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Journal of Comparative Psychology Copyright 1997 by the American Psychological Association, Inc.

1997, Vol. 111, No. 4, 370-378 0735-7036/97/$3.00
Food Transfers Through Mesh in Brown Capuchins
Fr a n s B. M. d e Wa a l
Emory University
Capuchin monkeys (Cebus apella) share food even if their partner is behind a mesh restraint.
Pairs of adult capuchins were moved into a test chamber in which 1 monkey received
cucumber pieces for 20 rain and the other received apple slices during the following 20 min.
Tolerant transfers of food occurred reciprocally among females: The rate of transfer from
Female B to A in the second test phase varied with the rate from Female A to B in the first test
phase. Several social mechanisms may explain this reciprocity. Whereas this study does not
contradict cognitively complex explanations (e.g., mental record keeping of given and
received food), the results are consistent with a rather simple explanation: that food sharing
reflects a combination of affiliative tendency and high tolerance. The study suggests that
sharing mechanisms may be different for adult male capuchins, with males sharing food more
readily and less discriminatingly than females.
In a classical study, Nissen and Crawford (1932) pre-
sented juvenile chimpanzees (Pan troglodytes) with the
opportunity to share valuable items, such as food, through
bars. Bars prevent the dominant of a pair from acquiring the
other' s possessions through force or intimidation. Interindi-
vidual transfers under this condition must, therefore, be of a
partly voluntary nature. Some of the chimpanzees in Nissen
and Crawford' s tests did indeed share.
Evidence for spontaneous food .sharing in chimpanzees
has been mounting ever since, both in the field (e.g., Boesch
& Beesch, 1989; Goodall, 1963; Teleki, 1973) and in
captivity (e.g., de Waal, 1989; Silk, 1979). Similar behavior
has been reported for the chimpanzee' s closest relative, the
bonobo (Pan paniscus; de Waal, 1992; Hohmann & Fruth,
1993; Kuroda, 1984). Some of these studies support the
suggestion of Nissen and Crawford (1932, p. 415) that "i t is
entirely possible that this sharing was, essentially, barter on
a ' credit' or deferred basis. " Thus, de Waal' s (1989) data on
plant food sharing in a large captive colony of chimpanzees
are consistent with the hypothesis that tolerance in relation
to food evolved, at least in part, as a form of reciprocal
altruism (see Trivers, 1971).
Apart from sharing between mother and offspring, chim-
panzees frequently share among unrelated adults, mainly
among males and between males and females. These sharing
tendencies may have evolved in the context of cooperative
The research was made possible by support from the National
Science Foundation (IBN-9321195) and by a grant from the
National Institutes of Health to the Yerkes Regional Primate
Research Center, Emory University (RR-00165). The Yerkes
Primate Center is fully accredited by the American Association for
Accreditation of Laboratory Animal Care.
I am grateful to Lisa Parr as well as Peter Verbeek, Shannon
Varner, and Allison Davis for assistance with the experiments,
observations, and data administration.
Correspondence concerning this article should be addressed to
Frans B. M. de Waal, Living Links Center, Yerkes Primate Center,
Emory University, Atlanta, Georgia 30329. Electronic mail may be
sent to dewaal@emory.edu.
hunting: For one individual to assist another with the capture
of prey, there may need to be a reward at the end. Indeed,
Boesch' s (1994) field data suggest that male chimpanzees
that participate in a hunt are more likely to receive meat
from the possessor of the carcass than male chimpanzees,
regardless of rank, who fall to contribute to the hunt but are
attracted to its product. Cooperative acquisition of high-
energy, concentrated food is rather unique in the primate
order. Perhaps as a result, few primate species regularly
share food outside the mother-offspring context (Feistner &
McGrew, 1989).
Members of the genus Cebus differ from most other
monkeys and resemble chimpanzees and bonobos by a high
degree of food-related tolerance. Not only is there a high
level of tolerance by adult capuchins toward immature
individuals (Fragaszy, Feuerstein, & Mitra, 1997; Janson,
1986, 1988), but the adults also share among themselves: In
captive studies, both edible and inedible objects are ex-
changed peaceably without the usual dyadic asymmetries of
dominance and subordination (de Waal, Luttrell, & Canfield,
1993; Thierry, Wunderlich, & Gueth, 1989).
Capuchin monkeys are specialized in the exploitation of
both plant and animal foods of high energetic value, which
they achieve through strength, skill, and the destruction of
palm fronds (Freese & Oppenheimer, 1981; Izawa, 1978,
1990; Izawa & Muzino, 1977). Perry and Rose (1994)
confirmed earlier reports by Newcomer and deFarcy (1985)
and Fedigan (1990) that wild Cebus capucinus capture coati
pups (Nasua narica). They observed monkeys beg for and
share the meat of pups. I f present during the raid, coati
mothers formidable adversaries for a capuchin-sized mon-
key- - def end their offspring. Cooperation among the mon-
keys could conceivably increase capture success, as also
suggested for hunts on squirrels (Sciurus variegatoides)
documented in the same capuchins by Rose (in press). Even
though it is as yet unclear how comparable these situations
are with the cooperative hunt of chimpanzees, the possibility
exists of a convergent evolutionary basis for food sharing in
capuchins and chimpanzees (Rose, in press).
370
CAPUCHIN FOOD SHARING 371
The present study t ook as its starting point the observation
that brown or tufted capuchin monkeys (Cebus apeUa)
readily share food when pl aced in adjacent cages separated
by a mesh restraint similar to the experi ment with chimpan-
zees by Nissen and Crawford (1932). In the first study of this
kind, a bowl with fresh grapes was pl aced in one subj ect ' s
cage well out of reach of the other subject. Food transfers
were observed at least once in every test, occasionally
involving active giving; that is, the possessor wal ked up to
the mesh partition and pushed food to the other side. The
large majority of food transfers, however, fol l owed passive
patterns (de Waal et al., 1993).
Possessors could easily monopol i ze food by staying away
from the mesh partition or by at least keeping the food away
f r om it. It was significant, therefore, that they failed to do so.
This observation, confu' med by hundreds of subsequent
tests, together with the virtual absence of aggressive behav-
ior during and following tests, makes me reject the sharing-
under-pressure hypothesis or tolerated theft hypothesis,
according to which sharing is a f or m of appeasement of
potentially hostile beggars (Blurton Jones, 1987). The
following alternative explanations of food sharing in the
mesh paradi gm will be considered, listed here from the
simplest to the cognitively most demandi ng hypothesis:
1. Disinterest: The monkeys are not interested in what
happens to their food. The part ner' s access to it is a
by-product of the tendency of food possessors to carry food
around, scatter it, and eat it near the partition.
2. Affiliation and tolerance: The monkeys do take the
partner into account, bot h by avoiding certain partners and
by being attracted to others. Food transfers are the product of
a combination of affiliation with and tolerance of particular
partners.
3. Deliberate but unconditional sharing: The monkeys
purposel y bring food to particular partners and share with
them, but they do so unconditionally. That is, the sharing is
part of l ong-t erm relationships not determined by recent
interaction.
4. Calculated reciprocity: The monkeys keep track of
gi ven and recei ved favors, maki ng food sharing contingent
on the recent receipt of food from the same partner or the
receipt of other social "currenci es" (see Seyfarth & Cheney,
198g).
Even i f food sharing were found to be reciprocally
distributed, this result could come about in multiple ways.
The affiliation and tolerance mechani sm (Hypothesis 2
above), for example, would automatically lead to reciprocal
sharing provi ded attraction bet ween individuals is mutual.
This possible mechani s m was dubbed symmet ry-based
reciprocity in relation to reciprocal food sharing and alliance
format i on in chimpanzees. It failed to explain the observed
reciprocity in this species, however, because reciprocity
correlations persisted after correction for dyadic affiliation
rates (de Waal, 1989; de Waal & Luttrell, 1988). Further-
more, chimpanzees show partner-specific sequences of recip-
rocal exchange of services, a result unexplained by mere
symmet ry ( de Waal, 1997). With regards to capuchin
monkeys, on the other hand- - and also other animals show-
ing reciprocal exchange (e.g., vampi re bats, Desmodus
rotundus, Wilkinson, 1984; impala, Aepyceros melampus,
Hart & Hart, 1992)---symmetry-based reciprocity remains a
likely mechani sm.
Here, I report experiments on the same brown capuchins
as used by de Waal et al. (1993) but this t i me tested more
systematically and in greater detail. The mai n purpose of this
first round of testing was to determine whether Hypot heses 1
and 2 mi ght be sufficient to explain the monkeys' behavior.
Me t hod
Subjects
The Yerkes capuchin colony consisted of two separate social
groups of Cebus apella. Each group included 2 adult males and 4 or
5 adult females, totaling 13 adult subjects. All 11 offspring in the
groups were infants or early juveniles except for 1 male who was
3.5 years old at the beginning of the study. Seven adult females had
1 offspring, and 2 adult females had 2 offspring at the onset of
study.
Because most of the monkeys were of unknown background, the
Therion Corporation (Troy, NY) conducted DNA profile analyses
on blood samples of all 13 adults as well as 5 juveniles burn into the
colony. One adult male, on breeding loan from the University of
Georgia, was known to be unrelated to all other adults. Two
probe--enzyme combinations (OPT-02/Hae III and OPT-05/Hae III)
were used to assay the genomes. By combining the two indepen-
dent probes, an average of 38 genetic markers were assayed per
individual. The mean (--+ SD) band-sharing coefficient (BSC) of 6
known kinship relations (mother--offspring and sibling pairs) was
0.762 - 0.059. For 10 possible or likely kinship relations (i.e.,
alpha males with immatures conceived during their tenure as well
as relations among age-peer immatures in the same group), the
mean BSC was 0.640 + 0.092. The BSC for the above two
categories combined was significantly higher than that for relations
among the 12 adult monkeys of unknown background (i.e.,
0.544 -4- 0.075), t(80) = 6.36, p = .0001. On the basis of these
results, and the even lower DNA similarity among known nonkin
(i.e., relations with the unrelated breeding male), a BSC above 0.6
was taken to indicate potential kinship and a BSC above 0.7 to
indicate likely kinship. Accordingly, of the 36 pairs of adult
monkeys housed in the same group, only 1 pair was likely to be
related, whereas 2 pairs were potentially related. Kinship was
subsequently ignored in the data analysis.
Housi ng
The capuchin facility offered indoor/outdoor housing for two
monkey groups with a total of 25 m2of floor space for one group
and 31 m 2 for the other. No~a~aUy, the monkeys had free access to
the entire space. Visual contact between the groups was controlled
by an opaque screon. The facility included a separate office with
windows through which researchers could monitor the monkey
area. During pair testing, however, the experimenter followed the
monkeys' behavior on a TV screen set up in this area.
Each of the two monkey pens was partitioned into three sections
by means of one chain-link partition and one opaque partition (i.e.,
the outer wall). There were interconnecting doors between adjacent
sections. Between the two distant sections ran a tunnel. The floors,
made out of concrete, were covered with sawdust indoors but were
uncovered outdoors. The monkeys received ad libitum water and
monkey chow and a daily tray with bread, fruits, and vegetables in
the late afternoon after testing has been concluded.
372 DE WAAL
Experi ment al Procedures
A mobile test chamber made of vinyl-coated mesh was attached
to the front of a group's indoor pen. The test chamber was divided
by inserting a partition, providing each subject in a pair test with a
72 × 60 × 60-cm space. Bowls could be attached to the outside of
the chamber on either side, well out of reach of the monkey on the
other side (see Figure 1). The back of the test chamber was opaque
to prevent visual contact between test subjects and group mates.
Monkeys entered the chamber either directly from the pen or from
a transport box. The separation procedure took approximately 10
min, after which the monkeys were allowed to habituate to the test
chamber for 10 min. Following this, the experimenter brought
food, turned on a video camera, and left the animal area. Video
registration on Super-VHS covered the behavior of both subjects
along with a time display in tenths of seconds.
The main experimental series was a delayed exchange test
(DET) in both directions on all dyads among adult group mates (72
DETs). In each DET, Monkey A received cucumber pieces for 20
rain after which the bowl was removed. The bowl was then filled
with apple pieces and given to Monkey B for 20 min. During the
next DET on the same pair of subjects, the order between Monkeys
A and B was reversed.
Randomly selected pairs of adult group mates were subjected to
the same test but with the food order changed to first apple and then
cucumber (19 reversed DETs). Furthermore, each adult monkey
was tested individually, without a partner in the test chamber, with
either cucumber or apple in a 20-min control test (26 tests). Finally,
each adult was given a choice of either a piece of apple or a piece of
cucumber. The experimenter held the different foods in different
hands, showing the food to the subject (making sure the subject
noticed the contents of both hands), before moving the hands to
within reach of the subject. Then the subject was permitted to take
food from either hand. These food preference tests (FPTs) were
given on three separate occasions to each monkey (39 tests).
Tests were conducted in the morning and early afternoons when
the monkeys had not yet received any fruits and vegetables. No
subject was tested more than once per day. Transcription of the
videotaped tests was very detailed. Every 30 s the location of
subjects in relation to the partition and the partner was recorded by
dividing each individual section in three equal parts (Distance 1 =
close to the mesh partition; Distance 2 = intermediate distance, and
Distance 3 = at the far end of the test chamber, away from the
partner). Following de Waal et al. (1993), food interactions were
divided into the following types:
Cheek-to-cheek: cheek-to-cheek begging or other close inspec-
tion of the possessor's food without attempting to take it.
Hand-cup: holding a hand under the mouth of the possessor as a
begging gesture or in an attempt to collect dropping pieces.
Collect-distant: collection or attempted collection, through the
mesh partition, of food that is out of the possessor's arm's reach or
behind the possessor's back.
Collect-near: one individual waits for discarded pieces, collect-
ing or trying to collect them from within the possessor's reach.
Drop-inside: dropping or leaving a major piece of food within
reach of the other on the possessor's side regardless of actual food
transfer.
Drop-through: possessor appears to deliberately drop, push, or
throw food in front of the other thereby working it through the
mesh partition.
Accidental drop-through: food is dropped through the mesh
partition, but as the result of messy food consumption or food
dumping by the actor.
Food giving: possessor gives or pushes food with its hands or
mouth to the other in a way that seems directed at the other.
Forced claim: taking food out of the other's hands or mouth
despite resistance.
Unsuccessful forceful attempt: grabbing at the possessor's food
or threatening the possessor.
Relaxed claim: re, aching through the mesh, in full view of the
possessor, while removing some or all food directly from the
possessor's hands or mouth in a relaxed manner without aggression
or use of force.
Unsuccessful relaxed claim: unsuccessful reaching for food held
by the possessor.
In the present analysis, measures include the total frequency of
food transfer (number of times the nonpossessor collects or
receives food from the possessor's side) and the number of tolerant
food transfers (same as before, but excluding collect-distant). The
ethogram further included measures of social interaction (e.g.,
grooming, play, aggression) and vocal exchange (e.g., repeat
hoots).
Figure 1. Schematic drawing of the pair-test setup. One subject at
a time receives food from a bowl attached to the outside of the
chamber. A mesh partition divides the test chamber, preventing
direct access to the food by the other subject. In a rare instance of
active sharing, a male (right) hands a piece of food to a female who
reaches through the mesh to accept it. Both subjects visually
monitor the transfer. This drawing (by the author) was made from
an actual video still.
Social Relationships
Global observation sessions lasted 30 min and covered the social
activity of an entire group. The ethogram included 72 entry types
concerning agortistic behavior of various intensifies, interactions
over food, sexual contacts and invitations, the frequency and
duration of allogrooming, proximity relations, approach-with-
drawal, intergroup vocal exchange, play, and so on. Duration
behaviors, such as proximity, were collected with a 5-rain point-
sampling procedure; other behaviors were recorded on an all-
occurrences basis. Observations were spoken into a tape recorder
and entered into a computer file on the same day codified as
time/actor/behavior/recipient.
Since the establishment of the colony in 1989, approximately
three global observations have been conducted per group per week.
The computerized database provides background information on
dominance relations, affiliation patterns, grooming, and reproduc-
tive behavior. The present analysis was limited to the records of an
18-month period during which the food experiments were con-
ducted. The dominance order and social relationships appeared
stable throughout this period.
CAPUCHIN F O O D SHARING 373
Statistics
Nonparametric statistics have been applied whenever possible
by comparing data per subject. That is, behavior per subject across
tests of the same type (but with different partners) was averaged
and compared in a matched design (Wilcoxon signed paired ranks
test) with behavior of the same subject in tests of a different type.
Several data manipulations, such as multiple correlations and
multivariate analyses, required parametric statistics, however.
Resul t s
Behavi oral Descri pt i on
By pooling the records on the entire round of testing,
combining both DETs and reversed DETs, I analyzed the
characteristics of 9,896 interactions over food. Table 1
summarizes the results. Interactions not resulting in an
actual food transfer constituted 43% of the sample. These
interactions mostly concerned expressions of interest in the
ot her' s food by means of repeat hoots, cupping of a hand
under the possessor' s chin, or staring closely at food held by
the other. There was also a substantial number of drop-
throughs, drop-insides, and attempts to collect food that did
not result in an actual transfer.
Food transfers from the possessor' s to the partner' s side
consisted mainly of collect-distant and collect-near and a
much smaller proportion (0.9 %) of direct taking by means
of a relaxed claim or hand-cup. In 5% of the transfers,
possessors played a facilitating role by manipulating food on
the mesh partition, eating sloppily near the mesh, or bringing
a major piece, often without having tasted from it, to the
partition to drop it there on their own side leaving it within
the ot her' s reach. Only in 0.3% of all transfers did food
directly change hands or was pushed through the mesh to the
waiting recipient in an apparently intentional manner (drop-
through and food giving; see Table 1).
Negative responses by food possessors occurred in 4% of
the interactions over food. The majority of these responses
Table 1
Food-Related Behavioral Frequencies Separately
f or Interactions Near the Mesh Partition That Led
to a Food Transfer and Those That Did Not
Food transfer
Food interaction No Yes
Cheek-to-cheek begging 66 0
Hand-cup 45 9
Collect-distant 437 2,241
Collect-near 490 3,061
Drop-inside 297 224
Drop-through 27 14
Accidental drop-through 22 7
Food giving 56 4
Forced claim 0 25
Unsuccessful forceful attempt 66 0
Relaxed claim 0 43
Unsuccessful relaxed claim 83 0
Note. Results are pooled for all tests.
consisted of turning away, jumping back, pulling the food
away, or slapping the partner. Overtly agonistic behavior,
such as threats, lunges, or screams, occurred in only 0.3 % of
all food interactions. Similarly, attempts at forcibly taking
food were rare even in the most dominant subjects and
remained mostly unsuccessful: 0.9 % of all food interactions
(forced claim and unsuccessful forceful attempt; see Table 1).
Food Preference
Twelve of the 13 adult monkeys chose apple more often
than cucumber in the food preference tests (binomial t e s t :
p < .01, two-tailed). Apple was selected 67% of the time in
the 39 FPTs.
Rat e of Food Transfer
The mean number of food transfers was calculated for
each individual possessor with male (M) and female (F)
partners. These means were subjected to a repeated measure
analysis of variance (ANOVA) comparing the rate of food
transfers in M-M, F-F, M-F, and F-M directions. In the first
phase of the DETs, the sex of the possessor made a
significant difference, F(1, 11) = 4.98, p < .05 (two-tailed)
but not the sex of the partner ( F = 0.01), nor was there a
significant interaction effect ( F = 0.16). Male subjects,
especially the 2 alpha males, shared more than did female
subjects in the first test phase. Applied to the second test
phase, the same ANOVA yielded no significant differences
although the trend was in the same direction, that is, on
average more sharing by ma l e subjects regardless of their
partner' s sex, F(1, 11) = 3.43, ns.
The mean (___ SEM) rate of food transfer in the first phase
of the DETs, when 1 monkey had cucumber, was 13.7___ 1.7
compared with 34.7 ___4.5 in the second phase, when the
other monkey had apple. Instead of this being related to the
test phase, however, it was related to food type. In reversed
DETs, in which first apple and then cucumber were pre-
sented, more sharing occurrext in the first rather than second
test phase. To test for a possible effect of food type, I
compared interactions in the reversed DETs with those in
standard DETs for those 19 dyads that had been subjected to
both test types. A 2 × 2 ANOVA yielded a significant effect
of food type on the rate of transfer, F(1, 72) = 18.82, p <
.001 (two-tailed) but no such effect for test phase, F(1, 72) =
1.53, ns. Hence, regardless in which order the two food types
were presented, transfers of apple were more frequent than
transfers of cucumber.
Changes Over Time
Figure 2 gives the rate of food transfer to the partner
during the first and second test phases separately for apple
and cucumber. Apart from the generally higher rate of
transfer of apple demonstrated before, the graph shows that
apple sharing was distributed unequally over the test phase,
reaching its peak in the second 5-rain block regardless of
whether apple was provided as the first food (DETs) or the
l ~ l t T a t l q m m e S e c o n d T e s t
: Apple
1 4
1 2
374 DB WAAL
1 ' 5 6 - i 0 l l ] 1 5 1 ~ ' 2 0 1"5 6 - i 0 1 1 " 1 5 1 6 - ' 2 0
Figure 2. The mean (+ SEM) number of food transfers per individual possessor per 5-min block
from its side of the test chamber toward the other side. In the delayed exchange test (DET), 1 subject
received cucumber slices in the first 20 rain of testing, after which the other subject received apple
slices in the second 20 min. The order of food was reversed in reversed DETs. This graph shows
separate results for both test types. The transfer rate for apple is higher than that for cucumber
regardless of whether apple was provided first or second.
second food (reversed DETs). Cucumber sharing, in con-
trast, showed a relatively flat profile.
According to the affiliation and tolerance hypothesis (see
the introduction), one might expect the distance between
partners to follow a similar profile as the food transfers, that
is, the shortest distances in the second 5-rain block. Figure 3
shows the mean distance to the mesh partition for each
individual food possessor during the first test phase regard-
less of partner. As can be seen, the distance dropped steadily
throughout this test phase, with the greatest distance at the
beginning and the shortest distance toward the end of the
20-min period. A similar gradual decrease in distance to the
partition occurred during the second test phase (not shown).
The same data demonstrate a difference between first
possessors of apple (DETs) and cucumber (reversed DETs).
In the first 5-rain block, apple possessors stay away from the
mesh more than cucumber possessors (W'dcoxon test on
mean distance per individual possessor, T = 11, N = 12, p <
.05, two-tailed). Toward the end of the first phase, in
contrast, apple possessors were on average closer to the
mesh partition than were cucumber possessors (T = 9.5,
N = 11, p < .05, two-tailed). No significant differences
between apple and cucumber possessors were found in the
second test phase.
Rel at i ons hi p Vari abl es
Three dyadic measures of social relationships served as
independent variables in an analysis of sharing during DETs.
These measures derived from 18 months of global observa-
tions overlapping with the period of food testing. The three
dyadic measures were the following: rank distance, the
number plus one of other adults ranking between two
individuals (rank was determined by the outcome of agonis-
tic and approach-retreat interactions in the group); agonistic
rate, the hourly rate of agonistic incidents and approach-
avoidance interactions between 2 monkeys in the group; and
3.0-
2.5.
2.0-
1.5
- - o . - Cucumber
: Apple
1-'5 6-io 11-'15 16-'20
MINUTES
Figure 3. Distance indexes during the first test phase for cucum-
ber possessors (delayed exchange tests [DETs]) and apple possess-
ors (reversed DETs). The index is the mean (-+ SEAt) distance from
the mesh partition for each individual food possessor, with distance
categories ranging from 1 (close to the mesh) to 3 (away from the
mesh).
CAPUCHIN FOOD SHARING 375
proximity, point-sampled contact-sitting and grooming be-
tween 2 monkeys in the group as a percentage of the number
of samples collected.
These variables were compared in a multivariate design
with dyadic rates of food transfer. The prediction, based on
earlier studies of food tolerance in macaques (de Waal,
1991), was that food transfers would be most common
between partners with few agonistic interactions, high levels
of proximity, and short rank distances.
The initial analysis, which covered all relationships
among adults, produced no significant correlations. A subset
of dyads, however, showed surprisingly strong correlations
in the predicted direction (i.e., 14 female-female dyads in
which the possessor was dominant). A multiple correlation
coefficient of R = .71 was found in the first test phase. This
coefficient increased to R = .85 if the dependent variable
was restricted to tolerant food transfers (i.e., excluding the
collect-distant category). For this last multiple correlation,
each of the independent variables was found to make a
significant contribution. These contributions are listed here
in order of importance with one-tailedp values for 9 degrees
of freedom: agonistic rate (partial correlation coefficient,
pr = -. 72, t = 3.26, p < .01), rank distance (pr = -. 57, t =
2.19, p < .05), and proximity (pr = .54, t = 2.02, p < .05).
A similar, albeit less pronounced outcome was found if
the dominant female was the possessor in the second test
phase. The multiple correlation for tolerant transfers was
R = .59, and significant partial correlations were found for
agonistic rate (pr = -.53, t = 1.99, p < .05) and rank
distance (pr = -.53, t = 1.99, p < .05) but not proximity
(pr = .21, t = 0.68, ns). Other dyadic categories, such as
pairs involving adult males or female-female dyads in
which the possessor was not dominant, failed to show
significant correlations between social relationships in the
group and the rate of food transfer during testing.
Reciprocal Exchange
The number of food transfers during the second test phase
of the DETs, from the second possessor to the first, was
compared with the number of transfers that the second
possessor had obtained during the first phase. Measured over
all dyads, the Spearman correlation between these two
variables was p = .15 (N = 72, z = 1.23, ns), but limited to
tolerant transfers it was a significant p of .29 (z = 2.43, p <
.01, one-tailed). The latter correlation, which strongly hints
at a reciprocal exchange of food, was evaluated by subject.
Spearman correlations were calculated per subject across the
5 or 6 (depending on group size) adult partners it had been
tested with. Seven of the 9 adult females showed positive
correlations between given and received tolerant transfers,
but only 1 of the 4 males did. Correlations were particularly
low for both alpha males (see Figure 4).
Comparison With Controls
Individual means for two parameters in the first test phase
of DETs and reversed DETs were compared with the same
subjects' behavior during controls: (a) distance from the
mesh partition and Co) food transportation rate, that is, the
number of times a sizable food item (e.g., an entire piece
taken directly from the bowl) was carried toward the mesh
partition to be left within reach of the partner (or, in controls,
within the area where a hypothetical partner could reach it).
No significant differences in distance were.found between
DETs and controls, but the Wansportation rate of cucumber
Figure 4. For each possessor in delayed exchange tests, the rate of food transfer toward the partner
during the second test phase is compared with the rate of transfer received from the same partner
during the first phase. This analysis is limited to tolerant transfers (i.e., excludes food collection at a
distance from the possessor). The graph shows Spearman rhos between outgoing and received
transfers per individual subject with each of its 5 or 6 test partners. Hatched bars indicate adult males
and shaded bars adult females. Alpha subjects are marked with an asterisk.
376 DE WAAL
pieces in the first test phase was lower than in controls. The
drop was significant for subordinate possessors (T = 7, N =
11, p < .05, two-tailed) but not for dominant possessors
(T = 14.5, N = 9, ns). Cucumber transportation in DETs and
controls was not significantly related: Spearman p = - . 14
(N = 13, ns).
Reversed DETs, in which the first food received was
apple, showed rather contrary results. For 11 of the 13
subjects, the distance to the mesh was reduced in the first
phase of reversed DETs compared with controls (T = 16,
N = 13, p < .05, two-tailed). This distance decrease was
most pronounced during the final time block. The food
transportation rate, on the other hand, was unaffected in the
reversed DETs regardless of the possessor' s relative rank
(T = 21, N = 9, ns). A significant positive correlation was
found between each individual' s apple transportation rate in
reversed DETs and controls: p = .57 (N = 13, p < .05).
Di scussi on
Brown capuchins show a surprising level of social
tolerance. Even i f possessors can easily monopolize food,
there is a high rate of food transfer toward nonpossessors. To
my knowledge, no nonhuman primates other than chimpan-
zees and capuchins have been tested in the mesh paradigm.
Perhaps this reflects the expectation, based on the absence of
spontaneous food sharing in the group context, that most
other primates will not engage in transfers through mesh.
Schaub' s (1995) findings on long-tailed macaques (Ma-
caca fascicularis) tested in a different apparatus may be
illustrative of how most other primates would behave: The
mere presence (and occasional threats) of dominant individu-
als strongly suppressed attempts by subordinate individuals
to access food. Schaub described his findings in terms of
threshold distances at which dominant monkeys inhibit the
behavior of subordinates (see Kummer & Cords, 1991). The
present study shows that capuchins have few inhibitions
even at close distances (e.g., within ann' s reach). Aggression
was virtually absent, and large quantities of food were
moved from one section of the chamber to the other. At the
same time, it should be kept in mind that active sharing of
food was rare (0.3% of the transfers), as was direct taking of
food from the hands or mouth of the possessor (0.9%). The
vast majority of transfers was passive in that food was
collected through the mesh after having been dropped by the
possessor.
The higher rate of food transfer when possessors had
apple compared with cucumber was most likely due to the
fact that apple crumbles easily when eaten or manipulated,
whereas cucumber does not. As a result, many more
fragments of apple were laying around by the end of a test
than fragments of cucumber, which resulted in more reach-
throughs by the partner to collect scraps.
It is unclear at this point what, i f anything, the control
tests (tests without a partner) reveal about the motivations
underlying the monkeys' behavior. The presence of a partner
reduced the tendency to transport cucumber pieces to the
mesh partition but not the tendency to transport apple pieces.
This is puzzling because apple is favored over cucumber.
Why would the food that both the possessor and the partner
are least interested in be "hel d back" in pair tests? One
possibility is that the monkeys are motivated to socialize in
pair tests and that apple can be built into these interactions
because of the shared interest, whereas cucumber cannot.
Because of this, cucumber is carded around in cont r ol s- -
when there is little else for the subject to do- - wher eas this
food takes on secondary importance in pair tests, hence is
left behind when possessors approach their partner. Apple, in
contrast, is kept in possession or nearby even when proxim-
ity with the partner is established, and pairs spend more time
together by the end of tests with apple than with cucumber. If
food does indeed serve as a social facilitator, this was not
part of the original list of hypotheses, and the idea needs
further development.
A second possibility is that, when confronted with a
choice between a social partner and cucumber, food possess-
ors simply drop the food and choose to be with the partner,
whereas the same choice when the food is apple is resolved
by them trying to have both, that is, sit next to the partner
while keeping the apple in possession. This compromise
automatically results in frequent food transfers i f the level of
tolerance is high enough. In this view, food sharing may be
the outcome of two conflicting tendencies shown particu-
larly when both partners and food are highly preferred.
The data suggest striking sex differences. First, more food
found its way to the partner when a male than when a female
monkey was the possessor. Second, agonistic and social
relationships in the group failed to predict how much food
partners obtained from male possessors, but these variables
did have predictive value with regards to female possessors.
And third, for male monkeys there was no correlation
between the amount of food received from a partner in the
first test phase and the amount transferred to this partner in
the second phase, whereas for female monkeys such a
correlation was found. If one accepts food transfer rate as an
indicator of the possessor' s sharing tendency, the best way to
put this is that male monkeys share more generously and less
discriminatingly compared with female monkeys, and their
sharing is not necessarily mutual.
For female capuchins, in contrast, there exists a signifi-
cant correlation between agonistic and social relationships in
the group and the food transfer rate as dominant possessors.
Perhaps this relation is expressed because dominant females
have fewer constraints on their behavior than subordinate
females. Dominant females tend to share most with adults of
both sexes with which they normally spend much time
together and have few agonistic encounters, and to whom
they are close in rank. In addition, the majority of female
monkeys show reciprocal food transfers in that the amount
of food transferred to a partner in the second test phase can
be predicted on the basis of the amount received from the
same partner in the first test phase. Given the effect of social
relationships on their behavior, the reciprocal sharing among
female monkeys could well be the product of symmetry-
based reciprocity (see the introduction).
The differences between male and female capuchins are
interesting from the perspective of the evolution of sharing.
For male capuchins, particularly alpha males, food sharing
CAPUCHIN FOOD SHARING 377
might be a paternal investment strategy; that is, when
females and juveniles receive food from a male, this may
benefit this male' s progeny either directly or through the
mother. The explanation for this behavior may be sought in
kin selection. For adult female capuchins, on the other hand,
kin selection cannot be the entire explanation. It may apply
to female sharing with relatives in the group, but many
adults are unrelated to them, and in the tests female monkeys
also shared with these subjects. Hence, reciprocal altruism
may need to be part of an evolutionary explanation of female
sharing tendencies.
This is not to say that I understand the exact mechanism of
reciprocity in the case of capuchins. Of the four hypotheses
listed in the introduction, the first can be rejected because of
clear indications for a partner effect in femal e-femal e dyads.
Most data reported here are consistent with the second
hypothesis according to which sharing is explained by a
combination of affiliative tendencies and social tolerance.
The only finding that seems to counter this hypothesis is that
association between subjects near the mesh partition is
differently distributed over time than the food transfer rate.
Yet, the mere fact that subjects associate more toward the
end of the test, when they generally have run out of food,
does not disprove that sharing earlier in the test was a
product of affiliative tendencies.
An increasing number of ongoing studies on capuchins,
both in the field and in captivity, investigates social phenom-
ena of the kind studied thus far mainly in Old World
primates. Topics of interest include female bonding, the
nature of mal e-mal e relations, the function of grooming,
intergroup relations, and coalition formation. The more one
learns about capuchins, the more compl ex the picture
becomes. The latest findings, for example, include that
grooming among female capuchins is directed down the
hierarchy in Cebus olivaceus and C. apeUa but not C.
capucinus (O' Brien, 1993; Parr, Matheson, Bernstein, & de
Waal, 1997; Perry, 1996), that male capuchins engage in
intense reunions after separation (Matheson, Johnson, &
Feuerstein, 1996), and that reconciliation occurs after aggres-
sion (Verbeek & de Waal, in press). Given the obvious
richness of capuchin social life, it is quite possible that these
monkeys reciprocally exchange a wide range of "curren-
cies, " from allonursing to agonistic alliances, and from food
sharing to coordinated hunting. For example, the tendency in
female capuchins to groom l ower ranking partners may be
related to exchange i f low-ranking females lend support to
or voluntarily share food with high-ranking females.
There quite likely has been a tendency to underestimate
the social complexity of New World monkeys (Strier, 1994).
Therefore, i f for the moment the second explanation of the
results of the experiments is favored, it is nevertheless good
to realize that Hypotheses 3 and 4 are by no means
contradicted. These hypotheses assume higher levels of
volition and calculation in the food exchange (see the
introduction). I am currently setting up a new round of
testing, with additional control procedures, that may help
differentiate Hypothesis 2 from cognitively more demanding
explanations.
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Recei ved December 5, 1996
Revi si on received March 18, 1997
Accept ed March 20, 1997 •
Acknowledgment of Ad Hoc Reviewers
The Editor thanks the following persons for reviewing manuscripts. (Numbers in parentheses
indicate assistance with more than one manuscript.)
Charles I. Abramson
James R. Anderson (2)
Ki m Bard
Kent Berridge
Jean Geary Boal
Richard Byrne
Josep Call
Douglas Candland
Ni col a Clayton
George Collier
Marina Cords
Jill A. Davenport
Bertrand Deputte
Claude Dumas
Nathan Emery
John Fentress
Christine Filion
Gordon Gallup
Mi mi Hal pem
Marc Hauser
Michael Hennessy
Harol d A. Hertzog, Jr.
Charles Janson
Caroline E Keating
Suzanne MacDonal d
Peter MacNei l age
Brenda McCowan
William McGr ew
Warren Meck
Tom Mi nor
Robert Mitchell
J. Bruce Overmi er
Donald Owings (2)
Davi d I. Perrett
Duane Quiatt
Scott Robinson
Robert A. Rosellini
Lael a Sayigh
Robert Seyfarth (3)
Davi d Sherry
Marci a L. Spetch
Davi d Washburn
Gregory Charles
Westergaard
Ian Whishaw