Toward a comparative socioecology of the genus Macaca: Different dominance styles in rhesus and stumptail monkeys

Captive studies can make a unique contribution to primate socioecology by documenting species-typical social dispositions under controlled conditions. Recent theories seek to connect the dominance relationships, group cohesiveness, and feeding ecology of primates. The present study explores the first two aspects by comparing the social organization of rhesus (Macaca mulatta) and stumptail monkeys (M. arctoides). Data were collected over a period of eight years, with five different methods, on three well-established captive groups in identical environments. The groups were found to share one characteristic: a clear-cut, linear formal dominance hierarchy as expressed in teeth-baring displays. The two main study groups (one of each species) differed significantly, however, with respect to nine of eleven behavioral measures. In addition to a previously reported higher frequency of reconciliation in the stumptail group, this group showed (1) more frequent but less severe aggressive behavior, (2) greater symmetry of contests, (3) greater social tolerance, (4) more nonagonistic approaches, and (5) more allogrooming. The differences can be summarized as a contrast in dominance “style,” with the stumptails having a more relaxed style and placing greater emphasis on social cohesion than the rhesus monkeys. An egalitarian attitude was also reflected in approach behavior: contacts in the rhesus group were mostly initiated by dominants, whereas contacts in the stumptail group were initiated independent of rank. Comparisons with a second rhesus group, and with published reports, suggest that while some of the observed differences are probably representative of the two species, considerable intraspecific variation does exist, and a more comprehensive program of comparative studies is needed.     

A simple ethological monitoring system to assess social stress in group-housed laboratory rhesus macaques.

The increasing awareness of the importance of social housing of laboratory primates results in the establishment of group housing in many facilities. Our aim was to develop a set of manageable tools to allow continuous monitoring of social relations within groups and to establish an objective, scientific ground on which changes in group composition could be based. We studied 38 adult rhesus monkeys (Macaca mulatta) grouped as five one-male/multi-female groups using focal sampling. We recorded the occurrence and direction of aggressive and non-aggressive social interactions as well as time spent inactive in proportion to social contacts, feeding and other activities. The present analysis clearly identified low-ranking animals with none or few affiliative contacts and who also spent much time inactive and separated from other low-ranking animals. This suggests that the present approach results in useful information concerning compatibility between group members and enables identification of animals experiencing high social stress.     

Behavioural and hormonal responses of male rhesus monkeys introduced to females in the breeding and non-breeding seasons.

Six adult male rhesus monkeys were introduced individually to an all-female group for 10 days during the mating season. The initial aggressive responses of the females were rapidly replaced by positive social behaviour, and each male achieved alpha status and had access to social and sexual partners. A repetition of this paradigm in the non-breeding season produced significantly more female aggression, and no male attained high rank or engaged in sexual or other social behaviour. Male testosterone levels rose following introduction to the females in both seasons, but were significantly higher during the breeding season. Hormonal levels following removal from the females suggest a complex interplay between social, sexual and seasonal variables and recent social experiences. The differences in female social behaviour with newly introduced males, as a function of season, suggest an explanation for the seasonal limitation of male troop transfers.     

Impaired reconciliation in rhesus macaques with a history of early weaning and disturbed socialization

An attempt had been made to create five social groups from rhesus macaques with a history of early separation from their mothers, early weaning and hand feeding and, in most cases, previous housing in single cages. We investigated the exchange of affiliative behaviours after an aggressive encounter and selective attraction to the former opponent, a phenomenon previously well described in rhesus monkeys and called reconciliation. Evidence for reconciliation was only found in one of the five groups studied (corrected conciliatory tendency=13%). This group consisted of younger animals that had, at least temporarily, been living together after separation from their mothers. In the other groups studied, containing animals with a varied background, aggressive interactions were not followed by affiliative behaviours or attraction between former opponents. Our results indicate that the use of reconciliatory behaviours in adult monkeys is dependent upon social training. Lack of functional reconciliation might be one of the explanations to the severe and uncontrolled aggression previously found in groups of rhesus macaques created from animals with disturbed early socialization.     

Observations on the behaviour and ecology of the Patas monkey (Erythrocebus patas) in the Waza Reserve, Cameroon

Observations on the behaviour and ecology of Patas monkeys in Cameroon complement those made in Uganda by Hall (1965) and contribute to an understanding of the proximate factors involved in the maintenance of Patas social structure and to seasonal changes in their behaviour and ecology. The heterosexual groups had a mean size of 21. Five all-male groups were seen. High proportions of similarly sized infants indicate that there is a birth season at Waza from November to January inclusive. At the peak of the dry season intergroup contacts were very common at the water holes. The frequency of agonistic encounters increased remarkably at this time, especially between monkeys of different groups. The nature of these encounters indicated that the harem males are effective in driving off extragroup males and that females and juveniles are instrumental in maintaining space and social exclusiveness between heterosexual groups. The frequency of interspecific encounters also increased at the peak of the dry season.     

Coping with social tension: Sex differences in the effect of food provision to small rhesus monkey groups

In previous research, male chimpanzees (Pan troglodytes) were found to be more ‘conciliatory’ than females, in that after aggressive incidents males more often engaged in socially positive contact with former opponents. The first part of the present paper presents similar results for a large breeding troop of rhesus monkeys (Macaca mulatta). To investigate further the possible sex difference in postconflict behaviour, a series of experiments was carried out on small isosexual groups of young rhesus monkeys, three male and three female groups. Food competition was created by providing either a single apple piece (Monopoly test) or a handful of small pieces (Equality test). Observations lasted for 30 min, and behaviour in tests without food provisioning was also recorded. The predicted response to food was an increase in aggression followed by restorative behaviour, such as grooming. In Equality tests both sexes showed similar responses, i.e. increased aggression and decreased grooming and cohesiveness. In Monopoly tests, however, their responses differed. After the aggression increase, which occurred in all groups, males showed a significant increase in grooming and cohesiveness, whereas females showed the (non-significant) opposite trend. Another sex difference was that changes in grooming and aggression frequencies were related to the rank order in female groups, but not in male groups. Since there was no evidence for a direct causal connection between grooming and aggression, a new model is introduced which links grooming behaviour to the type of food provision rather than to the social disturbance by aggression. According to this model inequality in food distribution causes social tensions. Males actively try to reduce these tensions, whereas females do not. Some alternative explanations are also discussed.     

Effects of artificial feeding on aggressive behaviour of rhesus monkeys in India

Artificial feeding of rhesus monkeys (Macaca mulatta), which provides the major food source for most rhesus groups in rural and urban habitats, is common practice in India. Such feeding results in significant increases in aggressive competition within the monkey groups: during feeding periods the frequencies of aggressive threats, chases, and attacks increased two to six times above those of non-feeding periods in each of eight different groups. Fighting behaviour did not increase in most groups studied, but did show a rise in one large urban group in Calcutta. The implications of these results for the management of primate breeding colonies are discussed.     

Effect of stressor factors on the behavior of monkeys. III. The behavior of rhesus macaques during immobilization stress

The three-hour immobilizational stress in two groups of males of rhesus monkeys at the age of 7-8 and 10-12 years has been investigated. The reaction on the stress has been established to depend on the age of animals. The young males bear the stress easier, their behaviour after it is practically normal. The normal behaviour of the elder animals restores during 24 hours after immobilization. A comparative analysis of hamadryas baboons and rhesus monkeys behaviour during this type of stress has been carried out. These species differ by their reaction on stress: Papio hamadryas serve as a model of hard depressive stress, the rhesus monkeys--a model of slight-stimulative stress. The peculiarities of stress bearing depend on the selected species, age of the animal, the type of social organization and individual features of behaviour.     

Observations on agonistic behaviour of Clarias gariepinus larvae and juveniles under different densities and feeding frequencies in a controlled environment

Ten-day-old African catfish larvae, Clarias gariepinus , were stocked in aquaria at 5, 13, 22, and 30 larvae per liter with fish at each density being fed three and six times per day over 35 days. Fish were fed with an artificial diet in excess of their satiation requirements at each feeding. Every week total length was determined for samples of 25 fish per tank and all fish were counted at weekly intervals. Behaviour patterns were categorized into timed behaviour (i.e. resting, swimming and browsing), and frequency events e.g. number of contacts, aggressive contacts and number of head or body attacks. Fish at the lowest density grew faster than fish at the other densities. Feeding frequency had no effect on growth. With increasing densities fish less frequently changed timed behaviour patterns while spending a greater percentage of the time swimming. Aggressive behaviour was highest at the lowest density but remained uninfluenced at densities greater than five fish per litre. The high feeding frequency provoked a higher rate of aggressive contacts than the low feeding frequency. A suggested explanation was that these fish were more often in anticipation of food and consequently more active between feedings. In summary, it was shown that density had an effect on duration behaviour patterns such as resting and swimming, while feeding frequency significantly influenced frequency events, in particular the rate of aggressive behaviour. The study contributes to an understanding of factors influencing C. gariepinus juvenile behaviour and suggestions for follow-up experiments are discussed.     

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.     

Self-aggression in macaques: Five case studies

Spontaneous self-aggressive behaviors were observed in five adult male rhesus monkeys (Macaca mulatta) housed at a university facility. All were individually caged, were free of intercurrent disease, and were being utilized in ongoing research studies. The self-aggressive behaviors observed included self-biting, self-clasping, self-slapping, self-rubbing and threatening of body parts. In several cases, wounds were inflicted and medical treatment was required due to the severity of the lesions. A review of the animals' clinical histories revealed an increased level of self-aggressive behavior in four of five monkeys during such stressful or stimulating conditions as movement of the animal to a new cage, movement of animals out of the room or escape of other monkeys from their cages. The frequency with which these behaviors occurred was quantitated experimentally. The results revealed an increased level of self-aggressive behavior in two of these animals during the videotaped sessions in response to aggressive contacts with the investigator. In contrast, one monkey exhibited self-aggressive behavior both clinically and experimentally in the absence of environmental stimuli or human contact. Clinical management of self-aggressive monkeys included housing monkeys only with physically smaller primates, decreasing the level of environmental stimuli, and drug therapy. Haloperidol was used with success in one animal that exhibited severe self-aggressive behavior.     

Age-related changes in diurnal rhythms and levels of gonadotropins, testosterone, and inhibin B in male rhesus monkeys (Macaca mulatta)

Testosterone shows circadian rhythms in monkeys with low serum levels in the morning hours. The decline relies on a diminished frequency of LH pulses. Inhibin B shows no diurnal patterns. In elderly men, the diurnal rhythm of testosterone is blunted and inhibin levels fall. Here we explore whether aging exerts similar effects in the rhesus monkey. We collected blood samples from groups of young (6-9 yr) and old (12-16 yr) male rhesus monkeys at 20-min intervals for a period of 24 h under remote sampling via a venous catheter. We determined moment-to-moment changes in plasma levels of testosterone, FSH, and LH by RIA, and of inhibin B by ELISA. We found significant diurnal patterns of testosterone in both groups. The circadian rhythm in testosterone was enhanced in older monkeys. Testosterone levels and pulse frequencies dropped significantly below those of young monkeys during midday hours. Diminished pulse frequency of LH appeared to be responsible for the midday testosterone decrease in old monkeys, while LH and testosterone pulse frequency did not change in young monkeys at corresponding time points. Old monkeys showed extended periods of LH-pulse quiescence in the morning and midday hours. Inhibin B and FSH levels were generally lower in old monkeys compared with the young group, but neither inhibin B nor FSH showed circadian rhythms. We conclude from these data that old rhesus monkeys have a more prominent circadian rhythm of LH and testosterone resulting from an extended midday period of quiescence in the hypothalamus-pituitary-gonadal axis.     

A ten-month study of endogenous testosterone levels and behaviour in outdoor-living female rhesus monkeys (Macaca mulatta)

Endogenous testosterone levels were measured in association with sexual, aggressive, and social/affiliative behaviors in 11 outdoor-housed female rhesus monkeys over a ten-month period. Several behaviors (sex directed toward the male, sex received from the male, aggression directed toward the male, submission directed toward the male, submission directed toward the female, and groom another female) were significantly (p<0.05) positively correlated with testosterone in from one to five females. No trends were strong enough across all females to suggest that any of these correlations have species-wide significance. Factor analysis revealed clearcut clusters of behaviors, but elevations in testosterone were not strongly associated with any of these clusters. It is concluded that endogenous testosterone levels have little measurable effect on overt behavior in female rhesus monkeys.     

Species preference by infant macaques with controlled social experience

In Experiment 1, infant Japanese monkeys and rhesus monkeys were artificially reared in pairs with conspecific or heterospecific monkeys. Preferences of these monkeys for a variety of pictures of Japanese monkeys and rhesus monkeys were repeatedly tested during the first 1 or 2 years of life. The duration of lever-pressing responses to see those pictures was a measure of the preference. All monkeys, Japanese or rhesus, preferred pictures of rhesus monkeys to pictures of Japanese monkeys, without regard to their social experiences. Experiment 2, with an adult Japanese monkey as the subject, and Experiment 3, with different pictures as stimuli, suggested that this preference was not a consequence of any bias in the pictures used. In Experiment 4, a Japanese monkey reared by a rhesus foster mother and rhesus monkeys reared by Japanese monkey mothers received the same preference test. The Japanese monkey infant preferred to see pictures of rhesus monkeys. However, rhesus infants did not show clear species preferences. These results suggest that infants of both Japanese and rhesus monkeys have a native tendency to prefer to see physical characteristics of rhesus monkeys over Japanese monkeys.     

Social enrichment of the environment with infants for singly caged adult rhesus monkeys

The practicability of social enrichment for singly caged adult rhesus monkeys was examined. Twenty-nine weaned rhesus monkey infants were removed from breeding troops to avoid overcrowding and were placed with unfamiliar singly caged adults. An adult-infant pair was considered compatible when (1) the two animals started huddling with each other within the first 5 days after pair formation and (2) the infant showed no signs of depression and took its share from a limited amount of favored food. Adult-infant pairs were compatible in 90% (26/29) of cases. Compatibility depended neither on the sex, age, and origin of the adult nor on the sex of the infant. There was no evidence that partners lost interest in each other during 7–11 months of follow-up observations. Three adults exhibiting stereotypical behavior abandoned their peculiar habits after they had lived with their young companions for 4 months. It was concluded that the often-heard notion that rhesus monkeys are highly aggressive should not prevent simple attempts to provide singly caged animals with a companion.     

An analysis of dyadic interactions of male Japanese monkeys (Macaca fuscata fuscata) in a cage-room observation

This is a laboratory observation (Home-cage and observation room) for individual and social behavior of four male Japanese monkeys. The monkeys were placed in a dyadic and trio situation with the purpose to investigate the relationships between aggressive and affinitive factors which regulated their social behaviour. Total amounts of attacks and receiving groom showed a consistent order for four monkeys through the pairwise conditions, which was presumed to indicate a dominance order. Grooming and mounting behavior, however, were influenced by the particular dyadic interactions, probably social attraction, rather than dominance order itself. The presence of the third animal facilitated such a social preference between animals positioned closely in the rank order as well as elicited aggression from the dominant animals.     

Development of visual preference for closely related species by infant and juvenile macaques with restricted social experience

Japanese and rhesus monkeys aged between 9 months old and 5 yrs old pressed a lever to see a variety of pictures of seven macaque species. These monkeys had various restricted social experience: namely, either reared by humans with conspecific or heterospecific peers, or cross-fostered between these two species. Rhesus monkeys tended to prefer seeing rhesus monkeys best among the pictures of the seven species without regard to their age or social experience. Japanese monkeys having restricted experience also liked to see rhesus monkeys better than Japanese monkeys, but not the best among the seven species. In a previous study, mother-reared infants of Japanese monkeys preferred seeing pictures of their own species over those of rhesus monkeys. These results suggest a dissociation of the determinants of this basic social preference: rhesus monkeys prefer to see their own species by nature while Japanese monkeys may learn to prefer their own species.     

Effects of prenatal androgens on rhesus monkeys: A model system to explore the organizational hypothesis in primates

After proposing the organizational hypothesis from research in prenatally androgenized guinea pigs (Phoenix, C.H., Goy, R.W., Gerall, A.A., Young, W.C., 1959. Organizational action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65, 369–382.), the same authors almost immediately extended the hypothesis to a nonhuman primate model, the rhesus monkey. Studies over the last 50 years have verified that prenatal androgens have permanent effects in rhesus monkeys on the neural circuits that underlie sexually dimorphic behaviors. These behaviors include both sexual and social behaviors, all of which are also influenced by social experience. Many juvenile behaviors such as play, mounting, and vocal behaviors are masculinized and/or defeminized, and aspects of adult sexual behavior are both masculinized (e.g. approaches, sex contacts, and mounts) and defeminized (e.g. sexual solicits). Different behavioral endpoints have different periods of maximal susceptibility to the organizing actions of prenatal androgens. Aromatization is not important, as both testosterone and dihydrotestosterone are equally effective in rhesus monkeys. Although the full story of the effects of prenatal androgens on sexual and social behaviors in the rhesus monkey has not yet completely unfolded, much progress has been made. Amazingly, a large number of the inferences drawn from the original 1959 study have proved applicable to this nonhuman primate model.     

The relationship between aggressive behavior and menstrual cycle stage in female rhesus monkeys (Macaca mulatta)

The aggressive behavior of eight adult female rhesus monkeys, living in a captive social group, was studied prior to and during a breeding season extended by vasectomizing all the adult males in the group. Female reproductive status was ascertained by: recording all adult female-adult male copulations, detecting menstruation by vaginal swabbing, and analyzing serum progesterone levels by radioimmunoassay. Females were more aggressive during the follicular stage of their menstrual cycle than the luteal stage or during the period prior to the onset of seasonal ovarian activity. Increases in aggression were limited to increases in the milder forms of agonistic behavior, primarily threatening gestures. Although the females showed their highest rates of noncontact aggressive response categories during the follicular stage, several showed highest rates of contact aggressive response categories in the precycling period.     

Comparison of the Reconciliation Behavior of Stumptail and Rhesus Macaques

Observations were made following spontaneous aggressive incidents in a breeding group of captive stumptail macaques (Macaca arctoides). Participants were observed both during the first 10 min following the aggressive incident, and during matched-control observations. Data on 670 pairs of former opponents were collected, and compared with a sample of 573 such pairs of rhesus macaques (M. mulatta), which had been observed with identical methods in a previous study. Selective attraction between opponents was confirmed for the stumptail monkeys, i.e. both the absolute and the relative rate of nonagonistic body contact between individuals increased after aggression between them. The species was found to be considerably more conciliatory than rhesus monkeys, and to have a remarkably rich repertoire of reassurance gestures. The most characteristic conciliatory behavior is the hold-bottom ritual, in which one individual (usually the subordinate) presents its hindquarters, and the other (usually the dominant) clasps the other's haunches. The high rate of reconciliation among stumptail monkeys extended to all relationship classes, and a correlation with the closeness of social bonds (measured as time spent in association) could not be demonstrated. Because of the generality of the species' high peacemaking tendencies it is assumed that group cohesiveness is of great survival value in the wild.