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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.

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.

Human language is thought to have evolved from non-linguistic communication systems present in the primate lineage. Scientists rely on data from extant primate species to estimate how this happened, with debates centering around which modality (vocalization, gesture, facial expression) was a likely precursor. In 2011, we demonstrated that different theoretical and methodological approaches are used to collect data about each modality, rendering datasets incomplete and comparisons problematic. Here, 10 years later, we conducted a follow-up systematic review to test whether patterns have changed, examining the primate communication literature published between 2011 and 2020. In sum, despite the promising progress in addressing some gaps in our knowledge, systematic biases still exist and multimodal research remains uncommon. We argue that theories of language evolution are unlikely to advance until the field of primate communication research acknowledges and rectifies the gaps in our knowledge.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships. Publisher PDF

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.

This research was supported by the Research Incentive Grant of The Carnegie Trust for the Universities of Scotland (grant no. RIG008132) attributed to A.R.L. 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. Postprint

International audience; Allogrooming in primates serves not only a hygienic function, but also plays a crucial role in maintaining strong affiliative bonds between group members, which in turn, underpin the emergence of cooperative behavior. In contrast, although allopreening occurs in many avian species, we know little about its social functions. Our study addresses this issue by investigating allopreening in a broad comparative data set including six corvid and nine parrot species. We assessed whether rates of allopreening initiations, proportion of time spent allopreening, and the number of grooming partners in captive group-housed birds were comparable to patterns observed in captive chimpanzees and bonobos. While parrots and corvids were found to have similar rates of social grooming to bonobos and chimpanzees, Pan species dedicated significantly more time to social grooming. Animals in larger groups had more grooming partners, but when controlling for the number of potential partners, birds tended to have fewer grooming interaction partners than Pan species. We then investigated whether allopreening in parrots and corvids was predicted by behavioral markers of affiliative social bonds (close physical proximity, active feeding, and low levels of agonistic behavior). Results revealed that providing allopreening to a partner was significantly predicted by often being in close proximity, but not engagement in active feeding or agonistic behavior. We examined the region allopreened in a subset of species and found that preening a partner's head was predicted by both close physical proximity and active feeding, while body allopreening was only predicted by close physical proximity. Head preening may confer more hygienic benefits to recipients, and thus, may be more selectively provided to valued partners. Results support the hypothesis that allopreening in corvids and parrots helps maintain social bonds with an individual's most important social partners, showing some similarities to allogrooming in primates.

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?’

Infant-directed speech (IDS) is a special speech register thought to aid language acquisition and improve affiliation in human infants. Although IDS shares some of its properties with dog-directed speech (DDS), it is unclear whether the production of DDS is functional, or simply an overgeneralisation of IDS within Western cultures. One recent study found that, while puppies attended more to a script read with DDS compared with adult-directed speech (ADS), adult dogs displayed no preference. In contrast, using naturalistic speech and a more ecologically valid set-up, we found that adult dogs attended to and showed more affiliative behaviour towards a speaker of DDS than of ADS. To explore whether this preference for DDS was modulated by the dog-specific words typically used in DDS, the acoustic features (prosody) of DDS or a combination of the two, we conducted a second experiment. Here the stimuli from experiment 1 were produced with reversed prosody, meaning the prosody and content of ADS and DDS were mismatched. The results revealed no significant effect of speech type, or content, suggesting that it is maybe the combination of the acoustic properties and the dog-related content of DDS that modulates the preference shown for naturalistic DDS. Overall, the results of this study suggest that naturalistic DDS, comprising of both dog-directed prosody and dog-relevant content words, improves dogs’ attention and may strengthen the affiliative bond between humans and their pets. Electronic supplementary material The online version of this article (10.1007/s10071-018-1172-4) contains supplementary material, which is available to authorized users.

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.

Funding: This study was funded by an European Research Council Consolidator grant (ERC_CoG 2016_724608) awarded to KS (https://erc.europa.eu/funding/consolidator-grants). 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. Publisher PDF

Facilities housing captive animals are full of staff who, every day, interact with the animals under their care. The expertise and familiarity of staff can be used to monitor animal welfare by means of questionnaires. It was the goal of our study to examine the association between chimpanzee (Pan troglodytes) welfare, happiness, and personality. To these ends we collected two waves of welfare and subjective well-being ratings of 18 chimpanzees housed at the Edinburgh Zoo and one set of ratings of 13 chimpanzees housed at Fundació Mona. Ratings were made on a welfare questionnaire that included 12 items related to stress, psychological stimulation, and behavioural indicators of negative and positive welfare states, and a 4-item subjective well-being questionnaire. In addition, ratings were made on the 54-item Hominoid Personality Questionnaire and an abbreviated version of this scale consisting of 37 antonym pairs. We used generalizability theory to test whether welfare ratings generalized across items, raters, chimpanzees, and time. We then assessed the validity of the welfare and subjective well-being questionnaires by examining their associations with behaviour. Finally, we tested whether the welfare and subjective well-being ratings were associated with personality. Welfare ratings generalized across items, raters, chimpanzees, and time. Principal components analysis and regularized exploratory factor analysis indicated that ten welfare items and all four subjective well-being items formed a single dimension (welfareSWB). LASSO regression found that lower welfareSWB was associated with regurgitation, coprophagy, urophagy, and decreased proximity to nearest neighbour. A linear model that adjusted for age, sex, and facility, indicated that higher Extraversion and lower Neuroticism were related to higher welfareSWB. Welfare ratings were reliable and associated with subjective well-being and personality, demonstrating that staff ratings are a valid and potentially valuable tool for chimpanzee welfare assessment.

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. Postprint

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.

The unique challenges faced by animals living in zoos can lead to the production of anxiety-related behaviours. In this study we aimed to understand what specific factors may cause chimpanzees to display these behaviours. In non-human primates, displacement behaviours, such as self-scratching and yawning, are considered markers of anxiety and stress, and Regurgitation and Reingestion (R/R) is considered an abnormal behaviour with negative consequences for physical health. We examined the possible triggers of R/R, scratching, and yawning in a group of zoo-housed chimpanzees and followed this up with an analysis of long-term data to examine further aspects of R/R behaviour. In the first study we conducted focal observations on 18 adult chimpanzees at Edinburgh Zoo, UK, in addition to all occurrence sampling of visitors using flash photography, screaming and banging on the glass in the exhibit. 158 h of data were analysed and Generalised Linear Mixed Models revealed that yawning was significantly more likely if there was a long period of time since the last feed and when there were moderate numbers of visitors in the zoo. There were trends that yawning was more likely to occur if children screamed and that scratching was more likely to occur if visitors used flash photography. R/R occurred most often within 40 min of a feed, but was not affected by the inter-feed interval preceding that feed, positive or negative social interactions, or visitor numbers or behaviour. As there was no obvious daily trigger for R/R, an analysis of long-term data (2009 to 2015) was conducted to investigate if social or dietary factors affected rates of R/R over a larger timescale. It was found that R/R rates in the months before a significant diet change were not different from R/R rates in the months after, but it was found that R/R rates decreased over the five-year period. Lastly, we found no evidence that the introduction of individuals engaging in R/R lead to resident chimpanzees habitually adopting the behaviour, despite considerable opportunities to observe it. These findings have implications for welfare interventions aimed to reduce R/R and/or anxiety behaviours in captive populations and for the translocation of individuals that are known to engage in R/R between groups.

Vocal communication is common in the animal kingdom. Researchers often examine vocal communication in nonhuman primates (primates) with the aim of identifying similarities and differences with human language and speech, in order to trace the evolutionary origins of our complex communication system. Primates can produce distinct calls in response to specific events, such as the discovery of a certain predator, and listeners seem to understand what these calls refer to. Although on the surface there are similarities between this type of communication and human referential words, the mental processes that underlie them may be very different. While in general the flexibility shown by primate receivers may demonstrate some commonalities with humans, there is much more controversy over whether there are similarities between the production of primate vocalizations and language. It is widely accepted that primates, unlike humans, lack the ability to generate new vocalizations. Although this means primates have a closed repertoire of calls that cannot be expanded, primates are capable of combining their existing calls to generate new messages. The degree of voluntary control and intentionality involved in the use of calls is also a matter of debate, with recent evidence on both a neural and behavioral level challenging traditional assumptions that primate vocalizations are used in an automatic, reflexive manner. More research is needed to examine the mental processes underlying communicative behavior in both the producer and the receiver. In the future adopting a more holistic, multimodal approach to studying primate communication is likely to challenge and ultimately improve our understanding of primate communication and the evolution of human language. Keywords: communication; vocalizations; primates; evolution; language; speech; monkey; chimpanzee; intentionality

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.

Essay writing is often a fundamental component of assessment in higher education, therefore we need to find effective ways of encouraging students to develop strong writing skills. This study aimed to evaluate the efficacy of an interactive exercise designed to demonstrate the importance of essay structure and organisation. During an essay-writing seminar over four academic years, 3rd year undergraduate students (N=510) were given 5 minutes to assign a grade category (1st, 2:1, 2:2, 3rd) to an essay. Half the students marked a well-structured essay, and half marked a poorly-structured version that contained slightly more content, but students were blind to this manipulation. The grades awarded by the students to each type of essay were then disseminated. We hypothesised that students would award higher marks to the well-structured essay, and that this exercise would increase awareness of the importance of structuring essays. Results revealed that the well-structured essays were significantly associated with high marks (1st/ 2:1s) and poorly-structured essays significantly associated with low marks (2:2/ 3rd) and this pattern was consistent across four cohorts. Significantly more students reported that structure was the most important element in essay writing after this exercise than before, indicating it was effective in highlighting the importance of structure, and 91% of students reported that the session had increased their awareness of the importance of structure. The results support the use of this exercise to increase student awareness of the importance of essay structure and indicates that actively involving students in the assessment process may improve students? understanding of expectations We hope the exercise assessed in the current study will be used in other educational programmes where essay writing is a core part of assessment.

Animals communicate using a vast array of different signals in different modalities. For chimpanzees, vocalizations, gestures and facial expressions are all important forms of communication, yet these signals have rarely been studied together holistically. The current study aimed to provide the first comprehensive repertoire of flexibly combined (‘free’) multimodal (MM) signals, and assess individual and contextual factors influencing production of, and responses to, unimodal (UM) and MM signals in wild chimpanzees. In total, 48 different free MM signals were produced. MM signals were produced at a significantly lower rate than UM signals, but 22 of 26 focal animals were observed to produce free MM signals. The relative production rates of different types of UM and MM signals differed significantly between the behavioural contexts investigated, showing flexible use of signals across contexts. In contrast, individual factors such as age, sex or rank of signaller did not appear to influence the type of signal produced or the likelihood of eliciting a response. Finally, we compared recipient responses to free MM grunt-gesture signals and matched UM component signals and found that these MM signals were more likely to elicit a response than a grunt alone, but were as likely to elicit a response as the gesture alone. The overall findings point to a widespread capacity for wild chimpanzees to flexibly combine signals from different modalities and highlight the importance of adopting a multimodal approach to studying communication.

Long-distance calls have a variety of functions in different animal species. However, where multiple functions are proposed for a single long-distance call type, little is known about their relative importance. Chimpanzees are one species where several functions have been proposed for their long-distance call, the pant hoot. In this study, we investigated the effect of social factors, including the rank of the caller, party size, fission-fusion rates, and the presence of estrus females as well as ecological factors including the type of food consumed and travel time, on male chimpanzee (Pan troglodytes schweinfurthii) pant hooting, in order to identify the key correlates of this behavior. The wild male chimpanzees of the Kanyawara community, Uganda, produced more pant hoots on days when there were frequent changes in the male, but not female, composition of the focal's party. This factor accounted for the largest amount of variation in pant hoot production, and we found that males were more likely to repeat a call prior to rather than after fusion with other males, suggesting that the calls facilitate fusion. Pant hoots therefore seem to play a pivotal role in regulating grouping dynamics in chimpanzees. Our study also shows that pant hooting was positively correlated with the rank of the caller, the presence of parous females in estrus, and the consumption of high-quality food, suggesting that pant hoots signal social status or social bonds when between-male competition is high. This study supports the view that pant hoots fulfill a complex social function.

Pseudoreplication (the pooling fallacy) is a widely acknowledged statistical error in the behavioural sciences. Taking a large number of data points from a small number of animals creates a false impression of a better representation of the population. Studies of communication may be particularly prone to artificially inflating the data set in this way, as the unit of interest (the facial expression, the call or the gesture) is a tempting unit of analysis. Primate communication studies (551) published in scientific journals from 1960 to 2008 were examined for the simplest form of pseudoreplication (taking more than one data point from each individual). Of the studies that used inferential statistics, 38% presented at least one case of pseudoreplicated data. An additional 16% did not provide enough information to rule out pseudoreplication. Generalized linear mixed models determined that one variable significantly increased the likelihood of pseudoreplication: using observational methods. Actual sample size (number of animals) and year of publication were not associated with pseudoreplication. The high prevalence of pseudoreplication in the primate communication research articles, and the fact that there has been no decline since key papers warned against pseudoreplication, demonstrates that the problem needs to be more actively addressed.

Duetting or chorusing behaviour occurs in a wide variety of animals and is posited to fulfil various important functions including territory defence and social bonding. The structure of calls produced in choruses might be shaped in a way that facilitates such joint vocal displays. In this study, we test the hypothesis that flexibility to modify the temporal structure of chimpanzee pant-hoots, vocalisations often given jointly with other individuals, facilitates chorusing. The results of this study, which was conducted on two communities of wild chimpanzees in Uganda, support this hypothesis. First, the duration of the build-up phase of the pant-hoot correlated with the latency with which the partner joined in the call, suggesting that males prolong the duration of the build-up to allow others to join in the call and to increase the likelihood of a chorus occurring. Second, the loud climax phases were significantly longer when produced in choruses than alone, which suggests that males prolong this part of the call when calling in choruses. Within chorus pant-hoots, there was a positive relationship between the number of climax elements given by two calling partners, suggesting that males adjust the temporal structure of their call to mirror their partner's call. We conclude that the basic acoustic structure of chimpanzee pant-hoots and the flexibility with which males adjust the duration of the constituent phases promote chorusing, and that the temporal structure of this rather stereotyped vocalisation is sensitive to fine details of the vocal responses of the audience.

Ethnoprimatology is an important and growing discipline, studying the diverse relationships between humans and primates. However there is a danger that too great a focus on primates as important to humans may obscure the importance of other animal groups to local people. The Waorani of Amazonian Ecuador were described by Sponsel [Sponsel (1997) New World Primates: Ecology, evolution and behavior. New York: Aldine de Gruyter. p 143–165] as the “natural place” for ethnoprimatology, because of their close relationship to primates, including primates forming a substantial part of their diet. Therefore they are an ideal group in which to examine contemporary perceptions of primates in comparison to other types of animal. We examine how Waorani living in Yasuni National Park name and categorize primates and other common mammals. Although there is some evidence that the Waorani consider primates a unique group, the non-primate kinkajou and olingo are also included as part of the group “monkeys,” and no evidence was found that primates were more important than other mammals to Waorani culture. Instead, a small number of key species, in particular the woolly monkey (Lagothrix poeppigii) and white-lipped peccary (Tayassu pecari), were found to be both important in the diet and highly culturally salient. These results have implications for both ethnoprimatologists and those working with local communities towards broader conservation goals. Firstly, researchers should ensure that they and local communities are referring to the same animals when they use broad terms such as “monkey,” and secondly the results caution ethnoprimatologists against imposing western taxonomic groups on indigenous peoples, rather than allowing them to define themselves which species are important. Am. J. Primatol. 75:1117–1128, 2013. © 2013 The Authors. American Journal of Primatology Published by Wiley Periodicals, Inc.

There is an ongoing debate about the adaptive function of chimpanzee's food-associated calls. Here, we tested a new hypothesis that food-associated calls in male chimpanzees function to signal that the calling individual is likely to initiate or prolong feeding. We propose that the signal functions to coordinate activities between individuals and that its ultimate function is to retain the nearby individuals in proximity. To test this hypothesis, we collected data on social and ecological correlates of food-associates calls in male chimpanzees. The results of this study, which was conducted on the Kanyawara community in the Kibale National Park, Uganda, show that males tended to feed for significantly longer after giving food-associated calls upon initiating feeding than after remaining silent. The type of audience had a significant effect on food calling, with males producing food-associated calls more often when males rather than females and preferred rather than neutral male social partners were in close proximity. However, the total party or male party size did not correlate with food calling behaviors, suggesting that the signal “targets” those in close proximity. Finally, a male feeding partner was more likely to remain with the focal until the end of a feeding bout after the focal gave a food-associated call at the beginning of the feeding bout than when he was silent. These results support our hypothesis and suggest that one of the functions of food calling in chimpanzees might be signaling that the caller is likely to initiate and prolong a feeding bout. This information might be used by receivers to make the decision whether or not to stay with the calling individual on a feeding patch or leave him (fission). The study suggests therefore that ultimately the function of food calling might be to coordinate feeding behaviors between males. Am. J. Primatol. 75:726-739, 2013. © 2013 Wiley Periodicals, Inc.

Chimpanzees are highly territorial and have the potential to be extremely aggressive toward unfamiliar individuals. In the wild, transfer between groups is almost exclusively completed by nulliparous females, yet in captivity there is often a need to introduce and integrate a range of individuals, including adult males. We describe the process of successfully integrating two groups of chimpanzees, each containing 11 individuals, in the Budongo Trail facility at the Royal Zoological Society of Scotland's Edinburgh Zoo. We use social network analysis to document changes in group dynamics within this population over the 16 months following integration. Aggression rates were low overall and members of the two original groups engaged in significantly fewer aggressive interactions over time. Association and grooming data indicate that relationships between members of the original groups became stronger and more affiliative with time. Despite these positive indicators the association data revealed the continued existence of two distinct subgroups, a year after integration. Our data show that when given complex space and freedom to exhibit natural fission–fusion groupings, in which the chimpanzees choose whom they wish to associate and interact with, the building of strong affiliative relationships with unfamiliar individuals is a very gradual process. Am. J. Primatol. 75:254-266, 2013. © 2012 Wiley Periodicals, Inc.

This research was supported by The British Psychological Society Summer Bursary, awarded to Lauren Hogan. 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. Postprint

Individuals with Asperger's syndrome (AS) often have difficulties with social interactions and conversations. We investigated if these difficulties could be attributable to a deficit in the ability to linguistically converge with an interlocutor, which is posited to be important for successful communication. To that end, participants completed two cooperative tasks with a confederate, which allowed us to measure linguistic alignment with the confederate in terms of lexical choice, syntactic structure and spatial frame of reference. There was no difference in the performance of individuals with AS and matched controls and both groups showed significant alignment with the confederate at all three levels. We conclude that linguistic alignment is intact in adults with AS engaged in structured, goal-directed social interactions.

Long-distance calling is a common behaviour in animals, which has various important social functions. At a physiological level, calling is often mediated by gonadal hormones such as testosterone (T), particularly when its function is linked to intra-sexual competition for mates or territory. T also plays an important role in the development of vocal characteristics associated with dominance in humans. However, the few available studies of T and vocal behaviour in non-human primates suggest that in primates, T has less influence on call production than in other animals. We tested this hypothesis by studying the relationship between T concentrations and pant-hooting in wild male chimpanzees (Pan troglodytes schweinfurthii) of the Kanyawara community in the Kibale National Park, Uganda. We found three kinds of correlation. Hourly T averages were positively associated with hourly rates of pant-hooting. Monthly T levels were likewise correlated with monthly rates of pant-hooting after controlling for other influences such as fission-fusion rates. Finally, males with high T levels had higher peak frequency at the start of the call climax. These results suggest that T affects the production of pant-hoots in chimpanzees. This implies that the pant-hoot call plays a role in male-male competition. We propose that even in cognitively sophisticated species, endocrine mechanisms can contribute to regulating vocal production. Significance statement: Many animals produce long-distance calls. The production of these calls is often modulated by gonadal hormones such as testosterone, especially if the calls are involved in competition between males for mates or territory. However, comparatively little is known about the influence of testosterone over the vocal behaviour of non-human primates, especially among great apes. In this study, we examined the relationship between testosterone and pant-hooting in wild male chimpanzees. We found that testosterone levels were associated with pant-hoot rates and one acoustic feature of the call. More specifically, males pant-hooted more often and produced pant-hoots with higher peak frequencies during periods of elevated testosterone levels. These results imply that gonadal hormones are involved in regulating vocal behaviour in chimpanzees and support the view that pant-hoots play a role in male-male competition.

Summary 1. Understanding human resource extraction is crucial for conservation science, allowing accurate assessments of system sustainability and testing key assumptions about human resource users. 2. We apply ecological methods and principles to Global Positioning System (GPS) data on human movement to investigate the ecological and behavioural differences between human hunters and non-hunters, a method which can be reproduced with any species which routinely return to a central place. The integration of movement ecology and habitat selection can greatly augment the applicability and scope of both disciplines, and we explore the issues that arise from integration, because of the differing data types and methods used by each approach. 3. We propose an adaptable methodological framework which can be used to combine movement ecology and habitat selection when using data from GPS tracking devices, whether from human or animal foragers. The methodology is based on three steps and can be implemented in the free downloadable statistical program R, using the full code in the Data S1. 4. First, we show that net squared displacement, coupled with nonlinear mixed-effects models, is suitable for quantifying characteristics of small-scale movement, such as daily travel patterns, and extracting parts of these journeys for analysis. 5. Secondly, having extracted part of a journey, biased random bridges use the auto-correlated GIS tracking data to create a utilization distribution (UD) for each individual. This method includes movement between known locations to estimate use intensity in an area. 6. Finally, the UD can be analysed by a resource utilization function which relates the intensity of use to landscape features of an area to identify habitats selected by an individual. This can be used to predict use of the landscape at larger scales for both individuals and an entire population. 7. This methodological framework is a flexible method to accurately assess human and animal resource use and movement through the natural environment.

P.F. was funded by Swiss National Science Foundation (310030_143359) and European Research Council project grants to K.Z. (PRILANG 283871). Conflict and aggressive interactions are common phenomena in group-living animals and vocal behaviour often plays an important role in determining their outcomes. In some species, vocal signals seem to provide bystanders with information about the nature of an ongoing aggressive interaction, which can be beneficial for the victims. For example, in chimpanzees and some other primates, victims adjust their screams depending on the composition of the by-standing audience, probably to solicit their support. Considerably less is known, however, about the role of other call types produced by victims of aggression. In this study, we focused on the fact that, immediately after screams, chimpanzee, Pan troglodytes schweinfurthii, victims often produce 'waa' barks, but little is known about their function. Our results showed that for screams, but not 'waa' barks, production was dependent on the audience composition with victims being more likely to scream when adult or late-adolescent males were in close proximity. We also found that after 'waa' barking, but not screaming, victims were more likely to retaliate against and less likely to reconcile with their aggressors, and that 'waa' barking was more common after victims had received support from other party members. These results suggest that, in chimpanzees, victims of aggression vocalize with a dual social strategy of attempting to recruit support from bystanders and to repel their attackers by signalling readiness to retaliate. We conclude that victim scream and 'waa' bark calls, although often produced during the same agonistic event, are directed at different audiences and fulfil different social functions, and that these calls can mediate both aggressive interactions and aggressor-victim relationships following aggression. Postprint

Chimpanzees produce acoustically distinct calls when encountering food. Previous research on a number of species has indicated that food-associated calls are relatively widespread in animal communication, and the production of these calls can be influenced by both ecological and social factors. Here, we investigate the factors influencing the production of food-associated calls in wild chimpanzees and examine whether male chimpanzees produce food-associated calls selectively in the presence of important social partners. Male chimpanzees form stable long-term social relationships with each other, and these social bonds are vital in enabling a range of cooperative activities, such as group hunting and territory defence. Our data show that males were significantly more likely to produce food-associated calls if an important social partner was nearby, regardless of the size of the audience or the presence of oestrus females. Call production was also mediated by the size of the food patch and by whether or not the food could be monopolised. The presence of important social partners explained most of the variation in male calling behaviour, indicating that food-associated calls are socially directed and serve a bonding function.

When experiencing aggression from group members, chimpanzees commonly produce screams. These agonistic screams are graded signals and vary acoustically as a function of the severity of aggression the caller is facing. We conducted a series of field playback experiments with a community of wild chimpanzees in the Budongo Forest, Uganda, to determine whether individuals could meaningfully distinguish between screams given in different agonistic contexts. We compared six subjects' responses to screams given in response to severe and mild aggression. Subjects consistently discriminated between the two scream types. To address the possibility that the response differences were driven directly by the screams' peripheral acoustic features, rather than any attached social meaning, we also tested the subjects' responses to tantrum screams. These screams are given by individuals that experienced social frustration, but no physical threat, yet acoustically they are very similar to screams of victims of severe aggression. We found chimpanzees looked longer at severe victim screams than either mild victim screams or tantrum screams. Our results indicate that chimpanzees attend to the informational content of screams and are able to distinguish between different scream variants, which form part of a graded continuum.

Chimpanzees produce specific vocalizations, ‘rough grunts’, when encountering food, and it has been suggested that these calls vary acoustically depending on the food type discovered by the caller. Nearby listeners often behave as if the calls are meaningful to them, indicating that the calls may function as referential labels for particular foods. We investigated whether rough grunt variants are the result of callers responding to specific food types or relative food preferences. We recorded calls from captive individuals in response to nine different food items, which could be ranked as high, medium or low preference. Individuals consistently produced three acoustically distinct grunt variants to the three food preference classes. There was no evidence that chimpanzees produced individual labels for food types of low and medium preference. However, calls to high-preference food types differed significantly in their acoustic structure. These acoustic patterns remained stable over trials, suggesting that rough grunts have the potential to serve as semantic labels for individual high-preference food types. We were unable to replicate these findings with a set of recordings from the wild, although most other aspects of calling behaviour remained identical. We discuss these discrepancies between the wild and captivity and suggest that the emergence of referential labels for food items may be a by-product of the special circumstances found in captive settings.

Summary The evolutionary origins of the use of speech signals to refer to events or objects in the world have remained obscure. Although functionally referential calls have been described in some monkey species [1, 2], studies with our closest living relatives, the great apes, have not generated comparable findings. These negative results have been taken to suggest that ape vocalizations are not the product of their otherwise sophisticated mentality and that ape gestural communication is more informative for theories of language evolution [3, 4]. We tested whether chimpanzee rough grunts, which are produced during feeding contexts [5–8], functioned as referential signals. Individuals produced acoustically distinct types of “rough grunts” when encountering different foods. In a naturalistic playback experiment, a focal subject was able to use the information conveyed by these calls produced by several group mates to guide his search for food, demonstrating that the different grunt types were meaningful to him. This study provides experimental evidence that our closest living relatives can produce and understand functionally referential calls as part of their natural communication. We suggest that these findings give support to the vocal rather than gestural theories of language evolution.

Although food sharing is a habitual aspect of chimpanzee (Pan troglodytes) life, sharing of plant foods between unrelated adults is rare. Observations of such behavior have typically been interpreted as the outcome of a process by which individuals that are otherwise unable to gain access to the food manage to obtain a nutritional benefit. Here we present behavioral details and an acoustic analysis regarding an observation of food sharing between unrelated adult wild chimpanzees that we suggest cannot be explained using traditional nutrition-based models. Instead we propose that the exchange is only understandable as a socially important event, and we cite two further observations in the same population that support this suggestion.

This work was supported by the National Evolutionary Synthesis Center (NESCent) through support of a working group led by C.L.N. and B.H. NESCent is supported by the National Science Foundation (NSF) EF-0905606. For training in phylogenetic comparative methods, we thank the AnthroTree Workshop (supported by NSF BCS-0923791). Y.S. thanks the National Natural Science Foundation of China (Project 31170995) and National Basic Research Program (973 Program: 2010CB833904). E.E.B. thanks the Duke Vertical Integration Program and the Duke Undergraduate Research Support Office. J.M.P. was supported by a Newton International Fellowship from the Royal Society and the British Academy. L.R.S. thanks the James S. McDonnell Foundation for Award 220020242. L.J.N.B. and M.L.P. acknowledge the National Institutes of Mental Health (R01-MH096875 and R01-MH089484), a Duke Institute for Brain Sciences Incubator Award (to M.L.P.), and a Duke Center for Interdisciplinary Decision Sciences Fellowship (to L.J.N.B.). E.V. and E.A. thank the Programma Nazionale per la Ricerca–Consiglio Nazionale delle Ricerche (CNR) Aging Program 2012–2014 for financial support, Roma Capitale–Museo Civico di Zoologia and Fondazione Bioparco for hosting the Istituto di Scienze e Tecnologie della Cognizione–CNR Unit of Cognitive Primatology and Primate Centre, and Massimiliano Bianchi and Simone Catarinacci for assistance with capuchin monkeys. K.F. thanks the Japan Society for the Promotion of Science (JSPS) for Grant-in-Aid for Scientific Research 20220004. F. Aureli thanks the Stages in the Evolution and Development of Sign Use project (Contract 012-984 NESTPathfinder) and the Integrating Cooperation Research Across Europe project (Contract 043318), both funded by the European Community’s Sixth Framework Programme (FP6/2002–2006). F. Amici was supported by Humboldt Research Fellowship for Postdoctoral Researchers (Humboldt ID 1138999). L.F.J. and M.M.D. acknowledge NSF Electrical, Communications, and Cyber Systems Grant 1028319 (to L.F.J.) and an NSF Graduate Fellowship (to M.M.D.). C.H. thanks Grant-in-Aid for JSPS Fellows (10J04395). A.T. thanks Research Fellowships of the JSPS for Young Scientists (21264). F.R. and Z.V. acknowledge Austrian Science Fund (FWF) Project P21244-B17, the European Research Council (ERC) under the European Union’s Seventh Framework Programme (FP/2007–2013)/ERC Grant Agreement 311870 (to F.R.), Vienna Science and Technology Fund Project CS11-026 (to Z.V.), and many private sponsors, including Royal Canin for financial support and the Game Park Ernstbrunn for hosting the Wolf Science Center. S.M.R. thanks the Natural Sciences and Engineering Research Council (Canada). J.K.Y. thanks the US Department of Agriculture–Wildlife Services–National Wildlife Research Center. J.F.C. thanks the James S. McDonnell Foundation and Alfred P. Sloan Foundation. E.L.M. and B.H. thank the Duke Lemur Center and acknowledge National Institutes of Health Grant 5 R03 HD070649-02 and NSF Grants DGE-1106401, NSF-BCS-27552, and NSF-BCS-25172. This is Publication 1265 of the Duke Lemur Center. Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution. Postprint

The production of structured and repetitive sounds by striking objects is a behavior found not only in humans, but also in a variety of animal species, including chimpanzees (Pan troglodytes). In this study we examined individual and social factors that may influence the frequency with which individuals engage in drumming behavior when producing long distance pant hoot vocalizations, and analyzed the temporal structure of those drumming bouts. Male chimpanzees from Budongo Forest, Uganda, drummed significantly more frequently during travel than feeding or resting and older individuals were significantly more likely to produce drumming bouts than younger ones. In contrast, we found no evidence that the presence of estrus females, high ranking males and preferred social partners in the caller's vicinty had an effect on the frequency with which an individual accompanied their pant hoot vocalization with drumming. Through acoustic analyses, we demonstrated that drumming sequences produced with pant hoots may have contained information on individual identity and that qualitatively, there was individual variation in the complexity of the temporal patterns produced. We conclude that drumming patterns may act as individually distinctive long-distance signals that, together with pant hoot vocalizations, function to coordinate the movement and spacing of dispersed individuals within a community, rather than as signals to group members in the immediate audience.