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.     

Resumption of seasonal breeding patterns in male and female rhesus monkeys transferred from an indoor to an outdoor environment

Seasonal aspects of social behavior and sex steroid levels were observed in two groups of rhesus monkeys from March through December. One group (3 males, 7 females) had lived outdoors for several years. The other group (6 males, 5 females), transferred outdoors in late February, had lived indoors for several years. In March-April, the long-term outdoor residents displayed the expected seasonal pattern of sexual behavior, characterized by absence of complete sequences of copulatory behavior. At this time the indoor-adapted group displayed high levels of copulatory behavior. Thereafter, frequencies of sexual behavior of the two groups were similar. Testosterone in the males was positively correlated with frequency of sexual behavior in each group. Females in the indoor-adapted group displaced menstrual cycles in March and April and 3 of 5 became pregnant at this time. The two remaining indoor-adapted females continued to display ovulatory cycles, but little sexual behavior, throughout the summer. Interestingly, two females in the outdoor-adapted group also displayed summer ovulatory cycles; without concomitant sexual activity. These data show that the disruption of seasonal breeding patterns produced by lengthy indoor housing remains briefly apparent following transfer outdoors, but is substantially overcome within a few months.     

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.     

The behavioral thresholds of testosterone in castrated male rhesus monkeys (Macaca mulatta)

To determine the lowest doses of testosterone propionate (TP) that cause clearcut behavioral changes in castrated male rhesus monkeys (behavioral thresholds), observations were made on eight males during successive 4-week treatment periods while they received daily doses of TP ranging from 25 μg to 12.8 mg subcutaneously. Males were tested with each of the same four ovariectomized females (32 pairs, 1408 one-hour behavior tests). Two females were untreated and the other two received either 5 or 15 μg estradiol benzoate sc per day. TP injections were given at 1600 hr, and plasma samples were obtained at 0800 hr (352 samples). Individual males had widely different behavioral thresholds from 50 μg up to 3.2 mg TP per day. Males showed two types of response: A, a graded increase in ejaculatory activity as plasma testosterone values increased, and B, an all-or-none type of response in which there were ho further increases in ejaculation with increasing plasma levels once the behavioral threshold had been reached. At levels below the physiological range, small changes in plasma testosterone were associated with marked changes in behavior. The female partner exerted a pronounced effect upon the responses of males to TP treatment.     

Timing of prenatal androgen exposure: anatomical and endocrine effects on juvenile male and female rhesus monkeys

Prenatal androgen shapes genital differentiation. In humans, genital anatomy determines sex of rearing and subsequent behavioral development. Rhesus monkey genital anatomy and neuroendocrine function are sexually differentiated, and behavioral development occurs in a complex social environment. We investigated prenatal hormonal influences on sexual differentiation by suppressing or increasing androgens in male and female rhesus monkeys. Pregnant multiparous female rhesus monkeys received 35-40 days of testosterone enanthate (TE) treatment, androgen antagonist (flutamide, FL) treatment, or vehicle starting on gestation day (GD) 35 or 40 (early) or GD 110 or 115 (late). Exogenous androgen increased neonatal LH secretion in females when given early and altered female genital differentiation when administered either early or late. TE treatment, early or late in gestation, had no measurable effects on male genital differentiation or neuroendocrine function. Early FL treatment, however, radically altered male genital differentiation, producing in two cases males with a urethral opening separate from the glans. In females, early FL treatment produced detectable alterations in genitalia consistent with a reduced exposure to prenatal androgen, suggesting that female rhesus monkeys are naturally exposed prenatally to meaningful levels of T. Late FL treatment reduced male penis size and increased neonatal T secretion, but had no effect in females. This is the first study to block endogenous prenatal testosterone in rhesus monkeys, thereby altering sexual differentiation. These findings illustrate the complexity of prenatal influences on anatomical and neuroendocrine development. The relationship between the anatomical changes reported here and sex differences in behavior is currently under investigation.     

Social dominance and reproductive behavior in male rhesus monkeys

Altmann's model describing the relationship of social dominance to breeding behavior in some non-human primate species has been tested using data from the Cayo Santiago rhesus colony. Although some of the model's assumptions are clearly not met by field observations, a good fit is often found for groups containing relatively few sexually mature, non-pregnant females. It is suggested that genetic change could be rapid under conditions described by this model. It is estimated that a “beneficial mutation” could spread through all the breeding males in as little as six generations regardless of group size. The speed at which an allele can spread through the group is discussed in terms of the mean length of female receptivity.     

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.     

Food preference of young rhesus monkeys fed marginally zinc deficient diets

Zinc deprivation has been shown to produce hypogeusia in rhesus monkeys but the possible consequences of altered taste sensitivity for food preference and selection is not known. We studied 13 rhesus monkeys (2.5 to 3 years of age) for food preference in a structured choice situation. These animals were fed two levels of dietary zinc: marginally zinc deprived (fed 4 μg zinc/g diet from conception and throughout development;N=6), or control (fed a 100 μg zinc/g diet throughout the study;N=7). Preference for familiar vs unfamiliar food items, order of food preferences, persistence in retrieval of preferred and nonpreferred foods, and preference under four deprivation periods were examined. Animals were offered a choice of two food items, both containing minimal zinc levels, and food choice and latency of choice were measured. Results indicate that animals fed the marginal zinc diets had reduced preference for unfamiliar foods relative to controls and different patterns of food preference. These results may be relevant to maintenance of appropriate food selection in marginally zinc deprived populations.     

Behavioral characteristics of rhesus monkeys in a multiple-choice environment

The present work deals with dynamics of formation of complex alimentary behaviour of rhesus monkeys in multialternative environment. A detailed informational analysis of the obtained results allowed to reveal the properties of processing of proprioceptive information in the course of learning and to understand the characteristics of behaviour of the examined monkeys.     

Behavioral effects of enrichment on pair-housed juvenile rhesus monkeys

Among captive primates, inanimate environmental enrichment can lead to measurable changes in behavior indicative of an improvement in psychological well-being. Although this has been demonstrated repeatedly for singly caged primates, the relationship is not as well studied for pairhoused animals. Study of the pair-housed setting has become increasingly relevant because of the social housing mandate of the Animal Welfare Act regulations. We therefore observed 68 juvenile rhesus monkeys born in 1988 and 1989 and living in mixed-sex pairs from the ages of 2 to 3 years. All pairs were compatible. Half of the pairs received two types of enrichment, while the remaining pairs served as controls. Enriched and control juvenile subjects differed in the amount of time that they spent being inactive, playing, and drinking, but did not differ in the amount of time they spent interacting with their partner. Grooming and play were the two most common socially directed activities in both groups, a species-appropriate pattern. Males played more and vocalized less than did females. Overall, enriched and control subjects spent equivalent amounts of time located within a social distance of one another, but there was some difference between groups in allocation of behaviors while near the pairmate. Environmental enhancers were frequently utilized, and led to relatively small changes in behavior between control and enriched subjects, suggesting that the presence of a partner for juvenile rhesus monkeys acts as a form of enrichment that may dilute the effects of inanimate environmental enhancements. © 1994 Wiley-Liss, Inc.     

Effects of alprazolam on fear-related behavioral, hormonal, and catecholamine responses in infant rhesus monkeys.

We tested the effects of various doses of the triazolobenzodiazepine alprazolam on behavioral, hormonal, and neurochemical responses of infant rhesus monkeys under three conditions of separation from their mothers: alone, in the presence of a human who stared at them, and in the presence of a human who avoided eye contact. Alprazolam affected stress-induced responses in all three of these classes. Unrelated to its effects on the stress response, alprazolam appears to reduce the function of brain dopamine systems.     

Spatial cognition in rhesus monkeys: male superiority declines with age.

Twelve young (4-7 years of age) and 14 old (20-27 years of age) male and female rhesus monkeys were tested on seven cognitive tasks. Males and females performed similarly on tasks of object memory and executive function, but young males outperformed young females on a spatial memory task (Delayed Recognition Span Test) that requires the identification of a new stimulus among an increasing array of serially presented stimuli. This superior level of spatial ability in young males declined sharply with age, so that old males did not perform significantly better than old females. These findings in the nonhuman primate suggest that biological rather than sociocultural factors underlie the sex differences in cognition and their diminution with age.     

The association between rank and reproductive success of male rhesus monkeys

The paternity of 202 of 220 offspring of rhesus monkeys housed in six separate half-acre field cages at the California Primate Research Center was determined by genetic marker techniques. Reproductive success of the adult males was statistically significantly correlated (r = 0.76, P <0.0005) with rank. Marked systematic changes in reproductive success were, however, observed for two adult males during the three years covered by this study. Based upon these results and those of another study, it is argued that changes in rank position typically follow, rather than precede, changes in reproductive success.     

Factors affecting social behavior and reproductive success of male rhesus monkeys

This paper reviews aspects of life history that influence the reproductive success of male rhesus monkeys. Recent theories propose that there is some optimum level of inbreeding for each population and that behaviors related to group transfer by males are the result of selection pressure toward such an optimum. Group changing by males is clearly linked to the effects of testosterone at sexual maturation. A male’s maternal genealogical rank is not consistently related to the age at which it leaves the natal group, but social interactions within the natal group may influence the age of departure. Choice of the new group is influenced by the operational sex ratio and the presence of maternal relatives. Rank in the new group is positively correlated with seniority. Seniority, in turn, is influenced by the rank of the male’s natal group, his mother’s genealogical rank, and the presence of male siblings in the new group. Much of this effect is due to the high mortality of males born to females and/or groups of low rank. Most studies show a positive association between male reproductive success and rank. Males from high-ranking groups and/or maternal genealogies that join groups containing brothers tend to remain in those groups longer, attain a higher rank, and probably achieve higher levels of reproduction than other males.     

Threshold for behavioral response to testosterone in old castrated male rhesus macaques

The sexual behaviors of old, intact (N = 5) and old, castrated (N = 6) rhesus macaque males were compared in six series of pair tests with receptive females. The castrated monkeys were tested when untreated and when given five doses of testosterone propionate (TP; 0.004, 0.016, 0.064, 0.256, and 1.024 mg/kg of body weight) in consecutive months. The serum testosterone (T) level was determined for each male before and after each series of tests. When untreated, none of the castrated males ejaculated, and yawning was significantly less in these monkeys than in intact males-no other behavioral measures differed significantly. Within 2 weeks of daily injections of 0.004 mg of TP/kg, two males ejaculated, and all differences in measures of ejaculation were eliminated. A third male ejaculated after 1 week of treatment with 0.016 mg of TP/kg. Yawning values did not differ during and after treatment with 0.064 mg of TP/kg. Although final mean serum T levels were six times higher in castrated (24.3 ng/ml) than in intact males (4.2 ng/ml), sexual performance levels did not exceed those of intact males.