Male Social Behavior and Dominance Hierarchy in the Sulawesi Crested Black Macaque (Macaca nigra)

In a 6-week study of the social behavior of wild Sulawesi crested black macaques (Macaca nigra), we found a linear and transitive dominance hierarchy among the six adult males in one social group. Dominance rank, as determined by the direction of supplantations, correlated strongly with percentage of time near more than four neighbors, frequency of grooming received from adult females, and percentage of time with an adult female as nearest neighbor. These results suggest that high-ranking males are socially attractive. Adult females sexually solicited high-ranking males more often than low-ranking males, but frequency of copulation was not correlated with dominance rank. Frequency and intensity of aggression between males are strongly correlated with rank distance, but aggression toward females was greatest for mid-ranking males. Males of all rank displayed significantly more aggression toward sexually receptive females than toward females in other estrous states. These data indicate that male Sulawesi crested black macaques display a social organization similar to that reported for multimale groups in other macaque species rather than the egalitarian social organization described for female Sulawesi macaques.     

Agonistic and Affiliative Relationships of Adult Female Howlers (Alouatta palliata) in Costa Rica Over a 4-Year Period

We observed 12 adult female mantled howlers (Alouatta palliata), which have been part of Group 2 at Hacienda La Pacifica, Guanacaste Province, Costa Rica, via focal animal sampling during portions of July and August of 1988 and 1990–1992 (7–9 females/year, 955.3 hr of observation). We used agonistic interactions and time in proximity (<1 m) as indices of social relationships. The rate of female–female agonistic interactions was 0.38/hr (yearly range: 0.24 to 0.51/hr). Yearly dominance hierarchies, based on outcomes of dyadic agonistic interactions, varied in linearity between 60.7 and 94.6%. Adult females spent 7.10% of their time in proximity to another adult female (yearly range: 1.04–15.64%) and 4.95% of their time in proximity to an adult male (yearly range: 2.27–7.51%). Using yearly dominance ranks, we tested proximity patterns for differences based on rank and presence of dependent offspring. In 3 of the 4 years, high-ranking females spent significantly greater proportions of their time in proximity with other females than did low-ranking females. Time in proximity with the 3 or 4 adult males was not associated with rank. Having a dependent infant was not related to the proportion of time in proximity to females or males, and females, especially top-ranking ones, spent more time in proximity to females with dependent infants than to females without infants. These results show that social relationships in mantled howler groups are dynamic and generally support predictions made by von Schaik (1989) regarding scramble-type, female competitors. We also discuss the roles of immigrations, infants, and male relationships in the patterning of social relationships.     

The behavior of postreproductive females in a wild population of toque macaques (Macaca sinica) in Sri Lanka

I compared the behavior of three old postreproductive females in a wild population of toque macaques (Macaca sinica)in Polonnaruwa with those of reproductive females via focal-animal sampling techniques. Postreproductives foraged less, slept more, and were less active overall than reproductive females were. They also had significantly lower rates of agonistic behavior, were more peripheral, and had lower frequencies of overall affiliative contact. Although postreproductives initiated contact with others as frequently as reproductives did, group members initiated contact with them significantly less than they did with reproductive females. Postreproductives associated more with adult females than reproductives did and less with adult and subadult males than high-ranking reproductives did. Juvenile and infant females associated more frequently with reproductive females of high or low rank than with postreproductives. Postreproductives resembled low-ranking reproductive females in giving less grooming to others than they received. This contrasts with high-ranking females, which gave more grooming to others than they received. The results suggest that old age and cessation of reproduction are evident through the manifestation of distinct behavioral characteristics in toque macaque females.     

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.     

Alloparental behavior in a captive group of spider monkeys (Ateles geoffroyi) at the Auckland zoo

I studied alloparental behavior in a captive group of spider monkeys at the Auckland Zoo using seven infants as focal subjects and assessed the effects of age, sex, and reproductive status of alloparents on patterns of infant-other interaction. Adult males initiated interactions with infants most often, followed by adult females. Immature individuals interacted with infants infrequently. Infants themselves initiated contact with adult males more often than with other members of the group. Alloparental behavior in spider monkeys differs from that in most other species in that the infant is an active rather than a passive participant in alloparental interactions. I discuss the patterns of infant-other interaction in relation to the social structure and dispersal patterns of Ateles.     

Mating patterns,mate choice,and birth season heterosexual relationships in free-ranging rhesus macaques

Birth season adult heterosexual nonkin relationships of 50 free-ranging female rhesus macaques (Macaca mulatta) in two social groups at Cayo Santiago, Puerto Rico were examined using focal follow (289 hr) and ad lib data. Eighty-eight percent of subjects had at least one relationship characterized by particularly high frequencies of spatial proximity, grooming, or both. These were designated “friendships.” Males intervened in aggressive interactions more frequently on behalf of Friends than non-Friends. Female aggressive support of males was extremely rare. Higher-ranking males experienced more friendships than lower-ranking males. High-ranking females had higher-ranking Friends than low-ranking females. Older females had higher-ranking Friends than younger females. Females groomed high-ranking Friends more than they were groomed by them, whereas they groomed low-ranking Friends less than they were groomed by them. In one social group, high-ranking females were more likely than low-ranking females to groom their Friends more than they were groomed by them. Males were more responsible than females for spatial proximity maintenance in 9 of 14 Friend dyads for which sufficient data were available. Neither male nor female dominance rank affected responsibility for proximity maintenance in Friend dyads. Eight of 24 females had friendships with males with whom they had completed copulations during their conception peri-ovulatory period of the preceding mating season. Two of 19 females completed peri-ovulatory copulations with Friends during the following mating season. Friendship was not correlated with either of two demonstrated female mate choice indicators: (1) proximity maintenance during estrus; or (2) cooperation with male “hip-grasp” courtship attempts. Males directed “muzzle-up” courtship signals at lower rates toward Friends than toward non-Friends. These and other investigators' results indicate that (1) protection from aggression is the primary benefit to female rhesus macaques of birth season heterosexual relationships; (2) the most effective protectors are in greatest demand as Friends; and (3) friendship has no effect or an inhibitory effect on mate choice in this species. Benefits to males of friendships were not apparent from this study but may include coalitional support against lower-ranking males.     

Breeding-season relationships of immature male rhesus monkeys with females. I. Individual differences and constraints on partner choice

Several aspects of breeding-season relationships with mature females are described for free-ranging immature male rhesus monkeys (Macaca mulatta)on Cayo Santiago. At puberty, immature males are still groomed by mature females, as they were as infants, but no longer receive active protection from females other than their mothers. A further, potentially beneficial, aspect of their associations with females lies in the opportunities to observe closely the tactical social and sexual interactions of receptive females with adult males. However, immature males themselves rarely copulate with females. Developmental constraints may explain the finding that most females observed by immature males were relatives but that high-ranking males showed a particular preference for adolescent relatives, whereas the preference of low-ranking males was for adult relatives. A further finding was that while there was a tendency for immature males to devote a greater proportion of their total observation time to females that ranked above their mothers than to those of inferior rank, these were also the females from which males received the most aggression, while most of the females with which the males groomed or copulated were lower ranking than the males’ mothers. Of three hypotheses concerning three possible types of social constraint which might account for such a finding, the data supported only one—that particular levels of aggression within these relationships are compatible only with certain other elements (observations), and not with others (grooming, copulation).     

Body mass of wild ring-tailed lemurs in Berenty Reserve,Madagascar, with reference to tick infestation: a preliminary analysis

In 1999, we measured the body mass of 101 wild ring-tailed lemurs (Lemur catta) inhabiting the Berenty Reserve, Madagascar. In addition, we counted the number of ticks [Haemaphysalis (Rhipistoma) lemuris Hoogstraal, 1953] infesting their facial skin and external auditory meatuses. For both males and females, the body mass appeared to increase until the age of 3 years. With the apparent exception of infants, there were no sexual differences in body mass. Within a group, higher-ranked adult males tended to be heavier than lower-ranked males. In contrast, there was no consistent correlation between the body mass of females and their ranks. Among the study groups, there was a small difference in body mass and significant difference in the number of ticks infesting the facial skin and external auditory meatuses. In particular, lemurs of a group who inhabited an area of gallery forest in the study area exhibited the smallest values of body mass and were severely infested with ticks. Such group variations were not consistently correlated with the reproductive parameters of the study groups. In three groups moderately infested with ticks, ticks infested adult males and subadults more heavily than adult females, juveniles, and infants.     

Long-term changes in dominance ranks among ring-tailed lemurs at Berenty Reserve, Madagascar

A study was conducted between 1989 and 2001 to monitor changes in the dominance ranks among adult ring-tailed lemurs (Lemur catta) at Berenty Reserve, Madagascar. Adult females were observed to be dominant over adult males. Their rank fluctuated greatly. However, in some troops, female rank orders were fairly stable over a period of several years. In general, male ranks were more unstable than female ranks. Most young females aged 3 years occupied the lowest ranks among adult females. However, several were also observed to have attained relatively higher ranks, placing them right beneath their high-ranking mothers; this suggested the existence of dependent ranks. Mothers were dominant over their daughters. Similarly, older sisters were usually dominant over younger sisters. The mean duration of alpha status for females was 1.95 years, although considerable variation was observed in the duration of the alpha status (1–5 or more years). Most young males aged 3 years initially occupied the lowest ranks in their natal troops, and then they migrated to non-natal troops around the age of 4 years. They ascended in rank between the ages of 4 and 6 years, although there was considerable variation in the acquirement of high rank. The mean duration of alpha status for males was 2.2 years. Larger males were observed to occupy higher ranks. Occasionally, both males and females showed intense aggression (i.e., targeting aggression) towards others.     

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.     

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).     

Birth-season interactions of adult female Japanese Macaques(Macaca fuscata) without newborn infants

The affiliative interactions of 11 adult female Japanese macaques that did not deliver an infant during the 1981 birth season of the Arashiyama West troop were examined. Consideration was given to the effects of kinship as a structuring element in these birth-season interactions and to the degree of association with various categories of troop members based on age, sex, and (in the case of adult females) whether or not the females were new mothers. Females without infants interacted predominantly with their yearling off-spring, although it was the behavior of the offspring that precipitated the interaction. These females were active in soliciting affiliation with nonkin new mothers, whereas female matrilineal relatives with new infants approached and remained in proximity to them more than did nonrelated new mothers. Females without newborns groomed and approached nonkin infants more than infants within their own matriline, and these infants were predominantly those of females in the highest-ranking matriline of the troop. Adult males were responsible for 40% of all grooming received from nonkin by the females without newborns, and these males approached them significantly more than did other adult females without infants. These patterns demonstrate that the structure of social relationships is influenced by the particular dynamics of troop contexts such as birth seasons, as well as by enduring, broad-based affinities which are less affected by cyclic changes in troop context.     

Factors Affecting Reproduction and Mortality Among Baboons in the Okavango Delta,Botswana

We present results of a 10-year study of free-ranging gray-footed chacma baboons (Papio ursinus griseipes) in the Okavango Delta of Botswana. The majority of deaths among adult females and juveniles were due to predation, while infants were more likely to die of infanticide. There were strong seasonal effects on birth and mortality, with the majority of conceptions occurring during the period of highest rainfall. Mortality due to predation and infanticide was highest during the 3-mo period when flooding was at its peak, when the group was more scattered and constrained to move along predictable routes. The reproductive parameters most likely to be associated with superior competitive ability—interbirth interval and infant growth rates—conferred a slight fitness advantage on high-ranking females. However, it was counterbalanced by the effects of infanticide and predation. Infanticide affected high- and low-ranking females more than middle-ranking females, while predation affected females of all ranks relatively equally. As a result, there were few rank-related differences in estimated female lifetime reproductive success.     

Symmetrical patterns in non-agonistic social interactions found in unprovisioned Japanese macaques

Non-agonistic social interactions in an unprovisioned troop of Japanese macaques (Macaca fuscata yakui) were analyzed with the spacing between individuals, leading-following interactions, and exchange of social grooming. The most frequent interactions were found between kin-related females. Unrelated females stayed with one another rather frequently, but rarely exchanged social behaviors. Interactions between males and females were infrequent though they were occasionaly observed between high-ranking males and high-ranking females. Very frequent exchange of grooming was observed between males, and even high-ranking males exchanged grooming more frequently with males than with females. Most non-agonistic social interactions in the study troop were based on bidirectional exchange of social behaviors, in which no clear tendency relevant to dominance or sex was found; while in provisioned Japanese macaque troops, associations between males and females, between unrelated females, and between males were formed mainly be subordinates' active roles in associative behaviors. This seems relevant to the idea that dominance grealty influence social life in provisioned troops. The present study provides guidelines for interspecific comparison of social interaction patterns of macaque species.     

Male and Female Reproductive Success in <Emphasis Type="Italic">Macaca sylvanus</Emphasis> in Gibraltar: No Evidence for Rank Dependence

The relationship between social rank and reproductive success is one of the key questions for understanding differences in primate social group structures. We determined the paternity of 18 infants in a social group of Barbary macaques (Macaca sylvanus) born over a period of 6 yr in the provisioned, free-ranging colony in Gibraltar. We successfully used 13 pairs of primers of variable microsatellite loci to amplify DNA from blood and hair samples and applied the computer programs CERVUS 2.0 and KINSHIP 1.3 to assign paternity to 13 candidate males. We collected data for 19 females that had given birth to 66 infants over a period of 7 yr. We used paternity analyses and female birth records to test the hypothesis that social rank is correlated with reproductive success. Results showed that numbers of paternities and maternities were equally distributed among all reproducing individuals in the social group regardless of rank. Subadult males reproduced as often as adult males. High-ranking females did not start to reproduce earlier than low-ranking females. Interestingly, there was a tendency toward a positive correlation between the ranks of mothers and the ranks of the corresponding fathers. It might be concluded either that a correlation between social rank and reproductive success is generally absent in Barbary macaques or that artificially favorable environmental conditions in Gibraltar preclude any correlation between social rank and reproductive success.     

Sex Differential Behavior of Immature Hanuman Langurs (Presbytis entellus) in Ramnagar, South Nepal

We investigated sex differences in the social behavior of immature Hanuman langurs (Presbytis entellus) in the light of sex-specifically different life-courses and Hanuman langur characteristics, such as the individualistic dominance hierarchy and the rarity of intragroup coalitions among adult females. We observed four immature female and four immature male langurs—all members of the same free-ranging multimale multifemale group in Ramnagar, South Nepal—from November 1992 to February 1993 for 288 hr via focal-animal and instantaneous sampling techniques. Immature females spent significantly more time in proximity to other group members than immature males did. They had more physical contact and groomed more. Other immature females were their preferred social partners. Immature males also preferred like-aged females. They restricted their relationships with other immature males to proximity and occasional grooming. Monitoring was directed especially toward adult males. Female behavior can be interpreted as oriented toward integration into the female social network and their age-inverted dominance hierarchy. Males seem to prepare for leaving their natal group and for future strong intrasexual competition.     

Effects of group composition on agonistic behavior of captive pigtail macaques,Macaca nemestrina

We surveyed agonistic behaviors of 20 captive groups of pigtail macaques (Macaca nemestrina) housed under identical spatial conditions. Fifteen groups contained one male each; the other five groups contained no adult males. Groups included six to twelve adult females, some of which had infants with them. We found no relationship between social density of groups and incidence of agonistic behavior, but significantly more contact aggression (grab, hit, push, bite) and noncontact aggression (chase, open-mouth “threat,” bark vocalization) occurred among females in groups containing no males than in those containing one male each. Apparently, males played an important role in the inhibition of intragroup conflict. We also found that females in groups containing males exhibited less noncontact aggression if infants were present than if no infants resided in their groups. Thus, competition of females over infants must not have been an important constituent of intragroup conflict under the conditions of this survey.     

Agonistic Interactions and Matrifocal Dominance Rank of Wild Bonobos (Pan paniscus) at Wamba

I studied dominance relations in a wild group of bonobos at Wamba, Democratic Republic of Congo. Although agonistic interactions between males occurred frequently, most of them consisted only of display, and physical attacks were infrequent. Dominance rank order seemed to exist among males, but its linearity is unclear. Dominant males rarely disturbed copulatory behavior by subordinate males. However, high-ranking males usually stayed in the central position of the mixed party and, so, would have more chance of access to estrous females. Among females, older individuals tended to be dominant over younger individuals. However, agonistic interactions between females occurred rather infrequently, and most consisted of displacement without any overt aggressive behavior. Dominance between males and females is unclear, but females tended to have priority of access to food. The close social status between males and females may be related to the prolonged estrus of females and their close aggregation during ranging. Existence of a male's mother in the group and her dominance status among females seemed to influence his dominance rank among males. Young adult males whose mothers were alive in the group tended to have high status. In some cases, change in dominance between high-ranking males was preceded by a corresponding change in dominance between their mothers. As the dominance status of females is similar to that of males, mothers may be able to support their sons to achieve high status, stay in the center of the mixed party, and so have greater access to females, which may maximize the number of descendants of the mothers.     

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.     

Utilization of space by adult and juvenile groups of captive chimpanzees (Pan troglodytes)

A systematic analysis of space utilization in the home enclosures of four adult and three juvenile social groups of chimpanzees (Pan troglodytes) was conducted at the Primate Foundation of Arizona. The locations of all members of each group (excluding nursing infants) were recorded several times per week over a 3-month period. Adult chimpanzees were observed significantly more often in small vs large cages, on upper vs lower levels, and near cage perimeters vs cage centers. Analyses of sex differences in adults revealed that adult females are largely responsible for these space use patterns; adult males show only a significantly higher usage of perimeter areas. Individual differences were found in the habitual use of certain enclosure sites. Juveniles show no spatial patterns with regard to the above parameters but appear to evenly use all available space. Both adults and juveniles were observed to be in contact with mesh barriers more often than with solid walls. These findings suggest important elements that should be incorporated into the caging design of captive chimpanzee facilities.