Anim. Behuv.

, 1995, 50, 144-1453

On the relation between social dynamics and social learning
SABINE COUSSI-KORBEL* & DOROTHY M. FRAGASZYt
*Laboratoire de Primatologie-Biologique Evolutive, CNRS URA 373, Universitt de Rennes I
fPsychology Department, University of Georgia
(Received 20 May 1994; initial acceptance 12 September 1994;
final acceptunce 15 March 1995; MS. number: 466X)
Abstract. Experimental studies on social learning in animals have commonly centred on the psycho-
logical processes responsible for learning, and neglected social processes as potential inlluences on both
the likelihood of social learning and the type of information that can be acquired socially. A model
relating social learning to social dynamics among members of a group is presented. Three key
hypotheses of the model are (1) behavioural coordination in time and/or space supports the process of
social learning; (2) different kinds of coordination differentially support acquisition of different kinds of
information; and (3) the various forms of behavioural coordination will be differentially affected by
social dynamics. Several predictions relating inter-individual and group differences in social dynamics to
social learning that follow from these hypotheses are presented,
,i 1995 The Association for the Study of Animal Behaviour
Traditionally, social learning among animals has
been studied experimentally by psychologists
interested in demonstrating the phenomenon, and
in identifying the psychological processesrespon-
sible for learning (reviewed in Galef 1988; Heyes
1993; Laland et al. 1993). The typical experimen-
tal design has made use of a model and an
observer, isolated from other conspecifics. In
contrast, social learning has been considered by
ethologists and ecologists in relation to its contri-
butions to adaptive variations of behaviour within
groups over time, and as a source of variations of
behaviour across groups of the same species. At
present, these two traditions of research on the
same topic have little to say to one another.
The understanding of social learning from eco-
logical and comparative perspectives would be
aided by experimental attention to social learning
in groups rather than in individuals (Lepoivre
& Pallaud 1985). Heartening developments in
this direction are now occurring. For example,
Lefebvre (in press) suggests focusing on the
relations between competitive foraging strategies
and social learning. Lefebvres research pro-
Correspondence: D. M. Fragaszy, Psychology Depart-
ment, University of Georgia, Athens, GA 30602-3013,
U.S.A. (email: cmspsy37@uqu.ec.uga.edu). S. Coussi-
Korbel is at the Station Biologique, Laboratoire de
Primatologie-Biologique Evolutive, Universitd de Rennes
1, 35380 Paimpont, France.
gramme includes observations of spontaneous
interactions among free-ranging birds, as well
as traditional experimental studies of observer/
demonstrator pairs. Patterns of social learning
among the birds (Columbids) studied by Lefebvre
and co-workers reflect in part the frequent for-
mation of transient social groupings of relative
strangers during foraging (Giraldeau & Lefebvre
1986). Many animals, however, live for long
periods within the same social unit, and even birds
that form transient flocks may also spend much
time within stable social units, such as nesting
colonies (Hausberger, in press). Within stable
social groups, long-term social relationships
develop, and dynamic social processes influence
all aspects of life. Thus social learning takes place
within a structured social context for many ani-
mals. It seems likely that the specific social context
in which a group-living animal finds itself influ-
ences its opportunities for social learning, and per-
haps also its propensity to learn certain things from
certain individuals. This aspect of social learning
has not received the formal attention it deserves.
In this paper, we address the issue of social
learning in relation to social dynamics among
members of a group with stable membership. Two
dimensions of variation in social learning are of
interest to us: within group and between group,
including between species. Both are relevant to the
ecological and evolutionary significance of social
0003-3472/95/121441+08 $12.00/O D 1995 The Association for the Study of Animal Behaviour
1441
1442 Animal Behaviour, 50, 6
learning. To be able to discuss both of these
dimensions of variation, we need a general frame-
work to talk about social learning that is task- and
species-independent. Therefore, we adopt a con-
ceptual framework of social learning in terms of
behavioural coordination between individuals, and
in terms of the kind of information that may be
acquired by an observer from a demonstrator. That
is, we neglect for the moment the psychological
mechanisms of learning (i.e. the distinctions
between facilitation, enhancement, imitation, etc.).
Differences across species in social learning
have been proposed to reelect cognitive differ-
ences, most notably in comparisons of humans
with other species (e.g. Tomasello et al. 1993). It is
beyond the scope of this paper to evaluate the
evidence that cognitive factors are responsible
for individual and species differences in social
learning between animals. We simply note that
the obvious differences presented by humans
compared with other species in attributional
capacities, for example, are greater than those
found in comparisons of other animal species. A
presumed cognitive difference is merely a default
explanation for species differences in social learn-
ing among non-human animals. Here, we wish to
avoid the problem of identifying cognitive versus
social sources of species differences in social learn-
ing. As long as tests of our model can make use of
tasks that are easily within the capability of all
individuals studied, and as long as fundamental
differences in social cognitive skills (e.g. attribution)
are not involved, a cognitive explanation for species
differences is unlikely. The same argument applies
to individual differences within species.
In the following sections of this paper, we (1)
distinguish different forms of information that can
be acquired from another individuals activity; (2)
elaborate our conception of behavioural coordi-
nation; (3) consider the type of coordination that
supports obtaining each kind of information from
the behaviour of a conspecific; (4) consider the
relationship between social dynamics and behav-
ioural coordination; and (5) present several test-
able predictions drawn from this approach which
can address species differences in social learning.
TRANSMISSION OF INFORMATION
THROUGH BEHAVIOUR
A first requirement for the occurrence of social
learning is a stimulus that both draws the learners
attention and provides it with information. We
conceive of information being provided from
one animal to another through three forms of
stimulation.
(1) Affective stimuli, through affective displays
(in several modalities; e.g. visual, olfactory, audi-
tory). Also, stereotypical fixed action patterns that
trigger the same patterns in others, and species-
typical behaviour that results in species-normal
imprinting.
(2) Physical stimuli reflecting previous activity
(residual traces: Sherry & Galef 1984), such as a
scent or an object or surface that has been altered
by previous activity (gnawed sections, etc.).
(3) Activity stimuli, through movement and
interaction with other animals or objects in the
environment during ongoing activity.
These forms of socially provided stimuli are not
exclusive. Indeed, in many, if not most, situations,
all three will be present. For example, in the
common situation in which animals are feeding
near one another, each animal may be moving,
making sounds through its movements, providing
scents through its mastication and other process-
ing of foodstuffs, leaving bits of food nearby, and
occasionally making vocalizations associated with
feeding and contentment. The significance of the
categorization of the forms of stimuli available for
social learning for our purposes is that it allows us
to consider the predominant form of information
available in a given situation to a potential
learner. This, in turn, allows a more precise con-
sideration of the kinds of information that the
learner can acquire in that situation. All of these
forms of stimuli may contribute to social learning.
Their distribution across species should be related
to the social, sensory, behavioural and cognitive
characteristics of individuals in each species.
COORDINATION OF BEHAVIOUR
Behdvioural coordination is common to all forms
of social learning. In principle, we may distinguish
between two main forms of coordination: comple-
mentary (where behavioural asymmetry results)
and isomorphic (where behavioural similarity
results). Complementary coordination may occur,
for example, in teacher/pupil, mother/infant,
expert/scrounger or dominant/subordinate pairs,
where one individual modulates its behaviour
precisely to differ from another or to produce
Coussi-Korbel & Frugaszy: Social Ieurning
I-413
change in the other. For example, Giraldeau &
Lefebvre (1987) studied foraging in flocks of
pigeons, Columba livia, housed in an aviary. In
these flocks, when one individual used a special-
ized technique to obtain food, its foraging
successes were accompanied by scrounging in
others. Scroungers developed consistent comple-
mentary behavioural patterns in this situation.
This is an outcome similar to that seen in
dominant/subordinate pairs of chimpanzees, Pun
troglodytes, and mangabeys, Cercocebus f. torquu-
PUS, in which a more dominant individual exploits
the activities of subordinates (e.g. Menzel 1973;
Coussi-Korbel 1994). Although complementary
coordination involves a social transmission of
information, with the exception of teacher/pupil
relationships, it inhibits rather than supports the
transmission of a particular behaviour pattern,
skill or habit between members of a group, at least
as long as the particular social conditions support-
ing its occurrence are maintained (Giraldeau
& Lefebvre 1986; Anderson et al. 1992). For
example, Giraldeau & Lefebvre (1986) showed
that scroungers did not learn to obtain food
directly by opening a container as long as
scrounging was an effective option.
*
More often, social learning involves isomorphic
coordination of behaviour. An isomorphic co-
ordination of behaviour patterns between two or
more conspecific individuals occurs when one
individuals activity channels the attention of its
conspecific to an activity or an element in the
environment, such that behavioural similarity
between the two individuals increases. Coordi-
nation of behaviour in this sense is necessarily
sequential, rather than simultaneous. That is, A
provides a model for B as opposed to instances
where an external stimulus is responsible for
behavioural similarity in A and B. The conspecific
observer may acquire some general information
from the conspecific demonstrator, such as the
timing (through behavioural coordination in time)
or the location (through behavioural coordination
in space) of an activity and sometimes both
(through behavioural coordination in time and in
space). It may also learn more specific information
about the event or situation through further
observation of the demonstrator and/or through
its own activities. Although behavioural coordi-
nation involves actions already in an individuals
behavioural repertoire, it could contribute to
learning a new contingency when the socially
facilitated actions are exploratory or ha~c tile
effect of producing novel outcomes when applied
in new circumstances (Fragaszy et al. 1994).
Note that behavioural coordination in tjnlc
does not involve physical proximity across
individuals. In the former. observation of a con-
specific stimulates an individual to engage in sonl~
activity (e.g. feeding) while relatively distant
in space. Through monitoring the activities ot
others, the observer is brought up to date ;md
can synchronize its activities with those of others.
Behavioural coordination in this manner aids
group cohesion, and in that sense makes an
important contribution to social life. even in
species that do not exhibit more elaborated forms
of coordination in space or space and time. Main-
tenance of group cohesion may contribute to
detection and avoidance of predators, efficient
exploitation of resources, or other commonly pro-
posed advantages of group living. This argument
has been made by Boinski (1987) for squirrel
monkeys, Saimiri, and by several authors for flock
foraging birds (Crook 196 1; Ward & Zahavi 1973:
Krebs 1974; Emlen & Demong 1975; Clayton
1978).
Behavioural coordination in space does not
require proximity between individuals either.
In this form of coordination, an individual
approaches a place where another individual has
been active, but does so only after the other has
left. The first individual must tolerate the second
individual approaching the place or object the first
individual has vacated. In this case, naive indi-
viduals may learn about essential characteristics
of the environment through information provided
in the form of physical alterations of the environ-
ment which persist after the activity in question
has ended. In both this and the first form of
coordination, the observer is likely to acquire only
general information about essential features of the
environment from the demonstrator (such as the
affective value of the site or activity). It must
gain more specific information through its own
activities (at a distant site, or at a later time).
Only behavioural coordination in space and
time involves physical proximity between indi-
viduals. In this strong form of behavioural co-
ordination, an individual approaches the same site
as another and engages in a similar activity simul-
taneously with the other at that site (e.g. both
feed). This can involve using the same patterns
of action as the conspecific demonstrator (e.g.
1444 Animal Behaviour. 50, 6
applying the same types of food-processing behav-
iour), or the observer may behave somewhat
differently (for example, sniffing and inspecting a
food, rather than consuming it). This form of
coordination affords the observer its best oppor-
tunity to acquire detailed information from the
demonstrator about action, substrate and out-
come. This type of information is most related to
the forms of social learning commonly described
as emulation (Tomasello et al. 1987) or imi-
tation. To the extent that specific information
about ongoing activities is most easily acquired
when close by another, transmission of this type
of information is most constrained by achieve-
ment of a specific kind of behavioural coordi-
nation, which is in turn dependent upon social
dynamics.
In any case, the extent of behavioural coordi-
nation between individuals can be a useful predic-
tor of social learning. Learning (as an outcome) is
distinguished by a relatively long-lasting change in
behaviour; momentary adjustments in behaviour
are not considered as evidence of learning. Co-
ordination of behaviour involves behavioural
modifications in the short term. Coordination is a
behavioural process that supports social learning,
but it is not itself evidence of the outcome of
learning (that is, long-term behavioural change).
We are interested in both process and outcome,
but in this paper, we deal primarily with the
process.
DIRECTED SOCIAL LEARNING:
IDENTITY CAN MAKE A DIFFERENCE
We make a distinction between social learning
that occurs irrespective of the identity of the active
individual (that is, Non-specific social learning)
and social learning that occurs differentially as a
function of the identity of the active individual
(Directed social learning). In Non-specific social
learning, one individuals behaviour towards an
object or event increases the likelihood that any
other individual will display altered behaviour
towards the same object or event. In Directed
social learning, the identity of the active individual
influences its salience for the observer. That is,
particular individuals are more influential models
for certain individuals than are others. To con-
clude that Directed social learning has occurred,
as opposed to Non-specific social learning, one
has to show that individual identity influences the
transmission of information. Both Directed and
Non-specific forms of social learning can involve
all three forms (l-3 above) of socially provided
stimulation.
The difference between Non-specific and
Directed social learning is not necessarily related
to the form of information, the nature of the
cognitive process that allows an individual to
acquire information from the activity of another,
or the complexity of what can be learned. Rather,
it is the possibility of modulation of social learn-
ing as a function of pre-existing social relation-
ships that varies between Non-specific and
Directed social learning.
The distinction between Non-specific and
Directed social learning is important, biologically,
because whereas the first form permits behav-
ioural synchronization and homogeneity within
groups, the second form permits these outcomes
and several others as well. Directed social learning
can (1) support within-group differentiations of
behaviour, (2) increase the efficiency with which
specific information is transmitted across mem-
bers of a social group, as for example directional
transmission from parents to offspring, and (3)
a special case of (2) increase the efficiency of
information transmission from an individual with
unique information to others (i.e. from an
informed individual to naive individuals). All of
these characteristics add to the flexibility with
which members of a social group can accommo-
date to changing environmental and social con-
ditions. The opposite side of the coin is that,
owing to its reliance on pre-existing social re-
lationships, in Directed social learning, socially
acquired information does not spread evenly, in
time and/or in extent, through a group. These
features are relevant to the ecological significance
of social learning at the population level (Laland
& Plotkin 1990; Laland et al. 1993). Non-specific
social learning is more likely to support behav-
ioural homogeneity within groups or populations;
Directed social learning is more likely to support
variability of behaviour within an individual
through time or among members of a group at
any moment in time.
The clearest way to determine the occurrence of
Directed social learning, and to evaluate its con-
sequences for the transmission of information
among members of a social group or population,
is to manipulate experimentally the information
Coussi-Korbel & Fragaszy: Social learning
1445
possessed by different individuals in a social
group. Studies by Menzel (1973, 1974) with a
group of young chimpanzees and by De Groot
(1980) with weaver birds, Quelea quelea, consti-
tute pioneering efforts in this regard. In these
studies, coordination was studied in terms of
group movement patterns with respect to a hidden
goal, and exploitation of a hidden goal, the
identity and location of which only one individual
knew. Both studies showed that naive individ-
uals were more likely to follow the informed
individual than a naive conspecific in all circum-
stances. For the chimpanzees, Menzel (1973)
further noted the existence of a leadership hierar-
chy. That is, the readiness of naive chimpanzees
to follow a conspecific with privileged information
about the environment was a function of pre-
existing social relationships, and was parelleled by
the informed individuals readiness to share the
hidden food with its followers. In our terminol-
ogy, the birds as well as the chimpanzees dis-
played Directed social learning since informed
individuals were more effective models for a
naive animal than its naive conspecifics. However,
the chimpanzees performed a stronger form of
Directed social learning than did the bit& because
the identity of the informed animal additionally
influenced its salience for the naive conspecific.
We would therefore expect more variability of
behaviour through time within the group among
the chimpanzees than among the birds, because
individual chimpanzees will vary in the salience
they attach to specific others.
In a more descriptive vein, but with similar
aims, Cambefort (1981) studied the transmission
of information about the location of hidden food
in free-ranging baboons, Papio ursinus and vervet
monkeys, Cercopithecus aethiops. Cambefort
found group-specific patterns of information
transmission. The information spread through
certain pivotal individuals (the first to discover the
food) in vervet monkeys. In baboons, the food
was first discovered almost instantaneously by
juveniles, which then transmitted the information
to other age classes through their feeding activi-
ties. In our terminology, baboons apparently
exhibited Directed social learning because
juveniles learned from other juveniles more
readily than did adults. Vervet monkeys did not
display Directed social learning; all individuals
learned equally quickly from those that discovered
the food.
Most experimental studies of social learning
have made use of test paradigms that prevent
Directed social learning from being evident. Often
a single subject is exposed to a single model, and
the outcome of the exposure is monitored. To
detect Directed social learning one must demon-
strate that particular individuals acquire more
information from certain individuals than from
others. For example, demonstration of consistent
orders of transmission, such as from parents to
offspring or within an age class, is evidence of
Directed social learning. Transmission in Non-
specific social learning would be expected to fol-
low variable patterns of physical proximity among
individuals and would not result in consistent
patterns across time. Directed social learning is
likely to occur in groups where social dynamics
affect the salience of various individuals for
each other, and the probability of behavioural
coordination between specific individuals.
Social dynamics may favour the occurrence
of one or the other form of social learning.
For example, potato-washing among Japanese
macaques, Macaca jiiscata, spread very slowly
through the group in which this behaviour origi-
nated (see Nishida 1987 for a review). It has been
argued that the slowness of the spread of potato-
washing rules out imitative learning (Galef 1990;
Visalberghi & Fragaszy 1990a, b). On the other
hand, the patterned nature of the spread of
potato-washing (first to a juvenile peer, then the
innovators mother, then other juvenile peers, and
later or not at all to non-related adults) fits our
notion of Directed social learning, although the
necessary experimental procedures are lacking
from this field description to draw a strong con-
clusion on this point. Social dynamics among
Japanese macaques (moderately hierarchical and
with strong matrilineal relationships) would
support Directed social learning.
A METRIC FOR SOCIAL DYNAMICS
How can we characterize social dynamics within
groups in a manner general enough to support
comparisons across groups? The particular char-
acteristics of social interaction that are most
informative with regard to social functioning of
dyads within groups, and of whole groups relative
to other groups, will no doubt vary across species.
Moreover, social dynamics and, more generally,
1446 Animal Behaviour, 50, 6
behavioural responsiveness may vary across
groups within species, as is evident when compar-
ing captive groups of the same species held in
varying circumstances. It is beyond the scope of
this paper to formulate a detailed framework
suitable for characterizing all social groups along
the several potentially relevant dimensions of
social dynamics. However, differences in the fre-
quency and degree of spatial proximity sought
and tolerated between individuals are very evident
across species, and can often be related to other
well-studied aspects of social behaviour, such as
dominance structures, group cohesion etc. (see,
for example, Mason 1971, 1978; Thierry 1987; de
Waal & Luttrell 1989). Within groups, striking
asymmetry across dyads in social spacing is often
evident, as for example in species in which matri-
lineal relationships are expressed in social spacing
(e.g. rhesus macaques, M. mulatta). Frequent spa-
tial proximity outside of kinship (friendships) is
also common within groups, even those typically
exhibiting well-developed status relationships
(Cheney & Seyfarth 1990; Butovskaya 1993).
Given the evident correlation between spatial
affinity (which includes both seeking and tolerat-
ing proximity) and other important aspects of
social dynamics, and given the broad comparative
purpose of our model, it seems best at this time to
focus on the single variable of social spacing
(proximity) as the clearest summary of social
dynamics among individuals. In short, we propose
characterizing dyads within a group, or a group
among a set of groups (or species), as exhibiting a
certain pattern of social dynamics largely on the
basis of social spacing, as has Mason (1978).
THE RELATIONSHIP BETWEEN
SOCIAL DYNAMICS AND SOCIAL
LEARNING
In our conceptual framework, social learning by
an individual is supported by its behavioural
coordination with other individuals. The forms of
behavioural coordination likely to be achived by
certain dyads depend upon the social dynamics
among members of that group. In this way, social
dynamics influence the likelihood of social learn-
ing, and to the extent that what is learned is
affected by what forms of coordination occur,
social dynamics influence what is learned socially.
For example, more specific information about
actions (e.g. their form, orientation or timing) can
be given by means of ongoing behaviour than
through affective or residual trace information.
To the extent that information about ongoing
activities is most easily acquired when close by
another, the closer the proximity and the longer
and more frequently such proximity is attained
between individuals, the more likely they will
acquire more specific information from each
other. It also seems likely that the more proximity
is tolerated, the more likely that an observer may
augment socially acquired information with infor-
mation gained through its own activities at the
same place or with the same object at the same
time, or soon after, it has seen another individual
at that place. We think this general scenario of the
relations among social learning and tolerance is
likely to be the case among diurnal primates, for
example.
We predict that more extensive and more fre-
quent behavioural coordination in time and space
will be achieved among groups exhibiting an
egalitarian or tolerant style of social dynamics.
This style of social dynamics can support both
isomorphic coordination (where behavioural simi-
larity results) and complementary coordination
(where behavioural asymmetry results). Among
groups exhibiting a despotic or less tolerant style
of social dynamics, behavioural coordination in
space but not in time, or behavioural coordination
in time while relatively distant in space should
predominate. When coordination does occur
jointly in time and space, it is more likely to be
complementary (e.g. exploitative) in a despotic
group than in an egalitarian group. The frequency
of the other forms of coordination should depend
on the extent to which group members have access
to particular places and objects, and/or on the
extent to which they are able to focus attention on
events. Moreover, in species exhibiting a despotic
style of social dynamics, coordination should
occur at unequal rates across dyads in the group.
There is one additional manner in which we see
social dynamics affecting social learning, and that
is through its influence on attention (particularly
visual attention). We assume that visual attention
to others sets the stage for behavioural coordi-
nation. Thus, to the extent that social dynam-
ics direct an individuals visual attention to
particular others, they will affect the likelihood
that an individual will acquire information from
the behaviour of those others. Affiliative and
status relationships affect the likelihood of each
Coussi-Korbel & Fragaszy: Social learning
1447
individual attending visually to each other indi-
vidual in the group (Chance & Jolly 1970). A
recent study by Nicol & Pope (1994) suggests the
influence of previously developed social relation-
ships on visual attention to others in a social
learning context. In Nicol & Popes study, the
social transmission of key-pecking in small flocks
of adult laying hens, Gallus gallus domesticus, was
affected by the pre-existing social relationship
between observers and demonstrator. Observers
that were exposed to socially dominant demon-
strators learnt more quickly than those that were
exposed to socially subordinate or unfamiliar
demonstrators.
Demands for attention to others can also limit
attention to other events, and this can lead to
differential ability to focus on any particular other
individual as a source of information about the
non-social environment. Demands for frequent
visual monitoring of the social environment can
vary across individuals within a group in accord
with their current age, sex or social status (Alberts
1994) and across species. Squirrel monkeys,
Saimiri sciureus, and tamarins, Saguinus labiatus,
afford an example of how visual regard can vary
across species and within groups in ways relecant
to opportunities for social learning. Squirrel mon-
keys live in large groups which, in captivity at
least, exhibit modestly hierarchical organization,
whereas tamarins typically live in family groups.
In a variety of captive settings, squirrel monkeys
interrupted their foraging activities to monitor
their group mates more often than did tamarins.
Tamarins looked proportionally more frequently
at non-social targets when they interrupted forag-
ing (Caine & Marra 1988). Moreover, the degree
to which individual squirrel monkeys visually
scanned the social environment was related to
their social status. Lower-ranking individuals
monitored others more often than did higher-
ranking individuals. Even when space was
increased, and when an external distraction (a
potentially frightening novel object) was present,
the differences between the species in the extent of
social monitoring remained (Caine & Marra
1988).
We would predict that acquisition of infor-
mation from any particular other individual
would be lessened to the extent that the observer
cannot maintain its focus on that individual,
owing to competing attentional demands. For
example, compared with tamarins, squirrel
monkeys would be less likely to focus attention
upon another for more than brief moments, and
thereby less likely than tamarins to acquire
information from another about the non-social
environment.
In addition to influencing the probability and
form of attention and behavioural coordination,
social dynamics influence whether an individual
acts on information that it has acquired through
observation of others in its social group. This can
affect the course of social learning, and it can also
affect our ability to detect that the observer has
learned something. For this reason, if one is
interested in evaluating whether social learning
has occurred, it is important to provide each
subject with equal access to the relevant materials
under non-competitive circumstances (Visalberghi
& Frdgaszy 1990b).
EXAMPLES OF THE RELATION
BETWEEN SOCIAL DYNAMICS AND
BEHAVIOURAL COORDINATION
Comparisons of heterosexual pairs of squirrel and
titi monkeys illustrate the relation between social
dynamics and behavioural coordination at the
species level. Heterosexual pairs of titi monkeys.
Cullicebus moloch, a monogamous species, look at
one another more often and for longer periods
than do heterosexual pairs of squirrel monkeys,
which in nature live in large mixed-sex groups
(Mason 1971; Phillips & Mason 1976). Titi
monkeys develop strong affiliative relationships
between pair mates, whereas squirrel monkey pair
mates do not. Titi monkeys display stronger co-
ordination of behaviour with the pair mate in time
and space in many circumstances, such as feeding.
exploring novel objects, and moving through a
novel space. Social relations between pair mates
are mutual and overwhelmingly affiliativc in titis.
but relatively aloof and asymmetrical in pairs of
squirrel monkeys, with the male occasionally
exerting control over contested resources, and the
female often simply avoiding confrontation with
the male (e.g. Mason 1971, 1978; Fragaszy &
Mason 1978; Mendoza & Mason 1989). In our
terminology, the larger degree of behavioural
coordination among pair mates in titis, which
follows from the social dynamics within the pair.
corresponds to a greater likelihood of social
learning in this species than in pairs of squirrel
1448 Animal Behaviour, SO, 6
Table I. Potential outcomes of social learning
Outcome
1. Facilitation of learning by naive individuals about
essential characteristics of their environment
2. Extensive or rapid change in the affective response
to an event or stimulus
3. Maintenance of social cohesion via synchronization
of activities among group members
4. Rapid acquisition of new skills or information by
naive individuals
5. Homogenization of behaviour within groups
monkeys. We predict, for example, that accept-
ance of a novel food would be more affected by its
concurrent acceptance by its pair mate in titis than
would be the case for squirrel monkeys.
A second example of relations between social
dynamics and behavioural coordination between
individuals is available from studies by Aisner &
Terkel (1992) on the social transmission of pine
cone opening in black rats, Rattus rat&s. These
rats live in the Jerusalem pine forests in Israel;
their primary source of nourishment is the seeds
contained within the pine cones. The rats obtain
the seeds by means of a complex feeding behav-
iour. The only way in which rat pups acquire
the necessary feeding technique is to observe an
experienced individual and to interact with the
experienced individual while it is feeding on the
same pine cone. Behavioural coordination in time
and space between experienced and naive animals
is, however, only possible between mother and
offspring pairs during the short period that the
pups remain with their mother. When the young-
sters grow older, their experienced mothers do not
tolerate the close proximity of their offspring.
Naive animals do not learn the technique when
they are forced to stay some distance away while
observing an experienced animal, even when they
have unlimited access to cones during observation.
A MODEL OF THE RELATION
BETWEEN SOCIAL LEARNING AND
SOCIAL DYNAMICS
Table I lists several likely outcomes of social
learning, and Table II presents a summary of our
model of the relation between social learning
outcomes and social dynamics, mediated through
behavioural coordination. Table II indicates four
different features of behavioural coordination and
social learning, which we predict will vary in
accord with the type of social dynamics character-
istic of the group, and three hypothetical types of
social dynamics, from highly egalitarian to highly
despotic. Egalitarian societies show even distri-
butions of aggression and affiliation across dyads
and symmetrical distributions between members
of a dyad. Despotic societies are characterized by
a high degree of asymmetry in the direction of
initiated aggression and the frequency of affiliative
interactions among dyads. That is, certain dyads
exhibit primarily agonistic interactions, others
exhibit primarily affiliative interactions, and
within dyads, the direction of agonistic inter-
actions is predictable. Intermediate societies dis-
play the asymmetries present in despotic societies,
but less intensively and perhaps not across all
unrelated dyads.
In egalitarian societies, proximity is rather simi-
lar among all members of the group. Tolerant
egalitarian societies are characterized by frequent
close proximity among their members. Family
groups of titi monkeys are good examples of
tolerant egalitarian societies (e.g. during feeding:
Fragaszy & Mason 1983). We would expect all
three forms of behavioural coordination to occur
frequently in tolerant egalitarian societies, result-
ing in an even transmission of socially acquired
information through the whole group or popu-
lation, and a predominance of Non-specific social
learning.
In societies exhibiting an intermediate style of
social dynamics, subgroups will be present within
which spatial tolerance will be greater. Behav-
ioural coordination in time and space occurs more
often within these subgroups, while the two other
forms of behavioural coordination (time only, or
space only) may occur equally often among all
members of the group. Groups of capuchin mon-
keys, C&us apella, are good examples of societies
with intermediate characteristics: dominance
relations are present, but manifested only oc-
casionally; aggressive interactions are infrequent;
tolerance of others is prominent (OBrien &
Robinson 1993; Fragaszy et al. 1994; A. Skolnick,
H. Devermann & I. Bernstein, unpublished data).
Stumptail macaques, M. arctoides, are also an
example of an egalitarian to intermediate society
(Thierry 1987; de Waal & Luttrell 1989;
Butovskaya 1993). In such a society, we expect
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1450
Animal Behaviour, 50, 6
transmission of detailed information about ongo-
ing behaviour to occur more often between certain
individuals as a function of pre-existing social
relationships, to the extent that coordination
jointly in time and in space must be achieved
to acquire this information. That is, specific
behavioural skills are likely to be passed through
Directed social learning, rather than Non-specific
social learning, in societies exhibiting an inter-
mediate style of social dynamics. Other types of
information which can be learned through behav-
ioural coordination in space or in time should
spread evenly through the group or population
(through Non-specific social learning), in accord
with the individuals propensities to pursue the
relevant forms of coordination.
Finally, in highly despotic societies, only a few
dyads present in the group exhibit frequent toler-
ated proximity. Rhesus macaques are a good
example here (de Waal & Luttrell 1989). In des-
potic societies, social constraints and asymmetri-
cal affiliative relationships make Non-specific
social learning, and the concomitant even and/or
rapid spread of socially acquired information
through a group or population, unlikely. In these
societies, shared access to places and objects is
most reliably evident between parent and young
offspring. Directed social learning thus can occur
etfectively only among certain dyads. Moreover,
Non-specific social learning would be restricted to
those forms of information that do not require
extensive coordination in space and time. Even
with the less restrictive forms of coordination,
Directed social learning may predominate, as indi-
viduals attention may be directed asymmetrically
to specific others in the group (as in hamadryas
baboons, Papio hamudryas; Kummer 1971).
Table II also indicates some potential outcomes
of the social transmission of information in each
type of social dynamics. Note that there is some
overlap in outcomes, but that a rapid expansion of
the behavioural repertoire (that is, appearance of
a new skill, such as exploiting a new food source
through an instrumental action) of a whole group
or population can be achieved through social
learning only if the social dynamics of that group
or population permit the transmission of such
information through Non-specific social learning.
This set of circumstances is not likely to be
common in nature. Social learning may broaden
the behavioural repertoire of groups in many
species, but it is not likely to do so very quickly.
The model leads to several predictions about
variations within and between groups in social
learning. First, the extent of spatial proximity
under ordinary conditions should correlate posi-
tively across dyads in a group with the frequency
of joint coordination in time and space when
activities of interest to others occur. To test this
hypothesis, one must compare dyads within a
group independently on the two variables of
spatial proximity (under routine conditions) and
coordination (during a specific perturbation or
challenge).
An extension of this hypothesis is that, within
despotic groups, one or more subgroups will be
present within which greater tolerance during
normative conditions is associated with greater
tolerance during challenging conditions (i.e. when
ongoing behaviour of another individual is
especially interesting to the observer). This pre-
diction is relevant to the occurrence of Directed
social learning.
Second, the degree of similarity to the demon-
strators behaviour achieved by an observer is
likely to be correlated with degree of proximity
achieved by the observer during the demonstra-
tors relevant ongoing behaviour. This prediction
depends on the assumption that the closer the
proximity between partners, the more detailed
information can be acquired. Hausberger (in
press) provides support for this prediction. Within
groups of starlings, Sturnus vulgaris, the number
of shared variants of song in any dyad reflects the
time spent in proximity by these dyads compared
to others in the same group. In some species, such
as many primates, individual testing might be
necessary to assess the observers performance,
because social dynamics within a group can
influence individual performance (Fragaszy &
Visalberghi 1990; Visalberghi 1990; Visalberghi
& Fragaszy 1990b).
A third prediction applies to between-group
comparisons. We predict that transmission of
information from ongoing behaviour (as through
joint coordination in time and space) will be
greater in more egalitarian groups (exhibiting
more homogeneous patterns of proximity) than
more despotic groups (exhibiting more hetero-
geneous patterns of proximity). First, social
dynamics can affect the information a demon-
strator provides. Individuals can inhibit behav-
iour or alter their behaviour as a function of
social constraints (as, for example, an informed
Coussi-Korhel & Frugaszy: Social leurning
1451
individual of low rank avoiding the site of hidden
food when a high-ranking companion is near by;
Coussi-Korbel 1994). Second, social dynamics can
affect the frequency and degree of joint coordi-
nation in time and space, which we predict best
supports the transmission of this kind of infor-
mation. Studies of social learning outcomes
comparing groups with different social dynamics
are needed for a proper test of the prediction.
A fourth prediction is that social dynamics will
influence behavioural coordination only, or most,
in the case of ongoing behaviour, and less in the
case of the other two classes of information. This
is more problematic to test for residual trace
information than for affective information,
because access to residual trace information might
vary within a group depending on the extent of
direct competition over access to it. For example,
if the site of another individuals activity attracts
interest, certain individuals among those attracted
to the site may pre-empt the approach of others.
In natural environments, direct competition over,
and potential monopolization of, residual trace
information is less likely than in captive environ-
ments (where space is more limited). Affective
information is less likely to be subject to monopol-
ization in any environment, as it is transient.
Of course, the type or quantity of information
that can be acquired by an individual from the
behaviour of others might depend upon cognitive
and sensory abilities, as well as social dynamics,
all other things being equal. This is relevant to
both within- and between-group comparisons, but
it is most obvious in cross-species comparisons.
We do not mean to imply that social dynamics are
the only basis for variation across individuals in
social learning. Clearly, sorting out the contri-
butions of multiple factors in any particular case
will require convergent evidence. In any case, for
an unbiased comparison of social learning across
groups or individuals, one must provide oppor-
tunities to obtain information which are within
the sensory and cognitive capacities of all indi-
viduals to be studied, and one must provide a
probable and accessible means for any possessor
of this information to express its knowledge in
behaviour. Variations of tasks that have clear
ecological validity and abiding salience for the
individuals under study (such as naturalistic for-
aging tasks) are more useful for this purpose than
presentation of novel tasks, the mastery of which
is inherently improbable. Novel tasks requiring
improbable actions may be needed to provide
unequivocal evidence of imitation (Visalberghi
& Fragaszy 1990a), but they are not needed
or desirable for an analysis of social learning
generally.
CONCLUSIONS
Advances in our conception of social learning as a
biologically significant phenomenon require con-
sideration of more factors than the psychological
mechanisms of learning (i.e. the distinctions
between facilitation, enhancement, imitation,
etc.). The field is in some danger of drowning in
semantic arguments over these issues (e.g. Galef
1988; Whiten & Ham 1992). The model presented
here looks at social learning from the perspective
of information acquired, rather than the psycho-
logical process responsible for its acquisition.
Therefore, it is independent of process-driven
arguments, with their thicket of semantic distinc-
tions. It generates a spectrum of testable hypoth-
eses concerning the relation between social
dynamics and social learning. It might contribute
to resolving the apparent paradox that some of
the most striking examples of social learning are
found in species that are phylogenetically distant
from humans (e.g. birds and rats) rather than in
primates. We agree with Laland et al. (1993) and
Box (1994) that the assumption of more extensive
or more sophisticated social learning in mammals
in general, and non-human primates in particular,
because of their phylogenetic proximity to our-
selves, is unwarranted. Social learning is more
likely to vary in biologically meaningful ways
as a function of social characteristics and social
setting, and the kinds of information that might
be transmitted socially, than as a function of
phylogeny per se. The contribution of sociality to
social learning, and to its variation within and
across groups, deserves our attention.
ACKNOWLEDGMENTS
The preparation of the manuscript was supported
by the University of Rennes I through the pro-
gramme Invitation dun chercheurlenseignant
etranger and by the Public Health Service of the
United States, through a Research Scientist
Development Award to D.M.F., and by a joint
grant from the Centre National de la Recherche
1452 Animal Behaviour, 50, 6
Scientifique and the Ministere de 1Education de
la Jeunesse et des Sports, France and by the
University of Rennes I to S.C.-K. We thank
Heather McKiggan, Hilary Box and Elisabetta
Visalberghi for commenting on a previous version
of the manuscript.
REFERENCES
Aisner, R. & Terkel, J. 1992. Ontogeny of pine cone
opening behaviour in the black rat, Ruttus rutfus.
Anim. Behav., 44, 321-336.
Alberts, S. C. 1994. Vigilance in young baboons: effects
of habitat, age, sex, and maternal rank on glance rate.
Anim. Behav., 41, 749-155.
Anderson, J. R., Fornasieri, I., Ludes, E. & Roeder, J.-J.
1992. Social processes and innovative behaviour in
changing groups of Lemur fulvus. Behav. Proc., 21,
101~112.
Boinski, S. 1987. Birth synchrony in squirrel monkeys
(Saimiri oerstedii): a strategy to reduce neonatal pre-
dation. Behav. Ecol. Sociobiol., 21, 393400.
Box, H. 0. 1994. Comparative perspectives in primate
social learning: new lessons for old traditions. In:
Current Primatology. Vol. II. Social Development,
Learning, and Behaviour (Ed. by J. J. Roeder, B.
Thierry, J. R. Anderson & N. Herrenschmidt),
pp. 321-327. Paris: Universitt Louis Pasteur Press.
Butovskaya, M. 1993. Kinship and different dominance
styles in groups of three species of the genus Macaca
(M. arctoides, M. mulatta, M. fascicularis). Folia pri-
matol., 60, 210-224.
Caine, N. G. & Marra, S. L. 1988. Vigilance and social
organization in two species of primates. Anim. Behav.,
36, 897-904.
Cambefort, J. P. 1981. A comparative study of culturally
transmitted patterns of feeding habits in the chacma
baboon Papio ursinus and the iervet monkey Cercop-
ithecus aethiops. Folia primatol., 36, 243-263.
Chance, M. R. A. & Jolly, C. 1970. Social Groups of
Monkeys, Apes and Men. London: Jonathan Cape.
Chenev, D. L. & Sevfarth, R. M. 1990. How Monkevs
See ;he World. Chicago:University of Chicago Press.
Clayton, D. A. 1978. Social facilitated-behavior. Q. Rev.
Biol., 53, 313-391.
Coussi-Korbel, S. 1994. Learning to outwit a competitor
in mangabeys (Cercocebus t. torquatus). J. camp.
Psychol., 108, 164-171.
Crook, J. H. 1961. The basis of flock organisation in
birds. In: Current Problems in Animal Behaviour (Ed.
bv W. H. Thorne & 0. L. Zanewill). DD. 125-149.
Cambridge: Cambridge Universit; Press. a
De Groot, P. 1980. Information transfer in a socially
roosting weaver bird (Quelea quelea; Ploceinae): an
experimental study. Anim. Behav., 28, 1249-1254.
Emlen, S. T. & Demong, N. J. 1975. Adaptive signifi-
cance of syncrhonized breeding in a colonial bird: a
new hypothesis. Science, 188, 1029-1031.
Fragaszy, D. M. & Mason, W. A. 1978. Response to
novelty in Saimiri and Callicebus: influence of social
context. Primates, 19, 31 l-331,
Fragaszy, D. M. & Mason, W. A. 1983. Comparisons of
feeding behavior in captive squirrel and titi monkeys
(Saimiri sciureus and Callicebus moloch). J. camp.
Psychol., 91, 3 l&326.
Fragaszy, D. M. & Visalberghi, E. 1990. Social processes
affecting the appearance of innovative behaviours in
capuchin monkeys. Folia primatol., 54, 155-165.
Fragaszy, D. M., Vitale, A. F. & Richie, B. 1994.
Variation among juvenile capuchins in social influ-
ences on exploration. Am. J. Primatol., 32, 249-260.
Galef, B. G. 1988. Imitation in animals: history, defi-
nition, and interpretation of data from the psycho-
logical laboratory. In: Social Learning. Psychological
and Biological Perspectives (Ed. by T. Zentall & B.
Galef), pp. 3-28. Hillsdale, New Jersey: Lawrence
Erlbaum.
Galef, B. G. 1990. Tradition in animals: field obser-
vations and laboratory analysis. In: Interpretation and
Explanation in the Study of Animal Behavior (Ed. by
M. Bekoff & D. Jamieson), pp. 7495. Boulder,
Colorado: Westview Press.
Giraldeau, L. A. & Lefebvre, L. 1986. Exchangeable
producer and scrounger roles in a captive flock of
feral pigeons: a case for the skill pool effect. Anim.
Behav., 34, 797-803.
Giraldeau, L. A. & Lefebvre, L. 1987. Scrounging
prevents cultural transmission of food-finding behav-
iour in pigeons. Anim. Behav., 35, 387-394.
Hausberger, M. In press. How studies on vocal com-
munication in birds contribute to a comparative
approach of cognition. Ethology.
Heyes, C. M. 1993. Imitation, culture and cognition.
Anim. Behav., 46, 999-1010.
Krebs, J. R. 1974. Colonial nesting and social feeding
as strategies for exploiting food resources in the
great blue heron (Ardea herodius). Behaviour, 51,
99-130.
Kummer, H. 1971. Primate Societies. Chicago: Aldine.
Laland, K. N. & Plotkin, H. C. 1990. Social learning
and social transmission of foraging information in
Norway rats (Raftus norvegicus). Anim. Learn. Behav.,
18, 246-251.
Laland, K. N., Richerson, P. J. & Boyd, R. 1993.
Animal social learning: toward a new theoretical
approach. In: Perspectiies in Ethology, Vol. 10 (Ed. by
P. H. Klonfer. P. P. Bateson & N. Thomson).
pp. 249-278. New York: Plenum.
Lefebvre, L. In press. The comparative method and the
ecology of learning: a study of imitation in Columbids
and their foraging associates. Behav. Proc.
Lepoivre, H. & Pallaud, B. 1985. Social facilitation in a
troop of Guinea baboons (Papio pupio) living in an
enclosure. Behav. Proc., 11, 405418.
Mason, W. A. 1971. Field and laboratory studies of
social organization in Suimiri and Cullicebus. In:
Primate Behavior: Developments in Field and Labora-
tory Research (Ed. bv L. Rosenblum). DD. 107-137.
New York: Academic Press.
I I.
Mason, W. A. 1978. Ontogeny of social systems. In:
Recent Advances in Primatology, Vol. I. Behaviour
(Ed. by D. J. Chivers & J. Herbert), pp. 5-14.
London: Academic Press.
Coussi-Korbel & Fragaszy: Social learning
1453
Mendoza, S. P. & Mason, W. A. 1989. Primate relation-
ships: social dispositions and physiological responses,
In:- Perspective; in Primate Biology (Ed. by- P. K.
Seth & S. Seth). DD. 1299143. New Delhi: Todav &
Tomorrows Print& and Publishers.
Menzel, E. W., Jr. 1973. Leadership and communication
in young chimpanzees. In: Precultural Primate Behav-
ior (Ed. by E. W. Menzel, Jr), pp. 192-225. Base]:
Karger.
Menzel, E. W. 1974. A group of young chimpanzees in a
one-acre field. In: Behavior of Nonhuman Primates
(Ed. by A. M. Schrier & F. Stollnitz), pp. 83-153.
New York: Academic Press.
Nicol, C. J. & Pope, S. J. 1994. Social learning in small
flocks of laying hens. Anim. Behav., 47, 1289-1296.
Nishida, T. 1987. Local traditions and cultural trans-
mission. In: Primate Societies (Ed. by B. Smuts, D.
Cheney, R. Seyfarth, R. Wrangham & T. Struhsaker),
pp. 462474. Chicago: University of Chicago Press.
OBrien, T. & Robinson, J. G. 1993. Stability of social
relationships in female wedge-capped capuchin
monkeys. In: Juvenile Prim&es: Life History,
Development, und Behavior (Ed. by M. Pereira &
L. Fairbanks), pp. 1977210. New York: Oxford
University Press.
Phillips, M. J. & Mason W. A. 1976. Comparative
studies of social behavior in Callicehus and Saimiri:
social looking in male-female pairs, Bull. psychonom.
Sot., 7, 55556.
Sherry, D. F. & Galef, B. G. 1984. Cultural transmission
without imitation: milk bottle opening by birds.*Anim.
Behav., 32, 937-938.
Thierry, B. 1987. Coadaptation des variables sociales:
lexemple des systemes sociaux des Macaques. Co/-
loques>~~A, 38, 92-100.
Tomasello, M., Davis-Dasilva, M., Camak, M. & Bard,
K. 1987. Observational learning of tool use by young
chimpanzees. Hum. Evol, 2, 175-183.
Tomasello. M.. Kruger. A. C. & Ratner. H. H. 1993.
Cultural learning. ?lehav. Brain Sri., 16, 495-552.
Visalberghi, E. 1990. Influences of aversive factors
on innovative behaviour in primates. In: Fete/
and Defense (Ed. by P. Brain, S. Parmigiani, R. J.
Blanchard & D. Mainardi), pp. 309-328. Chur:
Harwood Academic.
Visalberghi, E. & Fragaszy, D. M. 1990a. Do monkeys
ape? In: Language and Intelligence in Monkeys und
Apes (Ed. by S. Parker & K. Gibson), pp. 247-273.
Cambridge: Cambridge University Press.
Visalberghi, E. & Fragaszy, D. M. 1990b. Food-washing
behaviour in tufted capuchin monkeys, Cebus apclla,
and crabeating macaques, Macaca fasciculuris. Aninr.
Behav., 40, 829-836.
de Waal, F. B. M. & Luttrell, L. M. 1989. Towards
a comparative socioecology of the genus Maraca:
different dominance styles in rhesus and stumptail
monkeys. Am. J. Primifol., 19, 83-105.
Ward, P. & Zahavi, A. 1973. The importance of certain
assemblages of birds as information centres for food-
finding. Ibis, 115, 517-534.
Whiten. A. & Ham. R. 1992. On the nature and evol-
ution of imitationin the animal kingdom: reappraisal
of a century of research. Adv. Study B&v., 21,
239-283.