ANIMAL BEHAVIOUR, 2000, 60, 253261doi:10.1006/anbe.2000.1471, available online at http://www.idealibrary.com on

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dr,iesdesigned to exclude this symmetry-based explanation by testing each pair (N=16) of adult females on sixseparate occasions. There existed a significant covariation across tests of sharing in both dyadicdirections, a result unexplained by relationship symmetry. Moreover, control procedures (i.e. testing of afood possessor without a partner, or testing of two individuals with the same food or two different foodsat the same time) indicated that behaviour during food trials is not fully explained by mutual attractionor aversion. The monkeys take the quality of their own and the partners food into account, andpossessors limit transfers of high-quality foods. Instead of a symmetry-based reciprocity explanation, amediating role of memory is suggested, and a mirroring of social attitude between partners.

2000 The Association for the Study of Animal Behaviour

Very few nonhuman primates regularly share food out-side the parentoffspring context. The best-knownexamples are the anthropoid apes: in the field, bonobos,Pan paniscus, and chimpanzees, P. troglodytes, share largefruits and meat (e.g. Goodall 1963; Teleki 1973; Kuroda1984; Boesch & Boesch 1989; Hohmann & Fruth 1993),and in captivity, they share attractive plant foods (Silk1979; de Waal 1989, 1992).

Less widely known is the food sharing by a medium-sized Neotropical primate, the capuchin monkey (Cebusspp.). Not only do adult capuchins show remarkabletolerance towards immatures (Janson 1986, 1988;Fragaszy et al. 1997), adults also share amongst them-selves. In captivity, both edible and inedible objectschange possession peaceably among adults, without therank asymmetries characteristic of most other primatespecies (Thierry et al. 1989; de Waal et al. 1993).

Perry & Rose (1994) confirmed earlier reports byNewcomer & de Farcy (1985) and Fedigan (1990) thatwild Cebus capucinus capture coati pups (Nasua narica).

coordination among nest-raiding monkeys could con-ceivably increase capture success. This has also beensuggested by Rose (1997) for capuchins hunting squirrels(Sciurus variegatoides). Even if these situations are notidentical to the cooperative hunting of chimpanzees, andcertainly less well documented, there are grounds toassume convergent, hunting-related evolution of foodsharing in capuchins and chimpanzees (Rose 1997).

Food sharing offers opportunities for detailed researchinto reciprocal altruism (cf. Trivers 1971). That is, notonly a demonstration of reciprocal exchange and a deter-mination of the conditions that promote its evolution(for overviews see Ethology and Sociobiology, 9 (24), 1988;Dugatkin 1997), but also research into the underlyingmechanisms. Because of the required time delay betweengiven and received benefits (Rothstein & Pierotti 1988),reciprocal altruism is a more complex form of co-operation than mutualism. However, some believereciprocal altruism is rare or absent in nature (Clements &Stephens 1995; Connor 1995; Pusey & Packer 1997).Attitudinal reciprocity in foodmon

FRANS B.

Living Links, Yerkes Regional Primate Research Center a

(Received 14 January 1999;final acceptance 18 February

Capuchin monkeys (Cebus apella) share food even ifmoved into a test chamber in which one of them recarrot pieces for the next 20 min. Previous researctransfer in both directions across femalefemaleReciprocity across dyads can be explained, howevebetween two individuals, provided these tendencThey observed monkeys beg for and share the meat ofpups. Because coati mothers defend their offspring,

Correspondence: F. B. M. de Waal, Living Links Center, YerkesRegional Primate Research Center, Emory University, 954 NorthGatewood Road, Atlanta, GA 30329, U.S.A. (email: dewaal@emory.edu).

00033472/00/080253+09 $35.00/0 253aring among brown capuchineys

DE WAAL

Department of Psychology, Emory University, Atlanta

ial acceptance 7 June 1999;000; MS. number: A8391R)

arated by a mesh restraint. Pairs of capuchins wereved apple pieces for 20 min, and the other receivedad shown a correlation between the rate of foodyads. The present study confirmed this result.

by symmetry in affiliative and tolerant tendenciesdetermine food sharing. The present study wasThe few studies that have addressed the cognitiverequirements of reciprocal altruism have generally foundit hard to distinguish memory-based mechanisms, such asmental score-keeping, from simpler alternatives. Theexperimental manipulation of food availability, qualityand quantity in a food-sharing species allows the creation

2000 The Association for the Study of Animal Behaviour

254 ANIMAL BEHAVIOUR, 60, 2of situations in which services are predictably exchanged,hence in which contingencies between given andreceived behaviour can be examined. The first such studypresented juvenile chimpanzees with the opportunity toshare valuable items through bars (Nissen & Crawford1932). Since bars prevent the dominant of a pair fromusing force, interindividual food transfers under thiscondition are likely to be voluntary. Some of the chim-panzees did indeed share, and the authors suggested thatthis sharing was, essentially, barter on a credit or deferredbasis (Nissen & Crawford 1932, page 415).

De Waals (1989) data on plant food sharing in a largecaptive colony of chimpanzees are consistent with thehypothesis that tolerance in relation to food evolved, atleast in part, as a form of reciprocal altruism. This studyfound a positive correlation between the rates of foodtransfer in both directions within each dyad. The samestatistical approach has been applied to other spon-taneous social exchanges in primates, such as groomingand agonistic support, claiming the same positive result.Reciprocity correlations for monkeys are generally lowerthan for chimpanzees (e.g. Packer 1977; Seyfarth 1980; deWaal & Luttrell 1988), and it should be noted that studieson baboons have cast doubt on both the altruistic natureand reciprocal distribution of malemale coalitions(Bercovitch 1988; Noe 1990; but see Smuts 1985).

A correlation between given and received acts across anentire matrix of relationships can come about in multipleways. One possibility is that the correlation results from acommon underlying variable. The variable most in needof control is time spent in association: if members of aspecies were to direct aid preferentially to close associates,a reciprocal distribution would automatically resultdue to the symmetrical nature of association. The samesymmetry argument applies to kinship. This reciprocitymechanism, dubbed symmetry-based reciprocity, needsto be distinguished from calculated reciprocity whichreflects a contingency, based on mental record-keeping,between given and received services (de Waal & Luttrell1988). In most species for which reciprocal altruism hasbeen reported, including nonprimates such as vampirebats (Desmodus rotundus; Wilkinson 1984) and impala(Aepyceros melampus; Hart & Hart 1992), symmetry-basedreciprocity cannot be ruled out and this is a likelymechanism.

Whereas this issue can be addressed through statisticalcontrol of confounding variables (cf. de Waal & Luttrell1988), a more rigorous solution is to examine exchangesbetween individuals over time: does a service provided byindividual A to B increase the probability of a service by Bto A soon thereafter? Such temporal association is notpredicted by symmetry-based reciprocity. Following pre-liminary evidence for a temporal association betweengrooming and agonistic support in cercopithecinemonkeys (de Waal & Yoshihara 1983; Seyfarth & Cheney1984; Hemelrijk 1994), the first demonstration ofpartner-specific service exchange concerned chimpan-zees. It was found that after individual A had groomed B,Bs tendency to share food with A during a subsequent

food trial was greater than usual. Significantly, Bs sharingincrease was not general: sharing with individuals otherthan the grooming partner remained unaffected. Such asequence of events is hard or impossible to explainwithout the involvement of memory. Thus, chimpanzeesmay possess the cognitive capacities and social tendenciesrequired for calculated reciprocity (de Waal 1997b).

Indications of food-related reciprocity in browncapuchins, Cebus apella, also exist. One study docu-mented interactions between two entire captive groups ofmonkeys in which one group provided tools to a secondgroup, which then shared food obtained with these toolswith the first group (Westergaard & Suomi 1997). Thisstudy lacked appropriate controls, however: it remainedunclear whether tool and food transfers concerned thesame individuals, and whether the two services werecontingent upon each other.

Inspired by Nissen & Crawford (1932), our own exper-iments with this species use a mesh restraint between twomonkeys isolated from their group. Food transfers arecommon under this condition, occasionally involvingactive giving (i.e. the food possessor walks up to the meshpartition and pushes food to the waiting recipient on theother side). Based on records of 9896 food interactions, deWaal (1997a) reports that active giving was rare, however(i.e. 0.3% of food transfers), as was direct taking of foodfrom the possessors hands or mouth (0.9% of transfers).Negative responses by the possessor to attempts at foodcollection by the partner occurred in 4% of the inter-actions, mostly consisting of turning or jumping away,pulling the food away, or slapping the partner. Overtlyagonistic responses (i.e. threats and vocalizations) consti-tuted a small minority of these cases. Similarly, attemptsby dominant nonpossessors to forcibly take food wererare (0.9% of interactions), and usually unsuccessful.

The overwhelming majority of transfers followed apeaceful, passive mode (e.g. two monkeys sat side-by-sideat the partition while the nonpossessor reached throughthe mesh to collect pieces held or dropped by the posses-sor). This behaviour is not to be confused with so-calledtolerated theft, a mechanism that assumes aggressivepressure from nonpossessors (Blurton Jones 1987). Toler-ated theft appears a poor explanation of food sharing innonhuman primates (de Waal 1996, pp. 152153). Thepeaceable, relaxed nature of the food interactions in ourtest paradigm, the requirement of physical proximity,and the occasional rejections by food possessors, indicatethat food transfers result from selective tolerance by thepossessor combined with the nonpossessors interest.

Recently we reported reciprocal food transfers througha mesh partition among adult females. These femaleslived permanently together in a social group but weretemporarily removed for testing. Each combination offamiliar females was tested only once. One female ownedone type of food for 20 min, after which the other femaleowned another type for the next 20 min. It was foundthat the transfer rate from female A to B in the first testphase predicted the rate from B to A in the second phase(de Waal 1997a). The mechanism underlying this reci-procity could be rather simple, however. If food sharing isthe product of affiliative tendencies (sitting together at

the mesh partition) combined with high tolerance (allow-ing the other to take food), and if affiliative tendencies

whether the monkeys take partner presence into account

their food.

from the partition.In the present analysis, the central measure is the

255DE WAAL: CAPUCHIN FOOD SHARINGMETHODS

Subjects and Housing

The Yerkes capuchin colony consisted of two separatesocial groups of C. apella. Each group included two adultmales, and four or five adult females, totalling 13 adultsubjects in both groups. All 11 offspring in the groupswere infants or early juveniles except for one male thatwas 3.5 years old at the beginning of the study. Sevenadult females had one offspring, and two adult femaleshad two offspring at the onset of study.

Because most individuals were of unknown back-ground, we conducted a DNA profile analysis. Of the 36pairs of adults housed in the same group, only one pairwas likely to be related, and two pairs were consideredpotentially related (de Waal 1997a). The monkeys cameto us as juveniles and adults. We did not detect obviousbonds of kinship (e.g. immatures closely associating withparticular adult females), and it is unknown whether andhow they would know kinship relations. Kinship wassubsequently ignored in the data analysis.

The capuchin laboratory offered indoor/outdoor hous-ing for two monkey groups with a total of 25 m2 of floorspace for one group, and 31 m2 for the other. Normally,the monkeys had free access to the entire space. Visualcontact between the groups was controlled by an opaquescreen. The facility included a separate office withand whether they consider the partner a competitor forand tolerance are symmetrical between familiar females,food sharing based on these tendencies will automaticallybe reciprocal across dyads. Possibly, therefore, we foundyet another instance of symmetry-based reciprocity.

However, calculated or tit-for-tat reciprocity could notbe excluded, and the present series of experiments tries toclarify the underlying mechanism. It follows the samedesign and uses the same subjects as in the previousstudy, but now each pair of monkeys is tested repeatedlyon separate occasions. The question is whether individualAs sharing with B predicts Bs sharing with A on atest-by-test basis. If we assume stability in social relation-ships, relational symmetries such as mutual affiliationand tolerance cannot account for covariation of mutualsharing tendencies. If such covariation does exist initerated tests it suggests a contingency between givingand receiving.

Since our previous research indicated that adult malesshare less reciprocally than females (de Waal 1997a), thepresent study focuses on females. Apart from pair tests inwhich females could share mutually with a time delay, weadded control procedures intended to measure the degreeto which capuchins take environmental variables intoaccount. Control procedures included tests without apartner, and tests in which both partners received differ-ent foods at the same time. These procedures may revealwindows through which researchers could monitor themonkey area. During testing, however, the experimentersfrequency of tolerant food transfers defined as thenumber of times the nonpossessor collects or receivesfood from the possessors side either directly from thehands or mouth of the possessor or by picking updropped food from within easy arms reach and in fullview of the possessor. This measure excludes the collec-tion of food when the possessor had his or her backturned or had temporarily moved away from the par-tition. The exact amounts of transferred food were notmeasurable, but it was clear that most of the time thefood possessor ate the lions share, and the partner onlyreceived left-overs. Exceptions did occur, however, infollowed the monkeys behaviour on a video screen set upin the office.

Each of the two monkey pens was partitioned intothree sections by means of one chain-link partitionand one opaque partition (i.e. the outer wall). Therewere interconnecting doors between adjacent sections,and a tunnel between the two distant sections. Theconcrete floors were covered with saw dust indoors, butuncovered outdoors. The monkeys received ad libitumwater and monkey chow, and a daily tray with bread,fruits and vegetables in the late afternoon after the dayslast test.

Experimental Procedures

A mobile test chamber made of vinyl-coated mesh wasattached to the front of a groups indoor pen. The testchamber was divided by inserting a partition, providingeach subject in a pair test with an area of 726060 cm.Bowls were attached to the outside of the chamber oneither side, well out of reach of the monkey on the otherside (Fig. 1). The back of the test chamber was opaque toprevent visual contact between test subjects and group-mates. Monkeys entered the chamber either directly fromthe pen, or from a transport box. The separation pro-cedure took approximately 10 min, after which themonkeys were allowed to habituate to the test chamberfor another 10 min. Following this, the experimenterbrought food, turned on a video camera, and left theanimal area. Video registration on Super-VHS covered thebehaviour of both subjects along with a time counter intenths of seconds.

Tests were conducted in the morning and early after-noons when the monkeys had not yet received any fruitsand vegetables. Because no subject was tested more thanonce per day, repeated tests on a particular dyad werealways conducted on different days. Transcription of thevideotaped tests was very detailed (de Waal 1997a pro-vides an ethogram). Every 30 s, we recorded the locationof subjects relative to the partition and the partner bydividing each individual section into three equal parts(distance 1: within 24 cm of the mesh partition; distance2: 2548 cm from the partition; distance 3: at the far endof the test chamber, away from the partner, and 4972 cmwhich the food possessor moved an entire piece of foodto the mesh and let the other take it.

different hands, showing them to the subject (making

e sut achro

This drawing, by the author, was made from an actual video still (from

256 ANIMAL BEHAVIOUR, 60, 2Delayed exchange tests (DET)We conducted a series of DETs in both directions on all

dyads among adult groupmates. This was the only testseries including both males and females (72 DETs on 36dyads). Foods used were different from the DETs of ourprevious study, which used cucumber first and applesecond (de Waal 1997a). In the present series, in the firsttest phase individual 1 received a handful of apple pieces(half of a medium-sized apple) for 20 min, after which thebowl was removed. The bowl was then filled with carrotpieces (same amount as apple) and given to individual 2for 20 min in the second test phase. During the next DETon the same pair of individuals, the order between indi-viduals 1 and 2 was reversed. Even though apple isgenerally preferred over carrot (see Results), both areFigure 1. Schematic drawing of the delayed exchange test (DET). Onoutside. A mesh partition divides the test chamber, preventing direcsharing, a male (right) hands a piece of food to a female who reaches tfavoured foods resulting in empty bowls in all tests.

food (either cabbage leaves, grapes, or carrot pieces) at thesame time, for 20 min.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 onehand only. These tests were given whenever possible (i.e.when an individual was separated from others) to eachSolitary controls (Control)While in the possession of apple pieces, each adult was

tested alone for 20 min, leaving the other section of thetest chamber empty.

Food preference tests (FPT)Each adult was given a choice between two different

foods. The experimenter held small pieces of each food in

bject at a time receives food from a bowl attached to the chamberscess to the food by the other individual. In a rare instance of activeugh the mesh to accept it. Both subjects visually monitor the transfer.de Waal 1997a).adult male or female. The following foods were comparedReiterated DETsAll 16 dyadic combinations between familiar females

were subjected to five more applecarrot DETs with bothfemales always in the same roles of individuals 1 and 2.Because the objective was to determine whether sharingin both dyadic directions covaried across tests, tests withthe same individuals in reversed roles would have intro-duced an additional variable that might have interferedwith this objective. Together with the corresponding testfrom the initial DET series (above), this made for sixrepeat-trials per femalefemale dyad.

Same-food trade tests (SFT)Tests on female dyads in which both individuals

received apple pieces at the same time, for 20 min.

Different-food trade tests (DFT)Tests on female dyads in which individual 1 received

apple pieces whereas individual 2 received a different

on separate occasions for each individual: apple, cabbage,carrot, cucumber and grape. We conducted a total of 286food preference tests.

The order of testing followed two phases. In the firstphase of 8 months, the first series of DETs, whichincluded both males and females, was followed by theSFTs. Immediately upon completion of this phase, reiter-ated DETs on female pairs were interspersed with DFTsand Solitary controls in the second phase of 14 months.

Statistics

I made comparisons of individuals or dyads acrossconditions using the Wilcoxon signed-ranks test. This testis sensitive to both the direction and magnitude ofdifferences. I followed the procedures outlined byMundry & Fischer (1998), that is, I conducted asymptotictests only on data meeting the N>15 criterion, whereaswe used exact tests for smaller sample sizes. All tests weretwo-tailed, except those for reciprocity. I evaluated reci-

procity across tests within dyads using a randomizationtest, RT 2.1, programmed and explained by Manly (1997).

pl

257DE WAAL: CAPUCHIN FOOD SHARINGRESULTS

Partner Effect

I compared the behaviour of individual 1 across threedifferent conditions (Control: no partner present in theadjacent section of the test chamber; DET (phase 1):partner present, but has no food; SFT: partner present andhas the same food as individual 1) in femalefemaledyads. In all three conditions individual 1 possessed applepieces for 20 min.

Because we collected the controls by individual, dyadicdata on the other tests were converted to individual datafor comparison. I did this by averaging results acrossdifferent partners for each subject in the DET and SFTtests. The first comparison concerned the number ofpoint samples (out of 41 samples per test) at whichindividual 1 was in the area immediately adjacent to themesh partition. Figure 2 shows that the tendency to be inthis area was lowest in controls and highest in SFTs. Thedifference between the two was significant (Wilcoxon:T=1.5, N=7, Pcarrot>cabbage>apple. That apple was at the low end may beexplained by the fact that individual 1 herself had apple.The rate when individual 2 had grapes was higher thanwhen she had apple (Wilcoxon: Z=2.38, P=0.017, non-directional) or cabbage (Z=1.99, P=0.047), but nothigher than when she had carrot. Other differences forindividual 1 in Fig. 3 were nonsignificant.

0SFT

4 (b)Fr

equ

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2

3

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0

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Figure 2. Mean+SE number of (a) samples in which the female foodpossessor sat close to the mesh partition and (b) entire pieces of foodtransported and dropped near the mesh partition within reach of thepartner under the three conditions: control (in the absence of apartner), the first test phase of a delayed exchange test (DET, apartner without food), and during a same-food test (SFT, a partnerwith the same food).20

(a)

es

15Individual 2s tendency to sit close to the meshdecreased linearly with the attractiveness of her own

258 ANIMAL BEHAVIOUR, 60, 225

(a)

20

1510food: cabbage>carrot>apple>grape. When individual 2had grapes, the number of samples spent close to themesh did not differ significantly from when she hadapple, but was lower than when she had carrot (Z=2.92,P=0.036) or cabbage (Z=3.41, P

0259DE WAAL: CAPUCHIN FOOD SHARINGDISCUSSION

The simplest explanation of food sharing through a meshpartition in capuchins is that these monkeys pay little orno attention to the partner: they just move around withtheir food, and let the partner opportunistically takewhatever comes within reach. Whereas this so-calleddisinterest hypothesis cannot explain reciprocal sharing,a second relatively simple hypothesis is perfectly capableof doing so. Labelled symmetry-based reciprocity (deWaal & Luttrell 1988), this hypothesis assumes thatindividuals do take partner identity into account, bothby avoiding certain partners and by being attracted toothers. If attraction and aversion are symmetrical withineach dyad, and if attraction and aversion determine foodsharing, a reciprocal distribution of sharing will auto-matically result.

In our previous studies, the disinterest hypothesis wasrejected because of a significant correlation betweensocial relationships and the rate of food transfer (de Waal1997a). Dominant females tended to share most withadults of both sexes that were familiar groupmates ofsimilar rank and with whom they had had few agonisticencounters. Because the tendency to sit at the meshpartition during food tests and permit the other to collect

Transfers received

Figure 4. Mean+SE number of food transfers by individual 2to individual 1 in the second test phase following food transfersby individual 1 to individual 2 in the first phase above ( ) or below( ) individual 1s mean. Data for 16 femalefemale dyads, indicat-ing covariation of sharing in both directions within a dyad.18

Mea

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16food is influenced by the relation with the partner, thisopens the possibility of symmetry-based reciprocity (i.e.rates of food sharing based on symmetrical attraction oraversion between individuals).

The present study throws new light on the tendenciesinvolved in food transfers, including the question ofwhether sharing is an appropriate label for this phenom-enon. First, the amount of time females spent close to themesh partition depended on the quality of food in theirown possession and that in their partners possession.Specifically, females spent more time close to the meshwhen there was a partner versus no partner, but droppedfewer pieces of food near the mesh when a partner waspresent. This suggests attraction to the other while at thesame time a reluctance to leave food around whenanother monkey is nearby. The same reluctance to letanother monkey remove food was indicated by exper-iments in which both partners received food at the sametime: the more attractive the monkeys own food wasrelative to the others food, the less she would stay closeto the mesh. Conversely, the less attractive the individ-uals own food compared with the others, the more timeshe would spend close to the other. Thus, in addition tothe social relationship, several other variables seem toaffect the tendency to sit close to the mesh, such as thelikelihood that food will be taken, the partners interest inthe food, and the individuals own interest in the part-ners food. Time spent at the mesh partition was, there-fore, not simply a product of mutual attraction oraversion. Most importantly, these experiments on therole of food quality indicated that the monkeys take intoaccount the cost of losing food to the other. Thus,whereas our capuchins show extremely little aggressionin pair tests (see Introduction, and de Waal 1997a) com-pared with the whole group condition (Verbeek & deWaal 1997), an element of competition is clearly recog-nizable in pair tests.

This competitive element suggests that the monkeysbehaviour rests on more than tolerance. They seem awarethat the other may take their food, and they know how toprevent this, but nevertheless commonly adopt a positionin which the other can freely collect part of their food.Instead of sitting in the far corner, which would permitthem to clean out the food bowl undisturbed, theyvoluntarily create a context in which food is lost to theother. The cost of doing so is low (the food possessoreats the most, and probably, the best parts), but it ismore than most primates would ever do (for an illus-trative example concerning macaques, see Schaub 1995).Because of the active seeking of proximity in which foodtransfers can take place and the possessors otherwisegeneral passivity in the sharing process, the best term toemploy is facilitated taking: the possessor facilitates theprocess by approaching the other with food, while theother is permitted to take. This term recognizes the activeinvolvement of both parties, and avoids the humanconnotations of the term sharing.

The main argument against symmetry-based reciproc-ity in facilitated taking is the positive relation betweenfood permissiveness in both dyadic directions in reiter-ated tests on femalefemale dyads. Stable symmetrical

aspects of relationships, such as preferential associationbetween individuals, may explain reciprocity across

bility would be to manipulate or control the rate of

260 ANIMAL BEHAVIOUR, 60, 2food transfer in the first test phase, something we didnot do.

However, a more likely explanation is that what hap-pens in the first test phase sets the tone for the remainderof the test, including the second test phase. Note thatsuch an explanation assumes no strict contingencybetween given and received services, as required for cal-culated reciprocity (cf. de Waal & Luttrell 1988). Themechanism I propose is that rather than the amount oftransferred food, other aspects of the social interaction inthe first test phase matter at least as much in determiningproximity, tolerance and ultimately food transfer in thesecond test phase. If the first food possessor spends muchtime close to the other and tolerates the others foodcollection this may predispose the other to show a similarattitude towards the first individual later on in the test. Iffacilitated taking is mediated by such general social pre-dispositions, this would mean that, rather than keepingtrack of exact amounts of given and received food,the monkeys follow a simple tolerance-breeds-tolerancescheme.

This hypothetical mechanism, which I will dub attitu-dinal reciprocity, resides somewhere between symmetry-based and calculated reciprocity in terms of complexity. Itis less cognitively demanding than calculated reciprocity,because it does not assume mental score-keeping of givenand received services nor expectations about appropriatereturn-favours, or the punishment of cheating. It is morecomplex than symmetry-based reciprocity, however, inthat memory of previous events is implicated, which inturn affects current behaviour. Our work on food trans-fers after cooperation suggests a similar mechanism, inwhich joint action induces a positive, tolerant attitudetowards the partner (de Waal & Berger 2000). Atti-tudinal reciprocity follows from variability in social pre-dispositions, ranging from friendly to hostile, and atendency to adjust to the predisposition perceived in theother: if individual A acts friendly towards B, this stimu-lates B to act friendly towards A. Such mirroring ofattitudes may operate especially when time intervalsbetween events are short, and hence may explain our testresults. It is one more hypothesis to consider in studies ofproximate aspects of animal cooperation.

Acknowledgments

I am grateful to Michelle Berger, Julia Christou, DarrenLong and Richard Thompson for assistance with exper-iments and data administration. I thank David Stephens,Gerald Wilkinson and two anonymous referees for con-structive comments on the manuscript. This researchdyads, but they do not predict a cofluctuation offacilitated taking in both directions within each dyad.On the other hand, we cannot exclude the possibility thata short-term covariate, such as a pre-existing temporarybut symmetrical condition of the relationship betweenany two test subjects, underlies the behaviour in bothdyadic directions. The only way to exclude this possi-was made possible by support from the National ScienceFoundation (IBN-93221195) and a grant from theNational Institutes of Health to the Yerkes Regional Pri-mate Research Center (RR-00165). The research presentedhere was described in Animal Research Protocol Nos135-964 and 097-994, approved on 16 June 1999 by theInstitutional Animal Care and Use Committee of theYerkes Regional Primate Research Center, which is fullyaccredited by the American Association for Accreditationof Laboratory Animal Care.

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Attitudinal reciprocity in food sharing among brown capuchin monkeysMETHODSSubjects and HousingExperimental ProceduresFigure 1Delayed exchange tests (DET)Reiterated DETsSame-food trade tests (SFT)Different-food trade tests (DFT)Solitary controls (Control)Food preference tests (FPT)

Statistics

RESULTSPartner EffectEffect of Food QualityFigure 2Figure 3Reciprocity Across DyadsReciprocity Across Tests within DyadsFigure 4

DISCUSSIONAcknowledgmentsReferences