Aggressive Play and Communication in Rhesus Monkeys (Macaca mulatto)

Transcription

1 AMER. ZOOL., 14: (1974). Aggressive Play and Communication in Rhesus Monkeys (Macaca mulatto) DONALD SYMONS Department of Anthropology, University of California, Santa Barbara, California SYNOPSIS. One adaptive function that has been suggested for social play in higher primates is the learning, refining, or practicing of communicative skills. Despite the absence of experimental data, a comparison of the structure of aggressive play and communication may shed light on this hypothesis. The great majority of rhesus monkey agonistic interactions are mediated by stereotyped signals. Deprivation experiments have shown that appropriate interpretation and use of such signals requires early social experience. Such experience seemingly must have the following characteristics: (i) The relevant agonistic signals must occur, (ii) These signals must regularly be paired with other stimuli for appropriate responses to signals to be learned. Signals must produce regular responses in other monkeys for appropriate use to be learned. Aggressive play seems to be an unpromising context in which to learn, refine, or practice agonistic signals. These signals are not observed in play, and the signals that do occur are restricted to play and are not regularly paired with unconditioned stimuli. One reason for attempting a detailed description of aggressive play is to throw light on the adaptive functions of this activity (Symons, 1973). Kummer (1971) noted that the question of adaptive function is a key issue in the study of any pattern of behavior. Since immature animals of many species spend so much time and energy playing, play must be adaptive in that it must contribute to reproductive success (Loizos, 1967; Dolhinow and Bishop, 1970), for if it did not, playing animals would be at a selective disadvantage. Some writers have attributed the long period of immaturity in many higher animals to the necessity for youthful play (Groos, 1898; Washburn and Hamburg, 1965). Although many possible adaptive functions have been suggested for the play of nonhuman primates (see Symons, 1973, p. 165), there is little experimental evidence on this question. Miiller-Schwarze, in his 1971 review of ludic behavior in young mammals, wrote: "The amount of time and The field work discussed in this paper was partially supported by a Public Health Service grant number I wish to thank Naomi Bishop, Elvin Hatch, and Charlotte Symons for their critical comments on the manuscript. 317 paper spent on speculations on possible functions of motor play in immature animals is in inverse proportion to the amount of facts available on this question" (p. 240). As evidence for the importance of play, many writers have cited the experiments of Harlow and his associates that demonstrate severe behavioral deficits in rhesus monkeys {Macaca mulatto) raised without peers. Prolonged social deprivation produces monkeys which subsequently exhibit inadequate social and nonsocial play, avoid physical contact with other monkeys, are sexually incompetent, and are unable to inhibit aggression (Harlow, 1969; Harlow and Harlow, 1969). However, in such experiments there are many restrictions in addition to lack of play opportunity, and it is difficult to determine which of the restrictions are responsible for alterations in later behavior (Hinde, 1966; Marler and Hamilton, 1966; Bekoff, 1972). Dolhinow and Bishop (1970) write: "The problem remains whether it is peer contact or the act of playing that results in normal behavior, and this would be very difficult to test experimentally" (p. 175). The experimental difficulty clearly is that, when immature monkeys are allowed peer contact, they play.

2 318 DONALD SYMONS Several students of primate behavior have suggested that one important adaptive function of social play is the development of communicative skills (Mason, 1965). For example, Jolly (1972, p. 261) writes that in play young primates "... learn the physical gestures of communication. If one prefers not to say 'learn,' the practice certainly refines these gestures and increases the sensitivity of their use..." Dolhinow (1971, p. 69) writes: "Social cues and complex communication patterns are developed in the relative safety of play." Despite the absence of conclusive experimental data, it may still be possible to bring some evidence to bear on this hypothesis. In this paper I consider the structure of rhesus aggressive play and aggressive communication in order to answer the question whether rhesus monkeys learn, refine, or practice agonistic communication in aggressive play. COMMUNICATION Altmann (1967) described "communication" as the process whereby the behavior of one individual affects the probability of behavior of another. This very broad definition would include such acts as eating. I will use "communication" to refer only to acts that are specialized for this process, that is, acts which serve no important function in addition to communication (Altmann, 1967, p. 337). Higher primates communicate with recurring clusters of expressive elements primarily facial gestures, postures and vocalizations which may be characterized as signal patterns (Shirek-Ellefson, 1972). Such signals are often said to inform recipients of the "mood" of the signaller. Operationally, this means that the signaller expresses the probability that it will or will not engage in specific activities (Rummer, 1971). Agonistic signals indicate the likelihood of attack and flight. AGONISTIC COMMUNICATION IN RHESUS MONKEYS The communicative repertoire, especially the agonistic repertoire, of rhesus monkeys has been well described (Altmann, 1962; Hinde and Rowell, 1962; Rowell and Hinde, 1962, Sade, 1967) and there is substantial agreement among the descriptions. Agonistic communication varies along a continuum (Sade, 1967) and will be only broadly summarized here. Sade (1967) described an intense aggressive encounter he witnessed as follows: "... the attacking monkey charged, roaring and batting at another, then grabbed and held the victim while biting him on the back. As the attack began, the victim cowered away, grimacing and shrieking, presenting his hindquarters to the attacking monkey at the same time. Almost immediately the victim leapt away and fled, still shrieking and grimacing, and finally escaped after being bitten" (p. 100). The great majority of rhesus agonistic interactions, however, do not involve actual physical contact for they are mediated by signals. Gestures of attack, usually called threat, include lunging, jerking the head, or slapping the ground toward another monkey, staring with the eyes wide open, barking (also called growling or roaring), and giving an open-mouth threat, in which the mouth is open and tense with the lips covering the teeth. Piloerection often accompanies these signals. The usual responses to such a threat include presenting the hindquarters, fleeing, crouching or cowering, looking away, squealing or squeaking, and grimacing, a gesture in which the lips are retracted, exposing the clenched teeth. These signal-mediated interactions should be contrasted with fighting, defined here as an agonistic interaction in which there is physical contact and both animals act aggressively. THE DEVELOPMENT OF COMMUNICATIVE SKILLS The basic form of these gestures, postures, and vocalizations occurs unlearned in monkeys raised in social isolation (M0ller et al., 1968). There is, however, convincing evidence that rhesus monkeys require social experience to appropriately use and understand these signals. Mason has even suggested that the social inadequacies found among rhesus raised in social isolation are largely a result of failure to acquire communicative skills. Mason (1961a) writes: "Among the specific factors which are responsible

3 PLAY AND COMMUNICATION IN RHESUS MONKEYS 319 for orderly social interactions, species-specific gestures appear to be of particular importance.... The behavior of Restricted monkeys suggests that the effective development of these elementary forms of social coordination and communication is dependent upon learning" (p. 290). In a later paper Mason (19616) concludes: "... one of the consequences of social restriction is failure to acquire effective elementary communicative skills "which serve to coordinate and control the form and direction of social interactions" (p. 698). Miller et al., (1967) have experimentally confirmed Mason's hypothesis. They trained feral rhesus and rhesus that had been raised in total social isolation for the first year of life to perform an instrumental response (bar pressing) to a visual stimulus to avoid shock. All monkeys readily learned this response. Then the monkeys were paired in all possible combinations in a "cooperativeavoidance" paradigm in which the conditioned stimulus was presented to only one of the pair (the sender) who lacked the response bar. The facial expression of the sender was transmitted via closed-circuit television to the second of the pair (the receiver). The receiver did not see the conditioned stimulus but did have available the bar which allowed both monkeys to avoid the shock. The experimenters found that feral monkeys were able to utilize the facial expressions of other ferals to avoid shock. However, ferals were unable to utilize the expressions of isolate monkeys, suggesting that isolates were ineffective senders of communicative signals. Isolates were also poor receivers, whether the senders were ferals or isolates, suggesting they had failed either to interpret or attend to socially significant visual signals. A second experiment also supports Mason's hypothesis. Normal adult rhesus monkeys usually avoid mutual eye contact, presumably because this gesture (staring) is a mild rhesus threat. However, Mitchell (1972) has shown that rhesus raised in social isolation for the first 6 to 12 months of life do not subsequently avoid eye contact. Mitchell found that adult male isolates would often return to stare into a feral male's eyes after having just been beaten by that feral in a fight. Such staring generally precipitated another fight. Sackett (1966) has shown that open-mouth threat produces unlearned fear responses in infant rhesus monkeys. Monkeys were raised in isolation from birth to 9 months. During this time, the only visual input they received was colored slides of monkeys engaged in various activities, and control slides of non-monkey subjects. In one procedure^ the experimenter controlled the input, scoring the monkeys' reaction. In a second procedure the monkeys were allowed to leverpress to expose specific slides. Sackett found that in monkeys from 2.5 to 4 months of age, pictures of open-mouth threat elicited a high frequency of disturbance behaviors (rocking, huddling, self-clasping, fear, and withdrawal), and that during this period there was a marked decline in lever-pressing to expose slides of threat. However, these disturbance responses waned about 110 days after birth. Sackett suggested that waning occurred because the consequences that sometimes follow threat in the normal environment were absent in the test situation. In a later review of the role of experience in the development of rhesus monkeys Sackett and Ruppenthal (1973) reached the following conclusion: "... although the development of monkey infants may include complex, unlearned responses underlying social attachment and communication, the mere existence of unlearned processes does not ensure adequate development. Such unlearned responses, that provide a bias toward biologically appropriate behavior, must seemingly be reinforced by specific experiences during infancy" (p. 83). If Sacket and Ruppenthal are correct, the question then becomes, "What are the specific reinforcing experiences underlying the development of agonistic communication, and does aggressive play provide such experiences?" There seem to be two requirements for such reinforcing experiences: (i) The relevant agonistic signals must, in fact, occur, (ii) These signals must be regularly paired with some other stimuli for appropriate responses to signals to be learned. For example, a monkey playing a dominant role by giving threat, or threat-like signals must follow these signals with attack, or attack-

4 320 DONALD SYMONS like, behavior. Submissive signals must be similarly followed by flight, or at least by non-attack, by a monkey playing a subordinate role. A signal must produce a regular response in another monkey for appropriate use to be learned. For example, a threat by monkey A must regularly produce counterthreat by monkey B or submission by monkey C. It is therefore worth examining aggressive play with the above requirements in mind. AGGRESSIVE PLAY AND COMMUNICATION IN RHESUS MONKEYS The following description is based on my recently completed study of aggressive play in a group of free-ranging rhesus monkeys (Symons, 1973). This work consisted of 300 hr of close-range field observation made over a 6-month period in on La Cueva Island in Puerto Rico, and the study of approximately 2650 ft of super-eight, high speed (54 frames per second) motion picture film which were taken during field work. Aggressive play is considered to consist of two intergrading types of behavior, playfighting (rough-and-tumble, or contact play) and play-chasing (approach-avoidance, or noncontact play). Play-chasing is self-explanatory, the animals often adopting gaits, such as gamboling or staggering, which are restricted to the play context. Play-fighting is a structured activity in which monkeys seem to attempt simultaneously to bite and not be bitten. For example, a monkey lying on its back and being bitten on the throat may reach behind the head of the biter, grasp the skin, and pull the biter's head back. Alternatively, the monkey being bitten may curl and push the biter's head away with its feet. Or it may push the biter's head away with a hand. These movements have in common that the bite is broken. However, specialized agonistic visual and auditory signals were not observed during the 2351 play-fighting and 662 play-chasing bouts observed in the field at close range between individually known monkeys, nor were such signals seen in the analysis of motion picture film. A variety of gaits, postures and gestures occur before play-fighting sequences, all of which, except ear flattening and eyelid exposure, are confined to the context of play. These actions may be roughly divided into those that seem to indicate intention to play (i.e., are given by an approaching monkey) and those that seem to invite or solicit play (i.e., are given by a stationary animal or one moving away from the invited partner). In practice these are not genuinely discrete categories. No signals are seen that are exclusively used by an approaching monkey, but some, by their nature, preclude approach by the signaler. The two movements sporadically observed in a play context that are also seen in other contexts are flashes of the unpigmented eyelids and ear flattening. Shirek-Ellefson (1972) observed lowering of the eyelids occasionally before and during the social play of crab-eating macaques (Macaca irus). She notes that in crab-eating macaques exposure of the unpigmented eyelids is the mildest form of "pucker face," a gesture predictive of a variety of non-agonistic approaches. Simple exposure of the eyelids has not been reported in rhesus. Ear flattening is rarely observed before rhesus play. This movement occurs as a component of a variety of communicative gestures in rhesus monkeys including open-mouth threat, fear grimace, and lip-smacking, a gesture sometimes accompanying non-agonistic approach (Altmann, 1962; Hinde and Rowell, 1962; van Hoof, 1967; Sade, 1967). Ear flattening alone has not been reported to be a social signal in rhesus monkeys. In the context of play it seems to function as part of play soliciting and is sometimes given by a monkey about to move away from the partner being solicited. Play-fighting mimics fighting behavior, previously defined as an agonistic interaction with physical contact in which both animals act aggressively. Since fighting in rhesus monkeys has never been studied, fighting and play-fighting cannot be compared in detail. The fundamental difference is probably that play-fighting is slower in tempo and more inhibited. For example, no bite made in play was ever observed to break the skin. Unlike fighting, play-fight-

5 PLAY AND COMMUNICATION IN RHESUS MONKEYS 321 ing among animals of all ages is silent and piloerection does not occur. However, if play-fighting and agonistic interactions in general are compared, it has been noted that the overwhelming majority of agonistic interactions in rhesus monkeys involve not fighting, but only gestures of threat and submission. Even when there is contact, actual fighting does not usually occur because the attacked monkey reacts submissively rather than fighting back. Play-fighting in rhesus monkeys does not mimic these agonistic interactions. In rhesus aggressive play there are no gestures of threat or submission. In fact, one of the conspicuous features of play-fighting is that neither monkey adopts a submissive role. When a rhesus monkey is "play-attacked" it usually responds with play-fighting. This is in striking contrast to most normal adult aggression in which the response to attack by a dominant monkey is submission by the subordinate. The only facial expression consistently observed in aggressive play is the relaxed open-mouth face, or play-face, a gesture that occurs only in the play context. The primate play-face has been extensively discussed (Altmann, 1962; Goodall, 1965; van Lawick-Goodall, 1968; Loizos, 1967; van Hoof, 1967, 1972). There is general agreement that this gesture communicates (or metacommunicates) a playful mood, the intention to play-fight but not to fight. This gesture is regularly given by an approaching monkey about to initiate play, by the approached monkey, and by a stationary monkey about to turn and gambol or stagger away from a potential play partner in play solicitation. It is predictive only of play, not of any specific subsequent movement. CONCLUSION Aggressive play seems to be an unpromising context in which to learn, refine or practice agonistic signals. Neither requirement for appropriate reinforcing experiences is met by aggressive play. First, agonistic signals are absent from play. Signals that do occur in play are not used in other contexts. Second, if Sackett and Ruppenthal (1973) are correct in suggesting that rhesus monkeys require reinforcement to learn appropriate responses to communicative signals, then a to-be-conditioned stimulus (e.g., open-mouth threat) must be paired with an unconditioned stimulus (e.g., being bitten). For a monkey to learn to use a signal appropriately the signal (e.g., staring) must reliably produce a response (e.g., attack or flight) in another monkey. In aggressive play the gestures that do occur are not reliably followed by specific acts, and do not produce specific responses. For example, a playface is usually followed by approach by the gesturing monkey, but the monkey may remain stationary or move away from a play partner. A play-face given by one monkey may produce approach or play-flight in a second. Even if certain gestures of play-fighting were similar enough to adult rhesus agonistic communication for transfer of training to occur, such learning would be inappropriate. The response to a play-face is usually to give a play-face, approach and play-fight; the response to open-mouth threat, which play-face somewhat resembles, is usually to flee or to give a submissive gesture. The entire structure of play-fighting is unlike most rhesus agonistic situations. In a play-fight, both monkeys adopt the same, active fighting role. In agonistic situations, one monkey usually adopts the dominant role, giving threat signals, and the other the subordinate role, giving submissive signals. This is not to deny that aggressive play may facilitate the development of agonistic communication in rhesus in general ways such as familiarizing monkeys with each other, increasing physical tolerance to conspecifics, or habituating monkeys to looking at faces for meaningful social signals. However, the context of aggressive play does not seem to provide the necessary opportunities or contingencies for the learning, practicing, or refining, in the ordinary sense of these words, of agonistic signals.

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