Development of partner preferences in Japanese Macaques (Macaca fuscata): Effects of gender and kinship during the second year of life

Quantitative data are presented on the effects of subject sex, partner sex,and kinship on the social interactions of 18 juveniles of the Oregon troop of Japanese macaques (Macaca fuscata).Data on these subjects as infants were also used to detail maturational changes in partner sex preferences. Nine males and nine females, whose multiparous mothers represented a cross section of dominance ranks, were observed using a focal-animal technique. Juveniles of both sexes engaged in more proximity, contact, grooming, mounting, aggression, and social play with kin than with nonkin partners. They initiated less contact with females and more contact with males during their second year. They initiated more grooming and aggression during their second year than their first year, with females displaying a strong preference for grooming females and males specifically aggressing males more during the second year. Aggression was higher between same-sexed partners than between opposite-sexed partners. Males engaged in more social interactions with males during the second year than the first year of life. Males played more than females during both years. Males played more with males during the second year than the first year, and males played with males more than did females during the second year. We conclude that sex differences in behavioral frequencies become evident during the first year of life, and sex differences in partner preferences emerge during the second year of life.     

Grooming behavior of spider monkeys (Ateles geoffroyi) on barro colorado Island,Panama

Quantitative grooming data are presented for free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Republic of Panama. A total of 126 grooming sessions was recorded, with an average session length of 2.0 min (range, 0.1 to 10.0 min). Grooming was an infrequent behavior; on average, individuals allocated only 2.5% of their daily activity to grooming. Two daily peaks of grooming activity were observed, one near midday and another in the late aftermoon between 1600 and 1700. Adult females groomed most frequently, followed by males and then juveniles. Juveniles were the most frequent recipients of grooming, followed by females and then males. Individual preferences were observed primarily between mother-offspring, male-male, and juvenile-male grooming partners in this male-bonded fission-fusion, species. Grooming interactions reflect many of the social characteristics of spider monkey societies: intraclass grouping preferences, long period of juvenile dependence, male philopatry, and female dispersal.     

Grooming Partners of Immature Blue Monkeys (Cercopithecus mitis) in the Kakamega

I report results of a 4-year study, which profiles grooming partners of immature blue monkeys in a Kenyan rain forest. The analysis focuses on the degree to which mothers and offspring were preferred grooming partners and on sex differences in grooming partners. Subjects ranged in age from 0 to 6 years and were members of one study group in which kinship relations were known from long-term study. Immatures often had their mothers as the top-ranked partner. Even more reliably, however, adult females had their offspring as top-ranked immature partners. As offspring grew older, they tended to fall in the rank ordering of their mothers' immature grooming partners, especially when younger siblings were born. Immature males had fewer grooming partners overall than female peers did. Thus, immature females diversified their partners more than males did, especially by establishing grooming relations with immature female partners. Immatures of both sexes had more female partners than expected by chance. Observed sex differences suggest that immature female blue monkeys may use grooming to cultivate relationships with long-term future benefits. It is less clear that the grooming of immature males functions in this way. Immatures of both sexes may also use grooming to maintain relationships of current value, to practice for future social exchange, and to keep clean, and some of their grooming may be in the primary interest of their partners, rather than themselves. In general, immature blue monkeys resemble the immatures of other catarrhine taxa in the way in which grooming is distributed among various partners.     

Agonistic Interactions of Juvenile Savanna Baboons

19 juvenile members of known genealogies in two wild baboon groups were studied over a 16-month period to compare the ontogeny of agonistic experience and dominance relations for males and females. Juveniles of all age-sex classes were disproportionately likely to receive aggression from and submit to adult males per unit of time spent in proximity. This pattern intensified with increasing juvenile age. With age, juvenile females more often submitted to unrelated adult females from higher-ranking families, whereas this was not true for juvenile males. All juveniles received aggression from older group members more often during feeding than was expected by chance. High rates of agonistic interaction with unrelated adult females accounted for old juvenile females (3–5.5 years-old) interacting agonistically more frequently than male age peers and young juveniles of either sex (1–2.5 years-old). Adult females were also more aggressive toward females among young juveniles, suggesting that adult females target females among juveniles for aggression and resistance to rank reversal. Within juvenile age groups, males dominated all females and all younger males, irrespective of maternal dominance status. Dominance relations among female age-peers were generally isomorphic with relations among their mothers. No juvenile targeted any older male for rank reversal. Males targeted all older females, whereas females typically targeted only older females from families lower-ranking than their own. The strong sexual dimorphism in adult body size in baboons may explain why juvenile males' dominance relations with peers and adult females are not structured along lines of family membership as is true for the less dimorphic macaques. Acquisition of higher agonistic status probably allows juveniles of both sexes to increase their success in within-group feeding competition during late stages of juvenility, which, in turn, could affect important life-history traits such as age at menarche and adult body size.     

Patterns of affiliation among immature rhesus monkeys (Macaca mulatta)

The affiliative interaction patterns of the immature members of a group of rhesus monkeys at the Yerkes Regional Primate Research Center reflected a strong bias toward matrilineal kin, although this effect was modified by age and sex variables. Association with kin decreased with age, particularly for males. Juvenile males showed less of a kin bias in their behavior than did juvenile females, especially for grooming. Juvenile males also exhibited a preference for interaction with other males. The diminished association with kin and the same-sex bias may be reinforced in adolescence as adult males begin to aggressively target adolescent males involved in agonistic encounters with females or immatures. Adolescent males did not decrease their levels of social interaction relative to those of adolescent females; however, these males preferentially associated with other males (predominantly their own age-sex class) and specifically avoided females and younger animals, both kin and nonkin. Avoidance may diminish conflicts with females or immatures which could result from association, thereby decreasing the potential for selective aggressive interference by adult males. Juvenile and adolescent females maintained strong ties with their kin and preferentially associated with other females and immatures. The breadth of interaction of females with other females may facilitate the establishment of dominance relationships as females mature. Familiarity and predictability may also decrease the necessity of more severe agonistic interaction.     

Social behavior of infant and mother Japanese Macaques (Macaca fuscata): Effects of kinship,partner sex,and infant sex

The behavioral interactions of 22 infant and mother Japanese macaques with other group members were studied. Focal-animal observations were made from the time of each infant’s birth until 1 year of age. Infants and mothers both displayed exceedingly strong preferences for associating with matrilineal kin and, specifically, for female kin. The degree of genetic relatedness was positively correlated with levels of spatial proximity, contact, grooming, aggression, and play. Overall frequencies of interactions with nonkin were very low, and partner sex was not an important factor in interactions with nonkin. There were no significant differences between male and female infants in interactions with kin versus nonkin. There was only one significant difference between male and female infants in interactions with males versus females: female infants showed stronger preferences for initiating proximity with females over males than did male infants. Because mothers provide the focal point for infant interactions during the first year of life, we compared the behavior of infants and mothers. Mothers were the recipients of more social interactions than were infants, mothers engaged in more grooming than did infants, and infants engaged in more social play than did mothers. These findings are only partially consistent with kin-selection theory, and the inadequacies of studying matrilineal kin discrimination to test kin selection are reviewed. The near-absence of infant sex differences in associations with social partners suggests that although maternal kin other than the mother are important to infant socialization, they probably do not contribute to the development of behavioral sex differences until after the first year of life.     

Social segregation in male,but not female yearling rhesus macaques (Macaca mulatta)

Males and females of many species sex‐segregate, ranging from complete separation of habitats to social segregation within the same space, sometimes varying across seasons and lifespan development. Mechanisms for such segregation are not well understood, though some have suggested that sex differences in preferred juvenile behaviors lead to greater behavioral compatibility within than between sexes. This within‐sex behavioral compatibility may be the source of sex‐segregation. As juvenile behavioral sex differences are well‐documented in rhesus monkeys, we examined sex‐segregation patterns of yearling rhesus monkeys engaged in three different types of behavior: rough play, parallel play, and grooming. We observed male and female rhesus yearlings from five stable long‐term age‐graded social groups of 67–183 animals. Behavioral observations were designed to collect equal numbers of rough play, grooming, and parallel play bouts. In addition, sex composition and proximity to adults was recorded for each bout. Across all behaviors, more all‐male groups and fewer mixed sex‐groups were observed than expected by chance. All‐female groups occurred at the level expected by chance. Thus, males sex‐segregated regardless of type of behavior, while females did not sex‐segregate. Female groups were observed in proximity to adults more often than expected by chance. These results suggest that behavioral compatibility may produce sex‐segregation in male yearling rhesus monkeys, possibly preparing males and females for different social roles and segregation as adults. Am. J. Primatol. 72:87–92, 2010. © 2009 Wiley‐Liss, Inc.     

Quantitative observations of grooming behavior in free-rangingMacaca mulatta

Quantitative methods of observation and analysis were used in a 12-month study of grooming behavior of free-rangingMacaca mulatta on La Cueva Island at La Parguera, Puerto Rico. Observations lasting 30–120 minutes were made from eight positions on the island at a standard time of day when monkeys were either feeding or resting. Two dependent variables were obtained: (1) the number of monkeys present in the observation area were noted by age and sex class at five-minute intervals throughout each observation, and (2) the frequency of grooming encounters was tabulated by the age and sex class(es) of groomer and recipient. These data were computed as grooms/hour/possible interacting combination of monkeys. Grooming frequencies were higher in non-feeding situations than when monkeys were feeding. The largest social group had the lowest mean grooming rates, while the smallest group had the highest grooming frequencies. More grooming occurred during the November-to-February mating season than at other periods of the year. Adult females were involved in over 60% of all grooming behavior, juveniles participated in 25% of the grooming, while adult males groomed females, primarily during the mating season, and rarely groomed other males or juveniles. Genealogical relationships, levels of group aggression and the feeding or resting context all influenced the frequency of grooming. This study provides support for the hypothesis that the basic social unit for rhesus macaques consists of a core of adult females with their juvenile and infant progeny.     

Activity and ranging patterns of Colombian woolly monkeys in north-western Amazonia

In this study, I revise three aspects of the socioecology of woolly monkeys (genus Lagothrix) that might give us a better understanding of the patterns found in this species: (1) the association between temporal variation in fruit abundance and diet, activity, and ranging patterns; (2) the individual trade-offs associated with living in small or large groups, and (3) the relationship between social dominance and foraging success. Using behavioral and ecological data collected during 3 years in Tinigua Park, Colombia, I found that woolly monkeys tend to avoid open-degraded forests, where fruit production is generally lower than it is in mature forests. Diet and activity budgets were highly associated with temporal patterns of fruit production. Daily path length was positively correlated with group size and monthly fruit abundance, and negatively correlated with habitat quality. I found differences in activity budgets and the diet preferences of different age/sex classes. For example, adult males rest more and juveniles play more than other classes. Juveniles and adult females without infants look for arthropods more often than adult males and females with young infants, who showed the highest frequencies of fruit feeding. Dominant adult males were not consistently the most efficient foragers on fruits according to two different indexes. Most of these results are consistent with the expectations from strong intra-group competition for resources. However, females with infants received benefits during feeding similar to those of dominant adult males, which may be mediated by differential aggression from males to other group members (juveniles and females without infants).     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Allogrooming Behavior and Grooming Site Preferences in Captive Bonobos (Pan paniscus): Association with Female Dominance

I tested the utility of Seyfarth's (1977) model of rank-related attractiveness to explain the distribution of allogrooming behavior among captive bonobos (Pan paniscus). Adult female bonobos generally have high social status and may be dominant over males. As predicted by the model, I found that high-ranking adult females received most allogrooming within each of the four investigated groups. Among adult female-adult female dyads, however, allogrooming was not clearly associated with dominance rank. Contradictory to predictions of the model, the highest-ranking females were responsible for most displacements over allogrooming, and grooming competition is positively correlated with dominance rank. In the second part of this study, I investigated the social significance of allogrooming body site preferences. Bonobos direct significantly most allogrooming to the face of conspecifics, and high- and low-ranking individuals, as well as males and females, differ significantly in their preferences for certain allogrooming sites. Subordinates and males tended to avoid facial grooming and preferred the back and anogenital region, while high-ranking individuals and females directed most allogrooming to the face and head of grooming partners. Data from this study support the hypothesis that high-ranking females are the most attractive grooming partners within a female-centered bonobo society. Many other aspects of allogrooming behavior, however, are not consistent with the model of rank-related attractiveness.     

Early life maternal sociality predicts juvenile sociality in blue monkeys

Maternal effects are widespread in living organisms though little is known about whether they shape individual affiliative social behavior in primates. Further, it remains a question whether maternal effects on affiliative behavior differ by offspring sex, as they do in other physiological systems, especially in species with high levels of adult sexual dimorphism and divergence in social niches. We explored how direct and indirect experiences of maternal affiliative behavior during infancy predicted affiliative behavior approximately 1–6 years later during the juvenile period, using behavioral data from 41 wild blue monkey juveniles and their 29 mothers, and controlling for individual age, sex, and maternal rank. Female juveniles spent less time grooming with any partner and with peers the more maternal grooming they received during infancy, whereas males groomed more with any partner and with peers. Similarly, the more that mothers groomed with other adult females during subjects’ infancy, female subjects played less with peers, and male subjects played more as juveniles. Further, this maternal effect on social behavior appears specific to early life, as the same aspects of mothers’ sociality measured throughout subjects’ development did not predict juvenile behavior. Overall, our results suggest that both direct and indirect experience of mother's affiliative behavior during infancy influence an individual's affiliation later in life that sexes respond differently to the maternal affiliation, and that the first year of life is a critical window.     

Grooming,rank, and agonistic support in tufted capuchin monkeys

Studies investigating the relation between allogrooming and social rank in capuchin monkeys (genus Cebus) have yielded inconsistent results. In this study, we investigated the relation between grooming, agonistic support, aggression and social rank in a captive group of tufted capuchin monkeys (C. apella). Differently from most previous studies, we based our analyses on a relatively large database and studied a group with known genealogical relationships. Tufted capuchin females did not exchange grooming for rank‐related benefits such as agonistic support or reduced aggression. Coherently with this picture, they did not groom up the hierarchy and did not compete for accessing high‐ranking grooming partners. It is suggested that a small group size, coupled with a strong kin bias, may make the exchange of grooming for rank‐related benefits impossible or unprofitable, thus eliminating the advantages of grooming up the hierarchy. We provide several possible explanations for the heterogeneity of results across capuchin studies that have addressed similar questions. Am. J. Primatol. 71:101–105, 2009. © 2008 Wiley‐Liss, Inc.     

The Development of Local Song Preferences in Female Cowbirds (Molothrus ater): Flock Living Stimulates Learning

We carried out two experiments across 2 yr on song perception in female cowbirds (Molothrus ater). In the first experiment, juvenile and adult female brown‐headed cowbirds, living in same‐sex flocks in outdoor aviaries, were periodically tutored with recordings of local male cowbirds’ songs. In the spring, four adult male cowbirds were placed with half of the females for a 12‐d period. We then tested song preferences of all females by measuring copulation solicitation displays during the breeding season. We found that the females exposed only to tape‐tutor songs preferred those songs to those of the unfamiliar males used as companions and that the females allowed to interact with males preferred their songs over the familiar tape‐tutor songs. These data establish the modifiability of female cowbirds’ song preferences at the level of local song. In a second experiment, we studied the playback responses of juvenile females, hand‐reared from the egg, who were tape‐tutored only in the spring in the presence or absence of adult females. There were no differences between the responses of juveniles housed with or without adult females and the hand‐reared juveniles were significantly less responsive to song than adult females. Adult females responded more to familiar songs than to the unfamiliar songs: juvenile females made no such distinction. Taken as a whole, these data are the first to document that female cowbirds’ song preferences for local song can be reshaped by post‐natal experience. These data complement recent study in cowbirds and other species showing that socially more complex contexts reveal plasticity in female song preferences that are not apparent when learning opportunities are constrained by impoverished laboratory settings.     

Playmate relationships among individuals of the Japanese monkey troop in arashiyama

Observations of play behavior were made on a troop of Japanese monkeys for five months. The troop consisted of 125 animals during the study period. Only 104 animals were observed playing with the troop members while the other 21 animals were never observed playing with other individuals. Two-member play was the most frequent. On the average, a monkey played with 20.7 individuals. A total of 6,068 play bouts were observed. The frequency of play appeared to be affected by age, sex, and degree of relatedness. One-year-old infant males played most with other members and the frequency of play decreased with age. Between monkeys whose disparity of age was less than two years, 5,763 bouts (95.0% of the total) were observed. Moreover, among sameaged monkeys who comprised 10.6% of the possible pair combinations, 2,739 play bouts (45.1%) were observed. Juvenile males played with same-sexed peers more than with opposite-sexed peers, whereas older juvenile females appeared to play with infants of both sexes. Individuals who were related and similarly-ranked tended to play together. There was no apparent preference for animals to play with the offspring of the highest-ranking female. Dominance rank of infnats and juveniles was primarily affected by rank of their mothers and to a lesser extent by play partners. Dominance rank of older juvenile males is more likely to be affected by play partners than females. It may be a critical time for males when they leave their natal troop and join a new troop. The timing of troop shifting by males seemed to be affected by the presence or absence of play-mates. For male Japanese monkeys, play is very important in developing social bonds. Play may act to perpetuate social bonds, enhance the chance of survival, and may contribute to their future reproductive success.     

A case report of a male rank reversal in a group of wild white-faced capuchins (Cebus capucinus)

During the course of a study of social relationships in wild, white-faced capuchins at Lomas Barbudal, Costa Rice (May 1990–May 1993), the alpha male was deposed by a subordinate male. The rank reversal was preceded by a decline in proximity maintenance by females to the alpha male, and an increase, in the amount of aggression directed toward the alpha male by the beta female and her female coalition partners. At the time of the rank reversal, females switched from giving thegargle vocalization exclusively to the old alpha male to gargling to the new alpha male; however, juveniles were less consistent with regard to which male they gargled to. At the time of the rank reversal, most adult females reduced the time spent in proximity and grooming with the old alpha male, and increased the time spent in proximity and grooming with the new alpha male. In contrast, juveniles' patterns of affiliation with males did not change in a predictable way following the reversal. The social strategies employed by capuchin monkeys during this rank reversal are compared with those of chimpanzees.     

Proximal Spacing Between Individuals in a Group of Woolly Monkeys (Lagothrix lagotricha) in Tinigua National Park, Colombia

I studied proximal spacing within a group of woolly monkeys (Lagothrix lagotricha) during 7 months at Parque Nacional Tinigua, Colombia. I collected a total of 1188 instantaneous samples on focal individuals, recording the number and age/sex class of individuals that were in contact with, <2 m from, <5 m from the focal animal. The results indicate that proximate spacing reflects social affinities and is related to mother–infant relationship and social grooming. Subadult females and adult males are the sex/age classes with the lowest number of individuals in proximity. There are low proximity between adult females and between adult males and high frequencies of nearness between mother and offspring. Associations between males and females were usually low, but in some cases males showed preferences for a given female. There was a relatively gradual increase in spacing between mothers and their offspring as they became older. Old juvenile males were associated chiefly with other males—mostly subadults—whereas juvenile females maintained some proximity only to their mothers. There are also differences in spacing behavior according to different activity types.     

Dominance,grooming, and clasped-sleeping relationships among bonnet monkeys in India

Social relationships, including dominance, grooming, and clasped-sleeping, were studied in a troop of bonnet monkeys (Macaca radiata) at Dharwar, India, the study period lasting two months and a half. Three measurements, the peanut test, the drinking test, and the spatial distribution test, were used to analyze dominance relationships. The peanut test showed a straight linear ranking order among adult males and females; however, among females drinking and spatial distribution orders are slightly different from that of feeding (peanut test). Grooming was observed more frequently between adult female and adult female and was seldom observed between adult male and juvenile female or between juvenile male and juvenile female. Apparently all monkeys tend to groom with females. On the other hand, monkeys of the same sex tend to sleep with each other. It is clear that monkeys select their partners when they groom and sleep.     

Seasonal Differences in Social Behavior among Adult and Juvenile Meadow Voles,Microtus pennsylvanicus

Seasonal differences in behavioral interactions between wild-caught adult and juvenile meadow voles, Microtus pennsylvanicus, were measured in paired encounters in a neutral arena. Seasonal differences existed in the adult-juvenile paired encounters. Early in the breeding season (May—Aug.) paired encounters between adult males and juvenile males were more agonistic than other adultjuvenile pairings. Late in the breeding season (Sep.—Dec.) adult female-juvenile male encounters were more agonistic than other adult-juvenile pairings. Odor preferences of juveniles were determined in a Y-maze olfactometer. Juveniles did not demonstrate seasonal differences in odor preference. Males preferred the odor of adult females to the odor of adult males or their own odor. Females preferred the scent of an adult male to the odor of an adult female, but did not show a preference between their own odor and the odor of an adult male or an adult female. The results are consistent with hypotheses that state in a promiscuous species, females should be philopatric, and males should disperse as a consequence of adult competition. The data suggest that agonistic behavior by adults may regulate juvenile dispersal and recruitment, and define the composition of overwintering groups.     

Social organization of white‐headed langurs (Trachypithecus leucocephalus) in the Nongguan Karst Hills,Guangxi, China

The number of males per group is the most variable aspect of primate social organization and is often related to the monopolizability of females, which is mainly determined by the number of females per group and their reproductive synchrony. Colobines show both inter‐specific and intra‐specific variations in the number of males per group. Compared with other colobine species, little is known about the social organization of white‐headed langur (Trachypithecus leucocephalus), despite its endangered status and unusual limestone habitat. As a part of a long‐term study of the white‐headed langurs in the Nongguan Karst Hills, Guangxi, China, we quantitatively investigated their social organization by analyzing census data from 1998 to 2003. The population censuses revealed that the predominant social organization of bisexual groups was the one‐male group, similar to a previous report on this species and many other Asian colobines. In such groups, one adult male associated with 5.1 adult females, 0.1 sub‐adult males, 2.6 juveniles and 2.9 infants on average, with a mean group size of 11.7 individuals. In addition, three multi‐male groups were recorded, consisting of 2–3 adult males, 1–5 adult females, 0–2 sub‐adult males, 0–7 juveniles and 0–2 infants. They did not contain more adult females than the one‐male groups and were unstable in group membership. The langurs outside bisexual groups were organized into small nonreproductive groups or lived as solitaries. The nonreproductive groups averaged 1.3 adult males, 1.3 sub‐adult males and 2.6 juveniles. Juvenile females were present in such groups on 52.4% of all occasions. As predicted by the monopolization model, the prevalence of the one‐male pattern in this species may mainly be attributed to the small number of females in the group. The possible reasons for the occurrence of multi‐male groups and the presence of juvenile females in nonreproductive groups are also discussed. Am. J. Primatol. 71:206–213, 2009. © 2008 Wiley‐Liss, Inc.