Liran Samuni

Oxytocin reactivity during intergroup conflict in wild chimpanzees

Significance Warfare is one of the most pervasive problems among human societies, and understanding mechanisms involved in in-group cooperation and favoritism is of paramount importance. Wild chimpanzees share key features of humans’ intergroup conflict, in terms of in-group coordination, coalitionary support, and out-group hostility. The hormone oxytocin may regulate humans’ intergroup conflict, although tests in natural settings are lacking. We found strong evidence that, like in humans, oxytocin is involved in chimpanzee intergroup conflict. Both intergroup conflict anticipation and participation involved high urinary oxytocin levels, irrespective of intragroup affiliations or potential threat by rivals. These results are indicative of similar physiological processes involved in intergroup violence and intragroup support in both species, likely supporting behavior that is adaptive during intergroup conflicts. Intergroup conflict is evident throughout the history of our species, ubiquitous across human societies, and considered crucial for the evolution of humans’ large-scale cooperative nature. Like humans, chimpanzee societies exhibit intragroup coordination and coalitionary support during violent intergroup conflicts. In both species, cooperation among group members is essential for individuals to gain access to benefits from engaging in intergroup conflict. Studies suggest that a contributive mechanism regulating in-group cooperation during intergroup conflicts in humans involves the neuropeptide hormone oxytocin, known to influence trust, coordination, and social cognition, although evidence from natural settings is lacking. Here, applying a noninvasive method, we investigate oxytocinergic system involvement during natural intergroup conflicts in wild chimpanzees. We found that chimpanzees of both sexes had significantly higher urinary oxytocin levels immediately before and during intergroup conflict compared with controls. Also, elevated hormone levels were linked with greater cohesion during intergroup conflicts, rather than with the level of potential threat posed by rival groups, intragroup affiliative social interactions, or coordinated behavior alone. Thus, the oxytocinergic system, potentially engendering cohesion and cooperation when facing an out-group threat, may not be uniquely human but rather a mechanism with evolutionary roots shared by our last common ancestor with chimpanzees, likely expediting fitness gains during intergroup conflict.

Socially learned habituation to human observers in wild chimpanzees

Abstract Habituation to human observers is an essential tool in animal behaviour research. Habituation occurs when repeated and inconsequential exposure to a human observer gradually reduces an animal’s natural aversive response. Despite the importance of habituation, little is known about the psychological mechanisms facilitating it in wild animals. Although animal learning theory offers some account, the patterns are more complex in natural than in laboratory settings, especially in large social groups in which individual experiences vary and individuals influence each other. Here, we investigate the role of social learning during the habituation process of a wild chimpanzee group, the Waibira community of Budongo Forest, Uganda. Through post hoc hypothesis testing, we found that the immigration of two well-habituated, young females from the neighbouring Sonso community had a significant effect on the behaviour of non-habituated Waibira individuals towards human observers, suggesting that habituation is partially acquired via social learning.

Variation in hunting behaviour in neighbouring chimpanzee communities in the Budongo forest, Uganda

Hunting and sharing of meat is seen across all chimpanzee sites, with variation in prey preferences, hunting techniques, frequencies, and success rates. Here, we compared hunting and meat-eating behaviour in two adjacent chimpanzee communities (Pan troglodytes schweinfurthii) of Budongo Forest, Uganda: the Waibira and Sonso communities. We observed consistent between-group differences in prey-species preferences and in post-hunting behaviour. Sonso chimpanzees show a strong prey preference for Guereza colobus monkeys (Colobus guereza occidentalis; 74.9% hunts), and hunt regularly (1–2 times a month) but with large year-to-year and month-to-month variation. Waibira chimpanzee prey preferences are distributed across primate and duiker species, and resemble those described in an early study of Sonso hunting. Waibira chimpanzees (which include ex-Sonso immigrants) have been observed to feed on red duiker (Cephalophus natalensis; 25%, 9/36 hunts), a species Sonso has never been recorded to feed on (18 years data, 27 years observations), despite no apparent differences in prey distribution; and show less rank-related harassment of meat possessors. We discuss the two most likely and probably interrelated explanations for the observed intergroup variation in chimpanzee hunting behaviour, that is, long-term disruption of complex group-level behaviour due to human presence and possible socially transmitted differences in prey preferences.

Reward of labor coordination and hunting success in wild chimpanzees

Cooperative hunting and meat sharing are hypothesized as fundamental to human life history adaptations and biological success. Wild chimpanzees also hunt in groups, and despite the potential of inferring ancestral hominid adaptations, it remains unclear whether chimpanzee hunting is a cooperative act. Here we show support for cooperative acquisition in wild chimpanzees since hunters are more likely to receive meat than bystanders, independent of begging effort. Engagement in prey searches and higher hunt participation independently increase hunting success, suggesting that coordination may improve motivation in joint tasks. We also find higher levels of urinary oxytocin after hunts and prey searches compared with controls. We conclude that chimpanzee hunting is cooperative, likely facilitated by behavioral and neuroendocrine mechanisms of coordination and reward. If group hunting has shaped humans’ life history traits, perhaps similar pressures acted upon life history patterns in the last common ancestor of human and chimpanzee.Liran Samuni et al. examined meat sharing behavior and oxytocin in wild chimpanzees, elucidating the mechanism facilitating cooperation. They find that hunters are more likely to receive food independent of begging, suggesting that prosocial behaviors are rewarded in primates, likely facilitated by oxytocin.

Flexible decision-making in grooming partner choice in sooty mangabeys and chimpanzees

Living in permanent social groups forces animals to make decisions about when, how and with whom to interact, requiring decisions to be made that integrate multiple sources of information. Changing social environments can influence this decision-making process by constraining choice or altering the likelihood of a positive outcome. Here, we conceptualized grooming as a choice situation where an individual chooses one of a number of potential partners. Studying two wild populations of sympatric primate species, sooty mangabeys (Cercocebus atys atys) and western chimpanzees (Pan troglodytes verus), we tested what properties of potential partners influenced grooming decisions, including their relative value based on available alternatives and the social relationships of potential partners with bystanders who could observe the outcome of the decision. Across 1529 decision events, multiple partner attributes (e.g. dominance ranks, social relationship quality, reproductive state, partner sex) influenced choice. Individuals preferred to initiate grooming with partners of similar global rank, but this effect was driven by a bias towards partners with a high rank compared to other locally available options. Individuals also avoided grooming partners who had strong social relationships with at least one bystander. Results indicated flexible decision-making in grooming interactions in both species, based on a partners value given the local social environment. Viewing partner choice as a value-based decision-making process allows researchers to compare how different species solve similar social problems.

Urinary oxytocin levels in relation to post-conflict affiliations in wild male chimpanzees (Pan troglodytes verus)

ABSTRACT Many animals living in social groups have evolved behaviors to resolve conflicts between group members, behaviors thought crucial for maintaining stable group life. Several hypotheses, based mainly on observational data, aim to explain how post‐conflict (PC) affiliations, such as reconciliation and consolation, resolve conflicts by restoring relationships and/or alleviating anxiety. To examine a potential endocrinological mechanism of PC affiliations, we used an experimental‐like procedure to investigate whether the oxytocinergic system is activated during naturally observed reconciliations, receiving bystander PC affiliations and aggressions not followed by PC affiliations in wild male chimpanzees. We compared urinary oxytocin (uOT) levels after reconciliations, receiving bystander PC affiliations or aggressions without affiliations with two control conditions: affiliations without previous aggression and after time periods without social interactions. We furthermore tested the ‘valuable relationship’ hypothesis of reconciliation, as well as the influence of relationship quality between individuals engaged in each of the three behavioral conditions involving aggression on uOT levels. We found that the probability to reconcile a conflict increased with increasing relationship quality between opponents, thus our results support the ‘valuable relationship’ hypothesis. However, relationship quality did not influence uOT levels, while behavioral condition had a significant effect on uOT levels. uOT levels after reconciliations, receiving bystander PC affiliations and affiliations not related to conflicts were higher than after aggressions alone and time periods without social interactions. Overall, our results indicate that the oxytocinergic system is activated during affiliative interactions, whether occurring as reconciliation, bystander PC affiliation or affiliation alone. We conclude that the oxytocinergic system, in addition to building and maintaining social relationships, also takes part in repairing them. HIGHLIGHTSuOT levels after reconciliation and bystander PC affiliation were higher than uOT levels after aggression alone.uOT levels were higher after any condition involving affiliation than uOT levels after a non‐social control condition.Aggressions alone did not elevate uOT levels.Relationship quality did not have a significant effect on uOT levels.

Circadian rhythms of urinary cortisol levels vary between individuals in wild male chimpanzees: a reaction norm approach

Investigating the repeatability of trait variation between individuals, that is the amount of individual variation in relation to overall phenotypic variation, indicates an upper level of heritability and reveals whether a given trait may be subject to selection. Labile traits are characterized by high levels of flexibility and consequently low trait repeatability is expected. Indeed, research examining glucocorticoid levels in various non-mammal species found low repeatability scores. However, mammals may be different in this respect as (i) differential maternal care early in life has the potential to prime hypothalamic-pituitary-adrenal axis functioning and (ii) allelic variation affecting hypothalamic-pituitary-adrenal axis functioning has been reported. Individuals often differ from each other in average and/or plastic labile trait expression, two aspects that can be described using a reaction norm approach. Both consistent and flexible reaction norm expression has been argued to serve adaptive purposes, depending on the stability and predictability of environmental conditions. Here we investigated both trait and reaction norm repeatability of urinary cortisol levels in wild adult male chimpanzees. To capture the expression of the circadian urinary cortisol rhythm of individual males over time, urine samples were collected throughout the day. In total data of 30 males collected over a period of 8 years were included in the dataset. No male was sampled over the whole 8-year period however. We found minor levels of trait repeatability but considerable reaction norm repeatability. This implies a minor role of genetic or priming factors on cortisol excretion, but reveals that males differ consistently in average urinary cortisol levels and the shape of the circadian urinary cortisol rhythm. Relating these results to fitness parameters will provide answers to questions on the adaptive value of reaction norm repeatability of this labile hormonal trait in the future.

Human coronavirus OC43 outbreak in wild chimpanzees, Côte d´Ivoire, 2016

Dear Editor, A number of pathogens have been described to circulate between humans and non-human primates. The close relatedness between these hosts is thought to support pathogen transmission. Due to their rapid spread and difficult containment, airborne pathogens raise the greatest concerns. Common human respiratory viruses such as the human respiratory syncytial virus (HRSV), the human metapneumovirus (HMPV) and the human rhinovirus C, have caused lethal outbreaks in wild habituated great apes. Strict prevention measures have been adopted to mitigate the risk of disease introduction at great ape research sites, allowing habituation programmes to maximize positive effects on wildlife conservation. However, transmission of infectious agents may still occur. Here we report the transmission of the human coronavirus (HCoV) OC43 to wild chimpanzees (Pan troglodytes verus) living in the Taï National Park, Côte d ́Ivoire. These chimpanzees are habituated to human presence, and are in the focus of long-term observatory studies since the ’80s. All members of the three communities (North, South and East) are individually known. Between late December 2016 and early January 2017, a mild respiratory outbreak was observed in the East chimpanzee community (currently composed of 33 individuals). Daily monitoring by trained personnel identified sporadic coughing and sneezing throughout the group, mainly in morning hours. No other symptom was observed. Factors such as forest density, chimpanzee group fission–fusion and amount of time spent on the ground vs. on trees strongly influence whether individuals can be observed on a daily basis. In such conditions, the detection of disease onset and follow-up of symptoms’ course over time as well as the collection of samples is very complicated. During this outbreak, symptoms were reported once in at least nine individuals; of these, six were consistently identified as symptomatic on three consecutive days (Fig. 1, bold names). Fecal samples were collected as part of a continuous non-invasive health monitoring program and shipped to the Robert Koch Institute for analyses. To expand our window of investigation to non-outbreak times, a total of 59 samples collected from 18 individuals of this community between November 2016 and February 2017 were tested. This number reflects all available samples for the time frame of interest. We performed a PCR screening targeting major respiratory viruses including HRSV and HMPV, adenoviruses (AdVs), coronaviruses, enteroviruses, influenza A and B viruses, parainfluenza viruses and rhinoviruses. PCR and sequencing identified the HCoV-OC43 in 14/ 59 samples, collected from 11 individuals, including those where symptoms were consistently reported (Fig. 1). HCoV-OC43 positive samples were collected within the time frame of observed respiratory disease outbreak, whereas samples collected before and after were negative. The detection in feces exclusively during the outbreak supports the hypothesis of this coronavirus being responsible for the observed mild respiratory symptoms. With the exception of AdVs, all other tests were negative. Adenoviruses were however detected in 49/59 samples across outbreak and non-outbreak times. Along with the evidence of AdVs being widely carried by wild great apes and shed in feces, the continuous detection points towards an unlikely involvement in this outbreak. Since 2008, the Taï Chimpanzee Project has implemented a mandatory quarantine for any individual intending to approach the chimpanzees. To control for

An assessment of the efficacy of camera traps for studying demographic composition and variation in chimpanzees (Pan troglodytes)

Demographic factors can strongly influence patterns of behavioral variation in animal societies. Traditionally, these factors are measured using longitudinal observation of habituated social groups, particularly in social animals like primates. Alternatively, noninvasive biomonitoring methods such as camera trapping can allow researchers to assess species occupancy, estimate population abundance, and study rare behaviors. However, measures of fine‐scale demographic variation, such as those related to age and sex structure or subgrouping patterns, pose a greater challenge. Here, we compare demographic data collected from a community of habituated chimpanzees (Pan troglodytes verus) in the Taï Forest using two methods: camera trap videos and observational data from long‐term records. By matching data on party size, seasonal variation in party size, measures of demographic composition, and changes over the study period from both sources, we compared the accuracy of camera trap records and long‐term data to assess whether camera trap data could be used to assess such variables in populations of unhabituated chimpanzees. When compared to observational data, camera trap data tended to underestimate measures of party size, but revealed similar patterns of seasonal variation as well as similar community demographic composition (age/sex proportions) and dynamics (particularly emigration and deaths) during the study period. Our findings highlight the potential and limitations of camera trap surveys for estimating fine‐scale demographic composition and variation in primates. Continuing development of field and statistical methods will further improve the usability of camera traps for demographic studies.

Neuroendocrine mechanisms of hunting and food sharing in wild chimpanzees

Intergroup encounters can have a substantial impact on individual fitness by altering access to resources and increasing risk of injury and death. Numerical advantage is usually of para- mount importance to maintain access to resources in between group contests. However, factors affecting payoffs can also be involved in determining intergroup encounter outcome and inten- sity. The most investigated so far has been location, often found to be relevant in explaining contest result and level of aggression. Other factors, such as proportion of infants and female reproductive state have yet to be thoroughly examined. Our aim was to investigate whether fe- male reproductive state and proportion of infants, together with group size and location, played a role in determining the outcome and intensity of intergroup encounters. We collected data for 9 consecutive months on 3 habituated groups of crested macaques ( Macaca nigra ) in the Tang- koko Nature Reserve (North Sulawesi, Indonesia), yielding information on 163 intergroup en- counters. Encounters tended to finish in a draw when groups were of similar sizes and both used the location of the encounter with similar frequency. Odds of winning an encounter (i.e. displac- ing the other group) were higher for those groups that used the encounter area more frequently and had lower proportions of both fertile females and females with infants. The longer the en- counter, the more likely it was to be aggressive, especially when group sizes were similar. Our data support previous findings that location and group size play an important role in determin- ing the nature and outcome of encounters. However, they suggest that intergroup encounters are influenced by a broad range of factors that affect the competitive ability of groups. Our study provides evidence that intergroup relationships in primates are more context dependent than previously thought.Lemur Abundance in the Lowland Rainforest of Tsitongambarika, Southeastern Madagascar : Altitudinal and Latitudinal ComparisonsBiomechanical analyses of great ape arboreal locomotion in a natural environment are scarce, thus limiting attempts to correlate behavioural and habitat differences with variation in skeletal morphology. Vertical climbing is a crucial locomotor and foraging strategy of great apes and the hands are critically important to maintaining stability on irregular, arboreal substrates. However, little is known about arboreal grips and hand postures, or how these might vary with forelimb posture during vertical climbing on natural substrates of different sizes. This is particularly true of mountain gorillas, which are considered the least arboreal of all African apes and for which the characteristics of vertical climbing have not yet been studied. The aim of this study was to compare temporal kinematics of hand and forelimb use during vertical climbing in wild, habituated mountain gorillas (Gorilla beringei beringei) of the Bwindi Impenetrable Forest (Uganda) and sanctuary chimpanzees (Pan troglodytes) of the Chimfunshi Wildlife Orphanage Trust (Zambia) to assess differences in climbing styles that may relate to variation in hand or forelimb morphology and body mass. We investigated hand and forelimb posture coupled with temporal gait parameters during vertical climbing (both ascent and descent) in 15 mountain gorillas and eight chimpanzees, using video records ad libitum. In both apes, forelimb posture was correlated with substrate size during both ascent and descent climbing. Both apes used power grips and a diagonal power grip, involving three different thumb postures. Gorillas showed greater ulnar deviation of the wrist during climbing than chimpanzees, and the thumb played an important supportive role when vertically descending compliant substrates in gorillas. Comparisons of temporal gait parameters indicated that large-bodied gorillas exhibited significant longer cycle duration, lower stride frequency and generally a higher duty factor than chimpanzees. This study revealed that wild mountain gorillas adapt their climbing strategy to accommodate their large body mass in a similar manner found in captive western lowland gorillas, but that our sanctuary chimpanzees showed less variation in their climbing strategy within a natural environment than has been documented in captive bonobosMany primates face spatial and temporal fluctuations in food availability, which can significantly affect their ability to meet nutritional requirements. Anthropogenic disturbances and influences, such as agriculture, human presence and infrastructures, can further impact seasonal food availability, dietary composition and nutrition. Primates residing in anthropogenic landscapes often incorporate cultivars into their diets. However, the nutritional drivers behind cultivar consumption are poorly understood. We examined variations in chimpanzee (Pan troglodytes verus) macronutrient intake from wild and cultivated foods between sexes and seasons over a 1year period in Bossou, Guinea. We used the geometric framework of nutrition to examine proportional contributions of macronutrients to the diet and nutrient balancing. We conducted continuous focal observations of adult individuals ( n = 10) to record all feeding bouts and conducted nutritional analyses of plant foods (25 wild species; 11 cultivated species). We found no sex differences in chimpanzees for wild or cultivated food or macronutrient intakes; however, females showed higher intakes of total food (i.e. wild and cultivated combined), digestible fibre (NDF), and protein when controlling for metabolic body mass. There were no differences in wild or cultivated food intake between seasons; however, lipid and protein intake from cultivars were higher when wild fruit availability was low. Chimpanzees maintained a constant proportional intake of protein while allowing carbohydrates and lipid intakes to vary. Furthermore, they were able to maintain a consistent balance of protein to non-protein (carbohydrates, lipids, and NDF) energy across the year. Our results suggest that Bossou chimpanzees suffered little seasonal constraints in food quality or availability since they were able to combine their consumption of available wild and cultivated foods to achieve a balanced diet. These findings contribute significantly to our understanding of primate nutritional requirements and their ability to meet these in disturbed environments.