Relationships in six groups of rhesus monkeys I. Networks

Monkey groups are characterized in terms of their networks of relationships. Six groups, each consisting of one adult male, several adult females and immatures, were studied over the same time period. This provided data on interaction patterns within groups and the ways in which individuals' kinship, backgrounds, idiosyncrasies, age and sex affected their interactions. Consistencies and changes in group networks in the course of time and in the face of events such as births, deaths, separations, and introductions are given special attention. Principles of networks are discussed with reference to problems of social structure such as cohesion, permeability, communication, stability and competition.     

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.     

Quantitative analysis of small group interaction in rhesus monkeys

The effect of role relations on social interaction in small groups of rhesus monkeys was examined quantitatively, through use of an interval scale of social behavior. Concurrent pair interactions were tabulated for all possible combinations in 24 triad groups: Six groups containing three males; six groups containing three females; six groups of one male, two females; and six groups of two males and one female. A specific behavior which involves participation of all three animals at once, the incitement interaction, was found to quantitatively alter each monkey's reaction to other social behaviors displayed at the same time. The interaction demonstrates the monkeys' attention to and manipulation of role relations. In all triad types one could quantitatively document the fact that the most subordinate monkey established a role with the most dominant monkey which allowed it some freedom to behave less submissively when interacting with the middle ranking monkey. This general phenomenon in role relations may contribute to group cohesiveness.     

Paternity exclusion in six captive groups of rhesus monkeys (Macaca mulatta)

Five genetic markers were employed to attempt to identify the fathers of 135 Macaca mulatta offspring living in large outdoor field cages. Family studies of two of these markers to confirm mode of inheritance of phenotypes had not heretofore been reported. Of the 284 exclusions required to identify the fathers of all 135 monkeys, 198 (or 70 percent) were possible using only these five genetic polymorphisms. For 58 (or 43 percent) of these 135 offspring the father was identified. These data were applied to estimate the association between dominance rank of fathers and reproductive success. Fertility of first- and second-ranking fathers was judged to be about twice as high as that of third- and fourth-ranking fathers.     

Social status modifies estradiol activation of sociosexual behavior in female rhesus monkeys

Estrogen (E2) has activational effects on sexual motivation and mitigating effects on anxiety-like behaviors that can be attenuated with chronic exposure to psychosocial stress. Some studies suggest that this attenuation can be overcome by higher doses of E2, while others show that chronic psychosocial stress may alter the mechanisms of E2 function, thus reducing any positive benefit from higher doses of E2. To determine the interaction between psychosocial stress and E2 dose on behavior, we examined the scope of attenuation across a suite of socioemotional behaviors, including reproduction, affiliation, aggression, submission, and anxiety-like behaviors on 36 ovariectomized female rhesus monkeys. Females were exposed to graded psychosocial stress, established by an intrinsic female dominance hierarchy, where subordinate animals receive high amounts of harassment. Our data show that E2 dose-dependently increased sexual motivation and male-affiliation in dominant (e.g. low-stress) females, while subordinate females showed no positive effects of E2, even at higher doses. In addition, contact aggression was attenuated in dominant females, while non-contact aggression was attenuated in both dominant and middle-ranking females. These results suggest that the stress-induced attenuation of E2's activational effects on sexual behavior and affiliation with males may not be overcome with higher doses of E2. Furthermore, the observed behavioral consequences of psychosocial stress and E2 dose may be dependent on the behaviors of all the females in the social-group, and better resolution on these effects depends on isolating treatment to individuals within the group to minimize alterations in social-group interactions.     

Inbreeding in three captive groups of rhesus monkeys

Using electrophoretic and serological genetic markers each of 17 potentially inbred matings in three groups of rhesus monkeys could be classified as either inbred or noninbred matings. Although nine of these 17 matings involved either father-daughter or paternal half-sib matings, only 7.4 were expected by chance alone. At least two, and possibly as many as three, of the nine cases of inbreeding involved father-daughter matings. Thus, no evidence of avoidance of inbreeding was observed in the closed captive groups of rhesus monkeys studied. Colony management policies must be developed to minimize the opportunity for or the deleterious effects of both father-daughter and half-sib matings. Furthermore, kin selection theory should consider why kin recognition, if it occurs, does not lead to avoidance of inbreeding.     

Proteomic analysis of the nucleus accumbens in rhesus monkeys of morphine dependence and withdrawal intervention

It has been known that the reinforcing effects and long-term consequences of morphine are closely associated with nucleus accumbens (NAc) in the brain, a key region of the mesolimbic dopamine pathway. However, the proteins involved in neuroadaptive processes and withdrawal symptom in primates of morphine dependence have not been well explored. In the present study, we performed proteomes in the NAc of rhesus monkeys of morphine dependence and withdrawal intervention with clonidine or methadone. Two-dimensional electrophoresis was used to compare changes in cytosolic protein abundance in the NAc. We found a total of 46 proteins differentially expressed, which were further identified by mass spectrometry analysis. The identified proteins can be classified into 6 classes: metabolism and mitochondrial function, synaptic transmission, cytoskeletal proteins, oxidative stress, signal transduction and protein synthesis and degradation. Importantly, we discovered 14 proteins were significantly but similarly altered after withdrawal therapy with clonidine or methadone, revealing potential pharmacological strategies or targets for the treatment of morphine addiction. Our study provides a comprehensive understanding of the neuropathophysiology associated with morphine addiction and withdrawal therapy in primate, which is helpful for the development of opiate withdrawal pharmacotherapies.     

Observations on the activity patterns and social interactions of a captive group of blackcapped or brown capuchin monkeys (Cebus apella)

Studies were conducted on a captive group of 16 blackcapped capuchin monkeys (Cebus apella), with observations being carried out for a total of 75 hr over a 6 month period. Records were kept of their activities and spatial distribution according to weather type and time of day. Evidence of a social hierarchy was sought and was characterized primarily by the stability of the environment in which the animals live, dominance playing little part. The behaviour of the blackcapped capuchin has been studied previously in captivity (Dobruruka, 1972;Weigel, 1979); this study is, however, unique in that the troop under observation enjoys more freedom. Weather had no effect on the rank order of behavioural activities but did affect both activity levels and distribution of individuals. TheCebus apella troop spent around 50% of its active time foraging and eating, 7–10% of this time walking and around 30% of the time inactive. These values lie between those reported for caged and wild animals. Social interactions contributed more than 10% of the time budget, which is greater than wild populations. The study here thus provides an interesting link between information collected from wildCebus apella populations and that from rather more restricted troops.     

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.     

Control of postpartum mating behavior in free-ranging rhesus monkeys

This paper explores the effect that a dependent rhesus macaque infant (Macaca mulatta) has on the timing of its mother's resumption of mating. Toward this end, behavioral data from the rhesus populations at Tughlaqabad, India, and Cayo Santiago, Puerto Rico, are compared. Specifically, the intervals between parturition and subsequent resumption of mating for individual parous females are examined in order to shed light on the relative importance of environmental and internal factors (such as lactational infertility) in the control of rhesus mating behvior. At both study sites it was found that the later a given female gave birth during a birth season the shorter was her parturition-mating interval and the younger was her infant when she resumed mating activity. It is suggested that this finding is the result of an interaction of environmental and internal factors; both act in concert to determine how soon after parturition a particular rhesus female will resume mating activity.     

Seasonal breeding in rhesus monkeys: Influence of the behavioral environment

The accepted model of breeding seasonality in rhesus monkeys states that females become reproductively active in response to an environmental cue and that males become sexually active in response to ovulating females. This model must be modified to include direct responses of the male to the physical environment, endocrine responses of males to sexual activity, and responses of the female to the sexual activation of fellow group members. The complex set of social stimuli that influences the breeding readiness of both sexes may serve to delimit more precisely the annual periods of conception and birth than would be the case if each individual responded only to the changing physical environment.     

Chronic Pseudomonas aeruginosa endobronchitis in rhesus monkeys: II. A histopathologic analysis

We have recently established a rhesus monkey model of chronic Pseudomonas aeruginosa (PA) endobronchitis by bronchoscopic instillation of PA-embedded agar beads. All experimental animals developed chronic neutrophilic endobronchitis similar to chronic PA endobronchitis in cystic fibrosis (CF). Histopathologic studies further confirmed similarities to chronic PA endobronchitis in CF, including marked peribronchial inflammation, epithelial damage, presence of degraded cilia and ciliary abnormalities, appearance of PA bacterial clusters, mucosal hyperplasia, goblet cell hypertrophy/hypersecretion, airway obstruction, alveolar abnormalities, bronchiectasis, and fibrosis.     

Dihydrotestosterone propionate effects on dominance and sexual behaviors in gonadectomized male and female rhesus monkeys.

One triad of male and two triads of female gonadectomized rhesus monkeys were observed as social groups assembled for repeated hour-long sessions. Social relationships were measured in terms of aggressive behavior between the members of each group in order to determine the dominance hierarchical order. Sexual performance was assessed for each male, before and after castration, in tests with an estrogen-stimulated ovariectomized female. Similar measures were made when the same female was periodically introduced to the all-male triad. When dihydrotestosterone propionate (DHTP) was administered for a period of 6 weeks to the middle-ranking member of each group, social status changes occurred in two groups, one male and one female, resulting in the elevation of the treated monkeys to the highest rank in the dominance hierarchy. In the other female group, aggressive behavior was increased with DHTP treatment of the middle-ranking female. Somatic effects, particularly a gain in body weight, occurred in all treated animals. Yawning behavior also increased significantly in those animals receiving DHTP. The latter two effects returned toward pretreatment levels following the cessation of hormone injection; however, changes in dominance hierarchy persisted to the end of the experiment, 6 weeks following the last DHTP treatment.     

Aging in the musculoskeletal system of rhesus monkeys: II. Degenerative joint disease

In order to discuss the rate and onset of adult aging in rhesus monkeys, 55 adult animals from the Wisconsin Regional Primate Research Center and the University of Wisconsin Psychology Primate Laboratory were examined. Degenerative joint disease (DJD) at the hip and spine was scored, and loss of passive joint mobility at the hip was measured. Development of DJD at both the hip and spine was significantly and positively correlated with age. Spinal changes, especially at the thoraco/lumbar intervertebral symphyses, appeared to develop somewhat more rapidly than hip degeneration. In some individuals, DJD was observed soon after the completion of growth, but pronounced changes seldom occurred before the middle of the second decade of life. Similarly, age-dependent losses of passive joint mobility appeared to begin early in ontogeny and to become increasingly pronounced in the aging adult. Although interspecific comparisons are difficult due to intraspecies and intraindividual variation, the timing of musculoskeletal aging in the rhesus spine and hip differs from that observed in humans in a way that parallels previously documented species differences in patterns of musculoskeletal growth. These observations and data on age-related change in other systems, suggest that rates and durations of many ontogenetic processes in rhesus monkeys are approximately three times as fast and one-third as long as those of the corresponding human processes. Importantly, differences in the timing of reproduction do not appear to follow the same scaling factor observed in other systems. Although reproduction may, therefore, be under separate control, the consistent pattern observed in other aspects of somatic growth and aging supports the hypothesis (Cutler, 1976; Sacher, 1978) that evolutionary changes in ontogeny have resulted from selection acting upon a few genes with widespread regulatory effects.     

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

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