Kinship,association, and social relationships in rhesus monkeys (Macaca mulatta)

Data on social interactions with matrilineal kin were collected from two groups of rhesus monkeys for 6 years. All behavioral states, including time within one meter of another, involved kin more often than would be expected by chance. Significant associations were also found between kinship and the frequencies of various forms of agonistic as well as affiliative acts. Frequency of social interaction, however, was not a simple function of time in proximity. Although animals spent more time with kin than nonkin they had more aggressive interactions with kin. Moreover, aggression was biased toward the more serious forms of expression in interactions with kin. Time spent in association was neither predictive of the rate of aggressive interaction nor reduced by high rates of aggressive interaction. Rather than association time influencing rates of interaction, association time may be the consequence of a history of aggressive and affiliative exchanges. Preferential association and high rates of aggressive interaction with kin may be possible due to the existence of compensating social mechanisms nullifying the negative influence of specific aggressive encounters. © 1993 Wiley-Liss, Inc.     

Acute changes in social composition and agonistic behavior in male vervet monkeys (Cercopithecus aethiops sabaeus)

Among nonhuman primates the composition of social groups influences the interactions of group members. We assessed the effects of acute changes in social composition on behavior among 15 adult male vervet monkeys (Cercopithecus aethiops sabaeus). Subjects were observed in their basal social groups which comprised 3 adult males, 2–4 adult females, and offspring; and in two subgroups consisting of either two or three adult males. Agonism and vigilance increased in smaller groups relative to basal conditions, while subjects in two-male groups displayed more aggression than those in three-male groups. These findings suggest that, among male vervet monkeys, acute disruption of stable social groups increases aggressive behavior, and that the amount of agonism is influenced by the composition of the consequent subgroups. © 1992 Wiley-Liss, Inc.     

Grooming, social bonding, and agonistic aiding in rhesus monkeys

An analysis of simultaneous grooming bouts in a captive group of rhesus monkeys (Macaca mulatta) failed to provide evidence of competition to groom high ranking partners. Not only were grooming supplantations rare, but the highest ranking individuals performing grooming did not groom the highest ranking animals receiving grooming. Lower ranking partners, however, did more grooming in nonkin dyads. Grooming partners aided one another in agonistic episodes, but the individual receiving the aid did not groom the individual providing the aid more than vice versa. Kin dyads did aid and groom one another at greater than expected rates, but the aider did not receive the greater proportion of grooming in the dyad. Males participated in more grooming than expected, but their grooming was not related to aiding either with regard to one another or female partners. Animals that were targeted in joint aggression, or aided against, received significantly less grooming from their opponents. A general social relationship expressed in partner preferences, social grooming, and agonistic aiding better explained the observed pattern than any model based on the exchange of services for favors in different currencies.     

Reciprocity in play,grooming, and proximity in sibling and nonsibling young rhesus monkeys

Play, grooming, and proximity, and the degree to which these were reciprocated between pairs, were studied in immature sibling and nonsibling rhesus monkeys (Macaca mulatta)in four established captive groups over two seasons. “Interaction reciprocity” and “partner reciprocity” were assessed for each dyad for each of the three behaviors. In play, interaction reciprocity was based on the ratio between the play initiations by each dyad member,in grooming on the ratio between the grooming durations by each dyad member, and in proximity on the relative responsibility for proximity maintenance. Two or three most frequent (top) partners for each behavior were found for each individual. If two monkeys were among each other’s top partners, they were said to be reciprocal partners. Monkeys played with nonsiblings as much as with siblings but spent more time grooming and in proximity with siblings than with nonsiblings. Same-age nonsiblings (peers) were more frequent partners than other nonsiblings for each behavior. Siblings’ grooming interactions were more reciprocal than those of nonsiblings. There was no such effect for play and proximity. All-male dyads tended to be more reciprocal in play interactions, and all-female dyads tended to be more reciprocal in grooming interactions. In play, but not in grooming or proximity, the interaction reciprocity of reciprocal partners was higher than that of nonreciprocal dyads. It is argued that the three behaviors have similar roles in infant’s social development but they differ in the expression of this role. Hence the reciprocity patterns vary with the behavior.     

Importance of cooperation and affiliation in the evolution of primate sociality

The idea that competition and aggression are central to an understanding of the origins of group‐living and sociality among human and nonhuman primates is the dominant theory in primatology today. Using this paradigm, researchers have focused their attention on competitive and aggressive behaviors, and have tended to overlook the importance of cooperative and affiliative behaviors. However, cooperative and affiliative behaviors are considerably more common than agonistic behaviors in all primate species. The current paradigm often fails to explain the context, function, and social tactics underlying affiliative and agonistic behavior. Here, we present data on a basic question of primate sociality: how much time do diurnal, group‐living primates spend in social behavior, and how much of this time is affiliative and agonistic? These data are derived from a survey of 81 studies, including 28 genera and 60 species. We find that group‐living prosimians, New World monkeys, Old World monkeys, and apes usually devote less than 10% of their activity budget to active social interactions. Further, rates of agonistic behaviors are extremely low, normally less than 1% of the activity budget. If the cost to the actors of affiliative behavior is low even if the rewards are low or extremely variable, we should expect affiliation and cooperation to be frequent. This is especially true under conditions in which individuals benefit from the collective environment of living in stable social groups. Am J Phys Anthropol 128:84–97, 2005. © 2005 Wiley‐Liss, Inc.     

Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support

Social primates spend a significant proportion of their time exchanging grooming with their group companions. Although grooming is mainly exchanged in kind, given its hygienic and tension-reducing functions, it is still debated whether grooming also provides some social benefits, such as preferential access to resources (e.g., food or mating partners). In this study we analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima. We tested the tendency of monkeys to reciprocate the amount of grooming received, and to direct their grooming up the hierarchy. Then we analyzed the relation of grooming to three of its possible benefits: reduced aggression, increased tolerance over food, and agonistic support against a male aggressor. The data were analyzed by means of row-wise matrix correlations. Grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both the study groups. No significant relationship was found between grooming and aggression. Conversely, grooming favored tolerance over food, since it was positively correlated with presence on the same food patch, close proximity, and close approaches (both within 1 m) during feeding. Grooming was also positively related to agonistic support against adult males, although this relationship became nonsignificant when we controlled for kinship. Although these results are not definitive, they suggest that monkeys may derive various social benefits from grooming. This conclusion is supported by the fact that in various primate species animals tend to prefer high-ranking individuals as grooming partners.     

Food sharing and affiliation: An experimental and longitudinal study in cockatiels (Nymphicus hollandicus)

Food sharing has attracted much attention because of its apparently altruistic nature and its link to prosociality. However, food sharing has been mostly studied in a reproductive context, during courtship and parental care, where the fitness benefits are obvious. We still lack a clear understanding of the functions of food sharing outside any reproductive context and within social groups of same‐aged peers. Previous studies suggest that cofeeding, the action to let another animal feed from the same monopolizable food source, may be used to build and strengthen bonds between individuals. This may be particularly crucial in social birds forming long‐term associations between mates or siblings such as psittacids and corvids. Here, we investigated food sharing and affiliative behaviors such as allopreening in a psittacine species, namely in a group of captive juvenile cockatiels (Nymphicus hollandicus) consisting of five siblings and five unrelated birds. Our main objective was to study the developmental pattern of food sharing over time and its implication in social bonding depending on kinship, affiliation, and sex. Studying cockatiels in this context is providing many new information since most of the studies on food sharing in birds focused on corvids. We found that, contrary to jackdaws, cockatiels continued to share food with multiple individuals, although the frequency of cofeeding as well as the number of cofeeding partners decreased over time. Cockatiels shared more food with their siblings than with other conspecifics but they were not more likely to do cofeeding with birds of the opposite sex. We also found evidence that young cockatiels exchanged more food with those from whom they received food (reciprocity) and, to a lesser extent, allopreening (interchange), than from other cockatiels. Our findings suggest that in cockatiels, food sharing within social groups serves the formation (and maintenance) of affiliative bonds, especially between siblings, rather than pair bonds, but might additionally be explained by reciprocity, interchange, and harassment avoidance.     

Affiliative relationships between adult males and immature group members in naturally occurring ringtailed lemurs (Lemur catta)

Affiliative relations between adult males and immature group members were studied in three naturally occurring groups of ringtailed lemurs (Lemur catta) over a 12-month period at Beza-Mahafaly Reserve, southwestern Madagascar. No statistically significant difference was found in rates of affiliative interactions between adult males and older immatures (juveniles and adolescents) over reproductive seasons. However, some of the adult males in two focal groups increased their rates of affiliative behaviors with older immatures during the lactation and subsequent 1993 postmigration periods. Female involvement with infants during lactation season, the increasing independence of juveniles and adolescents, and length of male tenure may be factors contributing to such a pattern. Neither adult males nor immatures were significantly responsible for the initiation and maintenance of proximity in male-immature dyadic interactions. Neither dominance rank nor age-class of the adult male affected their rates of affiliative behavior with immatures. The majority of focal males exhibited an interest in infants and occasionally participated in alloparental care. It is suggested that adult males can benefit from affiliative relations with immatures in terms of opportunities for greater spatial centrality in the group, which can lead to enhanced predator protection and greater opportunities to develop affiliative relationships with females. Immatures can benefit from affiliation with males in relation to enhanced predator detection and protection, alloparental care, and opportunities to develop social skills. Am J Phys Anthropol 103:163–171, 1997. © 1997 Wiley-Liss, Inc.     

Infant-directed behavior in young rhesus monkeys: Sex differences and effects of prenatal androgens

Young (3–4 years old) laboratory-reared rhesus monkeys were observed in five 15-minute tests with 1–15-day-old infants. Males and females were equally likely to investigate infants. Females communicated more with infants by grin-lipsmacking and gurgling–-gestures that were not shown by any males. More females presented the ventrum to infants than did males. Females contacted infants more than did males by grooming, crouching over, and having full body contact with them. To see whether prenatal androgens produced the male pattern of response, we conducted similar tests with pseudohermaphrodites (prenatally androgenized genetic females) and neonatally castrated males. On most sexually dimorphic behaviors, pseudohermaphrodites behaved more like females than like males. Castrated males, like females and pseudohermaphrodites, crouched over infants more than did intact males. Castrated males differed from females only on one infant-directed response, the grin-lipsmack. These comparisons showed that defeminization of the repertoire of infant-directed responses was measurable only in intact males. We conclude accordingly that prenatal androgens alone are not responsible for defeminization of this repertoire and that a contribution from postnatal androgens is likely to be necessary.     

Peaceful primates: affiliation, aggression, and the question of female dominance in a nocturnal pair-living lemur (Avahi occidentalis)

Affiliation/agonism and social dominance are central factors determining social organization in primates. The aim of our study is to investigate and describe, for the first time, the intersexual relations in a nocturnal and cohesive pair‐living prosimian primate, the western woolly lemur (Avahi occidentalis), and to determine to what extent phylogeny, activity mode, or the cohesiveness of pair partners shape the quality of social interactions. Six pairs of western woolly lemurs were radio‐collared in the dry deciduous forest of northwestern Madagascar. More than 874 hr of focal animal sampling were conducted. All occurrences of social interactions involving a focal animal were recorded. The rate of affiliation between pair partners was significantly higher than the rate of agonism. Western woolly lemur pairs' interactions were extremely peaceful. All decided agonistic conflicts (N = 15) were exclusively initiated and won by the female. No female showed spontaneous submission toward her male partner. These results are in line with those of diurnal cohesive pair‐living anthropoid primates. Findings support the hypothesis that social relations in pair‐living primates are linked to the cohesiveness of pair partners in time and space irrespective of phylogeny and activity mode. Am. J. Primatol. 73:1261–1268, 2011. © 2011 Wiley Periodicals, Inc.     

Adjustments and adaptations to indoor and outdoor environments: Continuity and change in young adult rhesus monkeys

Optimal environments for captive primates are assumed to be those which simulate certain ecological features and elicit a wide range of species-typical behavior patterns. Outdoor environments are often thought to be more suitable than indoor environments in that they provide more space and potentially higher levels of stimulation. The purpose of this study was to compare the long-term behavioral responses of several groups of animals that had been reared identically during the first two years of life and then exposed to different environments. Two groups were moved into separate “enriched” indoor pens while one group was moved to an outdoor area covering approximately 5 acres. The monkeys were observed during the first year of life and again in these different environments between the ages of 6 and 10. Although behaviorally similar during the first year of life, monkeys developed different response patterns to indoor and outdoor environments. Contrary to commonly held views, indoor monkeys were not more aggressive, nor did they show higher levels of stereotypical behavior. Instead, indoor monkeys exhibited higher levels of grooming, sexual posturing, tactile/oral exploration, and passive visual behavior than their outdoor counterparts. These differences are consistent with the reconciliation model of de Waal. Individual monkeys also showed remarkable stability in certain traits over the 5-year period. © 1992 Wiley-Liss, Inc.     

The influence of behavioral context and social characteristics on the physical aspects of social grooming in rhesus monkeys

The extent to which dominance status and sex can influence the physical act of grooming was examined in two groups of rhesus monkeys. Both the sex and the dominance status of the groomee, but not of the groomer, were found to affect the body sites groomed and the positions assumed by the animals during the grooming bout. Females were groomed more on the back and head and less on the tail, rump, upper leg, and lower arm than males. Females with infants tended to face away from the groomer. Higher-ranking groomees were groomed more on the tail and rump and less on the upper leg and back than lower-ranking groomees. Higher-ranking groomees spent more time lying down during grooming than lower-ranking groomees, while lower-ranking groomees faced away from the groomer more then higher-ranking groomees. The behavioral interactions just prior to and immediately after grooming were also recorded. Although the onset of grooming was preceded by social interactions between the partners, the end of grooming was followed by a complete break in interactions. Particular types of social signals displayed by the groomee just prior to grooming were highly correlated with the grooming of specific body sites. These results suggest that the groomee controls the behavior of the groomer by the social signals it displays and the positions it maintains during the grooming bout. Thus, the grooming act itself may play an important role in the social relationships between group members.     

Dominance hierarchy and social relationships in a group of Captive black-and-white snub-nosed monkeys (Rhinopithecus bieti)

Different types of dominance hierarchies reflect different social relationships in primates. In this study, we clarified the hierarchy and social relationships in a one-male unit of captive Rhinopithecus bieti observed between August 1998 and March 1999. Mean frequency of agonistic behaviour among adult females was 0.13 interactions per hour. Adult females exhibited a linear hierarchy with a reversal of 10.9%, indicating an unstable relationship; therefore, R. bieti appears to be a relaxed/tolerant species. The lack of a relationship between the agonistic ratio of the adult male towards adult females and their ranks indicated that males did not show increased aggression towards low-ranking females. Differentiated female affiliative relationships were loosely formed in terms of the male, and to some extent influenced by female estrus, implying that relationships between the male and females is influenced by estrus and not rank alone. A positive correlation between the agonistic ratio of adult females and their ranks showed that the degree to which one female negatively impacted others decreased with reduction in rank. Similarly, a positive correlation between the agonistic ratio of females and differences in rank suggests that a female had fewer negative effects on closely ranked individuals than distantly ranked ones. These data indicate that rank may influence relationships between females. A steeper slope of regression between the agonistic ratio and inter-female rank differences indicated that the extent of the power difference in high-ranking females exerting negative effects on low-ranking ones was larger during the mating season than the birth season, suggesting that rank may influence the mating success of females.     

Relation between the dominance rank of female rhesus monkeys and their access to males

Systematic observations were made on 12 measures of the sexual, aggressive, and social interactions of 24 male–female pairs of rhesus monkeys in six social groups, each consisting of one male and four ovariectomized females tested in a large room. Each female in a group was treated in turn first with estradiol alone and then with estradiol and progesterone in combination. When hormone-treated, the female was also observed during pair tests with the male in the same large observation room (four males, eight females, 240 group tests, 240 pair tests). The dominance ranks of females during group tests were determined post hoc by means of the dominance index [Zumpe & Michael, American Journal of Primatology 10:291–300, 1986]. In all six groups, the most dominant female virtually monopolized the male, and the subordinate females' interactions with the male, assessed during pair tests, were almost completely suppressed during group tests. This “dominant female effect” was a robust phenomenon that depended solely on female dominance rank. It was independent of the identity and hormonal status of females and of the social preferences of males as expressed in pair tests. These findings demonstrate the existence of female mate competition in an Old World primate.     

The neuroscience of affiliation: forging links between basic and clinical research on neuropeptides and social behavior

Animal studies point to the role of two neuropeptides-oxytocin and vasopressin-in the regulation of affiliative behaviors including mating, pair-bond formation, maternal/parenting behavior, and attachment. These findings may have important implications for understanding and treating clinical disorders marked by social deficits and/or disrupted attachment. This review focuses on advances made to date in the effort to forge links between basic and clinical research in the area of neuropeptides and social behavior. The literature on oxytocin and its involvement in stress response, affiliation, and prosocial behavior is reviewed, and the implications of these findings for such disorders as autism as well as other social and stress-related disorders including social phobia, post-traumatic stress disorder, and some personality disorders are considered. Finally, unresolved issues and directions for future research are discussed.     

Seasonal breeding in rhesus monkeys: Influence of the behavioral environment

The accepted model of breeding seasonality in rhesus monkeys states that females become reproductively active in response to an environmental cue and that males become sexually active in response to ovulating females. This model must be modified to include direct responses of the male to the physical environment, endocrine responses of males to sexual activity, and responses of the female to the sexual activation of fellow group members. The complex set of social stimuli that influences the breeding readiness of both sexes may serve to delimit more precisely the annual periods of conception and birth than would be the case if each individual responded only to the changing physical environment.