How can a multimodal approach to primate communication help us understand the evolution of communication?

Scientists studying the communication of non-human animals are often aiming to better understand the evolution of human communication, including human language. Some scientists take a phylogenetic perspective, where the goal is to trace the evolutionary history of communicative traits, while others take a functional perspective, where the goal is to understand the selection pressures underpinning specific traits. Both perspectives are necessary to fully understand the evolution of communication, but it is important to understand how the two perspectives differ and what they can and cannot tell us. Here, we suggest that integrating phylogenetic and functional questions can be fruitful in better understanding the evolution of communication. We also suggest that adopting a multimodal approach to communication might help to integrate phylogenetic and functional questions, and provide an interesting avenue for research into language evolution

The language void: the need for multimodality in primate communication research

Theories of language evolution often draw heavily on comparative evidence of the communicative abilities of extant nonhuman primates (primates). Many theories have argued exclusively for a unimodal origin of language, usually gestural or vocal. Theories are often strengthened by research on primates that indicates the absence of certain linguistic precursors in the opposing communicative modality. However, a systematic review of the primate communication literature reveals that vocal, gestural and facial signals have attracted differing theoretical and methodological approaches, rendering cross-modal comparisons problematic. The validity of the theories based on such comparisons can therefore be questioned. We propose that these a priori biases, inherent in unimodal research, highlight the need for integrated multimodal research. By examining communicative signals in concert we can both avoid methodological discontinuities as well as better understand the phylogenetic precursors to human language as part of a multimodal system

Chimpanzees Extract Social Information from Agonistic Screams

Chimpanzee (Pan troglodytes) agonistic screams are graded vocal signals that are produced in a context-specific manner. Screams given by aggressors and victims can be discriminated based on their acoustic structure but the mechanisms of listener comprehension of these calls are currently unknown. In this study, we show that chimpanzees extract social information from these vocal signals that, combined with their more general social knowledge, enables them to understand the nature of out-of-sight social interactions. In playback experiments, we broadcast congruent and incongruent sequences of agonistic calls and monitored the response of bystanders. Congruent sequences were in accordance with existing social dominance relations; incongruent ones violated them. Subjects looked significantly longer at incongruent sequences, despite them being acoustically less salient (fewer call types from fewer individuals) than congruent ones. We concluded that chimpanzees categorised an apparently simple acoustic signal into victim and aggressor screams and used pragmatics to form inferences about third-party interactions they could not see

Reply to Fischer et al

We welcome the correspondence from Fischer and colleagues regarding our recent paper on vocal learning in chimpanzee food grunts [1]. Fischer et al. make two challenges to our paper's conclusions, which we address here

Exploration of potential triggers for self-directed behaviours and regurgitation and reingestion in zoo-housed chimpanzees

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.Peer reviewe

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

Data collection with the New Caledonian crows was funded by an International Seedcorn Award from the University of York to M.L.L. This study was supported by a Rutherford Discovery Fellowship (A.H.T.). Our data are deposited at: http://dx.doi.org/10.5061/dryad.dq04j [48].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 behavior 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 behavior to explicitly seek this information.Publisher PDFPeer reviewe

Pseudoreplication in Primate Communication Research : 10 Years On

Pseudoreplication is the statistical error of collecting numerous datapoints from a single unit (such as an individual), which are not independent, and applying statistical methods that assume independence of data. Importantly, pseudoreplication increases the chances of Type 1 errors (i.e., false positives), bringing findings and conclusions based on pseudoreplicated analyses into question. Ten years ago, Waller et al. (2013) published a paper highlighting the prevalence of statistical pseudoreplication throughout the nonhuman primate communication literature. In this current study, we examined the literature published since the original publication (between 2009 and 2020; 348 papers) to assess whether pseudoreplication is still as widespread as it was, if it has become more problematic, or if the field is beginning to overcome this issue. We find that there has been a significant decrease in pseudoreplication over the past ten years (38.6% then, compared with 23.0% now). This reduction in pseudoreplication appears to be associated with an increase in the use of multilevel models throughout primatology (which allow for nonindependent data to be nested appropriately). Pseudoreplication was historically more prevalent in research using observational (vs. experimental) methods and those working with wild (vs. captive) primates. However, these biases do not seem to exist in more recent literature with a more comparable likelihood of pseudoreplication seen across the field regardless of methods. Although these current findings relate specifically to primate communication research, we think they will translate broadly across nonhuman communication research, and throughout biology. We continue to emphasise the need to monitor these issues, as although now seen at much lower rates, pseudoreplication is still present and therefore potentially impacting the accuracy of findings

Referential gestures are not ubiquitous in wild chimpanzees : alternative functions for exaggerated loud scratch gestures

Royal Zoological Society of Scotland for providing core funding for Budongo Conservation Field Station. This work was supported by the ERC grant awarded to KS (ERC_CoG 2016_724608).A fundamental aspect of human communication is our ability to refer to external objects and events through both words and gestures (such as pointing), yet the evolutionary origins of such signals remain obscure. Apes, living in their natural environments, rarely or never point, but it has been claimed that male chimpanzees, Pan troglodytes schweinfurthii, from the Ngogo community, Uganda, habitually use exaggerated loud scratches (ELSs) to refer to specific body locations where they wish to be groomed (Pika & Mitani, 2006, Current Biology, 16(6), 191–192). This study suggested continuity between referential abilities in humans and our closest living relatives, making it an important finding to replicate in other populations. Hence here, we compared whether ELSs are used in a referential manner across four wild communities of eastern chimpanzees (Ngogo, Kanyawara, Sonso and Waibira). Our data show that scratchers were significantly more likely to receive grooming in the scratched location at Ngogo compared to the other three sites. At the latter sites this response occurred at low rates and signallers did not seem to pursue this goal. This suggests that ELSs do not function referentially at these sites, and the published findings from Ngogo were not replicated. Further exploration into alternative functions of ELSs in the Kanyawara community revealed that, in this community, this signal functions to initiate grooming bouts and to reengage partners during grooming pauses. Individuals who produced the signal to initiate grooming were likely to offer grooming. In contrast, during grooming bouts, groomers produced ELSs to request reciprocation of grooming from their partner. Our study demonstrates that chimpanzees do not ubiquitously use the ELS in a referential manner, but that they can use this gesture in a highly flexible fashion, with signal function depending on the intricate details of the social contexts in which they are produced.Publisher PDFPeer reviewe

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

Many morphs : parsing gesture signals from the noise

AM was funded by a Leverhulme Early Career Fellowship. CH, GB, KEG, CG, and AS were supported by funding from the European Research Council under Gestural Origins Grant No: 802719. KS and CW were supported by funding from the European Research Council under Grant No: ERC_CoG 2016_724608. We thank all the staff of the Budongo Conservation Field Station, its founder Vernon Reynolds, and the Royal Zoological Society of Scotland who provide core funding.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.Peer reviewe