On knowing it's only play: The role of play signals in play fighting

Pergamon

Aggression and Wolent Behavior, Vol. 1, No. 3. pp. 249-268, 1996 Copyright 0 1996 Elsevier Science Ltd Printedin the USA. All rights reserved 1359-1789/96 SIX00 + .@I

SSDI 1359-1789(95)00016-X

ON KNOWING IT’S ONLY PLAYr THE ROLE OF PLAY SIGNALS IN PLAY FIGHTING Sergio M. Pellis and Wvien C. Pellis Department of Psychology, University of Lethbridge, Canada

ABSTRACT. Pluyjighting

in many species contains behavioral elements of direct aggression; that is, those behavior patterns that are used to threaten and contact opponents. Although many investigators have alleged that there are play sign&s that can be used to unambiguously distinguish playfilfrom nonplayful aggression, the existence of such signals is mainly anecdotal and correlational. For most species, such signals are either not present, or are not present with suflcient regularity to function as unambiguous markers of play. In most play&l encounters, participants seem able to use contextual cues to assertain whether the actions of the partner are afiliative or not. Where play promoting signals do appear to exist, they are ofen general purpose afiliative signals rather than ones specific to play. Such signals are most often associated with situations where the play&l intentions of the performer may be ambiguous to the recipient. In these situations, such signals appear to be crucial in avoiding escalation to serious aggression. The danger of escalating from play to aggression is most often reported as animals become sexually mature and stronger Also, it is in early adulthood that members of a social group compete for dominance. In these situutions, a signal “this is play” may not be suflcient. Instead, signals that can retroactively appease a play partner with “I was only kidding, ” may be very important so as to manipulate, and thus obfuscate, the true intent of the action. When present, the signals occurring in play are highly variable in form and context, which is what would be expectedfor such subtle social manipulation. We suggest that species with more complex social relationships, where individuals are likely to probe and test their relationships with play fighting, are most likely to be the ones that make the most sophisticated use of such signals.

BECAUSE ANIMALS during play use behavior patterns from other functional contexts (Heymer, 1977; Milk, 1981), it is often difficult to distinguish instances of actual play from instances of immature or incomplete behavior (Ewer, 1968). As most play occurs in immature animals (Fagen, 198 l), this issue is a major problem. If all instances of immature behavior that are difficult to classify were labeled play (Groos, 1898), then such a label would have little practical and conceptual value (Martin, 1984). Indeed, for play fighting or rough-and-tumble Correspondence should be addressed to Sergio M. Pellis, Department of Psychology, Lethbridge, Alberta, Canada TlK 3M4. E-mail address: [email protected] 249

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play, where many animals use the behavior pattems of agonism (Meaney, Stewart, & Beatty, 1985), making a distinction between what is serious and what is not serious should also be a problem for the interactants. One solution is to define play fighting "operationally in a given species by the presence of play-signals and by the absence of agonistic communication" (Fagen, 1981, p. 48). Other criteria often included in a definition of play such as it is repetitious, out of context, and does not serve an immediate purpose (Bekoff & Byers, 1981), can also apply to such phenomena as cage stereotypies (Mason, 1991) and the onset of new behavioral systems during development (Coppinger & Smith, 1989; Hogan, 1988). The central role of play signals is that they provide unambiguous observable markers that inform the observer that what is being observed is play and not something else. In this way, the play-like interactions of juvenile insects (Oloman, Breed, & Bell, 1976) and fish (Wyman & Ward, 1973) can be classified as immature aggression, whereas those of some juvenile mammals and birds can be classified as play-fighting (Fagen, 1981). The view that play fighting can be distinguished from immature aggression by the absence of threat and the presence of play promoting signals, is widespread among both play researchers (e.g., Aldis, 1975; Barber, 1991; Bekoff, 1975; Fagen, 1981; Smith, 1982; Symons, 1974, 1978a), and authors of the secondary literature (e.g., Grier & Burk, 1992; Leger, 1992; Manning & Dawkins, 1992; Poole, 1985). Some researchers have cautioned that play signals have not been identified in species that by other criteria appear to play (LeResche, 1976), or have noted that even when present in a species, such signals are neither always present during play fighting (Maple & Zucker, 1978), nor are necessarily detectable by the recipient when they are (Aldis, 1975). In this review, we will show that not only are most so-called play signals not universal amongst species that engage in play fighting, but also that many such signals are not unique to play. Therefore, play signals are not the answer to our need for an objective criterion with which to unambiguously distinguish play fighting from serious fighting. Further, we will show that agonistic signals are pervasive during play fighting. This not only adds to our difficulty as observers, but heightens the problem of understanding how the interactants are able to interpret the actions of their partners. For most situations, it would appear that animals can distinguish playful intent by contextual cues or by some subtle aspects of how their partners move, rather than by the type of behavior patterns performed. At present, what these cues are remains a mystery, however we, as observers, appear to recognize play subjectively and usually achieve agreement with other observers (Miller, 1973). In some situations these subtle cues are insufficient; therefore, amicable signals appear to be necessary so as to ensure the continuance of play. By focusing on such situations, new insights can be gained about not only the role of play-promoting signals, but also of the functions of play fighting. AGONISTIC SIGNALS DURING PLAY FIGHTING Although it has been repeatedly claimed that agonistic signals are absent during play fighting (see above), there are numerous cases where agonistic signals are reported. Further, such signals are not necessarily used to terminate play or to escalate into a serious fight, but instead, may occur as part of the ongoing playful interaction. Unfortunately, in most cases, such signals are not documented with sufficient detail to allow generalizations about how widespread or frequent they are. Nonetheless, examples from a range of species serve to illustrate that a definition of play fighting which claims that it can be identified by the absence of such signals is flawed. One pattern of agonistic encounter in adult male ring-tailed lemurs L e m u r c a t t a involves rubbing the distal part of the tail with the scent glands on the wrist and then waving the tall at the opponent. This stylized sequence of threat can precede or preclude physical combat. Juvenile male ring-tailed lemurs similarly anoint and tail wave during play fighting, even

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though the wrist glands have not as yet matured (Gould, 1990; Jolly, 1966). Adult gorillas Gorilla gorilla threaten opponents by short charges that are sometimes followed by a slap or a hip slam. Similarly, infants and juveniles perform this threatening action during play fighting (Schaller, 1963). Chest beating, another agonistic threat of gorillas, is also frequently performed during play fighting by juveniles (Brown, 1988; SchaUer, 1970). Head tosses and neck twists are movements used to threaten opponents in a variety of sheep and goat species. These elements also typically occur during play (Geist, 1971; Schaller, 1977). Ear flattening is a common defensive threat element in the repertoire of many mammals (Andrew, 1963) and has also been reported in the play fighting of several species (e.g., Schaller, 1972; Sussman, 1974; Weigel, 1979). Opening the mouth is another threat signal (Andrew, 1963) that can be performed during play fighting (Schaller, 1972), and when used by the recipient of a playful attack, can block further attempts by the partner to gain contact (Pellis, 1981, 1984; Pellis & Pellis, 1994). Snarling, a defensive threat, is sometimes associated with playful defense in lions Panthera leo (Schaller, 1972). Similarly, various facial expressions, typical of offensive and defensive threat, occur in the play fighting of canids (Bekoff & Byers, 1981; Feddersen-Petersen, 1991; Fox, 1970) and black bears Ursus americanus (Henry & Herrero, 1974). During both adult agonism and juvenile play fighting, Steller sea lions Eumetopias jubatus perform noncontact boundary displays (Gentry, 1974). Kittens Felis catus use a lateral display during play fighting (Barrett & Bateson, 1978) that is also used as a defensive threat during serious fighting (Leyhausen, 1979). The bouncing threat display of adult patas monkeys Erythrocebus patas (Hall, 1965; Hall & Mayer, 1967) sometimes occurs during juvenile play fighting (Hall, Boelkins, & Goswell, 1965). Therefore, numerous examples exist that show threat signals occurring during social play. In order to understand why such signals may be prevalent during play fighting, the developmental context of play needs to be considered. Aggression may best be thought of as consisting of two major types (see Geist, 1971; Schaller, 1977; Walther, 1974): (a) direct aggression, which includes both overt threats, such as warnings of imminent attack, and actual contact; and (b) indirect aggression, during which the animal attempts to assert or achieve dominance not by test of strength, but by intimidating the opponent solely through its use of rank symbols. Signals produced in these two aggressive contexts have different meanings. As noted by Walther (1974), in a threat display the signal means "I am ready to fight you," whereas in a dominance display it means "I am the greatest." In general, dominance displays mature relatively late in ontogeny. For example, Schaller (1977) plotted the incidence of behavioral elements of direct aggression (including both threats and direct contact) and of indirect aggression against age for three species of caprinids (i.e., goats and sheep), and found that as the frequency of direct aggression decreased with age, that of indirect aggression increased (see Figure 32 on page 221 and Figure 37 on page 248 in Schaller, 1977). That is, behavioral elements of direct aggression, including both those of threat and contact, were at their highest occurrence in the juvenile period, when most play fighting occurs. It is likely that with increasing age, fighting becomes riskier as the animals become stronger (Alvarez, 1993). Consequently, there is a need to have either a reputation or an obvious badge of status that can act to reduce the likelihood of engaging in overt fights. In this way, indirect aggression behavior patterns emerge to replace the occurrence of direct aggression. For example, as young adult male Grant's gazelle Gazella granti mature, the incidence of dominance displays increases and the occurrence of overt fights decreases (Walther, 1974). Vertebrates use a variety of badges and signals to communicate status, such as horns, antlers, and tusks in ungulates (Geist, 1966, 197 l), plumage patterns in birds (e.g., Moiler, 1987; Rowher, 1975; Wilson, 1992), scent marking in many mammals (e.g., Gosling & MacKay, 1990; Hurst, 1987), and accoustic signals by a variety of taxa (e.g., Clutton-Brock

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& Albon, 1979; Davies & Halliday, 1978; Leonard & Horn, 1995). Of course, size is an important signal in itself (e.g., LeBoeuf, 1977). Behavior patterns that are used as dominance displays take advantage of these badges of status (Geist, 1978). Not surprisingly then, both the badges and the associated behavior patterns do not mature until later in development. For example, it may take up to 20 years for a male gorilla to achieve a size massive enough to intimidate rivals (Schaller, 1963). Rats Rattus norvegicus can identify the odor from a dominant male (Brown, 1979; Krames, Carr, & Bergman, 1969), but these odor cues are not produced until adulthood (Thor, 1979; Thor & Holloway, 1982). Many dominance displays are derived from offensive threats; and submissive displays, being the opposite of dominance displays, are frequently derived from defensive threats (Walther, 1974). Therefore, both dominance and submissive displays are more distantly related to combat tactics than are threat displays. Many threat displays have been derived from the intention movements preceding combat. For example, caprinids use a jerk, where the head is lowered downward or sideways as an implied head butt (Schaller, 1977). The correlated developmental maturation of both threats and combat motor patterns during earlier stages of development and the dissociation of these behavior patterns with those of indirect aggression, further support the idea that both overt threats and overt combat motor patterns are closely linked motivationally. For species where sufficient detail is provided, such as for mountain sheep Ovis canadensis, behavioral elements of offensive and defensive threat have been shown to be common occurrences during the play fighting of juveniles (Geist, 1971). Therefore, the proposition that play fighting involves the use of combat tactics in the absence of associated threatening behavior patterns (e.g., Fagen, 1981; Symons, 1974) is not correct. Rather, the data for caprinids show that in the early phases of development, both aspects of direct aggression (threat and contact) are prevalent, and both occur during play (Schaller, 1977). Given that most play is performed by juveniles, and that indirect aggression typically matures after the juvenile phase, it is the behavioral elements of indirect aggression that are rare in juvenile play fighting. A revised definition of play fighting would state: Play fighting involves the use of the behavior patterns of direct aggression including both threat and contact, but without the usual consequences of such behavior when performed in a more serious context (although see Pellis, 1993). If some species rarely use the threat elements of direct aggression in their play (e.g., rhesus monkeys Macaca mulatta; Symons, 1978a), and others use them extensively (e.g., mountain sheep, Geist, 1971), it becomes an empirical issue to discern which do and which do not, and why this may be so. Clearly, using data from one species or one taxonomic group to generalize for all others is not appropriate (Pellis, 1988). If during play fighting animals threaten one another, how do they (and we) know it is only play? For example, Figure 1 shows that as one kitten approaches another, the recipient raises itself, flattens its ears and turns laterally arched in the direction of its partner (a-d). Yet the attacking kitten still lunges at the partner and they engage in a playful wrestle (e-h). If this display were performed in earnest, it would inhibit such an attack (Leyhausen, 1979). Also note that the defensive cat lowers its tail, which is a threatening gesture, whereas the attacker keeps its tail raised, which is an affiliative gesture (CameronBeaumont, 1995). Of course, the defensive threat by the recipient of the playful attack may be missing some essential ingredients, such as associated vocalizations, or some degree of visibility of the teeth. Even so, this changes the definition of play fighting from threat signals being absent, to threat signals being present but incomplete. This, in turn, raises a number of empirical issues about graded displays, and what constitutes a complete display. Clearly, if in the presence of threat signals, be they complete or incomplete, animals can judge the context to be a playful one, then they are not making that judgment by the absence of such signals.

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FIGURE 1. A sequence of play fighting in 8-week-old kittens is shown. As the male on the left approaches the female (a), she stands, flattens her ears and adopts a lateral stance (b-e). The male then proceeds to lunge and attack her nape, which leads the female to roll defensively onto her back (e-h). Tracings are made from a videotaped sequence (Pellis, work in progress).

PLAY SIGNALS DURING PLAY FIGHTING The other half of the definition proposed by Fagen (see above) is that there exist unique behavioral elements that act to communicate playfulness to a playmate. Even in the presence of threat signals, the use of such play signals could offset any doubt about the playful nature of the encounter. The issue then becomes how good is the evidence that these elements serve as signals conveying the message "this is play. 'q For most presumed play signals, the evidence is strictly correlational, with certain behavioral elements being present in many play fights (Bekoff, 1975). Indeed, many reports in the literature merely state that a play signal similar to that reported by some other author was observed. A careful reading of both the primary and secondary literature on play signals reveals that many different phenomena may be being lumped together into a unitary category. Meaney et al. (1985) show three photographs of play fighting with the caption "Note the open mouth approach in each case" (pp. 6, 7), where the open mouth face is thought to be a widespread play signal in primates and carnivores (Fagen, 1981). Two o f these photographs depict play in wolves and the third shows play in vervet monkeys. In the first photograph of lBateson (1955) initially introduced the concept of play signals in terms of the ability of such signals to act as qualifiers to subsequent signals. For example, if one animal observes that another is preparing to deliver a bite, how does the recipient know that the bite to come is going to be playful or serious? The solution is a signal(s) that informs the partner that what is to follow is playful and not serious. Therefore, the play signal is metacommunicatory; one that qualifies the meaning of subsequent actions. That is, a play signal means "What is to follow will be playful." Symons (1978a) criticized this view, arguing that more simply, a play signal can mean "'this is play." For further analysis of this concept and the debate over the exact meaning of play signals see Mitchell (1991). For our purposes, it is irrelevant whether play signals involve metacommunication or communication. What is crucial is that it is by the presence of these presumed play signals that animals can supposedly differentiate between playful and nonplayful encounters.

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wolves, the performer is lying on its back facing toward the lower jaw of the partner who is squatting above. The performer's mouth is about half-open, and it is not clear whether he/she is approaching the partner. Meanwhile, the partner's ears are rotated backwards, and partially flattened (this feature of defensive threat is not mentioned by the authors). In the second photograph of wolves, the performer's ears are rotated forward, and its mouth is fully open and seems to be approaching the side of the neck. Meanwhile, however, the recipient of this so-called signal has its head turned away and is biting another wolf. In the third photograph, two pairs of vervet monkeys are shown, three of whom have their mouths wide open. One pair is hanging upside down from a branch, head to head, with their faces obliquely facing each other. The one facing the photographer has both upper and lower teeth exposed. The other pair is sitting upright on a branch, and one has a fully open mouth, and is facing its partner. Note that its teeth are not showing. Meanwhile, the partner has its head cocked obliquely toward the other and its mouth is just beginning to open. These three photographs are supposed to show instances of the same phenomenon; yet, the open mouths depicted in each case differ in both form and context. Such confusing examples abound in the literature. For example, a photograph on page 65 in McDonald Pavelka (1993) shows one Japanese macaque juvenile sitting next to another with its mouth open, yet in near contact with the side of its partner's neck, as if about to bite. Meanwhile, the partner, with its mouth partially open and teeth showing, is looking forward and away from the other's head. Again, this is reported by the author as an example of an open mouth play face. Although Brown (1994) states that the open mouth play face promotes playful contact and differs from agonistic open mouth threats, in the adjoining photograph of two subadult lions, it is the lion leaping backwards, away from the approaching partner who has an open mouth and its ears flattened! We suspect that the idea of the existence and role of play signals has become so pervasive that supposed instances are reported uncritically. Indeed, data from other sources are recast with the play signal label, even though no such claim had been made in the original. Two such examples occur in a textbook by Poole (1985). On page 107, a tracing of a play fighting sequence in the meerkat Suricatta suricatta is presented that had been originally published by Wemmer and Fleming (1974). The two meerkats are standing upright in an embrace with their mouths open. One then rotates its head towards the other and bites it on the cheek. In the caption by Poole, this sequence is said to illustrate the open mouth play face. However, it was not described as such in the original paper by Wemmer and Fleming, nor were any other play signals mentioned. In the second example, two behavior patterns in sheep and goats, the head toss and neck twist, are labeled as play signals (Table 4.4 on p. 102). Yet, in consulting works on ungulate behavior (Geist, 1971; Schaller, 1977; Walther, 1984), these are classified as sexual and agonistic signals. When they occur in juvenile play, they have not been labeled as play signals, but as agonistic and sexual signals that occur during play fighting (Geist, 1971). These examples illustrate that play signals are not unambiguous markers of play, but rather, that because these behaviors occur during play, they are often labeled as play signals. If the use of signals during play fighting is to be analysed meaningfully, an objective criteflon needs to be applied. Fagen (1981) provides the basis for such a criterion in the sentence preceding the quotation above, where he notes that play signals have "non-essential properties" (p. 48). During play fighting, one animal attempts to gain an advantage over its partner, who in turn attempts to avoid being so disadvantaged (e.g., Aldis, 1975; Fagen, 1981; Pellis, 1988; Smith, 1982; Symons, 1978a). In this context, a movement that is essential for playful attack or for playful defense should not be considered as a play signal. For example, if one monkey lunges and grabs at the back of another, and its partner then leaps out of the tree, it would seem illogical to label either the grab or the leap as a play signal, if the object of the play fight were to grab and hold down the opponent. If, on the other hand, the approach-

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ing monkey produced a unique vocalization or hand gesture before making the grabbing attempt, then such a vocalization or gesture, because it is not essential in either holding an opponent down, or in avoiding being held, would likely be a candidate as a play signal. Using this nonarbitrary criterion, some of the confusion arising from the above described examples can be clarified. One well known behavior pattern that has been labeled a play signal is the so-called play bow reported in various species of canids (Bekoff, 1972), lions (Schaller, 1972) and occasionally in some species of monkeys (Fagen, 1981). In this behavior pattern, one of the play partners lowers its forequarters. This behavior pattern is often performed at the beginning of the play fight, but can also occur sporadically during an ongoing play fight. In some canids, the play bows occurring at the beginning of a play fight are more stereotyped in both duration and form than those occurring during the course of a play fight (Bekoff, 1974). The stereotypy at the outset is strong evidence for the functional use of this motor pattern as a play signal conveying the message "I want to play." Recently, Bekoff (1995) has shown that when actions that can be misinterpreted are performed, such as bites, bows are likely to be performed. Using the above criterion, it would follow that biting or other contact would occur in the absence of bows. The function of the bows supposedly is to initiate or maintain the playful interaction, not to gain or avoid a bite. However, the requisite analysis to draw this conclusion has not been conducted. That bowing can be a useful tactic during interactions is illustrated by the behavior of cutting horses, a type of American quarterhorse trained to corral cattle. By bowing in front of a cow, the horse shifts its weight onto its hindlimbs, and so places itself in a position from which it can rapidly respond to the cow's movements. Therefore, if the cow charges, the horse can rapidly swerve away by pivoting on its hindlimbs; and if the cow runs away, it can quickly push off with its hindlimb and follow. That is, the bow provides an optimal stance which enhances the horse's maneuverability and maximizes the efficient execution of any one of several options (see photographs on pages 62-65 and 116-119 in Self, 1969). From personal experience, we know that when playing with a dog, the bow posture results in a highly maneuverable, hard-to-catch animal. Although most often present in play, such bows also occur in sexual encounters (Bekoff, 1974) and in combat (B. Gorny, personal communication, 1995). Before it is concluded that the play bow is functionally present in the play fight to signal playful intent, its possible functional involvement in playful combat itself must be ruled out. Another well known and frequently reported play signal is the so-called open mouth play face (van Hoof, 1967). Many reports of this presumed play signal note its association with close quarter contact and biting (e.g., Chevalier-Skolnikoff, 1974; Fedigen, 1972; Pellis, 1984; Poole, 1978; Sussman, 1974; van Lawick Goodall, 1968). For most species of primates and carnivores, play fighting involves biting. Indeed, to bite without being bitten back appears to be the major goal of the encounter (Aldis, 1975). However, a bite cannot be delivered without opening the mouth, and therein lies the problem. If opening the mouth is essential for attacking the opponent, then it cannot simultaneously be a nonessential behavioral element that is present for its communicatory function. 2 Detailed contextual analyses could reveal that opening the mouth in a given situation was irrelevant to biting, thus supporting the proposition that the open mouth serves a function other than one essential for playful combat. For example, in 7-9-week-old polecats Putorius putorius, open mouths occur as a 2It is widely accepted that the open mouth is derived from an intention to bite (e.g., Archer, 1992). However, most of the literature that reports the presence of an open mouth does not merely report it as one animal opening the mouth so as to bite another, but so as to provide a play signal. What is missing from most of the available literature is direct evidence that the open mouth serves this communicatory function (Bekoff, 1975, 1995).

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failure to achieve a bite on the evading partner. This clearly illustrates that the mouth is opened for biting and not to signal. However, at 15 weeks, the open mouth is displayed to the partner, and may even be emphasized by sideways head movements (Poole, 1978). Opening the mouth, therefore, is not "essential" for biting. This example provides compelling evidence that a communicatory function is added to the opening of the mouth with age. Structural uniformity over myriad species, or even within single species, would provide support for the play face being a play signal. A survey of the literature on primates reveals that the facial configuration can vary markedly among species, and also within the same species (Table 1). Indeed, the variation can cause confusion on what exactly is being reported. For example, both for the ruffed lemur Varecia variegata variegata (Pereira, Seeligson, & Macedonia, 1988) and the Celebes macaque Macaca nigra (Nickelson & Lockard, 1978), researchers reported that the animals exhibit a play face that is the same as that described by van Hoof (1967). However, as van Hoof (1967) describes variations for each of the facial elements comprising the open mouth face, it is not clear which variant may best describe these two species. Further, the Celebes macaque was reported by van Hoof (1967) as differing from other species in using a retracted lip grimace rather than the typical play face (Thierry, Demaria, Preuscroft, & Desportes, 1989). Structurally, then, it is not clear that the same "signal" is uniformally being reported, and that if it does function as a signal, that it has the same meaning in all its variations. Despite claims that it is unlike the open mouth threat gesture (Shirek-Ellefson, 1972), many instances of the open mouth seen during play fighting act as defensive threats. For example, detailed frame-by-frame analysis of the orientation of the open mouth by attacking and defending juvenile oriental small clawed otters Anonyx cinerea shows that while defenders maintain the open mouth when oriented face-to-face, the attacking otter opens its mouth when oriented towards the opponent's cheeks, the main play target for biting (Pellis, 1984). Similarly, the opening of the bill in juvenile Australian magpies Gymnorhina tibicen during play fighting reveals the same pattern (Pellis, 1981). That is, the defender blocks the partner's attacks by facing it with the mouth or bill open. In patas monkeys and ring-tailed lemurs, over 50% of all open mouths are performed by the defending playmate, with most deterring the partner from persevering with the attack. Many of these defensive open mouths are accompanied by other facial gestures that in other contexts are generally regarded as agonistic, such as raising the eyebrows in patas monkeys, and lowering the ears in lemurs (Pellis & Peilis, 1994). Also, when used for attacking, the open mouth is strongly associated with subsequent biting. There is no convincing evidence that the mouth is opened for communicatory purposes rather than being a necessary precursor for biting. Indeed, both attacking otters and magpies open their mouths/bills at orientations directed at the target areas bitten or pecked during play fighting, not to orientations that enhance the visibility of the open mouth (Pellis, 1981, 1984). It should not be concluded that the bow and the open mouth never function as play promoting signals. As already noted, some of the evidence by Bekoff (1995) and Poole (1978) provide support for such a function. The problem is that for many species, both actions may be essential in play fighting for other functions. Such alternative functions need to be excluded analytically before the role of these actions as play signals can be judged. Nevertheless, there are cases of actions that a priori would seem nonessential to the function of playful attack and defense, which serve as promising examples of play signals. The typical play face of the douc langur Pygothrix nemaeus (Kavanagh, 1978) involves closing the eyes, and exposing the white eyelids. Usually its mouth is held closed at the same time. Indeed, a langur may maintain this face while approaching another from several meters away, sometimes even falling off a branch in the attempt (Kavanagh, 1978). This example shows that not only does such a face have no functional utility in playfully attacking a part-

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TABLE 1. Configuration of the Face During the Primate Play Face Facial Elements

Configuration (Citation a)

Eyes

wide open (Redican, 1975), closed (Chevalier-Skolnikoff, 1974; Kavanagh, 1978; van Hoof, 1962), narrowed (Chavalier-Skolnikoff, 1974; Loizos, 1967; Voland, 1977; van Hoof, 1967; Marriott & Salzen, 1978), outer corners pulled up (Bolwig, 1964; van Hoof, 1967), drawn together (Bolwig, 1964; van Hoof, 1967), normal (Shirek-Ellefson, 1972; van Hoof, 1962).

Gaze

directed at partner (Preuschott, 1992), occasionally directed at partner (van Hoof, 1962, 1967; Weigel, 1979), eye to eye contact avoided (Chevalier-Skolnikoff, 1974; Marler, 1965), relaxed/unfocused (Bolwig, 1964; van Hoof, 1967).

Mouth

wide open (Freeman & Alcock, 1973; Maple & Zucker, 1978; Andrew, 1963; Kavanagh, 1978; van Hoof, 1967, 1972; Loizos, 1967; Chevalier-Skolnikoff, 1974), partially open (Fischer & Nadler, 1978; Chevalier-Skolnikoff, 1974; Marriott & Salzen, 1978), opened in an oval (or rounded) shape (Dolhinow, 1978; Weigel, 1979), closed (Kavanagh, 1978).

Mouth comers

retracted (Voland, 1977; van Hoof, 1967, Bolwig, 1964), partially retracted (Oppenheimer, 1977), retracted into a smile (van Hoof, 1967), rounded (Kirkevold et al., 1982; Preuschott, 1992), normal (Preuschott, 1992; Redican, 1975; Loizos, 1967).

Lips

relaxed (de Waal, 1988), pulled back into smile (Nickelson & Lockard, 1978), upper lip tense(tight)/curled over (or slid over) top teeth (Preuschott, 1992; Redican, 1975; van Hoof, 1967; Bolwig, 1964), lower lip tense/rolled inward (Preuschott, 1992), parted, covering teeth (Andrew, 1963; van Hoof, 1972; Chevalier-Skolnikoff, 1974).

Teeth

upper and lower teeth exposed (van Lawick-Goodall, 1968; van Hoof, 1967), lower teeth exposed (Voland, 1977; Preuschott, 1992; Redican, 1975; van Hoof, 1967; Loizos, 1967; Chevalier-Skolnikoff, 1974; Bolwig, 1964; Marriott & Salzen, 1978), no teeth exposed (Fagen, 1981; Andrew, 1963; van Hoof, 1972; ChevelierSkolnikoff, 1974; Oppenheimer, 1977; Pereira et al., 1988), only canines and incisors exposed (Weigel, 1979).

Brow

raised (Fischer & Nadler, 1978; Redican, 1975; Chevalier-Skolnikoff, 1974; Bolwig, 1964; Weigel, 1979), depressed (Bolwig, 1964), normal (van Hoof, 1962, 1967; Marriott & Salzen, 1978; Weigel, 1979).

Ears

flattened (Redican, 1975; Chevalier-Skolnikoff, 1974; Sussman, 1974; Weigel, 1979), normal/relaxed (van Hoff, 1967; Shirek-Ellefson, 1972; Marriott & Salzen, 1978; Weigel, 1979).

aMultiple citation for different states of the same facial element indicates that one species can exhibit multiple states for that character.

ner, but that it can actually be detrimental to this goal. Baldwin and Baldwin (1978) describe the play face of the howler monkey Aloutta palliata as an open mouth grin which is performed at one or two ann lengths away from the partner. At such a "safe" distance, use of

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this expression is more likely to be communicatory rather than essential for either playful attack or defense. In other species, such a grin or open mouth face may be combined with some other "nonessential" actions (e.g., shaking the head from side to side). For example, the woolly monkey Lagothrix lagothricha, may approach a partner with a grin, then shake its head violently before making contact (Andrew, 1963). Such combinations of gestures, however, can also precede other forms of amicable contact (Oppenheimer, 1973), and so are not restricted to play. Rapidly shaking the head from side to side, with or without other facial gesturing, has been reported in the play of a variety of species (e.g., Eisenberg & Kuehn, 1966; Kirkevold & Crockett, 1987; van Hoof, 1967; Watson & Croft, 1994). Again, such shaking of the head has no immediate functional utility for the attack of an opponent. It is also usually performed in an orientation that is visible or otherwise detectable by the partner, such as in the head shakes preceding play fighting in spider monkeys Ateles geoffroi (Pellis & Pellis, work in progress). For such signals to be useful in promoting playful contact, it would be expected that they be used more frequently in contexts of ambiguity (Symons, 1978a). Both the characteristic douc face and the head shake of the spider monkeys are performed more frequently when adults engage in play fights than when juveniles do (Kavanagh, 1978; Pellis & Pellis, work in progress). Therefore, both these nonessential gestures seem to be primarily performed for their function of promoting playful contact. Unfortunately, both these signals are general purpose ones, used for promoting several forms of amicable social contact, not only play (Kavanagh, 1978; Oppenheimer, 1977). If they are not unique to play, these signals cannot serve as unambiguous markers that distinguish play from nonplay. However, that they are used during play in these species shows that contact promoting signals can be used to facilitate play fighting in at least some situations. Even though vocalizations associated with agonistic threat appear to be rare during play fighting (e.g., snarl in lion play; Schaller, 1972), a large diversity of species have been reported to produce characteristic sounds during play fighting (e.g., Aldis, 1975; Fagen, 1981; Freeman, 1975; Hall, 1965; Henry & Herrero, 1974; Pellis, 1979; Poole, 1966; Rasa, 1984; Svihla, 1931). In many cases, the vocalizations produced are soft and low volume. Furthermore, changes in frequency of vocalizing (Rasa, 1984) or pitch structure (Goedeking & Immelmann, 1986) vary with the intensity of play, suggesting that these vocalizations are modulated by playful motivation (Biben & Symmes, 1986). In none of these reports, however, is evidence provided that causally links these vocalizations to the function of promoting play fighting, that is that they are play signals. There is evidence for some primates that the vocalizations they produce during play are signals, but not play promoting signals. Only in species with allomothering do the young produce play vocalizations, and as they are modified versions of infantile dislress calls, they may serve as possible signals for maternal retrieval (Masataka & Kohda, 1988). In squirrel monkeys Saimiri scuireus, this maternal attention getting function may have been expanded to stimulating vigilance in adult troop members (Biben & Symmes, 1986). A group of juveniles were placed in a separate enclosure from the troop adults. When the juveniles vocalized during play, the adult females not only became more vigilant, but they directed their attention five times more often toward an area from which a threat was likely to come, rather than to the juveniles themselves (Biben, Symmes, & Bernhard, 1989). These findings suggest that the function of vocal play signals in such cases is to engage the adults in protective behavior while the juveniles are vulnerable. Indeed, this function may account for the occurrence of play vocalizations during solitary play (e.g., Rasa, 1984). Again, while this example does not demonstrate that play signals are used to promote playful contact between individuals, it illustrates that signals are being used during play. Even though some examples of behavioral elements occurring immediately before and during play fighting meet the criterion proposed to qualify as signals, the unavoidable con-

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clusion is that purported play signals fail to qualify as unambiguous markers that can distinguish all play fighting from all nonplay. Such signals are neither consistently present in all play fights of species that possess them (e.g., Maple & Zucker, 1978), nor are they reported for all species that engage in play fighting (Fagen, 1981). Therefore, when present, they can and should be used to help distinguish play from nonplay; however, it is inappropriate to claim that play fighting can be routinely distinguished from immature serious fighting on the basis of play signals. It must be accepted that probably in the majority of cases animals can use contextual cues to discriminate between an approaching animal's playful versus nonplayful intentions. A major issue becomes that of identifying the contextual cues that are relevant to such a discrimination. Who is the playful initiator, and to whom the playful initiation is directed, seem to be obvious for such contextual cueing (Hayaki, 1985); however, so might be the style of the behavior, where timing, strength, and rhythm are important (Schwartzman, 1979). Why, then, are play promoting signals sometimes used? W H E N CONTEXT IS NOT E N O U G H

Because play fighting, like other forms of play, is most frequent during the juvenile phase, and the behavior patterns performed are typically divorced from the consequences arising from the serious use of such behavior (Fagen, 1981), most functional studies focus on the delayed benefits such playful activity may serve (Martin & Caro, 1985). Less attention has been directed to the immediate benefits of play (e.g., Barber, 1991; Geist, 1978). One possible immediate function of play fighting is that it may be used to establish and maintain dominance relationships, but this idea has been subject to considerable debate (e.g., Aldis, 1975; Carpenter, 1934; Symons, 1978b; Waiters, 1987). However, this debate has focused on juveniles. In contrast to the more affiliative pattern of play fighting by juveniles, postpubertal play fighting in a number of species has been reported to be rougher and more likely to escalate to serious aggression (e.g., Biben, 1986; Fagen, 1981; Geist, 1971; Takahashi & Lore, 1983). These rougher forms of play fighting are consistent with interactions reflecting competition for dominance (Humphreys & Smith, 1987). For example, Parquette (1994) has shown that in adolescent chimpanzees Pan troglodytes schweinfurtii, play fighting can be used by individuals as part of a strategy to increase dominance or to maintain dominance. Similarly, Neill (1976) reported that adolescent boys establish their dominance by increasing the intensity of their play, but once it has been established, more gentle forms of play are then used to maintain it. Of course, it is possible that play serves different functions at different ages. For example, juvenile play appears to be important for male rats to develop appropriate sexual performance, especially with regard to orienting to the partner (Larsson, 1978). In contrast, in sexually mature male rats, play appears to be involved in the maintenance of dominance-subordinance relationships (Pellis, Pellis, & McKenna, 1993). Other species may exhibit other kinds of idiosyncractic functions for play (Coppinger & Smith, 1989), and evolutionarily, current functions may differ from ancestral functions (Byers, 1984). As suggested in the study by Neill (1976), play fighting postpubertaily can be used in two forms, a gentler version that serves to maintain affiliation, and a rougher version that serves to establish dominance. This possibility is further supported by the finding that whereas popular boys use more affiliative play fighting within the group, unpopular boys tend to use a rougher, more competitive form of play fighting when they engage in play with the more subordinate members of the peer group of popular boys (Pellegrini, 1988, 1989). In rats., play fighting does not appear to be necessary to establish dominance-subordinance relationships prepubertally, but does seem to be used postpubertally by subordinate males to maintain familiarity with the dominant (Pellis & Pellis, 1991, 1992, 1993). Therefore, play fighting may be useful for either maintaining social relationships or probing and testing them. That

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play fighting may have these two distinct social functions is further supported by the sparring fights of cervids (i.e., deer). Sparring, in many ways, is similar to what has been described as play fighting in other mammalian species, and is clearly distinguishable from dominance fights, where injury and death are not uncommon (Geist, 1982). Importantly, even though similar for most deer species reported, the function of sparring can differ. For example, in Old World deer, and recent derivatives in the New World (e.g., elk Cervus elephus, reindeer Rangifer tarandus), sparring may provide a tactile assessment of fighting ability, and so may help to establish dominance relationships before the rut (Barrette & Vandal, 1990; Geist, 1982). In contrast, for New World deer Odocoileus spp, sparring is initiated by younger males to develop and maintain a coalition with a dominant buck (Geist, 1981). Therefore, in the first case, deer are using a more playful form of combat to establish dominance and so are reducing the risk of escalated fighting during the rut, while in the second case, deer are using sparring to affiliate with a dominant animal, which may permit the younger buck access to females and to intimidate other adult bucks. We suggest that the primary function of postpubertal play fighting is that of social manipulation, either to recruit or maintain "friendships," or to improve one's status position in the group. For the latter purpose, one animal has to test and probe its relationship with another. If such probing reveals weakness, the performer can increase the intensity or roughness of play or even switch to more explicitly agonistic behavior. In this way, the performer may intimidate the opponent, thus gaining access to current or future resources (Fagen, 1981). But what if such rough play meets with strong resistance? The problem is then to back down, or de-escalate the encounter. An amicable signal that conveys the message "it was only play" would be invaluable. Play fighting in humans provides an insight into the functional utility of such a signal. As already pointed out, the most frequently reported gesture to be regarded as a play signal is the open mouth play face of primates. Unfortunately, given that biting the opponent is the most frequently occurring goal during the play fighting of most primate species (Aldis, 1975; Symons, 1978a), it becomes difficult to distinguish between opening the mouth to bite and opening the mouth to signal play intention. Recall Fagen's (1981) definition that a play signal has to be nonessential to the play fight. In humans, play fighting involves grabbing, pulling, kicking, punching, and holding the opponent on the ground, but biting is rarely reported (Aldis, 1975; Blurton-Jones, 1967; Fry, 1987). In addition, it has been postulated that laughing, a facial and vocal expression strongly associated with play fighting in humans (Blurton-Jones, 1967, 1972), is derived from the primate open mouth play face (van Hoof, 1972). In contrast, frowning is highly correlated with aggression, and occurs rarely in play fighting (Blurton-Jones, 1967, 1972). The association between laughing and play fighting, and frowning and serious fighting, has been shown in a number of studies, and appears to be robust across cultures (see Boulton, 1994, for review). Further, both adults and children rate such facial expressions highly when asked their criteria for recognizing play fighting (Costabile et al., 1990; Smith & Lewis, 1985). From all this evidence it may be concluded that play fighting can be reliably distinguished from serious fighting by both participants and observers using the laughing facial expression as their key cue. Importantly, such a ubiquitous signal would reduce the likelihood of an accidental escalation to serious fighting when play fighting. A closer analysis of the evidence suggests a more subtle use for laughing and related facial gestures. When asked to rate videotaped sequences of social encounters as either playful fighting or serious fighting, 8-11-years-olds reported using facial expressions to rate behavior as play in only about 5% of cases (Boulton, 1993a). It is possible that such a low rating is due to the low visibility of facial gestures in videotaped sequences (Boulton, 1994). An alternative explanation is that when asked, people report the most obvious and easy manner to describe features of overt behavior. When asked to actually evaluate a real encounter, observers use more subtie cues relating to the manner in which actions are performed, something that is much more

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difficult to describe and concisely report. Indeed, studies show that when asked a priori to rate behavior as being play or not, subjects claim to use facial gestures, but when asked to rate actual encounters, they predominantly use the actions of the interactants to make their judgments (Costabile et al., 1990; Smith & Lewis, 1985). Further, even though not common, some episodes of play fighting, which were reported as such by the participants, involve frowns (Boulton, 1991). This clearly shows that even in the presence of a facial expression associated with aggression, children can still recognize play. Therefore, when observing others engaging in play fighting, or when so involved oneself, it would seem that subtle cues about the context and manner of movement are being used to identify play. When engaged in play, however, a participant is not always privy to the actions of the partner. In 79 cases of serious fighting observed in school grounds, 14% arose when a playful assault received an aggressive retaliation (Boulton, 1993b). Such episodes suggest that there are contexts in which the intentions of the initiator are ambiguous. This is well illustrated by an example given by Aldis (1975). A boy pushed another boy into a swimming pool from behind. The boy then emerged from the water and turned to face the perpetrator. They then engaged in further playful contact when the perpetrator laughed. If the perpetrator had maintained a stern look, we suspect that the boy in the pool could easily have interpreted the push as unfriendly. Another example, from Desmond Morris' television series The Human Animal (episode 6 "Beyond Survival"; a BBC production, 1994), also illustrates the timing of signaling in an encounter. Three boys are play fighting: two are engaged in mock boxing and kicking, when the third approaches from behind one of the others and gives him a round house kick to the head, knocking him to the ground. During the approach and the kick, the perpetrator has a relaxed or a concentrated expression on his face. As the victim turns to face the perpetrator, the latter laughs and then withdraws backward while maintaining a face-to-face orientation with the boy he kicked. Again, by laughing, the boy may be signaling that the kick had been a friendly one. In both the examples given above, the attacking boy only exhibits the play expression when his partner responds to his action by turning to face him. Therefore, the play signal is used tactically during the encounter to convey a specific meaning about how the preceding action should be interpreted. Smiling, which appears to be a more general purpose affiliative signal 3 (Lockard, Fahrenbruch, Smith, & Morgan, 1977), is reported not only to promote

3Laughter and smiling were at one time considered to be part of a continuum of graded intensities. Van Hoof (1972) later suggested that they derived from two distinct phylogenetic precursors, "the relaxed open mouth face" and the "silent bared-teeth display," respectively. Detailed contextual analyses of these two patterns in both infra-human primates (e.g., Preuschroft, 1992), and humans (Lockard et al., 1977) have shown that the former is associated with play, whereas the latter is associated with other forms of amicable encounters. Therefore, in this view, laughter is the homolog of the primate play face (van Hoof, 1989). However, in some species, such as mandrills Mandrillus sphinx, gelada baboons Theropithecus gelada (van Hoof, 1967) and Tonkean macaques Macaca tonkeana (Thierry et al., 1989), the silent bared teeth display has been exaggerated and apparently used in the place of the relaxed open mouth face. Furthermore, even though laughter is used in more playful contexts, and smiling in more tense social interactions, smiling has also been incorporated into more playful settings in humans (Lockard et al., 1977). Similarly, various grades of grinning (grimacing) has been noted in the play of other species (e.g., Baldwin & Baldwin, 1978; Dolhinow, 1978; Goodall, 1965). Therefore, while it seems likely that laughter and smiling have separate origins, there is evidence for a convergence of function in at least some species. Whether these speculations are correct or not, the presence of two graded affiliative facial signals, and their possible interaction, provides much opportunity for subtle signaling during play. Indeed, it may be due to this blending of different signals that such difficulties in being able to isolate the play face occur (see Table 1). As noted by Schwartzman (1979), "I wish to play with you" or "'this is play" may not be a static signal, but rather, a flexible repertoire that can deal with the dynamic changes during play.

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playful contact, but also to act as appeasement during intensive social encounters, diffusing possible misunderstandings (Fridlund et al., 1990; Goldenthal, Johnston, & Kraut, 1981). Indeed, Fridlund (1994) suggests that using smiling during play may say "don't take me seriously" (p. 305), which is precisely the kind of signal needed for the de-escalation described above. However, humans have more cortical control over their facial expressions than do infra-human primates (Gazzaniga & Smylie, 1990), and so the use of such subtle, highly precise play signals may not be as readily available to other animals. Nonetheless, two exampies illustrate how such signals may be used to advantage. Chimpanzees have been reported to use attention-getting gestures so as to get play partners to look at their play faces (Tomasello, Geist, & Frost, 1989). One female gorilla has been reported to use her hand to hide her play face and thus delay the onset of playful contact (Tanner & Byrne, 1993). In both cases, the animals may be using some alternative method to modulate the signal value of an emotional expression. Alternatively, there may be subtle modifiers to the facial expression during play fighting. As already noted in Table 1, in the so-called play face, each part of the face can occur with different configurations; variations on the arrangement of these components may provide subtle differences in meaning (e.g., Zeller, 1986). For example, based on Goodall's (1965) description of facial gestures in chimpanzees during play fighting, Loizos (1967) notes that in socially ambiguous situations, the increased baring of the teeth in the play face may act as a form of appeasement, given that the grin has an appeasement function. Play fighting in the service of complex social manipulation is more likely to produce ambiguous contexts and, hence, require the use of signals that can clarify the meaning of an action. Given that such manipulative play fighting is more likely to be used postpubertally, then the appropriate signals needed to rectify mistakes would be expected to be completely developed by sexual maturity (e.g., Poole, 1978). CONCLUSIONS Play fighting is not distinguishable from serious fighting by either the absence of threat signals nor by the presence of unique play-promoting signals. For some species, under some conditions, such criteria may well be useful for making this distinction. In Steller sea lions, for example, the young perform a head toss during playful encounters that does not occur in adults (Gentry, 1974). However, as shown in this paper, these criteria do not have universal applicability. If play fighting is not merely low intensity or immature aggression, then there have to be objective, empirical grounds by which play fighting can be justifiably classified as a separate category of behavior. The criteria, other than the presence of play signals, that are used in most definitions of play (see Appendix A in Fagen, 1981) do not unambiguously apply to play. Whether objective criteria can be established to distinguish between playful and serious fighting awaits empirical determination. Nonetheless, whether play signals are unique to play fighting or not, evidence has been presented that indicates that under some conditions, some species do seem to use signals that promote playful contact. The issue is why they are used when they are. We suggest that if the play fighting of some species functions to test and probe social relationships (Fagen, 1981), especially postpubertally (Parquette, 1994), then play signals may be useful to manipulate the situation to the best advantage of the performer. For instance, if one animal increases the aggressiveness of a play encounter, and the opponent shows weakness, then dominance can be asserted. However, if the opponent exhibits a willingness to escalate the encounter to a more aggressive level, the initial animal may use a play signal to diffuse the situation. This view predicts that such signals should be used retroactively by the animal making the initial escalation. Conversely, if some age or dominance asymmetry is already present and obvious, the superior animal may need to signal playful intent. For exam-

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pie, dominant coyotes are more successful in soliciting play with subordinates when the encounter is preceded by a play bow (Bekoff, 1974). Alternatively, the subordinate may need to signal its friendly intent. For example, adult subordinate male rats continue to rotate to supine when contacted playfully by a dominant male rat (Pellis & Pellis, 1992); this may signal their submissiveness (Pellis et al., 1993). As different species may use play fighting in somewhat different ways to modulate social relationships (Parquette, 1994), the exact role that play promoting signals may serve in each species cannot, at this stage of our understanding, be prejudged. A review of some of the literature on play fighting by humans supports the view that under most circumstances, both participants and third party observers are able to distinguish play fighting from serious fighting by the performers' actions. However, facial gestures are sometimes used to make such a distinction. The little anecdotal evidence available supports the hypothesis that such an obvious signal as laughing can be used tactically when there is a danger of the playful encounter escalating to a more aggressive level. Species in which the presumed play signals are not directly relevant to attack and defense during play fighting, such as the laughter of humans and the head shaking of some other mammals, are the most appropriate for more detailed analyses of the role of play signals in play fighting. Given that some signals used to promote playful contact may be unique to play, whereas others (probably the majority) are general purpose signals promoting amicable contact in many social contexts, we suggest a terminological modification. That is, signals that are useful in initiating and maintaining play should be referred to as play promoting signals, not play signals. After all, some play signals may serve to stimulate parental protection (Biben et al., 1989), or block further contact (Pellis, 1981, 1984; Pellis & Pellis, 1994). Using play signals as a unitary category can lead to any signal that occurs in play being so classified, even though the term play signal has a specific functional implication (i.e., promoting playful contact). The classification of signals that occur in play into more diverse functional categories would enhance not only the analyses of such signals, but also the communication among researchers.

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