Acquisition of predator knowledge from alarm calls via one-trial social learning in monkeys

This work was funded by the Swiss National Science Foundation Agreement project grants 31003A_166458 (KZ) and 310030_185324 (KZ), and the Swiss National Centre of Competence in Research (NCCR) Evolving Language, Swiss National Science Foundation Agreement #51NF40_180888 (KZ).How do animals learn to classify the world and what is the role of social learning during this process? Here, we show that young sooty mangabeys, Cercocebus atys, of Taï Forest, Côte d’Ivoire, learn to rapidly classify an unfamiliar predator by attending to others’ alarm calls and that such knowledge is retained over long periods. We experimentally exposed subjects to chimeric predator models with both snake- and leopard-like features, combined with playbacks of conspecific snake (N=12) or leopard alarms (N=13). Adults classified the chimeras as non-threatening but for juveniles, we found that one single alarm call exposure was sufficient to allocate the chimera to the snake or leopard category, suggesting plausibility judgments in experienced adults. We then retested N=10 juveniles with the same models more than a year after their first experience and found that they continued to show their original response, indicating long-term retention of socially learned predator categorisation.Publisher PDFPeer reviewe

The development of communication in alarm contexts in wild chimpanzees

Funding: The Royal Zoological Society of Scotland provided core funding to the Budongo Conservation Field Station. This research was financially supported by FP7-IDEAS-ERC (324115), the Agence Nationale de la Recherche (ANR-10-LABX-0087 IEC and ANR-10-IDEX-0001-02 PSL) and by the Swiss National Science Foundation (31003A_166458).Animals have evolved a range of communicative behaviours in the presence of danger. Although the mechanisms and functions of some of these behaviours have been relatively well researched, comparatively little is known about their ontogeny, including how animals learn to inform social partners about impending danger. In adult chimpanzees, behaviours in response to dangers involve several channels, particularly alarm calls and simultaneous gaze alternations with nearby recipients. Gaze alternations may allow inexperienced individuals to learn from more experienced ones by assessing their reactions to unfamiliar objects or events, but they may also provide the basis for more advanced social referencing. Here, we were interested in the development of these two common behaviours, alarm calling and gaze alternations, in wild chimpanzees (Pan troglodytes schweinfurthii) confronted with a threat. Using a cross-sectional design, we investigated those in 8 infant and 8 juveniles by experimentally exposing them to an unfamiliar but potentially dangerous object, a large, remotely controlled, moving spider model. For alarm calling, we found a positive relation with age, starting at around 28 months, although alarm calls were not consistently emitted until after 80 months. For gaze alternations, we found no age effect, with some of the youngest infants already showing the behaviour. Although its function remains unclear in infant and juvenile chimpanzees, gaze alternations emerge early in chimpanzee development. Alarm calling may require more advanced developmental stages, such as greater perceptual abilities, categorical capacities or more sophisticated social cognition, i.e. an understanding that danger is a collective experience that requires communication.Publisher PDFPeer reviewe

Chimpanzee quiet hoo variants differ according to context

The study was funded by the Leverhulme Trust, the British Academy, the Leakey Foundation, the European Union’s Horizon 2020 research and innovation programme under grant agreement No. 679787, the Max Planck Society and the Swiss National Science Foundation (grants P300PA_164678, CR13I1_162720 and 31003A_166458). We thank the Royal Zoological Society of Scotland for providing core support for the Budongo Conservation Field Station.In comparative studies of evolution of communication, the function and use of animal quiet calls have typically been understudied, despite that these signals are presumably under selection like other vocalisations, such as alarm calls. Here, we examine vocal diversification of chimpanzee quiet ‘hoos’ produced in three contexts - travel, rest and alert - and potential pressures promoting diversification. Previous playback and observational studies have suggested that the overarching function of chimpanzee hoos is to stay in contact with others, particularly bond partners. We conducted an acoustic analysis of hoos using audio-recordings from wild chimpanzees (Pan troglodytes schweinfurthii) of Budongo Forest, Uganda. We identified three acoustically distinguishable, context-specific hoo variants. Each call variant requires specific responses from receivers to avoid breaking up the social unit. We propose that callers may achieve coordination by using acoustically distinguishable calls, advertising their own behavioural intentions. We conclude that natural selection has acted towards acoustically diversifying an inconspicuous, quiet vocalisation, the chimpanzee hoo. This evolutionary process may have been favoured by the fact that signallers and recipients share the same goal, to maintain social cohesion, particularly amongst those who regularly cooperate, suggesting that vocal diversification has been favoured by the demands of cooperative activities.Publisher PDFPeer reviewe

Social support reduces stress hormone levels in wild chimpanzees across stressful events and everyday affiliations

We acknowledge Royal Zoological Society of Scotland for providing core funding to BCFS and Leakey Foundation (R.M.W., C.C., T.D., K.Z.), British Academy (C.C.), Leverhulme Trust (K.Z.) and Max Planck Society (R.M.W., C.C. and T.D.) for funding the research.Stress is a major cause of poor health and mortality in humans and other social mammals. Close social bonds buffer stress, however much of the underlying physiological mechanism remains unknown. Here, we test two key hypotheses: bond partner effects occur only during stress (social buffering) or generally throughout daily life (main effects). We assess urinary glucocorticoids (uGC) in wild chimpanzees, with or without their bond partners, after a natural stressor, resting or everyday affiliation. Chimpanzees in the presence of, or interacting with, bond partners rather than others have lowered uGC levels across all three contexts. These results support the main effects hypothesis and indicate that hypothalamic-pituitary-adrenocortical (HPA) axis regulation is mediated by daily engagement with bond partners both within and out of stressful contexts. Regular social support with bond partners could lead to better health through daily ‘micro-management’ of the HPA axis, a finding with potential medical implications for humans.Publisher PDFPeer reviewe

Urinary Cortisol, Aggression, Dominance and Competition in Wild, West African Male Chimpanzees

High dominance status is associated with fitness benefits in many social mammals. Yet, attaining and maintaining a high social status often comes with elevated energetic costs. Dominance rank-related exposure to energetic and psychosocial stressors is predicted to vary depending on the type of breeding system, the means a high rank is acquired and maintained, and the stability of the dominance hierarchy. Using behavioral data and urinary cortisol levels, we investigated whether a high dominance rank is associated with elevated energetic costs in Taï male chimpanzees and whether the relationship between male dominance rank and cortisol levels varies between stable and unstable dominance periods. Additionally, we investigated potential sources of energetic and psychosocial stress linked to competition over dominance status and mating opportunities. We found that higher-ranking males gave more aggressions than lower-ranking males in stable and unstable dominance periods, but that dominance rank and urinary cortisol levels were not associated in either period. Urinary cortisol levels were higher in all males in unstable compared to stable dominance periods, whereas aggression rates showed the reversed pattern, with higher rates in stable periods. Our results indicate that dominance maintenance is not associated with elevated physiological stress for dominant Taï male chimpanzees, and that social instability exposed all males to psychosocial stress, despite lower rates of aggressive interactions. Overall, these findings suggest that male chimpanzees adjust competitive behavior to context dependent conditions, possibly by means of predictability of outcomes of social interactions, and use conflict management strategies, such as avoidance of aggression potentially diminishing the risk of escalation

First observation of a chimpanzee with albinism in the wild : social interactions and subsequent infanticide

Maël Leroux was funded via the Swiss National Science Foundation grant awarded to Simon W. Townsend (31003A_153065). Pawel Fedurek was funded via the European Research Council project grant awarded to Catherine Crockford (grant agreement number: 679787).Albinism- the congenital absence of pigmentation- is a very rare phenomenon in animals due to the significant costs to fitness of this condition. Both humans and non-human individuals with albinism face a number of challenges, such as reduced vision, increased exposure to ultraviolet radiation, or compromised crypticity resulting in an elevated vulnerability to predation. However, while observations of social interactions involving individuals with albinism have been observed in wild non-primate animals, such interactions have not been described in detail in non-human primates (hereafter, primates). Here, we report, to our knowledge, the first sighting of an infant with albinism in wild chimpanzees (Pan troglodytes schweinfurthii), including social interactions between the infant, its mother, and group members. We also describe the subsequent killing of the infant by conspecifics as well as their behavior towards the corpse following the infanticide. Finally, we discuss our observations in relation to our understanding of chimpanzee behavior or attitudes towards individuals with very conspicuous appearances.Publisher PDFPeer reviewe

Population-specific call order in chimpanzee greeting vocal sequences

This study was funded by the Max Planck Society and the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation program awarded to C.C. (grant agreement no. 679787) and ERC (Prilang GA283871) and by Leverhulme Trust Research Leadership Award. Core funding for the Taï Chimpanzee Project has been provided by the Max Planck Society since 1997 and for Budongo Conservation Field station by the Royal Zoological Society of Scotland.Primates rarely learn new vocalisations, but they can learn to use their vocalizations in different contexts. Such ‘vocal usage learning’, particularly in vocal sequences, is a hallmark of human language, but remains understudied in non-human primates. We assess usage learning in four wild chimpanzee communities of Taï and Budongo Forests by investigating population differences in call ordering of a greeting vocal sequence. Whilst in all groups, these sequences consisted of pant-hoots (long-distance contact call) and pant-grunts (short-distance submissive call), the order of the two calls differed across populations. Taï chimpanzees consistently commenced greetings with pant-hoots whereas Budongo chimpanzees started with pant-grunts. We discuss different hypotheses to explain this pattern and conclude that higher intra-group aggression in Budongo may have led to a local pattern of individuals signalling submission first. This highlights how within-species variation in social dynamics may lead to flexibility in call order production, possibly acquired via usage learning.Publisher PDFPeer reviewe

Consistency of Social Interactions in Sooty Mangabeys and Chimpanzees

Predictability of social interactions can be an important measure for the social complexity of an animal group. Predictability is partially dependent on how consistent interaction patterns are over time: does the behavior on 1 day explain the behavior on another? We developed a consistency measure that serves two functions: detecting which interaction types in a dataset are so inconsistent that including them in further analyses risks introducing unexplained error; and comparatively quantifying differences in consistency within and between animal groups. We applied the consistency measure to simulated data and field data for one group of sooty mangabeys (Cercocebus atys atys) and to groups of Western chimpanzees (Pan troglodytes verus) in the Taï National Park, Côte d'Ivoire, to test its properties and compare consistency across groups. The consistency measures successfully identified interaction types whose low internal consistency would likely create analytical problems. Species-level differences in consistency were less pronounced than differences within groups: in all groups, aggression and dominance interactions were the most consistent, followed by grooming; spatial proximity at different levels was much less consistent than directed interactions. Our consistency measure can facilitate decision making of researchers wondering whether to include interaction types in their analyses or social networks and allows us to compare interaction types within and between species regarding their predictability.Peer Reviewe

The effect of warning signs on the presence of snare traps in a Ugandan rainforest

BCFS receives core funding from the Royal Zoological Society of Scotland. The Budongo Snare Removal Project is funded by Oakland Zoo. PF was funded by the European Research Council project grant to CC (grant agreement number: 679787). DPD was funded by the National Science Centre (grant number: 2020/04/X/NZ8/00865).Since chimpanzee (Pan troglodytes) conservation often involves local human populations, conservation strategies must consider psychological factors that impact their behavior. In Budongo Forest, Uganda, for example, local communities commonly engage in snare trap (hereafter: snare) setting for wild meat. This illegal activity posits a substantial threat to wild chimpanzees, causing permanent wounds or death for those who are snared. Despite various schemes previously implemented to address snare setting?an activity that is fueled by poverty, the problem and its detrimental impact on chimpanzees persists. Here, we experimentally tested a novel intervention, a systematic display of specially designed warning signs aimed at local poachers. We monitored the presence of snares before and after introducing these signs over a total period of two years and compared it with that of a similar sized control area with no intervention. Results show that snares were less likely to be present during the ?sign? period than during the ?non-sign? period in the experimental but not in the control area. We discuss the potential of this cost-effective intervention for limiting illegal activities that pose a severe threat to chimpanzees and other species inhabiting tropical forests.Publisher PDFPeer reviewe

Sourcing high tissue quality brains from deceased wild primates with known socio-ecology

1. The selection pressures that drove dramatic encephalisation processes through the mammal lineage remain elusive, as does knowledge of brain structure reorganisation through this process. In particular, considerable structural brain changes are present across the primate lineage, culminating in the complex human brain that allows for unique behaviours such as language and sophisticated tool use. To understand this evolution, a diverse sample set of humans' closest relatives with varying socio-ecologies is needed. However, current brain banks predominantly curate brains from primates that died in zoological gardens. We try to address this gap by establishing a field pipeline mitigating the challenges associated with brain extractions of wild primates in their natural habitat. 2. The success of our approach is demonstrated by our ability to acquire a novel brain sample of deceased primates with highly variable socio-ecological exposure and a particular focus on wild chimpanzees. Methods in acquiring brain tissue from wild settings are comprehensively explained, highlighting the feasibility of conducting brain extraction procedures under strict biosafety measures by trained veterinarians in field sites. 3. Brains are assessed at a fine-structural level via high-resolution MRI and state-of-the-art histology. Analyses confirm that excellent tissue quality of primate brains sourced in the field can be achieved with a comparable tissue quality of brains acquired from zoo-living primates. 4. Our field methods are noninvasive, here defined as not harming living animals, and may be applied to other mammal systems than primates. In sum, the field protocol and methodological pipeline validated here pose a major advance for assessing the influence of socio-ecology on medium to large mammal brains, at both macro- and microstructural levels as well as aiding with the functional annotation of brain regions and neuronal pathways via specific behaviour assessments