Social play, a widespread phenomenon in mammals, is a multifunctional behavior, which can have many different roles according to species, sex, age, relationship quality between playmates, group membership, context, and habitat. Play joins and cuts across a variety of disciplines leading directly to inquiries relating to individual developmental changes and species adaptation, thus the importance of comparative studies appears evident. Here, we aim at proposing a possible ontogenetic pathway of chimpanzee play (Pan troglodytes) and contrast our data with those of human play. Chimpanzee play shows a number of changes from infancy to juvenility. Particularly, solitary and social play follows different developmental trajectories. While solitary play peaks in infancy, social play does not show any quantitative variation between infancy and juvenility but shows a strong qualitative variation in complexity, asymmetry, and playmate choice. Like laughter in humans, the playful expressions in chimpanzees (at the different age phases) seem to have a role in advertising cooperative dispositions and intentions thus increasing the likelihood of engaging in solid social relationships. In conclusion, in chimpanzees, as in humans, both play behavior and the signals that accompany play serve multiple functions according to the different age phases.
Citation: Cordoni G, Palagi E (2011) Ontogenetic Trajectories of Chimpanzee Social Play: Similarities with Humans. PLoS ONE 6(11): e27344. doi:10.1371/journal.pone.0027344
Editor: Andrew Iwaniuk, University of Lethbridge, Canada
Received: August 31, 2011; Accepted: October 13, 2011; Published: November 16, 2011
Copyright: © 2011 Cordoni, Palagi. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: The authors would like to thank University of Pisa, which hosts the research (computer use and permitting an employer, the corresponding author, to perform the research). ZooParc de Beauval and Dierenpark Amersfoort offered some free meals to the observers and a car from the B&B to the zoo and vice versa. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: ZooParc de Beauval and Dierenpark Amersfoort were funders of this study. This does not alter the authors' adherence to all the PLoS ONE policies on sharing data and materials.
Due to its multifunctional and complex nature, play is one of the most difficult behaviors to study –. Play apparently is difficult to define and definitions vary widely among researchers. For instance, in humans, there is considerable confusion surrounding the definition of play. In fact, in the child development literature, a variety of children's social and non-social behaviors are grouped under the term “play” . For clarity, in this paper we will use ethological and sociobiological definition of play , , .
Ethologists and sociobiologists often define play as all activity, which has no clear, immediate benefits. Frequently, play seems to involve an array of motor patterns, both typical of serious functional contexts (e.g. agonistic, antipredatory, and mating behavior) – as well as playful actions . However, the main difference between playful and serious contexts is not in the actual behavioral patterns, but how they are performed , . Burghardt  listed five criteria that a behavior must follow to be considered play; a playful behavior must be incompletely functional, rewarding/voluntary, structurally or temporally modified, performed in a repeated manner, and initiated in a relaxed context .
Physical activity play is one of the most common forms of play. It typically implies locomotor-rotational/acrobatic (LR-play) patterns that can be carried out both solitarily and socially. Rough and tumble play (R&T), is characterized by fighting elements (performed in non-serious way), which involve more than one player –. Here, we focus on social, physical activity involving both LR-play and R&T.
Social play is widespread in mammals . This behavior has different functions according to species, sex, age, relationship quality between playmates, group membership, context, and habitat –. Clearly then, play joins and cuts across a variety of disciplines. It leads directly to inquiries connecting individual development with species adaptation. It is not surprising that comparative studies of play behavior can make contributions to a wide variety of fields .
Social play is a fundamental component of the behavioral repertoire of the youngsters of many species of mammals, including humans, and its developmental trajectories (onset, peak, and offset) have evolved in concert with the extension of the immaturity period , –. Social play is first experienced between mother and offspring. Many good examples come from human and non-human primates , . Peek-a-boo, a typical mother-child game, also occurs in the great apes as do other locomotor activities that involve bouncing, throwing, and swinging infants . Interactions with their mothers represent for infants a good starting-point to learn how to manage play sessions (fine-tuning) that will later be transferred and fully developed in peer-peer interactions , , . The quality and quantity of mother-infant play seem to predict the quality and frequency of infants' play with peers , . However, peer-peer play can remediate deficits in mother-infant play and contribute sufficiently to normal social development in monkeys , great apes , and children –. This suggests that infant-infant play is important for acquiring social competence and developing affinitive bonds.
Primate social play in older immature subjects also functions to establish a dominance order among individuals. Individuals acquire information on the strength and weakness of group members by engaging in R&T (humans , ; chimpanzees, ).
In chimpanzees social play serves different functions at different ages (Hypothesis 1) , , , . According to Hypothesis 1, chimpanzee play should vary in modality (e.g. asymmetry in R&T, competition), complexity (variability in the play patterns used), selectivity of playmates (e.g. age selectivity), and frequency as a function of individual age classes (Prediction 1).
One of the most important reasons for studying play in chimpanzees is to shed light on the biological roots of human behavior. Due to their phylogenetic closeness and prolonged immaturity phase , , , , chimpanzees and humans have similar developmental pathways for play (Hypothesis 2). Accordingly, both species should show similar play parameters (e.g., modality, complexity, selectivity of playmates, and frequency) across age-classes (Prediction 2).
Specific facial displays (the relaxed open-mouth display or play face is usually associated with pant-like vocalizations) often accompany play sessions , ,  In primate species, facial displays are a fundamental key for successfully managing play bouts . Playful facial signals have to be considered as an integral part of play behavior development . Great apes perform playful facial displays via two different configurations; play face (PF), where the mouth is open with only the lower teeth exposed, and full play face (FPF), where the mouth is opened with upper and lower teeth exposed. Some authors contend that the two expressions are used differently in relation to the intensity of play , , . In humans, laughter, which is a universal expression , , seems to derive from non-human primate play faces and pant-like vocalization . Recently, an affect-induction hypothesis has been proposed to elucidate the function of human laughter: this expression does not give simple information, but induces a positive influence on the receiver behavior –. Humans and apes smile spontaneously during pleasurable experiences, including visual, auditory, and tactile stimulation. Smiles and play faces, being the expression of positive emotional states, reinforce the behaviors that elicited them in the first place. Such kind of visual reinforcement is essential for learning in infants, when mothers smile at babies to encourage desired behaviors (see – for an extensive review).
Although playful facial configurations can differ across species , they may have a common role in signaling non-agonistic intent to a playmate and/or in expressing emotion even when alone ,  (Hypothesis 3). If in chimpanzees play faces are used in a strategic way and function to signal benign intent, they should vary in frequency, timing, and type (PF & FPF) according to the age of playmates (Prediction 3a). If play faces mainly signal internal emotional states of the player , they should not necessarily vary across the playmates' ages (Prediction 3b).
The present study was carried out on two captive groups of Pan troglodytes hosted at the ZooParc de Beauval (S. Aignan sur Cher, France) and the Dierenpark Amersfoort (Amersfoort, The Netherlands). The Beauval colony was composed of 2 adult males, 8 adult females, 3 juvenile males, 2 juvenile females, 2 infant males and 2 infant females; the Amersfoort colony was made up of 2 adult males, 9 adult females, 2 juvenile females, 2 infant males and 2 infant females (Table 1).
Via focal animal sampling  we collected data on both social and solitary play behavior: Locomotor/Rotational-play (LR-play), Rough&Tumble (R&T), Object play (O-play). See the Methods and Table 2 for the definitions.
Predictions 1 & 2: There should be age-related changes in the frequency and content of chimpanzee play (P1) and strong similarities between chimpanzee and human play development (P2)
Frequency of play
Social play (LR−play+R&T) was significantly more frequent than solitary play (O−play+LR−play) both in infants (I) (Exact Wilcoxon's T = 0, ties = 0, n = 8, P = 0.008) and juveniles (J) (Exact Wilcoxon's T = 0, ties = 0, n = 7, P = 0.016). However, infants performed solitary play more often than juveniles (Exact Mann-Whitney U = 11.0, nI = 8, nJ = 7, P = 0.050); social play did not differ between the two age categories (Exact Mann-Whitney U = 22.5, nI = 8, nJ = 7, P = 0.558) (Figure 1). Solitary play accounted for 29.27%±5.9SE of all play behavior in infants and for 14.45%±5.2SE, in juveniles.
The age of the playmates (see Methods for definition) affected the play invitation (PINV, see Table 2 for definition) distribution (ANOVA randomization F = 3.756, nJJ = 21, nJI = 23, nIJ = 23, nII = 24, P = 0.006) (Figure 2). The post-hoc test revealed the following significant differences: PINVJJ>PINVJI (randomization test for two independent samples t = −2.9, P = 0.005), PINVII>PINVIJ (t = 2.02, P = 0.030), and PINVII>PINVJI (t = 2.50, P = 0.005).
R&T distribution was also affected by the age of playmates (ANOVA randomization F = 17.95, nJJ = 10, nJI = 24, nII = 11, P = 0.000). Post-hoc tests revealed that I-I play levels were significantly higher than those of I-J and J-J (randomization test for two independent samples: J-J vs J-I: t = 0.666, P = 0.518; J-J vs I-I: t = −4.152, P = 0.000; J-I vs I-I: t = 5.077, P = 0.000) (Figure 3). On the other hand, no difference was found in the LR-play distribution according to the age of playmates (ANOVA randomization F = 0.99, nJJ = 10, nJI = 24, nII = 11, P = 0.379). We limited these analyses to those dyads performing at least two play sessions.
We defined an Asymmetry Index (AI) to quantify the level of asymmetry that characterized a play session. The index was defined as the number of unidirectional patterns performed by A minus the number of unidirectional patterns performed by B on the total number of patterns (unidirectional and bidirectional, see Methods for definitions) forming the session (session length). By subtracting the number of unidirectional patterns performed by B from those performed by A, we obtained an estimate of difference between unidirectional patterns which was independent of the length of the play session. However, in order to be more conservative for the calculation of the asymmetry index we considered only the dyads performing at least five play sessions, each one composed of at least ten unidirectional play patterns. For each dyad the median of the index was calculated and entered into the analysis.
The mismatched (I-J) and matched (I-I and J-J) dyads did not differ in the median values of AI (Two independent randomization test t = 0.623, nmismatch = 13, nmatch = 19, P = 0.560).
Focusing on the matched dyads (I-I and J-J), we found that the AI values of play between infants were higher than those between juveniles (Two independent randomization test t = 1.902, nII = 10, nJJ = 9, P = 0.040).
In order to estimate the variability of play patterns forming a single play session we defined the Play Complexity Index (PCI) as the number of different types of play patterns performed by playmates within a single session on the total number of patterns forming that session. To be more conservative, we calculated the PCI by considering only the dyads performing at least five play sessions each one composed by at least ten play patterns (both unidirectional and bidirectional). For each dyad the median of the index was calculated and entered into the analysis.
The PCI differed across the age-class combination (ANOVA randomization F = 10.497, nJJ = 10 dyads, nIJ = 17 dyads, nII = 10 dyads, P = 0.000). Post-hoc tests revealed a significant difference between J-J and I-J dyads (JJ>IJ: two independent randomization test t = −3.534, nJJ = 10 dyads, nIJ = 17 dyads, P = 0.002) and between J-J and I-I dyads (JJ>II: t = −4.156, nII = 10 dyads, nJJ = 10 dyads, P = 0.001); no significant difference was found between I-I and I-J dyads (t = 0.963, nII = 10, nIJ = 17, P = 0.368) (Figure 4).
Solid horizontal lines indicate medians; length of the boxes corresponds to inter-quartile range; thin horizontal lines indicate range of observed values. Only significant results are reported.
Prediction 3a: If in chimpanzees play faces are used in a strategic way and function to signal benign intent, they should vary in frequency, timing, and type (PF & FPF) according to the age of playmates.
Prediction 3b: If play faces mainly signal internal emotional states of the player, they should not necessarily vary across the playmates' ages.
Play signal frequency
Infants and juveniles did not differ in the overall frequency of play signals (PF+FPF per play session) (Exact Mann Whitney U = 26, nI = 8, nJ = 7, P = 0.867). Both infants and juveniles performed more facial displays (PF+FPF per play session) during social rather than solitary play (I, Exact Wilcoxon's T = 0, ties = 0, n = 8, P = 0.008; J, Exact Wilcoxon's T = 1, ties = 0, n = 7, P = 0.03).
Play signal timing
We calculated how many times a playful facial display was performed at the beginning or in the middle of each play session in order to evaluate if the signal was used to initiate or maintain the session. Immature chimpanzees displayed play signals significantly more often to maintain rather than to initiate a social play session (Randomization paired t test: t = 6.715, n = 42, P = 0.000). The result did not change even considering all the possible age-class combinations separately (Randomization paired t test I-I: t = 3.476, nII = 12 dyads, P = 0.000; I-J: t = 4.843, nIJ = 20 dyads, P = 0.000; J-J: t = 5.305, nJJ = 11 dyads, P = 0.003). We entered into the analysis only those sessions formed by at least three play patterns.
Preferential use of different play signals
The Play Signal Index (PSI) was defined to analyze the preferential use of the variants of playful facial displays (PF or FPF) with respect to the total amount of playful facial signals performed. The index was calculated as follows [(PF-FPF)/(PF+FPF)] as suggested by Palagi . The PSI can be either positive or negative depending on the relative amount of facial expressions performed. Values can vary from −1 (only FPF performed) to +1 (only PF performed). If the value of PSI is 0, PF and FPF are performed with the same frequency.
To analyze the use of the variants of playful facial displays (PF and FPF) as a function of the age of the performers, we compared the Play Signal Index (PSI) between infants and juveniles. The PSI did not differ between the two age classes (Exact Mann Whitney U = 23, nI = 8, nJ = 7, P = 0.588; mean infant PSI = 0.32±0.11SE, mean juvenile PSI = 0.33±0.12SE).
Infants directed play signals (PF+FPF per play session) towards peers and juveniles with comparable levels (Exact Wilcoxon's T = 14, ties = 0, n = 8, P = 0.641) (Figure 5a); whereas, juveniles tended to direct play signals towards other juveniles more than towards infants (T = 2, ties = 0, n = 7, P = 0.058) (Figure 5b).
Play signal and play asymmetry
No correlation was found between the median values of playful facial display per play session and the median values of asymmetry index during play session involving mismatched dyads (J-I) (Correlation via randomization r = −0.331; n = 13, P = 0.242). On the contrary, there was a positive correlation between the median values of playful facial display per play session and the median values of asymmetry index during play session involving matched dyads (I-I and J-J) (r = 0.72; n = 19, P = 0.009). Testing the I-I and J-J dyads, separately, we found a significant positive correlation in the former (Correlation via randomization r = 0.735; n = 10, P = 0.042) and no correlation in the latter (r = 0.467; n = 9, P = 0.194).
As it occurs in humans, play in chimpanzees varied according to the age of the players in relation to different parameters such as modality, complexity, selectivity of playmates, and frequency (Prediction 1 and 2 supported, Table 3). Play signals did not vary in terms of frequency, timing and type across the ages of playmates, even though we found interesting results indicating that both infants and juveniles perform playful facial displays in a strategic way (Prediction 3a partially supported). Moreover, we found that playful expressions were performed even when chimpanzees played alone, thus suggesting that PF and FPF may be directly linked to the emotional state of the sender (Prediction 3b supported).
In humans, the three types of physical activity play (rhythmic stereotypies, exercise play, R&T) show three successive peaks, thus reflecting different functions for these different forms of play  (Table 3). Our finding on solitary play is in agreement with data coming from children. Even though parallels across ages of different species have to be taken cautiously, there is a marked overlapping between the percentage of solitary play in infant (29.27%±5.9SE) and juvenile chimpanzees (14.45%±5.2SE) with those of preschoolers (0–3 yrs; 17%–23%) and kindergarten-aged children (3–6 yrs; 17%), respectively – (Prediction 2 supported). Such overlapping seems to disappear when we consider social play. In humans, the transition from solitary to social play occurs during the preschool period ; whereas, in chimpanzees social play constantly covers a wide time-window, from infancy (0–3 years) to juvenility (4–7 years). However, if within social play we consider R&T, there are striking similarities between humans and chimpanzees (Prediction 2 supported). Consistent with our findings, Scott and Panksepp  demonstrated that R&T play is at a plateau until children are at least 7-years old.
Play effectiveness in the development of social skills often means a choice of an appropriate playmate . Even though studies of children's social play rarely focused on the effects of age on partner choice, it seems that human and non-human primates show selectivity for peers, especially in terms of strength/size matching (Prediction 2 supported, see Table 3) , . In humans, for example, this is true also for 9-month-old babies, who show peer preference when they watch movies of same-age infants . In chimpanzees, the selectivity for play partner choice may be evaluated by analyzing the directionality of play invitations. Our data showed that chimpanzees invited peers to play more often than non-peers, thus suggesting a preference to engage in play with matched individuals (Prediction 1 supported). Accordingly, other studies, carried out both in captivity and in the wild, demonstrated that immature chimpanzees tend to play with partners who are closest to themselves in age; for juveniles playing with infants might not have been challenging enough because of their limited motor skills and, on the other hand, for infants playing with juveniles might be too dangerous , .
Infant-infant dyads performed R&T more frequently than infant-juvenile and juvenile-juvenile dyads did (Prediction 1 supported); on the other hand, no difference was found for LR-play. Although, it was difficult to make direct comparisons between chimpanzee and human R&T due to the lack of quantitative data in children across different age stages , , some parallels seem to emerge. As in humans, the functions of R&T in chimpanzees shifted through the different developmental stages (Prediction 2 supported, see Table 3). In infancy, R&T seemed to have a role in socialization and in developing motor and psychological skills , . In juveniles, R&T begins to include competitive elements that will be used by animals to establish social dominance relationships , , . In humans, up to around 11 years, most evidence suggests that the great majority of R&T is purely playful, and that when play fighting does turn into real fighting, this is due to a lack of social skills and not the conscious manipulation that characterizes adolescents' R&T , . Accordingly, Pellegrini  found that adolescent R&T was positively correlated with aggression and negatively correlated with social preference, thus suggesting that R&T could be a sort of training to acquire information on partner's skills; this information will be useful in the future to gain an advantage during real fights.
The asymmetry index of social play sessions seems not to be affected by the size and age of the players; however, when focusing on the matched dyads we found an interesting result. Social play between infants seems to be characterized by a higher degree of asymmetry compared to social play between juveniles (Prediction 1 supported). As play in juveniles is more competitive than in infants, the former have to restrain themselves in order to maintain as much as possible a symmetrical session and to limit the risk of escalation into serious fighting , . Such an interpretation agrees with data on human youngsters, whose play bouts can turn into overt aggression ,  (Prediction 2 supported). The unbalanced play sessions between infants may reflect different degrees of maturity in motor skills and/or the lack of capacity to fine-tune sessions due to difficulties in performing self-handicapping (a playmate, independently from his/her age, puts him/herself into unnecessary disadvantageous positions or situations) ,  and motor inhibition . This conclusion is supported by the lower complexity of infant play sessions characterized by few motor patterns which are highly repeated (see Fig. 4). In this view, the simpler R&T performed by infants could be a sort of training to assemble a more complex and sophisticated form of R&T typical of juvenility (play for play itself) (Prediction 1 supported). When playing with infants, juveniles have to self-handicap, promote reciprocal role-taking, and limit the number of types of patterns used. This capacity, also known as high-level response inhibition, relies on control mechanisms in anterior (in particular prefrontal) cortical areas , . This explains the lack of difference in play complexity recorded between I-I and I-J dyads. The higher complexity level recorded in juvenile dyads suggests that juvenile play is characterized by a greater number of innovative and unpredictable elements, thus indicating the development of novel control mechanisms in the cerebral cortex , . The experience gained by switching between different play patterns may improve behavioral flexibility in chimpanzees in order to cope with unexpected situations (the training for the unexpected theory, ). Some studies on humans correspond to our data; the ability of children to switch activities during R&T was correlated with their capacity to face new social challenges ,  (Prediction 2 supported).
Considering playful signals, infants and juveniles performed facial expressions with comparable frequency to maintain a playful interaction, thus indicating that there is no quantitative variation in the use of the two facial signals relating to the age of the performer. Moreover, no difference was found in the use of the two variants (PF and FPF) of play signals according to the age-phase. If we ended our analysis here, we should have to affirm that the Prediction 3a is not supported. However, the use of playful expressions varied according to the asymmetry of the session in infants, and to the receiver identity in juveniles (Prediction 3a partially supported). In infants, whose play sessions were the most unbalanced, we found a positive correlation between the frequency of playful facial displays and the degree of asymmetry characterizing each single session. In juveniles, we found that most of the facial signals were directed towards other juveniles. This result is not surprising if we consider the high complexity and competition levels characterizing chimpanzee juvenile play. Probably, when play becomes more competitive, as occurs in juvenile chimpanzees and humans , , , there needs to be clearer signaling to maintain the session and to avoid it turning into overt aggression . Therefore, like laughter in humans (Duchenne laughter: , , , ), the playful expressions in chimpanzees (at the different age phases) seem to have a role in advertising cooperative dispositions and intentions thus increasing the likelihood of engaging in solid social relationships (Prediction 3a partially supported, see Table 3).
The presence of play faces during solitary play both in infant and juvenile chimpanzees indicates that, like in humans, playful facial displays can be an expression of an emotional state  (Prediction 3b supported), thus suggesting that infants of both species have the capacity for self-reflection or self-awareness (the precursors to more complex forms of social cognition, ). Recently, Pellis and Pellis  demonstrated that the role of play signals in self-regulating emotional state is also present in spider monkeys. Yet, there are some greater cognitive overlap and developmental similarities between Pan and Homo than between either and other primate species. This makes clear why the Pan genus offers special insights into the Homo genus in relation to some general aspects of play that are true for all species that play irrespective of their phylogenetic relationships .
In conclusion, like in humans, play in immature chimpanzees shows a number of changes, both quantitative and qualitative, across the ontogenetic pathway from infancy to juvenility, thus suggesting that chimpanzee play can have different functions according to the developmental stages of animals. This appears to be valid also for playful facial displays which, both in humans and chimpanzees, seem to function in modulating/enhancing social interactions and in expressing private emotions.
Materials and Methods
This study was approved by University of Pisa (Animal Care and Use board). Since the study was purely observational the committee waived the need for a permit. The study was conducted with no manipulation of animals.
The study species
The chimpanzee (Pan troglodytes) and bonobo (Pan paniscus) are the closest living relatives to humans . These great apes share many basic features with humans. Both have a high level of behavioral flexibility and individuals aggregating into cohesive multimale-multifemale societies . Chimpanzees live in communities, whose members form temporary parties that vary in size and composition . The species is characterized by male philopatry and female dispersal, with females leaving their natal groups after reaching sexual maturity.
Similar to humans, a close bond with the mother characterizes behavioral development in chimpanzees that lasts until well after weaning. They have a long transition to independence . Chimpanzee infants are in constant contact with their mother until about sixteen weeks. At this age, they remain out of contact (less than 5 m) from the mothers for few minutes per bout. Mothers continue to nurse and carry their offspring for about 4–5 years . One-year-old infant chimpanzees begin to play with other infants often leaving their mothers for more than 10 m for several minutes . Older siblings, when present, are the primary source of social interactions, but social contacts also include unrelated peers .
In this paper, we followed the age categories provided by Sugiyama  and classified immature subjects as follows: infants (I) from 0 to 3 years and juveniles (J) from 4 to 7 years (see Table 1 for age classification and sibling relation).
The study groups
The Beauval colony lived in an enclosure composed by indoor and outdoor facilities of about 200 m2 and 2000 m2, respectively. The indoor facility was formed by two large enclosures that were placed in a glasshouse. The group received abundant food (vegetables, fresh fruits, nuts, grains, and yogurt) at 9.00 a.m., 2.00 p.m., and 4.30 p.m.
The Amersfoort colony was hosted in an enclosure made of indoor and outdoor facilities of about 80 m2 and 400 m2, respectively. The chimpanzees were fed three times a day (11.00 a.m., 1.00 p.m. and 3.00 p.m.) with pellets, vegetables, fruits, rice and nuts, that were scattered on the ground.
Both Beauval and Amersfoort enclosures were equipped with trunks, lianas, ropes, and platforms so the chimpanzees could move freely in all three dimensions.
Observations took place over a 6-hour period, 6 days per week (also covering the feeding-times) from October 2001 to February 2002 for the Beauval colony (for a total of 90 days) and from May to October 2004 for the Amersfoort colony (for a total of 91 days). Before systematic data were collected, the four observers underwent an 80-hour training period to become skilled in animal identification and behavioral pattern distinction. Training was over when the percentage agreement on animal and behavior recognition reached 95% among the observers  and when the Cohen's kappa was higher than 0.70 .
The authors with the two assistants were able to collect all playful interactions (see Table 2 for the behavioral item definition) by focal animal sampling method. All individuals were observed for exactly the same number of hours: 31 hrs of observation for the Beauval colony and 35 hrs of observation for the Amersfoort colony.
A solitary play session started when a lone individual performed a play pattern (see Table 2). If the bout started again after a delay of 10 s it was counted as a new play session.
A social play session was deemed to begin when one partner directed any playful behavior towards a playmate and ended when the participants stopped their activities or one of them moved away . If the bout started again after a delay of 10 s it was counted as a new play session. For both social and solitary play sessions we recorded: i) playmate identity, ii) play patterns and their chronological sequence iii) context (circumstance in which play took place, e.g. feeding, sexual). For an accurate description of social play patterns see Table 2. Social play patterns were classified as unidirectional, when it is possible to distinguish an actor and a receiver (PBIT, PRE, PRUN, PSL, TK, PPS, PBR, PRCO, PST) and bidirectional, when the playmates are both actor and receiver (PIRO, ACP, SO).
Moreover, within social play we distinguished between locomotor-rotational (LR-play) and rough and tumble play (R&T). When a play session was characterized by the absence of any kind of physical contact, that session was labeled as LR- play , .
We also collected data on play invitations. A play invitation occurred when an animal approached a potential playmate, interacted with him/her by one of the play pattern considered (Table 2), and then ran away. Play invitations were labeled as PINV and PINV* according to the presence or absence of play sessions following the invitation.
For each play session, we recorded two variants of the playful facial displays: Play Face (PF, mouth is opened with only lower teeth exposed) and Full Play Face (FPF, mouth is opened with upper and lower teeth exposed) , , , . For each playful facial display performed by the animals, we registered signaler and receiver identity (directionality) and the exact chronological sequence of the visual signals (strategic use of the signal, e.g. to initiate or maintain a play session).
Data analysis focused on the 15 immature individuals (7 juveniles and 8 infants). Due to the non-normality of data and the small sample size (N = 15) nonparametric statistical tests were applied to the analyses performed at the individual level . We made use of exact tests according to the threshold values suggested by Mundry & Fischer . Non-parametric statistics was performed by using SPSS 12.0. The Wilcoxon matched-pair signed-ranks test (corrected for ties) was used for comparing i) the frequency of social and solitary play and ii) play signal directionality as a function of the age of playmates. The U-Mann Whitney test was used to contrast the level of playful facial displays (PF and FPF) performed by infants and juveniles.
When performing dyadic comparisons we used randomization procedures to avoid pseudo-replication due to non-independence of data (the same individual is included in more than one dyad, therefore dyads are not independent data-points). Specifically, randomization tests were employed with a number of 10,000 permutations using resampling procedures. In order to evaluate whether age significantly affected play distribution we analyzed data at the dyadic level (Infant-Infant, I-I; Infant-Juvenile, I-J; Juvenile-Juvenile, J-J) by applying the ANOVA randomization test . Randomization post-hoc tests were used to determine which pairs of age combinations significantly differed. The two-independent randomization test was employed to assess whether possible differences existed between the Asymmetry Index (AI) of matched (I−I+J−J) and mismatched dyads (I-J). The correlation via randomization was used to assess possible correlations between play and grooming and play and agonistic contacts. All the dyadic analyses were performed by using Resampling Procedures 1.3 by David C. Howell (freeware).
All the analyses were two-tailed and the level of significance was set at 5%; however, trends (p<0.1) were also discussed.
Thanks are due to Rosarita Palomba and Francesca Ballo for support in data collection; F. di Luni for enlightening discussion; Roscoe Stanyon for the critical review of the manuscript and for his accurate linguistic revision.
Conceived and designed the experiments: GC EP. Performed the experiments: GC EP. Analyzed the data: GC EP. Contributed reagents/materials/analysis tools: GC EP. Wrote the paper: GC EP.
- 1. Burghardt GM (2005) The Genesis of Animal Play: Testing the Limits. Cambridge, , Massachusetts: MIT Press. 500 p.
- 2. Pellegrini AD (2009) The role of play in human development. New York: Oxford University Press. 278 p.
- 3. Power TG (2000) Play and Exploration in Children and Animals. Mahwah, , New Jersey: L. Erlbaum. 497 p.
- 4. Pellis SM, Pellis VC (2009) The playful brain: venturing to the limits of neuroscience. Oneworld Publications. 257 p.
- 5. Burghardt G (2011) Defining and recognizing play. In: Pellegrini AD, editor. The Oxford Handbook of the Development of Play. New York: Oxford University Press. pp. 9–18.
- 6. Bekoff M (2001) Social play behaviour: cooperation, fairness, trust, and the evolution of morality. J Consc Stud 8: 81–90.
- 7. Martin P, Caro TM (1985) On the functions of play and its role in behavioral development. Adv Stud Behav 15: 59–103.
- 8. Pellis SM, Pellis VC (1996) On knowing it's only play: the role of play signals in play fighting. Aggr Viol Behav 1: 249–268.
- 9. Petru M, Špinka M, Charvátová V, Lhota S (2009) Revisiting play elements and self-handicapping in play: a comparative ethogram of five Old World monkey species. J Comp Psychol 123: 250–263.
- 10. Bekoff M, Allen C (1998) Intentional communication and social play: how and why animals negotiate and agree to play. In: Bekoff M, Byers JA, editors. Animal Play: Evolutionary, Comparative, and Ecological Perspectives. Cambridge: Cambridge University Press. pp. 97–114.
- 11. Loizos C (1967) Play behaviour in higher primates: a review. In: Morris D, editor. Primate Ethology. Chicago, , Illinois: Anchor Books. pp. 226–282.
- 12. Mancini G, Palagi E (2009) Play and social dynamics in a captive herd of gelada baboons (Theropithecus gelada). Behav Proc 82: 286–292.
- 13. Palagi E, Antonacci D, Cordoni G (2007) Fine-tuning of social play in juvenile lowland gorillas (Gorilla gorilla gorilla). Devel Psychobiol 49: 433–445.
- 14. Palagi E, Cordoni G, Borgognini Tarli SM (2004) Immediate and delayed benefits of play behavior: New evidence from chimpanzees (Pan troglodytes). Ethology 110: 949–962.
- 15. Pellis SM, Pellis VC (2007) Rough-and-tumble play and the development of the social brain. Curr Dir Psychol Sci 16: 95–98.
- 16. Pellegrini AD, Smith PK (1998) Physical activity play: the nature and function of a neglected aspect of play. Child Dev 69: 577–598.
- 17. Breuggeman JA (1978) The function of adult play in free-ranging Macaca mulatta. In: Smith EO, editor. Social Play in Primates. New York: Academic Press. pp. 169–191.
- 18. Poirier FE, Bellisari A, Haines L (1978) Functions of primate play behavior. In: Smith EO, editor. Social Play in Primates. New York: Academic Press. pp. 143–168.
- 19. Dolhinow P (1999) Play: a critical process in the developmental system. In: Dolhinow P, Fuentes A, editors. The nonhuman primates. Mountain View, California: Mayfield Publishing Company. pp. 231–236.
- 20. Pellegrini AD, Dupuis D, Smith PK (2007) Play in evolution and development. Dev Rev 27: 261–276.
- 21. Cordoni G (2009) Social play in captive wolves (Canis lupus): not only an immature affair. Behavior 146: 1363–1385.
- 22. Antonacci D, Norscia I, Palagi E (2010) Stranger to familiar: wild strepsirhines manage xenophobia by playing. Plos one 5(10): e13218. doi:10.1371/journal.pone.0013218.
- 23. Palagi E (2007) Play at work: revisiting data focussing on chimpanzees (Pan troglodytes). J Anthropol Sci 85: 153–164.
- 24. Diamond J, Bond AB (2003) A comparative analysis of social play in birds. Behaviour 140: 1091–1115.
- 25. Fagen R (1981) Animal Play Behavior. New York: Oxford University Press. 684 p.
- 26. Fairbanks LA (2000) The developmental timing of primate play. A neural selection model. In: Parker ST, Langer J, McKinney ML, editors. Biology, brains, and behavior - the evolution of human development. Santa Fe: School of American Research Press. pp. 211–219.
- 27. Pellis SM, Iwaniuk AN (2000) Comparative analyses of the role of postnatal development on the expression of play fighting. Dev Psychobiol 36: 136–147.
- 28. Biben M, Suomi SJ (1993) Lessons from primate play. In: MacDonald K, editor. Parent-child play: descriptions and implications. pp. 185–196. Albany: State University of New York Press.
- 29. MacDonald KB, Parke RD (1984) Bridging the gap: parent-child play interactions and peer interactive competence. Child Dev 55: 1265–1277.
- 30. Tamis-LeMonda CS, Bornstein MH (1993) Play and its relations to other mental functions in the child. In: Bornstein MH, editor. The role of play in the development of thought. pp. 17–28. W. Damon (Series Ed.), New Directions for Child Development, No. 59. San Francisco: Jossey Bass.
- 31. Tomasello M, Gust DA, Evans A (1990) Peer interaction in infant chimpanzees. Folia Primatol 55: 33–40.
- 32. Howes C (2011) Social play of children with adults and peers. In: Pellegrini AD, editor. The Oxford Handbook of the Development of Play. New York: Oxford University Press. pp. 231–244.
- 33. Suomi SJ, Harlow HF (1972) Social rehabilitation of isolate reared monkeys. Devel Psychol 6: 487–496.
- 34. Spijkerman RP, van Hooff JARAM, Dienske H, Jens W (1997) Differences in subadult behaviors of chimpanzees living in peer groups and in a family group. Int J Primatol 18: 439–454.
- 35. Pellegrini AD (1988) Elementary school children's rough-and-tumble play and social competence. Dev Psychol 24: 802–806.
- 36. Pellegrini AD (1992) Preference for outdoor play during early adolescence. J Adol 15: 241–254.
- 37. Pellegrini AD (1993) Boy's rough-and-tumble play, social competence, and group composition. Brit J Dev Psychol 11: 237–248.
- 38. Pellegrini AD (1995) A longitudinal study of boy's rough-and-tumble play and dominance during early adolescence. J Appl Dev Psychol 16: 77–93.
- 39. Smith PK, Boulton M (1990) Rough-and-tumble play, aggression, and dominance: perceptions and behavior in children's encounters. Hum Devel 33: 271–282.
- 40. Paquette D (1994) Fighting and playfighting in captive adolescent chimpanzees. Aggr Behav 20: 49–65.
- 41. Mendoza-Granados D, Sommer V (1995) Play in chimpanzees of the Arnhem zoo: self-serving compromises. Primates 36: 57–68.
- 42. Palagi E (2006) Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): implications for natural social systems and interindividual relationships. Am J Phys Anthropol 129: 418–426.
- 43. Waller BM, Dunbar RIM (2005) Differential behavioural effects of silent bared teeth display and relaxed open mouth display in chimpanzees (Pan troglodytes). Ethology 111: 129–142.
- 44. van Hooff JA, Preuschoft S (2003) Laughter and smiling: the intertwining of nature and culture. In: de Waal FBM, Tyack PL, editors. Animal social complexity: Intelligence, culture, and individualized societies. Cambridge, MA: Harvard University Press. pp. 260–287.
- 45. van Lawick-Goodall J (1968) The behaviour of free-living chimpanzees in the Gombe Stream Reserve. Anim Behav Monogr 1: 161–311.
- 46. de Waal FBM (1988) The communicative repertoire of captive bonobos (Pan paniscus), compared to that of chimpanzees. Behaviour 106: 183–251.
- 47. Lefcourt H (2000) Humor: the Psychology of Living Buoyantly (Vol. 4). New York Boston Dordrecth London Moscow: Kluwer Academic/Plenum Publishers. 210 p.
- 48. Provine RR (2000) Laughter: A scientific investigation. New York: Viking. 258 p.
- 49. Davila-Ross M, Allcock B, Thomas C, Bard KA (2011) Aping Expressions? Chimpanzees produce distinct laugh types when responding to laughter of others. Emotion, DOI:10.1037/a0022594 (in press).
- 50. Fridlund AJ (1991) Sociality of solitary smiling: potentiation by an implicit audience. J Personal Soc Psychol 60: 229–240.
- 51. Russell JA, Bachorowski JA, Fernández-Dols JM (2003) Facial and vocal expressions of emotion. Ann Rev Psychol 54: 329–349.
- 52. Bachorowski JA, Owren MJ (2003) Sounds of emotion: production and perception of affect- related vocal acoustics. Ann Ny Acad Sci 1000: 244–265.
- 53. Mehu M, Grammer K, Dunbar RIM (2007) Smiles when sharing. Evol Hum Behav 28: 415–422.
- 54. Owren MJ, Bachorowski JA (2003) Reconsidering the evolution of nonlinguistic communication: the case of laughter. J Nonverbal Behav 27: 183–200.
- 55. Niedenthal PM, Mermillod M, Maringer M, Hess U (2010) The Simulation of Smiles (SIMS) model: Embodied simulation and the meaning of facial expression. Behav Brain Sci 33: 417–433.
- 56. Keltner D, Bonanno GA (1997) A study of laughter and dissociation: distinct correlates of laughter and smiling during bereavement. J Personal Soc Psychol 73: 687–702.
- 57. Gervais M, Wilson DS (2005) The evolutions and functions of laughter and humor: a synthetic approach. Q Rev Biol 80(4): 395–430.
- 58. Palagi E (2008) Sharing the motivation to play: the use of signals in adult bonobos. Anim Behav 75: 887–896.
- 59. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49: 227–265.
- 60. Lyon ME, Canning , PM (1995) The Atlantic day care study. Prepared for the Department of National Health and Welfare, Ottawa, Canada. 16 p.
- 61. Rubin KH, Maioni TL, Hornung M (1976) Free play behaviors in middle and lower class preschoolers: Parten and Piaget revisited. Child Dev 47: 414–419.
- 62. Rubin KH, Watson KS, Jambor TW (1978) Free play behaviors in preschool and kindergarten children. Child Dev 49: 534–536.
- 63. Scott E, Panksepp J (2003) Rough-and-tumble play in human children. Aggr Behav 29: 539–551.
- 64. Sanefuji W, Ohgami H, Hashiya K (2006) Preference for peers in infancy. Inf Behav Dev 29(4): 584–593.
- 65. Pusey AE (1990) Behavioural changes at adolescence in chimpanzees. Behaviour 115: 203–246.
- 66. Pellegrini AD (2002) The development and possible function of rough-and-tumble play. In: Hart CH, Smith PK, editors. Handbook of social development. Oxford: Blackwell. pp. 438–454.
- 67. Humpreys AP, Smith PK (1987) Rough-and-tumble play, friendship, and dominance in school children: evidence for continuity and change with age. Child Dev 58: 201–212.
- 68. Smith PK (2010) Cyberbullying: the European perspective. In: Mora-Merchan J, Jäger T, editors. Cyberbullying: A cross-national comparison. Landau: Verlag Emprische Padagogik. pp. 7–19.
- 69. Bauer EB, Smuts BB (2007) Cooperation and competition during dyadic play in domestic dogs, Canis familiaris. Anim Behav 73: 489–499.
- 70. Schlaghecken F, Sisman R (2006) Low-level motor inhibition in children: evidence from the negative compatibility effect. Adv Cog Psychol 2: 7–19.
- 71. Bell HC, Pellis SM, Kolb , B (2010) Juvenile peer play experience and development of the orbitofrontal and medial prefrontal cortices. Behav Brain Res 207: 7–13.
- 72. Foroud A, Whishaw IQ, Pellis SM (2004) Experience and cortical control over the pubertal transition to rougher play fighting in rats. Behav Brain Res 149: 69–76.
- 73. Spinka M, Newberry RC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76: 141–168.
- 74. Saunders I, Sayer M, Goodale A (1999) The relationship between playfulness and coping in preschool children: A pilot study. Am J Occup Ther 53: 221–226.
- 75. Pellis SM, Pellis VC (1997) Targets, tactics and the open mouth face during play fighting in three species of primates. Aggr Behav 23: 41–57.
- 76. Schmidt KL, Cohn JF (2001) Human facial expressions as adaptations: evolutionary questions in facial expression research. Yearbook Phys Anthropol 44: 3–24.
- 77. Pellis SM, Pellis VC (2010) To whom the play signal is directed: a study of headshaking in black-handed spider monkeys (Ateles geoffroyi). J Comp Psychol 125: 1–10.
- 78. Parker ST, McKinney ML (1999) Origins of intelligence: the evolution of cognitive development in monkeys, apes, and humans. Johns Hopkins University Press. 404 p.
- 79. Fleagle JG (1999) Primate adaptation and evolution, 2nd ed. San Diego: Academic Press. 596 p.
- 80. Goodall J (1986) The Chimpanzees of Gombe: Patterns of Behavior. Boston MA.: Harvard University Press. 673 p.
- 81. Nishida T (1968) The social group of wild chimpanzees in the Mahale Mountains. Primates 9: 167–224.
- 82. Kuroda S (1989) Developmental retardation and behavioral characteristics of Pygmy chimpanzees. In: Heltne PG, Marquardt AE, editors. Understanding chimpanzees. Chicago: Chicago Academy of Sciences. pp. 184–193.
- 83. Sugiyama Y (1994) Age-specific birth rate and lifetime reproductive success of chimpanzees at Bossou, Guinea. Am J Primatol 32: 311–318.
- 84. Martin P, Bateson P (1986) Measuring behavior-an introductory guide. Cambridge: Cambridge University Press. 187 p.
- 85. Kaufman AB, Rosenthal R (2009) Can you believe my eyes? The importance of inter-observer reliability statistics in observations of animal behaviour. Anim Behav 78: 1487–1491.
- 86. Palagi E, Paoli T (2007) Play in adult bonobos (Pan paniscus): modality and potential meaning. Am J Phys Anthropol 134: 219–225.
- 87. Palagi E, Mancini G (2011) Playing with the face: playful facial “chattering” and signal modulation in a monkey species (Theropithecus gelada). J Comp Psychol 125: 11–21.
- 88. Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. New York: McGraw-Hill. 399 p.
- 89. Mundry R, Fischer J (1998) Use of statistical programs for nonparametric tests of small samples often lead to incorrect P values: examples from animal behaviour. Anim Behav 56: 256–259.
- 90. Manly BFJ (1997) Randomization, bootstrap and Montecarlo methods in biology. London: Chapman and Hall. 455 p.