Social relationships between adult male and female rhesus macaques: 1. Sexual consortships

The sexual relationships of 15 adult male rhesus macaques (Macaca mulatta), of one social group in the Cayo Santiago colony, Puerto Rico, were studied during the 1981 mating season. Two criteria were used to determine whether or not a focal male was in consort in a given 20-min observational sample. One hundred and thirty-two consortships were recorded. The distribution and duration of all consortships, and the distribution of those consortships that coincided with the estimated time of conception, were positively correlated with male dominance rank and length of tenure. Correlations with dominance were stronger than those with tenure. Older females had more consortships with focal males than younger females. There was no relationship between female rank and the distribution of consortships. Consortships did not give exclusive access to receptive females although they may do in feral situations. Males were primarily responsible for maintaining proximity in about two thirds of consortships. The four top-ranking males were primarily responsible in all but one of their consortships. Almost all of those in which the female was primarily responsible involved younger, slightly lower-ranking males. This pattern may have resulted from the females being attracted to the latter males although other interpretations are possible. The partner who was primarily responsible for maintaining proximity also tended to be the predominant groomer, supporting the view that grooming plays a role in the maintenance of sexual consortships. Almost a third of consortships were with females who had conceived, suggesting that males could not accurately assess female reproductive state. Consortships maintained by the male were longer than those maintained by the female. Males may try to increase their chances of fertilising a female by prolonging the consortship. High-ranking males may have been more successful at this, resulting in the positive correlation between male dominance rank and consortship duration.     

Styles of male social behavior and their endocrine correlates among low-ranking baboons

We have previously studied the relationship between social subordinance (by approach-avoidance criteria) and physiology among male olive baboons (Papio anubis) living freely in a national park in Africa. In stable hierarchies, subordinate individuals have elevated basal glucocorticoid concentrations and a blunted glucocorticoid response to stress, as well as a prompt suppression of testosterone concentrations during stress. These facets have been interpreted as reflecting the chronic stress of social subordinance. In the present report, we find that these endocrine features do not mark all subordinate individuals. Instead, endocrine profiles differed among subordinate males as a function of particular stylistic traits of social behavior. A subset of subordinate males was identified who had significantly high rates of consortships, a behavior usually shown only by high-ranking males. Such behavior predicted the beginning transition to dominance, as these males were significantly more likely than other subordinates to have moved to the dominant half of the hierarchy over the subsequent 3 years. In keeping with this theme of emerging from subordinance, these individuals also had significantly larger glucocorticoid stress-responses, another feature typical of dominant males. However, these subordinate males also had significantly elevated basal glucocorticoid concentrations; it is suggested that this reflects that stressfulness of their overt and precocious strategy of reproductive competition. In support of this, subordinate males with high rates of covert “stolen copulations” did not show elevated basal glucocorticoid concentrations. A second subset of subordinate males were the most likely to initiate fights or to displace aggression onto a third party after losing a fight. These males had significantly or near-significantly elevated testosterone concentrations, compared to the remaining subordinate cohort. Moreover, these males had significantly lower basal glucocorticoid concentrations; this echoes an extensive literature showing that the availability of a displacement behavior (whether aggressive or otherwise) after a stressor decreases glucocorticoid secretion. In support of this interpretation suggesting that it was the initiation of these aggressive acts which attenuated glucocorticoid secretion, there was no association between glucocorticoid concentrations and participation (independent of initiation) in aggressive interactions. Thus, these findings suggest that variables other than rank alone may be associated with distinctive endocrine profiles, and that even in the face of a social stressor (such as subordinance), particular behavioral styles may attenuate the endocrine indices of stress. Am. J. Primatol. 42:25–39, 1997. © 1997 Wiley-Liss, Inc.     

Endocrine aspects of social instability in the olive baboon (Papio anubis)

The relationships among social status and the cortisol and testosterone stress-response were studied in the non-natal male members of a troop of olive baboons (Papio anubis) before and during a period of social instability. The unstable period was characterized by dominance interactions that were more frequent, more inconsistent, and produced less linear hierarchies than during the stable period. These changes occurred predominantly among the high-ranking males. Such males engaged in coalitions and consortship harassments at a higher rate during the unstable period than during the stable period. Finally, high-ranking males had the highest rates of involvement in and initiation of escalated fighting during the unstable period, in contrast with the stable period. A number of endocrine correlates of instability emerged. During the stable period, high-ranking males (by reproductive criteria) showed an endocrine profile different from that of subordinates. They had the lowest basal cortisol titers, the largest and fastest increases in cortisol titer during stress, and had elevated testosterone titers during stress. None of these attributes was found in high-ranking males during the unstable period. Males during the unstable period had elevated basal cortisol titers, suppressed cortisol responsiveness to stress, and no longer showed elevated testosterone titers during stress. When psychological advantages associated with social status in a stable social environment were lost, endocrine efficiency previously associated with social status was apparently also lost. Further, high-ranking males, who were most aggressive exclusively during the unstable period, had the highest absolute titers of testosterone exclusively during the unstable period. Thus, elevated testosterone and high levels of aggression were unrelated to social status during the period of social stability, but were traits associated with dominant individuals during the unstable period.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. II. Influence of Male Rank and Possible Competition for Partners

Allogrooming contributes to the development and maintenance of social relationships, including those that involve alliances, in many primate species. Variation in relatedness, dominance rank, and other factors can produce variation in the value of others as grooming partners. Several models have been developed to account for variation in the distribution of grooming in relation to dominance ranks. These start from the premise that individuals are attracted to high-ranking partners, but time limits, direct competition, and prior grooming engagement between high-ranking individuals can constrain access to them. Sambrook et al. (1995) formalized some of these models and showed the importance of taking group size variation into account when assessing them. Chimpanzees form multimale communities in which males are the philopatric sex. Males commonly associate and groom with each other; they also form dominance hierarchies and form alliances that influence dominance ranks and mating success. Both male rank and the rank distance between partners are significantly correlated with the distribution of grooming between males in an extremely large chimpanzee community at Ngogo, Kibale National Park, Uganda, that has more males than any other known community. High-ranking males had more grooming partners than mid- or low-ranking males. Grooming predominantly went up the dominance hierarchy, but was also concentrated among males that were close in rank. Rank and rank distance apparently both affected grooming independently of reciprocity in grooming and independently of the frequency with which males associated in temporary parties. However, the data do not clearly indicate how constraints on access to partners might have operated. Published data from a smaller chimpanzee community at Mahale show no rank or rank distance effect on male grooming. These results and earlier, conflicting findings on the association between dominance rank and grooming in male chimpanzees indicate that variation in group size, i.e., the number of males per community, probably influences the strength of any such effects, as happens for grooming between females in several cercopithecine species. Data on coalitions at Ngogo support the argument that high-ranking males are valuable social partners, and similarity in strategies of alliance formation may influence the distribution of grooming.     

Social relationships between adult male and female rhesus macaques: II. non-sexual affiliative behaviour

The social relationships of adult male rhesus macaques (Macaca mulatta) in Group I of the Cayo Santiago colony were studied over a period of 14 months. Relationships were found in which adult males and sexually mature females were persistently close to one another in nonsexual contexts, both within and across seasons. Males of long tenure and high dominance rank tended to have more female partners, and more persistent relationships, than more recent immigrants of lower rank. Correlations with length of tenure were stronger than those with dominance rank. Closely-related females tended to have persistent relationships with the same male. In most cases the female was primarily responsible for maintaining proximity in non-sexual contexts. Dyads which were persistently within 5 m of each other in the birth season were more likely to form a consortship in the subsequent mating season than those which had a brief relationship. A similar tendency was apparent in the 1 m data but it was not statistically significant. There was no association between persistent proximity during the birth season and the occurrence of long, or multiple consortships, nor with the maintenance of proximity or direction of grooming between consort partners. The pattern of consortships was not closely related to the formation of persistent relationships in the subsequent birth season. Females occasionally received protection from their male partners and, in some cases, spent more time in the feeding corral with them than did other females. Affiliative relationships can be very enduring and may have long-term benefits that were not apparent during the study period.     

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.     

Perineal swellings: a social and endocrine advantage for Barbary macaque females (Macaca sylvanus)

This study focuses the relationship between social rank, intersexual behavior, age, fecal cortisol equivalent excretion rates and perineal swelling size in contraceptive-treated Macaca sylvanus females. Behavioral data and fecal samples were collected during a twenty-week period from 24 females. Females were categorized with regard to perineal swelling (enlarged or reduced), and to their dominance rank (high or low); we found that swelling size was not associated with it. However, females with an enlarged perineum received more male grooming interactions, had closer spatial relations to males, and received significantly more interventions from males than did the others. Endocrinologically, females with enlarged swelling showed decreased fecal cortisol equivalent excretion rates. Multiple regression models showed a positive relationship between the extent of the swelling size and grooming, inspection and spatial relation. There was a negative relationship between the extent of swelling size and fecal cortisol equivalents. These results imply that enlarged perineal swellings among implanted Barbary macaque females have a greater impact on intersexual contact and adrenocortical activity than does social rank or age.     

Sex differences in the behaviour of immature captive lowland gorillas

Studies of the behaviour of 26 (12 males and 14 females) captive infant and juvenile lowland gorillas showed clear sex differences. Females showed greater interest in young infants and were more active in nest building as well as in solitary and social grooming. Males were more active in locomotive, dominance, and aggressive behaviour and in social play. Hand-rearing further increased aggression. Males were more aggressive when they lived with only one partner, and they rose in rank even above older females, a pattern that has not been observed in naturally reared gorillas.     

季节和等级顺位对雄性黄山短尾猴粪样皮质醇水平的影响

在长期的进化选择压力下,灵长类动物大多数群居生活,群体中的动物个体也面临来自群内成员强度不一的社会压力,压力大小的重要生理指标通常用其体内的皮质醇水平的变化来衡量.季节性繁殖的黄山短尾猴(Macaca thibetana),群体内的个体有严格的社会等级,是研究等级顺位与社会压力水平之间关系的理想研究对象.我们采集13只...     

Correlates of Male Consortship Rate in Free-Ranging Rhesus Macaques (Macaca mulatta)

Male–male competition for access to receptive females can take the form of nonrecurring fights and/or a sustained contest over mating opportunities. Male physical condition has been linked to dominance rank and reproductive success in species characterized by intrasexual fights for dominance and access to females. In group-living species characterized by endurance rivalry, however, factors contributing to male reproductive success are less well understood. In such species, particularly seasonally breeding ones with low sexual dimorphism and seniority-based rank, age and social factors other than rank may prove important. In the absence of genetic data, male mate guarding or consortship can serve as an indicator of male reproductive success. To evaluate the contribution of age and intragroup sociality to male consortship rate, I collected behavioral data during one nonmating and one mating season in two social groups of free-ranging rhesus macaques that experience no predation or food scarcity. Higher-ranking males, younger males, or males that exhibited lower rate of intrasexual aggression had higher consortship rates. Male–female dyads that groomed outside consortship did not form consortships as often as dyads that did not engage in nonconsort grooming. This is the first study to identify the significance of male–male aggression and male–female affiliation to male consortship rate in a species characterized by endurance rivalry, high male rank stability, and strong female mate choice. Social behaviors and male age may be particularly important in determining male reproductive success in populations experiencing high food availability and a lack of predation, which are typical of an increasing number of vertebrates in areas densely populated by humans.     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. I. Partner Number and Diversity and Grooming Reciprocity

Allogrooming serves many social functions in primates. Grooming can help individuals to service social relationships generally, sometimes reciprocally, and may be particularly important in the development and maintenance of alliances. However, time constraints limit the number of partners with whom one individual can groom enough to maintain cooperative relationships. As a result, the size of its grooming network may reach an asymptote as the size of its group increases, and it may distribute its grooming less equally among potential partners. Chimpanzees live in multimale, fission-fusion communities; males are philopatric, and commonly associate and groom with each other. Males form within-community alliances that influence dominance rank and access to mates, and allies groom with each other regularly; males also cooperate in aggression between communities. The chimpanzee community at Ngogo, in Kibale National Park, Uganda, is unusually large and has more males than any other known community. Field data show that adult Ngogo males groomed far more with other adult males than with females or with adolescent males, in contrast to a previous report (Ghiglieri, 1984). Adolescent males groomed adults much more than the reverse; males groomed and were groomed by females about equally. Individual males groomed mostly with a small number of other males. On average, males at Ngogo had only slightly more male grooming partners overall and had the same number of important partners as those of males in a much smaller community in the Mahale National Park, Tanzania, and they distributed their grooming less equitably. These results fit those expected if limits on available grooming time cause males to have a loyalty problem as the number of potential grooming and alliance partners increases. Despite differences in the extent and equitability of their grooming networks, males at both Ngogo and Mahale showed reciprocity in grooming. Grooming reciprocity has been demonstrated for captive chimpanzee males, but the Ngogo findings are the first demonstrations of reciprocity in wild communities.     

Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigena)

Concentration of the hormone cortisol is often used as an indicator of stress, and chronically high cortisol levels are often associated with poor health. Among group living animals that compete for resources, agonistic social interactions can be expected to contribute to variation in cortisol levels within and among individuals over time. Reproductive tactics of males can change with individual quality, relatedness, and social structure, and affect cortisol levels. In gray-cheeked mangabey (Lophocebus albigena) groups, male rank is an important factor in social interactions, and males also move between groups while actively competing for females or sneaking copulations. During a 20-month study we observed the social behavior and collected 461 fecal samples from 24 adult male gray-cheeked mangabeys from five groups in Kibale National Park, Uganda. Aggressive interactions and the presence of females at the peak of sexual swelling were associated with elevated cortisol concentrations in all males. Independently, dominant (i.e., highest-ranking) males within groups had higher cortisol concentrations than subordinate males, and immigrant males had higher cortisol concentrations than dominant males.     

Physiological and social influences on mounting behavior of troop-living female monkeys (Macaca fuscata)

Female mounting behavior was studied in a troop of Japanese macaques during one breeding season. Of 79 sexually active females, mounting behavior during consortships was shown by 50 females; 13 only with males, 20 with both males and females, and 17 only with females. Several factors associated with reproductive state influenced the expression of mounting activity. Recency of parturition influenced the mounting by females regardless of the type of partner. Females that had not given birth the previous spring (four to six months prior to the period of observation) were more likely both to mount partners and to produce an infant the following spring. These findings suggest the existence of a common factor, perhaps associated with lactation, inhibitory both to expression of mounting and to female fertility. Additionally, females that mounted were more likely to do so in consortships that followed than in those that preceded conception. This last finding suggests that, in this social context, the endocrine conditions of early pregnancy facilitated mounting to a greater extent than those associated with the cyclic ovary. Separate statistical analyses examined possible influences of age, dominance rank, and kinship on the likelihoods of mounting and being mounted. None of these factors influenced female mounting. Results suggest that the expression of mounting by females was more influenced by reproductive state than by social characteristics of the partner.     

Social grooming in Tonkean macaques (Macaca tonkeana)

The distribution, form, and contexts of occurrence of social grooming were studied in two captive groups of Tonkean macaques (Macaca tonkeana), using interaction-dependent sampling. The social events surrounding grooming had little influence on its form, the participants' behavior being shaped mainly by physical constraints. Adult females were most often involved in grooming interactions. Grooming between adult females appeared more intimate than that between adult males and females. Kinship and dominance had no effect on the form or distribution of social grooming among adult females. It is concluded that social systems that are characterized by mild dominance relations allow individuals the freedom to interact in the way and with whom they wish.     

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.     

Why should an aged male baboon ever transfer troops?

Dispersals by subadult or adult male baboons are common. In contrast, the occasional transfer of aged baboons is puzzling, given the physical dangers of transfer and the cognitive demands of mastering the ecological and social rules of a new troop. The present data suggest a possible explanation for such transfers in a study of two troops of olive baboons (Papio anubis) in Kenya. Aged males who remained in the troop in which they had been dominant were subjected to significantly higher rates of approach-avoid interactions by the current high-ranking cohort (i.e., the individuals they had dominated years past) when compared to males who had transferred into the troop in their old age. Thus, transfer in old age offers the advantage of relative anonymity. Of the 14 males who progressed into older adulthood in the same troop in which they were in their prime, seven ultimately transferred to a different troop. The seven who remained and the seven who transferred did not differ in the rate at which they were subjected to approach-avoid interactions. However, those who remained had significantly higher rates of various affiliative behaviors (copulations, consortships, grooming and contact with females, and positive interactions with infants). Thus, amid the disadvantages of an old age spent in the troop in which a male baboon was in his prime, a high degree of social affiliation might constitute a sufficient disincentive against transferring. © 1996 Wiley-Liss, Inc.     

Effect of female sexual displays on the endocrine physiology and behaviour of male white-crowned sparrows, Zonotrichia leucophrys

In photoperiodic birds, endocrine responses to behavioural interactions between males and females may be involved in temporally "fine-tuning" the onset of reproduction to yearly variations in the environment. This study examined the endocrine and behavioural responses of male White-crowned sparrows ( Zonotrichia leucophrys ) to changes in the endocrine state of the female, as signalled by changes in her behaviour. Males on different photoperiodic regimes were paired with oestrogen-treated, sexually receptive females. Males exposed to gonadostimulatory long days mounted and copulated with oestrogen-treated females even before gonadal development was complete. These males had higher plasma levels of testosterone and luteinizing hormone and maintained enlarged testes longer than control males paired with untreated, nonreceptive females. Males maintained on nonstimulatory short days also mounted oestrogen-treated females; however, testes of these males remained nonfunctional and their plasma levels of testosterone and luteinizing hormone were basal. Thus, reproductive function of photostimulated males is profoundly affected by changes in the endocrine state and behaviour of the female. However, male sexual behaviours are expressed in response to visual and auditory stimuli from the female regardless of male hormonal condition or photoperiodic treatment.     

Low-ranking individuals present high and unstable fecal cortisol levels in provisioned free-ranging adult male rhesus macaques (<Emphasis Type="Italic">Macaca mulatta</Emphasis>) during the birth season in a mountain area of northern China

Social hierarchy commonly exists in animal societies, affecting both the endocrine functioning and the behavior of animals. In nonhuman primates, the relationship between social rank and cortisol levels varies across species and even within species. Here, we assessed the relationships between social rank and fecal cortisol levels in adult male Taihangshan macaques (rhesus macaques, Macaca mulatta tcheliensis) from the provisioned, free-ranging Wulongkou-2 (WLK-2) group inhabiting Wulongkou Scenic Area, Jiyuan, China. From March to May 2014, we recorded 195 agonistic behaviors and collected 54 fresh fecal samples from eight adult male Taihangshan macaques. Males were assigned a social rank according to an agonistic behavior matrix, and enzyme-linked immunosorbent assay was then used to measure the cortisol concentration in the fecal samples. We found that social rank among the eight male Taihangshan macaques in WLK-2 group followed a strict linear hierarchy, and that fecal cortisol levels were significantly higher and more variable in low-ranking males than in more dominant individuals. Age was not significantly associated with social rank or fecal cortisol levels. Our results suggest that social rank and maintenance of the social hierarchy within the WLK-2 group is a chronic stressor, with low-ranking males maintaining heightened stress levels and enlarged reactive scope relative to dominant males. This provides new support for the theory that social environment can influence endocrine functioning.     

Mechanisms of sexual selection: sexual swellings and estrogen concentrations as fertility indicators and cues for male consort decisions in wild baboons

Male mate-guarding episodes ('consortships'), are taxonomically widespread, yet costly to individual males. Consequently, males should bias consortships toward females with whom the probability of conception is high. We combined data on consortships with visual scoring of sexual swellings and assays of fecal estrogen concentrations (fE) in a wild population of baboons (Papio cynocephalus) to test the hypotheses that sexual swellings are reliable indicators of (1) within-cycle timing of ovulation, (2) differences in conception probability among females that differ in maturational stage, and (3) conceptive versus non-conceptive cycles of parous females. We also evaluated whether adult males might rely on swellings or other estrogen-dependent signals (e.g., fE) for mate-guarding decisions. We found that sexual swellings reflected conception probability within and among cycles. Adult males limited their consortships to the turgescent phase of cycles, and consorted more with adult females than with newly cycling adolescents. The highest ranking (alpha) males discriminated more than did males of other ranks; they (1) limited their consortships to the 5-day peri-ovulatory period, (2) consorted more with adult than with adolescent females, and (3) consorted more with adult females on conceptive cycles than on non-conceptive cycles, all to a greater extent than did males of other ranks. Male mate choice based on sexual swellings and other estrogenic cues of fertility may result in sexual selection on these female traits and enhance dominance-based reproductive skew in males. Alpha males are the least constrained in their mating behavior and can best take advantage of these cues to mate selectively.     

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.