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International Journal of Primatology, Vol. 23, No. 3, June 2002 (°

C 2002)

Social Learning and Primate Reintroduction

D. M. Custance,1,3 A. Whiten,2 and T. Fredman2
Received July 6, 2000; accepted July 12, 2001

Research on social learning may be of use in the conservation of primates, es-

pecially great apes, through (a) promoting their public image, (b) identifying
specific adaptations, and (c) devising reintroduction training programs. We
surveyed all the instigated social learning studies in primates published since
1950 in order to assess their usefulness to devise reintroduction training pro-
grams. We identified 99 publications containing 130 data sets from 27 species
of primates. Great apes produced significantly more positive social learning
effects than either cercopithecines or cebids. There was also an enhanced social
learning effect when skilled demonstrators were used. Our survey indicates
that the scientific understanding of many aspects of primate social learning
relevant to conservation, including its function, learning spatial route plot-
ting, food and sleeping site location, predator avoidance and detection, and
the effect of model and tutee status, would benefit from greater research. Fu-
ture instigated studies on primate social learning would be most informative
for reintroduction if they included ecologically valid tasks presented to ≥2
similarly composed social groups, one of which functioned as a control, i.e.,
without being exposed to a model.
KEY WORDS: primate; reintroduction; social learning.

It seems ironic that as scientists strive to uncover the roots of human

culture by studying extant nonhuman primates (Kawamura, 1959; Nishida,
1987; Tomasello et al., 1993; Whiten et al., 1999), human technical and cul-
tural advances are largely responsible for driving most primate species to the
1 Department of Psychology, Goldsmiths College, University of London, Lewisham Way, New
Cross, London SE14 6NW, United Kingdom.
2 Scottish Primate Research Group, School of Psychology, University of St. Andrews, FIFE
KY16 9JU, Scotland, United Kingdom.
3 To whom correspondence should be addressed; e-mail: d.custance@gold.ac.uk.

479

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480 Custance, Whiten, and Fredman

brink of extinction. According to recent figures, many primate species will

not avoid imminent extinction without concerted conservation efforts. Of
the 158 species of primates surveyed by the International Union for Conser-
vation of Nature (I.U.C.N.) in 1996, 96 species were placed in the high-risk
categories of critically endangered, endangered and vulnerable, and a fur-
ther 40 were judged to be at risk: conservation dependent or near threatened.
Although these statistics are certainly gloomy, it is possible that social learn-
ing, both in terms of research on the subject and the primates’ own abilities,
could help. We aim to outline ways in which social learning could be useful
in the conservation of primates.

THE SCOPE AND SIGNIFICANCE OF SOCIAL LEARNING

Definitions of social learning have been the subject of fierce debate

(Galef, 1988; Whiten and Ham, 1992). We adopt Galef’s (1996, p. 8) opera-
tional definition of social learning, as instances in which the acquisition of
behavior by one animal is influenced by social interaction with others. Ac-
cordingly, social learning, is of particular interest because it underpins cul-
tural transmission. According to Whiten and Ham (1992), cultural transmis-
sion constitutes socially learned behavioral conformity that spreads through
a population. If such conformity then spreads across generations, it becomes
a cultural tradition.
According to Whiten and Ham (1992), there ≥7 social mechanisms ca-
pable of contributing to cultural transmission. Rather simple cognitive pro-
cesses underlie many of them. For example, stimulus enhancement involves
an animal learning a new behavior simply because it has its attention brought
to novel stimuli by the actions of a model. Other mechanisms are more com-
plex. Imitation involves an individual learning at least some part of the form
of a behavior as a direct result of observing a model (Whiten and Ham,
1992). Researchers have suggested that imitation, so defined, requires com-
plex cognitive operations like cross-modal, visual-tactile/kinaesthetic trans-
fer (Heyes, 1993; Mitchell, 1993). While many species may be capable of
the simpler forms of social learning, the most convincing evidence for imita-
tion in primates is from great apes (Heyes, 2001; Tomasello and Call, 1997;
Visalberghi and Fragaszy, 1990).

THE ROLE OF SOCIAL LEARNING

IN PRIMATE CONSERVATION

Social learning could be relevant for conservation in several ways. For

example, the complex social learning abilities of great apes could be used to
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Social Learning and Primate Reintroduction 481

promote the significance of primates to the public, thereby helping to raise

funds for conservation. In addition, if cultural traditions are characteristic
of some primate species, they may play important roles in their adaptations.
Evidence for cultural traditions in the manufacture and use of tools and in
techniques for obtaining foods supports this view (Byrne and Byrne, 1993;
McGrew, 1992). Social learning then assumes more than promotional signif-
icance: it may be essential to sustain critical knowledge and competencies
within primate communities. However, the most direct application of social
learning research to primate conservation appears to be as a method for skill
training in preparation for reintroduction. Accordingly, this is the focus of
our review.
Reintroduction is the attempt to establish captive-raised organisms in
an appropriate wild environment (Stanley-Price, 1991; Stuart, 1991). Sev-
eral projects have attempted to reintroduce captive-raised primates to the
wild (Brewer, 1978; Dietz et al., 1994; Gadsby et al., 1994; Galdikas, 1980;
Heltne, 1985). However, according to Beck et al. (1994), none of them has
been successful in meeting the criterion of Griffin et al. (1989); establishing
a fully self-sustaining population. Only the Golden Lion Tamarin Project
(GLTP) has shown a clear trend toward success. In 1997, 88% of the golden
lion tamarin population founded by reintroductees were wild-born. Survival
of wild-born individuals was at an average of 65% over all age classes.
After 13 years, the population of reintroduced monkeys had risen to 200
and there were 38 births in 1996 alone: “These trends suggest that the rein-
troduced population would continue to grow without further reintroductions
of captive-born animals” (GLTP Web-site, 1997).
An obvious requirement for successful reintroduction is that the sub-
jects survive long enough to breed and to found a self-sustaining population
(Sarrazin and Barbault, 1996). Shepherdson (1994) proposed that a period of
training or structured support could help to ensure survival on release. How-
ever, previous prerelease training programs have proved time-consuming
and expensive (Kleiman et al., 1991). In addition, it is not clear that they
have been of very much use (Beck, 1997). This is where social learning could
come into play. Box (1991) suggested that social learning might be an effi-
cient method of skill-training. In fact, Beck (1997) took this idea so seriously
that he suggested one could capture an already successfully reintroduced
tamarin and integrate it into a group of naı̈ve monkeys, in the expectation
that they might benefit from exposure to the experienced individual.
Beck’s (1997) proposal is exciting, but it is risky in that one could com-
promise the survival of an already successfully reintroduced monkey. In light
of the potential risks, one would only want to use social learning as a training
technique if one could be reasonably sure that it would be an efficient way in
which to promote survival skills. The presumed advantage of social learning
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482 Custance, Whiten, and Fredman

is that it increases speed and efficiency in the acquisition of certain biolog-

ically important behaviors (Visalberghi and Fragaszy, 1990). Although this
might seem a feasible hypothesis for the function of social learning, it has
still not been very widely or directly tested in primates (Galef, 1999).
Lefebvre (1995) is one of the few researchers to have analyzed the rates
of transmission in some of the presumed cultural traditions of primates.
He demonstrated that 16 of 21 data sets on feeding innovations fit curves
of accelerating learning rates: “Rapid and temporally accelerating rates of
learning are central to both evolutionary . . . and population . . . models of
cultural transmission” (Lefebvre, 1995, p. 228). Even though many of the
data sets exhibited accelerated learning, it does not automatically follow
that such patterns of social learning would convey an adaptive advantage
to reintroduced primates. Of particular concern is the fact that some of the
traditions spread very slowly. Potato washing, wheat washing and fish eat-
ing in the Japanese macaques of Koshima Islet took 8–10 years before they
yielded an accelerated function. However, the situation is more encourag-
ing for chimpanzees. Several of their cultural traditions yielded accelerated
functions within days or months. Mango-eating in the Mahale chimpanzees
showed an accelerated function within 60 s (Takasaki, 1983)!
Reports of spontaneous behavioral innovations in wild primates are
extremely important, but they are also relatively rare. Not only is there an
element of luck in witnessing such events but also researchers must possess
sufficient experience and skill to recognize their importance and to collect
appropriate data. One can supplement such field data by conducting studies
in which one deliberately introduces a target behavior into a group of pri-
mates in order to record the subsequent rate and pattern of acquisition. In
fact, researchers have conducted a relatively large number of deliberately
instigated studies of social learning.
Most instigated studies on social learning in primates were focussed on
mechanisms of transmission rather than on adaptive function (Galef, 1999).
Although identifying precise mechanisms of transmission is a legitimate sub-
ject of scientific investigation, in terms of devising reintroduction training
programs, there are more basic functional questions that one must address
first:
1. To what extent does learning in a social context promote efficient
behavioral acquisition in comparison to nonsocial (individual) learn-
ing? Under certain conditions, exposure to a novel task within a so-
cial group can actually inhibit acquisition (Giraldeau and Lefebvre,
1987).
2. Does introducing a skilled model to a naı̈ve primate group convey
an adaptive benefit? To answer this question, instigated studies must
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Social Learning and Primate Reintroduction 483

present target behaviors or tasks that convey survival or reproductive

benefits in the wild.
3. What kinds of target behavior are most likely to elicit a social learning
effect?
4. What are the best social contexts for promoting social learning: pairs,
small or large groups, peer groups, groups comprising of mixed ages,
sexes and ranks? The effect of dominance is an important, but rela-
tively neglected area of research in primate social learning. Drea and
Wallen (1999) found that low-status monkeys inhibited their perfor-
mance on a color discrimination task in the presence of dominants.
5. Which individuals constitute the best models, i.e., in terms of their
age, gender and rank?
6. What are the interspecific differences in rates and patterns of so-
cial learning? Studies that present similar tasks to different species
are particularly useful to assess interspecific differences (Cambefort,
1981).

INSTIGATED SOCIAL LEARNING STUDIES SINCE 1950

Obviously, no study can address all the issues listed above. Therefore,
we surveyed scientific literature to identify all the instigated social learning
studies in primates published since 1950, the era of modern methodological
sophistication. We assessed each study in terms of 6 factors:
1. Ecological validity: target behavior is ecologically valid if it was di-
rectly derived from behavior in wild conspecifics. Target behavior is
partially ecologically valid, if it was likely to be related to the be-
havior of wild individuals but was not directly derived from specific
observations. Target behavior is ecologically invalid if it bore very
little resemblance to the behavior of wild conspecifics.
2. We divided the living conditions of subjects into 3 categories: wild,
semiwild or captive. Semiwild subjects had become somewhat free-
ranging and partially self-sufficient after being released by humans
into a designated area.
3. We divided the social context in which participants observed a tar-
get behavior into 5 categories. Pair(D) indicates studies in which
researchers divided the subjects into observer-demonstrator pairs.
Pair indicates studies in which researchers divided the participants
into naı̈ve pairs. SG(D) indicated studies in which researchers placed
a knowledgeable demonstrator in a social group. SG indicated stud-
ies that presented tasks or problems to a social group that did not
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484 Custance, Whiten, and Fredman

contain a knowledgeable demonstrator. Human indicated studies in

which individual subjects watched a human demonstrator.
4. We noted, wherever possible, the age, sex and rank classification of
the demonstrators or innovators. The innovator was the individual
that first solved a problem set in a pair or social group that did not
already contain a trained demonstrator.
5. We recorded whether there was an individual learning control group.
If a study does not include an individual learning control condition,
it can be difficult to assess the benefits of using a skilled demonstra-
tor in terms of rates and likelihood of behavioral acquisition. We
also recorded whether the study used a within-participant control.
In within-participant designs, researchers present a target behavior
to subjects for a period before introducing a model. Via the control,
one can estimate the likelihood of a subject solving a problem or
performing a task without observing a model. Unfortunately, within-
participant designs preclude one from directly comparing individual
learning rates with social learning rates because subjects in the social
learning condition potentially benefit from prior individual exposure.
Nevertheless, if it seems very unlikely that an individual would have
learned a target behavior without access to a model, then one can
still conclude that a positive social learning effect has occurred.
6. We divided social learning effect into 5 categories: Yes(+) is when
there was evidence that the subjects performed a functionally rele-
vant behavior or solved a problem more quickly or efficiently after
exposure to a demonstrator versus individual learning. Sometimes
the acquired target behavior involved the inhibition of a response,
such as in snake avoidance. Yes is when social learning was evident,
but either there was no information about social versus individual ac-
quisition rates or the task was functionally irrelevant to the primate,
e.g., reproducing arbitrary gestures. No(−) is when the presence of
other individuals inhibited rates of acquisition. No is when no social
learning was discernible. ? is when the data did not allow an inde-
pendent judgement about the presence of social learning or rates of
acquisition.

We did not attempt to differentiate mechanisms of transmission. There

is much debate about how to define and to identify different social learning
mechanisms (Galef, 1988; Heyes, 1994; Whiten and Ham, 1992). These con-
siderations, together with the quantity of information in the papers surveyed
led us to conclude that such differentiation is beyond the scope of our review.
Our survey included 99 publications containing 130 data sets from
27 species of primates. We divided them into 7 behavioral categories: food
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Social Learning and Primate Reintroduction 485

selection, food location, food and water related manipulations, object related
manipulations, tool-use, predator or object avoidance, social behaviors, and
gestures. We summarized the information for each behavioral category in
7 tables, which are available on the Internet at <http://chimp.st-and.ac.uk/
cultures> along with a full bibliography; alternatively they are available from
D. M. Custance. Table I provides a summary of the information we collected.
Figure 1 displays the number of data sets and their associated social
learning effects in 6 taxonomic categories. The prosimians include 2 species
of lemurs and small-eared bush babies; the callitrichids include common mar-
mosets; the cebids are two species of capuchins, squirrel monkeys and dusky
titis; the atelids include 3 species of spider monkeys; and the cercopithecines
include 7 species of macaques, mandrills, vervets, and 3 subspecies of baboon.
We show great apes with their data (a) combined and (b) separated generi-
cally. The greatest number of data sets are from cebids, cercopithecines and
the great apes, especially Pan.
The data can be used to help answer whether learning in a social con-
text promotes the efficiency or likelihood of behavioral acquisition. Positive
social learning effects are revealed in 82.6% of great ape data sets, 56.8%
of cercopithecine data sets and 37% of cebid data sets. The remaining taxo-
nomic categories had too few data sets to justify comparisons. It is possible
that the number of positive social learning effects was elevated by the fact
that positive results are more often published than negative ones are. Never-
theless, Fig. 1 suggests that great apes may produce proportionally more pos-
itive social learning effects than the other taxa do.
A 2 × 3 Chi square test, comparing the number of positive social learn-
ing effects (Yes(+) and Yes) against the number of negative effects or no
effect (No(−) and No) in the cebids, cercopithecines and great apes, revealed
significant differences among the 3 groups (X 2 = 16.325, df = 2, p = .0003).
Post hoc tests revealed no significant difference between cebids and cerco-
pithecines (X 2 = 3.029, df = 1, p = .082), but there were significant differ-
ences between cebids and the great apes (X 2 = 16.644, df = 1, p < .0001)
and between cercopithecines and the great apes (X 2 = 7.453, df = 1, p =
.006). Therefore, the great apes produced significantly more positive social
learning effects, in comparison to negative effects or no effect, than either
the cebids or cercopithecines.
However, if one wishes to assess how effective social learning might
be as a reintroduction training technique, there is a potential problem with
combining the Yes(+) and Yes data. Yes(+) indicates that there is evidence
of accelerated learning rates versus individual learning, while Yes only indi-
cates that some form of social learning or influence is present, but with no
information about social versus individual acquisition rates. One would only
want to use social learning as part of a reintroduction training programme, if
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486

Table I. Summary of information from a survey of instigated studies on primate social learning
Behavioral No. of publications Taxonomic Ecologically Living Social Social
International Journal of Primatology [ijop]

category (no. of data sets) categories N valid N conditions N context N IL control N learning effect N

Food selection 13 (16) Callitrichids 2 No 0 Captive 12 Pairs(D) 4 Yes 8 Yes(+) 9

Cebids 5 Partially 15 Wild 5 SG(D) 4 Within-P 1 Yes 0
Atelids 1 Yes 2 SG 8 No 7 No(−) 0
Cercopithecines 9 No 8
? 1
Food location 9 (10) Prosimians 1 No 6 Captive 8 Pairs(D) 4 Yes 1 Yes(+) 5
Cebids 1 Partially 2 Wild 2 SG(D) 2 Within-P 5 Yes 2
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Cercopithecines 7 Yes 2 SG 4 No 4 No(−) 0

Great apes 1 No 3
? 0
Food related 16 (17) Prosimians 3 No 3 Captive 17 Pairs(D) 8 Yes 10 Yes(+) 6
manipulations Callitrichids 3 Partially 14 Wild 0 Pairs 1 Within-P 5 Yes 5
Cebids 3 Yes 0 SG(D) 1 No 3 No(−) 2
Cercopithecines 5 SG 3 No 3
Great apes 4 Human 5 ? 2
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Object related 16 (22) Atelids 3 No 17 Captive 22 Pairs(D) 3 Yes 1 Yes(+) 6

manipulations Cebids 5 Partially 3 Wild 0 Pairs 2 Within-P 11 Yes 8
Cercopithecines 2 Yes 2 SG(D) 0 No 10 No(−) 2
17:12

Great apes 14 SG 7 No 0
Human 10 ? 8
Tool-use 29 (37) Cebids 7 No 27 Captive 35 Pairs(D) 3 Yes 7 Yes(+) 8
Cercopithecines 7 Partially 5 Wild 3 Pairs 3 Within-P 11 Yes 12
Great apes 20 Yes 6 SG(D) 6 No 19 No(−) 4
SG 16 No 9
Custance, Whiten, and Fredman

Human 12 ? 6
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Predator and 10 (10) Cercopithecines 8 No 4 Captive 10 Pairs(D) 7 Yes 7 Yes(+) 9
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object Great apes 2 Partially 2 Wild 0 Pairs 0 Within-P 1 Yes 1

avoidance Yes 4 SG(D) 1 No 2 No(−) 0
SG 1 NA 1 No 0
Human 0 ? 0
Social 11 (13) Cebids 1 No 9 Captive 13 Pairs(D) 1 Yes 1 Yes(+) 0
behaviors Cercopithecines 4 Partially 1 Wild 0 Pairs 0 Within-P 8 Yes 8
and gestures Great apes 8 Yes 1 SG(D) 1 No 2 No(−) 0
SG 1 No 4
Human 8 ? 0
International Journal of Primatology [ijop]

Note. A full study-by-study database is available in 7 tables at <http://chimp.st-and.ac.uk/cultures> or from D. M. Custance N = number of data
sets. SG = social group without a demonstrator, SG(D) = social group with a demonstrator, Pairs = pairs without a demonstrator, Pairs (D) =
observer–demonstrator pair, Human = a human acted as demonstrator. IL control = individual learning control, Within-P = within participants
design. Yes(+) = the participants performed a functionally relevant behavior or solved a problem more quickly or efficiently after exposure
to a demonstrator compared to individual learning. Yes = social learning was evident, but either there was no information about social versus
individual acquisition rates or the task was functionally irrelevant to the primate (e.g., reproducing arbitrary gestures). No(−) = the presence of
Social Learning and Primate Reintroduction

other individuals inhibited rates of acquisition. No = no social learning discernible. ? = the data did not allow an independent judgement about
the presence of social learning or rates of acquisition.
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488 Custance, Whiten, and Fredman

Fig. 1. The number of data sets within 9 taxonomic categories and related social learning
effects (great ape data shown combined and also separately at the level of the genera).
Yes(+), Yes, No(−), No, and ? (Table I).

one had evidence to suggest that it increases the efficiency with which poten-
tial reintroductees acquire functionally important behaviors. Since the Yes
category provides no information that pertains to efficiency of acquisition,
these data were excluded from the next set of analyses.
When we compared cebids, cercopithecines and great apes in terms
of the number of positive versus no or negative social learning effects, but
excluding the Yes data, a significant main effect remains (2 × 3 Chi square:
X 2 = 9.6, df = 2, p = .008). Figure 1 indicates that cebids produced more
negative social learning effects (No(−) and No) than positive ones (Yes(+)),
while the cercopithecines produced roughly equal numbers of positive and
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Social Learning and Primate Reintroduction 489

negative effects and the great apes produced more positive than negative
effects. The difference between the cebids and cercopithecines approached
on significance (X 2 = 3.8, df = 1, p = .051) with the cebids producing less
positive results in comparison to negative ones than the cercopithecines
did. There is a significant difference between the cebids and the great apes
(X 2 = 9.37, df = 1, p < .002), but not between the cercopithecines and the
great apes (X 2 = 2.67, df = 1, p = .103). Therefore, the great apes produced
significantly more accelerated social learning effects versus negative or no
effect when compared to cebids, but not to cercopithecines.
The degree to which a positive social learning effect is produced
may depend upon whether the task or problem presented to the partici-
pants is ecologically valid or not. Figure 2 shows the percentage of data
sets that were deemed ecologically valid, partially valid, and invalid to-
gether with their associated social learning effects (excluding ‘?’). There
were relatively few ecologically valid tasks. However, even the tasks deemed
not or partially ecologically valid produced a reasonably high proportion
of positive social learning effects. A 2 × 3 Chi square test comparing the
3 categories of ecological validity in terms of whether there was a positive
social learning effect (Yes(+)) versus a negative or no effect (No(−) and
No) showed no significant difference (X 2 = 3.52, df = 2, p = .172). There-
fore, we did not exclude data from ecologically invalid tasks from further
analyses.
It is still important to evaluate whether any particular kind of tar-
get behavior elicits a positive social learning effect and in which species.
Figure 3 shows the number of data sets for 9 categories of behavior. They
are partly based upon those suggested by Box (1991) as being important
skills for primate reintroductees to learn if they are to survive in the wild.
One of the categories, object manipulation, had the least obvious rele-
vance to behaviors needed for survival in the wild, except in relation to
nest-building, which we show separately. Many of the object manipula-
tion tasks had no obvious functional relevance for the primate participants,
e.g., Mignault (1985) presented chimpanzees with the task of putting a
diaper on a doll. Figure 3 indicates that all of the behavioral categories,
except for food selection and tool use, had slightly more positive social
learning effects than negative or no effect. Interestingly, the category of
predator avoidance, in which nonlearning in the wild would be critical,
is the one category to produce only positive (Yes(+) and Yes) effects.
However, a 2 × 8 Chi square, excluding spatial route plotting since there
were no data sets pertaining to this category, yielded no significant dif-
ference among the behavioral categories in terms of positive (Yes(+))
versus negative or no (No(−) and No) social learning effect (X 2 = 8.03,
df = 7, p = .154).
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490 Custance, Whiten, and Fredman

Fig. 2. The percentage of data sets within 3 categories of ecological validity and the related
social learning effects. Yes(+), Yes, No(−), No, and ? (Table I).

Figure 3 shows that there were almost twice as many data sets relating
to tool-use than any other behavioral category. This is remarkable given that
chimpanzees are the only species of nonhuman primate known to use tools
habitually in the wild, other than orangutans (Van Schaik et al., 1996) and
capuchins (Boinski, 2001)). One might expect to find more positive social
learning effects for chimpanzees in tool tasks than for any other species. As
predicted, Pan troglodytes versus all other species on tool tasks produced
significantly more positive social learning effects (Yes(+)) versus negative
or no effect (No(−) or No): Fisher’s exact test, p = .018.
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Social Learning and Primate Reintroduction 491

Fig. 3. The number of data sets within 9 behavioral categories and the related social learning
effects. FS = food selection, FL = food location, FM = Food related object manipulation,
Tool = tool-use task, OM = object manipulation (with no associated food reward), Route =
spatial route plotting, Predator = predator detection and avoidance, Nest = nest building,
Social = social behaviors, e.g., gestural communication or parenting behaviors. Yes(+), Yes,
No(−), No, and ? (Table I).

Irrespective of species or taxonomic category, does the presence of a

skilled demonstrator enhance the chances of producing a positive social
learning effect? Figure 4 shows the number of data sets with or without
a demonstrator and the associated positive (Yes(+)) versus negative or no
(No(−) and No) social learning effect. Apparently, a demonstrator increases
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492 Custance, Whiten, and Fredman

Fig. 4. The number of data sets within 4 social contexts and the related social learning effects.
SG = social group without a demonstrator, SG(D) = social group with a demonstrator, Pair =
2 naı̈ve participants, Pair(D) = observer–demonstrator pair. Yes(+), Yes, No(−), No, and ?
(Table I).

the likelihood of producing a positive social learning effect. A 2 × 2 Chi

square revealed significantly more positive social learning effects in the data
sets with a demonstrator compared to those without one (X 2 = 6.37, df =
1, p = .012).
The composition of the social groups also had a significant effect (Fig. 4).
We used a 2 × 3 Chi square test to compare social groups without a
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Social Learning and Primate Reintroduction 493

demonstrator (SG), social groups with a demonstrator (SG(D)), and

observer–demonstrator pairs (Pair(D)), There were only 5 data sets made
up of pairs without a demonstrator, hence they could not be included. There
is a significant difference in the number of positive (Yes(+)) versus negative
or no (No(−) and No) social learning effect (X 2 = 10.6, df = 2, p = .005).
A 2 × 2 post hoc test showed that there is no significant difference between
SG and SG(D) (X 2 = 2.64, df = 1, p = .104). However, the result was in
the predicted direction with SG(D) producing proportionally more positive
social learning effects than SG. There is no significant different between
SG(D) and Pair(D) (X 2 = .692, df = 1, p = .406). In contrast, there is a sig-
nificant difference between SG and Pair(D) (X 2 = 10.4, df = 1, p = .001).
Compared to SG, Pair(D) produced proportionally more positive social
learning effects versus negative or no effect.
The present results suggest that one can gain enhanced social learning
effects by presenting primates, either in pairs or possibly in a social group,
with a knowledgeable demonstrator. An important related question is, which
individuals constitute the best demonstrators? Forty-four of the data sets
contained information on the demonstrators or innovators. In 24 sets of
data, there was more than one demonstrator or innovator of mixed rank,
age and sex. Therefore, it was difficult to assess the comparative strengths of
one category of demonstrator or innovator over another. In the remaining
20 data sets, there were too few cases in each age and sex category to assess
the relative effectiveness of one category over another. Only 7 data sets
included the dominance rank of the demonstrator or innovator.
Direct interspecific comparisons of social learning are important in
terms of establishing differences in mechanisms, rates and patterns of trans-
mission. Eighteen of the surveyed publications, involving 11 different tasks,
compared the social learning of 2–5 species on the same task. Six of the
11 tasks were designed principally to compare specific differences in mech-
anisms of transmission. Four of the tasks (Cambefort (experiment 2) 1981;
Fairbanks, 1975; Visalberghi and Fragaszy, 1990; Westergaard, 1988) com-
pared interspecific differences in rates of acquisition. Only Cambefort
(experiment 1, 1981) compared both the rates and patterns of cultural trans-
mission exhibited by two species—(vervets and Chacma baboons)—when
presented with the same task.

DISCUSSION

We conclude that published studies of social learning provide rather

limited information for devising primate reintroduction training programs.
This is partly because they were focused on mechanism instead of function.
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494 Custance, Whiten, and Fredman

A large number of positive social learning effects came from tasks that did
not measure rates of acquisition on functionally relevant tasks, i.e., ones with
a Yes versus a Yes(+) designation (Fig. 1). Even in tasks that did measure
rates of acquisition, it was often difficult to assess the biological relevance of
the advantage gained by social learning. Only a small proportion of the data
sets involved tasks that were based directly on behaviors that are performed
by conspecifics in the wild (Fig. 2). In addition, only one study (Hannah
and Brotman, 1990) could measure effects at the level of survival of infants.
However, they found no difference in subsequent mothering behavior and
infant survival when they compared female chimpanzees given an infant to
foster versus ones housed with skilled lactating mothers and their infants,
but without an infant to foster themselves.
There is no social learning study involving pithecids, colobines or lesser
apes and in prosimians, callitrichids and atelids there is not enough data to
form a general conclusion about their social learning abilities (Fig. 1). In
the cebids and cercopithecines, there were almost equal numbers of positive
versus negative or no social learning effects. However, the great apes showed
an elevated positive social learning effect; thus, it is likely that they would
benefit from the use of social learning in a skill-training program though,
more social learning studies are needed, particularly on gorillas.
There are few studies that directly compared social learning in different
species of primates on the same task. Many of them had rather ecologically
invalid tasks or focussed on mechanisms of transmission rather than function.
Only 4 studies include comparative rates of behavioral acquisition, and only
Cambefort (1981) recorded both the rates and patterns of acquisition in
2 species of primates on the same task. We need more studies like it.
There is no study on the social learning of spatial route plotting in pri-
mates (Fig. 3). There are only 3 studies on the social learning of nest building
and no study on social learning of sleeping site location. Many of the studies
on the social learning of food location in primates present rather artificial
tasks (Darby and Riopelle, 1959; Feldman and Klopfer, 1972). Figure 3 also
indicated that all of the studies on predator detection and avoidance yielded
positive social learning effects. However, most of these studies focused on
snake avoidance. We found no social learning studies in primates on the ac-
quisition of feline or raptor fear, although these are often important primate
predators.
There are few studies in which a skilled demonstrator was introduced
to a wider social group (Fig. 4). Although studies that use observer–demons-
trator pairs are informative about social learning, training procedures based
on separating group members into pairs are often inappropriate for rein-
troduction for practical reasons. For many species, it is difficult and time-
consuming to habituate group members to being separated into pairs. In
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Social Learning and Primate Reintroduction 495

addition, separating primates from a group formed for reintroduction could

disrupt social relations and hence prove counter-productive. Therefore, stud-
ies that present target behaviors to naturally composed social groups, rather
than artificially formed pairs, could provide important information for de-
vising primate reintroduction training programs. SG(D)), studies are most
informative when they incorporate an individual learning control condition,
which allows one to assess the benefits of providing a skilled demonstrator
versus leaving a naı̈ve group to solve a task for themselves. However, only
one study in the survey (Voelkl and Huber, 2000) presented a partially eco-
logically valid task to 2 similarly composed social groups, in which one but
not the other was exposed to a knowledgeable demonstrator.
The survey provided little useful information on which individual would
make the best model or demonstrator in terms of age, sex and rank. Many
publications failed to provide even the most basic details on the identity or
status of the model used. The identity of the most effective demonstrator will
partly depend on the social organization of the species. Social dynamics have
an important effect on social learning (Coussi-Korbel and Fragaszy, 1995)
and the interpersonal relationship between observer and demonstrator is im-
portant (Russon and Galdikas, 1995; Wechkin, 1970). Cambefort’s findings
(experiment 1, 1981) suggest that different species prefer different models.
Huffman (1996) pointed out that there may be different transmission routes
for different behaviors; and one may suppose that juveniles and adolescents
target different models than infants do (Russon and Galdikas, 1995). Hence,
the effect of model status—age, rank and sex—on social learning constitutes
a potentially fruitful area for future research.
We are also left with the issue of which individuals would make the best
tutees in a social learning reintroduction training program. The GLTP offers
perhaps the best insight regarding the appropriate status of tutees. Among
the reintroduced golden lion tamarins, juveniles achieved better survival
rates than adults did. On release, younger monkeys displayed greater be-
havioral flexibility and adaptability (Beck, 1997; Kleiman et al., 1991). Simi-
larly, in wild and semiwild Japanese macaques, juveniles were most often the
first to discover novel behavior patterns and first to learn them by observing
or accompanying others (Kawai, 1965; Suzuki, 1965). Hence, it would seem
best to use juvenile tutees.

A SPECIFIC RECOMMENDATION FOR FUTURE RESEARCH

As long as primatologists focus more on mechanisms of transmission

than on function, social learning research will continue to provide limited
salient information for reintroduction. However, it might be possible to de-
vise procedures that address both mechanism and function.
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496 Custance, Whiten, and Fredman

An increasingly preferred procedure to study mechanisms of transmis-

sion is Dawson and Foss’ (1968) alternative morphs technique. Two separate
groups of participants are shown alternative methods to manipulate the same
object. Because both groups have their attention brought to the same envi-
ronmental locus, stimulus enhancement is equated. The important measure
is whether the subjects will reproduce at least some part of the behavioral
form shown to them more than the alternative. For example, we have tested
several different species of primates via an alternative morphs artificial fruit
(Caldwell and Whiten, 1999; Custance et al., 1999, in press; Stoinski et al.,
in press; Whiten et al., 1996). The top of the fruit was held shut by two rods
wedged across it. The subjects were in two groups: one group saw the rods
being twisted out while the other saw them being poked out. We then mea-
sured whether the participants that saw poke would poke more than twist
and vice versa.
We propose that an alternative morphs task, like the artificial fruit one,
could be combined with a Cambefort-like (1981) procedure, and that the
resultant data sets could be further analyzed by testing to see whether they
fit Lefebvre’s (1995) curves of accelerated function. With enough subjects,
one could present a 2-action task to 3 similarly composed social groups. One
could train a member of group A to model poke, a member of group B
to model twist, and group C could be left to solve the task for themselves
without a model. Such a design incorporates a partially ecologically valid task
that not only tests for imitative learning but also allows one to evaluate the
effect that a knowledgeable model has on rates and patterns of behavioral
acquisition in a social group.
In summary, there seem to be many areas for potentially fruitful re-
search in primate social learning: function, food location, spatial route plot-
ting, predator detection, and model and tutee status, to mention just a few.
Increased empirical investigations into these areas will not only greatly ben-
efit our scientific understanding of primate social learning but also could
be useful when devising primate reintroduction training programs. Both
science and conservation will benefit, if future instigated studies use ecolog-
ically valid tasks presented to ≥2 similarly composed social groups, one of
which functions as a control, i.e., without being exposed to a model.

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