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Reciprocity in primates: do unto others as you would have them do unto you

Primates have a long memory. If someone does somebody else a favour, the latter will remember it, and return the favour over extended periods. This reciprocation works better if the monkeys are emotionally involved with their partners.

Apparently primates (and other animals) often behave for the benefit of another individual. For example, they groom and help each other during fights. The evolution of cooperation has been an important topic of research for the last 50 years, because it is not immediately obvious how natural selection could favour such cooperative behaviours. Scientists have devised several possible explanations for the evolution of cooperative behaviours. In this research area one of the most controversial topics is reciprocity, the basic idea being that apparently altruistic behaviours can be favoured by natural selection if animals can switch the roles and return the favour.

Although appealing, this hypothesis was criticized because of the lack of convincing examples and because reciprocity was believed to be too difficult (cognitively speaking) for animals. Over the last ten years, we have addressed these issues using a variety of different approaches. We relied on meta-analyses of published data to show that primates do in fact reciprocate one of their most common cooperative behaviour, grooming, and also exchange it for help during fights. We carried out naturalistic observations and experiments, followed by detailed analyses of the time frame of the reciprocation of various cooperative behaviours (grooming, coalitions, tolerance over food sources) to show that monkeys are able to reciprocate previously received favours over an extended period of time. Finally, we carried out several experiments exploring the emotional consequences of receiving cooperative and uncooperative interactions and testing the cognitive basis of reciprocity.

In primates, and probably in other animals, the choice of a preferred partner seems to be based on the emotional and social bond that monkeys develop with their group mates. Our studies showed that the cognitive requirements of reciprocity were probably overestimated and that reciprocity can well be based on an emotionally based account of cooperation received. Reciprocity appears to be a widely spread and well-developed phenomenon in primates and in many other animals.

You bully me, but is there someone who bullies you?

When a macaque is attacked by another group companion, he can ask for help using specific types of behaviour and vocalizations. But who should he ask? If the macaque is keen, he will ask for help neither a subordinate nor a kin of his opponent. That is it. Macaques, indeed, do understand the social relationships that link toghether other individuals.

We, human scientists, commonly describe the social organization of primates in terms of hierarchies of dominance (who bullies who) and of kinship (who is a relative of whom). Dominance and kinship are in fact believed to be two main pillars of primate societies. Although we have known for decades that dominance hierarchies and kinship are the main determinants of primate social relationships, there is still a question to answer: “what monkeys know about social relationships?”.

In principle, we can imagine two possibilities: first, monkeys could have a “self-centred” view of their social world, knowing only who is dominant (or subordinate) to them, or who are their own kin, but would have no idea of the social relationships that link the other individuals. Second, monkeys could have an “objective” view of their social world, and be aware that also the other individuals have their own kin and their own dominance relations. According to the first hypothesis, dominance hierarchies and kinship structures would be unknown to monkeys, which only understand their personal social relationships. According to the second hypothesis, monkeys would have some form of mental representation of the social structure of the group they live in. Given that we cannot ask the monkeys directly, these are hypotheses that are not easy to test. We took advantage of the recruitment behaviour of Japanese macaques, to try to understand what they know about social relationships.

When a macaque is attacked by a group companion, it can “ask for help” using specific types of behaviour and vocalizations. Who a macaque asks for help informs us about its ability to recognize the dominance and kin relations of its companions. In fact, if a macaque knows the dominance and kin relations of its group companions, then it should ask for help individuals that are dominant over their opponent (in contrast to being simply dominant to themselves) and individuals that are not the kin of their opponent. Japanese macaques did follow these rules in recruiting their allies, thus showing in this way, that they have an “objective” view of their social world and some understanding of the social relationships that link other individuals.

In later studies, we also showed that monkeys are very interested in observing the social interactions of their group mates, that they build their extensive social knowledge by observing others, and that those individuals having the best social knowledge also acquire a definite social advantage.

Cooperation in solving a task: I know you might help me, but I do not know precisely how

In order to get a food reward, two capuchins have to simultaneously pull two handles.Do they succeed in teamwork and do they learn to coordinate their action to reach the goal? Not at all. They learn to take into consideration the presence of the partner by the handle but not his behaviour. But with some help...

O330  COOP - Pippi  Paquita

Figure. Pippi and Paquita solving a cooperation task (Photo by Elisabetta Visalberghi).

A study conducted in our Primate Center investigated capuchin monkeys’ cooperation abilities. A pair of capuchins faced a cooperative task: two monkeys that were free to move in a big cage had to jump on a platform and simultaneously pull two handles to obtain food. It turned out that, to some extent, they learn to take into consideration the presence of the partner by the handle but not the partner’s behaviour. When a monkey saw the other one coming on the platform, it pulled the handle more often when the other monkey was getting near the handle itself (although it didn't programmaticly pull the handle at the same time the other monkey did. It is important to underline that both of them were still willing to pull the handle even if their partner was no longer on the platform. This experiment suggested that capuchins’ success didn't rely on understanding the role of the partner.

When the experimental paradigm was slightly modified, capuchins started to achieve some success. In a study of Mendres and de Waal (2000), capuchins faced the same task but with some differences: they were housed in a smaller cage where they weren't free to move; when only one of them pulled the handl, it weighted more than when they pulled it toghether; if one individual pulled for some seconds and the other joined after a while, then they both were successful. These kinaesthetic information proved to be essential for capuchins’ understanding of each other role in a cooperative task. Probably then, the duration and the multimodal nature of the feedback that each actor gets from partecipating in a cooperative task, improve monkeys learning ability.

Conflict management: capuchin monkeys use grooming as a declaration of peace

Capuchin monkeys have a peaceful way to prevent conflicts that may arise in stressful situations such as feeding competition: they groom each other. Indeed, they make grooming, not war.

grooming ritagliato per sito

Figure. Grooming in a group of Sapajus libidinosus (left; photo Noemi Spagnoletti) and Sapajus nigritus (right; photo Brandon Wheeler)

Conflict management represents an important set of mechanisms that help group-living animals to cope with the negative effects of competition and to maintain the benefits of group life. We investigated conflict management in capuchin monkeys, both in captivity and in the wild, by combining the study of conflict prevention and of post-conflict resolution. In this way, we showed that these two sets of mechanisms are both part of the behavioral repertoire of primates.

These studies showed that capuchin monkeys are able to manage the negative consequences of impending feeding competition using grooming as an efficient instrument of conflict prevention. Nevertheless, when aggression did occur, capuchin monkeys coped with its negative consequences by reconciling with their former opponent, and such reconciliation successfully reduced post-conflict anxiety. Also, by experimentally manipulating the visibility between neighboring groups, we showed that, contrary to expectations, hostility between groups did not result in increased group cohesion (to deal with the external threat), but in contrast translated into increased within-group aggression and tension. 

A poster showing results of the experiment on visibility (in italian)

Conflict management: the complex consequences of aggression in mandrills

In mandrills, aggression is not a dyadic affair. When two mandrills have a fight, the consequences can spread across the group and involve multiple individuals. 

Other studies on conflict management focused on mandrills. After a fight, mandrills used different behavioral patterns to reconcile depending on the identity of their former opponent and the risk of approaching it. They used grooming to reconcile with their kin and visual signals exchanged from a distance to attain reconciliation with those opponents that most frequently renew their aggression. Mandrills seem therefore to be aware of the danger that the group mates represent for them and behave accordingly.

On receiving aggression, mandrills often "redirect" this aggression to another individual, that is, they attack others. We showed that group mates can approach and exchange friendly behaviors with victims of aggression in order to prevent being the target of this redirected aggression. We also discovered that redirected aggression is often targeted at the relatives of the original aggression. In this way, mandrills can "punish" their aggressors and prevent further aggression.

Overall, mandrills seem to have a rather complex set of behaviors used to manage and resolve their conflicts. 

Reciprocity in primates: do unto others as you would have them do unto you

Primates have a long memory. If someone do somebody else a favour, the latter will remember it, and return the favour over extended periods.This reciprocation works better if the monkeys are emotionally involved with their partners.

Apparentely primates (and other animals) often behave for the benefit of another individual. For example, they groom and help each other during fights. The evolution of cooperation has been an important topic of research for the last 50 years, because it is not immediately obvious how natural selection could favour such cooperative behaviours. Scientists have devised several possible explanations for the evolution of cooperative behaviours. In this research area one of the most controversial topics is reciprocity, the basic idea being that apparently altruistic behaviours can be favoured by natural selection if animals can switch the roles and return the favour.

Although appealing, this hypothesis was criticized because of the lack of convincing examples and because reciprocity was believed to be too difficult (cognitively speaking) for animals. Over the last ten years, we have addressed these issues using a variety of different approaches. We relied on meta-analyses of published data to show that primates do in fact reciprocate one of their most common cooperative behaviour, grooming, and also exchange it for help during fights. We carried out naturalistic observations and experiments, followed by detailed analyses of the time frame of the reciprocation of various cooperative behaviours (grooming, coalitions, tolerance over food sources) to show that monkeys are able to reciprocate previously received favours over an extended period of time. The choice of a preferred partner is probably based on the emotional and social bond that monkeys develop with their group mates. Our studies showed that the cognitive requirements of reciprocity were probably overestimated and that reciprocity can well be based on an emotionally based account of cooperation received. Reciprocity appears to be a widely spread and well developed phenomenon in primates and in many other animals. 

You bully me, but is there someone who bullies you?

When a macaque is attacked by another group companion, he can ask for help using specific types of behaviour and vocalizations. But who should he ask? If the macaque is keen, he will ask for help neither a subordinate nor a kin of his opponent. That is it. Macaques, indeed, do understand the social relationships that link toghether other individuals.

We, human scientists, commonly describe the social organization of primates in terms of hierarchies of dominance (who bullies who) and of kinship (who is a relative of whom). Dominance and kinship are in fact believed to be two main pillars of primate societies. Although we have known for decades that dominance hierarchies and kinship are the main determinants of primate social relationships, there is still a question to answer: “what monkeys know about social relationships?”.

In principle, we can imagine two possibilities: first, monkeys could have a “self-centred” view of their social world, knowing only who is dominant (or subordinate) to them, or who are their own kin, but would have no idea of the social relationships that link the other individuals. Second, monkeys could have an “objective” view of their social world, and be aware that also the other individuals have their own kin and their own dominance relations. According to the first hypothesis, dominance hierarchies and kinship structures would be unknown to monkeys, which only understand their personal social relationships. According to the second hypothesis, monkeys would have some form of mental representation of the social structure of the group they live in. Given that we cannot ask the monkeys directly, these are hypotheses that can't be easily tested. We took advantage of the recruitment behaviour of Japanese macaques, to try to understand what they know about social relationships.

When a macaque is attacked by a group companion, it can “ask for help” using specific types of behaviour and vocalizations. Who a macaque asks for help informs us about its ability to recognize the dominance and kin relations of its companions. In fact, if a macaque knows the dominance and kin relations of its group companions, then it should ask for help individuals that are dominant over their opponent (in contrast to being simply dominant to themselves) and individuals that are not the kin of their opponent. Japanese macaques did follow these rules in recruiting their allies, thus showing in this way, that they have an “objective” view of their social world and some understanding of the social relationships that link other individuals.

If you care, yawn me back!

Contagious yawning is a signal of empathy. Look for “contagion” in humans and gelada baboons and you will find that it is not a matter of spatial proximity, age or sex…what matters is social bonding. Friends yawn together more than strangers!

sbadiglio contagioso per sito

Figure. (From Left to right) Yawn in ring-tailed lemur (photo Elisabetta Palagi), sifaka (photo Ivan Norcia) and in gelada baboon (photo Elisabetta Palagi)

The emotions, or the empathy for other individuals, is crucial for complex social interactions. It was suggested that yawn contagion in humans (homo sapiens) is related to our emphatic capacities. We run a study to find out the effect of different variables (e.g., country of origin, sex, yawn characteristics) on yawn contagion. Overall, the results demonstrated that yawn contagion is affected primarily by the emotional closeness between individuals (the rate of contagion was greatest in response to a kin, then friends, then acquaintances, and at last strangers), while it is not affected by other variables, such as gender and nationality. 

It is presently unclear whether this capacity is uniquely human or if we share it with other primates, especially monkeys. Recently, we discovered that in gelada baboons (Theropithecus gelada) yawning is contagious between individuals, especially those that are socially close, as it occurs in humans. In particular, we found that the contagiousness of yawning is correlated to the level of grooming. This indicaties that, it is the emotional proximity rather the spatial proximity, that mainly affects yawn contagion in this particular species of baboons. Adult females, which represent the core of the geladas’ groups, have an enhanced sensitivity and emotional tuning toward companions. In fact, adult females showed a precise matching of different yawning types, suggesting the existence of a mirror mechanism that activates shared representations at a neural level. All these findings support the idea that contagious yawning reveals an emotional connection between individuals. This phenomenon, here demonstrated in monkeys, could be a building block for a full-blown empathy. 

In play we trust!

Playing and grooming: such different types of behaviour for the same purpose. As for grooming in capuchin monkeys, in fact, bonobos, gorillas and chimpanzees play to prevent conflict and favour a peaceful resolution of stressful situations.

sequenza gioco gorilla by elisabetta palagi per sito

Figure. Sequence of play in captive gorilla (photo Elisabetta Palagi)

Playing behaviour is an ontogenetic trait in many mammalian species and it is widely believed to have an important role in the assembly of adult behaviour. However, play may be at work also during some peculiar situations that favour cohesion and social manipulation. We demonstrated that in bonobos, chimpanzees, and gorillas social play increases around feeding time and, as it occurs for grooming in capuchin monkeys, play is a good tool to limit the probability of aggression and to favour a peaceful co-feeding. 

Another topic of research focuses on the study of the ontogenic playing trajectories of chimpanzees in comparison with humans. Chimpanzee play, both solitary and social, shows many changes from infancy to juvenility. While solitary play peaks during infancy, social play does not show any quantitative variation between infancy and juvenility but shows a strong qualitative variation regarding the complexity, asymmetry, and playmate choice. The playful expressions in chimpanzees (that vary troughout the different age phases) seem to have a role in advertising cooperative dispositions and intentions (like laughter in humans) thus increasing the possibility of engaging in solid social relationships. In chimpanzees, as in humans, both playing behaviour and the signals that accompany it serve multiple functions according to the different age phases. 

Capuchins’ facial displays

Robinia, a female capuchin, looks in your eyes raising her eyebrows and forehead. What is she doing? She is trying to court you while displaying her most gorgeous scalp lift! Capuchins, indeed, are among the monkey species with the richest repertoire of facial displays.

facial display per sito

Figure. (Left) Relaxed open-mouth, in which the upper tooth rows remained covered by the upper lips, is performed during play interactions. (Right) Silent bared-teeth is used by capuchins during affiliative contexts as well as to signal submission to the dominant (drawings by Arianna De Marco).

Facial displays are important for communication, and their ontogeny has been studied primarily in humans, chimpanzees and macaques. We investigated the ontogeny, communicative function and target of facial displays in two species of capuchin monkeys: the tufted capuchins (Cebus apella) and the white-faced capuchins (Cebus capucinus). In Cebus apella facial displays are absent at birth and develop as infants grow older. Lip-smacking (which is associated with an affiliative type of behaviour both when performed and received by a young capuchin) appears at about 1 month of age, followed by scalp-lifting (affiliative behaviour), relaxed open-mouth (affiliative and playing behaviours), silent bared-teeth (affiliative behaviour), open-mouth silent bared-teeth displays (playing, affiliative and submissive behaviours) and finally the open-mouth threat face (agonistic behaviour). All these facial displays are reciprocated except the agonistic one. Infants of tufted capuchin perform most facial displays in the same contexts of the adults, with an exception for the silent bared-teeth display that youngsters use primarily, or exclusively, in affiliative contexts. Interestingly, facial displays are exchanged very often with peers, less frequently with the adults and almost never with the mother.

Research on the white-faced capuchins, was carried out in the Primate Centre of the Louis Pasteur University of Strasbourg, in France. We recorded both facial displays commonly used by the tufted capuchin (such as relaxed open-mouth, lip-smacking, open-mouth threat-face, silent bared teeth and open-mouth silent bared-teeth) and new ones as the protruded-lip face and the tongue-out. Surprisingly, researchers never observed the scalp-lifting display, one of the most common displays characterizing tufted capuchins. Generally, facial displays have the same communicative functions in both species. But there are some differences. For example, while in the tufted capuchin the silent bared-teeth indicates submission as well as affiliation, in the with-faced capuchin conveys only a positive message. Indeed, white-faced capuchins seem to lack of ritualized signals of submission. Morphological and functional variations in the facial displays of different species, are related to the different social-dynamics of the tufted and white-faced capuchins. 

Researchers involved

Dr. Arianna De Marco, Dr. Luciana Massaro, Dr. Elisabetta Palagi, Dr. Eugenia Polizzi di Sorrentino, Dr. Gabriele Schino and Dr. Elisabetta Visalberghi

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