Aggression and Reconciliation in Cebus capucinus

P1: GLB/GVH/FZI/GRJ P2: GYK/GNI

International Journal of Primatology [ijop] PP448-371020 July 31, 2002 17:13 Style file version Nov. 19th, 1999

International Journal of Primatology, Vol. 23, No. 5, October 2002 ( C© 2002)

Aggression and Reconciliation in Cebus capucinus

Jean-Baptiste Leca,1 Isabelle Fornasieri,2 and Odile Petit1,3

Received March 17, 2000; revised September 5, 2000; accepted April 29, 2001

Most data relating to aggressive and conciliatory behaviors are from OldWorld primates. We recorded agonistic interactions and post-conflict behav-iors in a group of 12 white-faced capuchins (Cebus capucinus). After aconflict, we followed the aggressee as the focal individual during a 10-minpostconflict period. We also conducted matched-control observations on thesame individual. Conflicts involving physical contact were significantly bidi-rectional, and conflicts without physical contact were preferably unidirec-tional. Reconciliation was not be demonstrated at the group level. However,reconciliation occurred in kin and non-kin male/female dyads: their concilia-tory tendencies were 48.1% and 21.2%, respectively. White-faced capuchinsreconciled mainly during the first minutes after the end of the conflict. In kinand non-kin male/female dyads, selective attraction occurred, and aggressorswere more likely to initiate affiliative contacts than aggressees. Hold-bottomand mount while emitting loud vocalizations were the most characteristic be-haviors of reconciliation. Possible links may exist between aggressive andconciliatory patterns and other social variables.

KEY WORDS: capuchins; conflict; conflict resolution; social organization.

INTRODUCTION

The study of aggression and reconciliation provides useful informationto qualify social relationships in primate groups. Reconciliation is affilia-tive contact between former opponents shortly after conflict (de Waal and

1Equipe d’Ethologie et Ecologie Comportementale des Primates, Centre d’Ecologie etPhysiologie Energetiques, UPR CNRS 9010, Strasbourg, France.

2Faculte de Psychologie et des Sciences de l’Education, Universite Louis Pasteur, Strasbourg,France.

3To whom correspondence should be addressed; e-mail: [email protected].

979

0164-0291/02/1000-0979/0 C© 2002 Plenum Publishing Corporation



980 Leca, Fornasieri, and Petit

van Roosmalen, 1979). Most data relating to aggressive and postconflict in-teractions come from research conducted on Old World monkeys and apes(Aureli and de Waal, 2000). The topic is underinvestigated in New Worldspecies. In Macaca, interspecific comparisons have raised questions aboutthe relationships between agonistic and conciliatory behaviors and othersocial variables, such as strictness of the dominance hierarchy, interindivid-ual tolerance and group cohesiveness (Thierry, 1986; de Waal and Luttrell,1989; Petit et al., 1997). In order to improve our understanding of the overallpattern of social organization in a given species and to elucidate some of itsevolutary origins, comparative studies should be extended to other genera.

The four species of Cebus are quite variable in social patterns and be-havioral adaptability (Fragaszy et al., 1990; Izawa, 1979; Manson, 1999). Al-though aggressive interactions have been documented in capuchins, mostauthors were interested in socioecological issues such as food competition(Rose, 1994; Phillips, 1995), intergroup encounters (Perry, 1996a), sex differ-ences (Janson, 1984; Fedigan, 1993; Perry, 1997) and dominance relationships(Perry, 1996b, 1998a,b). Little information is available concerning qualitiesof agonistic behaviors, such as intensity or symmetry. The occurrence ofpostconflict behaviors was reported in white-faced capuchins (Cebuscapucinus) (Perry, 1995, 1998a) but no focused study was conducted. Theonly study of reconciliation in Cebus was conducted on brown capuchins(Cebus apella), which showed conciliatory tendency, but only following fightsin the absence of highly attractive food (Verbeek and de Waal, 1997). Re-searchers have investigated the occurrence of reconciliation in other NewWorld monkeys (Saguinus labiatus: Schaffner and Caine, 2000; Saimiri sci-ureus: Pereira et al., 2000; Callithrix jacchus jacchus: Westlund et al., 2000).However, they included close-proximity as a conciliatory interaction. Ac-cordingly, their results are not truly comparable with more conventionalstudies, that defined explicit affiliative contacts as reconciliation.

Our aim is three-fold: (1) to determine the overall patterning of agonis-tic behaviors in white-faced capuchins; (2) to investigate whether reconcili-ation occurred among them, and if so, to elucidate the form of postconflictattraction: timing, initiative and behavior patterns and (3), to assess possi-ble links among aggressive and conciliatory patterns and other variables ofsocial organization.

METHODS

Subjects and Housing

The group of white-faced capuchins was established in 1989 at thePrimatology Center of the Louis Pasteur University, Strasbourg, France.



Aggression and Reconciliation in Cebus capucinus 981

During the study, the group contained 12 individuals of 3 separate lineages.Four adult males and 3 adult females (>5 years old), 2 subadult males and2 subadult females (3–5 years) and one juvenile male (1–3 years) were sam-pled. Four births and one removal occurred during the study. The genealogyof the group is shown in Fig. 1.

We distinguished two different housing conditions: an enclosure inthe first period and semifree ranging in the second period. From Marchto July 1997, the group was maintained in a 70-m2 indoor/outdoor enclo-sure with 3 compartments: a 20-m2 outdoor compartment and 30-m2 and20-m2 indoor compartments. The enclosure contained wooden bars, plat-forms and chains. During observations, the monkeys were confined to the30-m2 indoor compartment. From August 1997 to September 1999, the grouplived and was observed in a one-acre outside park with natural vegetation.A 25-m2 connected indoor compartment had a concrete floor and metalsitting perches. The monkeys had free access to both indoor and outdoorareas. Commercial primate pellets and water were available ad libitum inthe indoor area; fresh fruit and vegetables were provided once a week butnot during observations.

Procedure

We observed the monkeys between 09.00 and 12.00 h and between 14.00and 17.30 h, from February 1997 to September 1999 except in December,January and August. One observer recorded spontaneous agonistic interac-tions involving individuals >1 year old via all-occurrence sampling(Altmann, 1974). In the semifree-ranging condition, only 10 of 397 aggres-sive interactions were not seen by the observer. We use only conflicts ob-served from the outset. However, most conflicts occurred while individ-uals were resting or engaged in social activities, during which, the groupwas highly cohesive and all occurrences of aggressive interactions could becollected.

An agonistic interaction is a display of aggressive behavior by an indi-vidual and a response by the recipient of the aggression. We recorded silentor vocal facial threat, lunge, swipe, bounce, chasing, pushing, hitting, grab-bing, wrestling, biting, and counteraggression as aggressive behaviors, whileavoidance, flight, cowering, and scream are nonaggressive and especiallyperformed by the aggressee. We defined two degrees of conflict intensity ac-cording to physical contact: conflicts with physical contacts—pushing, hitting,grabbing, wrestling, biting—and conflicts without physical contact: silent orvocal facial threat, lunge, swipe, bounce, chasing. We used only the highestintensity pattern to define one aggressive interaction.




Fig. 1. Genealogy of the white-faced capuchin subjects.




We distinguished two levels of symmetry in conflicts according to theaggressee’s response: unidirectional and bidirectional. An unidirectionalconflict includes avoidance or cowering by the aggressee. When the receiverdisplays counteraggressive patterns, the conflict is bidirectional.

If the same two opponents were involved in two successive conflictsin <1-min, we considered the two conflicts as a single aggression. After anagonistic interaction involving a physical contact and/or a lunge of >2 m,the aggressee was followed as the focal individual during a 10-min postcon-flict period (PC) via the procedure described by de Waal and Yoshihara(1983). We conducted a 10-min matched-control period (MC) on the samefocal individual on the next possible observation day and started within arange of 15 min before and 15 min after the starting time of the PC pe-riod. We divided both periods into blocks of 30 sec. At the start of eachblock, we recorded the social activity of the focal individual and the iden-tity of its contact partners. During the following 30 sec, we scored any in-teraction involving the focal individual. If the focal monkey was involvedin an agonistic interaction ≤15 min before a planned MC, we postponedthe observation until the next day. Before starting the matched-control pe-riod, the observer waited until the focal individual and the aggressor were≤5 m apart (York and Rowell, 1988). In the semifree-ranging condition,we also matched the weather—sunny and rainy—and the general activity ofthe group—foraging/locomotion and social activities/resting—of the corre-sponding PC. Before starting an MC observation, we controlled the weatherconditions and the general group activities. When the same conditions werenot met ≤7 days, we discarded the PC. In case of polyadic conflicts, i.e.,involving >2 individuals, we noted only the initial agonistic dyad.

Behavioral Definitions for White-Faced Capuchins

Aggressive Behaviors

Facial threat (Perry, 1996a; open mouth, bared teeth: Oppenheimer,1973): the mouth is opened and the lips are drawn back so that the teeth arevisible; the monkey lays its ears back, knits its brow and stares at anotherindividual; the display may be silent or combined with a vocal threat. Head-flag (Perry, 1996a; glance: Oppenheimer, 1973): the monkey jerks its headtoward a prospective coalition partner and then resumes a stare or a facialthreat toward its opponent; the headflag is the most common behavior usedin coalition partner recruitment. Overlord (Oppenheimer and Oppenheimer,1973; double threat: Fedigan, 1993): one monkey climbs on another mon-key’s back and clasps its hands around the bottom monkey’s chest so that




their heads are stacked on top of one another facing an opponent. Usuallyboth monkeys display a facial threat at the same opponent while in thisposition.

Affiliative Behaviors

Dance (Perry, 1996a): one monkey runs back and forth in slow mo-tion, while staring at another monkey. The dancer usually exhibits a duckface and pirouettes. Often, both monkeys dance simultaneously. The dancemay be accompanied by grunts, an intense gargle or a wheeze. Duck-face(Perry, 1996a; protruded-lips: Oppenheimer, 1973): one monkey stares atanother while protruding its lips so that they resemble a duck’s bill. Threetypes of clasping are distinguished: (i) hold-back: one monkey climbs on apartner’s back and clasps its hands around the bottom partner’s chest whilewalking in pair with interlaced tails; one or both monkeys may display aduck face and emit a loud vocalization such as grunts or an intense gargle;(ii) hold-bottom (mobile mount: Perry, 1995): one monkey clutches the otherfrom behind with both hands at hip level and may repeatedly thrust itspelvis against the genital region of the other, while walking in pair; one orboth monkeys may display a duck face and emit a loud vocalization suchas grunts or an intense gargle; (iii) hold-breast (hug: Oppenheimer, 1973):one monkey embraces another monkey front-to-front; this behavior is usu-ally mutual and accompanied by a twitter. Intense gargle (Perry, 1996a): aloud, rhythmic, raspy and throaty vocalization. Pirouette (Perry, 1996a): themonkey fixes its gaze on another monkey, twists its head from side to side,spins its body around, and looks over the shoulder or under the arms orlegs at the monkey toward which the behavior is directed. Twitter (Perry,1995): this vocalization is a series of rapid, high-pitched squeaks. Wheeze(Perry, 1996a): a very high-pitched prolonged vocalization that descends inpitch.

Data Analysis

We ranked individuals>1 year old in a dominance hierarchy accordingto the direction of avoidances and unidirectional aggressions. We recordeddata from spontaneous events and in the context of drinking competitionaround a single source of orange juice (9 2-h tests during 3 periods). We car-ried out hierarchical rank order analysis with the aid of Matman, editedby Noldus (de Vries et al., 1993). We calculated the improved index of




linearity (h’) (de Vries, 1995). We considered a social disturbance period(May 1999), which represented 70 conflicts and 65 PC-MC pairs, separatelyin the analyses. The analysis of aggression is based on 149 conflicts in theenclosure and 297 conflicts in the semifree-ranging condition. To be includedin statistical tests, each individual had to be involved in ≥3 agonistic inter-actions. The analysis of reconciliation is based on 105 PC-MC pairs in theenclosure and 279 PC-MC pairs in the semifree-ranging condition. The dataset consists of 54 PC-MC involving kin and 330 pairs involving non-kin. Kinrelations are of three kinds: mother/offspring, siblings or half-siblings, andgrandmother/grandchildren.

In order to determine whether reconciliation occur in white-facedcapuchins, we compared the timing of the first affiliative contact betweenformer opponents during one PC period with that during the correspondingMC. If individuals interacted sooner in the postconflict than in the matched-control period or only in the postconflict period, the opponent pair is at-tracted. If the converse occurred, the pair is dispersed. When there was nocontact between opponents or if contact occurred at the same time in bothperiods, the pair is neutral (de Waal and Yoshihara, 1983). We calculated theconciliatory tendency (CT) as follows: (number of attracted pairs—numberof dispersed pairs)/total number of pairs (Veenema et al., 1994). To be takeninto account in statistical tests, each individual had to be involved in ≥3PC-MC pairs.

We analyzed results via parametric statistical tests (ANOVAs) andnonparametric statistical tests: Wilcoxon signed ranks test, Friedman test,sign test, Kolmogorov-Smirnov test, chi-square test with Yate’s continuitycorrection (Siegel and Castellan, 1988).

RESULTS

Aggression

We conducted Wilcoxon tests to test the differences in rates and pat-terns of conflicts between the enclosure and the semifree-ranging conditions,based on means of individual values. The rate of conflict is significantlyhigher in the enclosure condition than in the semifree-ranging condition(1.15 vs. 0.76 conflict/hr for the whole group; N= 9, T= 42, p= 0.01). How-ever, there is no statistically significant difference in the patterns of aggres-sion between the two housing conditions, either in intensity: conflicts involv-ing physical contact represented 54% of conflicts in the enclosure and 49%of conflicts in the semifree-ranging condition (N = 9, T = 29, p = 0.25) or




in symmetry (bidirectional conflicts represented 40% of the conflicts in theenclosure and 45% of the conflicts in the semifree-ranging condition; N= 9,T = 17, p = 0.52). Consequently, we pooled data related to conflicts in thetwo housing conditions in subsequent analyses.

In the semifree-ranging condition, a 3-week period (May 1999, 52 hrsof observation) of social disturbance occurred in the group. The highest-ranking female and her daughter were outranked and replaced by subor-dinate males. If we consider the period before social disturbance and theperiod after social disturbance, the conflict rate changed as follows: pre-disturbance (0.75 conflict/hr), disturbance period (1.34 conflicts/hr), post-disturbance (0.63 conflict/hr). We conducted Friedman tests, based on indi-vidual data, to test conflict rates and patterns among the 3 periods. Thereis a statistically significant difference among the 3 periods in the rate ofaggression (χ2 = 6.9, d.f. = 2, p = 0.03). Analyses posthoc showed that thedisturbance period was characterized by a significant increase of conflict rate(p < 0.05). There was also a statistically significant change in the intensity(χ2 = 11.0, d.f. = 2, p = 0.004) and symmetry (χ2 = 8.6, d.f. = 2, p = 0.01)of aggression among the 3 periods. Analyses posthoc showed that duringthe disturbance period, conflicts without physical contact were significantlymore frequent than conflicts with physical contact (p < 0.05) and unidirec-tional conflicts were significantly more frequent than bidirectional conflicts(p < 0.05). Accordingly, we discarded the period with 70 conflicts in subse-quent analyses.

Influence of Age, Sex, and Dominance

We tested the effect of age and sex on the distribution of conflicts via2-way ANOVAs, with aggressees as focal. Aggression was directed primarilytowards females versus males (F1,8 = 9.9, p = 0.01) and towards subadultsrather than adults (F1,8 = 8.2, p = 0.02). Although subadult females tendedto receive more aggression than other age and sex classes (Fig. 2) it did notconstitute a statistically significant interaction (F1,8 = 3.6, p = 0.09).

We verified the linearity of the dominance hierarchy via the de Vries’test. During the predisturbance period, all adult males were individuallydominant over adult females, except the highest-ranking female and herdaughter, which ranked immediately below the top-ranking male (h’= 0.89,p< 0.001). Moreover, aggression was directed primarily down the hierarchy(Wilcoxon signed ranks test: N = 10, T = 52, p = 0.01). After the distur-bance period, the linearity was also verified (h’ = 0,87, p < 0.001) and ag-gression was directed primarily down the hierarchy (Wilcoxon signed rankstest: N = 11, T = 63, p = 0.002) (see Fig. 2).




Fig. 2. Effect of age and sex of the aggressee on the mean number of conflicts.

Patterns of Aggression

Many conflicts involved physical contact (mean = 55.0 ± 6.1%) andbites were common (m = 6.2 ± 1.8%). However, wounds were excep-tional (m = 0.6 ± 0.2%). Among bidirectional conflicts (m = 45.1 ± 6.2%),symmetrical interactions between opponents were mainly due to counter-aggression with headflag behaviors from the aggressee (m = 70.8 ± 6.7%)rather than physical counterattack (m = 29.2 ± 4.1%). A third of the con-flicts were polyadic (m = 33.6 ± 5.0%), i.e. involving >2 individuals. A fewof them were redirected aggression (m = 10.4 ± 2.2%), but the majority(m= 89.6± 5.0%) were aggressive interventions involving coalition recruit-ment of a third individual directed towards the initial aggressor or aggressee.Among aggressive interventions, 15.6 % (±3.8) included overlords. Bidirec-tional conflicts were much more frequent between kin (m = 77.0 ± 6.9%,N = 61) than between non-kin opponents (m = 40.0 ± 5.8%, N = 385).

To assess whether intensity of aggression was related to symmetry inconflicts, we distinguished 4 types of conflicts: bidirectional conflicts withphysical contact, undirectional conflicts with physical contact, bidirectionalconflicts without physical contact and unidirectional conflicts without phys-ical contact. To compare the numbers of the 4 types of conflicts, we con-ducted an ANOVA with repeated measures, with intensity and symmetryas independent factors and individual scores as a dependent variable. There




Fig. 3. Percentages of different types of conflict.

is no effect of intensity (F1,10 = 0.63, NS) and symmetry (F1,10 = 0.85, NS)on individual conflict rates. However, there is a significant interaction be-tween intensity and symmetry (F1,10 = 39.7, p = 0.001) (Fig. 3). Analysespost hoc showed that unidirectional conflicts without physical contact are sig-nificantly more frequent than unidirectional conflicts with physical contact(F1,10 = 14.0, p = 0.004). Among bidirectional conflicts, aggressions involv-ing physical contact are significantly more frequent than aggressions withoutphysical contact (F1,10 = 26.7, p = 0.001).

When we considered the mean duration of conflicts (dependent vari-able), ones with physical contact were significantly longer than conflicts with-out physical contact (F1,10 = 5.5; p = 0.04; Fig. 4) and bidirectional conflictswere significantly longer than unidirectional conflicts (F1,10 = 52.8; p=0.001;Fig. 4). However, there is no significant interaction effect between intensityand symmetry (F1,10 = 4.4; NS).

Reconciliation

Occurrence of Reconciliation

Before calculating the conciliatory tendency for the whole group, wecompared the corrected conciliatory tendencies among the different condi-tions and periods. From individual data, there is no statistically significant




Fig. 4. Mean duration of different types of conflict.

difference between the conciliatory tendencies in the two housing conditions(25.0 vs. 16.7%, Wilcoxon signed ranks test: N= 9, T= 21, p= 0.37). Thus, wepooled the number of PC-MC pairs in the two housing conditions. Among449 PC-MC pairs, 182 were attracted, 99 were dispersed and 168 neutral. Theconciliatory tendency of the group is 18.5%. If we consider the period beforesocial disturbance and the period after social disturbance, the conciliatorytendency of the group changed as follows: predisturbance (CT = 22.9%),disturbance period (CT = −11.3%), postdisturbance (CT = 20.7%). Via aFriedman test, based on individual data, we compared the corrected con-ciliatory tendencies among the 3 periods; there is a statistically significantdifference (χ2 = 9.6, d.f.= 2, p= 0.008). Analyses post hoc showed that thedisturbance period was characterized by a significant decrease of the cor-rected conciliatory tendencies (p < 0.05). Consequently, we discarded thisperiod, which represented 65 PC-MC pairs, in the following analysis.

Of the remaining 384 PC-MC pairs, 168 were attracted, 77 were dis-persed and 139 neutral. Thus, the representative conciliatory tendency ofthe group is 23.7%. With respect to the 11 focal individuals, 8 showed moreattraction than dispersion in their interactions with the opponent, 2 showedmore dispersion and one had neutral results (sign test, one-tailed, p= 0.055).

Because of this borderline result, we conducted further analyses basedon dyads to provide more convincing evidence for reconciliation in the studygroup (Watts, 1995). The first analyses focused on dyads of kin-relatedindividuals (male/male, female/female, male/female). Among 54 PC-MCpairs, 36 were attracted, 10 were dispersed and 8 neutral. The conciliatory




tendency of this type of dyad is 48.1%. With respect to the 7 dyads, allshowed more attraction than dispersion in their interactions with the op-ponent (sign test, one-tailed, p = 0.008) demonstrating the occurrence ofreconciliation among kin.

The second analyses focused on non-kin dyads. Among 330 PC-MCpairs, 132 were attracted, 67 were dispersed and 131 neutral. In non-kinfemale/female dyads, among 49 PC-MC pairs, 19 were attracted, 11 were dis-persed and 19 neutral. Via tests of non-kin female/female dyads, we failedto find reconciliation. With respect to the 7 dyads, 3 showed more attrac-tion than dispersion in their interactions with the opponent, 2 showed moredispersion and 2 had neutral results (sign test, one-tailed, NS). In non-kinmale/male dyads, over 88 PC-MC pairs, 37 were attracted, 21 were dispersedand 30 neutral. Via tests of non-kin male/male dyads, we demonstrated noreconciliation. With respect to the 12 dyads, 8 showed more attraction thandispersion in their interactions with the opponent and 4 showed more dis-persion (sign test, one-tailed, NS). In non-kin male/female dyads, among193 PC-MC pairs, 76 were attracted, 35 were dispersed and 82 neutral. Theconciliatory tendency of this type of dyad is 21.2%. Finally, when consid-ering non-kin male/female dyads, reconciliation was clearly demonstrated:with respect to the 22 dyads, 15 showed more attraction than dispersion intheir interactions with the opponent, 3 showed more dispersion and 4 hadneutral results (sign test, one-tailed, p = 0.004). Consequently, we limitedsubsequent analyses of reconciliation to kin dyads and non-kin male/femaledyads.

Timing of Postconflict Contacts

To determine the timing of reconciliation, we studied the distributionover time of the first affiliative contact between former opponents for bothobservation periods (Figs. 5 and 6). A Kolmogorov-Smirnov test showedthat PC and MC distributions differed significantly for kin dyads (D = 0.46,one-tailed, p < 0.001) as well as for non-kin male/female dyads (D = 0.14,one-tailed, p < 0.025). The greatest difference between the cumulative ob-servations was reached at 1.5 min for kin-related dyads and at 2 min fornon-kin male/female dyads. This means that most reconciliations occurredin the first 2 min following the end of conflict.

Selective Attraction

In order to confirm that selective attraction occurred between formeropponents and was not merely the result of a general increase in affiliation




Fig. 5. Frequency of the first affiliative contact between the former opponents in a 10-min periodfor kin dyads (PC = postconflict period; MC = matched-control period).

Fig. 6. Frequency of the first affiliative contact between the former opponents in a 10-min periodfor non-kin male/female dyads (PC = postconflict period; MC = matched-control period).




between group members, we calculated the total number of partners con-tacted by the focal individual in the course of an observation period. Then,we expressed the number of former opponents contacted and the numberof other partners contacted as percentages of the total number of contactpartners. We compared PC and MC periods for each focal individual. Fromindividual percentages, we compared PC and MC periods via a sign test.As expected, former opponents contacted at a higher frequency in the PCperiod for kin-related individuals (71.2% vs. 60.5%, relative frequency ofcontact higher in PC than in MC for 5 individuals, equal for 2; sign test,one-tailed, p= 0.031) and for non-kin male/female dyads (54.8% vs. 41.5%,relative frequency of contact higher in PC than in MC for 9 individuals, lowerfor 2; sign test, one-tailed, p = 0.033).

Nature of Conflicts and Probability of Reconciliation

To determine whether the probability of reconciliation is related to thenature of the preceding conflict (intensity and symmetry), we calculatedthe corrected conciliatory tendencies for different types of conflicts and foreach focal individual. The two factors are not independent and thereforedata did not permit use of ANOVAs. We conducted the analysis on non-kinmale/female dyads. We did not analyze the kin dyads because of insufficientdata. There is no statistically significant effect in the probability of recon-ciliation in conflict intensity (Wilcoxon signed ranks test: N = 9, T = 25,p = 0.41), or in conflict symmetry (N = 9, T = 34, p = 0.10).

Initiation and Behaviors of Reconciliation

To test whether the initiation of reconciliation was affected by the pre-vious conflict, we compared the numbers of first affiliative contacts initiatedby the aggressor and the aggressee in the PC and all contacts occurring inthe MC periods. Aggressors were more likely to initiate affiliative contactsthan aggressees in the PC period, whereas the converse occurred in the MCperiod. This result holds for dyads of kin-related individuals (PC: 69.0%of initiatives by aggressors, n = 42; MC: 40.0%, n = 35; χ2 = 5.4, d.f. = 1,two-tailed, p= 0.02) and for non-kin male/female dyads (PC: 53.7% of initia-tives by aggressors, n= 82; MC: 35.1%, n= 77; χ2 = 4.8, d.f.= 1, two-tailed,p = 0.03).

To assess whether specific behavior patterns were used in reconciliationby non-kin male/female dyads, we compared the frequency of occurrence




Table I. Reconciliation patterns during the different contexts of interactions for male/female dyadsa

Contexts of interactions

Behavior First PC contacts Subsequent PC All MC contacts χ2

patterns (n = 82) contacts (n = 34) (n = 77) (d.f. = 2) p

Clasping 21.9 35.3 0 18.6 <0.001Hold-breast 4.9 14.7 0 5.4 n.s.Hold-bottom 13.4 11.8 0 9.4 <0.01Hold-back 3.6 8.8 0 4.2 n.s.

Mount 2.4 26.5 1.3 7.8 <0.025Sniffing 2.4 17.6 12.7 4.0 n.s.Bodily contact 41.4 14.7 54.4 5.5 n.s.Manual contact 18.3 20.6 22.9 0.05 n.s.Play 4.9 11.8 7.6 0.2 n.s.Grooming 8.7 5.9 30.4 5.4 n.s.

aFor each behaviour pattern, values are given as percentages of the number of interactionsbetween former opponents.

of each pattern for first PC contacts, subsequent PC contacts, and MCcontacts. Nine behavior patterns were distinguished (Table I). Hold-bottomand mount were the most used patterns of reconciliation by the capuchins.They are significantly more frequent in the PC than in the MC period; nostatistically significant difference appeared for the other patterns accordingto contexts of interactions (Table I).

When we considered PC-MC pairs between kins (N = 54), in additionto the former specific conciliatory behaviors, the capuchins used 2 otherbehavior patterns specifically for reconciliation: hold-back (first PC= 9.2%,subsequent PC = 12.3%, all MC = 0%; χ2 = 9.5; d.f. = 2; p = 0.008) andhold-breast (first PC = 23.7%, subsequent PC = 3.2%, all MC = 1.9%;χ2 = 10.1; d.f. = 2; p = 0.005). They preceded 56.4% of the conciliatoryclasping behaviors with a dance.

DISCUSSION

The results showed a high proportion of bidirectional conflicts. Thiswas also occurred in a group of wild white-faced capuchins, in which aggres-sive signals frequently elicited counter-aggression (Rose, 1994). In our studygroup, most bidirectional conflicts involved headflag behaviors by the ag-gressee. Conflicts involving physical contact were generally bidirectional andconflicts without physical contact were preferentially unidirectional. Kinshipappeared to enhance the proportion of bidirectional conflicts.




Aggressive interventions occurred in about one conflict out of four. Thisis consistent with previous studies in wild white-faced capuchins, in whichcoalitionary aggressions within and between sex classes involved specificagonistic alliance behavior: overlord (Perry, 1996b, 1997, 1998b).

With regard to postconflict behaviors, we demonstrated the occurrenceof reconciliation for kin and non-kin male/female dyads, which representedmore than half the dyads of the group and involved all group members.Perry (1995) could not definitely demonstrate the occurrence of reconcilia-tion. However, she argued that the equivocal results obtained in her studywere mainly due to the small data set (70 PC-MC pairs). Reconciliation oc-curs in many nonhuman primates. Considering methodological and evolu-tionary aspects, interspecific comparisons in conciliatory tendencies are valid(Kappeler and van Schaik, 1992). The overall conciliatory rate in white-facedcapuchins is within the ranges of species with moderate tendencies, such aslong-tailed macaques (Macaca fascicularis: Aureli et al., 1989). In browncapuchins (Verbeek and de Waal, 1997), affiliative postconflict behaviorsappeared less frequently than in white-faced capuchins. Such marked in-terspecific differences occur both in rate and form of reconciliation, evenamong congeneric species, e.g., in Macaca (Aureli et al., 1989, 1993, 2000;Chaffin et al., 1995; Demaria and Thierry, 1992; de Waal and Ren, 1988;Petit et al., 1997; Thierry, 1986, 2000).

Most reconciliations occurred in the first 2 min after a conflict, which issimilar to times reported for most other species (Kappeler and van Schaik,1992). However, in the wild, reconciliation in white-faced capuchins ap-pears to be significantly delayed, i.e., >30 min after the end of a conflict(Perry, 1995). Delayed reconciliation might be associated with the arboreallifestyle of the species: wild arboreal monkeys maintained great interindi-vidual distances while foraging (Phillips, 1995), and reconciliations might bepostponed until the group settled down for a long period (Verbeek and deWaal, 1997). But this argument differs from findings on other highly arborealmonkeys; in long-tailed macaques, the timing of reconciliation was similar inthe wild and in captivity (Aureli, 1992; Aureli et al., 1989). Relative delayedreconciliation (5–20 min following conflict) also occurred in a captive browncapuchin group (Verbeek and de Waal, 1997). Further studies, both in thewild and in captivity, are needed to know whether environmental conditionsinfluence the timing of reconciliation in capuchins.

Most primate species use no particular behavior pattern to reconcile(Aureli et al., 1989, 1993; Cords, 1988; Matsumura, 1996: York and Rowell,1988). Several behaviors—clasping and mount—were more frequently usedby white-faced capuchins in the context of reconciliation, as in chimpanzees(de Waal and van Roosmalen, 1979), Guinea baboons (Petit and Thierry,




1994a) and stump-tailed macaques (de Waal and Ren, 1988; de Waal andYoshihara, 1983).

In most cases, postconflict contacts involved more intense patterns thancontacts during the matched-control periods. Intense behaviors include so-cial grooming, mount, social play, and clasp accompanied by vocal expres-sions (Abegg et al., 1996; Petit and Thierry, 1994b). Our subjects showed par-ticularly intense reconciliatory contacts, such as hold-bottom and mounting.Similar sociosexual behaviors occur in wild white-faced capuchins (Mansonet al., 1997), mostly in socially tense situations such as conflicts (Baker, 1996;Perry, 1997). Clasping plays an important role in tension regulation in manyprimate species (Thierry, 1984), and it could be an index of interindividualtolerance in a social organization (de Waal, 1988). It could function as anappeasement mechanism when opponents are close to one another, and itmay prevent renewed attack (Call et al., 1999). Moreover, brown capuchins(Verbeek and de Waal, 1997) and white-faced capuchins (Perry, 1998a) com-monly exchanged postconflict signals that also occurred during their elabo-rate courtship behavior, which are accompanied by loud vocalizations, suchas grunts or an intense gargle. Like stump-tailed macaques, capuchins mayemit loud vocal signals during conciliatory reunions to announce the eventto the rest of the group and to draw other participants into the peacemakingprocess (de Waal and Ren, 1988). This hypothesis seems to fit the arboreallifestyle of capuchins: in dense tropical forest, loud vocalizations may in-form group members about important social events such as the end of aconflict.

Agonistic patterns and postconflict behaviors are related to the con-straints of the social organization of a species (Gore, 1992; Thierry, 2000).Many social characteristics appear to covary among macaque social organi-zations. The patterns of reconciliation, in particular, are correlated with theform of aggression and the asymmetry of dominance relationships. Broadercomparative projects aim to elucidate some of the evolutionary processesthat produced the social organizations (de Waal and Luttrell, 1989; Petitet al., 1997; Thierry, 1986, 1990). We need interspecific comparative studieson social behavioral patterns and variables in Cebus as we have for Macaca.Our results show that white-faced capuchins display a high rate of bidirec-tional conflicts and intense conciliatory behaviors. The behavioral patternsmay indicate a high level of interindividual tolerance, which is consistent withprevious studies of Cebus capucinus showing typical male tolerance and pro-tectiveness of infants (Rose, 1994) and alpha male tolerance of other malesto access to females (Fedigan, 1993). Cebus displays great variability in ge-netic, behavioral, life-historical and social characteristics, which makes themimportant for comparative research (Fragaszy et al., 1990).




ACKNOWLEDGMENTS

We thank Filippo Aureli, Susan Perry and Bernard Thierry for theirsuggestions and criticisims and Ana Maria Ducoing for correction of theEnglish.

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Aggression and Reconciliation in Cebus capucinus

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