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.     

Determinants of behavioral rhythmicity during artificial menstrual cycles in rhesus monkeys (Macaca mulatta)

Reproductive success in many mammals depends on synchrony between copulation and ovulation, which is insured by the phenomenon of heat in the female. Certain anthropoid primates including rhesus monkeys do not show heat but may copulate throughout the menstrual cycle, especially when pairs are isolated from conspecifics. In social groups, however, mating mostly occurs around midcycle. We wished to test the hypothesis that copulations are more closely linked to ovulation when males have simultaneous access to several females in different cycle phases. Artificial menstrual cycles were therefore induced by giving hormones to ovariectomized female rhesus monkeys observed in small social groups that each consisted of four females and one male. The cycles of two hormone-treated femlab in each group were either made to synchronize or be offset by 7-day increments so that the estradiol peak of one female occurred 7 days before, and 7 and 14 days after, the estradiol peak of the other. Radioimmunoassay of plasma samples (N = 224) confirmed the timing of the estradiol peaks. Results from eight unique male-female groups (4 males, 8 females, 16 male-female pairs, 718 tests) fully supported the hypothesis. Compared with synchronized cycles, the amplitudes of rhythmic changes in offset cycles were reduced for ejaculations made by males but greatly enhanced for ejaculations received by females. We propose that this socio-hormonal integration of behavior in the group is highly adaptive and enhances the reproductive success of both males and females.     

Sexual behavior and urinary ovarian hormone concentrations during the lowland Gorilla menstrual cycle

Sexual behaviors were recorded and urinary concentrations of total estrogens and pregnanediol-3-glucuronide (Pdg) measured during six normal menstrual cycles from two female lowland gorillas in a stable, captive group. Frequencies of female presentations, mounts, and copulations were positively associated with peak estrogen values but not with elevations of Pdg. These results support the observation that sexual behaviors in the gorilla occur most frequently in the periovulatory period and that copulations serve primarily a sexual function.     

Sexual behavior and serum hormone levels in aging rhesus males: effects of environmental change

Old (N = 9) and middle-aged (N = 9) rhesus males (Macaca mulatta) that were housed in the same type of home cage and the same room for several years were moved to a new location in an adjacent building. Their sexual behavior and hormone levels in the weeks preceding the move were compared to those after the move. The hypothesis that the nonspecific sensory stimulation provided by the move would increase levels of sexual behavior was not supported by the data. To the contrary, the percentages of tests with contacts, mounts, and penile erections, and the rate of contacting the female, decreased significantly for both old and middle-aged males. The intromission rate of middle-aged, but not of old, males also decreased. In consonance with previous findings, middle-aged males displayed significantly higher levels of sexual activity than did old males. The differences were observed both before and after the move. Serum testosterone levels did not differ between middle-aged and old males, and the move did not produce significant changes in testosterone levels. Serum cortisol levels were significantly higher immediately after the move (1 hr) but returned to premove levels the following day.     

Sleep-wake cycles in rhesus monkeys during Spacelab flight simulations

Neurophysiological data has been obtained in orbital flight from various non-human Primates. Aboard Russian satellites during both Bion and Biocosmos missions, impairments in duration and organization of the states of vigilance were observed in rhesus monkeys during flight: increase in nocturnal awakening, decrease of Rapid Eye Movements-sleep (REM-sleep). It was assumed that weightlessness played a role in these changes. The former "Rhesus Project", a joint program between CNES and NASA, was devoted to physiological studies using the rhesus monkey as a human model aboard Spacelab, during 14 to 16 day orbital flights. In the first stage of this project, we investigated the effect of experimental conditions as well as specific restraint and confinement on the circadian sleep-wake rhythm in a group of rhesus monkeys. Prior to flight, our aim was to determine quantitatively and qualitatively sleep-wake cycles. These control data would thus be compared with inflight data in order to assess the influence of weightlessness.     

Changing frequency of pulsatile luteinizing hormone and progesterone secretion during the luteal phase of the menstrual cycle of rhesus monkeys

Experiments were conducted to examine the pulsatile nature of biologically active luteinizing hormone (LH) and progesterone secretion during the luteal phase of the menstrual cycle in rhesus monkeys. As the luteal phase progressed, the pulse frequency of LH release decreased dramatically from a high of one pulse every 90 min during the early luteal phase to a low of one pulse every 7-8 h during the late luteal phase. As the pulse frequency decreased, there was a corresponding increase in pulse amplitude. During the early luteal phase, progesterone secretion was not episodic and there were increments in LH that were not associated with elevations in progesterone. However, during the mid-late luteal phase, progesterone was secreted in a pulsatile fashion. During the midluteal phase (Days 6-7 post-LH surge), 67% of the LH pulses were associated with progesterone pulses, and by the late luteal phase (Days 10-11 post-LH surge), every LH pulse was accompanied by a dramatic and sustained release of progesterone. During the late luteal phase, when the LH profile was characterized by low-frequency, high-amplitude pulses, progesterone levels often rose from less than 1 ng/ml to greater than 9 ng/ml and returned to baseline within a 3-h period. Thus, a single daily progesterone determination is unlikely to be an accurate indicator of luteal function. These results suggest that the changing pattern of mean LH concentrations during the luteal phase occurs as a result of changes in frequency and amplitude of LH release. These changes in the pulsatile pattern of LH secretion appear to have profound effects on secretion of progesterone by the corpus luteum, especially during the mid-late luteal phase when the patterns of LH concentrations are correlated with those of progesterone.     

Ultrasonographic assessment of the endometrium in rhesus monkeys during the normal menstrual cycle

This study was undertaken to determine whether cyclical changes in the endometrium of the rhesus monkey could be observed by using ultrasound. Three indices of endometrial size were examined: the antero-posterior (or ventro-dorsal), longitudinal, and transverse diameters. Changes in the ultrasonic reflectivity of the endometrium were also assessed. We have attempted to correlate these endometrial parameters with the hormonal status of the animal. Ultrasonography was performed for an average of 12 consecutive days during 19 menstrual cycles. All ultrasonic recordings were normalized to the day of the estradiol (E2) peak (Day 0). We found that the reflectivity of the endometrium was dependent on the stage of the cycle: during the follicular phase, the endometrium appeared less echogenic (darker) compared to the myometrium; in the luteal phase, the endometrium was more echogenic (lighter). During the follicular phase (Days -9 to 0), there was a linear increase in the antero-posterior (p less than 0.001), longitudinal (p less than 0.05), and transverse (p less than 0.001) diameters. In the luteal phase (Days 1-15), no significant changes were observed in these diameters. An estimated endometrial volume (EEV) was obtained by the product of the antero-posterior, longitudinal, and transverse diameters. Each animal observed during the follicular phase (n = 14) exhibited a peak in the EEV, which correlated with the day of the E2 peak (p less than 0.01). From this study, we conclude that the sonographic appearance of the endometrium of the rhesus monkey reflects the cyclical changes that occur during the menstrual cycle.(ABSTRACT TRUNCATED AT 250 WORDS)     

Copper levels in cervical mucus during normal menstrual cycles

To establish the pattern of copper levels in cervical mucous, individual samples were taken from 10 normal women (aged 23-46), 2-3 times per week during the cycle. Analysis using a modification of the Stoner and Dasler wet ash microtechnique showed the lowest amounts of copper per 100 mg of dried ash (mean-3.2 mcg) in the ovulatory phase. The highest amount of copper was found in the secretory phase (mean 19.4 mcg). The copper level seemed to vary directly with the level of endogenous progesterone and inversely with the level of endogenous estrogen. No significant correlation between age and amount of copper secreted could be established because of the small size of the study.     

On the correlation between sexual behavior and ovarian hormone level during the menstrual cycle in captive Japanese monkeys

The amount of estradiol and progesterone in the systemic blood plasma of six adult female Japanese monkeys was measured by radioimmunoassay. Data on heterosexual pairing tests was also collected and examined for correlation with these hormones. The relationship between ovarian hormones and frequency of ejaculation varied with each female. In nine normal menstrual cycles, the frequencies of invitation and approach by the female reached peaks on the day of the estradiol surge, after which they rapidly decreased. Frequencies of male behaviors including approach, leaving, invitation, and yawning significantly decreased during the luteal phase, as compared with those at the midcycle. Grooming by both sexes of the partner reached low points during the late follicular phase. The number of ejaculations per test increased significantly at the midcycle and reached a maximum a few days after the estradiol surge. The present results suggest that female proceptivity is highly correlated with the amount of estradiol, but her attractiveness is little correlated with estradiol and is lowered by progesterone.     

Photoperiod and ovulatory menstrual cycles in female macaque monkeys

Macaques (Macaca mulatta and M. assamensis) which had been maintained on a 12L :12D light cycle for the previous 4 years and had 25-35-day menstrual cycles were randomly assigned to two groups. Those in Group 1 were kept in 12L :12D for 13 months. Those in Group 2 were subjected to three successive 5-month periods of 20L :4D, 4L :20D and 20L :4D. There were no significant differences between the two groups in the frequency, duration and percentage of ovulatory menstrual cycles, suggesting that photoperiod is not the sole regulator of seasonal breeding in these animals.     

Infant-directed behavior of rhesus monkeys during their first pregnancy and parturition

To determine whether pregnancy influences the response of rhesus monkeys towards infants, 11 females were observed during 15-min exposures to a 1- to 15-day-old infant at 1- to 2-week intervals throughout pregnancy. No evidence was found for increasing willingness to contact infants as pregnancy progressed. The parturition of 5 of these females was observed, which included 1 live breech birth. These primiparae all established ventral contact with their infants at birth, though most of them appeared to passively allow the infant to initiate contact while their own attention was directed at licking the birth fluids.     

The effect of dietary crude fiber levels on rhesus monkeys during quarantine.

A study was conducted to determine the effect of dietary crude fiber level on intestinal disorders in the feral rheusus monkey (Macaca mulatta) during the first 60 days of the quarantine period. Three experimental baked diets containing 2.4%, 7.0%, and 9.8% crude fiber and a commercially extruded diet containing 2.2% crude fiber were fed during the study. The morbidity rate of intestinal disorders at the 7% crude fiber level was 1.4%, which was significantly less (p less than 0.05) than the 11.1%, 12.5%, and 20.8% morbidity for the monkeys fed the diets containing 2.4%, 9.8%, and 2.2% crude fiber, respectively. Monkeys fed the 7% crude fiber diet had a mean number of treatment days for intestinal disorders per monkey of 0.014, which was significantly lower (p less than 0.05) than the 0.9, 0.5, and 1.4 days for those fed the 2.4%, 9.8%, and 2.2% fiber diets, respectively.     

Opiatergic inhibition of pulsatile luteinizing hormone release during the menstrual cycle of rhesus macaques

The endogenous opioid peptides (EOPs) may inhibit the rate of hypothalamic gonadotropin-releasing hormone (GnRH) release and hence the frequency of pulsatile luteinizing hormone (LH) release, particularly in the luteal phase of the menstrual cycle. Our objectives were to compare the effects of an opiate antagonist, naloxone (NAL), on the patterns of LH, estradiol-17 beta (E2), and progesterone (P4) secretion during the follicular and luteal phases of the macaque menstrual cycle. Plasma levels of E2, P4, and bioactive LH were measured in serial, 15-min blood samples during 8-hr infusions of NAL (2 mg/hr) or saline, either on Days 5 or 6 of the follicular phase (FN and FS, n = 5 and 4, respectively) or on Days 8, 9, or 10 of the luteal phase (LN and LS, n = 5 each) of a menstrual cycle. The pulsatile parameters of each hormone were determined by PULSAR analysis and the correspondence of steroid pulses with those of LH were analyzed for each cycle stage in each animal. As expected, LH mean levels and pulse frequencies in LS monkeys were only about one-third of those values in FS animals. NAL had no effects on pulsatile LH, E2, or P4 release during the follicular phase. In contrast, luteal phase NAL infusions increased both LH mean levels and pulse frequencies to values which were indistinguishable from those in FS animals. LH pulse amplitudes did not differ among the four groups. Mean levels and pulse frequencies of P4 secretion in LS monkeys were about 4- and 14-fold greater than those values in FS animals. Mean levels and pulse amplitudes of P4 release in LN animals were greater than those values in all other groups. LH and E2 pulses were not closely correlated in follicular phase animals, and this pulse association was not altered by NAL. In FS monkeys, LH and P4 pulses were not correlated; however, NAL increased this LH-p4 pulse correspondence. LH and P4 pulses were closely correlated in luteal phase animals and this association was not affected by NAL. Our data suggest that the EOPs inhibit the frequency of pulsatile LH secretion in the presence of luteal phase levels of P4. During the midfollicular phase when LH pulses occur every 60 to 90 min, the opioid antagonist NAL alters neither the pulsatile pattern of LH release nor E2 secretion, but NAL may directly affect P4-secreting cells.     

Assessing menstrual cycles with urinary hormone assays

The Study of Women's Health Across the Nation (SWAN) is a multiethnic cohort study of middle-aged women enrolled at seven US sites. A subset of 848 women completed a substudy in which their urinary gonadotropins and sex steroid metabolites were assessed during one complete menstrual cycle or up to 50 consecutive days. Urine was analyzed for LH, FSH, estrone conjugates (E1c), and pregnanediol glucuronide (Pdg). To prepare for serial analysis of this large, longitudinal database in a population of reproductively aging women, we examined the performance of algorithms designed to identify features of the normal menstrual cycle in midreproductive life. Algorithms were based on existing methods and were compared with a "gold standard" of ratings of trained observers on a subset of 396 cycles from the first collection of Daily Hormone Substudy samples. In evaluating luteal status, overall agreement between and within raters was high. Only 17 of the 396 cycles evaluated were considered indeterminate. Of the 328 cycles rated as containing evidence of luteal activity (ELA), 320 were considered ELA by use of a Pdg threshold detection algorithm. Of 51 cycles that were rated as no evidence of luteal activity, only 2 were identified by this algorithm as ELA. Evaluation of the day of the luteal transition with methods that detected a change in the ratio of E1c to Pdg provided 85-92% agreement for day of the luteal transition within 3 days of the raters. Adding further conditions to the algorithm increased agreement only slightly, by 1-8%. We conclude that reliable, robust, and relatively simple objective methods of evaluation of the probability and timing of ovulation can be used with urinary hormonal assays in early perimenopausal women.