Sexual behavior in aging male rhesus macaques: Effects of test duration on sexual performance

The sexual behavior displayed by nine old (20-year and older) rhesus (Macaca mulatta) males in 10-min tests was compared to that displayed in 1-hr tests. The tests were part of a long-term study on the decline in male sexual activity that accompanies old age. The males were paired with 10 ovariectomized, estrogentreated females in two blocks of 10 tests; each male was tested once with each female in each test block. The percentages of males that achieved intromissions and ejaculated in the two test blocks were the same (P < 0.05). Although the percentage of tests in which males displayed these behaviors was higher in the longer-test block (P > 0.05), there was a significant positive correlation of performance in 10-min tests with performance in 1-hr tests. Assuming a random distribution of contacting, mounting, intromission, and ejaculation throughout the hour, we would have predicted a significantly lower number of these behaviors in the first 10 min of the 1-hr tests than we actually observed. The mean percentages of 1-hr tests with contacting, mounting, intromission, and ejaculation was significantly lower than that of 10-min tests conducted with the same males 11 years earlier. Thus, the decline in sexual performance was not an artifact of the limited (10-min) test duration.     

Ejaculation by male rhesus in the absence of female partners

The number of ejaculatory plugs found beneath the cages of male rhesus over a 14-month period indicated a high incidence of ejaculation in the home cage in the absence of a female partner. Frequency of ejaculation in the home cage was not related to concurrent tests of sexual behavior with receptive females. Moreover, ejaculation in the home cage within 22 hr or less of sex tests did not affect the frequency of ejaculation in tests with stimulus females. Long- and short-term vasectomized males ejaculated as frequently in their home cages as nonvasectomized males. No ejaculatory plugs, of course, were found beneath the cages of males castrated 2 years earlier.     

Sexual deprivation and its influence on testosterone levels and sexual behavior of old and middle-aged rhesus males

After approximately 6 mo without access to a receptive female, eight old (19 to 25 yr) and eight middle-aged (9 to 15 yr) males were given nine daily 10-min tests of sexual behavior with receptive females. Three ovariectomized, estrogen-primed females served as partners. Blood samples were taken from the males at 0900 and 2100 h on 2 consecutive days before and after the series of nine behavioral tests. Serum levels of testosterone (T) were measured by means of radioimmunoassay. There were no significant differences between serum T levels after 6 mo of sexual deprivation and after the nine tests of sexual behavior, nor did serum T levels differ between middle-aged and old males. Serum T levels were significantly higher in the 2100-h samples than in the 0900-h samples for both groups. The nocturnal increases in serum T, both absolute amounts and percentages of increase, did not differ between middle-aged and old males. Repeated daily testing had little effect on the major components of male sexual behavior. Middle-aged males outperformed old males; middle-aged males had higher rates of contracting the female, mounting and intromitting. They ejaculated earlier and had a greater percentage of tests with ejaculations than did old males.     

Aging and primate male sexual behavior

Old male rhesus macaques display less sexual behavior than young and middle-aged males. The decrease in sexual activity occurs without a statistically significant decline in gonadal hormones or change in diurnal patterns of serum T, DHT, or LH. Levels of sexual activity are not increased by administering T to old intact males. However, the hormone is effective in increasing sexual behavior in old long-term-castrated males. Performance can be increased to levels observed in equally old untreated intact males. Readily detectable physical disabilities of old age have been observed to impair sexual performance, but the observed general decline in sexual activity cannot be accounted for by known physical disabilities. Novelty, as represented by a change in female partner or by a change in environment, has not increased sexual performance in old rhesus males. Only when old males were paired with empirically selected preferred females is their sexual behavior increased to levels displayed by young males. Drugs reported to increase levels of sexual behavior in rats have thus far been less effective in old rhesus males than powdered rhinoceros horn has been in man. The probable absence of a placebo effect in rhesus males should increase their usefulness as an animal model for the study of sexual behavior in aging men.     

Hormonal and social factors affecting evoked sexual behavior in Rhesus monkeys

Male rhesus monkey sexual behavior occurring spontaneously or evoked by remotely-controlled hypothalamic stimulation was studied in dominant and subdominant males with both dominant and subdominant, estrogen-treated or untreated, ovariectomized females. The behavior was quantified in terms of number and duration of ejaculatory sequences, number of thrusts, and number of mounts per sequence. Little or no spontaneous sexual behavior was observed with an untreated ovariectomized female. However, evoked sexual behavior with the exception of evoked ejaculation could be obtained whether the females were treated or untreated. Spontaneous and evoked sexual behavior was directed towards both dominant and subdominant females. The female chosen by the male was in part determined by the dominance status of the female. Evoked sexual behavior differed from spontaneous behavior in terms of an increased number of thrusts per mount, an increased number of ejaculations per session, and a decrease in latency between ejaculatory sequences.     

Sexual behavior of wild Barbary macaque males (Macaca sylvanus)

Recent assertions that the Barbary macaque (Macaca sylvanus) is a multiple-or serial-mounting species are incorrect. Data are presented from over 300 copulations observed among wild Moroccan Barbary macaques which establish empirically that males of this macaque species are single mounters. The average length of an ejaculatory copulation was 8.7 sec, with a range of 6 to 14 sec. Ejaculation occurred an average of 6.3 sec after mounting, with an average of nine pelvic thrusts per ejaculation. Males appeared capable of ejaculating twice within 16 min, and three consecutive times within 37 min. Characteristically, only one mount and ejaculation occurred during a sexual association between an estrous female and each of her consorting males. Schemes of macaque evolution which incorrectly classify Barbary macaques as a multiple-mounting species should be viewed cautiously.     

Ejaculation by male rhesus as a function of the female partner

Nine adult male rhesus monkeys were given eight 10-min tests of sexual behavior with eight ovariectomized female rhesus pretreated with estradiol benzoate. Males differed significantly in the number of tests during which they ejaculated, and females differed in the frequency with which specific males ejaculated when tested with them. With phylogenetic increase in neocortex, pair compatibility may be as important as hormonal stimulation in regulating male sexual performance. If this is correct, the problem of understanding the determinants of primate sexual behavior becomes more formidable.     

Effects of testosterone on the behavior of male cynomolgus monkeys (Macaca fascicularis)

To determine the threshold doses of testosterone propionate (TP) that cause clear-cut behavioral changes in the sexual behavior of castrated male cynomolgus monkeys, observations were made on three males during successive 5-week treatment periods while they received daily subcutaneous doses of 100 μg TP increasing in octaves to 25.6 mg TP. Males were tested with each of the same two ovariectomized, estrogen-treated females (6 pairs, 330 1-hr behavior tests). To mimic the diurnal plasma testosterone rhythm, TP injections were given at 1600 hr and blood samples were obtained at 0800 hr (141 samples). Male ejaculatory activity increased at the threshold dose of 200 μg TP per day giving plasma testosterone levels of 830 ng/100 ml, which is in the physiological range of 600–1600 ng/100 ml for intact males. This threshold dose was eight times higher than in rhesus monkeys on a dose per kilogram body weight basis. There was a further marked increase in ejaculatory performance at higher doses (6.4 to 25.6 mg) giving supraphysiological plasma levels of 4000–9000 ng/100 ml. There were individual differences in the behavioral changes occurring with TP treatment, and the female partner modulated the effects. These findings were generally similar to those obtained with male rhesus monkeys, but certain species differences were noted.     

Diurnal patterns of testosterone, dihydrotestosterone, estradiol, and cortisol in serum of rhesus males: Relationship to sexual behavior in aging males

This study was carried out to determine differences between old and young rhesus males in levels and diurnal patterns of testosterone, dihydrotestosterone, cortisol, and estradiol, and to determine correlations between these hormones and sexual behavior of the old males. Blood was drawn from old (n = 9) and young (n = 9) rhesus males over 5 consecutive days at 0900, 1300, and 2100 hr. The two groups of males did not differ in mean serum levels of testosterone, dihydrotestosterone, or estradiol at any time. Although the old and young did not differ in cortisol levels at 0900 and 1300 hr, the cortisol levels at 2100 hr were lower in the old males. Diurnal variations in testosterone, dihydrotestosterone, and cortisol were comparable in old and young males. Mean serum levels of estradiol were significantly higher at 0900 hr than at 1300 hr in the old males, whereas in the young males estradiol levels did not differ with time of day. There was a significant positive correlation between testosterone and yawning rate, and cortisol levels were correlated positively with rate of contacting, rate of mounting, and percentage of tests with erections. The decline in sexual performance of old rhesus males cannot be attributed to changes in the levels or diurnal patterns of testosterone, dihydrotestosterone, or estradiol, but lower cortisol levels in old males may contribute to the decline in sexual behavior.     

Estradiol administration and the sexual activity of castrated male rhesus monkeys (Macaca mulatta)

To examine whether estradiol might be effective in maintaining sexual behavior after castration or after testosterone withdrawal, we have observed male rhesus monkeys during daily 1-hr tests alternately with each of two ovariectomized, estradiol-treated females (four males, four females, eight male-female pairs, 798 tests). Estradiol (2-5 micrograms/kg sc/day) or vehicle was administered in counterbalanced order immediately after castration and again immediately after withdrawal of testosterone propionate treatments (800 micrograms and 1.6 mg sc/day). There were no significant differences in behavior during vehicle and estradiol treatments to indicate that estradiol helped to maintain male sexual activity. Instead, estradiol treatment tended to interfere with the capacity to intromit. This supported the results of other studies, namely, that the systemic administration of estradiol does not enhance the sexual behavior of castrated male macaques, and raises questions about the role of both aromatization and estrogen receptors in the male primate brain.     

Decrease in sexual initiative and responsiveness in female rhesus macaques (Macaca mulatta) during pregnancy

Although the sexual behavior of female rhesus macaques (Macaca mulatta) has been reported to decrease during pregnancy, systematic studies have been largely confined to reports of male behavior. Therefore, we designed a study to examine changes in female sexual behavior during pregnancy. Six cycling multiparous female rhesus macaques were paired during the periovulatory period of the menstrual cycle and during the first and second halves of pregnancy with six sexually experienced males of the same species. Each female was paired with the same male in all tests. The means of the behavioral measures scored on days 11–13 of the menstrual cycle, 35–56 of pregnancy, and 147–168 of pregnancy were compared. Females showed a significant decrease in the present contact ratio and the rate of threat-aways during pregnancy. Males showed lower rates of threatening-away, contacting, mounting, intromitting, and ejaculating when females were pregnant. The extent to which the decrease in male sexual behavior can be accounted for by an increase in female rejection is uncertain, but it is probably as significant as any loss of attractiveness that might accompany pregnancy.     

Effects of ovarian hormones on the behavior of captive Macaca fascicularis

To examine the effects of ovarian hormones on the behavior of female Macaca fascicularis and their male partners, daily 1-hr behavior tests were conducted while ovariectomized females were (1) untreated, (2) given estradiol benzoate (EB) (5 μg subcutaneously [s.c.]/day), (3) given estradiol benzoate together with increasing doses of progesterone (P) (5 mg, 10 mg, and 20 mg. s.c./day), and (4) given testosterone propionate (TP) (0.25 mg s.c./day) (six pairs, 540 tests). Weekly blood samples were analyzed by radioimmunoassay for plasma hormone levels (81 samples). Estrogen treatment produced plasma estradiol levels similar to those of intact females during the late follicular phase of the menstrual cycle. Additional progesterone at the lowest dose produced plasma progesterone levels similar to or somewhat higher than those during the midluteal phase, while higher doses produced supraphysiological levels. Androgen treatment resulted in plasma levels well above the physiological range. Hormone treatments produced highly significant effects on the sexual, social, and aggressive interactions of the pairs. As in rhesus monkeys, estrogen increased male and female sexual activity, and increasing doses of additional progesterone reversed these effects. Unlike in rhesus monkeys, testosterone propionate increased both female sexual motivation (invitations) and also male sexual activity and ejaculatory performance. The direction of the hormone-dependent changes in grooming and aggressive interactions confirmed earlier results with intact females and indicated that aggressive interactions and male grooming times were highest, and female grooming times were lowest, when copulatory activity was at its height.     

Relation between the hormonal status of the female and direct and redirected aggression by male rhesus monkeys (Macaca mulatta)

Each of 16 feral-reared male rhesus monkeys was paired with an ovariectomized female (8 females) during daily 60-min behavior tests (16 pairs). Each male received 8 consecutive tests with an untreated female, 8 tests when the female received injections of estradiol, and finally 8 tests after estrogen was withdrawn (total, 384 tests). Of the 16 males, 11 threatened sufficiently often for numerical analysis (“aggressive” males). Two of these males showed no changes either in sexual activity or in agonistic behavior when the females were estrogenized. In the remaining 9 males, there was increased sexual activity when the females were estrogenized and this was associated with a significant decrease in direct aggression (P < 0.01) and an increase in redirected aggression (P < 0.05). The demonstration in the same males of an inverse relation between threats directed toward and away from the female supports the hypothesis that threats directed away from the sexual partner represent aggression aroused by the partner that is redirected onto the environment when sexual interest increases.     

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.     

Copulatory behaviour of the bank voleMyodes glareolus: matings with one and two males do not make a difference

In promiscuous species in which females mate with more than one male during oestrus, males may increase their sperm expenditure or change their copulatory behaviour in response to the risk of sperm competition. I used an experimental approach to investigate the pattern of copulatory behaviour of the bank voleMyodes glareolus Schreber, 1780 depending on whether the female mated with one or two males. The work showed that the copulatory period of the bank vole lasted about 80 minutes and consisted of 4–5 ejaculatory series, with multiple intromissions preceding ejaculation. There were no significant changes in number of intromissions across the first four ejaculatory series, but I did find a relationship between number of intromissions and first ejaculation latency; also, ejaculation latencies grew shorter as the ejaculatory series proceeded. Litter size did not differ significantly between females that mated with one male and those mating with two, nor did the reproductive success of males that mated with the same female. Mating with an oestrus female appears to be advantageous for bank vole males even if they mate as the second one, and the risk of sperm competition did not trigger changes in male copulatory behaviour. The similar durations of the copulatory period and patterns of change of ejaculation latencies during copulations with one and two males point to the role of the female in temporal copulatory behaviour of the bank vole.     

Previous sexual experience alters the display of paced mating behavior in female rats

The present study tested whether the display of paced mating behavior in female rats over four weekly tests is affected by sexual experience and whether test parameters, i.e., ending the test based on time or number of stimulations received, influence behavioral changes. In Experiment 1A rats with nonpaced sexual experience returned to the male more quickly overall compared to sexually naïve rats in a 30-min test of paced mating behavior. In Experiment 1B, rats received four weekly 30-min tests with one, different, male rat partner each week. Over the four tests, rats returned to the male significantly more quickly after intromissions, but significantly more slowly after ejaculations. Experiment 2A tested whether sexual experience would influence paced mating behavior in tests with a 15-intromission end criterion and the male replaced after ejaculation. Rats tested weekly under 15-intromission test conditions returned to the male significantly more quickly after intromissions, but no behavioral change was observed after ejaculations. When those same rats were given a 30-min test of paced mating behavior (Experiment 2B), they returned to the male significantly more slowly after ejaculations. Collectively, these data show that sexual experience influences the display of paced mating behavior in female rats and that the test parameters interact with sexual experience to influence the nature of the changes. Sexual experience may facilitate behaviors that promote reproductive success in female rats.     

Adult partner preference and sexual behavior of male rats affected by perinatal endocrine manipulations

Intact adult male rats, in which aromatization of testosterone to estradiol was prevented pre- and/or neonatally by ATD (1,4,6-androstatriene-3,17-dione), were repeatedly tested for partner preference behavior (choice: estrous female vs active male). In consecutive tests increasing preference scores for the female were found. Neonatal ATD males showed significantly lower preference scores for an estrous female than controls or prenatal ATD males. Prenatal ATD caused preference scores only slightly lower than those of controls. Ejaculation frequencies were markedly reduced or even absent in neonatal ATD males. Prenatal ATD treatment only had no or a moderately lowering effect on ejaculation frequency. Lordosis behavior of adult intact males was more facilitated following neonatal ATD treatment than following prenatal ATD treatment. In a number of tests the serotonergic drug 8-OH-DPAT was injected prior to testing for sexual partner preference and copulatory behavior. DPAT significantly increased preference for an estrous female in all groups of males when interaction was possible, but had no effect when sexual interaction was prevented by wire mesh. DPAT was able to increase the number of ejaculators in nonejaculating groups (i.e., perinatally ATD-treated males). "Premature ejaculations," i.e., ejaculations with the first intromission, were frequently observed with DPAT treatment in all groups of males. In conclusion, the availability of neonatal estrogen (derived from testosterone) organizes, at least partially, the preference for an estrous female normally shown by adult male rats. The lack of neonatal estrogen causes males to be less masculinized, both in partner preference behavior and ejaculatory behavior, and less defeminized in lordosis behavior.(ABSTRACT TRUNCATED AT 250 WORDS)     

Sexual behavior of laboratory- and wild-born male Rhesus monkeys.

Rearing method has an important influence on the sexual performance of adult male rhesus monkeys. Testosterone levels and sexual behavior of laboratory-born and -reared adult males were compared with those of males born in the wild and brought to the laboratory as adults. The mean sexual performance level of colony-reared animals was significantly below that of males born in the wild but testosterone levels in the two groups did not differ significantly. Not all laboratory-reared males were sexually inadequate but less than 30% ejaculated in tests of sexual behavior. The sexual behavior and testosterone levels of adult males treated prenatally with testosterone propionate were found not to differ from those of untreated males reared in the same way. Conclusions about sexual adequacy based on 10-mm tests of sexual behavior differed very little from those based on 1-hr tests.     

Female sexual behavior displayed by androgenized female rhesus macaques

Adult, prenatally androgenized female rhesus macaques (female pseudohermaphrodites) that had been ovariectomized were treated with estradiol benzoate (20 micrograms/day) and paired with males at weekly intervals for 4 weeks beginning on Day 12 of injection. Their sexual behavior was compared to that of a control group of females. The sexual behavior of the males toward the two groups of genetic females (control females with normal female genitalia and hermaphrodites with well-formed male genitalia) was also observed. Females and hermaphrodites were equally receptive to male invitations to copulate. Although there were some differences in the specific components of proceptive behavior displayed by the two groups, the overall differences were negligible. Earlier studies had shown that infant and juvenile hermaphrodites resemble males in patterns of play and sexual behavior. When treated with testosterone as adults and paired with receptive females, they displayed mounting patterns typical of males--one of seven hermaphrodites achieved intromission and ejaculated. It has now been demonstrated that when treated with estrogen and paired with males, they responded as females. Hence, the capacity to behave sexually as males is not incompatible with the capacity to respond sexually as females under certain hormonal and environmental conditions.     

A quantitative description of copulatory and associated behaviors of captive marmosets (Callithrix jacchus)

Measurements of male and female copulatory behavior in pairs of common marmosets were made during 30-min mating tests (n = 170). For the male,both frequencies and latencies of mounting, pelvic thrusting, and ejaculatory behaviors were analyzed. For the female, frequencies of proceptive displays (tongue-flicking) and of sexual receptivity were measured. The sexual and associated behavior of the marmoset is compared to that of other primates and the suitability of this species for laboratory studies of neurohumoral mechanisms and sexual behavior is assessed.