Urinary oxytocin and social bonding in related and unrelated wild chimpanzees

Animals that maintain cooperative relationships show gains in longevity and offspring survival. However, little is known about the cognitive or hormonal mechanisms involved in cooperation. Indeed, there is little support for a main hypothesis that non-human animals have the cognitive capacities required for bookkeeping of cooperative exchanges. We tested an alternative hypothesis that cooperative relationships are facilitated by an endocrinological mechanism involving oxytocin, a hormone required for bonding in parental and sexual relationships across mammals. We measured urinary oxytocin after single bouts of grooming in wild chimpanzees. Oxytocin levels were higher after grooming with bond partners compared with non-bond partners or after no grooming, regardless of genetic relatedness or sexual interest. We ruled out other possible confounds, such as grooming duration, grooming direction or sampling regime issues, indicating that changes in oxytocin levels were mediated by social bond strength. Oxytocin, which is thought to act directly on neural reward and social memory systems, is likely to play a key role in keeping track of social interactions with multiple individuals over time. The evolutionary linkage of an ancestral hormonal system with complex social cognition may be the primary mechanism through which long-term cooperative relationships develop between both kin and non-kin in mammals.     

Food sharing in vampire bats: reciprocal help predicts donations more than relatedness or harassment

Common vampire bats often regurgitate food to roost-mates that fail to feed. The original explanation for this costly helping behaviour invoked both direct and indirect fitness benefits. Several authors have since suggested that food sharing is maintained solely by indirect fitness because non-kin food sharing could have resulted from kin recognition errors, indiscriminate altruism within groups, or harassment. To test these alternatives, we examined predictors of food-sharing decisions under controlled conditions of mixed relatedness and equal familiarity. Over a 2 year period, we individually fasted 20 vampire bats (Desmodus rotundus) and induced food sharing on 48 days. Surprisingly, donors initiated food sharing more often than recipients, which is inconsistent with harassment. Food received was the best predictor of food given across dyads, and 8.5 times more important than relatedness. Sixty-four per cent of sharing dyads were unrelated, approaching the 67 per cent expected if nepotism was absent. Consistent with social bonding, the food-sharing network was consistent and correlated with mutual allogrooming. Together with past work, these findings support the hypothesis that food sharing in vampire bats provides mutual direct fitness benefits, and is not explained solely by kin selection or harassment.     

Non-kin cooperation in bats

Many bats are extremely social. In some cases, individuals remain together for years or even decades and engage in mutually beneficial behaviours among non-related individuals. Here, we summarize ways in which unrelated bats cooperate while roosting, foraging, feeding or caring for offspring. For each situation, we ask if cooperation involves an investment, and if so, what mechanisms might ensure a return. While some cooperative outcomes are likely a by-product of selfish behaviour as they are in many other vertebrates, we explain how cooperative investments can occur in several situations and are particularly evident in food sharing among common vampire bats (Desmodus rotundus) and alloparental care by greater spear-nosed bats (Phyllostomus hastatus). Fieldwork and experiments on vampire bats indicate that sharing blood with non-kin expands the number of possible donors beyond kin and promotes reciprocal help by strengthening long-term social bonds. Similarly, more than 25 years of recapture data and field observations of greater spear-nosed bats reveal multiple cooperative investments occurring within stable groups of non-kin. These studies illustrate how bats can serve as models for understanding how cooperation is regulated in social vertebrates.     

Oxytocin is associated with infant-care behavior and motivation in cooperatively breeding marmoset monkeys

The neurohormone oxytocin (OT) is positively involved in the regulation of parenting and social bonding in mammals, and may thus also be important for the mediation of alloparental care. In cooperatively breeding marmosets, infants are raised in teamwork by parents and adult and sub-adult non-reproductive helpers (usually older siblings). Despite high intrinsic motivation, which may be mediated by hormonal priming, not all individuals are always equally able to contribute to infant-care due to competition among care-takers. Among the various care-taking behaviors, proactive food sharing may reflect motivational levels best, since it can be performed ad libitum by several individuals even if competition among surplus care-takers constrains access to infants. Our aim was to study the link between urinary OT levels and care-taking behaviors in group-living marmosets, while taking affiliation with other adults and infant age into account. Over eight reproductive cycles, 26 individuals were monitored for urinary baseline OT, care-taking behaviors (baby-licking, -grooming, -carrying, and proactive food sharing), and adult-directed affiliation. Mean OT levels were generally highest in female breeders and OT increased significantly in all individuals after birth. During early infancy, high urinary OT levels were associated with increased infant-licking but low levels of adult-affiliation, and during late infancy, with increased proactive food sharing. Our results show that, in marmoset parents and alloparents, OT is positively involved in the regulation of care-taking, thereby reflecting the changing needs during infant development. This particularly included behaviors that are more likely to reflect intrinsic care motivation, suggesting a positive link between OT and motivational regulation of infant-care.     

Co–Residence between Males and Their Mothers and Grandmothers Is More Frequent in Bonobos Than Chimpanzees

In long–lived social mammals such as primates, individuals can benefit from social bonds with close kin, including their mothers. In the patrilocal chimpanzee (Pan troglodytes spp.) and bonobo (Pan paniscus), sexually mature males reside and reproduce in their natal groups and can retain post-dependency bonds with their mothers, while immatures of both sexes might also have their paternal grandmothers available. However, quantitative information on the proportion of males and immatures that co-reside with both types of these close female relatives is limited for both species. Combining genetic parentage determination and group composition data from five communities of wild chimpanzees and three communities of wild bonobos, we estimated the frequency of co-residence between (1) mature males and their mothers, and (2) immature males and females and their paternal grandmothers. We found that adult males resided twice as frequently with their mothers in bonobos than in chimpanzees, and that immature bonobos were three times more likely to possess a living paternal grandmother than were immature chimpanzees. Patterns of female and male survivorship from studbook records of captive individuals of both species suggest that mature bonobo females survive longer than their chimpanzee counterparts, possibly contributing to the differences observed in mother–son and grandmother–immature co-residency levels. Taking into account reports of bonobo mothers supporting their sons'' mating efforts and females sharing food with immatures other than their own offspring, our findings suggest that life history traits may facilitate maternal and grandmaternal support more in bonobos than in chimpanzees.     

A friend in need is a friend indeed: Need-based sharing,rather than cooperative assortment,predicts experimental resource transfers among Agta hunter-gatherers

Despite much theorizing, the evolutionary reasons why humans cooperate extensively with unrelated individuals are still largely unknown. While reciprocity explains many instances of non-kin cooperation, much remains to be understood. A recent suite of models based upon ‘cooperative assortativity’ suggest that non-kin cooperation can evolve if individuals preferentially assort with certain cooperative phenotypes, such as helping those who help others. Here, we test these assortative hypotheses among the Agta, a population of Filipino hunter-gatherers, using an experimental resource allocation game in which individuals divide resources between themselves and camp-mates. Individuals preferentially shared with less cooperative individuals, arguing against cooperative assortativity as a mechanism sustaining resource transfers in this population. Rather, sharing was often based on the recipient's level of need, in addition to kin-based transfers and reciprocal sharing. Contrary to several recent theoretical accounts, in this real-world setting we find no evidence for cooperative assortativity influencing patterns of cooperation. These results may reflect the demands of living in a foraging ecology characterized by high resource stochasticity, necessitating need-based sharing as a system of long-term reciprocity to mitigate repeated subsistence shortfalls.     

Intranasal oxytocin increases social grooming and food sharing in the common vampire bat Desmodus rotundus

Intranasal oxytocin (OT) delivery has been used to non-invasively manipulate mammalian cooperative behavior. Such manipulations can potentially provide insight into both shared and species-specific mechanisms underlying cooperation. Vampire bats are remarkable for their high rates of allogrooming and the presence of regurgitated food sharing among adults. We administered intranasal OT to highly familiar captive vampire bats of varying relatedness to test for an effect on allogrooming and food sharing. We found that intranasal OT did not have a detectable effect on food-sharing occurrence, but it did increase the size of regurgitated food donations when controlling for dyad and amount of allogrooming. Intranasal OT in females increased the amount of allogrooming per partner and across all partners per trial, but not the number of partners. We also found that the peak effect of OT treatments occurred 30–50 min after administration, which is consistent with the reported latency for intranasal OT to affect relevant brain areas in rats and mice. Our results suggest that intranasal OT is a potential tool for influencing dyadic cooperative investments, but measuring prior social relationships may be necessary to interpret the results of hormonal manipulations of cooperative behavior and it may be difficult to alter partner choice in vampire bats using intranasal OT alone.     

布氏田鼠合作贮食行为及其影响因素

合作贮食是社会性动物应对食物匮乏的重要对策,但其内在的生态学机制尚未阐明。本文以布氏田鼠为研究对象,根据亲缘关系划分为亲缘组和非亲缘组。在人工实验箱中录像统计不同组别合作贮食行为占用时间的差异,探究亲缘关系对合作贮食行为的影响,并利用相关性分析探究亲缘组个体对贮食的贡献—收益关系以及与贮食行为相关的个体特征因素。结果表明,在组间水平上,与非亲缘组相比,亲缘组的布氏田鼠表现更多的合作贮食。在亲缘组个体水平上,不同个体对贮食的参与度和贡献度存在很大差异。个体对合作贮食的付出与其取食的收益呈显著负相关关系,并且个体合作贮食贡献越大,其睾丸指数和睾酮含量降低越显著。研究结果说明,亲缘关系的存在有利于布氏田鼠的合作贮食,但合作贮食贡献大的个体,其繁殖受到了抑制。     

Altruism in Forest Chimpanzees: The Case of Adoption

In recent years, extended altruism towards unrelated group members has been proposed to be a unique characteristic of human societies. Support for this proposal seemingly came from experimental studies on captive chimpanzees that showed that individuals were limited in the ways they shared or cooperated with others. This dichotomy between humans and chimpanzees was proposed to indicate an important difference between the two species, and one study concluded that “chimpanzees are indifferent to the welfare of unrelated group members”. In strong contrast with these captive studies, consistent observations of potentially altruistic behaviors in different populations of wild chimpanzees have been reported in such different domains as food sharing, regular use of coalitions, cooperative hunting and border patrolling. This begs the question of what socio-ecological factors favor the evolution of altruism. Here we report 18 cases of adoption, a highly costly behavior, of orphaned youngsters by group members in Taï forest chimpanzees. Half of the adoptions were done by males and remarkably only one of these proved to be the father. Such adoptions by adults can last for years and thus imply extensive care towards the orphans. These observations reveal that, under the appropriate socio-ecologic conditions, chimpanzees do care for the welfare of other unrelated group members and that altruism is more extensive in wild populations than was suggested by captive studies.     

How institutions shaped the last major evolutionary transition to large-scale human societies

What drove the transition from small-scale human societies centred on kinship and personal exchange, to large-scale societies comprising cooperation and division of labour among untold numbers of unrelated individuals? We propose that the unique human capacity to negotiate institutional rules that coordinate social actions was a key driver of this transition. By creating institutions, humans have been able to move from the default ‘Hobbesian’ rules of the ‘game of life’, determined by physical/environmental constraints, into self-created rules of social organization where cooperation can be individually advantageous even in large groups of unrelated individuals. Examples include rules of food sharing in hunter–gatherers, rules for the usage of irrigation systems in agriculturalists, property rights and systems for sharing reputation between mediaeval traders. Successful institutions create rules of interaction that are self-enforcing, providing direct benefits both to individuals that follow them, and to individuals that sanction rule breakers. Forming institutions requires shared intentionality, language and other cognitive abilities largely absent in other primates. We explain how cooperative breeding likely selected for these abilities early in the Homo lineage. This allowed anatomically modern humans to create institutions that transformed the self-reliance of our primate ancestors into the division of labour of large-scale human social organization.     

Vertebrate Predation and Food-Sharing in Cebus and Pan

Capuchins and chimpanzees are the only nonhuman primates apart from baboons known to prey systematically upon relatively large vertebrates. Vertebrate predation is common and well documented in Pan troglodytes, rare in Pan paniscus, and commonly reported but infrequently studied in Cebus. Food-sharing is common in both Pan species but rarely reported for wild capuchins. I present data on vertebrate predation and food-sharing by white-faced capuchins (Cebus capucinus) from ongoing field studies at Santa Rosa National Park, Costa Rica. We have observed 106 successful predation events resulting in the capture of 156 prey items during 2929 observation hr (5.35 prey per 100 hr). Squirrels and nestling coatis comprised half of the prey taken; the remainder were mainly nestling birds and eggs. Adult males took 52% of all prey and 67% of squirrels. Squirrels are actively hunted and about 65% of them are adults. I estimated that the average capuchin group kills 43–50 squirrels annually, mostly during the dry season. Capuchins hunt squirrels in groups 81% of the time, and 17% of hunts are successful. There is no evidence for cooperative hunting, but occasional collaboration is suggested. Rates of food-sharing were low (1.7 per 100 hr), and meat was the only food shared between adults. I compare predation and food-sharing in C. capucinus with published data for Pan troglodytes, primarily in Gombe and Taï National Parks. I discuss sex differences, hunting strategies, the relationship between hunting and food-sharing, and various ecological and social factors that may promote vertebrate predation in Pan and Cebus.     

Evolutionary routes to non-kin cooperative breeding in birds

Cooperatively breeding animals live in social groups in which some individuals help to raise the offspring of others, often at the expense of their own reproduction. Kin selection—when individuals increase their inclusive fitness by aiding genetic relatives—is a powerful explanation for the evolution of cooperative breeding, particularly because most groups consist of family members. However, recent molecular studies have revealed that many cooperative groups also contain unrelated immigrants, and the processes responsible for the formation and maintenance of non-kin coalitions are receiving increasing attention. Here, I provide the first systematic review of group structure for all 213 species of cooperatively breeding birds for which data are available. Although the majority of species (55%) nest in nuclear family groups, cooperative breeding by unrelated individuals is more common than previously recognized: 30% nest in mixed groups of relatives and non-relatives, and 15% nest primarily with non-relatives. Obligate cooperative breeders are far more likely to breed with non-kin than are facultative cooperators, indicating that when constraints on independent breeding are sufficiently severe, the direct benefits of group membership can substitute for potential kin-selected benefits. I review three patterns of dispersal that give rise to social groups with low genetic relatedness, and I discuss the selective pressures that favour the formation of such groups. Although kin selection has undoubtedly been crucial to the origin of most avian social systems, direct benefits have subsequently come to play a predominant role in some societies, allowing cooperation to persist despite low genetic relatedness.     

Chimpanzees share forbidden fruit

The sharing of wild plant foods is infrequent in chimpanzees, but in chimpanzee communities that engage in hunting, meat is frequently used as a 'social tool' for nurturing alliances and social bonds. Here we report the only recorded example of regular sharing of plant foods by unrelated, non-provisioned wild chimpanzees, and the contexts in which these sharing behaviours occur. From direct observations, adult chimpanzees at Bossou (Republic of Guinea, West Africa) very rarely transferred wild plant foods. In contrast, they shared cultivated plant foods much more frequently (58 out of 59 food sharing events). Sharing primarily consists of adult males allowing reproductively cycling females to take food that they possess. We propose that hypotheses focussing on 'food-for-sex and -grooming' and 'showing-off' strategies plausibly account for observed sharing behaviours. A changing human-dominated landscape presents chimpanzees with fresh challenges, and our observations suggest that crop-raiding provides adult male chimpanzees at Bossou with highly desirable food commodities that may be traded for other currencies.     

Validating the use of a commercial enzyme immunoassay to measure oxytocin in unextracted urine and saliva of the western lowland gorilla (<Emphasis Type="Italic">Gorilla gorilla gorilla</Emphasis>)

The neuroendocrine hormone oxytocin, which is an important physiological driver of social behavior and bonding, is increasingly being measured in conjunction with behavior to better understand primate sociality. To date no data are available on oxytocin concentrations within the genus Gorilla; however, as a result of their close genetic relatedness to humans, and tolerance-based social system, Gorilla represents an important group of study. The purpose of this study was to validate the measurement of urinary and salivary oxytocin in western lowland gorillas (Gorilla gorilla gorilla) to help facilitate future study of the interaction between oxytocin and behavior within the subspecies. The primary validation procedure was an intranasal challenge. Elevated oxytocin concentrations were observed in saliva samples taken 15–120 min post challenge. Urine levels remained within baseline range approximately 30 and 90 min following the challenge; however, elevated levels were observed 24 h post challenge. No diurnal variation was found in salivary samples taken at regular intervals throughout the day; however, morning urine samples had higher concentrations than afternoon samples. In addition, samples were collected opportunistically following three social events: play, breeding, and the death of a conspecific. Following the play bouts, salivary oxytocin was almost three times greater than baseline. Salivary oxytocin was also significantly higher 15 min post breeding compared to match-control samples. Following the death of a conspecific, the group mate’s urinary oxytocin concentrations decreased by half compared to a baseline period when the group was intact. This study provides a biological validation of the measurement of urinary and salivary oxytocin in western lowland gorillas. These results suggest that urinary oxytocin measurements are suitable for establishing baseline levels, as they represent the build up of the previous day’s concentrations, and salivary oxytocin measurements are suitable for assessing changes following specific events.     

Social Grooming in Bats: Are Vampire Bats Exceptional?

Evidence for long-term cooperative relationships comes from several social birds and mammals. Vampire bats demonstrate cooperative social bonds, and like primates, they maintain these bonds through social grooming. It is unclear, however, to what extent vampires are special among bats in this regard. We compared social grooming rates of common vampire bats Desmodus rotundus and four other group-living bats, Artibeus jamaicensis, Carollia perspicillata, Eidolon helvum and Rousettus aegyptiacus, under the same captive conditions of fixed association and no ectoparasites. We conducted 13 focal sampling sessions for each combination of sex and species, for a total of 1560 presence/absence observations per species. We observed evidence for social grooming in all species, but social grooming rates were on average 14 times higher in vampire bats than in other species. Self-grooming rates did not differ. Vampire bats spent 3.7% of their awake time social grooming (95% CI = 1.5–6.3%), whereas bats of the other species spent 0.1–0.5% of their awake time social grooming. Together with past data, this result supports the hypothesis that the elevated social grooming rate in the vampire bat is an adaptive trait, linked to their social bonding and unique regurgitated food sharing behavior.     

Cooperative problem solving in rooks (Corvus frugilegus)

Recent work has shown that captive rooks, like chimpanzees and other primates, develop cooperative alliances with their conspecifics. Furthermore, the pressures hypothesized to have favoured social intelligence in primates also apply to corvids. We tested cooperative problem-solving in rooks to compare their performance and cognition with primates. Without training, eight rooks quickly solved a problem in which two individuals had to pull both ends of a string simultaneously in order to pull in a food platform. Similar to chimpanzees and capuchin monkeys, performance was better when within-dyad tolerance levels were higher. In contrast to chimpanzees, rooks did not delay acting on the apparatus while their partner gained access to the test room. Furthermore, given a choice between an apparatus that could be operated individually over one that required the action of two individuals, four out of six individuals showed no preference. These results may indicate that cooperation in chimpanzees is underpinned by more complex cognitive processes than that in rooks. Such a difference may arise from the fact that while both chimpanzees and rooks form cooperative alliances, chimpanzees, but not rooks, live in a variable social network made up of competitive and cooperative relationships.     

Begging and social tolerance: Food solicitation tactics in young chimpanzees (Pan troglodytes) in the wild

The substantial role of food sharing in human evolution has been widely recognized, and food-soliciting tactics may have been critical in facilitating these transfers. Great apes, our closest living relatives, also use different food-soliciting tactics to obtain food from both kin and non-kin. However, the individual and social factors involved in requests for and subsequent transfers of food have been relatively little studied. Here, we examined which tactics (e.g., tactile gestures, taking actions, and vocalizations) infant chimpanzees (Pan troglodytes) employ to solicit food as well as the success of obtaining food from their conspecifics. Using a multimodal approach, we focused on food-related interactions in 14 chimpanzee infants of two different subspecies (P. t. schweinfurthii/verus) living in the communities of Kanyawara, Uganda, and Taï South, Côte d'Ivoire. Overall, we found that infants' solicitation tactics included mainly visual or tactile gestural requests and taking attempts, while vocalizations and gestures involving auditory components were rarely used. With increasing age, infants used more visual gestures when soliciting food from conspecifics other than the mother. If food was solicited from mothers or maternal kin, infants predominantly begged for food via (mechanically effective) taking attempts. In terms of subsequent food transfers, taking attempts were more successful than gestures. In light of the prevalent use of non-contact begging despite low rates of success, food solicitation in young great apes might also function to facilitate social tolerance and gain social information. We thus conclude that the food sharing context might represent a critical platform to learn and practice social rules underlying cooperative interactions, which can later be generalized across collaborative domains.     

Fruit sharing between wild adult chimpanzees (Pan troglodytes schweinfurthii): a socially significant event?

Although food sharing is a habitual aspect of chimpanzee (Pan troglodytes) life, sharing of plant foods between unrelated adults is rare. Observations of such behavior have typically been interpreted as the outcome of a process by which individuals that are otherwise unable to gain access to the food manage to obtain a nutritional benefit. Here we present behavioral details and an acoustic analysis regarding an observation of food sharing between unrelated adult wild chimpanzees that we suggest cannot be explained using traditional nutrition-based models. Instead we propose that the exchange is only understandable as a socially important event, and we cite two further observations in the same population that support this suggestion.     

Carrying, Sharing, and Hand Preference in Tufted Capuchins (Cebus apella)

We examined the relationship among carrying, food-sharing, and hand preference in tufted capuchins (Cebus apella). The rationale was to evaluate further the use of Cebus as an alternative primate model to Pan for behavior relevant to early hominid evolution. We first examined bipedalism and food-sharing within an established social group, and then examined the direction and strength of hand preference for food carrying in an expanded sample. Several aspects of capuchin behavior warrant discussion. First, bipedal carrying and food-sharing occurred more frequently when we provided bulky foods than when we provided smaller foods. Second, food-sharing was characterized by passive tolerance, rather than active giving, between subjects. Third, subjects shared food primarily with immatures and followed a pattern of reciprocal exchange. Finally, we found no evidence for population-level hand preference for carrying. We posit that an array of behavioral similarities among Cebus, Pan, and Homo evolved through convergent processes, and in this regard capuchins can be seen as an alternative primate model to chimpanzees for the evolution of early hominid behavior.     

Social vocalizations can release oxytocin in humans

Vocalizations are important components of social behaviour in many vertebrate species, including our own. Less well-understood are the hormonal mechanisms involved in response to vocal cues, and how these systems may influence the course of behavioural evolution. The neurohormone oxytocin (OT) partly governs a number of biological and social processes critical to fitness, such as attachment between mothers and their young, and suppression of the stress response after contact with trusted conspecfics. Rodent studies suggest that OT''s release is contingent upon direct tactile contact with such individuals, but we hypothesized that vocalizations might be capable of producing the same effect. To test our hypothesis, we chose human mother–daughter dyads and applied a social stressor to the children, following which we randomly assigned participants into complete contact, speech-only or no-contact conditions. Children receiving a full complement of comfort including physical, vocal and non-verbal contact showed the highest levels of OT and the swiftest return to baseline of a biological marker of stress (salivary cortisol), but a strikingly similar hormonal profile emerged in children comforted solely by their mother''s voice. Our results suggest that vocalizations may be as important as touch to the neuroendocrine regulation of social bonding in our species.