Multimodal communication and audience directedness in the greeting behaviour of semi-captive African savannah elephants.

Many species communicate by combining signals into multimodal combinations. Elephants live in multi-level societies where individuals regularly separate and reunite. Upon reunion, elephants often engage in elaborate greeting rituals, where they use vocalisations and body acts produced with different body parts and of various sensory modalities (e.g., audible, tactile). However, whether these body acts represent communicative gestures and whether elephants combine vocalisations and gestures during greeting is still unknown. Here we use separation-reunion events to explore the greeting behaviour of semi-captive elephants (Loxodonta africana). We investigate whether elephants use silent-visual, audible, and tactile gestures directing them at their audience based on their state of visual attention and how they combine these gestures with vocalisations during greeting. We show that elephants select gesture modality appropriately according to their audience's visual attention, suggesting evidence of first-order intentional communicative use. We further show that elephants integrate vocalisations and gestures into different combinations and orders. The most frequent combination consists of rumble vocalisations with ear-flapping gestures, used most often between females. By showing that a species evolutionarily distant to our own primate lineage shows sensitivity to their audience's visual attention in their gesturing and combines gestures with vocalisations, our study advances our understanding of the emergence of first-order intentionality and multimodal communication across taxa.

Selective deforestation and exposure of African wildlife to bat-borne viruses.

Proposed mechanisms of zoonotic virus spillover often posit that wildlife transmission and amplification precede human outbreaks. Between 2006 and 2012, the palm Raphia farinifera, a rich source of dietary minerals for wildlife, was nearly extirpated from Budongo Forest, Uganda. Since then, chimpanzees, black-and-white colobus, and red duiker were observed feeding on bat guano, a behavior not previously observed. Here we show that guano consumption may be a response to dietary mineral scarcity and may expose wildlife to bat-borne viruses. Videos from 2017-2019 recorded 839 instances of guano consumption by the aforementioned species. Nutritional analysis of the guano revealed high concentrations of sodium, potassium, magnesium and phosphorus. Metagenomic analyses of the guano identified 27 eukaryotic viruses, including a novel betacoronavirus. Our findings illustrate how "upstream" drivers such as socioeconomics and resource extraction can initiate elaborate chains of causation, ultimately increasing virus spillover risk.

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.

Applying collocation and APRIORI analyses to chimpanzee diets: Methods for investigating nonrandom food combinations in primate self-medication.

Identifying novel medicinal resources in chimpanzee diets has historically presented challenges, requiring extensive behavioral data collection and health monitoring, accompanied by expensive pharmacological analyses. When putative therapeutic self-medicative behaviors are observed, these events are often considered isolated occurrences, with little attention paid to other resources ingested in combination. For chimpanzees, medicinal resource combinations could play an important role in maintaining well-being by tackling different symptoms of an illness, chemically strengthening efficacy of a treatment, or providing prophylactic compounds that prevent future ailments. We call this concept the self-medicative resource combination hypothesis. However, a dearth of methodological approaches for holistically investigating primate feeding ecology has limited our ability to identify nonrandom resource combinations and explore potential synergistic relationships between medicinal resource candidates. Here we present two analytical tools that test such a hypothesis and demonstrate these approaches on feeding data from the Sonso chimpanzee community in Budongo Forest, Uganda. Using 4 months of data, we establish that both collocation and APRIORI analyses are effective exploratory tools for identifying binary combinations, and that APRIORI is effective for multi-item rule associations. We then compare outputs from both methods, finding up to 60% agreement, and propose APRIORI as more effective for studies requiring control over confidence intervals and those investigating nonrandom associations between more than two resources. These analytical tools, which can be extrapolated across the animal kingdom, can provide a cost-effective and efficient method for targeting resources for further pharmacological investigation, potentially aiding in the discovery of novel medicines.

In search of animal normativity: a framework for studying social norms in non-human animals.

Social norms - rules governing which behaviours are deemed appropriate or inappropriate within a given community - are typically taken to be uniquely human. Recently, this position has been challenged by a number of philosophers, cognitive scientists, and ethologists, who have suggested that social norms may also be found in certain non-human animal communities. Such claims have elicited considerable scepticism from norm cognition researchers, who doubt that any non-human animals possess the psychological capacities necessary for normative cognition. However, there is little agreement among these researchers about what these psychological prerequisites are. This makes empirical study of animal social norms difficult, since it is not clear what we are looking for and thus what should count as behavioural evidence for the presence (or absence) of social norms in animals. To break this impasse, we offer an approach that moves beyond contested psychological criteria for social norms. This approach is inspired by the animal culture research program, which has made a similar shift away from heavily psychological definitions of 'culture' to become organised around a cluster of more empirically tractable concepts of culture. Here, we propose an analogous set of constructs built around the core notion of a normative regularity, which we define as a socially maintained pattern of behavioural conformity within a community. We suggest methods for studying potential normative regularities in wild and captive primates. We also discuss the broader scientific and philosophical implications of this research program with respect to questions of human uniqueness, animal welfare and conservation.

Flexible grouping patterns in a western and eastern chimpanzee community.

Primate social organizations, or grouping patterns, vary significantly across species. Behavioral strategies that allow for flexibility in grouping patterns offer a means to reduce the costs of group living. Chimpanzees (Pan troglodytes) have a fission-fusion social system in which temporary subgroups ("parties") change in composition because of local socio-ecological conditions. Notably, western chimpanzees (P. t. verus) are described as showing a higher degree of bisexual bonding and association than eastern chimpanzees, and eastern female chimpanzees (P. t. schweinfurthii) are thought to be more solitary than western female chimpanzees. However, reported comparisons in sociality currently depend on a small number of study groups, particularly in western chimpanzees, and variation in methods. The inclusion of additional communities and direct comparison using the same methods are essential to assess whether reported subspecies differences in sociality hold in this behaviorally heterogeneous species. We explored whether sociality differs between two communities of chimpanzees using the same motion-triggered camera technology and definitions of social measures. We compare party size and composition (party type, sex ratio) between the western Gahtoy community in the Nimba Mountains (Guinea) and the eastern Waibira community in the Budongo Forest (Uganda). Once potential competition for resources such as food and mating opportunities were controlled for, subspecies did not substantially influence the number of individuals in a party. We found a higher sex-ratio, indicating more males in a party, in Waibira; this pattern was driven by a greater likelihood in Gahtoy to be in all-female parties. This finding is the opposite of what was expected for eastern chimpanzees, where female-only parties are predicted to be more common. Our results highlight the flexibility in chimpanzee sociality, and caution against subspecies level generalizations.

GesturalOrigins: A bottom-up framework for establishing systematic gesture data across ape species.

Current methodologies present significant hurdles to understanding patterns in the gestural communication of individuals, populations, and species. To address this issue, we present a bottom-up data collection framework for the study of gesture: GesturalOrigins. By "bottom-up", we mean that we minimise a priori structural choices, allowing researchers to define larger concepts (such as 'gesture types', 'response latencies', or 'gesture sequences') flexibly once coding is complete. Data can easily be re-organised to provide replication of, and comparison with, a wide range of datasets in published and planned analyses. We present packages, templates, and instructions for the complete data collection and coding process. We illustrate the flexibility that our methodological tool offers with worked examples of (great ape) gestural communication, demonstrating differences in the duration of action phases across distinct gesture action types and showing how species variation in the latency to respond to gestural requests may be revealed or masked by methodological choices. While GesturalOrigins is built from an ape-centred perspective, the basic framework can be adapted across a range of species and potentially to other communication systems. By making our gesture coding methods transparent and open access, we hope to enable a more direct comparison of findings across research groups, improve collaborations, and advance the field to tackle some of the long-standing questions in comparative gesture research.

News and Perspectives: Words matter in primatology.

Postings on social media on Twitter (now X), BioAnthropology News (Facebook), and other venues, as well as recent publications in prominent journals, show that primatologists, ecologists, and other researchers are questioning the terms "Old World" and "New World" due to their colonial implications and history. The terms are offensive if they result in erasing Indigenous voices and history, ignoring the fact that Indigenous peoples were in the Americas long before European colonization. Language use is not without context, but alternative terminology is not always obvious and available. In this perspective, we share opinions expressed by an international group of primatologists who considered questions about the use of these terms, whether primatologists should adjust language use, and how to move forward. The diversity of opinions provides insight into how conventional terms used in primatological research and conservation may impact our effectiveness in these domains.

Habitual ground nesting in the Bugoma Forest chimpanzees (Pan troglodytes schweinfurthii), Uganda.

We report the presence of habitual ground nesting in a newly studied East African chimpanzee (Pan troglodytes schweinfurthii) population in the Bugoma Central Forest Reserve, Uganda. Across a 2-year period, we encountered 891 night nests, 189 of which were classified as ground nests, a rate of ~21%. We find no preliminary evidence of socio-ecological factors that would promote its use and highlight local factors, such as high incidence of forest disturbance due to poaching and logging, which appear to make its use disadvantageous. While further study is required to establish whether this behavior meets the strict criteria for nonhuman animal culture, we support the argument that the wider use of population and group-specific behavioral repertoires in flagship species, such as chimpanzees, offers a tool to promote the urgent conservation action needed to protect threatened ecosystems, including the Bugoma forest.

Reindeer and the quest for Scottish enlichenment.

In the hall of animal oddities, the reindeer (Rangifer tarandus) is the only mammal with a color-shifting tapetum lucidum and the only ruminant with a lichen-dominated diet. These puzzling traits coexist with yet another enigma--ocular media that transmit up to 60% of ultraviolet (UV) light, enough to excite the cones responsible for color vision. It is unclear why any day-active circum-Arctic mammal would benefit from UV visual sensitivity, but it could improve detection of UV-absorbing lichens against a background of UV-reflecting snows, especially during the extended twilight hours of winter. To explore this idea and advance our understanding of reindeer visual ecology, we recorded the reflectance spectra of several ground-growing (terricolous), shrubby (fruticose) lichens in the diets of reindeer living in Cairngorms National Park, Scotland.

Decay rates of arboreal and terrestrial nests of Eastern chimpanzees (Pan troglodytes schweinfurthii) in the Bugoma Central Forest Reserve, Uganda: Implications for population size estimates.

Chimpanzees were once thought to sleep primarily in the trees, but recent studies indicate that some populations also construct terrestrial night nests. This behavior has relevance not only to understanding the behavioral diversity of Pan troglodytes, but also to the conservation of the species, given that nest encounter rates are often used to estimate great ape population densities. A proper estimate of decay rates for ground nests is necessary for converting the encounter rate of nests to the density of weaned chimpanzees. Here we present the results of the first systematic comparative study between the decay rates of arboreal and terrestrial chimpanzee nests, from the Bugoma Central Forest Reserve in western Uganda. We followed the decay of 56 ground and 51 tree nests in eight nest groups between April 2020 and October 2021. For 15 of the ground and 19 of the tree nests, we collected detailed information on the condition of the nests every two weeks; we checked the remaining 73 nests only twice. On average, ground nests lasted 238 days versus 276 days for tree nests (p = 0.05). Of the 107 total nests surveyed, 51% of tree and 64% of ground nests had disappeared after six months. Based on our results, we propose a modification of the formula used to convert nest density into chimpanzee density. Our results highlight the importance of taking into account potential differences in decay rates between ground versus tree nests, which will likely influence our understanding of the distribution of ground nesting behavior in chimpanzee across tropical Africa, as well as our estimations of the densities of ground nesting populations.

Object use in communication of semi-wild chimpanzees.

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

DeepWild: Application of the pose estimation tool DeepLabCut for behaviour tracking in wild chimpanzees and bonobos.

Studying animal behaviour allows us to understand how different species and individuals navigate their physical and social worlds. Video coding of behaviour is considered a gold standard: allowing researchers to extract rich nuanced behavioural datasets, validate their reliability, and for research to be replicated. However, in practice, videos are only useful if data can be efficiently extracted. Manually locating relevant footage in 10,000 s of hours is extremely time-consuming, as is the manual coding of animal behaviour, which requires extensive training to achieve reliability. Machine learning approaches are used to automate the recognition of patterns within data, considerably reducing the time taken to extract data and improving reliability. However, tracking visual information to recognise nuanced behaviour is a challenging problem and, to date, the tracking and pose-estimation tools used to detect behaviour are typically applied where the visual environment is highly controlled. Animal behaviour researchers are interested in applying these tools to the study of wild animals, but it is not clear to what extent doing so is currently possible, or which tools are most suited to particular problems. To address this gap in knowledge, we describe the new tools available in this rapidly evolving landscape, suggest guidance for tool selection, provide a worked demonstration of the use of machine learning to track movement in video data of wild apes, and make our base models available for use. We use a pose-estimation tool, DeepLabCut, to demonstrate successful training of two pilot models of an extremely challenging pose estimate and tracking problem: multi-animal wild forest-living chimpanzees and bonobos across behavioural contexts from hand-held video footage. With DeepWild we show that, without requiring specific expertise in machine learning, pose estimation and movement tracking of free-living wild primates in visually complex environments is an attainable goal for behavioural researchers.

L'étude du comportement animal nous permet de comprendre comment différentes espèces et différents individus naviguent dans leur monde physique et social. Le codage vidéo du comportement est considéré comme une référence: il permet aux chercheurs d'extraire des ensembles de données comportementales riches et nuancées, de valider leur fiabilité et de reproduire les recherches. Toutefois, dans la pratique, les vidéos ne sont utiles que si les données peuvent être extraites efficacement. La localisation manuelle de séquences pertinentes parmi des dizaines de milliers d'heures prend énormément de temps, tout comme le codage manuel du comportement animal, qui nécessite une formation approfondie pour être fiable. Les approches d'apprentissage automatique sont utilisées pour automatiser la reconnaissance de modèles dans les données, ce qui réduit considérablement le temps nécessaire à l'extraction des données et améliore la fiabilité. Toutefois, le suivi des informations visuelles pour reconnaître un comportement nuancé est un problème difficile et, à ce jour, les outils de suivi et d'estimation de la pose utilisés pour détecter le comportement sont généralement appliqués lorsque l'environnement visuel est hautement contrôlé. Les chercheurs en comportement animal sont intéressés par l'application de ces outils à l'étude des animaux sauvages, mais il n'est pas clair dans quelle mesure cela est actuellement possible, ni quels outils sont les mieux adaptés à des problèmes particuliers. Pour combler ce manque de connaissances, nous décrivons les nouveaux outils disponibles dans ce paysage en évolution rapide, proposons des conseils pour la sélection des outils, fournissons une démonstration pratique de l'utilisation de l'apprentissage automatique pour suivre les mouvements dans les données vidéo des grands singes sauvages et mettons nos modèles de base à disposition pour utilisation. Nous utilisons un outil d'estimation de la pose, DeepLabCut, pour démontrer l'apprentissage réussi de deux modèles pilotes d'un problème extrêmement difficile d'estimation et de suivi de la pose: les chimpanzés et les bonobos sauvages vivant dans la forêt et représentant plusieurs animaux dans différents contextes comportementaux à partir de séquences vidéo tenues à la main. Avec DeepWild, nous montrons que, sans nécessiter d'expertise spécifique en apprentissage automatique, l'estimation de la pose et le suivi des mouvements de primates sauvages vivant en liberté dans des environnements visuellement complexes est un objectif réalisable pour les chercheurs en comportement.

Shared community effects and the non-genetic maternal environment shape cortisol levels in wild chimpanzees.

Mechanisms of inheritance remain poorly defined for many fitness-mediating traits, especially in long-lived animals with protracted development. Using 6,123 urinary samples from 170 wild chimpanzees, we examined the contributions of genetics, non-genetic maternal effects, and shared community effects on variation in cortisol levels, an established predictor of survival in long-lived primates. Despite evidence for consistent individual variation in cortisol levels across years, between-group effects were more influential and made an overwhelming contribution to variation in this trait. Focusing on within-group variation, non-genetic maternal effects accounted for 8% of the individual differences in average cortisol levels, significantly more than that attributable to genetic factors, which was indistinguishable from zero. These maternal effects are consistent with a primary role of a shared environment in shaping physiology. For chimpanzees, and perhaps other species with long life histories, community and maternal effects appear more relevant than genetic inheritance in shaping key physiological traits.

Friends in high places: Interspecific grooming between chimpanzees and primate prey species in Budongo Forest.

While cases of interspecies grooming have been reported in primates, no comprehensive cross-site review has been published about this behavior in great apes. Only a few recorded observations of interspecies grooming events between chimpanzees and other primate species have been reported in the wild, all of which have thus far been in Uganda. Here, we review all interspecies grooming events recorded for the Sonso community chimpanzees in Budongo Forest Reserve, Uganda, adding five new observations to the single, previously reported event from this community. A new case of interspecies play involving three juvenile male chimpanzees and a red-tailed monkey is also detailed. All events took place between 1993 and 2021. In all of the six interspecific grooming events from Budongo, the 'groomer' was a female chimpanzee between the ages of 4-6 years, and the 'recipient' was a member of the genus Cercopithecus. In five of these events, chimpanzee groomers played with the tail of their interspecific grooming partners, and except for one case, initiated the interaction. In three cases, chimpanzee groomers smelled their fingers after touching distinct parts of the receiver's body. While a single function of chimpanzee interspecies grooming remains difficult to determine from these results, our review outlines and assesses some hypotheses for the general function of this behavior, as well as some of the costs and benefits for both the chimpanzee groomers and their sympatric interspecific receivers. As allogrooming is a universal behavior in chimpanzees, investigating the ultimate and proximate drivers of chimpanzee interspecies grooming may reveal further functions of allogrooming in our closest living relatives, and help us to better understand how chimpanzees distinguish between affiliative and agonistic species and contexts.

Towards a great ape dictionary: Inexperienced humans understand common nonhuman ape gestures.

In the comparative study of human and nonhuman communication, ape gesturing provided the first demonstrations of flexible, intentional communication outside human language. Rich repertoires of these gestures have been described in all ape species, bar one: us. Given that the majority of great ape gestural signals are shared, and their form appears biologically inherited, this creates a conundrum: Where did the ape gestures go in human communication? Here, we test human recognition and understanding of 10 of the most frequently used ape gestures. We crowdsourced data from 5,656 participants through an online game, which required them to select the meaning of chimpanzee and bonobo gestures in 20 videos. We show that humans may retain an understanding of ape gestural communication (either directly inherited or part of more general cognition), across gesture types and gesture meanings, with information on communicative context providing only a marginal improvement in success. By assessing comprehension, rather than production, we accessed part of the great ape gestural repertoire for the first time in adult humans. Cognitive access to an ancestral system of gesture appears to have been retained after our divergence from other apes, drawing deep evolutionary continuity between their communication and our own.

Dialects in leaf-clipping and other leaf-modifying gestures between neighbouring communities of East African chimpanzees.

Dialects are a cultural property of animal communication previously described in the signals of several animal species. While dialects have predominantly been described in vocal signals, chimpanzee leaf-clipping and other 'leaf-modifying' gestures, used across chimpanzee and bonobo communities, have been suggested as a candidate for cultural variation in gestural communication. Here we combine direct observation with archaeological techniques to compare the form and use of leaf-modifying gestures in two neighbouring communities of East African chimpanzees. We found that while both communities used multiple forms, primarily within sexual solicitation, they showed a strong preference for a single, different gesture form. The observed variation in form preference between these neighbouring communities within the same context suggests that these differences are, at least in part, socially derived. Our results highlight an unexplored source of variation and flexibility in gestural communication, opening the door for future research to explore socially derived dialects in non-vocal communication.

Recognition of visual kinship signals in chimpanzees (Pan troglodytes) by humans (Homo sapiens).

Associating with kin provides individual benefits but requires that these relationships be detectable. In humans, facial phenotype matching might help assess paternity; however, evidence for it is mixed. In chimpanzees, concealing visual cues of paternity may be beneficial due to their promiscuous mating system and the considerable risk of infanticide by males. On the other hand, detecting kin can also aid chimpanzees in avoiding inbreeding and in forming alliances that improve kin-mediated fitness. Although previous studies assessing relatedness based on facial resemblance in chimpanzees exist, they used images of captive populations in whom selection pressures and reproductive opportunities are controlled and only assessed maternity or paternity of adult offspring. In natural populations, the chances of infanticide are highest during early infancy, suggesting that young infants would benefit most from paternity concealment, whereas adults and subadults would benefit from the detection of all types of kin, including half-siblings. In our experiment, we conducted an online study with human participants, in which they had to assess the relatedness of chimpanzees based on facial similarity. To address previous methodological constraints, we used chimpanzee images across all ages, as well as maternal and paternal half-siblings. We found that kin status was detected above chance across all relatedness categories, with easier kin detection of father-offspring pairs, females, and older chimpanzees. Together, these findings support the existence of paternity confusion in infant chimpanzees and provide a possible mechanism for incest avoidance and kin-based social alliances in older individuals. (PsycInfo Database Record (c) 2022 APA, all rights reserved).