AMER. ZOOL.,
14:317-322
(1974).
Aggressive Play and Communication in Rhesus Monkeys (Macaca mulatto)
DONALD SYMONS
Department of Anthropology,
University of California,
Santa Barbara, California 93106
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 08623. 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.
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
PLAY AND COMMUNICATION IN RHESUS MONKEYS
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 gen-
319
erally 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-
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 1969-70 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-
PLAY AND COMMUNICATION IN RHESUS MONKEYS
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, ago-
321
nistic 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.
322
DONALD SYMONS
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