Social interactions among female rhesus macaques (Macaca mulatta) during the nonbreeding season: Responses to the introduction of males

When rhesus monkeys are observed in social groups during the breeding season, increases in interfemale aggression coincide with midcycle increases in sexual activity between males and females. However, some investigators have suggested that both aggressive and affiliative interactions between females are influenced by the presence or absence of males, irrespective of menstrual cycle stage. In the present study, social interactions among members of a captive group of rhesus females were measured during the non-breeding season in response to the introduction of rhesus males. Ovariectomized rhesus females (estrogen-treated or untreated) served as stimulus controls. Tests with males were characterized by significantly decreased interfemale proximity and grooming and significantly increased aggression from that seen in tests with stimulus females or in the absence of stimulus animals. Only interfemale proximity declined significantly during stimulus female tests, but results suggest that this may merely reflect a decline in this behavior that occurs across the course of the day. Estrogen treatment did not alter either the aggressive or affiliative behavior of stimulus females or group female response to stimulus females. The possibility is discussed that changes in interfemale interactions during tests with males reflect female interest in interacting with the male, particularly under social conditions that may limit such interactions.     

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

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

Serum testosterone, male dominance, and aggression in captive groups of vervet monkeys (Cercopithecus aethiops sabaeus)

The relationship of serum testosterone concentration to male dominance rank and frequency of aggression was investigated in stable vervet monkey social groups, each containing two or three adult males, several adult females, and their offspring. Dominance relationships were determined by noting an animal's success in intermale aggressive encounters. A striking finding was the marked within-subject variation in testosterone concentration: 5- to 10-fold fluctuations were often observed on successive days. When all 15 groups were considered together, testosterone concentration was unrelated to dominance rank. Although mean testosterone concentration for all dominant males was higher than the mean for all subordinate males, this difference was not significant. In a subset of 4 groups, the rate of aggression initiated was significantly correlated with same-day testosterone in dominant but not in subordinate males.     

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

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

Intermale aggression of subordinate resident long-evans rats

Dominant male rats were separated from their colonies and subordinate residents were tested for aggression after a two week period. Subordinate animals showed significant increases in body weight and aggressive behavior toward intruders. Replacement of the previously dominant male led to rank reversals in three of six colonies. To assess whether two weeks of separation from the dominant male was necessary for subordinate males to exhibit aggression towards conspecifics, another intruder test was given following an additional two weeks of social housing. At the conclusion of this test, the more aggressive resident was removed and a naive intruder was immediately introduced into the colony with the subordinate male resident and again at 1, 5, and 10 day intervals. Aggressive posturing by the subordinate resident increased immediately following the removal of the dominant male, and remained at a high level throughout the subsequent intruder tests. In contrast, biting was initially low but increased steadily throughout the period of separation. These findings demonstrated that social or situational changes within a colony can greatly influence the aggression of subordinate males.     

Sneaky Monkeys: An Audience Effect of Male Rhesus Macaques (Macaca mulatta) on Sexual Behavior

Males and females have different sexual interests and subsequently may show conflicting sexual strategies. While dominant males try to monopolize females, promiscuity benefits females and subordinate males. One way to escape monopolization by dominant males is to copulate in their absence. We tested this inhibitory effect of males on the sexual behavior of their group members in captive group‐living Rhesus macaques. Copulations between females and nonalpha males almost exclusively took place when the alpha male was out of sight. Furthermore, the inhibiting effect was not unique for the alpha male. An upcoming nonalpha male also inhibited copulations of its group members, and three other nonalpha males inhibited female copulation solicitations. Females adjusted their behavior to the presence of bystander males, as they initiated and accepted initiations more often in absence than in presence of bystander males. Although not significant, in males, a similar pattern was found. The observed reduction in mating behavior in presence of bystander males is in accordance with an “audience effect,” in which the behavior is modulated in relation to the presence or absence of third parties. This audience effect may serve as an important mechanism to reduce (aggressive) interruptions of subordinate male copulations.     

Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus)

Cortisol excretion in males of group living species is often associated with social rank and competition for oestrous females. Rank-related patterns of cortisol levels can be used to study mechanisms of rank maintenance and costs associated with mate competition. Bonobos (Pan paniscus) are interesting because males form a linear dominance hierarchy but are not dominant over females and therefore aggressive male-male competition over access to females alone is not considered to be a successful reproductive strategy. In this study on social correlates of urinary cortisol in wild male bonobos, we investigated the relationship between cortisol levels and several aspects of mate competition, including male rank, aggression rates, and association time with oestrous females. We found that cortisol levels correlated positively with dominance rank when oestrous females were present, but not when they were absent. This result is consistent with the idea that aggressive behaviour plays a minor role in maintenance of high rank. While aggression received from males and females explained within-individual variation in cortisol levels, it was the time spent in association with oestrous females that best explained between-individual variation in male cortisol levels. The observed increase in male cortisol may be associated with spatial proximity to oestrous females and could result from anticipated aggression from other group members, reduced feeding time in the males, or a combination of both.     

Removal of both antennae influences the courtship and aggressive behaviors in male crickets

To test whether insect antennae are necessary for eliciting courtship and aggression toward appropriate partners, we antennectomized adult male crickets (Gryllus bimaculatus) and observed their behavior toward other antennectomized males and intact females. At 7 days after removal of both antennae, pairs of antennectomized males were placed together; 80% displayed courtship behavior, generating courtship song by rubbing their forewings together, toward other antennectomized males, and 20% displayed aggressive behavior. Only 45% courted intact females. No intact males courted antennectomized males, and 80% displayed aggressive behavior. All intact males courted females. The results for males with one antenna removed were essentially the same as for intact males. These findings indicate that a high proportion of male crickets with both antennae removed court other males and fail to display male-male aggression, demonstrating that removal of antennae from male crickets induces male-male courtship and that an antenna is necessary for the expression of male-male aggression. Moreover, brain serotonin (5-hydroxytryptamine; 5-HT) levels in male crickets were significantly reduced at 7 days after removal of antennae. The reduction of 5-HT was detected primarily in the central body of the brain. Thus, 5-HT in the central body of the male cricket brain may be involved in the behavioral changes.     

The function of male aggressive displays towards females in mountain gorillas

In groups ofGorilla g. beringei, male aggression towards females regularly takes the form of male display. This paper examines male display towards females in two Karisoke study groups (Group 5 and Group BM) in 1989, a period when none of the females were new immigrants. Results are based on 259 hr of focal observations and 121 hr ofad libitum observations on male behaviors towards females. The goal is to see if the data are compatible with four non-mutually exclusive hypotheses to explain male displays towards females: (1) demonstration of male fighting abilities to influence female long term residence decision; (2) decrease potential competitive inequities between females; (3) provision to females of an occasion to confirm their subordinance to a male; and (4) short term influence on mating. First, male-female proximity was tested against proportion of male displays, to rule out the possibility that males display towards females simply because they happen to be close by. There was no association between proximity and male display. Dominant males were responsible for a higher proportion of displays than subordinate males. This is consistent with the idea that males display to demonstrate their fighting abilities, or their qualities as protector, since dominant males are the ones offering long term protection against infanticide and predators. Females that were in a position to transfer did not receive a higher proportion of male display, however. Long term resident dominant females received a higher proportion of displays from the dominant males, which is consistent with the idea that males attempt to decrease potential competitive inequities between females. There was an association between female appeasement reactions and male displays, which suggests that males display to create occasions for the females to confirm their subordinance to them. Estrous females did not receive a higher proportion of male displays, and there was no association between male display and copulation, suggesting that male displays are not a form of courtship aggression aimed at influencing mating in the short term.     

Female mate choice in vervet monkeys (Cercopithecus aethiops sabaeus)

Female mate choice was examined in a captive group of vervet monkeys (Cercopithecus aethiops sabaeus). Male-female interactions were examined under both dyadic and group conditions to determine whether females mate with different males under the two conditions. Results showed that all females preferred to mate with the alpha male under both dyadic and group conditions. Alpha females, however, were more successful than subordinate females in rejecting the sexual solicitations of subordinate males. Thus female dominance status played an important role in determining the degree to which females exercised mate choice.     

Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi)

Studies in anthropoid primates and other mammals suggest that reproductive season, rank, reproductive skew, aggression received, and social support are the major factors influencing glucocorticoid output. In which way these are also affecting adrenal function in lemurid primates has been studied rarely. Here, we examine the influence of reproductive season and rank on glucocorticoid output in male sifakas (Propithecus verreauxi), a species characterized by high breeding seasonality, a hierarchy among males and extreme reproductive skew towards dominant males. We established a fecal assay for non-invasively monitoring adrenal activity and collected 315 fecal samples during the reproductive and birth season from 10 male sifakas living in 5 groups in Western Madagascar. We found a significant effect of season on glucocorticoid output, with males exhibiting higher fecal glucocorticoid levels during the reproductive compared to the birth season in conjunction with an increase in overall aggression rates during the former period. Moreover, our data indicate a significant effect of rank on adrenocortical activity with dominant males exhibiting higher glucocorticoid levels than subordinate males in the reproductive season. However, dominant males did not differ significantly in rates of initiated or received aggression and rates of affiliative behavior from subordinates but showed significantly lower rates of submission. Given their highly formalized dominance relationships, we conclude that higher glucocorticoid output in dominant males during the 4-month reproductive season is likely related to higher energetic demands necessary to cope with the challenges of male reproduction rather than to physical demands of increased fighting frequency to maintain dominance status. High rank in sifakas may thus carry high costs, which, however, may be outweighed by monopolization of almost all paternities. In sum, our data generally support the findings on the relationship between environmental and social factors and glucocorticoid output found in non-lemurid primates.     

Ontogenetic changes and the stability of rhesus monkey dominance relationships

Dominance relationships were studied in a rhesus monkey group during five consecutive years. The group consisted of eight stable matriarchies and an adult male class which was replaced at the start, and again at the midpoint, of the study. Immature males were selectively harvested to maintain a sex ratio typical of natural troops. Maximum group size during the study was 77 animals.Dominance relationships were remarkably stable, with only 4.4% of dyads failing to show unidirectional relationships. Despite this stability, a linear ranking of all group members was not possible. Male dominance relationships with other males were among the most stable, following the fighting which ensued on male introductions. Male introductions did not disrupt female dominance relationships.Adult female dominance relationships were also quite stable, but immature females slowly achieved dominance over older sisters and females subordinate to their mothers. Such reversals were the result of processes lasting over many months. Many dominance assertions occurred prior to puberty but a significant number occurred following sexual maturity. Maturing females did not reverse dominance relationships according to any particular hierarchial order and, as a consequence, many were subordinate to animals that were dominated by others that they dominated.Although there was an alpha male that was dominant to all animals in the group, adult females dominated most adult males. Adult males, however, often reciprocated aggression directed at them. They almost invariably threatened or countercharged aggressive immature animals regardless of matriarchial membership. Adult males dominated some adult and most young females, even in families containing matriarchs and adult females to which the adult males always submitted.The dominance relationships of young males were similar to those of their sisters, until puberty. Young males did not necessarily bypass adult males that their mothers outranked, and often failed to win against adult females that their mothers dominated. Adolescent female aggression against females is seldom interfered with by adult males, and females may actively aid one another against males. In contrast, the aggression of young males often elicits interference by adult males, and young males often become the targets of redirected aggression in the group. As a consequence, whereas young females rise in rank to positions adjacent to their mothers, adolescent males often suffer losses to animals that they had dominated as juveniles.     

Hormonal responses to removal of a breeding male in the cooperatively breeding white-browed sparrow weaver, Plocepasser mahali.

The white-browed sparrow weaver (Plocepasser mahali) is a cooperatively breeding Ploceid finch that lives in groups of up to 11 individuals. Each group consists of a dominant breeding male and female and a varying number of nonreproductive birds that help feed young and defend the group territory. Experimental removal of the dominant male resulted in attempts by other males to take over the group. Removal of a subordinate, nonbreeding male, as a control, resulted in no change of status among group members. During takeover, there was a transitory increase in plasma levels of luteinizing hormone in the new dominant male, but no change in testosterone levels. As reported in previous investigations, dominant males tended to have higher levels of testosterone than females or subordinate males, but this was not related to the heightened aggression of the takeover. Plasma levels of luteinizing hormone, testosterone, and corticosterone did not differ between the other status groups. The possibility that luteinizing hormone, or a hitherto unidentified androgen, may regulate aggression in the white-browed sparrow weaver is discussed.     

Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females

A long-term study of immigrant male spotted hyenas (Crocuta crocuta) living in large multimale/multifemale groups (clans) demonstrated that males acquire social status by queuing. Maximumlikelihood estimates of parameters of a stochastic queuingmodel that assessed queuing discipline confirmed that immigrantmales respected the convention that their positions in a queueof typically 15 or more individuals was determined by theirsequence of arrival. Levels of aggression among males were low;males did not attempt to improve their social status throughphysical contests. Size and body mass did not influence malesocial status. The stability of queues was insured by an increasein the rate at which males formed coalitions against othermales as they rose in social status and by coalitions between high-ranked males and dominant females. High-ranked, long-tenuredmales chiefly consorted with ("shadowed") and focused theiraffiliative behavior on females of high reproductive valueand disrupted attempts by subordinate males to associate withthese females. High-ranked males also supported females againstlower-ranked males that harassed them. In contrast, lower-ranked,short-tenured males focused their affiliative behavior on young adult females and rarely shadowed or defended females. Malesthat did not disperse from their natal clan (nondispersers)quickly acquired top rank in the male social hierarchy. Irrespectiveof the social status acquired from their mother when young,nondisperser adult males submitted to all adult females.     

The development of affiliative and coercive reproductive tactics in male chimpanzees

Like many animals, adult male chimpanzees often compete for a limited number of mates. They fight other males as they strive for status that confers reproductive benefits and use aggression to coerce females to mate with them. Nevertheless, small-bodied, socially immature adolescent male chimpanzees, who cannot compete with older males for status nor intimidate females, father offspring. We investigated how they do so through a study of adolescent and young adult males at Ngogo in Kibale National Park, Uganda. Adolescent males mated with nulliparous females and reproduced primarily with these first-time mothers, who are not preferred as mating partners by older males. Two other factors, affiliation and aggression, also influenced mating success. Specifically, the strength of affiliative bonds that males formed with females and the amount of aggression males directed toward females predicted male mating success. The effect of male aggression toward females on mating success increased as males aged, especially when they directed it toward females with whom they shared affiliative bonds. These results mirror sexual coercion in humans, which occurs most often between males and females involved in close, affiliative relationships.     

Intergroup affiliative interactions and intergroup transfer of young male Japanese macaques (Macaca fuscata)

The social interactions between young male Japanese macaques (Macaca fuscata) and members of two adjacent groups were studied. Young males usually associated with members of a single group. Although some young males occasionally interacted with members of the neighboring group, the frequency of their intergroup affiliative interactions was much lower than that of their intragroup interactions. The intergroup affiliative interactions were less symmetrical than the intragroup interactions. Three- or four-year-old males who remained in their natal group interacted with males of the neighboring group, whereas males over 5 years old did not. Young males revealed a dramatic change in their association partners from males in one group to those in another during the course of their intergroup transfer. Males who remained in their natal group did not attempt to interact with females of the neighboring group. In contrast, males who had transferred to a non-natal group interacted with females in their natal group. It is suggested that intergroup affiliative interactions and intergroup transfer of young male macaques are influenced by close associations between males. The immediate motivation for transfer of young natal macaques may be some attraction to males outside their group rather than sexual attraction to unfamiliar females.     

Sexual activity of male rhesus monkeys introduced into a heterosexual group.

Unfamiliar males were introduced during the breeding season to a stable heterosexual group of rhesus monkeys to determine how the presence of more dominant resident males affected their mating activity and how their entry was received by resident females. Initially, new males were allowed access to females under controlled conditions both in the presence and absence of resident males, simulating situations which may occur under natural conditions. Results indicated that the sexual activity, including ejaculation rate, of the new males was initially inhibited by the presence of more dominant, resident males, but these inhibiting properties did not carry over to periods when the resident males were absent and were diminished with time. Group females preferentially directed their behavior towards the new males throughout the study. These data suggest that although entry of new males into a stable group is at low rank, their subsequent reproductive success may not be reduced and that the association with resident females may facilitate male rhesus transfer between groups observed during the breeding season.     

Greeting behavior during party encounters in captive chimpanzees

Party encounter situations were experimentally produced in a group of captive chimpanzees (Pan troglodytes verus) at the Primate Research Institute of Kyoto University, Japan. During weekends all subjects (two adult males and five adult females) usually stayed together in the rooms (Baseline condition). Under experimental conditions, we shut passages between rooms to divide the subjects into two groups. We examined the effects of temporal separation of group members on affiliative interactions, aggressive interactions, and simple proximity. The frequency of affiliative interactions between male and female chimpanzees and between female chimpanzees increased when they encountered one another after separation, irrespective of male identity or housing history. Therefore we considered affiliative interactions between males and females during party encounters as being the response between separated individuals. The same tendency was not found in the frequency of affiliative interactions between females or between males. Unlike affiliative interactions, neither aggressive interactions nor simple proximity were influenced by separation.     

Intermale affiliative behavior in ringtailed lemurs (Lemur catta) at the Beza-Mahafaly reserve, Madagascar

Intermale affiliative behavior was studied in three groups of naturally occurring ringtailed lemurs over a one-year period. The adult males in the sample exhibited affiliative behavior with all other males in their social groups; but affiliative behavior between some male-male dyads occurred markedly more often than between others. These dyads are called “preferred partnerships.” The formation of preferred partnerships did not appear to be influenced by male dominance rank or age-class. Furthermore, these partnerships were of a short-term nature, and none persisted throughout the entire study period. The following factors may explain the absence of rank or age effects, and the brevity of preferred partnerships: (1) frequent fluctuation in the male dominance hierarchy in each study group; (2) the fact that higher-ranking males may not offer specific benefits to lower-ranking males; and (3) the fact that male dispersal affected the male membership of each group over the 12-month study period. The focal males engaged in significantly more affiliative behavior during the lactation period compared with the other reproductive seasons. Migration partners may offer each other predator protection during the transfer process, and although males that transfer together do not engage in alliance or coalition behavior towards resident males, males transferring in pairs or threesomes are in a better position to spot and defend themselves against attack by resident males. Migration partners also provide social contact for each other while in the process of immigration.     

Male-female affiliative relationships in naturally occurring ringtailed lemurs (Lemur catta) at the Beza-Mahafaly Reserve,Madagascar

Affiliative behavior between adult male and female ringtailed lemurs was examined as part of a project concerning male affiliation with conspecifics of all age/sex classes. Males in three social groups were studied over a 12 month period. Male-female preferred partnerships existed, and were variable according to reproductive season. Dominance rank, age, or tenure of the male did not appear to affect either the number of partnerships or frequency of affiliative behaviors that males had with females. However, males residing in groups with fewer males exhibited both higher frequencies of affiliative interactions with females and were nearest neighbors to females more often than males living in a group containing more males. Females were found to be responsible for proximity maintenance of male-female dyads in the majority of cases. Neither reproductive season nor seasonal availability of food resources strongly affected the frequency of affiliative interactions between males and females, it is proposed that an important aspect of successful group membership for male ringtailed lemurs relates to the development of social relationships with adult females. Males can benefit from such relationships in terms of greater centrality to the spatial core of the group, which can result in enhanced predator protection, greater opportunities for social contact, and potentially greater access to estrous females. © 1996 Wiley-Liss, Inc.