Aggression and Reconciliation in Cebus capucinus

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

Affiliation Between Aggressors and Third Parties Following Conflicts in Long-Tailed Macaques (Macaca fascicularis)

Studies on cercopithecine monkeys have shown that soon after an agonistic conflict, victims have increased rates of affiliation with the agressor—reconciliation—but not with other group members. Postconflict affiliation is thought to function to restore disturbed relationships and to reduce social tension. This study on a captive group of long-tailed macaques (Macaca fascicularis) is focused on postconflict affiliative behavior of the aggressor. Increased rates of contact between female aggressors and kin of the victim occurred, as well as between female aggressors and their own kin. Furthermore, there were increased rates of contact between aggressors—males and females—and other group members. The increase in contacts with the victim's kin was selective, i.e., it could not be ascribed to the increased contact tendency with group members in general, and was not a side effect of the aggressor's proximity to the victim due to reconciliation. The increase in contacts with own kin was not selective. The fact that male aggressors do not have increased postconflict contacts with their kin or with kin of the victim is in agreement with the notion that males are less integrated in the nepotistic matrilineal network than females are. The fact that studies by others that focused on the victim evidence no increase in postconflict contacts with kin of the opponent or with other group members may be explained by the aggressor's larger influence over the postconflict situation: to reduce social tension, it might be more effective to affiliate with the aggressor than with the victim. Our findings emphasize that conflicts influence the behavior of other monkeys besides the direct contestants and, thus, indicate that the disturbance of social homeostasis is a matter of concern for all group members.     

Postconflict Behavior Among Male Japanese Macaques

Reconciliation was first described more than 20 years ago. Since then, it has been observed in many mammals (mainly primates) but data on postconflict behavior among males are still scarce because they usually aggressively compete for mating partners, rarely maintain amicable relationships with one another. Accordingly, reconciliation is expected to occur at low rates. Although this is true for Japanese macaque males, the subspecies on Yakushima Island (Macaca fuscata yakui) seems to represent an exception as grooming among males occurs often. We analyzed postconflict behavior among them and discuss the possible factors that may favor the occurrence of grooming and reconciliation. Selective attraction between former opponents—reconciliation—occurred soon after conflicts. Consolation—affiliative interactions between a focal animal and group members other than the former opponents occurring earlier in PCs than in MCs—was absent among males. Conciliatory tendency is higher for Yakushima macaque males (0.31) versus that in studies on the other subspecies Macaca fuscata. We discuss differences in the behavioral ecology of the 2 subspecies, the ecological and social factors that may favor the occurrence of reconciliation, and the possible benefits that males gain from grooming exchange and reconciliation.     

Nonconceptive Sexual Behavior in Bonobos and Capuchins

Sexual behavior by infecundable females, and by same-sex and adult-immature dyads, occurs in wild and captive bonobos (Pan paniscus). Proposed functions of these behaviors, in social primates generally, include practice, paternity confusion, exchange, and communication as well as appeasement. We used this framework to interpret and to compare observations of sexual behavior in a captive bonobo group and a wild white-faced capuchin (Cebus capucinus) group. In both species, (a) sexual behavior was no more frequent in cycling females than in pregnant or lactating females and (b) same-sex and adult-immature dyads engaged in as much mounting or genitogenital contact as adult heterosexual dyads did. The species differed in that (a) bonobos engaged in sexual behavior 65 times as frequently as capuchins, (b) only bonobos engaged in sexual contact other than ventrodorsal mounting during focal observation, and (c) bonobo sexual contact was concentrated most heavily in socially tense situations in adult female–female dyads, whereas capuchin sexual contact was concentrated most heavily in socially tense situations in adult male–male dyads. These data and published literature indicate that (a) practice sex occurs in both species, (b) paternity confusion may be a current function of C. capucinus nonconceptive sex, (c) exchange sex remains undemonstrated in capuchins, and (d) communication sex is more important to members of the transferring sex—female bonobos and male capuchins—than to members of the philopatric sex.     

Reconciliation in three groups of lion-tailed macaques

We studied postconflict behavior in three captive groups of lion-tailed macaques (Macaca silenus). After a conflict, we monitored the aggressee as the focal individual during a 10-min postconflict period and made control observations the following day on the same individual. Selective attraction between former opponents occurred in the first minutes of the postconflict period. The conciliatory tendency was relatively high, about 40%. Although no specific behavior was used to reconcile, postconflict contacts were especially intense and a rich repertoire of affiliative patterns was exihibited. With regard to the rate and form of reconciliation, lion-tailed macaques resemble Sulawesi macaques, which belong to the same phyletic lineage. We also discuss the possible interrelations between conciliatory patterns and other characteristics of social organization.     

Postconflict Behavior of Spectacled Leaf Monkeys (Trachypithecus obscurus). II. Contact with Third Parties

We studied the postconflict interactions with group members other than the former opponent in two groups of spectacled leaf monkeys. We found no evidence of redirection of aggression towards other group members. Victims and aggressors sought affiliative contacts with uninvolved third parties. There was no evidence for consolation—affiliative contact initiated by an uninvolved third party, directed towards victims of aggression—in either group when all affiliative behaviors were considered. However, embracing was a characteristic first-contact interaction between individuals involved in aggression and third parties. This finding mirrors the results concerning reconciliation in spectacled leaf monkeys. Accordingly, embracing may be a true consolatory behavior in this species. When contacts with third parties occurred before or in the absence of reconciliation, the timing of such contacts fell within the time window during which reconciliation normally occurs. These contacts also resulted in affiliation levels twice that of baseline levels, supporting the idea that these contacts may function as a form of substitute reconciliation. We discuss these results in light of recent theories concerning postconflict behavior in primates.     

Response Toward Novel Foods and Novel Objects in Wild Cebus apella

Animals respond to novel stimuli via explorative or neophobic behavior or both. The coexistence of these responses toward novel foods may be a successful adaptive strategy for a generalist species such as Cebus apella, because it allows the gradual introduction of new foods into the diet and reduces the risk of poisoning by ingestion of large amounts of toxic compounds (Glander, 1982; Milton, 1993; Visalberghi, 1994). Neophobia has been studied mostly in captivity. We investigated responsiveness to novelty in a group of 25–30 wild tufted capuchins (Cebus apella) in Iguazü National Park (Argentina). They had been habituated to visiting sites where bananas were provided on three elevated platforms. We presented novel stimuli on an adjacent platform. There were 4 experimental conditions with 10 sessions each: the Novel Food condition, the Novel Object condition, the Control condition, in which the platform was empty, and the Banana condition. In the Novel Food and Novel Object conditions, a new stimulus—food or object—was on the platform during each session. The Banana condition provided information on capuchin response to a familiar preferred food. Overall, capuchins were less responsive toward novel objects than toward novel foods; however, although cautious, they ate small amounts of the novel foods. Age affected individual responsiveness toward novel foods, whereas sex affected responsiveness toward novel objects. Capuchins ignored the empty platform. Our findings are in agreement with the idea that tufted capuchins can adapt to new habitats by gradually exploiting new food sources.     

Social Aspects of Fur-rubbing in <Emphasis Type="Italic">Cebus capucinus</Emphasis> and <Emphasis Type="Italic">C. apella</Emphasis>

Capuchins rub particular plant materials into their pelage, a behavior for which most authors have proposed a medicinal function (Baker in American Journal of Primatology 38:263–270, 1996, Baker, M. (1998). Fur Rubbing as Evidence for Medicinal Plant Use by Capuchin Monkeys (Cebus capucinus): Ecological, Social, and Cognitive Aspects of the Behavior. Dissertation thesis. University of California Riverside; DeJoseph et al. in Journal of the American Academy of Dermatology 46:924–925, 2002). Individuals fur-rub solitarily or in groups, but researchers have not conducted studies to understand the differences. We investigated the link between the form of fur-rubbing and other social variables in 2 capuchin species. We supplied 2 captive groups —white-faced capuchins and tufted capuchins— with citrus fruit and onions and explored the behavioral processes and social aspects underlying the activity. We documented the occurrence, number of participants, and effect of recruitment behaviors in fur-rubbing subgroups. We investigated the role of kinship, affiliation, and dominance relationships in accounting for fur-rubbing groups. There is a significant difference in the form of fur-rubbing between white-faced and tufted capuchins. White-faced capuchins fur-rubbed mainly in subgroups and performed a particular behavior to recruit prospective participants, whereas tufted capuchins fur-rubbed mainly alone, and showed no particular motivation to be joined by other group members. White-faced capuchins could fur-rub together frequently, whatever their degree of kinship, affiliation, or dominance interval. In tufted capuchins, fur-rubbing appeared to be significantly affected by kinship and dominance.     

Postconflict Behavior of Spectacled Leaf Monkeys (Trachypithecus obscurus). I. Reconciliation

Studies of postconflict behavior have focused on Old World primates, particularly on members of the cercopithecines and chimpanzees. We present data on patterns of reconciliation in two captive groups of spectacled leaf monkeys, members of the Colobinae. Reconciliation occurred at a high rate relative to that in other primate species and within the first minute following a conflict. Friendly postconflict contact was usually initiated by aggressors in one group, and by recipients in the other. But, there was no difference in postconflict initiative to contact in comparison with MCs. These two groups showed behavioral specificity in the context of postconflict reunions. Ventroventral embracing was a common, explicit (de Waal, 1993) form of reconciliation. The intensity of aggression and situations in which the victim responded aggressively had no effect on the likelihood of reconciliation occurring. The postconflict behavior of both groups lends further support to the relationship-quality hypothesis (Aureli et al., 1989). Kinship and rank distance and had no effect on reconciliation, though affiliation levels correlated positively with the tendency to reconcile. These results indicate that spectacled langurs are among the more tolerant of the species studied so far.     

Postconflict behavior among female Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in the Qinling Mountains, China

For group-living primates, the information on postconflict management is crucial for understanding primate competition and cooperation. However, such information is poorly known for snub-nosed monkeys, especially for wild populations. In this study, from September 2007 to June 2008, we investigated postconflict behavior among adult females Sichuan snub-nosed monkeys Rhinopithecus roxellana within one-male units in a wild, provisioned group in the Qinling Mountains of China by means of the time-rule method and the PC-MC method. We obtained a total of 81 PC-MC pairs and each individual was involved in only 0.004 aggressive behavior per observation hour. The first affiliative behavior was more likely to occur within the first minute after a conflict. The postconflict affiliative behaviors most often seen were contact-sit, embrace and grooming. The affiliative contacts between adult females occur due to selective attraction, I.e. Reconciliation. The pattern of postconflict affiliation demonstrates that the R. Roxellana belongs to a tolerant species.     

Monomorphic Region of the Serotonin Transporter Promoter Gene in New World Monkeys

Genetic variation in the human serotonin system has long been studied because of its functional consequences and links to various neuropsychiatric and behavior‐related disorders. Among non‐human primates, the common marmosets (Callithrix jacchus) and tufted capuchins monkeys (Cebus apella) are becoming increasingly used as models to study the effects of genes, environments, and their interaction on physiology and complex behavior. In order to investigate the independent functions of and potential interactions between serotonin‐related genes, anxiety and neuropsychiatric disorders, we analyzed the presence and variability of the serotonin transporter gene‐linked polymorphic region (5‐HTTLPR) in marmoset and capuchin monkeys. By PCR and using heterologous primers from the human sequence, we amplified and then sequenced the corresponding 5‐HTT region in marmosets and capuchins. The resulting data revealed the presence of a tandem repeat sequence similar to that described in humans, but unlike humans and other Old World primates, no variable length alleles were detected in these New World monkeys, suggesting that if serotonin transporter is involved in modulating behavior in these animals it does so through different molecular mechanisms. Am. J. Primatol. 74:1028‐1034, 2012. © 2012 Wiley Periodicals, Inc.     

Coping with Acute Crowding by Cebus apella

Traditionally, scientists believed that crowded housing conditions increased aggression in animals. Recent research on captive primates fails to support a linear relationship between population density and aggressive behavior. Our study is the first to investigate the effects of acute crowding on a New World primate. We observed brown capuchins (Cebus apella) under 2 different spatial conditions: a control that offered the full indoor space in the enclosure and a short-term experimental condition that restricted the capuchins to approximately half the amount of space of the control condition. We compared rates of self-grooming, aggression, contact sitting, social grooming, and play between both conditions. We conducted a mixed factorial ANOVA at the individual level while taking subject sex and age class into account. Intense aggression, play, and social grooming decreased significantly in crowded conditions, suggesting that capuchins avoid social encounters if spatially confined. Their strategy for coping with acute crowding via a decrease in all forms of social behavior is intermediate between chimpanzee and macaque strategies in similar experiments. The only behavior to increase under crowding was a nonsocial, self-directed behavior with the potential of reducing arousal: self-grooming.     

Why Be Vigilant? The Case of the Alpha Animal

We compared patterns of vigilance behavior in a male- and a female-dominant species—white-faced capuchins and ring-tailed lemurs—and used the results to test four hypotheses to explain vigilance behavior in primates. Adult male white-faced capuchins spent significantly more time vigilant than females did, and much male vigilance appeared to be directed toward males from other social groups. This finding supports the protection of paternity hypothesis. No sex difference existed in vigilance behavior among the ring-tailed lemurs, and subjects of both sexes exhibited more vigilance toward predators/potential predators than toward extragroup conspecifics, which supports the predator detection hypothesis. A trade-off argument, suggesting that females tolerate males in a group in return for greater male vigilance, does not apply to ring-tailed lemurs in our study. In both the male-dominant capuchins and the female-dominant ring-tailed lemurs, the alpha subject in the majority of the study groups was significantly more vigilant than other group members were. In white-faced capuchins, the alpha male mates more often than subordinate males do; therefore, the greater degree of vigilance exhibited by the alpha male may correspond to the protection of his reproductive investment. In ring-tailed lemurs, there can be more than one matriline in a group. Thus, the greater amount of vigilance behavior exhibited by the alpha female may be related to protection of her matriline, which could ultimately lead to greater inclusive fitness. Alpha subjects in our study groups exhibited certain behaviors more frequently or exclusively. Accordingly, there may be a constellation of behaviors characteristic of alpha animals.     

Carrying, Sharing, and Hand Preference in Tufted Capuchins (Cebus apella)

We examined the relationship among carrying, food-sharing, and hand preference in tufted capuchins (Cebus apella). The rationale was to evaluate further the use of Cebus as an alternative primate model to Pan for behavior relevant to early hominid evolution. We first examined bipedalism and food-sharing within an established social group, and then examined the direction and strength of hand preference for food carrying in an expanded sample. Several aspects of capuchin behavior warrant discussion. First, bipedal carrying and food-sharing occurred more frequently when we provided bulky foods than when we provided smaller foods. Second, food-sharing was characterized by passive tolerance, rather than active giving, between subjects. Third, subjects shared food primarily with immatures and followed a pattern of reciprocal exchange. Finally, we found no evidence for population-level hand preference for carrying. We posit that an array of behavioral similarities among Cebus, Pan, and Homo evolved through convergent processes, and in this regard capuchins can be seen as an alternative primate model to chimpanzees for the evolution of early hominid behavior.     

Reconciliation in Captive Chimpanzees: A Reevaluation with Controlled Methods

Affiliative postconflict reunions—reconciliations—of former opponents were first demonstrated in the chimpanzees at the Arnhem Zoo. Since then methods have been considerably refined, and reconciliation has been demonstrated in a large number of primates and also some gregarious nonprimates. This study, conducted with a different captive group, is the first to use the revised methodology with chimpanzees. We analyzed a total of 297 agonistic conflicts with the PC–MC method: we observed focal individuals for 15 min after a conflict and during matched control observations the next day. The mean conciliatory tendency of the 16 chimpanzees was 41%, with a range in different age-sex classes of 58% (among adult females) to 19% (among adult vs. immature males). After conflicts, former opponents were selectively attracted to one another. Preferential contact with previous opponents persisted when activity level during matched controls was controlled for statistically. Opponents that were frequent grooming partners reconciled more frequently, but the frequency of agonistic support had no such effect. Our findings thus confirm the existence of reconciliation in chimpanzees, which show one of the highest conciliatory tendencies among primate species.     

Conflict and postconflict behaviour in captive black-and-white snub-nosed monkeys (<Emphasis Type="Italic">Rhinopithecus bieti</Emphasis>)

Black-and-white snub-nosed monkeys (Rhinopithecus bieti) have almost never been the subject of any behavioural observations in captivity. This study was aimed at providing preliminary information about agonistic and reconciliation behaviour in a group kept at the Kunming Institute of Zoology in China. Established procedures were used for this investigation (i.e., the postconflict/matched-control method and the time-rule method). Intra-group aggression rates were quite low. Postconflict affiliation as well as selective attraction of former opponents to each other following conflicts was demonstrated. Former opponents contacted each other earlier in postconflict periods than in matched-control periods. The average conciliatory tendency of all focal individuals combined was 54.5%. After an agonistic interaction, the first affiliative contact between former aggressors usually took place within the first minute. The behaviours most often shown as first affiliations after a conflict were body contact, mount, touch, and hold-lumbar, of which the latter is an explicit reconciliatory gesture. Furthermore, the adult male intervened non-aggressively in 84% of all conflicts (n=25) among the adult females. Overall, the patterns of aggression and reconciliation observed in R. bieti bear many of the traits that characterise tolerant primate species.     

Scratching as a Window into the Emotional Responses of Wild Tufted Capuchin Monkeys

Emotional responses to social interactions and the associated behavioural measures (e.g., self‐directed behaviours, SDBs) have been little studied in New World monkeys, especially in wild settings. In this study, we investigated the factors affecting anxiety in a wild group of tufted capuchin monkeys (Cebus apella nigritus) using self‐scratching (hereafter scratching) as its measure. Scratching was more strongly affected by the social context than by individual characteristics. Indeed, inter‐individual variability was not explained by the age, sex and dominance rank of the monkeys. The monkeys scratched themselves more often when being distant from other group members than when in close proximity with them, suggesting that even short‐distance separation from group members may be an important factor affecting capuchins emotional response. The risk of receiving aggression seemed also to elicit anxiety, as scratching was higher when in proximity to more dominant individuals and females, which were the categories of group members that were more aggressive. By contrast, scratching was lower when in proximity to more secure partners, like kin. Finally, scratching rates following the receipt of aggression were higher than at baseline, indicating a post‐conflict increase in anxiety. Overall, our results contribute to the understanding of the factors affecting emotional responses in capuchin monkeys, confirming and expanding previous findings in other animal species.     

Hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella)

The purpose of this study was to examine the hierarchical complexity of combinatorial manipulation in capuchin monkeys (Cebus apella). Two experiments were conducted. In Experiment 1 capuchins were presented with an apparatus designed to accommodate the use of probing tools. In Experiment 2 the same capuchins were presented with sets of nesting containers. Five of the ten subjects used probing tools and seven subjects placed objects in the containers. The capuchins' behavior reflected three hierarchically organized combinatorial patterns displayed by chimpanzees and human infants. Although the capuchins sometimes displayed the two more complex patterns (“pot” and “subassembly”), their combinatorial behavior was dominated by the simplest pattern (“pairing”). In this regard capuchins may not attain the same grammar of manipulative action that has been reported for chimpanzees and young human children. © 1994 Wiley-Liss, Inc.     

True anting by the capuchin,Cebus capucinus

I observed capuchins (Cebus capucinus) putting ants (Camponotus sericeiventris) in their fur at Corcovado National Park, Costa Rica. The behavior was similar to “anting” in passerine birds. The literature on anting in birds is reviewed and compared with the relevant references on self-annointment behavior in mammals.     

Activity Patterns,Home Range Size,and Intergroup Encounters in <Emphasis Type="Italic">Cebus albifrons</Emphasis> Support Existing Models of Capuchin Socioecology

Variation in ranging behavior, social organization, and feeding ecology among capuchins (Cebus spp.) is a classic example of how closely related species may be differentially adapted to their local environments. Marked differences in all 3 areas occur among Cebus spp. between the untufted capuchins (Cebus capucinus, C. olivaceous, and C. albifrons) and the tufted capuchins (C. apella, C. xanthosternos, C. nigritus, and C. libidinosus). The key socioecological distinction between the 2 groups has traditionally been that, compared with the tufted group, untufted capuchins eat more ripe foods, as befits their more gracile masticatory system; range more broadly in search of high-quality foods; and live in larger groups with more males and more agonistic interactions between groups. Here I assess how well the basic socioecological characteristics —activity budget, ranging— of previously unstudied Ecuadorian Cebus albifrons fit within this model. Few researchers have conducted studies on Cebus albifrons, despite its prominent role in the initial development of the model for socioecology of Cebus. The results of my 1-yr study of a single social group support the model’s general characterization of untufted capuchins in ranging and feeding behaviors, but also suggest that direct ecological and demographic effects, in addition to adaptation to local conditions, may explain additional variation in group size across species of Cebus.