Development in Japanese macaques (Macaca fuscata): Sexually dimorphic behavior during the first year of life

We have documented several sexually dimorphic patterns of behavior that develop during the first year of life in infant Japanese macaques and their mothers. Mothers treated their infants differently by sex—mothers of males broke contact with them and retrieved them more frequently than did mothers of females. And mothers of male infants moved more frequently than did mothers of female infants. Male infants played more, played in larger groups, and mounted more frequently; female infants groomed and spent more time close to other monkeys in larger social groups than did males. Female infants were also punished by other group members more frequently than were male infants. We conclude that male and female Japanese macaque infants receive differential treatment early in life by both their own mothers and other animals, and males and females in turn treat their mothers and other animals differently. There appears to be a reciprocal relationship between the behavior of infants, mothers and other social partners that contributes to the development of sexually dimorphic patterns of behavior.     

Social Play among Juvenile Bighorn Sheep: Structure,Development, and Relationship to Adult Behavior

A 27-mo study of bighorn sheep (Ovis canadensis) was conducted to examine the structure and development of social play among lambs, and to compare that behavior with the behavior of yearlings and adults. Male lambs played more than females and exhibited a larger repertoire. The behavior patterns used by lambs in social play were the same as those used by adults in intrasexual conflict and courtship. However, the repertoire of lambs was more limited than that of adults. Lambs chose partners closest in age to interact with, regardless of sex. Results were consistent with the hypothesis that play serves to develop physical skills and strength.     

Urine Marking and Territoriality in Galago alleni (Waterhouse, 1837 — Lorisoidea,Primates) — A Field Study by Radio-telemetry

Behavioral interactions among color-marked individual Vidua chalybeata that shared common song dialects were observed for 5 years in two populations at Lochinvar National Park, Zambia. Social interactions involved ♂♂ visiting and competing for mating sites and ♀♀ visiting ♂♂ in an apparent sampling of potential copulating partners. Differences in mating success among the polygynous ♂♂ were compared with male behavior and territory resources, and criteria were developed to test the importance of intrasexual male competition and female mate choice in explaining the mating system of the populations. Song behavior best explained differences in mating success of ♂♂ with lesser effects of neighboring ♂♂ and the defensible resources around the call-sites. The social organization of song populations resembles that of a dispersed lek with ♀♀ visiting many ♂♂ but mating with few ♂♂. We discuss the observations on indigobirds in relation to behavioral selection, sexual selection, and mating systems. Mating systems of certain populations and species are compared using statistics of individual mating success.     

Sex differences in adolescent rhesus monkey (Macaca mulatta) Behavior

Sex differences in the behavior of 2.5- to 4.5-year-old rhesus monkeys, living in two social groups approximating natural compositions, were studied over a period of 3 years. Both sexes interacted significantly more often with members of their own sex in agonistic and affiliative interactions even when total rates and durations for male and female subjects did not differ. Strong sexual segregation was also seen in proximity, nonspecific contact, and huddling partners. Males were more involved in play and sex than were females and engaged in these activities primarily with other males. Females did more grooming than males, but groomed both male and female partners. Females also appeared to interact with a wider age range of partners than did males. Although total participation in aggressive interactions did not differ between the two sexes, females used more active forms of agonistic expression than did males. These differences in the behavior of adolescent rhesus are hypothesized to lead to social bonding among adolescent males, while females remain bonded to their matri-lines, including younger males and some fully adult males associated with matrilineal relatives. Adolescent males emigrate from their natal groups but retain sociality and bond to males and females in new groups as they become adult. © 1993 Wiley-Liss, Inc.     

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.     

Behavioral masculinization is independent of genital masculinization in prenatally androgenized female rhesus macaques

Genetic female fetuses were exposed transplacentally to testosterone propionate injected into their mothers either early (Days 40 through 64) or late (Days 115 through 139) in gestation. Early and late androgenized females (EAFs and LAFs, respectively) were raised with normal males and females that served as criteria for evaluating degree of behavioral masculinization induced by the prenatal androgen. EAFs were genitally virilized and LAFs were not. Males and untreated females differed reliably on five behavioral measures: males showed more mother-mounting, more peer-mounting, more rough play with peers, a preference for initiating play with male partners, and less grooming of mothers. Neither type of prenatally androgenized female showed masculinization of all five types of behavior. Compared with females, EAFs showed more mother-mounting, more peer-mounting, less mother-grooming, did not differ from females in rough play, and did not manifest a preference for male partners. LAFs, like females, groomed but did not mount their mothers, and did not show a preference for male partners; but unlike females they showed elevated rough play and mounting with peers. EAFs showed a statistically significant delay in puberty onset (menarche), but LAFs did not. Mothers inspected genitalia of their offspring more often if they were males than if they were females. Mothers of EAFs inspected their offspring's genitalia as often as mothers of males, but mothers of LAFs did not. No aspect of maternal behavior was associated with either the amount or kind of masculine behavior shown toward peers. We interpret the results to mean that genital virilization is independent of, and largely irrelevant to, the expression of those behavioral traits that characterize the juvenile male social role. Moreover, the individual behavior traits that are components of the juvenile male role are independently regulated by the organizing actions of androgen and have separable critical periods. Of the two major traits, mounting peers and rough play with peers, the latter has a greater requirement for androgenic stimulation late in prenatal life.     

Seasonal influences on rhesus monkey (Macaca mulatta) behavior

Seasonal differences in the behavior of 2.5- to 4.5-year-old female subjects and male subjects >2.5 years of age were studied in two rhesus monkey groups over a period of 6 years. The frequencies and durations of sexual acts and states were higher during the Fall in Georgia, USA, but were significant only with regard to female partners. Total time in social proximity, scores for proximity by partner without social interaction, nonspecific contact, grooming received, and noncontact forms of aggression with female partners were also higher in the Fall. Although more submission and agonistically ambiguous responses were received from female partners during the Fall, no seasonal pattern prevailed for responses performed. More contact aggression was directed to males in the Spring, and the pattern of agonistic behavior observed cannot be accounted for by males fighting over estrous females. Significantly more play was observed among subjects in the Fall, but the oldest males played more in the Spring. Some patterns, like huddling, were seen more in the Fall, but they may have been due to temperature differences. Seasonal differences in morphology and behavior cannot be attributed to a single variable, like temperature, level of gonadal hormones, or sexual competition, and may reflect a broader adaptation to seasonal variables.     

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.     

The ontogeny of social play in a feral troop of vervet monkeys (Cercopithecus aethiops sabaeus): The function of early play

We describe the ontogeny of social play over the first 30 weeks of age in a troop of feral vervet monkeys (Cercopithecus aethiops sabaeus) in Barbados. Play time increased rapidly for the first 10 weeks but remained relatively constant thereafter. The form of play changed with infant age; bouts became more frequent but of shorter duration. Play time, bout frequency, and bout duration at a given age differed between infants; younger infants altered their play patterns to complement those of older infants. All infants played more within their own year class than with older juveniles; play time increased with decreasing age difference between the infant and the play partner. Infants terminated a higher proportion of their play bouts the greater the age difference between themselves and their play partners. Preferred play partners are therefore individuals of similar age that will be similar in size and have matched motivation to play and form of play. Neither play time nor proportion of bouts initiated or terminated was correlated with the social rank of the play partner, which suggests that play is not directed toward individuals that may be high-value alliance partners. Maternal intervention in play occurred primarily when infants were<10 weeks old. It was not correlated with the age or social rank of the mother or with the age or social rank of her infant's play partner. Infants played more and terminated a lower proportion of their play bouts in the absence of their mothers than in their presence. Our results are consistent with the hypothesis that the primary function of early play is to enhance physical fitness and to develop coordination and other fighting skills, with minimal risk of injury.     

Puberty in male Japanese macaques (Macaca fuscata): Social and sexual behavior in a confined troop

The social and sexual behaviors of four groups of males (4, 5, 9, and 10 years old) were compared throughout one complete mating season in a confined troop of Japanese macaques (Macaca fuscata). The aim of this research was to document social behavior changes that occurred during adolescence and to relate them to changes in sexual behavior that occurred at puberty. The 4-year-old males all mounted females and ejaculated but they had significantly fewer ejaculations and female partners than did the older males. The 4-year-old males also showed a pattern of delayed development in tail carriage and courtship, and they played more frequently than the older males. There were no significant differences in the frequency of aggression among the groups, but both 4-year-old and 5-year-old males were displaced by adult males and females more frequently than were the older males. We concluded that the development of adult patterns of social behavior in this genus is not climactic, but occurs slowly one to two years after physiological puberty has been reached.     

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.     

Individual- and Sex-related Strategies of Wrestling Play in Captive Squirrel Monkeys

The play behavior of 10 juvenile squirrel monkeys (Saimiri sciureus) was observed for 7 months in both mixed-sex and same-sex laboratory social groupings to identify strategies by which individuals may derive maximum benefit from play. Two types of play wrestling were identified: directional if one partner was on top of and dominating the other, and nondirectional if both partners hung from a perch and clasped each other equally. Males (N=5) wrestled more often, had longer bouts, and used proportionately more directional wrestling than did females (N = 5). Initiation Behaviors, leading predictably to play, were performed preferentially to certain partners, independent of affiliative (huddling) preferences. Both sexes performed more Initiation Behaviors to same-sex partners. Individuals, regardless of sex, preferred play partners whom they could dominate during directional wrestling; with partners whom they could not dominate, they preferred nondirectional wrestling, where partners were equal. The observed preferences are interpreted as evidence for individual strategies maximizing winning at directional wrestling. Role reversal is discussed as a strategy encouraging play between youngsters of diverse abilities, and as a means of providing needed experience in a variety of social roles.     

Sex preferences in Jeju pony foals (Equus caballus) for mutual grooming and play-fighting behaviors

We investigated mutual grooming by Jeju pony (Equus caballus) foals to determine whether male foals preferentially interact with potential future sexual partners or competitors. We predicted that relative to female foals, male foals would exchange grooming more frequently with young mares and that in general, foals would mutually groom more frequently with the opposite sex rather than the same sex. Observing 53 foals between April and October 1998, we recorded 113 mutual grooming events. Male foals exchanged grooming with yearling mares more frequently than with their mother, while female foals exchanged grooming with their mother more frequently than with yearling mares. Contrary to the prediction, foals were not more likely to mutually groom with a foal of the opposite sex than with a foal of the same sex. In our study, 21 instances of play-fighting behavior followed mutual grooming between peers. Relative to intersexual grooming events, play-fighting was more likely to follow intrasexual mutual grooming, and male foals were much more likely to play fight than female foals. These results provide evidence that Jeju pony foals develop and maintain social relationships at the earliest stage of their lives. We suggest that early social experiences might influence social bonding later when the male foal begins to form a harem after separation from its mother.     

Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality

In temperate environments, early-born ungulates may enjoy a longer growth period before winter, and so attain a higher body mass and an increased probability of survival compared to late-born ones. We assessed the effects of maternal characteristics, forage quality and population density on kid birthdate, mass and survival in a population of marked mountain goats (Oreamnos americanus) in Alberta. The duration and timing of the birth season were similar in all years. Births were highly synchronised: 80% of kids were born within 2 weeks of the first birth. Maternal age, maternal social rank and density did not affect kid birthdate or mass. Previous breeding experience was not related to kid birthdate, but kids born to pluriparous mothers were heavier during summer than kids born to primiparous mothers. Male and female kids had similar mass and accumulated mass linearly during summer. Early-born kids were heavier than late-born kids. Faecal crude protein (FCP) in late spring and maternal mass were positively related to kid mass. Survival to weaning appeared higher for males (90%) than for females (78%), but survival to 1 year was 65% for both sexes. FCP in late spring, density, birthdate and mass did not affect kid survival to weaning in either sex. Survival to 1 year increased with FCP in late spring for females, but not for males. Survival to 1 year was independent of birthdate for both sexes, but heavy females survived better than light ones. Multiple logistic regression revealed a positive effect of mass on survival to 1 year when the sexes were pooled. Our results suggest that mountain goats are constrained to give birth in a short birth season synchronised with forage productivity.     

Socio-sexual behavior of female northern muriquis (Brachyteles hypoxanthus)

Female northern muriquis (Brachyteles hypoxanthus) are known to engage in frequent copulations with multiple partners, a pattern that in other primates has been attributed to various functions such as confusing paternity, reducing male aggression, or ensuring fertilization. However, in some female primates, promiscuity is restricted to times when conceptions are unlikely. We investigated whether female northern muriquis might exhibit a similarly mixed strategy by examining their mating, social, and activity patterns during their conception cycles versus other times. Systematic behavioral data were collected during an 18-month period between August 2001 and February 2003 on 13 adult females in a well-studied group at the RPPN-Feliciano Miguel Abdala, Minas Gerais, Brazil. Females mated on an average of 12.5+/-7.9 days during the study period, and spent significantly less time resting and engaging in non-sexual social behaviors, and significantly more time in sexual behaviors on days that they copulated than on days they did not. Three of the eight females for which sufficient data were available copulated significantly more often with their spatially closest non-kin associates, and four of five females that could be analyzed copulated significantly more often with their most frequent non-kin embrace partners. Comparisons between conception and non-conception periods revealed no differences in female activity budgets or in either the number of copulations or the number of different mating partners per female. Our results suggest that some females mate preferentially with close associates and social partners, but there is no indication that females alter their behavior during the cycles in which they conceive.     

Play in chimpanzees of the Arnhem Zoo: Self-serving compromises

In a colony of 25 chimpanzees maintained at Arnhem (The Netherlands), play behavior was studied for four months, yielding 1,651 play bouts involving the 11 oldest immature chimpanzees on which detailed data were collected during 88 focal animal samples of 30 min each. Play frequency and object play were negatively correlated with increasing age. These findings potentially reflect changing motivations during development and increasingly perfected skills. Like-aged partners were preferred play partners and older partners initiated play more frequently, probably because younger individuals feared rough responses by older immatures and waited until the latter initiated play bouts in a self-handicapped manner. Moreover, play was frequently interrupted by short breaks. This, in conjunction with the preference for like-aged partners, may be mechanisms to achieve and maintain compromises between the play partners' different interests in social play (which e.g. depend on sex and physical development) and to minimize the risk to being cheated. Males played significantly more often than females and played more chasing games. Male-male play was over-represented whereas female-female play was underrepresented. These facts potentially foreshadow sex differences in (wild) maturing chimpanzees, where males engage in more agonistic conflicts and tend to build coalitions.     

Social preferences based on sexual attractiveness: a female strategy to reduce male sexual attention

Male sexual harassment of females is common across sexually reproducing species and can result in fitness costs to females. We hypothesized that females can reduce unwanted male attention by constructing a social niche where their female associates are more sexually attractive than themselves, thus influencing the decision-making of males to their advantage. We tested this hypothesis in the Trinidadian guppy (Poecilia reticulata), a species with high levels of male sexual harassment. First, we confirmed that non-receptive females were harassed less when they were paired with a more sexually attractive (receptive) female than with another non-receptive female. We then found that, indeed, females exploit this as a strategy to reduce sexual harassment; non-receptive females actively preferred to associate with receptive over non-receptive females. Importantly, when given access only to chemosensory cues, non-receptive females still showed this preference, suggesting that they use information from chemical cues to assess the sexual attractiveness of potential female partners. Receptive females in contrast showed no such preferences. Our results demonstrate that females can decrease male harassment by associating with females that are more sexually attractive than themselves and that they perform active partner choices based on this relative attractiveness. We propose that this strategy is likely to represent an important pathway by which females can construct social niches that influence the decision-making of others to their advantage; in this case, to reduce the sexual harassment they experience.     

Sex differences in play among western lowland gorilla (Gorilla gorilla gorilla) infants: implications for adult behavior and social structure

Mammalian play is believed to improve motor skills as well as facilitate the development of social relationships. Given the marked sexual dimorphism in gorilla body size and the role assumed by the male in protecting the group from conspecifics and predators, the motor-training hypothesis of play predicts that male infants should exhibit higher frequencies of social play than female infants, and that males should prefer to play with other males. Given that adult female gorillas are strongly attracted to adult breeding males and form only weak social bonds with unrelated adult females, the social-relationship hypothesis of play predicts that female infants should prefer to play with males. These hypotheses were tested in a 22-month study of 12 gorilla infants, aged between 0-5 years, living in three zoological parks in Chicago and Atlanta. Consistent with the hypotheses, male infants played more than female infants did, and both male and female infants preferred to play with males rather than with females. These findings suggest that sex differences in play in the great apes and other primates can be predicted by the characteristics of adult behavior and social structure above and beyond the patterns of sex-biased dispersal or coalition formation with same-sex kin.     

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.     

The play partners of immature baboons

In a troop of free-ranging baboons, infants played predominantly with each other, and played most with the infant of the highest-ranking female in their mothers' subgroup. The frequency of infant play appeared to be affected both by age and by the number and ages of other infants in the troop. Juveniles and subadults played more with their siblings than with other animals of their siblings' age. Juvenile and subadult females played primarily with infants, and played most with infants whose mothers ranked higher than their own. Juvenile and subadult males played most with like-sexed peers. The distribution of play partners among immatures illustrates how demographic and maturational factors, as well as those related to kinship, may reinforce or counteract one another during development.