Boys and girls on the playground: sex differences in social development are not stable across early childhood

Sex differences in human social behaviors and abilities have long been a question of public and scientific interest. Females are usually assumed to be more socially oriented and skillful than males. However, despite an extensive literature, the very existence of sex differences remains a matter of discussion while some studies found no sex differences whereas others reported differences that were either congruent or not with gender stereotypes. Moreover, the magnitude, consistency and stability across time of the differences remain an open question, especially during childhood. As play provides an excellent window into children's social development, we investigated whether and how sex differences change in social play across early childhood. Following a cross-sectional design, 164 children aged from 2 to 6 years old, divided into four age groups, were observed during outdoor free play at nursery school. We showed that sex differences are not stable over time evidencing a developmental gap between girls and boys. Social and structured forms of play emerge systematically earlier in girls than in boys leading to subsequent sex differences in favor of girls at some ages, successively in associative play at 3-4 years, cooperative play at 4-5 years, and social interactions with peers at 5-6 years. Preschool boys also display more solitary play than preschool girls, especially when young. Nevertheless, while boys catch up and girls move on towards more complex play, sex differences in social play patterns are reversed in favor of boys at the following ages, such as in associative play at 4-5 years and cooperative play at 5-6 years. This developmental perspective contributes to resolve apparent discrepancies between single-snapshot studies. A better understanding of the dynamics of sex differences in typical social development should also provide insights into atypical social developments which exhibit sex differences in prevalence, such as autism.     

Development of Social Behaviour in Four Litters of Dogs (Canis familiaris)

The development of social behaviour in 4 litters of dogs was observed without interfering with the puppies from birth to 8 weeks of age. Direct and continuous observation was combined with video recording. Three of the litters were observed during one session of 2 h once a week, and the fourth litter during one session of 40 min twice a week. Social interactions were divided into 1) investigation of litter mates (licking, sniffing or investigating orally), 2) social play, 3) and interactions in which agonistic elements (dominance postures, threats, bites or submission) were displayed. The different forms of social interactions appeared for the first time when the puppies were between 14 and 21 days of age. Social investigation appeared first and was followed by play and agonistic interactions. From week 5, differences between the puppies in the tendency to initiate social play and agonistic interactions emerged. Generally, within the litters individual differences were consistent over weeks 6-8 (positive correlations between weeks), whereas the tendency in the puppies during these weeks were negatively correlated with those of week 3 (play) or weeks 3 and 4 (agonistic interactions), indicating a rebound effect for both play and agonistic behaviour. No significant correlations, however, were found for social investigation. More often than expected males played or engaged in agonistic with other males, whereas these behaviours occurred less often than expected between females. Both males and females, however, preferred male partners for agonistic interactions. No sex differences were found in the direction of social investigation. Agonistic behaviour was often responded to by play and play was often responded to by agonistic behaviour, and the results indicated that before 8 weeks of age differences in social behaviour between the puppies were already established.     

An investigation of playful behaviour in Rattus norvegicus and Mus musculus (Mammalia)

The playful behaviour of laboratory rats ( Rattus norvegicus ) was investigated in litters of five individuals with the mother present; parallel observations were made on mice ( Mus musculus ). Seven mixed litters containing four young rats and a young mouse fostered at birth were also observed.
Solitary play was recorded in both species and took a similar form but social play was only observed in rats. In rats, solitary play frequently preceeded social play.
The behavioural elements involved in the social play of Rattus norvegicus were described, and the majority of these were the playful equivalent of adult agonistic behaviour elements. These social play elements were found to be organized into definite sequences which differed from those of adult aggression. Each behavioural element was found to act as a social releaser.
Young mice did not respond playfully to social play from a rat litter mate; mice were less attractive to rats as playmates in comparison with fellow rats.     

The social behavior of a marmoset (Saguinus fuscicollis) group II: Behavior patterns and social interaction

The behavioral patterns and social interaction of a marmoset (Saguinus fuscicollis) group in a semi-naturalistic environment were observed for 14 months. The analysis showed that, of the 32 behavior patterns observed, the 10 most frequent accounted for over 97 per cent of the total behavior. One pattern, sit and look, accounted for 44 per cent of the total behavior. The two most frequent social behavior patterns, grooming and social play, were concentrated in different parts of the group. The focal point of grooming was the adult female; social play was characteristic of younger animals 4–20 months of age. These results were compared with other studies of marmosets and with primate studies on grooming and social play.     

Solitary and social play in wild Mus musculus (Mammalia)

Play behaviour was observed in wild caught Mus musculus housed in a semi-natural environment. The behaviour of interest (1) is very exaggerated and jerky in appearance. (2) occurs almost exclusively in highly enriched areas of the observation room, (3) disappears under stressful conditions and (4) occurs primarily in juveniles. Solitary and social play were observed. Aggressive and pouncing play were the two major types of social play seen. Juveniles were found to play with littermates significantly more often than with non-littermates but did not show a significant preference with respect to the sex of their play partners.     

The development of different types of play in gazelles: implications for the nature and functions of play

The development of play behaviour in Cuvier's gazelle, Gazella cuvieri, is described and compared with that of other species. Play was sub-divided into four different types: locomotor play, sexual play, play-fighting and object play. Developmental trends in the types considered were different, supporting the hypothesis that play is a heterogeneous category. Locomotor play started at high frequencies, and accounted for a major proportion of total play, but both measures declined from early months onwards. By contrast, sexual play and play-fighting were infrequent shortly after birth, increased thereafter reaching peaks between 4 and 6 months, and then decreased. The relative importance of these play types steadily increased until they became the predominant types of play. Object play remained infrequent at all ages, and accounted for a small proportion of total play. Young calves played mostly alone, but the proportion of social play increased with age, until all play became social. Before month 4 calves directed more invitations to play and sexual play than they received. Other peers were the major play partners of calves, followed by adult females. Calves directed a higher proportion of invitations and sexual play to adult females and males than they received from either class. These results are discussed in relation to other aspects of the calves' behavioural and social development, and it is argued that they are best explained if play is considered to have immediate benefits.     

Neonatal androgens influence the social play of prepubescent rats

The results of six experiments designed to investigate the hormonal basis of the sex differences in the occurrence of social play in the rat are reported. From the time of weaning animals were housed in mixed-sex, peer groups of six, composed of some treated and some untreated animals. Observations were made of the animals in these groups each day between Days 26 and 40 of life in Experiments 1, 3–6 and between Days 31 and 40 in Experiment 2. In Experiment 1 it was found that males castrated on Day 1 of life engaged in less social play than did intact males, and did not differ from normal females. In Experiment 2, castration carried out at 23 days of age had no effects on the frequency with which males engaged in social play. In Experiment 3, it was found that neonatal ovariectomy had no effect on the frequency with which female pups engaged in social play. In Experiment 4, females treated on Days 1 and 2 of life with either 250 μg of testosterone propionate or 250 μg of dihydrotestosterone engaged in social play at rates comparable to those of normal males, whereas treatment with 5 μg of estradiol benzoate had no such effect. In Experiments 5 and 6 it was found that neither the reduction of testosterone-derived estradiol (by implants of the aromatization blocker, androst-1,4,6-triene-3,17-dione) nor that of testosterone-derived dihydrotestosterone (by implants of the 5α-reductase blocker, testosterone 17β-carboxylic acid) during the early neonatal period (Days 1 to 10 of life) changed the frequency of social play in intact males. The results of these experiments indicate that the sex difference in the social play of prepubescent rats is dependent on the neonatal exposure to testosterone or to its 5α-reduced metabolite, dihydrotestosterone. The reduction of testosterone to dihydrotestosterone, however, would not appear to be a necessary step.     

Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): Implications for natural social systems and interindividual relationships

This study compares adult play behavior in the two Pan species in order to test the effects of phylogenetic closeness and the nature of social systems on play distribution. The social play (both with fertile and immature subjects) performed by adults did not differ between the two species. In contrast, in bonobos, play levels among fertile subjects were higher than in chimpanzees. Findings regarding levels of undecided conflicts (more frequent in bonobos) and formal submission displays (lacking in bonobos) confirm, in the two colonies under study, that bonobos exhibit "egalitarianism" more than chimpanzees. Some authors emphasized the importance of play-fighting for social assessment when relationships among individuals are not codified and structured according to rank-rules. Indeed, adult bonobos played more roughly than chimpanzees. Moreover, adult bonobos displayed the full play-face at a high frequency especially during rough play sessions, whereas in chimpanzees, the frequency of play signals was not affected by roughness of play. The frequency of social play among bonobo females was higher than in any other sex combinations, whereas no difference was found for chimpanzees. As a matter of fact, social play can be viewed as a balance between cooperation and competition. Among bonobo females, characterized by social competence and affiliation, social play might enhance their behavioral flexibility and increase their socially symmetrical relationships which, after all, are the basis for their egalitarian society.     

Social object play among young Japanese macaques (Macaca fuscata) in Arashiyama, Japan

Social object play (SOP), i.e., social play using portable object(s), among young Japanese macaques (Macaca fuscata; 0-4 years old) in the Arashiyama E troop was studied using a modified sequence sampling method from July to October 2000. SOP was a relatively common activity for most of the young macaques and often continued for long periods. Participants used many kinds of object, including edible natural objects and artificial objects, such as plastic bottles, but they never used provisioned food or wild fruit in SOP bouts. An analysis of long bouts (>/=0.5 min) revealed the following interactive SOP features: (1) at any given time, participants used only one object, and only one participant held the object; (2) during SOP play-chasing, the object holder was likely to be chased by others; (3) during long bouts, the object changed hands frequently; and (4) agonistic competition for an object among young macaques was rare. Combinations of sexes, ages, relative ranks, or matrilines of the object holder and non-holder did not affect the tendency that the holder was chased by non-holder(s) during play-chasing. Even when there was a change in object holders, the repetitiveness of this interactive pattern, i.e., that the holder would be chased during SOP bouts, distinguished the SOP structure from that of other types of social play without object(s). General proximate social play mechanisms, such as self-handicapping or role taking, were associated with SOP. Other mechanisms that affected SOP included the following: (1) young macaques treated an object as a target in play competition, and (2) 'being the holder of a target object' was associated with the 'role of the chasee.'     

The ontogeny of social play in a feral troop of vervet monkeys (Cercopithecus aethiops sabaeus): The function of early play

We describe the ontogeny of social play over the first 30 weeks of age in a troop of feral vervet monkeys (Cercopithecus aethiops sabaeus) in Barbados. Play time increased rapidly for the first 10 weeks but remained relatively constant thereafter. The form of play changed with infant age; bouts became more frequent but of shorter duration. Play time, bout frequency, and bout duration at a given age differed between infants; younger infants altered their play patterns to complement those of older infants. All infants played more within their own year class than with older juveniles; play time increased with decreasing age difference between the infant and the play partner. Infants terminated a higher proportion of their play bouts the greater the age difference between themselves and their play partners. Preferred play partners are therefore individuals of similar age that will be similar in size and have matched motivation to play and form of play. Neither play time nor proportion of bouts initiated or terminated was correlated with the social rank of the play partner, which suggests that play is not directed toward individuals that may be high-value alliance partners. Maternal intervention in play occurred primarily when infants were<10 weeks old. It was not correlated with the age or social rank of the mother or with the age or social rank of her infant's play partner. Infants played more and terminated a lower proportion of their play bouts in the absence of their mothers than in their presence. Our results are consistent with the hypothesis that the primary function of early play is to enhance physical fitness and to develop coordination and other fighting skills, with minimal risk of injury.     

Play in adult bonobos (Pan paniscus): modality and potential meaning

The aim of this study was to thoroughly investigate social play and its modalities among adult bonobos. We evaluated how play intensity varies according to the sex-class combination of the playmates and we also performed an analysis on social locomotor-rotational movements (L-R play) and contact interactions (C play). Rough and gentle play sessions were performed with comparable frequencies by male-female and female-female adult dyads, with play signals unlikely when the playmates strongly differed in age and in rank position. L-R play rates did not differ according to the sex-combination of the players; in contrast, C play sessions were particularly frequent among females. Play faces (play signals) were significantly higher during C play than L-R play sessions, thus suggesting that playmates assess reciprocally yet safely their relationships by using facial displays to avoid any kind of misunderstanding. Play was positively correlated with grooming and contact sitting interactions, suggesting that it may be used as a social enhancer. Finally, we found no correlation between both play contexts (L-R and C play) and age, size and rank differences of the players. In conclusion, we suggest that bonobos with their egalitarian society, peculiar social structure, and playful tendency represent an attractive testing subject to examine empirically many emerging hypotheses on adult play behavior.     

Adult–Adult Play in Primates: Comparative Analyses of its Origin, Distribution and Evolution

Comparative analyses were conducted on a data set derived from the literature so as to test several hypotheses which were developed to explain the distribution of adult–adult play fighting within the order primates. Ratings for play occurring in sexual and non‐sexual contexts were developed. Three hypotheses were evaluated: (i) that play occurring in non‐sexual social contexts is a byproduct of its use in sex; (ii) that the occurrence of play is related to its use for social assessment and manipulation, and so is more likely to be present in species with reduced familiarity between individuals; and (iii) that phylogenetic affiliation influences the likelihood that species within clades engage in play. We used independent contrasts to test the first two hypotheses, and both were significant, with the presence of play in sexual contexts accounting for 14–16% of the variance of play in non‐sexual contexts, and reduced social familiarity accounting for 30–40% of the variance in the occurrence of play in non‐sexual contexts. To test the third hypothesis, we mapped the occurrence of both types of play onto known phylogenies. The overlap was not congruent, indicating that phylogenetic relationships did not account for the distribution of play. Given that play in both sexual and non‐sexual contexts was more likely to occur in species with a social organization involving reduced frequency of contact between the sexes and other social group members, we suggest that the likely adaptive value of play fighting is as a tool for social assessment and manipulation. The possible factors that mitigate the use of play fighting for these purposes, such as the availability of other forms of communication that could serve similar functions, are discussed.     

The Development of Play in the South American Fur Seal

Play behaviour in the juvenile South American fur seal (Arctocephalus australis) is described for the period of dependence on the mother (up to 32 months). Play does not appear to be a unitary category of behaviour, but may be separated into four distinct types: terrestrial social and solitary play and swimming social and solitary play. These four types show different development profiles, and appear to serve different functions. Terrestrial solitary play and the two swimming play forms appear to be juvenile specializations, the first to enable very young seals to gain motor skills rapidly in order to avoid dangers from conspecifics, the second two to enhance antipredator behaviour and foraging ability during the gradual transition to independence. In contrast, social play may be best thought of as gaining social skills necessary in adult life, prior to dispersal post-weaning. Juvenile fur seals which do not wean in their first year show an upsurge in social play which is not seen in the other play types. This upsurge coincides temporally with the peak of social play of the new cohort, and is presumably elicited by them.     

Coevolutionary relationship between striatum size and social play in nonhuman primates

The striatum is a region of the brain specifically tied to the experience and anticipation of pleasure, reward, appropriate behavioral sequencing, cognition, learning, and social modulation. Furthermore, the striatum is connected neurologically and functionally to other brain regions associated with the exhibition of social play, such as the neocortex, cerebellum, and limbic system. For these reasons, the striatum is especially interesting to researchers of play behavior. Moreover, the caudate-putamen area of the striatum has been specifically implicated in laboratory studies of social play behavior. This study uses the phylogenetic comparative method of independent contrasts to test for an evolutionary relationship between striatum volume and a measure of social play in nonhuman primates. Relative volume of the primate striatum correlates with rate of social, but not nonsocial, play behavior across species, suggesting a coevolution of traits. The pleasurable and procedural aspects of social play behavior may be mediated in part by the striatum and further to its connection to dopaminergic pathways in the primate brain.     

The Right Time to Happen: Play Developmental Divergence in the Two Pan Species

Bonobos, compared to chimpanzees, are highly motivated to play as adults. Therefore, it is interesting to compare the two species at earlier developmental stages to determine how and when these differences arise. We measured and compared some play parameters between the two species including frequency, number of partners (solitary, dyadic, and polyadic play), session length, and escalation into overt aggression. Since solitary play has a role in developing cognitive and physical skills, it is not surprising that chimpanzees and bonobos share similar developmental trajectories in the motivation to engage in this activity. The striking divergence in play developmental pathways emerged for social play. Infants of the two species showed comparable social play levels, which began to diverge during the juvenile period, a ‘timing hotspot’ for play development. Compared to chimpanzees, social play sessions in juvenile bonobos escalated less frequently into overt aggression, lasted longer, and frequently involved more than two partners concurrently (polyadic play). In this view, play fighting in juvenile bonobos seems to maintain a cooperative mood, whereas in juvenile chimpanzees it acquires more competitive elements. The retention of juvenile traits into adulthood typical of bonobos can be due to a developmental delay in social inhibition. Our findings show that the divergence of play ontogenetic pathways between the two Pan species and the relative emergence of play neotenic traits in bonobos can be detected before individuals reach sexual maturity. The high play motivation showed by adult bonobos compared to chimpanzees is probably the result of a long developmental process, rooted in the delicate transitional phase, which leads subjects from infancy to juvenility.     

Social Play in the American Black Bear: Its Similarity to Canid Social Play and an Examination of its Identifying Characteristics

Bears evolved from a canid stock at quite a recent date (earlyMiocene). Despite this recent origin, bcars show substantialmorphological, physiologicai, and ecological differences whencompared to modern day canids. However, the display behaviorsof Canidae and Ursidae have remained remarkably similar. Inthis paper, the motor patterns of black bear social play aredescribed in detail. Numerous similarities between canid andursid social play are pointed out. Agonistic displays commonto both families are also pointed out. These behavioral similaritiessupport the principle that social behavior, particularly displaybehavior, will frequently be conservative in its evolution ascompared to the evolution of morphology, anatomy, or ecologicaladaptations. Beach (1945) stressed the importance of identifying and testingthe general characteristics of play. A large number of characteristicshave been suggested as being diagnostic of play, but these characteristicshave received very little testing. Five characteristics of socialplay were tested in this study, and two were found to be onlypartially valid for black bear social play. Extensive testingof the general characteristics of play on as wide a range ofspecies as possible is definitely recommended for future research.     

Monkeys (Macaca mulatta) raised only with peers. A pilot study

Four infant rhesus raised in a group (4-TT) and six raised in pairs (2-TT) were compared with eight infants raised on mother surrogates (SP) and twenty raised with real mothers (MP). When tested with peers early in life 4-TT and 2-TT subjects showed less play, hostility and sex, and the 2-TT subjects exhibited a preponderance of social cling. When tested as adults the 2-TT and 4-TT monkeys were below controls on measures of play, above controls on social proximity, hostility, and withdrawal, and the 2-TT subjects showed inadequate sexual adjustment. Data are interpreted as suggesting that behaviours normally associated with affectional ties can become so extreme as to inhibit normal social development.     

Exploration and Social Play in Squirrel Monkeys (Saimiri)

Squirrel monkeys (Saimiri) have been studied in a variety oflaboratory and natural environments. The frequency and formof exploration and social play vary considerably among differentenvironments. For example, in some environments, young monkeyshave been observed to play for 3 hr per day; but in one naturalenvironment, not a single bout of social play was seen duringa 10-week intensive study. Numerous intermediate levels of playactivity have been observed. Whereas many theories of play make it appear that play is essentialfor the development of sexual behavior, integrated roles introop structure, control of aggressive responses, social cohesion,etc., the data on squirrel monkeys indicate that social organizationand many normal social behaviors can develop without socialplay. However, the opportunity to play socially provides learningexperiences that increase the variety of each animal's behavioralrepertoire and the subtly of social cues to which it can respond.An adaptive modicum of competence can appear without socialplay, but the opportunity to play socially develops the competenceof animals beyond that modicum.     

灵长类社会玩耍的行为模式、影响因素及其功能风险

社会玩耍是指两个或两个以上个体共同参与的一种互作性玩耍行为,个体间的行为彼此适应并相互影响。社会玩耍行为在灵长类物种的社会交往过程中普遍发生,作为未成年个体一种重要的发育行为,其对个体的生存技能和成年后的繁殖成功具有重要影响。灵长类物种的社会玩耍不仅仅表现为追逐、摔跤、跳跃等一些常见行为,部分物种还发展出自己特有的行为。一般而言,社会玩耍在婴儿后期和青少年早期的发生频率最高,然后随着年龄增长直到成年时期,这类行为的平均发生频率将逐渐下降。未成年雄性个体要比同年龄段的雌性个体更喜欢玩耍,但常因物种、研究对象年龄等因素表现不同甚至相反;很多物种的个体喜欢与有亲缘关系的个体玩耍,或者与性别相同、年龄相仿、等级相近的个体玩耍。总之,非人灵长类个体社会玩耍的发育不但受环境参量如食物、场地等的影响,而且还与个体的年龄、性别、等级、亲缘关系等社群因素紧密相关。未成年个体在玩耍过程中,获得了身体机能的快速发育、完善了生存技能、建立了个体间的友好关系、增强了认识自身及适应周围环境的能力,从而为顺利过渡到成年期和履行自己的职能打好基础,但有时却需要承担玩耍过程中受伤甚至死亡的风险。玩耍作为灵长类社会的一种行为文化,对其研究有助于对人类自身行为进化的不断认识,相信这方面的理论将会得到后来者的不断创新和丰富,也期望这方面的理念及经验能被及时运用到保护繁育等实践活动中。