Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees

Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent–offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event—food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother–infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.     

Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal

The evolution and expression of different forms of cooperative behaviour (e.g. feeding, guarding, sentinel duties, etc.) are usually studied independently, with few studies considering them as a single syndrome. However, studies investigating individuals' investment across a suite of different behaviours reveal that they are correlated, suggesting a single mechanism determining the evolution and expression of cooperative behaviours. A hormonal mechanism could achieve this, and one possibility is oxytocin (OT), which affects several prosocial or alloparental behaviours independently. We show, using a double-blind experiment, that peripheral administration of OT to social, free-living meerkats Suricata suricatta elevates a suite of cooperative behaviours. Treated individuals increase their contributions to communal, cooperative activities (digging, guarding, pup-feeding and associating with pups) and decrease initiation of aggressive interactions, compared with a saline control. This suggests that different forms of cooperative behaviour form a single syndrome with a common causal basis. If our peripherally administered OT acts in the same way as the naturally released hormone, then a general tendency to prosociality may be modulated by this hormonal system. Therefore, it may be difficult for an individual to decouple expression of cooperative behaviours that provide the practitioner with benefits from those that provide the recipient with benefits. It may also explain why social species typically exhibit a suite of cooperative behaviours, without having to invoke independent evolution of each.     

Triadic social interactions operate across time: a field experiment with wild chimpanzees

Social animals cooperate with bonding partners to outcompete others. Predicting a competitor''s supporter is likely to be beneficial, regardless of whether the supporting relationship is stable or transient, or whether the support happens immediately or later. Although humans make such predictions frequently, it is unclear to what extent animals have the cognitive abilities to recognize others’ transient bond partners and to predict others'' coalitions that extend beyond the immediate present. We conducted playback experiments with wild chimpanzees to test this. About 2 h after fighting, subjects heard recordings of aggressive barks of a bystander, who was or was not a bond partner of the former opponent. Subjects looked longer and moved away more often from barks of the former opponents’ bond partners than non-bond partners. In an additional experiment, subjects moved away more from barks than socially benign calls of the same bond partner. These effects were present despite differences in genetic relatedness and considerable time delays between the two events. Chimpanzees, it appears, integrate memories of social interactions from different sources to make inferences about current interactions. This ability is crucial for connecting triadic social interactions across time, a requirement for predicting aggressive support even after a time delay.     

'Gatherings' of social grooming among wild chimpanzees: implications for evolution of sociality

Chimpanzees (Pan troglodytes) often groom in gatherings that cannot simply be divided into unilateral dyadic grooming interactions. This feature of grooming is studied at two different levels: grooming cliques and grooming clusters. Grooming cliques are defined as directly connected configurations of grooming interactions at any given moment, and when any member of a clique successively grooms any member of another clique within 5min and within a distance of 3m, all the members of both cliques are defined as being in the same grooming cluster. Twenty-seven types of cliques are observed, with the largest one consisting of seven individuals. Mutual and/or polyadic cliques account for more than 25% of all cliques. The size of grooming clusters varies from two to 23 individuals, and almost 70% of the grooming time is spent in polyadic clusters. Although adult males groom the longest in relatively smaller clusters (size=2-4), adult females groomed the longest in clusters of five or more individuals. A review of the literature implies that mutual and polyadic cliques occur less often in other primate species than in chimpanzees. The importance of overlapping interactions for these kinds of gatherings and its possible significance in the evolution of sociality is discussed in this article.     

Innovation in wild chimpanzees (Pan troglodytes)

Innovations of behavior have major implications for the concept of culture in animals. Innovation has rarefy been documented in wild animal populations. The chimpanzees of the Ta? National Park, C?te d’Ivoire, spontaneously included new patterns of behavior in their repertoire during our study. Some innovations were incorporated into a minority of the group members’ repertoire, whereas others, such as building day nests in trees and on the ground more frequently, became general behaviors. Similarly, new contexts for use of leaf- clipping behavior and novel ways of feeding on some leaves appeared and rapidly became part of the behavior of most group members. The environmental parameters were too stable to explain these new forms of behavior, as most of them took place within 1 month during the same dry season. In a similar way, leaf- grooming acquired a new function in Gombe chimpanzees. A process similar to social conventions could explain the emergence of these new functions for an existing behavior in a way rather similar to human “fashion. ” Three major characteristics of human culture — the absence of individual variations in the performance of the behavior, the general use of the behavior by group members, and the ability to modify the function of a behavior — characterize leaf-clipping in Ta? chimpanzees and leaf- grooming in Gombe chimpanzees.     

Association,ranging, and the social unit in chimpanzees of the Mahale Mountains,Tanzania

In order to characterize the social unit in chimpanzees, about which several conflicting views have been proposed, the proximity matrix among 55 recognized chimpanzees and the range covered by each of them are examined, on the basis of data obtained at the Mahale Mountains during 12 months in 1978–1979. It is shown once again that chimpanzees have a bisexual social unit (unit-group). Two such unit-groups were detected in the study area. All animals belonged to one of the two unit-groups except a few cycling females (and a juvenile male accompanied by his cycling mother) which were seen to associate alternately with members of two neighboring unit-groups, covering a whole range of one or even two unit-groups. The problem of such females is discussed in relation to the spatial relationships between the two unit-groups. Reexamining the membership of a unit-group, it is demonstrated that a unit-group was most likely patrilineal. While nulliparous females transferred between unit-groups, parous females tended to remain in a unit-group where they first gave birth to infants and to have several offspring therein. This appeared significant for ensuring recruitment of members of the next generation to a patrilineal unit-group. Although some adult males left their natal unit-group, they never joined the other. Male departure from a unit-group seemed to be forced by the other males and to be the sociological equivalent of going into exile, which is unique in nonhuman primates.     

The leaf-clipping display: A newly-discovered expressive gesture in wild chimpanzees

Chimpanzees of the Mahale Mountains, Tanzania were discovered to show an expressive gesture using leaves, termed as “leaf-clipping display”. This behavioural signal is directed by an adult male to an estrous female as a possessive behaviour, or by an adolescent male as a courtship display, or by an estrous female to an adolescent male also as a solicitation of copulation. The signal also is used toward human observers as a signal of food-demanding. This behaviour pattern might originate in a displacement tool-making behaviour in conflict situations. The leaf-clipping display has not been observed in any other chimpanzee populations studied, and may probably be one example of the tradition drift in wild chimpanzees.     

Paternity exclusion in a community of wild chimpanzees using hypervariable simple sequence repeats

We report the use of hypervariable simple sequence repeat (SSR) nuclear loci to study paternity in a community of wild chimpanzees ( Pan troglodytes schweinfurthii ) in Gombe National Park, Tanzania. All 43 living members of a habituated community were sampled and 35 were genotyped at 8 SSR loci using DNA amplified from hair. Paternity exclusions were performed for 25 chimpanzees including 10 for whom the mother was also genotyped. In each case 12–20 males were potential fathers based on their age and/ or direct observation of sexual behaviour. 179 tests involving potential father/offspring combinations were performed. In four cases the data permit the probable identification of the previously undetermined father; these are the first such determinations for free-ranging chimpanzees, and the first based on non-invasive sampling. In another four cases we were able to exclude all but two to five potential fathers, and in the remaining cases we were able to exclude all living males. For molecular ecologists SSR genotype databases offer important advantages over currently popular minisatellite DNA fingerprinting: they can be analysed unequivocally using traditional population genetics techniques and they can be expanded through time and space by other researchers.     

Urinary oxytocin as a noninvasive biomarker of positive emotion in dogs

A reliable assay based on physiological parameters that does not require subjective input from the owners is required to assess positive emotions in dogs. In addition, when viewed from an animal welfare perspective, physiological parameters should be collected in a noninvasive manner. Oxytocin (OT) is a biomarker that may be associated with a calm, relaxed state, and positive emotion. We measured the time-lapse in the concentration of plasma OT relative to urinary OT using a radioimmunoassay with sufficient sensitivity and low variability, and examined the relationship between OT and cortisol. Six dogs were injected with exogenous OT intravenously to increase the blood OT concentration. As a result, the highest concentration of urinary OT occurred 1 h after the injection, although there was little change in urinary cortisol. Moreover, to evaluate the influence of stimuli on urinary OT and cortisol, we provided three stimuli of eating food, exercising and stroking, all of which were assumed to inspire a positive emotion in dogs, and significantly increased urinary OT concentrations. Our findings indicate that urinary OT might be useful as a noninvasive and objective biomarker of positive emotion in dogs.     

Dynamics of social and energetic stress in wild female chimpanzees

Stress hormone measurements can reinforce and refine hypotheses about the costs of particular contexts or behaviors in wild animals. For social species, this is complicated because potential stressors may come from the physical environment, social environment, or some combination of both, while the stress response itself is generalized. Here, we present a multivariate examination of urinary cortisol dynamics over 6 years in the lives of wild female chimpanzees in the Kanyawara community of Kibale National Park, Uganda. We hypothesized that chimpanzee socioecology provides strong indications of both energetic and social stress to females, but that the salience of these stressors might vary over a female's life history in accordance with their changing reproductive costs and social interactions. Using linear mixed models, we found that urinary cortisol levels increased significantly with age but were also elevated in young immigrants to the community. Across reproductive states, cycling, non-estrous females had relatively low cortisol compared to lactating, estrous, or pregnant females. Aggression from males led to higher cortisol levels among estrous females, frequent targets of aggressive sexual coercion. In contrast, energetic stress was most salient to lactating females, who experienced higher cortisol during months of low fruit consumption. Low dominance rank was associated with increased cortisol, particularly during the energetically demanding period of lactation. The effects of female conflict were felt widely, even among those who were the primary aggressors, providing further evidence that long-term resource competition, while apparently muted, exerts a far-reaching impact on the lives of chimpanzee females.