Department of Animal
Behaviour, University of Cambridge,
U.K.
Abstract. Displacement activities are
behaviour patterns (mostly body care activities)
characterized by their apparent irrelevance to
the situation in which they appear. Scratching,
autogrooming, yawning and body shaking
are among the most commonly reported
displacement activities in non-human primates. A
review of the primate literature indicates that
displacement activities tend to occur in
situations of psycho-social stress and that
their frequency of occurrence is affected by
anxiogenic and anxiolytic drugs. In the light of
this evidence, it is suggested that displacement
activities can be used as indicators of
emotional states arising in a variety of primate
social interactions. Methodological problems
associated with such a use are discussed. The
hypothesis that displacement activities may also
have a communicative function in non-human
primates is not supported adequately by
available data.
According to the usual definitions,
displacement activities are behaviour patterns
exhibited by an animal that are 'apparently
irrelevant' to its ongoing activity (see
Tinbergen 1952; Zeigler 1964). For example, in
several sexual or agonistic contexts, passerine
birds can clean their bills or feathers, eat or
drink, or commit themselves to other activities
that apparently do not have any obvious
contextual relationship (Hinde 1953; Morris
1954; Rowell 1961). Similar examples have been
reported in other animal groups such as
arthropods, fish and mammals (e.g. Tinbergen
& van Iersel 1947; Sevenster 1961; Duncan
& Wood-Gush 1972; Hansen & Drake af
Hagetsrum 1984; Roper 1984). Displacement
activities are thought to occur in conflict
situations (i.e. when two incompatible
motivational tendencies are elicited simul-
taneously) or in situations in which an animal
is prevented from attaining its goal
(frustration; Tinbergen 1952; McFarland 1966).
Different hypotheses concerning the emergence of
displacement activities in these situations have
been advanced. Some authors have taken the view
that tension builds up during conflict, and that
this is in some way released by the performance
of displacement activity (e.g. Tinbergen 1952).
Others have suggested that the conflicting
tendencies inhibit each other, allowing a third
and irrelevant tendency to gain expression, so
giving rise to displacement activity (e.g. van
Iersel & Bol 1958). Another possibility is
that conflict and thwarting situations are
characterized by increased levels of arousal and
that in this condition activities emerge 'which
are prepotent in the animal's repertoire'
(Bindra 1959).
In recent years displacement activities have
been rather neglected as a topic of study. This
may have resulted in part from a difficulty in
recognizing these behaviour patterns. In fact,
some of the features initially suggested as
characterizing dis- placement activities (e.g.
the absence of evident external stimulation, and
morphological differ- ences from the same
behaviour patterns in their normal context)
proved not to be entirely reliable. For example,
it became apparent that (1) displace- ment
activities can be strongly influenced by their
normal causal factors (e.g. displacement
grooming by state of the plumage: van Iersel
& Bol 1958; displacement feeding by degree
of prior food deprivation: McFarland 1965) and
(2) under certain circumstances displacement
activities need not be incomplete or imperfectly
oriented but might be indistinguishable in form
or orientation from the same behaviour patterns
in normal con- texts (Morris 1954; but see Roper
1984). The virtual absence of reliable
morphological criteria to ident- ify
displacement activities has the consequence that
their identification is based almost exclusively
on a contextual analysis. Although the
occurrence of one displacement activity rather
than another in a given situation may be related
to the ongoing activity of the animal (e.g. its
posture; Tinbergen 1952), this behaviour usually
has no obvious relationship with the presumed
motivational state of the animal at that
moment.
In several recent studies conducted on
primates (Schino et al. 1988, 1990; Aureli &
van Schaik t991; Troisi et al. 1991), we have
suggested that the analysis of the occurrence of
displacement activities may provide insight into
the emotional state of an animal and that, in
spite of the problems of causal and functional
analysis, this descriptive behavioural category
could still provide a meaningful contribution to
the general understanding of animal behaviour.
The occurrence of displacement activities is
associ- ated with a state of internal conflict
in animals and such a condition of motivational
ambivalence is commonly believed to have an
emotional counter- part (e.g. in the form of
uncertainty or anxiety). It is well known that
experimentally induced conflict situations (e.g.
in traditional conflict tests such as punished
drinking) are accompanied by a wide variety of
autonomic responses including respiratory,
circulatory and thermoregulatory changes (e.g.
see Andrew 1956b). The physiological changes
associ- ated with autonomic activation can, in
fact, provide a set of stimuli arising from the
pelage or feathers, skin and blood vessels,
which might be expected to elicit a variety of
self-maintenance activities (among which
displacement activities are most common; see
Andrew 1956a, b). Without necessarily making
inferences about the mechanisms underlying
displacement activities, however, their
consistent association with the activation of
the autonomic nervous system would make them a
powerful tool to identify and analyse such
emotional states as uncertainty and anxiety, of
which the activation of the autonomic nervous
system is one of the more distinctive
characteristics.
In this paper we review current knowledge
about displacement activities in primates and
the information available to support the notion
that they may represent a useful behavioural
tool to investi- gate the emotional status
associated with social interaction in
primates.
EMOTIONS IN PRIMATES
Inferring an animal's internal state from
the observation of its behaviour is not a
completely new procedure for ethologists. For
example, ethologists have frequently assumed
that the motivational state underlying a given
posture can be assessed from the behaviour that
accompanies or follows it, for example, the
probability of a bird attacking or fleeing after
posturing (Moynihan 1955; Hinde 1970). Although
scientists routinely infer motivational states
such as hunger and fear, they are considerably
more reluctant to consider internal states
associated with social interactions, such as
affection or ambivalence, trust or jealousy. A
growing number of studies have recognized that
the cognitive capabilities of primates can be
expressed at their best in the social
environment, as opposed to the traditional
experimental contexts in which animals are
confronted with problem solving and tool use
(Jolly 1966; Humphrey 1976; Kummer 1982; Byrne
& Whiten 1988; Cheney & Seyfarth 1990).
However, while awareness of social relation-
ships by primates and their mental processes and
intentionality are now openly discussed,
references to feelings and emotions are
conspicuously lacking (but see Cheney &
Seyfarth 1990).
From studies on human subjects it is
apparent that emotion and cognition are closely
interwoven (see Hinde 1985). The elicitation of
an emotional state often depends on similarities
or discrepancies between aspects of the external
situation as it is perceived and what is desired
or expected. Complex social relationships are
likely to have a strong emotional component, for
the behaviour of a partner in an ongoing
relationship often confirms or disrupts
expectancies, interrupts behavioural sequences,
or arouses conflicting motivations.
Social interactions of primates take place
on a firm basis of recognition between
individuals and imply awareness by individuals
of the quality of relationships (e.g. in terms
of dominance rank, kin- ship, or friendship)
even between other individuals (Cheney &
Seyfarth 1990). As such, they are likely to
involve definite expectancies about any
interactant's responses. Moreover, the term
'negotiation', recently used to describe the
nature of a large part of the social
interactions of primates (e.g. see Dunbar 1988),
emphasizes that much interaction involves
attempts to control the partner or to adapt
one's behaviour to that of the partner. On these
grounds it is reasonable to believe that
socially living monkeys frequently experience
conflicting impulses, and that uncertainty and
anxiety are a more or less inevitable aspect of
social interaction. Since we cannot interview
the animals and ask them for their subjective
perceptions of certain situations and their
emotional reactions to them, we can only look
for physiological or behavioural indicators of
emotional states. The evidence pre- sented in
the following sections strongly suggests that
displacement activities may well be one of these
behavioural indicators in primates.
DISPLACEMENT ACTIVITIES IN
PRIMATES
Information on displacement activities in
primates is scanty. First of all, there is no
unequivocal agree- ment on which behaviour
patterns in the primate repertoire can actually
occur as displacement activities. Frequently
primatologists allude to the 'displacement'
nature of some behaviour patterns anecdotally
reported to occur in particular circumstances.
As in many other animal species, the behaviour
patterns most frequently reported as
displacement activities in primates include body
care activities.
Scratching and autogrooming are easily
observable body care activities in primates and
are among the most commonly reported
displacement activi- ties (scratching: Kummer
1968; Bertrand 1969; Russell & Russell 1985;
Diezinger & Anderson 1986; Easley et al.
1987; Schino et al. 1988, 1990; Aureli et at.
1989; Pavani et al. 1991; Aureli & van
Schaik 1991; autogrooming: Bertrand 1969; Goosen
1974a, b; Russell & Russell 1985; Troisi
& Schino 1987; Schino et al. 1988, 1990;
Lopez-Vergara et al. 1989; Aureli & van
Schaik, 1991). Displacement yawning has
frequently been reported (Carpenter 1934, 1940;
Hinde & Rowell 1962; Rowell & Hinde
1963; Kaufman & Rosenblum 1966; Kummer 1968;
Bertrand 1969; Redican 1975; Hadidian 1980;
Baenninger 1987; see also Easley et al. 1987;
Schino et al. 1988, 1990; Troisi et al. 1990)
and distinguished from normal yawning for
its being frequently repeated and the teeth more
clearly displayed (Bertrand 1969). In this view,
yawning acquires a threat meaning when
the performer looks directly at the addressee
(Bertrand 1969). Body shaking (a shaking move-
ment of the body similar to that displayed by a
wet dog) is referred to as a displacement
activity by Rowell & Hinde (1963), Schino et
al. (1988, 1990) and Aureli & van Schaik
(1991). Displacement feeding has sometimes been
reported (Schaller 1963; Bertrand 1969).
The fact that the occurrence of these
behaviour patterns is often irrelevant with
respect to their obvious biological function, or
to the stimuli that normally cause them,
supports the view that they can occur as
displacement activities. In the primate
literature, however, other behaviour patterns
have been considered as displacement activities
without reference to these generally agreed
standards of relevance. For example, male-male
genital presen- tation and mount were
categorized as displacement activities by
Bertrand (1969) and Russell & Russell (1985)
and included within tension behaviour by Easley
et al. (1987), because they are said to occur
out of their 'normal' context, i.e. a
heterosexual interaction, and because they are
'incomplete' com- pared with true sexual mounts.
Likewise, male monkeys carrying unrelated
infants were con- sidered to be performing
'pseudoparental acts' and the latter were
considered as displacement activities because
they did not occur in an 'appropriate' con- text
(Russell & Russell 1985). Although the
occurrence of the latter behaviour patterns
(e.g. the male-male mount in baboons) may be
related to an unstable social situation and risk
of aggression (see Chadwick-Jones 1989), their
inclusion in the category of displacement
activities only on the grounds of their
occurrence out of their most com- mon context
does not seem to be fully justified. In fact,
many behaviour patterns can have different
functions in different species and in different
contexts. For example, yawning that
occurs during an agonistic interaction may have
a definite threat meaning in baboons, Papio
cynocephalus anubis (Hall & De Vore 1965),
inter-male mount may be an assertive behaviour
(Chadwick-Jones 1989), and carrying an infant
can be used by male monkeys as a buffer against
other males' aggression (Deag & Crook 1971;
Hrdy 1976). If irrelevance to the ongoing
context is to be considered as one of the more
reliable clues to identifying displacement
activities, this seems not to be the case for
such behaviour, for a clear function is evident
in the context in which it is performed.
Therefore, it should not necessarily be argued
that a motivational conflict underlies the
exhibition of such behaviour.
DISPLACEMENT ACTIVITIES AS INDICATORS OF
EMOTIONS
Behavioural Evidence
Evidence indicates that primate displacement
activities are more frequent in stressful
situations. Some reports consist only of
anecdotal observations but in other cases
quantitative data have been provided. Increased
proximity between individuals occur- ring at
feeding sites or associated with direct social
interactions (e.g. an approach for grooming),
insofar as it brings about an increased
probability of aggression, is presumably
associated with behavioural ambivalence and
anxiety. There are anecdotal reports of
displacement activities occurring frequently in
such circumstances, such as Smuts' (1985)
description of a female olive baboon, Papio
anubis, undecided over whom to feed near: 'she
scratched herself several times, as baboons
often do before making a decision'. Likewise,
Hadidian (1980) observed that 'a low ranking
adult male Macaea nigra yawned repeatedly
after a dominant had approached and sat nearby'
and Bertrand (1969) that 'when a macaque is
approached by a dominant it may chew and even
swallow things that it would not normally eat'.
The increased occurrence of scratching and
autogrooming by macaques in proximity to a
higher-ranking individual has also been reported
quantitatively. For example, Troisi & Schino
(1987) found that, in group-living longtailed
macaques, Macaca fascieularis, female
autogrooming is more frequent within 1 m of the
alpha male than in the conditions of 'alone' or
'in passive contact'. Analogous results
concerning scratching behaviour in long-tailed
macaques were obtained by Pavani et al. (1991).
The increased frequency of displacement
activities in proximity to a dominant male may
be explained by considering this situation as
one in which two opposing social tendencies are
in conflict: the one to approach the male
further (e.g. in order to groom him or to sit in
bodily contact with him) and the tendency to
avoid the male test he attacks (Troisi &
Schino 1987). Diezinger & Anderson (1986),
examining the occurrence of scratching by rhesus
macaques, Maeaca mulatta, at a feeding site,
found that intermediate-ranking individuals are
the ones who scratch themselves most: 'these
individuals appear to be more aroused or
frustrated than dominants, who can easily
monopolize the food, and than subordinates, who
may stay clear of the feeding area and not even
try to get access to the food'.
Displacement activities are also reported to
occur frequently during or immediately after
agonistic interactions. According to Poirer
(1974), scratching is one of the most common
displacement activities of male colobines during
territorial conlicts. Among long-tailed
macaques, intra-group aggression is followed by
a dramatic increase in the rate of scratching,
body shaking and autogrooming by the victim
(Aureli et al. 1989; Aureli & van Schaik
1991). Among rhesus macaques as well, vic- tims
spend more time autogrooming after severe
aggression (de Waal & Yoshihara 1983). One
might argue that post-aggression body care
activities are merely due to pelage dishevelment
or tissue damage, especially if contact
aggression has occurred. However, this
explanation can be dismissed since
reconciliation (also when the analysis is
limited only to brief affiliative contacts) and
redirection are effective in reducing the rate
of these activities (Aureli & van Schaik
1991; see below). Displacement activities
occurring after an aggressive episode, instead,
might reflect the internal conflict between
with- drawing, because of the fear of renewed
attacks by the former aggressor, and
approaching, in order to achieve reconciliation.
Displacement activities might also reflect the
arousal due to the uncertainty about the future
social position, for victims are more likely to
receive further attacks (Aureli & van Schaik
1991) and less likely to be tolerated around
resources (Cords 1992).
Risk of aggression associated with
assessment of social status may also bring about
high levels of displacement activities. When two
unfamiliar female macaques are paired in a
relatively small cage, the delayed establishment
of clearcut dominance relationships brings about
a sharp increase in the frequency of scratching,
autogrooming and yawning over time
(Schino et al. 1990; see also Rowelt & Hinde
1963). In contrast, when unfamiliar macaques
rapidly display a formal indicator of status
differences such as the bared-teeth display,
displacement activities are much less frequent.
The pairing of familiar individuals, whose
dominance relationships have already been
established, results in the exhibition of
displacement activities with a frequency
comparable to that of the unfamiliar macaques of
the latter group. Thus, regardless of
familiarity with the partner, the uncertainty
about assessment of social status is associated
with high levels of body care patterns (Schino
et al. 1990). The relation between dominance
rank and the occurrence of displacement
activities, however, is not clear. High-ranking
individuals tend to yawn more often than
low-ranking ones in Celebes macaques, Macaca
nigra (Hadidian 1980), in long-tailed macaques
(Troisi et al. 1990) and in chimpanzees, Pan
troglodytes (te Boekhorst et al. 1991). This
difference fits well with the hypothesis that
yawning is also a mild form of threat.
However, no such difference is found among
Japanese macaques, Macaea fuscata (Troisi et al.
1990). Very inconsistent results have been found
for scratching. Subordinate long- tailed
macaques scratch themselves at higher rates than
dominant ones (Pavani et al. 1991). On the other
hand, in baboons and chimpanzees, domi- nant
individuals scratch more frequently (Easley et
al. 1987; te Boekhorst et al. 1991). The
relation between dominance rank and scratching
is likely to be context-dependent. In fact,
there is no difference relative to dominance
rank in the baseline rate Of scratching among
rhesus monkeys; however, in a feeding context,
scratching increases in intermediate-ranking
individuals (Diezinger & Anderson 1986).
Similarly, subordinate Japanese macaque females
scratch themselves more often than dominant ones
during pregnancy but not after giving birth
(Troisi et al. 1991).
The occurrence of displacement activities
has been reported to be more generally
associated with a decision-making process.
Kummer (1968) noticed high rates of scratching
by male hamadryas baboons, Papio hamadryas,
during the initial phases of group coordination
for movement. Before determining the final
direction to be taken, the male leader appears
to be pulled in various directions by the
centripetal tendency of the females and the
behaviour of the male neighbours. As a possible
consequence of these conflicting impulses, the
males scratch frequently before shifting
position (Kummer 1968). Similarly, Diezinger
& Anderson (1986) reported that scratching
occurs at a high frequency in close temporal
association with a change in behaviour and
interpreted it in terms of a moderate indecision
on behalf of the performer.
In the cases explored so far, displacement
activities emerged in situations involving
uncertainty about how to behave and about other
individuals' intentions. In other cases, an
increase in the frequency of displacement
activities has been reported in situations where
a motivational conflict was not immediately
identifiable. This seems to be the case with
Scucchi et al. (1991), who reported that, in
oppositely sexed pairs of long-tailed macaques
under laboratory conditions, male displacement
activities increase during the periovulatory
phase of the female menstrual cycle, suggesting
that the presence of an ovulating female brings
about a generalized increase in male
arousal.
Physiological and Pharmacological
Evidence
The hypothesis that primate displacement
activi- ties arc a behavioural manifestation of
uncertainty and anxiety requires physiological
and pharmacological validation. In the first
case, it should be demonstrated that the
exhibition of these behaviour patterns is
consistently accompanied by physiological
changes typical of these states such as
increased heart rate, blood pressure and plasma
levels of cathecolamines and corticosteroids
(e.g. Axelrod & Reisine 1984). In the second
case, it should be shown that drugs that are
effective in eliciting or reducing clinical
anxiety (i.e. anxiogenics and anxiolytics) would
be capable of, respectively, increasing and
reducing the rate of displacement activities.
However, since there are no unequivocal
physiological indicators of anxiety (e.g. see
Morrow & Labrum 1978) whereas effective
anxiolytic and anxiogenic drugs are currently
available, the pharmacological validation would
probably be more convincing.
Direct evidence that, in non-human primates,
displacement activities are associated with
autonomic activation is lacking, even though
circumstantial evidence suggests that this may
be the case. Among macaques, separate studies
have reported that both heart rate and frequency
of scratching increase following an episode of
aggression and both are reduced after the
individual is groomed (Schino et al. 1988;
Aureli et al. 1989; Boccia et al. 1989).
However, no study has investigated directly the
relation between physiological and behavioural
measures.
More information is available as far as the
effects of drugs on displacement activities are
concerned. Among non-human primates, there is
evidence that following some anxiogenic
treatments, together with the physiological
reactions typical of an autonomic activation,
behavioural expressions appear that are very
similar to displacement activities. For example,
treatment of chair-restrained rhesus monkeys
with the anxiogenic compound B-CCE elicits a
wide range of pliysiological (increased heart
rate, blood pressure and circulating cortisol)
and behavioural changes such as increased
vigilance and scratching (Ninan et al. 1982;
Inset et al. 1984; Crawley et al. 1985),
yawning and chewing (Lagarde et al.
1990). In the stumptailed macaque, Macaca
arctoides, electrical and pharmacological
activation of the locus coeruleus, a major brain
noradrenergic nucleus which has often been
implicated in anxiety, elicits scratching and
yawning (Redmond & Huang 1979). In
group-living adult female longtailed macaques,
the acute administration of the anxiolytic drug
lorazepam causes a selective reduction in the
frequency of scratching (Schino et al. 1991),
this being especially marked in low-ranking
animals. Lorazepam has similar effects on
autogrooming (A. Troisi & G. Schino,
unpublished data). Similarly, midazolam tends to
reduce scratching behaviour in 30-week old
rhesus monkey infants, while treat- ment of the
same infants with I3-CCE tends to increase the
frequency of scratching and is associated with a
marked increase in the infant's contact-seeking
and maintaining behaviour with the mother
(Maestripieri et al. 1992).
Although a physiological validation would be
helpful, both the behavioural and the pharmaco-
logical evidence support the intuitive belief
that displacement activities may be a
behavioural expression of a state of anxiety. As
such, they could constitute an effective tool
for quantifying the monkeys' emotional
reactiveness to social or environmental
stressors with a non-invasive, purely
observational method.
Applications of Behavioural Indicators of
Emotions
What could the usefulness of a
behavioural measure of an emotional state be? In
what way could it help to improve the general
understanding of primate behaviour? As
previously observed, many aspects of the complex
social environment of primates can be considered
as tension-producing. Accordingly, mechanisms
for social adaptation are likely to have
evolved. The notion that allogrooming can serve
as a tension-reduction mechanism is an old one
(e.g. Terry 1970) but, probably for the lack of
an operational definition of tension, it has
scarcely been supported quantitatively. By using
displacement activities (scratching,
autogrooming, yawning and body shaking)
as a measure of tension, Schino et al. (1988)
found that, in caged hetero- sexual pairs of
long-tailed macaques, female allogrooming
significantly reduces the frequency of male
displacement activities both during the course
of allogrooming and after it, this being pro-
portional to the amount of grooming received.
These observations concur with Boccia et al.'s
(1989) finding of a heart rate reduction in an
individual being groomed, in providing
quantitative support for the tension-reduction
hypothesis. A similar use of displacement
activities was made by Aureli et al. (1989) and
Aureli & van Schaik (1991) to gather
quantitative evidence that, among groupliving
long-tailed macaques, reconciliation after
agonistic encounters or redirection of
aggression against a third individual reduce the
victim's level of tension. When reconciliation
between former opponents takes place,
scratching, body shaking and autogrooming
occurring after an attack decline much more
rapidly to baseline levels than when no
reconciliation occurs. A similar reduction in
the scratching rate (but not in body shaking and
autogrooming) occurs after the redirection of
aggression. These findings allowed the authors
to suggest that the function traditionally
attributed to reconciliation, that is to repair
the social relationship between the two
opponents, may also involve the immediate effect
of reducing the victim's anxiety and tension
(Aureli et al. 1989). Interestingly, the
reoccurrence of aggression against the victim,
which is one of the possible causes of the
victim's anxiety, is also reduced by both
reconciliation and redirection (Aureli & van
Schaik 1991).
In the examples mentioned above,
displacement activities were used to assess the
function of another behaviour pattern. They
served to provide quantitative evidence that
affiliative interactions can be intimately
related to the emotional states of the animals
and, specifically, that they are effective in
reducing the social tension associated with
certain behavioural interactions. However, since
the emotional reactions to external stimuli are
largely dependent on the subjective perception
of such stimuli, displacement activities can
also represent a means to reveal and evaluate
quantitatively differences between individuals
in how they react to stressful situations. A
large part of the variability in behavioural
strategies adopted by animals in a variety of
circumstances is related to the different
perception of their social environment as poten-
tially threatening for themselves. Measuring the
emotional reactiveness of individuals to various
kinds of social confrontations may allow one to
understand how individuals perceive the quality
of the relationships between themselves or to
explore the extent to which they are able to
cope with an unfavourabte external
environment.
To give an example, marked differences in
mothering styles (e.g. in terms of the role
played in maintaining contact with the infant
and of the frequency of restraint of the infant)
among primiparous and multiparous macaque
mothers have often been ascribed to a higher
anxiety in the former, possibly related to their
inexperience in evaluating the potential threats
to the infant (Mitchell & Stevens 1969;
Hooley & Simpson 1981). In fact, Troisi et
al. (1991) provided quanti- tative support for
this hypothesis by finding positive correlations
between rates of scratching and maternal
possessiveness and warmth, two com- posite
measures of quality of relationship that reflect
a possessive maternal style. Furthermore, only
the frequency of scratching recorded after
parturition was correlated with a possessive
maternal style. In contrast, scratching recorded
before parturition was not correlated either
with postpartum scratching or with maternal
style. These results emphasize that females may
react differently to motherhood. In other words,
maternal possessiveness could not be predicted
on the basis of differences between individuals
in baseline emotionality (prepartum scratching),
but actually reflected an emotional condition
triggered by the presence of the infant.
The characterization of the emotional
response of an animal to a particular social or
environmental confrontation may help to explain
why that animal performs one particular
behaviour instead of another and why in similar
situations different individuals adopt different
behavioural strategies. Being paired with an
unfamiliar individual in a cage of limited
dimension may be considered a stressful
situation. The distance between individuals is
considerably reduced and the animals do not have
any opportunity to escape or to obtain
assistance from third parties to settle their
disputes. Schino et al. (1990) showed that, in
several caged pairs of unfamiliar female
longtailed macaques, the unresolved
establishment of dominance relationships,
possibly because asymmetries in perceived
relative power (see Datta 1983) were not
clearcut, did not allow affiliative interactions
to take place and resulted in a rise in tension.
Conversely, in other pairs, when asymmetries in
perceived relative power were likely to be
substantial, dominance relationships were
rapidly established and the individual who
perceived the situation as more threatening (as
suggested by its higher frequencies of
displacement activities) was the one to take the
initiative for affiliative interactions
(unpublished data). As suggested by these
examples, displacement activities can provide a
valuable tool to highlight the differential
perception of a stressful situation by
individuals and to predict the direction in
which their interaction will evolve. The
investigation of emotionality underlying
individual differences in behavioural strategies
is likely to be one of the areas in which the
study of displacement activities can be more
fruitful. Nevertheless, in this area much work
is still to be done.
Methodological Problems
The use of displacement activities as
indicators of emotions in primates is
complicated by a number of methodological
problems. One of them is the difficulty of
distinguishing conflict-related behaviour
patterns from their normal counterparts, that is
from the same behaviour patterns displayed as
comfort activities. The criteria of functional
or causal irrelevance are difficult to apply
when body care patterns are at issue because it
is easy to overlook the causal stimuli or the
functional conse- quences of comfort activities.
Some authors have suggested that the behavioural
morphology (i.e. the intensity and/or duration)
of primate displacement activities may be a
distinguishing feature (Diezinger & Anderson
1986). Others have expressed the same idea in
more categorical terms: 'a displacement activity
is always fragmentary and incomplete when
compared with the same activity carried out in
its normal mood and context' (Russell &
Russell 1985). Studies testing this hypothesis
(e.g. by correlating differences in morphology
with other behavioural or physiological changes
occurring in a stressful situation) are needed.
The few available data are conflicting. On the
one hand, among captive chimpanzees rough
scratching (i.e. when the action performed
includes the movement of the arm) performed by
the dominant male is more likely to be
associated with agonistic conflicts and
bluffdisplays than gentle scratching (i.e. when
scratching takes place only through movement of
the hand or fingers; te Boekhorst et al. 1991).
On the other hand, in longtailed macaques,
anxiolytic treatment decreases not only the
frequency but also the mean duration of
autogrooming (A. Troisi & G. Schino,
unpublished data). This finding suggests that
displacement autogrooming is not necessarily
shorter than 'hygienic' autogrooming and that
morphological differences between displacement
activities and their normal counterparts need
not necessarily be expected.
Another complicating factor is the necessity
of defining accurately the emotional state
associated with the occurrence of displacement
activities. In the primate literature, the term
'tension' has often been used to describe the
inferred subjective experience of the individual
exhibiting a displacement activity. We believe
that the use of the term 'tension' should be
limited to the description of social situations
involving latent hostility or opposition between
individuals. Referring to the subjective
experience of the animal, the term 'anxiety'
seems to be more appropriate for several
reasons. First, in the clinical literature,
anxiety is defined as a state of apprehension or
uneasiness that stems from the anticipation of
danger (American Psychiatric Association 1987),
and primate displacement activities are commonly
observed under circumstances where an individual
is confronting a potential source of danger.
Second, motivational conflict, which is thought
to be a possible mechanism responsible for
displacement activities, is the paradigm used in
experimental psychopharmacological research for
modelling anxiety. Third, anti-anxiety drugs
have been shown to decrease the frequency of
occurrence of displacement activities (see
above). In a previous paper, Troisi et al.
(1991) have pointed out, however, that conflict
and anxiety are not necessarily overlapping
emotional states: an extremely anxious
individual is unlikely to experience uncertainty
between alternative courses of action (i.e.
conflict) because of its marked tendency towards
escaping the stressful situation. If so,
displacement activities should only reflect
moderate levels of anxiety. Alternatively, if
autonomic activation independent of conflict is
the mechanism responsible for displacement
activities, it is plausible to assume that these
behaviour patterns would also occur in states of
intense anxiety or fear. Our current knowledge
does not allow us to give a definite answer to
the question what are the emotional states
associated with primate displacement activities?
Studies based on behavioural, physiological and
pharmacological data are needed to clarify this
crucial issue.
CONSEQUENCES AND FUNCTIONS OF
DISPLACEMENT ACTIVITIES
Considering the amount of time
and energy invested by non-human primates in
displacement activities, it is reasonable to
pose the question whether these behaviour
patterns serve some adaptive function(s).
Displacement activities might serve as a means
of limiting the costs related to an internal
conflict and act as re-regulating activities
that in some way keep the animal within optimal
physiological or psychological limits (this
hypothesis has been advanced for stereotyped
behaviour in general, see Mason 1991). For
example, one could speculate that displacement
activities reduce distress by focusing the
animal's attention away from noxious stimuli or
by causing physiological changes. In this latter
regard, it is interesting to note that behaviour
involving body contact such as allo- grooming
has been shown to release endogenous opioids in
monkeys (Keverne et al. 1989).
Another possible function of displacement
activi- ties is social communication. Social
animals are continuously faced with choosing
between different behavioural options whose
consequences and suc- cess will depend crucially
on the internal motivational state and probable
future behaviour of other animals. As a
consequence, natural selection will favour
animals that become sensitive to every
spontaneous emergence of behaviour in others
that could represent possible clues from which
their future responses may be predicted (Krebs
& Dawkins 1984). The exhibition of
displacement activities might convey information
about an animal's mood and motivational state
and be relevant in all kinds of social
interactions in which the assessment of the
other's intentions is crucial (e.g. contests).
Classical ethological studies have demonstrated
that, in a variety of species, displace- ment
activities have become incorporated into a
definite display through the process of
ritualization (see Tinbergen 1952). In non-human
primates, there is no evidence that conflict
behaviour has evolved into display behaviour. A
notable exception is 'symbolic feeding' in
mountain gorillas, Gorilla gorilla beringei.
About 5-10 % of the chest-beating displays by
silverbacked gorilla males are preceded by
ritualized feeding: vines or herbs are gently
placed between the lips but are not ingested.
Members of the group recognize symbolic feeding
and generally move away from the actor, thus
escaping the subsequent violent parts of the
display (Schaller 1963).
However, ritualization is not a prerequisite
for social communication through displacement
activities to occur and two other possibilities
remain: (1) the exhibition of displacement
activities by an animal may convey information
and produce behavioural changes in others
because animals may have learned from past
experience some behavioural contingencies (e.g.
that a repeated sequence of scratching bouts by
a dominant male is likely to be followed by
aggression); and (2) individuals are capable of
generalizing the relationship between the
exhibition of displacement activities and the
sub- sequent behavioural responses of the
performer. Primates recognize that they have
emotions and that others have emotions and use
the attribution of emotions to others as a means
to predict and explain their behaviour: in other
words, they have what has been termed 'a theory
of mind' (Premack & Woodruff 1978; Premack
1988; for discussion about the levels
ofintentionality see Dennett 1988; Cheney &
Seyfarth 1990; Kummer et al. 1990).
As far as non-human primates are concerned,
if systematic evidence for awareness of
knowledge and attribution to others is scanty
(see Cheney & Seyfarth 1990), evidence
referring to emotions is virtually non-existent.
Speculations about whether primates use
displacement activities to make inferences about
emotional states or intentions should first be
preceded by experiments in which these behaviour
patterns are examined in terms of the responses
they evoke in others. Goodall (1986) put forward
the hypothesis that displacement activities in
chimpanzees can 'reflect emotional states and
convey information to others regarding the mood
and the intentions of the individual concerned'.
She observed that, in the context of group
travelling, scratching on behalf of the leader
'can be a clear-cut signal, indicating that he
is about to go'. Similarly, 'a mother, having
moved to a low branch prior to descending a
tree, stops, glances at her infant, and gives
slow but vigorous scratches down her side. An
obedient infant responds rapidly, hurrying to
cling to her for the descent' (Goodall 1986). In
captive chimpanzees, scratching by the dominant
male is frequently followed by appeasement
displays ('pant grunt') by other individuals
(Cervi & van Hooff 1990; te Boekhorst et al.
1991). Since scratch- ing is also frequently
associated with bluffdisplays, it has been
suggested that other individuals may predict
through scratching when the male is about to
display or to attack and to prevent it with
appeasement behaviour (Cervi & van Hooff
1990; te Boekhorst et al. 1991). On the whole,
however, the evidence of a communicative
function of chimpanzee scratching is far from
being compelling and the possibility that, in
the above mentioned cases, the individuals
reacted to other elements (e.g. piloerection)
which preceded an attack cannot be ruled out.
Possible support for the hypothesis that primate
displacement activities can be used as signals
comes from the finding that scratching and
yawning are sensitive to some kind of
voluntary control because they increase
following food reinforcement (Louboungou &
Anderson 1987; Anderson & Wunderlich 1988;
Anderson et al. 1990). Because displacement
activities can be conditioned, these authors
suggested that these acts are not rigid and
reflex but instead they can be used as a
communicative gesture.
In the analysis of the possible functional
significance of displacement activities, it
should be mentioned that a communicative
function that is unrelated to their being an
expression of an emotional state has also been
postulated. Some authors have taken for granted
that the exhibition of displacement activities
in contests has the immediate function of
distracting the partner or the opponent from
certain physical features of the performer
(that, for example, might elicit its
aggressiveness) or concealing the performer's
real intentions about the prosecution of the
interaction. Trivers (1985), considering the
appearance of displacement activities during
animal contests, hypothezised that they '...
may, in fact, serve to distract attention from
salient features of the interaction'. Similarly,
De Waal (1986) observed that 'when chimpanzees
try to ignore each other's intimidation displays
or when two adversaries are waiting for the
first conciliatory overture to occur, they may
turn their attention to something unimportant or
carefully inspect details of their own body as a
way of hiding apparent embarrassment or
disappointment', and discussed displacement
activities within the general framework of
deception among primates. On this view,
displacement activities are not regarded as a
behavioural expression of an emotional state,
but rather, their exhibition would be aimed at
concealing the animal's real emotions and
intentions. They would be part of that
particular kind of deception termed
'distraction' (Whiten & Byrne 1988) in which
the agent manipulates the attention of another
individual by shifting it from one locus in the
environment to a second locus (e.g. from one
part of the body to another one). However, this
presumed functio n of displacement activities
relies entirely on a subjective impression of
the human observer and no evidence exists to
support the claim that the performer is actually
attempting to manipulate the other's
attention.
GENERAL CONCLUSIONS
Displacement activities are among the
easiest behaviour patterns to observe in the
primate repertoire. However, while other aspects
of primate behaviour are currently being
analysed in great detail, these behaviour
patterns receive little attention from
primatologists. In this paper we have reviewed
current knowledge about primate displacement
activities by pointing to their potential values
as a behaviourat indicator of emotional states
associated with social interactions. Even though
the use of displacement activities as
behavioural indicators of primate emotions is
currently complicated by a number of
methodological problems, this seems to be a
promising area of research for two different
reasons. First, findings emerging from this kind
of study are likely to improve our general
understanding of the causal mechanisms and
functional consequences of displacement
activities, which is important considering that
our knowledge of these aspects has not
progressed in the last two decades. Second, the
use of displacement activities as simple
behavioural measures of emotionality can favour
the adoption of the ethological approach by
those researchers such as physiologists or
psychopharmacologists who are less familiar with
the recording of spontaneous behaviour in freely
interacting primate subjects. In addition to
these general contributions, the use of
displacement activities as behavioural
indicators of primate emotions may have
important implications for specific areas of
primate research. Information on the emotional
reactiveness of animals to social and
environmental stimuli may shed light on how
certain behavioural profiles are determined as
well as on how predispositions to pathologies
may arise. A wide range of genetic-
environmental influences may give rise to
differences between individuals in emotional
reactiveness to stressors. This, in turn, will
affect the general pattern of interaction
between the individuals and their environment. A
particularly strict relationship between
emotions and behaviour may be argued for
primates whose social life entails a high degree
of cognitive capabilities. In these animals,
social behaviour may have evolved functional
characteristics aimed at coping specifically
with emotional states, and in particular at
reducing anxiety associated with social
interactions. However, this hypothesis, as well
as the fact that different behavioural responses
of individuals confronted with similar
conditions (e.g. motherhood) might reflect
differences in emotionality, has so far only
been a matter for speculation. Measuring
reliable physiological and behavioural
indicators of these emotional states (and
displacement activities may well be included
among the latter) allows one to turn these
speculations into testable hypotheses.
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