Study suggests sharing mechanisms may be different for adult male capuchins. Males share food more readily and less discriminatingly than females. Evidence for spontaneous food.sharing in chimpanzees has been mounting ever since.
Study suggests sharing mechanisms may be different for adult male capuchins. Males share food more readily and less discriminatingly than females. Evidence for spontaneous food.sharing in chimpanzees has been mounting ever since.
Study suggests sharing mechanisms may be different for adult male capuchins. Males share food more readily and less discriminatingly than females. Evidence for spontaneous food.sharing in chimpanzees has been mounting ever since.
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). 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The chimpanzee's service economy: Food for grooming. Evolution & Human Behavior, 18, 1-12. de Waal, F. B. M., & LuttreU, L. M. (1988). Mechanisms of social reciprocity in three primate species: Symmetrical relationship characteristics or cognition? Ethology & Sociobiology, 9, 101- 118. de Waal, F. B. M., Luttrell, L. M., & Canfield, M. E. (1993). Preliminary data on voluntary food-sharing in brown capuchin monkeys. American Journal of Primatology, 29, 73-78. Wilkinson, G. (1984). Reciprocal food sharing in the vampire bat. Nature, 308, 181-184. 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