Social Groups Of Rhesus Monkeys Research Articles

Influences of demographic, seasonal, and social factors on automated touchscreen computer use by rhesus monkeys (Macaca mulatta) in a large naturalistic group.

Animals housed in naturalistic social groups with access to automated cognitive testing vary in whether and how much they participate in cognitive testing. Understanding how demographic, seasonal, and social factors relate to participation is essential to evaluating the usefulness of these systems for studying cognition and in assessing the data produced. We evaluated how sex, age, reproductive experience, seasonality, and rank related to patterns of participation in a naturalistic group of rhesus monkeys over a 4-year period. Females interacted with the touchscreen systems more than males and were more likely to complete initial training. Age was positively correlated with touchscreen activity through adolescence in females, at which point seasonality and reproductive experience were stronger associates of participation. While monkeys in different rank categories did not differ in how much they interacted with the touchscreen systems, monkeys of different ranks tended not to work at the same times, perhaps reflecting avoidance of high ranking animals by those of lower rank. Automated cognitive testing systems for naturalistic social groups of rhesus monkeys can yield quality cognitive data from individuals of all ages and ranks, but participation biases may make it difficult to study sex differences or seasonal variation in cognition.

Gradual acquisition of visual discrimination tasks in a social group of rhesus monkeys (Macaca mulatta)

An established, captive colony of 74 rhesus monkeys (Macaca mulatta) was group-tested on a simultaneous visual discrimination problem and three reversals of the initial discrimination. The task incorporated important aspects of rhesus foraging behavior. Although other studies of communal groups of nonhuman primates have reported rapid learning, subjects in the present study showed no evidence of one-trial acquisition of the initial problem or of rapid learning-set formation across the reversal series. Instead, mean and individual performance, on all variables measured, improved gradually, both within and across series. Subjects appeared to “learn how to learn,” consistent with findings of traditional studies of individual discrimination learning. Our finding of gradual learning in group-living animals argues that the source of rapid learning in previous reports is not attributable to social influence or ecological relevance, but may reflect specific procedural or species differences between studies.

Old, socially housed rhesus monkeys manipulate objects

AbstractRecent research has indicated that old, individually housed monkeys show little interest in novel objects. Yet unanswered is whether this effect is caused primarily by age or housing condition. The purpose of this study was to assess the role of social living in promoting responsiveness to objects. We measured the rates of object manipulation in older animals, assessed responsiveness over time to particular objects as a measure of habituation, and examined social influences on object use. Several social groups of rhesus monkeys that contained older adults were studied. These groups were housed in indoor pens or in an outdoor enclosure, and all monkeys had continuous access to a variety of objects in their home environment. In contrast to previous studies of individually housed monkeys, our group‐housed monkeys showed sustained interest in objects. Old monkeys manipulated objects extensively, and this response was all the more significant, given that the objects were not novel. Monkeys housed in an outdoor enclosure showed object manipulation patterns that were not different from monkeys housed in indoor pens. However, females exhibited much higher object‐related responses than males. Social facilitation played a role in the reactions of some monkeys to objects. Patterns of social facilitation as well as avoidance were present in two of the three indoor groups that were observed. Failure to manipulate objects in rhesus macaques appears to be more a function of individual housing than of old age. Factors such as environmental complexity, social needs, and early experience should be considered in order to understand why individually housed rhesus monkeys are unresponsive to objects. © 1993 Wiley‐Liss, Inc.

Sexual preferences during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta)

Eight groups of rhesus monkeys each consisting of one male and four ovariectomized females were observed while two of the females were treated with hormones to produce artificial menstrual cycles. These were either synchronized or offset by 7-day increments. Sexually preferred females, defined by the numbers of ejaculations per test, received almost twice as many ejaculations as did non-preferred females during all synchronized and offset cycles and during all cycle phases. However, short-term changes in partner preference occurred when the midcycle phase of non-preferred females coincided with the middle or late progesterone phase of preferred females, suggesting a negative effect of progesterone on behavior during the menstrual cycle. There were highly significant differences between preferred and non-preferred partners for almost all of their sexual and social interactions, and preferred partners showed longer proximity and grooming times as well as higher levels of sexual activity. Partner preferences accounted for more of the behavioral variance between pairs than did female dominance, although males sought the proximity of dominant females independently of their partner preferences. Thus, in a setting uncomplicated by male mate competition, sexual preference by male rhesus monkeys is a robust phenomenon depending on complex interactions between dominance, hormonal status, and the individual behavior of female partners.

Female dominance rank and behavior during artificial menstrual cycles in social groups of rhesus monkeys (Macaca mulatta).

We recently reported (Michael & Zumpe: American Journal of Primatology 15:157-170, 1988) evidence for the hypothesis that copulations by pairs of rhesus monkeys are linked more closely to the ovulatory phase of the female's menstrual cycle when a male has access to several females in different cycle phases rather than access to females in the same cycle phase. We have now used data from this earlier study to assess the role of female dominance. Artificial menstrual cycles were induced with hormone injections in two of four ovariectomized females in eight social groups (each consisting of one male and four females). The artificial cycles were either synchronized or offset by 7-day increments. There were differences in the behavioral interactions of the higher-ranking (dominant) and lower-ranking (subordinate) hormone-treated females in each group. The amount of male sexual activity received by dominant and subordinate females differed little, but dominant females initiated significantly more sexual activity (P<.0001) than did subordinate females. Dominant females were significantly more aggressive (P<.0001) toward other females and received more direct and redirected aggression from males. Males generally initiated and maintained more social contacts with dominant than with subordinate females, and dominant females were less active than subordinates in initiating and maintaining social interactions with males. The findings provide new evidence for both female mate competition and mate choice by males for higher-ranking females.

Some issues in the abstraction of genetic structures of monkey societies

Genetic models of subdivided populations usually assume highly simplified fixed population structures. Studies of social groups of rhesus monkeys (Macaca mulatta) and hamadryas baboons (Papio hamadryas) indicate that populations of these monkeys possess complex, distinctive, highly dynamic population structures. The lack of correspondence between assumptions of ordinary genetic models and observations on real monkey populations seems sufficiently great that existing genetic models for subdivided populations cannot serve as theories for monkey populations. It is suggested that more adequate representations of genetic structures of populations of social species will be built with formalisms borrowed from linguistic and computer sciences.

Influence of olfactory signals on the reproductive behaviour of social groups of rhesus monkeys (Macaca mulatta).

Olfactory influences are important in the control of reproductive function in many mammalian species including primates. Previous studies have shown that a mixture of volatile aliphatic acids (copulins), normally present in the vaginal secretions of rhesus monkeys, can exert a stimulatory effect on the sexual behaviour of males when pairs are tested in small cages. The present study deals with the role of these substances when tested in social groups of rhesus monkeys housed in a large testing arena, the purpose being to assess the effectiveness of olfactory signals under more nearly naturalistic conditions. Each group consisted of one male with four long-term ovariectomized females from which the male could choose. A counter-balanced experimental design was used in which each female of a testosterone-treated pair was given applications to the sexual skin of either copulins or control ether immediately before each 1-h behaviour test. After 16 tests, the procedure was repeated with the previously untreated pair in each group, and nine groups were separately studied. Testosterone was used here simply to enhance female proceptivity. The results showed that females received significantly more ejaculations (P less than 0.05), mounting attempts (P less than 0.01) and mounts (P less than 0.05) when bearing copulins than when bearing control ether. There were positive responses to copulins in 12 of the 36 males-females pairs, involving all males, and positive responses to ether in five of 36 pairs, involving four males. Copulins resulted in a change in the choice of sexual partner in five males, but there were no changes in the choice of partner with ether. Social factors, such as dominance, could override the responses to olfactory signals, and there was a significant treatment order effect, but this was eliminated by the counter-balanced design. These findings indicate a significant role for olfactory communication in mate selection in a socially living higher primate.

Influence of estrogen-treated females on sexual behavior and male testosterone levels of a social group of rhesus monkeys during the nonbreeding season.

The effect of the sequential estradiol benzoate treatment of each of 6 ovariectomized (OVX) females on a social group of rhesus monkeys was examined during the period from May to August. The group was housed outdoors and was composed of 7 adult males and 5 intact females, in addition to the 6 OVX animals. Social behavior was observed and male testosterone levels were monitored before, during and after estrogen treatment of the OVX females. Behavior of an unmanipulated group was also examined, and no sexual behavior occurred in this control group from May through August. In contrast, the sexual behavior of both males and gonadally intact females of the experimental group increased when estrogen-treated females were present. Sexual behavior remained elevated after the estrogen-treated females had been removed and continued so into the breeding season. The sexual behavior of the untreated females was displayed in cycles about 26 days in length. Male testosterone levels increased to values typical of the breeding season. Aggressive and submissive behavior also increased during the treatment. These results confirm previous findings about the influence of estrogen-treated females on male sexual behavior, and present the first direct evidence of increased testosterone levels in this situation. In addition, the data suggest that the presence of estrogen-treated females can induce sexual behavior in the other females of the same social group.

Serum 17β-estradiol and progesterone associated with mating behavior during early pregnancy in female rhesus monkeys

The phenomenon of postconception mating behavior was examined in a social group of rhesus monkeys living in an outdoor compound. Periodic blood samples and daily vaginal swabs were obtained from nine females beginning several weeks prior to conception and continuing through 6 weeks of pregnancy to permit an assessment of ovarian hormonal events associated with mating during early pregnancy. Each of the females showed a discrete period of copulatory activity during the periovulatory period which ceased within several days after the 17β-estradiol (E 2) ovulatory peak. In agreement with earlier reports, only a percentage of subjects (44%) exhibited a period of postconception mating, with copulatory activity beginning 19.8 (± 1.9) days following the E 2 peak and continuing for 9.5 (± 1.3 days). Implantation bleeding was detected in all of the subjects with the onset 19.5 (± 0.68) days after the E 2 peak. The interval between the E 2 peak and the onset of implantation bleeding was similar for all females. However, the duration of implantation bleeding was significantly shorter in females who exhibited postconception mating. The females who displayed postconception copulatory activity had significantly lower mean serum progesterone concentrations (2.33 ± 0.24 ng/ml vs. 3.64 ± 0.37 ng/ml) during the period associated with implantation bleeding and copulatory behavior. Although both groups had elevated concentrations of serum E 2 during this period, levels in the females who displayed postconception mating were significantly lower (173.8 ± 19.2 pg/ml vs 223.9 ± 28.8 pg/ml). These data demonstrate that the occurrence of postconception mating behavior in this environment is associated with a distinct pattern of ovarian hormonal events, and analysis suggests that differences in steroid concentrations probably account for the observed differences in implantation bleeding and copulatory behavior during pregnancy.

Genetic differentiation among matrilines in social groups of rhesus monkeys

In rhesus monkey populations, animals related by descent to some female comprise a matriline or genealogy. Data on blood protein polymorphisms in the Cayo Santiago rhesus colony indicate that allele frequency variations among matrilines in social groups are large. These variations occur despite high levels of outbreeding. Computer simulation analyses indicate that pedigree or linear effect account for much of the observed genetic differentiation among genealogies. A sampling with correlation model in which genealogy sizes and average kinship levels are parameters predicts among matriline genetic differentiation. This study indicates that substantial genetic substructure is present within rhesus social groups. Our analyses also predict that large variances in allele frequencies should be common among social or trait groups based on kinship relationships.

Reproductive Behavior in the Rhesus Monkey: Social and Endocrine Variables

SYNOPSIS. Social groups of rhesus monkeys ( Macaca mulatto ) living in outdoor environments exhibit a distinct seasonal mating pattern and female rhesus are observed to be sexually receptive for discrete periods averaging about 9 days duration. In the laboratory environment mating occurs throughout the year and, in the pair test, female rhesus are observedto be sexually receptive through all phases of a menstrual cycle, with a periovulatory peak incopulatory behavior. The apparent conflict between results from field and laboratory studies has been difficult to resolve because of methodological limitations inherent in each study environment. Studies conducted on social groups of rhesus monkeys housed in outdoor compounds, an environment in which the species typical seasonal mating pattern is preserved and which allowsfor concomitant measurement of behavioral and hormonal variables, provided information about the covariance between female sexual behavior and ovarian cycles. Female copulations were observed only in association with ovulatory cycles, and were limited to the follicular and peri-ovulatory phases of such cycles, demonstrating that copulatory behavior in female rhesus monkeys is strongly influenced by cyclic hormonal variables. The studies also revealed that females tend to conceive on the first ovulatory cycle of the season, that there was no synchrony of cycles among the females, and that the best predictor of the timing of ovulation in a particular female is reproductive outcome in the previous year.

Effects of Methaqualone on Social Behavior in Monkeys &lt;i&gt;(Macaca mulatta&lt;/i&gt;&lt;i&gt;)&lt;/i&gt;

In an established social group of rhesus monkeys (macaca mulatta) consisting of 1 adult male, 6 adult females, 1 adolescent male and 2 infants, 3 subjects were selected to study the effects of intramuscular methaqualone (10 mg/kg) on behavioral changes in the treated animals, as well as the rest of the colony. Three drug trials alternating with saline controls given to the dominant male, a mid-ranking female and the adolescent male. 20 h of observations were made prior to treatment to serve as a baseline, using 40 discrete behaviors. For each drug and saline period, 2 h of continuous observation was directed towards each target animal (total 36 h), and 12-min behavioral samplings were carried out on each untreated subject in the colony (36 h). Dependent upon the sex and social rank of the subject, different behavioral changes occurred during drug treatment, which were consistent from trial to trial. New behaviors were observed, such as active grooming, autofellatio and masturbation in both males, while some previous behaviors disappeared or decreased. The mid-ranking female showed an increase in aggressive behavior. A biphasic action of the drug was also observed in all subjects. During the first 80--100 min, the males were mainly passive or engaged in grooming, but after this primary phase, they started either to masturbate or autofellate. After approximately 2 h, the social status and behavior of the animals returned to predrug levels. During the drug treatment, marked changes occurred in the behavior of other colony members, e.g. when the dominant male's vigilance was lowered, the highest ranking female replaced him in rank. In general, affiliative activities were increased under the influence of methaqualone, manifesting themselves mainly in grooming, hudding or sitting together: phenomena somewhat parallel to those described among humans taking the drug in group settings.

Effects of increased testosterone secretion on the behavior of adult male rhesus living in a social group.

Selected members of an all-male social group of rhesus monkeys were treated with twice-weekly injections of human chorionic gonadotropin (HCG) to determine the effects of the consequently increased androgen secretion on social behavior. Radioimmunoassay of blood samples confirmed significant increases in serum testosterone levels in each of 4 subject, but only 3 of these showed significant behavioral changes. The basic social structure of the group, including the dominance hierarchy, was not disrupted by the treatment with HCG. Rather, the behavioral changes which did not occur appeared to be intensifications of previously existing social relationship.

Sex and aggression during rhesus monkey group formation

Observational data from 16 newly formed social groups of rhesus monkeys were analyzed to identify patterns of behavior that correlated with the frequency and intensity of aggression directed toward females. The results revealed significant correlations between heterosexual behavior and female-female noncontact aggression and between female homosexual behavior and female-female contact aggression. The role of female homosexual behavior and its relationship to aggression in the formation of new groups is discussed.

Aggression within social groups of rhesus monkeys ( Macaca mulatta): Effect of contact between groups

Social contact between two groups of rhesus monkeys within tunnel-connected enclosures affected the frequency of aggressive interaction within each group. Contact decreased aggression within the subordinate group but increased it within the dominant group. When the dominance relationship between the two groups was experimentally reversed the effect of contact on intragroup aggression correspondingly reversed.

Parental Care in a Group of Free-Ranging Rhesus Monkeys (Macaca mulatta )Parental Care in a Group of Free-Ranging Rhesus Monkeys (Macaca mulatta )

The purpose of this paper is to describe and explore the significance of parental activities among Macaca mulatta. The phylogeny of care-giving behavior and the terminology that has been used in reference to it are discussed briefly.The focus of the paper is the presentation of original data from a continuous 15-month study of a free-ranging social group of rhesus monkeys in which the birth date and the mother of most individuals were known. Care giving was ubiquitous in the social group. Sex differences were minimal and, for the most part, quantitative rather than qualitative. The purpose of this paper is to describe and explore the significance of parental activities among Macaca mulatta. The phylogeny of care-giving behavior and the terminology that has been used in reference to it are discussed briefly.The focus of the paper is the presentation of original data from a continuous 15-month study of a free-ranging social group of rhesus monkeys in which the birth date and the mother of most individuals were known. Care giving was ubiquitous in the social group. Sex differences were minimal and, for the most part, quantitative rather than qualitative.

Behavior between two social groups of rhesus monkeys within two tunnel-connected enclosures.

Behavior between two social groups of rhesus monkeys within two tunnel-connected enclosures.

Agonistic behaviour of young rhesus monkeys after changes induced in social rank of their mothers

Four changes in the adult female dominance hierarchy were studied in a small, enclosed social group of rhesus monkeys. Rank changes were artificially induced by either the introduction of a ‘strange’ adult male at a time when the second-ranking female was in oestrus or by removal and reintroduction of the currently topranking female. Agonistic interactions were studied following each social manipulation. The mother-offspring dominance relationship was emphasized. Families (mother and offspring) were ranked in a new linear dominance hierarchy following each rank change. With one exception offspring directly reflected the rise or fall of the rank of the mother. Offspring both influenced and were influenced by the rank changes by either contributing to aggression towards other animals when the mother's rank rose or by suffering aggression simultaneously with the mother, including wounding, when the mother's rank fell. One 2 1 2 -year-old female acted independently of the mother and consistently achieved a social rank higher than that of the mother when the mothers rank fell.