently in humans and chimpanzees, or if they were inherited from our last common ancestor. Here we provide evidence of processing of highly varied (degraded and computer-generated) speech in a language competent bonobo, Kanzi. We took advantage of Kanzi's existing proficiency with touchscreens and his ability to report his understanding of human speech through interacting with arbitrary symbols called lexigrams. Specifically, we asked Kanzi to recognise both human (natural) and computer-generated forms of 40 highly familiar words that had been degraded (noise-vocoded and sinusoidal forms) using a match-to-sample paradigm. Results suggest that-apart from noise-vocoded computer-generated speech-Kanzi recognised both natural and computer-generated voices that had been degraded, at rates significantly above chance. Kanzi performed better with all forms of natural voice speech compared to computer-generated speech. This work provides additional support for the hypothesis that the processing apparatus necessary to deal with highly variable speech, including for the first time in nonhuman animals, computer-generated speech, may be at least as old as the last common ancestor we share with bonobos and chimpanzees.

Detecting joint attention events in mother-infant dyads: Sharing looks cannot be reliably identified by naïve third-party observers.

Joint attention, or sharing attention with another individual about an object or event, is a critical behaviour that emerges in pre-linguistic infants and predicts later language abilities. Given its importance, it is perhaps surprising that there is no consensus on how to measure joint attention in prelinguistic infants. A rigorous definition proposed by Siposova & Carpenter (2019) requires the infant and partner to gaze alternate between an object and each other (coordination of attention) and exchange communicative signals (explicit acknowledgement of jointly sharing attention). However, Hobson and Hobson (2007) proposed that the quality of gaze between individuals is, in itself, a sufficient communicative signal that demonstrates sharing of attention. They proposed that observers can reliably distinguish "sharing", "checking", and "orienting" looks, but the empirical basis for this claim is limited as their study focussed on two raters examining looks from 11-year-old children. Here, we analysed categorisations made by 32 naïve raters of 60 infant looks to their mothers, to examine whether they could be reliably distinguished according to Hobson and Hobson's definitions. Raters had overall low agreement and only in 3 out of 26 cases did a significant majority of the raters agree with the judgement of the mother who had received the look. For the looks that raters did agree on at above chance levels, look duration and the overall communication rate of the mother were identified as cues that raters may have relied upon. In our experiment, naïve third party observers could not reliably determine the type of look infants gave to their mothers, which indicates that subjective judgements of types of look should not be used to identify mutual awareness of sharing attention in infants. Instead, we advocate the use of objective behaviour measurement to infer that interactants know they are 'jointly' attending to an object or event, and believe this will be a crucial step in understanding the ontogenetic and evolutionary origins of joint attention.

Human listeners' perception of behavioural context and core affect dimensions in chimpanzee vocalizations.

Vocalizations linked to emotional states are partly conserved among phylogenetically related species. This continuity may allow humans to accurately infer affective information from vocalizations produced by chimpanzees. In two pre-registered experiments, we examine human listeners' ability to infer behavioural contexts (e.g. discovering food) and core affect dimensions (arousal and valence) from 155 vocalizations produced by 66 chimpanzees in 10 different positive and negative contexts at high, medium or low arousal levels. In experiment 1, listeners (n = 310), categorized the vocalizations in a forced-choice task with 10 response options, and rated arousal and valence. In experiment 2, participants (n = 3120) matched vocalizations to production contexts using yes/no response options. The results show that listeners were accurate at matching vocalizations of most contexts in addition to inferring arousal and valence. Judgments were more accurate for negative as compared to positive vocalizations. An acoustic analysis demonstrated that, listeners made use of brightness and duration cues, and relied on noisiness in making context judgements, and pitch to infer core affect dimensions. Overall, the results suggest that human listeners can infer affective information from chimpanzee vocalizations beyond core affect, indicating phylogenetic continuity in the mapping of vocalizations to behavioural contexts.

Chimpanzee lip-smacks confirm primate continuity for speech-rhythm evolution.

Speech is a human hallmark, but its evolutionary origins continue to defy scientific explanation. Recently, the open-close mouth rhythm of 2-7 Hz (cycles/second) characteristic of all spoken languages has been identified in the orofacial signals of several nonhuman primate genera, including orangutans, but evidence from any of the African apes remained missing. Evolutionary continuity for the emergence of speech is, thus, still inconclusive. To address this empirical gap, we investigated the rhythm of chimpanzee lip-smacks across four populations (two captive and two wild). We found that lip-smacks exhibit a speech-like rhythm at approximately 4 Hz, closing a gap in the evidence for the evolution of speech-rhythm within the primate order. We observed sizeable rhythmic variation within and between chimpanzee populations, with differences of over 2 Hz at each level. This variation did not result, however, in systematic group differences within our sample. To further explore the phylogenetic and evolutionary perspective on this variability, inter-individual and inter-population analyses will be necessary across primate species producing mouth signals at speech-like rhythm. Our findings support the hypothesis that speech recruited ancient primate rhythmic signals and suggest that multi-site studies may still reveal new windows of understanding about these signals' use and production along the evolutionary timeline of speech.

Infants' intentionally communicative vocalizations elicit responses from caregivers and are the best predictors of the transition to language: A longitudinal investigation of infants' vocalizations, gestures and word production.

What aspects of infants' prelinguistic communication are most valuable for learning to speak, and why? We test whether early vocalizations and gestures drive the transition to word use because, in addition to indicating motoric readiness, they (a) are early instances of intentional communication and (b) elicit verbal responses from caregivers. In study 1, 11 month olds (N = 134) were observed to coordinate vocalizations and gestures with gaze to their caregiver's face at above chance rates, indicating that they are plausibly intentionally communicative. Study 2 tested whether those infant communicative acts that were gaze-coordinated best predicted later expressive vocabulary. We report a novel procedure for predicting vocabulary via multi-model inference over a comprehensive set of infant behaviours produced at 11 and 12 months (n = 58). This makes it possible to establish the relative predictive value of different behaviours that are hierarchically organized by level of granularity. Gaze-coordinated vocalizations were the most valuable predictors of expressive vocabulary size up to 24 months. Study 3 established that caregivers were more likely to respond to gaze-coordinated behaviours. Moreover, the dyadic combination of infant gaze-coordinated vocalization and caregiver response was by far the best predictor of later vocabulary size. We conclude that practice with prelinguistic intentional communication facilitates the leap to symbol use. Learning is optimized when caregivers respond to intentional vocalizations with appropriate language.

Scratching beneath the surface: intentionality in great ape signal production.

Despite important similarities having been found between human and animal communication systems, surprisingly little research effort has focussed on whether the cognitive mechanisms underpinning these behaviours are also similar. In particular, it is highly debated whether signal production is the result of reflexive processes, or can be characterized as intentional. Here, we critically evaluate the criteria that are used to identify signals produced with different degrees of intentionality, and discuss recent attempts to apply these criteria to the vocal, gestural and multimodal communicative signals of great apes and more distantly related species. Finally, we outline the necessary research tools, such as physiologically validated measures of arousal, and empirical evidence that we believe would propel this debate forward and help unravel the evolutionary origins of human intentional communication. This article is part of the theme issue 'What can animal communication teach us about human language?'

Cooperation in children.

Cooperation is central to what makes us human. It is so deeply entrenched in our nature that it can be seen at the heart of every culture, whether it takes the form of group hunting, shared child-rearing, or large-scale, multi-national institutions such as the UN. And yet in contrast to the constancy of other forms of cooperation in non-human animals, such as termite-mound building or honey bee dancing, the changing face of human cooperation makes it seem more fragile, and its mechanisms more elusive. As with other features of our behaviour, human cooperation is the product of both genetic and cultural evolution. Studying cooperation in children, in different cultural environments, and in contrast to other species, provides a valuable window into the ways in which these two forms of inheritance interact over development, and a chance to distil out its constitutive components.

An exploration into the efficacy of public warning signs: A zoo case study.

Unauthorised feeding and touching of the animals by visitors to zoos and wildlife parks pose serious threats to the health of both animals and visitors alike. We tested the efficacy of four different "do not feed" signs designed to prevent zoo visitors from feeding a group of meerkats. Signs consisted of one of two different written messages and imagery of either a pair of watching human eyes, or meerkat pawprints as a control. Covert observation of visitor behaviour in the presence and absence of the signs was analysed. Visitors were significantly less likely to feed the meerkats when signs were present, than when they were absent. The effect of the signs was specific to the targeted behaviour in that feeding was reduced, but attempts to touch the meerkats increased with the presence of the signs. We did not find that the presence of watching eyes or the different wording on the signs affected the likelihood of visitors feeding the meerkats. We also examined factors that influenced the likelihood of visitors attending to the signs. We found that children were more likely to attend to signs than adults which has important implications for the design of such signs. Together our findings show that signs are effective in reducing the unwanted behaviours they target but may also result in displacement of these negative behaviours and that children are more likely to attend to these signs than adults.

Human behavioural discrimination of human, chimpanzee and macaque affective vocalisations is reflected by the neural response in the superior temporal sulcus.

Accurate perception of the emotional content of vocalisations is essential for successful social communication and interaction. However, it is not clear whether our ability to perceive emotional cues from vocal signals is specific to human signals, or can be applied to other species' vocalisations. Here, we address this issue by evaluating the perception and neural response to affective vocalisations from different primate species (humans, chimpanzees and macaques). We found that the ability of human participants to discriminate emotional valence varied as a function of phylogenetic distance between species. Participants were most accurate at discriminating the emotional valence of human vocalisations, followed by chimpanzee vocalisations. They were, however, unable to accurately discriminate the valence of macaque vocalisations. Next, we used fMRI to compare human brain responses to human, chimpanzee and macaque vocalisations. We found that regions in the superior temporal lobe that are closely associated with the perception of complex auditory signals, showed a graded response to affective vocalisations from different species with the largest response to human vocalisations, an intermediate response to chimpanzees, and the smallest response to macaques. Together, these results suggest that neural correlates of differences in the perception of different primate affective vocalisations are found in auditory regions of the human brain and correspond to the phylogenetic distances between the species.

Abilities to Explicitly and Implicitly Infer Intentions from Actions in Adults with Autism Spectrum Disorder.

Previous research suggests that Autism Spectrum Disorder (ASD) might be associated with impairments on implicit but not explicit mentalizing tasks. However, such comparisons are made difficult by the heterogeneity of stimuli and the techniques used to measure mentalizing capabilities. We tested the abilities of 34 individuals (17 with ASD) to derive intentions from others' actions during both explicit and implicit tasks and tracked their eye-movements. Adults with ASD displayed explicit but not implicit mentalizing deficits. Adults with ASD displayed typical fixation patterns during both implicit and explicit tasks. These results illustrate an explicit mentalizing deficit in adults with ASD, which cannot be attributed to differences in fixation patterns.

Function and flexibility of object exploration in kea and New Caledonian crows.

A range of non-human animals frequently manipulate and explore objects in their environment, which may enable them to learn about physical properties and potentially form more abstract concepts of properties such as weight and rigidity. Whether animals can apply the information learned during their exploration to solve novel problems, however, and whether they actually change their exploratory behaviour to seek functional information about objects have not been fully explored. We allowed kea (Nestor notabilis) and New Caledonian crows (Corvus moneduloides) to explore sets of novel objects both before and after encountering a task in which some of the objects could function as tools. Following this, subjects were given test trials in which they could choose among the objects they had explored to solve a tool-use task. Several individuals from both species performed above chance on these test trials, and only did so after exploring the objects, compared with a control experiment with no prior exploration phase. These results suggest that selection of functional tools may be guided by information acquired during exploration. Neither kea nor crows changed the duration or quality of their exploration after learning that the objects had a functional relevance, suggesting that birds do not adjust their behaviour to explicitly seek this information.

Is music enriching for group-housed captive chimpanzees (Pan troglodytes)?

Many facilities that house captive primates play music for animal enrichment or for caregiver enjoyment. However, the impact on primates is unknown as previous studies have been inconclusive. We conducted three studies with zoo-housed chimpanzees (Pan troglodytes) and one with group-housed chimpanzees at the National Centre for Chimpanzee Care to investigate the effects of classical and pop/rock music on various variables that may be indicative of increased welfare. Study one compared the behaviour and use of space of 18 animals when silence, classical or pop/rock music was played into one of several indoor areas. Overall, chimpanzees did not actively avoid the area when music was playing but were more likely to exit the area when songs with higher beats per minute were broadcast. Chimpanzees showed significantly fewer active social behaviours when music, rather than silence, was playing. They also tended to be more active and engage in less abnormal behaviour during the music but there was no change to either self-grooming or aggression between music and silent conditions. The genre of music had no differential effects on the chimpanzees' use of space and behaviour. In the second study, continuous focal observations were carried out on three individuals with relatively high levels of abnormal behaviour. No differences in behaviour between music and silence periods were found in any of the individuals. The final two studies used devices that allowed chimpanzees to choose if they wanted to listen to music of various types or silence. Both studies showed that there were no persistent preferences for any type of music or silence. When taken together, our results do not suggest music is enriching for group-housed captive chimpanzees, but they also do not suggest that music has a negative effect on welfare.

Exorcising Grice's ghost: an empirical approach to studying intentional communication in animals.

Language's intentional nature has been highlighted as a crucial feature distinguishing it from other communication systems. Specifically, language is often thought to depend on highly structured intentional action and mutual mindreading by a communicator and recipient. Whilst similar abilities in animals can shed light on the evolution of intentionality, they remain challenging to detect unambiguously. We revisit animal intentional communication and suggest that progress in identifying analogous capacities has been complicated by (i) the assumption that intentional (that is, voluntary) production of communicative acts requires mental-state attribution, and (ii) variation in approaches investigating communication across sensory modalities. To move forward, we argue that a framework fusing research across modalities and species is required. We structure intentional communication into a series of requirements, each of which can be operationalised, investigated empirically, and must be met for purposive, intentionally communicative acts to be demonstrated. Our unified approach helps elucidate the distribution of animal intentional communication and subsequently serves to clarify what is meant by attributions of intentional communication in animals and humans.

Diffusion of novel foraging behaviour in Amazon parrots through social learning.

While social learning has been demonstrated in species across many taxa, the role it plays in everyday foraging decisions is not well understood. Investigating social learning during foraging could shed light on the emergence of cultural variation in different groups. We used an open diffusion experiment to examine the spread of a novel foraging technique in captive Amazon parrots. Three groups were tested using a two-action foraging box, including experimental groups exposed to demonstrators using different techniques and control birds. We also examined the influence of agonistic and pilfering behaviour on task acquisition. We found evidence of social learning: more experimental birds than control birds interacted with and opened the box. The birds were, however, no more likely to use the demonstrated technique than the non-demonstrated one, making local or stimulus enhancement the most likely mechanism. Exhibiting aggression was positively correlated with box opening, whilst receiving aggression did not reduce motivation to engage with the box, indicating that willingness to defend access to the box was important in task acquisition. Pilfering food and success in opening the box were also positively correlated; however, having food pilfered did not affect victims' motivation to interact with the box. In a group context, pilfering may promote learning of new foraging opportunities. Although previous studies have demonstrated that psittacines are capable of imitation, in this naturalistic set-up there was no evidence that parrots copied the demonstrated opening technique. Foraging behaviour in wild populations of Amazons could therefore be facilitated by low-fidelity social learning mechanisms.