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12-1972 The evelopmeD nt of Social Interaction, Play, and Metacommunication in Mammals: An Ethological Perspective Marc Bekoff Washington University, [email protected]
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Recommended Citation Bekoff, M. (1972). The development of social interaction, play, and metacommunication in mammals: an ethological perspective. Quarterly Review of Biology, 412-434.
This Article is brought to you for free and open access by the Humane Society Institute for Science and Policy. It has been accepted for inclusion by an authorized administrator of the Animal Studies Repository. For more information, please contact [email protected]. THE DEVELOPMENT OF SOCIAL INTERACTION, PLAY, AND METACOMMUNICATION IN MAMMALS: AN ETHOLOGICAL PERSPECTIVE
BY MARC BEKOFF
Department of Psychology, Washington University St. Louis, Missouri 63130
ABSTRACT
Analysis of the dynamics of the ontogeny of social interaction is of critical impor- tance in order that behavioral development may be comprehended in its own right, and the relationship between infant and adult behavior understood. In this review, general concepts of behavioral development in mammals are discussed and analyzed, and the many variables that are involved are considered. When it is impossible to control or observe the social interaction of the developing organism in its natural environment, captive subjects should be used. There is increasing evidence that results obtained with the latter are related to social organization observed in the wild. Play behavior is operationally defined on the basis of a comprehensive review of the literature and of personal observations of the social development of canids. The essential "'need" for social interaction during infant life is discussed, as is the phe- nomenon of behavioral neoteny. The concept of metacommunication, and its rela- tionship to social development are analyzed, and the role of ritualization in the evolution of metacommunicative signals is considered.
GENERAL CONCEPTS OF BEHAVIORAL ONTOGENY All behavior presents us with a problem in development (Manning, 1971). In order to be A N UNDERSTANDING of the dy- able to understand adult social behavior, we namics of the ontogeny of social must know something of its development behavior is of critical importance (Clark, Wyon, and Richards, 1969), and the to evaluation of adult behavior. study of development cannot be separated Recently this problem has been from the study of the functions of the adult extensively reviewed in volumes animal (Tinbergen, 1951). However, attempts by Foss (1961, 1963, 1965, 1969), Newton and to analyze social interaction and social develop- Levine (1968), Bowlby (1969), Mussen (1970), mental processes in infants in terms of char- Tobach, Aronson, and Shaw (1971), Moltz acteristics that are only applicable to experi- 1971a), Schaffer (1971), and Denenberg (1972). enced organisms produce misleading and Fox (1971a) has recently reviewed the litera- ture and has also presented original experi- often meaningless results (Bekoff, 1972). As ments concerned with understanding the inte- Welker (1971) has stressed, concepts based grative development of brain and behavior in entirely on behavioral phenomena of mature canids, and Horwich (1972) has studied the animals cannot be used in understanding the ontogeny of social behavior in the gray squirrel behavior of neonatal animals. Indeed, the in great detail. Russian contributions to the mature behavioral repertoire itself can be un- field of behavioral ontogeny have recently been derstood fully only if its ontogenetic origins reviewed and summarized by Kovach (1971) are known (Welker, 1971). The behavior of a and by Slonim (1969, 1972). child must be viewed as being adapted toward
412
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survival as a child, as well as toward acquiring vestigating social interaction, the unit of information for later life (Blurton Jones, analysis should involve discrete motor action 1972a). patterns (e.g., Wiepkema, 1961; Grant, 1963; The use of the comparative approach (e.g., Nelson, 1964; Altmann, 1965; Poole, 1966, Lorenz, 1950) is valuable. By comparatively 1967, 1972; Lerwill and Makings, 1971; Rey- studying behavioral development, a compre- nierse, 1971; Stanley, 1971; Fox and Clark, hension of the causation and function of 1971; Bekoff, 1972; Blurton Jones, 1972b; species-characteristic behavior patterns may be McGrew, 1972) that are relatively simple, ob- realized. Lehrman (1962) wrote that a full servable, and measurable (Welker, 1971). In understanding of the organization and causa- this way, the time of first appearance of specific tion of behavior patterns can only be achieved actions (and sequences) may be noted, and by analysis of ontogeny; and Schneirla (1966) changes over time (in frequency, amplitude, or declared that behavioral ontogenesis is the motivational context) may be observed. Pre- backbone of comparative psychology. There- mature lumping must be avoided so that data fore, the comparative ontogenetic approach is are not lost irretrievably (Altmann, 1965), a powerful tool for studying social behavior. and if later analysis warrants, it is possible The two most important aspects of the that data may be lumped (e.g., action patterns ontogeny of social behavior are (1) the develop- combined) into a more manageable number of ment of control of agonistic behavior (e.g., categories. The recognition of individual ele- Scott, 1958) and the formation of dominance ments permits later quantitative description relationships; and (2) the development of non- and determination of relationships of the ele- agonistic social interactions (Bekoff, 1972). ments with each other (Russell, 1970). Although the present review is concerned with
the latter aspect, it must be stressed that an STUDIES IN CAPTIVITY overall analysis of the development of social interaction must account for both. For ex- Often the laboratory is the only place where ample, social deprivation experiments not only for certain species behavioral observations such deprive the developing organism of playful as those described above are possible; for a interactions, as is so often suggested (see number of important reasons, the natural Glickman and Sroges, 1966), but of all types habitat of the animal may be an unsuitable of social intercourse (see below). locale for making detailed observations of social The initial step of any developmental (and interaction - e.g., "who" did "what" to behavioral) study should be the establishment "whom," "how many times," and "when" (at of ethograms (a behavioral repertoire) and what age and in what motivational context) sociograms of the animal (s) under study (Tin- (Bekoff, 1972). Some of these reasons are as bergen, 1951; Russell, Mead, and Hayes, 1954; follows: (1) inability to control social interac- Hutt and Hutt, 1970). Smith and Connelly tion; (2) inability to identify particular in- (1972) have emphasized this point by writing dividuals; (3) interference by adults; and (4) that the most powerful tool in the ethologist's the fact that young animals often do not armory is the description of specific motor emerge from the den or are not weaned until patterns. To avoid premature (and irrelevant) well after the critical period of social develop- experimental manipulation, it must be known ment has passed. Behavior observed in cap- what behavior there is to be modified (Hutt tivity may be of great importance in the natural and Hutt, 1970), and also the normal range of environment, even though field workers have individual differences within a given species. not yet described it (Chance, 1962). As stressed A representative ethogram is presented in by Hopf (1970), hand-rearing is an indispensa- Table 1 (after Bekoff, 1972). Nelson (1964) has ble prerequisite to controlling environmental correctly pointed out that it is important to influences on an animal; by being able to follow realize that an analysis of behavior may in- the development of particular identifiable in- volve units as small as a muscle twitch or as dividuals, questions pertaining to development large as an entire pattern such as migration. can be answered (Birch, 1971; Lorenz, 1961). For behavioral studies concerned with in- In primates, Harlow and Harlow (1966) have
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TABLE 1
A developmental ethogram of motor action patterns in canids: category and code (after Bekoff, 1972)
I. NEONATAL (CONTACTUAL) - MAINTAINING SOCIAL PROXIMITY Chin-rest CR Contactual-circling CC Face-lick FL Inguinal response IR
II. AGONISTIC - INCREASING SOCIAL DISTANCE
Offensive Defensive Incomplete standing-over ISO Back-arch BA Standing-over SO Distress vocalization DV Aggressive vocalization AV Defensive gape DG Submissive grin SG
III. PASSIVE-SUBMISSIVE
aRolling-over RO aFace paw FP
IV. ACTIVE-SUBMISSIVE AND PLAY - DECREASING SOCIAL DISTANCE
Play-soliciting PS Self-play SP Rolling-over RO Leap L Leap-leap L-L Tail-wag TW Approach A Tail-wag approach TWA Exaggerated approach EA Face-paw FP
V. PLAY-FIGHTING AND AGONISTIC
Head-shake Hsh Hip-slam HS Approach/withdrawal A/W Scruff-bite intention SBI Scruff-bite SB Face-bite intention FBI Face-bite FB Face-bump FBp Face-paw FP General-body bite GB (leg, flank, etc.)
a Observed in different motivational contexts.
reported that their laboratory animals show the 1970; Fox, pers. commun.; Bekoff, pers. observ.). same sequence of play behavior between 2 and Klopfer (1972) has recently reported that ob- 3 months of age as do feral monkeys, and in the servations of mother-infant pairs of lemurs in Canidae, similar action patterns have been ob- captivity were not different from behavior served in both infant laboratory and non- relations observed in the field. Wootton (1972) laboratory animals (e.g., Ludwig, 1965; Bur- observed that the descriptions and interpreta- rows, 1968; Silver and Silver, 1969; Mech, tions of stickleback behavior observed in
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captivity (e.g., Tinbergen, 1951) are relevant for (e.g., Korner, 1971). When comparing dif- to behavior observed in the wild. This last ferent species, age-equivalence must be con- finding is particularly important, since the sidered (Himwich, 1971). Bekoff and Fo.x- behavior of the stickleback is used as an ex- (1972) have discussed variables that affect de- ample in many ethological models of motiva- velopment of the central nervous system, par- tion and behavior. ticularly in rodents, and it is not unlikely that Furthermore, and perhaps more significant, many of them, if not all of them, affect the is the possibility that behavioral development ontogeny of both brain and behavior in other recorded during observations on captive animals mammals. These include handling (see Morton, can be correlated with the social organization 1968, for a review of this literature), cage size and socio-ecological adaptations of the wild (Bell, Miller, and Ordy, 1971), birth mode counterpart (Sheppard and Yoshida, 1971; (caesarian versus vaginal delivery - Meier, 1964; Bekoff, 1972; Fox, in prep.). For example, it Meier and Garcia-Rodriguez, 1966; Grota, has been observed that captive red foxes Denenberg, and Zarrow, 1966), conditions at (Fox, 1969), coyotes (Silver and Silver, 1969; birth (e.g., hypoxia, asphyxia- see Meier, 1971, Bekoff, 1972), and male Richardson's ground for a review of this literature), and litter size squirrels (Sheppard and Yoshida, 1971) display (LaBarba and White, 1971). Poole (1966), agonistic behavior in an aggressive context studying the agressive play of polecats, stated very early in life, and that these animals are that the size and agility of the animal depended known to disperse in natural populations on the number in the litter from which it (Burrows, 1968; Yeaton, 1972; Fox, in prep.). came. Members of litters of two or three were In contrast, wolves and beagles, for example, often larger and more agile than those of seven show more playful behavior than do coyotes or eight. or red foxes during the first 5 weeks of life, Structural and functional changes in the and this could be correlated with their pack- central nervous system must also be considered type existence in natural populations, in which when studying the development of social inter- stable hierarchies and the maintenance of action. Complex and dramatic changes may be learned social affinities are essential for group- taking place in the organization of the young coordinated behavior (Etkin, 1964; Haber, animal's behavior, during a period when, to 1968; Bekoff, 1972). simple observation, the behavior does not seem Therefore, differences in social behavior in to be changing very drastically (Lehrman and captivity could reflect differences in social Rosenblatt, 1971). It has been demonstrated structure in the wild. Whether the effects are (Fox, 1971a; Bekoff, 1972) that changes in the circular, the differences in social structure being quality of interaction between canids at ap- in part a consequence of the social environ- proximately four weeks of age can be correlated ment in which the young develop, is a matter with maturational changes in the nervous sys- worthy of further study (Hinde, 1971 a). Mc- tem. Increased control over thermo-regulation Bride (1971) proposed that animal societies and increased locomotor ability seem to be can be thought of as structures in space, with responsible for the emergence of running and individuals as the building blocks, and the chase activity (see Bekoff, 1972). behavior of the animals providing its architec- ture. Suffice it to say, the observations noted SOCIAL RELATIONS OF THE INFANT above, all with supporting quantitative data, demonstrate the usefulness and relevance of Mother-infant (e.g., Foss, 1961, 1963, 1965, ontogenetic studies carried out on captive 1969; Sch6nberner, 1965; Bowlby, 1969; Esp- subjects. mark, 1969, 1971; Fogden, 1971; Gould, 1971; Moltz, 1971b; Rosenblum, 1971; Klopfer, 1972), VARIABLES IN DEVELOPMENTAL STUDIES other adult-infant (e.g., Spencer-Booth, 1970), There are many variables that must be juvenile-infant, and infant-infant (e.g., Bekoff, taken into consideration and must be con- 1972) relations must similarly be considered trolled during the course of any developmental when observing behavioral development. There study. Individual differences must be accounted is increasing evidence that father-infant and
This content downloaded from 130.85.193.23 on Thu, 25 Aug 2016 12:48:45 UTC All use subject to http://about.jstor.org/terms 416 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 47 other adult male-infant interactions are very im- frequency of occurrence of an earlier behavior portant in behavioral development of the young such as sucking, and differences in the develop- (e.g., Mitchell, 1969; Ransom and Ransom, ment of sucking behavior may in turn be related 1971; Klopfer, 1972), as is the role of "aunts" to variations in infant-infant or mother-infant (e.g., Hinde, 1965; Jolly, 1972). However, more interactions, or both. data are sorely needed concerning this aspect Van Lawick-Goodall (1971) presented data of adult-infant interactions. The sex of the which suggested that mothers who were the infant must also be considered (e.g., Jensen, most restrictive in curtailing their infants early Bobbitt, and Gordon, 1968). in life were at the same time the most solicitous Bekoff and Lockwood (pers. observ.) observed in other respects and also the most playful. It that a first-born beagle was handled much more is also known that there are differences in the and in a rougher manner than his littermates, responses of mothers and other adults to male and although in this litter all animals died in and female young (van Lawick-Goodall, 1968; early infancy, it would seem that the effects of Harlow, 1971; Harper, 1971), and that these birth order must be considered; whether the variations might account for there being ap- mother is primiparous or multiparous (inex- parent sex differences in the early social de- perienced or experienced) must also be a factor. velopment and interactions among primates Jay (1962, 1963) observed that multiparous (e.g., Latta, Hopf, and Ploog, 1967; Harlow, langur mothers treated their infants differently 1969). Sex differences were not observed in the than did primiparous mothers. The latter infant canids observed by me (Bekoff, 1972), handled their infants less competently and perhaps because the animals were hand-reared. startled them more frequently by sudden move- To date, observations in the field have not ments than did the former. Behavioral differ- clarified the above situation in the Canidae. ences between 30-month-old offspring of experi- In conclusion, it would be important to in- enced and inexperienced Rhesus mothers have vestigate further whether there are differences been reported by Mitchell, Raymond, Ruppen- in behavior toward male and female infants thal, and Harlow (1966); and Thoman, Barnett, in a wide variety of animal species, and like- and Leiderman (1971) found differences in the wise to study the extent to which individual feeding behavior of newborn humans to be a differences in temperament among "normal" function of parity of the mother. mothers (e.g., permissiveness) affect the develop- Time of birth might also be an important ment of their infants. As yet, there are no such variable to take into account (Baldwin, 1969). studies of the latter problem (Hinde, 1971a), In squirrel monkeys, infants born early in the which will be discussed below when the concept birth season at first have few playmates other of behavioral neoteny is considered. Both field than stronger and behaviorally more sophisti- and laboratory studies suggest that further work cated juveniles, while infants born late in the is necessary in order to tease out and under- birth season are the weakest and the most help- stand the complexities of the interactional ex- less of their age class, since there are more periences of a developing organism and to ac- infants with whom to interact (Hinde, 1971a). count for individual differences, since the gap Group composition (age, sex) and size are very in our knowledge of the normal behavior of important variables that must be accounted for mammals toward young is enormous, and the- (e.g., Wolfheim, Jensen, and Bobbitt, 1970; ories of development of this relationship must Crook, 1970; Kummer, 1971). take adequate account of the variety of rearing It is clear that subtle variations in the social conditions (Spencer-Booth, 1970). Furthermore, interactions of infants can markedly affect their there are limitations on cross-species generali- behavioral development, and furthermore, there zations (e.g., Seay, Schlottman, and Thorne, are reciprocal relations, in that a mother's 1970; Eisenberg, 1972). (adult's) behavior will vary with the responsive- ness of the infant and vice versa (Hinde, 1971b; A DEFINITION OF SOCIAL PLAY BEHAVIOR Lehrman and Rosenblatt, 1971). Koepke and Pribham (1971) reported that the rate of devel- The development of play behavior has been opment of play in cats may be related to the studied in many species (for reviews, see Beach,
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1945; Piaget, 1951; Welker, 1961, 1971; Gil- is performed during social interactions in which more, 1966; Loizos, 1966, 1967; Ewer, 1968; there is a decrease in social distance between Millar, 1968; Berlyne, 1969; Bekoff, 1972). Play the interactants, and no evidence of social in- with peers is one of the first non-mother- vestigation or of agonistic (offensive or de- directed activities to appear early in life (Poirer, fensive) or passive-submissive behaviors on the 1970) and is a voluntary activity (e.g., Huizinga, part of the members of a dyad (triad, etc.), al- 1939; Herron and Sutton-Smith, 1971). though these actions may occur as derived acts Satisfactory definitions of play are scarce. during play (Bekoff, 1972). In addition, there It is a phenomenon that is easier to describe is a lability of the temporal sequence of action then to explain (Darling, 1937). Lorenz (1956) patterns, actions from various motivational has exclaimed: "Don't ask me to give a defini- contexts (e.g., sexual and agonistic) being tion of play!" On the other hand, many theories combined (e.g., Ludwig, 1965; Loizos, 1966; about play have appeared in the literature Ewer, 1968) (Fig. 1). Infant contactual behaviors and these have been reviewed by Gilmore that have a passing biological basis (e.g., thermo- (1966), Millar (1968), and Berlyne (1969). Sub- regulation-discussed above) have been ex- jective definitions and those that are con- cluded (Bekoff, 1972), as have group feeding taminated by anthropomorphic and adulto- and sleeping. Play fighting can be detected by morphic overtones - e.g., play being described the intensity of the interaction, observation of as not real, not work, or not serious (Waelder, the various actions which are performed simul- 1933; Chateau, 1954; Heckhausen, 1964; Ste- taneously, and knowledge of the social develop- phenson, 1967) - do nothing more than mud- ment of the animals or species being observed. dle the issue. It is no wonder that Schlosberg Establishment of an ethogram and categoriza- (1947) and Berlyne (1969), twenty-two years tion of the various motor action patterns is an later, concluded that psychology would do well essential prerequisite (see Table 1) for under- to give up the category of play. Fortunately, standing behavioral ontogeny. neither psychologists, zoologists, nor philoso- As mentioned above, the literature is replete phers have abandoned the ship. If mathema- with studies making the above basic assump- ticians can calculate with imaginary numbers, tion of what play is (or is not); moreover, investigators of behavioral ontogeny should viewing the concept of play as I have defined it be able to deal with the concept of play. In- makes it a manageable concept and avoids deed, recent efforts using the observational, de- semantic difficulties. It is possible that there scriptive method have helped to unravel many may have to be modifications to fit various of the complexities of the concept of play (e.g., species; however, at least in the family Canidae, Hutt and Hutt, 1970; Bekoff, 1972; Blurton play behavior can now be studied and manipu- Jones, 1972b; McGrew, 1972). lation experiments conducted, since the nor- The basic problem seems to be in the termi- mal range of the frequency, amplitude, and nology used to describe the phenomenon of components of temporal sequences of motor play. This includes transference of concepts action patterns is known (Bekoff, 1972). derived from human experience (Tinbergen, This author (and apparently those who are 1963) and adult interpretations that fail to take still actively engaged in studying play) does into account the "umwelt" of the child. Play not agree with Welker (1971) that thorough indicates a form of behavior that is very serious studies of the developmental behavioral reper- and real for the infant and child (e.g., play toire of various organisms have not justified therapy -Axline, 1969), and should be studied the identification of play as a valid behavior in this light. class or a scientifically useful concept. Most Based on a comprehensive review of the studies to date have not actually entailed a literature and on many hours of observation highly detailed systematic design, such as of infant Canidae, I have offered an operational establishing an ethogram, carefully following definition of play behavior as follows - one the development of social interaction from day that is generally implied and infrequently stated to day during the early stages of socialization, in field notes and transcriptions of behavior or determining the normal range of behavior observations. Social play is that behavior which of the species under study (contra Tembrock,
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FIG. 1. AN EXAMPLE, OF ACTION PATrERNs FROM VARIOUS MOTIVATIONAL CONTEXTS 'BEING COMBINED DURING, A PLAY BoUT The animal on the left is displaying an aggressive face (e.g. snarling with vertical retraction of the lips) and simultaneously performing a face-oriented pDawing movement, in this case, a play-soliciting gesture. Subsequent interaction between this pair of anials was playful, and this provides a nice example of the fact that priority is almost invariably given to the play signal (e.g., Loizos, 1966).
1957; Bekoff, 1972; Blurton Jones, 1972b; Mc- amount of time and paper spent on specula- Grew, 1972). tions about motor play in immature animals While this article was in press, I discovered the is in inverse proportion to the amount of facts following article concerning play behavior in available on the question. In addition, Poirer primates: Doehinow, P. J., and N. Bishop. 1970. (1970) has added that detailed studies of the The development of motor skills and social rela- role of play in the socialization process are tionship among primates through play. Minn. lacking. Symp. Child Psychol., 4:141-198. It concludes that Harlow and Harlow (1961) listed five stages "play is a major category of adaptive behavior that must be understood if we are to understand in the development of play behavior in Rhesus primate behavior." This strongly supports the monkeys and later wrote that interactive play is position taken in the present paper. an essential element in the development of af- fectional behavior toward age-mates (Harlow
PLAY AND SOCIAL DEVELOPMENT and Harlow, 1966). Harlow and Suomi (1971), studying social recovery by monkeys reared in Although there has been a lack of definition isolation, stated that the most critical and valid of the phenomenon of play behavior, there measures of social recovery were those of social certainly has been no dearth of studies relating play to social development (see Sleet, 1971, contact and play. The increasingly complex for an exhaustive bibliography). There has processes of play provide the means and motives been a unanimous conclusion that the develop- for the development of the peer system (Har- ment of social behavior is intimately related to low, 1971). This appears to be true for a wide the ontogeny of social play. Most authors have range of animals (Bekoff, 1972; Blurton Jones, accepted the existence of play in a phenom- 1972b). enological sense (e.g., Mason, 1965), and The rationale behind play therapy (Axline, Muller-Schwarze (1971) has stressed that the 1969) and the infantile dynamics theories of
This content downloaded from 130.85.193.23 on Thu, 25 Aug 2016 12:48:45 UTC All use subject to http://about.jstor.org/terms DECEMBER 1972] DEVELOPMENT OF SOCIAL INTERACTION 419 play (which take into account the "umwelt" nicative skills are acquired during early social of the developing organism-e.g., Gulick, interaction, and the marked impairment in so- 1920; Lewin, 1933; Buytendijk, 1933; Piaget, cial ability exhibited by socially deprived mon- 1951) emphasize the point that play and social keys may be due, in part, to a lack of oppor- 'development are intimately tied. Play with tunity to develop communicative skills which peers is so important that Harlow (1969) and facilitate social interaction. This also appears to Tisza, Hurwitz, and Angoff (1970), studying in- be true in a variety of organisms such as fallow fant Rhesus monkeys and hospitalized children deer (Gilbert, 1968) and canids (Fox, 1971a), respectively, were able to demonstrate that in- and can also account for the findings of Kagan teraction with peers can override the effects of and Beach (1953) noted above. The ability of an separation from the mother and make it a less animal to "understand" intraspecific communi- traumatic experience. Causey (1956, cited by cative signals depends upon social experience Scott and Bronson, 1964) observed that in infant and social conditioning - e.g., the development dogs a littermat* was more effective than the of expectancies and learning of the context mother in reducing vocalizations in a strange (behavioral set + mood) in which various ac- environment. Harlow (1969) referred to the tions are performed - and this capacity is ac- above phenomena as a biological safety valve. quired through the totality of social experience Finally, Kagan and Beach (1953) reared infant of the infant. This will be discussed in depth male rats with mature females, and these males when the concept of metacommunication (after failed to develop normal sexual responses. They Bateson, 1955) is presented and re-evaluated. concluded that a pattern of play activity asso- Play is almost always observed when the more ciated with females had conditioned the young immediate physiological drives of. the infant so as to bar recognition of the females as sex (or adult) have been satisfied. In accord with objects. the hypothesis that play is not a primary Suffice it to say, data collected on a variety of activity (Meyer-Holzapfel, 1956a,b), Hafez, animals, both in the field and in the laboratory, Schein, and Ewbank (1969) have observed that have conclusively demonstrated that normal be- well-fed calves play more often than sick or havioral development depends on there being poorly fed ones, and Farentinos (1971) added adequate infant-infant interaction. Systematic further support with his observations that observations on a wider phyletic range of spe- play occurred after more immediate drives cies is sorely needed. Fortunately, such studies (e.g., hunger and sex) had been satisfied, and are beginning to appear in the literature (e.g., that territorial male Steller sea lions (in active Farentinos, 1971; Steiner, 1971). It must be territorial defense) were never observed in stressed once again that mother (adult)-infant any behavior that could be labeled as play. interactions are not totally indispensable, and Espmark (1969) also observed that play in roe when the mother (or another adult) is present, deer did not occur unless the motivation to she plays a role in the behavorial ontogeny perform some innate behavior to satisfy an of her offspring. Progeny from different rank- immediate physiological need had ceased. It ing animals may show differential development has been proposed quite frequently that the of social behavior (Kawai, 1958; van Lawick- reason why play is observed more in infants Goodall, 1968; Harper, 1970). Therefore, as al- than in adults is because infants are not re- ready stated, developmental studies must ac- sponsible for satisfying the various physiological count for the extent to which adults interact requirements of development (Millar, 1968). with particular infants (Hinde, 1971a; Spencer- If play activities are inhibited or prevented Booth, 1970). from developing because of the occurrence of certain environmental or physiological condi-
THE FUNCTIONS AND CONSEQUENCES OF PLAY tions, the behavioral repertoire may become severely distorted (Welker, 1971). Since so many animals appear to spend a lot Groos (1898) emphasized that young animals of time and energy at play while young, it is play in order to pre-exercise instincts in prep- necessary to consider the possible functions of aration for later life. He failed to recognize, play. Mason (1960) wrote that normal commu- however, the orderly progression of various de-
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velopmental stages of play and the effect of continued maintenance of social organization each stage on each subseqent stage (Harlow, and social affinities within a group (Etkin, 1964; 1971). Poole (1966), however, observed that in Haber, 1968; Bekoff, 1972). Estes and Goddard polecats the patterns involved in aggressive be- (1967) observed playful "pep-rallies" preceding havior are stereotyped and unmodified by ex- a hunt in African wild dogs. Learning and ex- perience; and Fox (1969) demonstrated that pression of certain social gestures and postures infant coyotes, when given their first prey-kill- during play in young animals may serve subse- ing session with live rats, will go through a quently to inhibit aggression and thus make ritualized prey-killing sequence without having possible the formation of stable group hier- ever played (with conspecifics or dead rats). archies (Jay, 1965). Harlow (1971) similarly These observations do not support Groos' concluded that during free social play, social theory. Welker (1971), in his detailed review roles develop and the rules of social intercourse of the literature, also concluded that the prac- are shaped and the control of immediate de- tice function of play has not been verified. mands and aggression is established; and Scott Leyhausen (1965) suggested that, through (1968) suggested that play may contribute to the play, cats enrich the scope of their experience development of group-coordinated and allelomi- and the range of their skills in many and di- metic behavior. Recently, Wickler (1970) has verse ways. They create play situations, and in written that comparative examinations of var- so doing, they learn more than ever would be ious socially-living vertebrates have shown that possible if they were limited exclusively to in- certain regular behavior elements serve for stinctive movements along the "one-way street" stabilization of their societies and that these of an unalterable sequence rigidly confined elements are not new, but are derived from to biologically relevant situations (Leyhausen, their behavior repertory (e.g., definition of play 1965). Barnett (1970) wrote that the function given above). of play in development is learning to learn Extensive data collected in this laboratory (deutero-learning), and Eisenberg (1966) noted provide evidence that the more social Canidae that play appeared to aid in the functional inte- (e.g., beagles and wolves) engage in more, play- gration of innate patterns. The concept of the ful interactions earlier in life than the more modification of motor action patterns through solitary species such as the red fox and coyote social experience and social conditioning re- (Fox and Clark, 1971; Bekoff, 1972). The former, quires further elaboration, and will be discussed unlike the latter animals, in which dominance in detail below. hierarchies are formed before the emergence of Brownlee (1954) studied play in domestic cat- play (most frequently by a severe dominance tle, and offered a physiological explanation for fight between 25-30 days of age -Fox and the function of play. He suggested that play in Clark, 1971; Bekoff, 1972), form their social cattle (and in other organisms) is a single in- hierarchies through playful interactions. As stinct, with its own drive, releasers, emotions, pointed out in the beginning of this review, consummatory phase, and goal. Cattle derive red foxes and coyotes are solitary and semi- physiological benefits from playing - e.g., in- solitary species respectively (Burrows, 1968; creased blood supply to the muscles involved Rue, 1969; Fox, 1972), and it is possible that and increased muscle tone. There is much evi- this early ontogeny of aggressive behavior (ob- dence that the use of various organs (e.g., the served both in captivity and in the wild) is eyes) is essential for structural maturation and responsible for later dispersal and a virtual the development of functional integrity (see absence of group coordinated behavior (e.g., Bekoff and Fox, 1972), and Brownlee's physio- hunting) as adults (e.g., Burrows, 1968; Hinde, logical explanation for the function of play 1971a; Fox, 1972). appears to be valid. Whether or not there is a "play drive," as he also suggested, is disputable IS THERE A PLAY DRIVE?" (see below). In canids, social play seems to be important The animal literature concerning play be- in learning to control the intensity of the bite havior is replete with unsubstantiated allusions (Fig. 2), and in facilitating the formation and to the existence of a "play drive." Specifically,
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FIG. 2. AN INHI1BITED BITE DURING PLAYFUL SOCIAL INTERACrION OF Two FoUR-MONTH-OLD COYOTES The dominance hierarchy has already been established. Note that the ears are pressed back. (From Bekoff, 1972.)
it is implied that an animal deprived of play cluded that there is little evidence that could activities will show an increase over the normal justify the postulation of an autonomous ac- amount of play behavior when subsequently tivity drive. He wrote that the critical variable allowed to perform such motor action patterns. seems to be experiential deprivation, rather Lorenz's psychohydraulic model (1950) would than activity deprivation per se. This sugges- be applicable in this line of reasoning. Hinde tion fits in nicely with the experimental evi- (1960), Beer (1968), and Henderson (1972), dence offered by Melzack (1952), Thompson and have concluded, however, that energy models Heron (1954), Melzack and Scott (1957), and of motivation based upon the existence of Melzack and Burns (1965), namely, that experi- unsubstantiated physiological processes (such as entially deprived dogs of many different breeds the building up of energy in a psychic reservoir) are hyperactive and extremely emotional upon should not be used in formulating or support- release from isolation. Fuller (1967) has re- ing behavioral themes. At this time, it would viewed the isolation-emergence syndrome. be unwise to use an unsupported model of It is therefore not appropriate at the moment behavioral motivation and drive to explain to speak of the existence of a specific play drive. such a controversial phenomenon as play. Fur- The methods that would have to be used to thermore, investigators have not adequately determine its presence (or absence) would not separated the drive for general motor activity only deprive a developing organism of play from the drive to play, if, in fact, either does experience, but of all types of social interaction, exist. and the isolation syndrome is very complex Lore (1968) has reviewed the literature con- (Fox, 1971a). The two formal attempts to inves- cerning the activity-drive hypothesis. He con- tigate the possibility of the existence of a play
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drive have produced divergent results. Muller- missive (coyote-beagle hybrids and wolf-male- Schwarze (1968), studying deer, found no evi- mute hybrids). In those instances when play- dence for the postulation of a play drive in soliciting by one animal did not result in any playful interaction (decrease in social distance), them, while Chepko (1971), observing infant self-directed play appeared to be a redirected goats, found that deprivation of play led to an form of social play, indicating the possible exis- increase above the norm in subsequent play tence of a "play drive." The soliciting animal behavior. Muller-Schwarze (1968), however, did had "metacommunicated" its intention and mood, not control for the effects of learning (Chepko, and when its expectation was not met, self- 1971); and Chepko (1971) did not control for directed play resulted. That this self-directed the effects of punishment. Bekoff and King play was not just the result of a general drive (unpubl.) observed that in infant beagles and for motor activity (e.g., Meyer-Holzapfel, 1956a,b) coyotes, after 24 hours of social isolation from is indicated by the fact that it was preceded by a their littermates, there was greater than usual play-soliciting gesture, indicating "desire" for a specific type of motor activity-social play. general activity during a subsequent period of social interaction with a peer. Since two ani- mals were being observed at the same time, SOCIAL EXPERIENCE AND THE DEVELOPMENT OF this increase in activity led to an increased COMMUNICATIVE AND METACOMMUNICATIVE interaction and to more play, as well as more SKILLS aggressive behavior. The frequencies of all types During early social interaction, communica- of behavior were elevated. tive skills are developed (e.g., Mason, 1960; In conclusion, the causes for restlessness after Miller, Caul, and Mirsky, 1967; Jolly, 1972). social deprivation are many. It appears to be One very important ability that must be ac- virtually impossible to verify experimentally quired early in life is that of being able to the existence of a play drive, because methodo- differentiate playful from non-playful interac- logical insufficiencies do not allow an experi- tions. Bateson (1955) observed primates play- mental manipulation that deprives an organism ing and concluded that "play could only occur solely of play experience (Glickman and Sroges, if the participant organisms were capable of 1966). Along these lines, the hypotheses of some degree of metacommunication, that is, of Harlow (e.g., Harlow and Harlow, 1966) and exchanging signals which could carry the mes- others, who state that socially deprived animals sage that 'this is play'." This message is con- are deficient in performing adult behaviors be- veyed by vocalizations, facial expression, and cause they were deprived of play experience as bodily gestures (e.g., style of approach) in pri- youngsters, need revision [see Meier (1965) and mates (Van Hooff, 1962, 1967; Altmann, 1962, Ewer (1968, p. 323) for further discussion of 1965, 1967; Schaller, 1963; Hall, 1967; Ploog, this point]. The effects that are produced by 1967, 1969) as it is in the Canidae (Darwin, using isolation techniques must be interpreted 1872; Rheingold, 1963; Ludwig, 1965; Fox, in terms of the methodological deficiencies. 1970a; Bekoff, 1972). Struhsaker (1967) has re- A very recent analysis of data collected by this corded a play call in vervet monkeys which may author has suggested the existence of a "play enhance the play bond between individuals and drive" in the infant canids observed. The meth- thus facilitate the occurrence of future play odology did not involve deprivation procedures (social isolation or experimenter intervention), encounters. Van Hooff (1972) discussed human but rather analyses of temporal sequences of be- laughter and smiling as being metacommunica- havior and qualitative and quantitative differ- tive signals. ences in behavior and activity, between the mem- Metacommunication involves communication bers of the dyads observed. about communication, and in metacommunica- Briefly, it has been demonstrated that self-di- tion there is contextual dependency (Cullen, rected play (e.g., tail-chasing) may serve as a 1972). Primates include in their behavioral substitute for social play, when the possibility repertoire a set of social messages that serve to for social play is blocked - e.g., when one animal affect the way in which other social messages are is intolerant of the proximity of its partner (coy- otes), or when one animal is either totally with- interpreted (Altmann, 1962). Kummer (1971) drawn (inactive) (beagles and wolves) or sub- wrote that primates use their vocalizations, ges-
This content downloaded from 130.85.193.23 on Thu, 25 Aug 2016 12:48:45 UTC All use subject to http://about.jstor.org/terms DECEMBER 1972] DEVELOPMENT OF SOCIAL INTERACTION 423 tures, and facial expressions to inform recipients or "unit" of a more complex sequence of be- of what could be called the present mood of havior; (2) generalization: the action pattern the actor, about what he is likely to do next. is observed in a variety of motivational con- Apart from expressing his own intentions, a texts; (3) individuation: the action pattern is monkey can also influence the intentions and observed in a more specific motivational con- moods of his fellows. In this way, animals are text; (4) integration: the action pattern becomes able to distinguish between playful and serious integrated with other action patterns and is [sic] encounters (Altmann, 1967). The same is consequently incorporated into a relatively pre- true for the Canidae (Bekoff, 1972), ground dictable sequence of behavior; and (5) sociali- squirrels (Steiner, 1971), and cats (Loizos, 1966). zation: the elicitation of the action pattern is Thus, preceding and accompanying play en- to some extent determined by the relationship counters, these animals will perform certain of one animal to another (e.g., in terms of domi- movements-e.g., primates: gamboling, and nance and subordination). The contribution of looking through their legs at their playmates experience and inhibition of responses "inap- (Altmann, 1962; Schaller, 1963; Van Hooff, propriate" to the situation are important in the 1967; Poirer, 1970); canids: play-bow or play- ontogeny of temporal sequences of motor action dance (Fox, 1970a; Bekoff, 1972). These move- patterns and their content. Therefore, as men- ments signal to the other members of the play tioned above, it is misleading to analyze a de- group that any aggressive behavior in the play veloping, inexperienced organism in terms of situation will not be real aggression. Even characteristics that are only applicable to ex- though jaw musculature and dentition are well perienced organisms (e.g., Welker, 1971; Bekoff, developed in adults, inhibited biting is ob- 1972). served. It is possible for metacommunication Fox (1971c) has recently stressed the point to break down, when, for example, the intensity that organisms are born with a set of species of interaction increases (e.g., loss of bite inhibi- characteristic behavior patterns, which can be tion -Fox, 1971b; Bekoff, pers. observ.). modified to varying degrees as a result of social The development of metacommunicative abil- experience and learning (see Fig. 3-2 in Fox, ities is intimately related to the dynamics of the 1968). Components of ongoing behavioral se- social ontogeny of a developing organism. Basic quences are synthesized through a series of communicative skills must be acquired for nor- transactional experiences (Kaufman, 1960); and mal behavioral development and eventual com- genetic, ontogenetic, experiential, and socio- petent performance during adult social inter- environmental variables are involved (Fox, actions. The concept of metacommunication 1971c). It has recently been demonstrated that must be thoroughly re-analyzed in this light species-characteristic action patterns do play a since, as Altmann (1967) has correctly stated, role in the various developmental sequences of the components underlying metacommunication social interaction observed in canids (Bekoff, are acquired during early life through social 1972). Mason (1971) similarly viewed the devel- interaction. Since the developmental studies opment of an individual organism as the out- that have been carried out on the Canidae over come of the interaction between genotypic tend- the past years have involved careful control of encies (e.g., the performance of certain motor social interaction, and life histories can be action patterns) and specific circumstances. accounted for (see Fox, 1971a; Bekoff, 1972), Therefore, it is essential to view the contribu- an attempt will be made to discuss and under- tions of heredity and environment as being stand metacommunication in proper perspec- fused at all stages of ontogenesis (Schneirla, tive as a developmental phenomenon. 1966; Fox, 1970b). Maturation and growth of the central nervous system, as well as normal THE DEVELOPMENT OF BEHAVIOR SEQUENCES behavioral ontogeny, require both proper ge- Fox and Clark (1971) presented an epigenetic netic endowment and appropriate environ- paradigm for the postnatal ontogeny of behav- mental stimulation, and are neither entirely ior patterns as follows: (1) maturation: the 'environment-expectant" nor "environment- gradual emergence of a given action pattern dependent" (Bekoff and Fox, 1972). Changes
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in either heredity or environment can affect pears to be a correspondingly longer period of the way in which a developing organism per- infancy, and more time for social interaction ceives and reacts to its environment (Fox, and play (Hebb, 1949; Tobach and Schneirla, J970b). [The reader is referred to Hebb (1953); 1968). The adaptive or survival value of pro- Lehrman (1953, 1970); and Lorenz (1965), for longed infancy is related to a "greater need discussions in depth of this controversial devel- for learning" rather than a "greater period in opmental issue.] which to learn" (Mason, 1968). This need is related to the relative paucity of fixed reflex-
BEHAVIORAL NEOTENY like patterns of behavior and a larger set of behavioral potentialities than was possessed by Incorporated in this whole notion of the phyletic predecessors (Mason, 1968). Animals development of behavioral sequences, which with an inherited repertory of perceptions and stresses the importance of social interaction for motor coordinations do not need this opportu- the developing organism, is the concept of be- nity, being already provided with such neural havioral neoteny. [See Montagu (1972) for a organization (Nissen, 1951). discussion of fetalization, neoteny, and pedo- It is clear that the "need" for social inter- morphosis from an anatomical-morphological action and the availability of a prolonged pe- point of view.] The concept of neoteny, which riod in which to interact are related. The para- takes into consideration the prolonged period dox that Herron and Sutton-Smith (1971) dis- of dependency on the mother (or other adults) cuss- namely, that play is usually thought to and the corresponding delayed personal respon- be non-productive, while at the same time it sibility of the infant for satisfaction of primary has been declared to increase in extent as one needs, can be used in the explanation of the ascends the phylogenetic scale- is really no phylogeny and ontogeny of behavior (Mason, paradox at all, since (1) play is a very produc- 1968). Fiske (1875; cited by Mirsky, 1968) re- tive activity, in so far as it allows the develop- garded the prolonged period of infancy as a ing organism to realize behavioral potentialities "period of plasticity . . . a door through which essential for normal behavioral development the capacity for progress can enter . . . (to) and adult life; (2) play exposes the animal to modify . . . inherited tendencies." Levy (1943) conspecifics and inanimate objects in its envi- used the term "infantilization" to refer to ac- ronment (like exploratory behavior), and there- tivities and communications by which a child fore experience about the socio-environmental (or other person) is encouraged to remain (or milieu may be gained; and (3) the channeling become) more dependent on another. [Jonas of innate motor action patterns into adaptive and Klein (1970) have recently discussed the sequences of behavior is mandatory for orga- concept of infantilization in man in terms of nisms in which there is a relative paucity of a disease-model of evolution.] Therefore, pro- innately determined sequences (e.g., Fox, 1971c; longed infancy in "higher" vertebrates, and an Mason, 1971; Fig. 3). Play is an essential func- increased time in which to develop the neces- tion of childhood, and the "open-system" of sary communicative and metacommunicative the developing organism may provide the door skills necessary for normal social development, for cultural influences (e.g., Huizinga, 1939; may involve reciprocal interaction between Itard, 1962; Lowenfeld, 1967; Kummer, 1971). mother (or other adults) and young, in that the behavior of one can alter the behavior of THE COMPONENTS OF METACOMMUNICATION the other and affect what occurs during early life. Individual differences among infants involv- A discussion of the development of the be- ing the degree of persistence of infantile needs, havioral components underlying metacommuni- and individual differences among mothers (e.g., cation can now be undertaken in light of the in permissiveness or restrictiveness) must be above. Since communication implies that the accounted for (as discussed above), in that the behavior of one animal is changed upon its period of dependency may be correspondingly perception of a signal from another animal shortened or lengthened. (Marler, 1967), play-intention signals are cer- As we ascend the phylogenetic tree, there ap- tainly communicative, and also metacommu-
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THE DEVELOPMENT OF SOCIAL INTERACTION 1970). An isolation-reared monkey may come to prefer a like-reared monkey on the basis of INCREASING AMOUNTS OF SOCIAL EXPERIENCE (DURING THE PROLONGED behaviors which that monkey does not perform PERIOD OF INFANCY-8EHAVIORAL NEOTENY) + INCREASING INDEPENDENCY (Sackett, 1970), because isolated animals have not developed metacommunicative skills. A SOCIALIZATION non-isolated animal may become an aversive
/ t \ META-COMMUN I CAT I VE stimulus to such an isolated one because of INTEGRATION SKILLS ACQUIRED (4) dissimilarities in behavior, facial expression, INFLUENCE OF t "_ and body posture (Sackett, 1970). A similar ALL SOCIAL INDIVIDUATION COMPAN IONS(3) t mechanism might also account for the findings GENERALIZATION of Leach (1972), namely, that children who had E = EXPERIENCE H = HEREDITY difficulty in separating themselves from their MATURATION (2) 51= SENSORY INPUT i2= SOCIAL mothers had reduced, unsatisfactory interactions EXPER I ENCE with peers. S + S2 Gilbert (1968), while studying the behavior H E(1) I I of fallow deer, observed that the most striking ENV I RONMENT- ENV I RONMENT EXPECTANT DEPENDENT effect of hand-rearing (without social experi-
FIG. 3. THE RELATIONSHIP BETWEEN HEREDITY, ence) is the cleavage of the social bond between ENVIRONMENT, THE DEVELOPMENT OF TEMPORAL SE- the fawn and its own kind. The elements that QUENCES OF BEHAVIOR WITH SOCIAL EXPERIENCE, are essential for herd organization - the co- BEHAVIORAL NEOTENY, AND METACOMMUNICATION hesion of individuals and the awareness of slight See text for explanation. Notes: (1) see Fox, 1968; Bekoff and Fox, 1972. (2) Scheme for the changes in mood by exchange of signals - have postnatal ontogeny of temporal sequences of motor been disintegrated. Finally, MacNamara (1972) action patterns (Fox and Clark, 1971). (3) See text wrote that infants learn language by first and Fox, 1968; Bekoff and Fox, 1972. (4) Ability to communicate mood and identify behavior sets determining, independently of language, the during social interactions. meaning which a speaker intends to convey to them, and uses meaning as a cue to language. nicative, in that they invariably elicit a playful Although metacommunicative signals might be response on the part of the recipient, detectable species-specific, it seems highly likely that addi- in terms of a change in body position, orienta- tional comparative ontogenetic studies will dem- tion, and spatial relationship (decreased social onstrate their existence within a wide phyletic distance). Causation may be implied by the range. Ramsay's statement (1969) that meta- behavior that is elicited (Blurton Jones, 1968). communicative messages are rare in animals is As the organism develops in terms of central premature. nervous system maturation, skeletal-muscular Clarity of the message is an essential pre- growth, and increased amounts of social experi- requisite, and in line with Tinbergen's (1951) ence, innate motor action patterns are chan- notion that a "social releaser" must be simple, neled into situation-specific behaviors (Fox, conspicuous, and specific and Morris's (1957) 1971c). The responsiveness to conspecific sig- concept of "typical intensity," play-intention nals may improve with experience, in that the signals must be unambiguous and not confused animal may learn through socialization (social with other behavioral signals, since they specify conditioning) to identify certain behavior sets what type of behavior is to follow. Morris (1957) and also to express and recognize mood and stressed that where a response is acting as an readiness to play. Signal context + expectancy agent of social communication, it is advanta- + mood (or readiness), which are expressed, geous for it to possess a certain constancy of perceived, and shared, are the underlying com- form in order to eliminate signal ambiguity. ponents of metacommunication (Bekoff, 1972). This is particularly important in the case of There is an intimate reciprocal relationship play signals, since it is essential that the mood between sender and receiver, and this may ac- of the ongoing interaction be maintained in a count for the fact that animals reared in similar manner appropriate to the initial stimulus (e.g., social environments display preferences for one a play invitation). another (e.g., Pratt and Sackett, 1967; Sackett, In canids, a particular motor action pattern,
This content downloaded from 130.85.193.23 on Thu, 25 Aug 2016 12:48:45 UTC All use subject to http://about.jstor.org/terms 426 THE QUARTERLY REVIEW OF BIOLOGY [VOLUME 47 the "play-bow" (Fig. 4; Fox, 1970a; Bekoff, been recorded (Van Hooff, 1967). Poirer (1970) 1972)-a crouching of the fore-part of the has accordingly observed that, in langurs, be- body with elevation of the hind-end - has been havior commonly associated with play initiation observed to be a situation-specific, social releaser seemed to attract the attention of prospective for play. Darwin (1872) first observed this and playmates. wrote that it occurred when the dog is in a
"humble and affectionate state of mind." In RITUALIZATION AND METACOMMUNICATION the dog and the wolf this action is also seen during the greeting of a familiar person (Schass- Cullen (1966) wrote that the process of rituali- burger, 1968; Fox and Bekoff, personal observa- zation results in increasing the conspicuousness tions). In coyotes, the play-bow develops into of signals with a concomitant decrease in am- a "play-dance" (Fox, 1970a). The message that biguity. Ploog (1970) has viewed ritualization is conveyed by this "appetitive" action results as involving the adaptive canalization of ex- in a decrease in social distance and playful, non- pressive behavior. As play in canids develops, aggressive interaction. Play-soliciting sequences it becomes species-typical and more ritualized often incorporate exaggerated approaches, ap- (an ontogenetic ritualization). Indeed, the char- proach/withdrawals (to initiate chase), face- acteristics listed by Morris (1966), referring to pawing, and infrequently face-licking, with the changes that occur during the evolution of soliciting animal wearing a "play-face," as de- ritualized behavior, closely parallel the char- scribed by Fox (1970a) in canids and by van acteristics of play behavior as listed by Loizos Hooff (1962, 1967) in primates. (1966, 1967) and by Ewer (1968) in their respec- Steiner (1971) observed play-soliciting signals tive reviews (e.g., reordering of sequences, repe- in ground squirrels, and interpreted them as tition, exaggeration, and fragmentation of being intention movements (movements indi- movements). Unfortunately, the process of cating "intent"), attention-getting devices, or ritualization has not been specifically studied both. Signals which draw the attention of the in the case of animal play (Thorpe, 1966). receiver (e.g., "Look here!") are described as During a play-bout, there is continuous feed- deictic (Lyons, 1972). Very often in dogs, a back from one participant to another, and the play-bow is accompanied by a loud bark (Fig. 4), ability to control aggressive behavior and react and in primates an audible "play-pant" has appropriately to the mood of the ongoing inter-
* e 4
4 -~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~
FIG. 4 A "PLAYBOW" ACCOMPANIED BY A BARK This social releaser for play is an intention movement and a bark, an attention-getting device (from Bekoff, 1972).
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action would benefit from increased ritualiza- patterns categorized in terms of the motiva- tion and greater amounts of social experience. tional context in which they appear. Subtle The function of a signal and the information intervening variables must be accounted for content are largely determined by the response and teased out in order to achieve a clearer of the recipient (Maurus and Ploog, 1971). It picture of the dynamics of behavioral ontogeny. is therefore necessary for the participants to be The developmental, comparative approach pro- aware of strategies and behavior sets, and like- vides a powerful tool for behavioral research; wise for the investigator to study them (Kum- and studies conducted on some captive animals mer, 1971). McBride (1971) wrote that during appear to be quite relevant, and their results a social encounter each animal "assembles" the intimately related to behavior and social organi- next block of responses to be emitted by using zation observed in their wild counterparts. information from the whole context of the The concept of behavioral neoteny is related interaction, but more specifically in the form to the whole of social ontogeny, in that animals of feedback from the behavior of the inter- that are born with a paucity of genetically fixed actant. behavioral sequences require a period in which The communicative "output" of one animal inborn motor action patterns become integrated is not necessarily identical to the "input" that and canalized into situation-specific contexts. the recipient registers (e.g., Vine, 1970), and Future studies should concentrate on investi- the inefficiency of transmission can be reduced gating the process by which adaptive chains of by either animal (Vine, 1970). It can be further temporal sequences of motor action patterns reduced by the ritualization of the particular are assembled, as well as determining the "adap- components of the message - e.g., facial expres- tive capacities" and potentials of the developing sions, gestures, body postures, and vocalizations. organism. In canids and in primates, the ritualization of Social interaction, consisting of both agonistic situation-specific signals has been instrumental and playful encounters, is essential for the in providing a foundation for the ability to normal behavioral development of an infant develop, and to use effectively, signals that mammal, and through this social experience carry a message which conveys a mood, and that communicative and metacommunicative skills indicate what is to follow in time (e.g., play). are acquired. Play is a valid class of behavior The appetitive action patterns involved in play and a useful developmental concept. The invitation have been reduced to their simplest process of ritualization has played an important components with a concomitant decrease in role in the development and elaboration of ambiguity. Accordingly, the requirement for specific metacommunicative signals - those con- playful interaction, both for developing orga- veying messages of mood and intent. nisms and for the maintenance of adult social organization, can be more effectively realized. ACKNOWLEDGEMENTS
I would like to thank Michael W. Fox for crit- SUMMARY AND CONCLUSION ically reading this manuscript and for the many helpful suggestions that he has offered over the More systematic studies of the development past years. The author's work was supported in of social interaction and of communicative skills part by PHS Training Grant GM-1900 and PHS are sorely needed. Developmental ethograms Grant ES-00139, through the Center for the Biology and sociograms must be established and action of Natural Systems, Washington University.
LIST OF LITERATURE
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