Does behavioral flexibility contribute to successful play among juvenile rhesus macaques?

Abstract

Animal play often resembles aggressive interactions, making it difficult for players and third parties to distinguish between the two types of behavior or to concur on aspects of play. In this sense, social play involves some degree of social risk, and players may benefit by behaving flexibly particularly when playing with unmatched partners. Here, we ask (1) whether social play among free-ranging juvenile rhesus monkeys (Macaca mulatta) is more likely to fail when partners are unmatched by sex, age, rank/kinship, or when their mothers are nearby and (2) whether juveniles behave flexibly to overcome these social risks. We first identify the factors contributing to play failure, by describing social attributes that are associated with negative outcomes of play. We then compare behavior for matched vs. unmatched partners by examining tendencies to (1) refrain from play, (2) engage in short play durations, and (3) use enhanced play signaling. Males were responsive to several play failure factors; they disproportionately used enhanced play signaling and played for short durations with unmatched partners, suggesting that they have social knowledge that supports attempts to cope flexibly with diverse play partners/situations. Females were less actively responsive to these factors. Although they refrained from playing with many unmatched partners, they did not adjust play tactics to the same degree. These sex differences may be related to differences in life histories; males preparing to disperse eventually may benefit from expanding their social networks through play, while philopatric females may have less need to do so. While social play provides many benefits for animals, play attempts may also involve risks of failure, from refusal by partners to escalation into aggression, particularly when players are mismatched physically or socially. Growing juveniles in despotic societies may be especially vulnerable to such risk. We ask whether juvenile rhesus monkeys behave flexibly when playing with mismatched partners in a way that may help them overcome such risks. We demonstrate that males, who typically emigrate from their natal groups, are indeed sensitive to mismatches in social characteristics or situations; they play in short durations and enhance their play signaling during play sessions involving mismatches. Females, who permanently remain in their maternal groups are less responsive. These sex differences suggest that juvenile males may hone social skills via playful interaction in preparation for emigration, while females have less need to do so.