Sexual behavior of maternally separated gibbons (Hylobates).

The effect of early maternal separation on the sexual behavior of captive gibbons was investigated because (a) maternal separation compromises sexual behavior of some nonhuman primates and (b) adequate sexual behavior is essential to species propagation. Most of the maternally separated gibbons (24/31) were sexually proficient. Sexual behavior overall did not differ significantly in relation to species, sex, origin (wild-vs. captive-born), or type of rearing facility (home vs. zoo). Sexual proficiency was not related to the age at separation from the mother, but it was associated with introduction within 19 months of age to a conspecific of less than 3 years of age and an absolute age difference of less than 2 years. Sexual proficiency was associated with rearing and adult housing in relatively large enclosures. Gibbons that were isolated from conspecifics between 6 months and 2 years of age were strongly attached to humans, but this did not prevent sexual proficiency. A greater proportion of males than females were adversely affected sexually by prolonged early social isolation. Inadequate sexual behavior was associated with fearfulness of conspecifics, which probably interfered with compatible social relationships, including duetting. Inadequate sexual behavior was but one aspect of a more general behavioral deficiency resulting from inadequate early socialization. Early maternal separation in gibbons is compatible with species-typical sexual behavior under the conditions described above. It is not necessary for gibbons to learn sexual and parental behavior by observing experienced adult conspecifics.

Penile erection: a reflection of sexual arousal and arousability in male chimpanzees.

A study was conducted to determine if sexual motivation in male chimpanzees, defined by the two components, sexual arousal and arousability, could be quantified by measuring penile erection during laboratory pair-tests of sexual behavior. Sexual arousal, the momentary level of sexual excitation, was quantified by single measurements on a scale of penile erection. Sexual arousability, the propensity for arousal, was quantified by the rate of approach to full erection and by mean erection scores. Sexual arousability, as defined, was related to the frequency of male courtship displays, copulations, and ejaculations, which were highest at midcycle and positively correlated with a quantitative measure of female anogenital swelling. Sexual arousal was negatively correlated with continued exposure to the female and least variable during midcycle. These operational definitions of sexual motivation in the male chimpanzee facilitate comparative research in which analogous indexes of sexual motivation are required such as when extrapolating from animal to human.

Separation and depression in infant gorillas.

Three 27-month-old infant gorillas living with their mothers and a silverbacked male were separated to a cage for 24 weeks. The infants initially showed threat responses and increased locomotion, characteristic of the protest stage of anaclitic depression in children. Within several days, these were replaced by dorso-ventral contact among the infants as well as self-holding and fetal positioning. Additionally, social and solitary play and object examination occurred at lower levels through separation than in the pre-separation condition. These changes were characteristic of the despair stage of separation. There was a substantial recovery of many infant nonsocial and social behaviors in the later months of the separation. Upon reunion, the infants did not immediately engage in attachment behaviors with their mothers, and spent more time in contact with each other than with their mothers for the first several days, indicating detachment. Following this, there was an increase in mother-infant attachment behaviors.

Sexual behavior of chimpanzees (Pan troglodytes): male versus female regulation.

We investigated the sexual behavior of 13 chimpanzees (Pan troglodytes) in 2 types of pair test in order to clarify the interaction of social variables with female hormonal state. The frequency of copulation in tests in which the partners were freely accessible to each other was related to the male's dominance over the female; copulation was less frequent and was related to social compatibility in tests in which the female controlled access. Copulation was related to female hormonal state in both types of test. The results demonstrate (a) an association between female hormonal state and sexual activity of chimpanzees, (b) the influence of social relationships on sexual interactions, and (c) the importance of focusing on female sexual behavior before copulation, rather than copulation per se, in research on sexual arousability of female primates.

Effects of an oral contraceptive on sexual behavior of chimpanzees (Pan troglodytes)

Behavioral and physiological effects of a combined oral contraceptive (OC) were studied in chimpanzees for comparative purposes related to (i) the ambiguity surrounding the effects of OCs on the sexuality of humans, (ii) the close biological relationship between chimpanzees and humans, especially with respect to endogenous sex hormones and sexual behavior, and (iii) the relatively greater behavioral sensitivity of the chimpanzee to changes in sex hormone levels such as those that accompany the use of OCs. Two different types of pair tests and detailed behavioral assessments were used to differentiate the hormonal effects of female behavior from social effects imposed by the male. Anogenital swelling and copulation were reduced during OC cycles, but the effect of the OC on copulation was directly related to the social and sexual relationship of the pair during natural cycles. The more compatible and more frequently copulating pairs in the natural cycles continued to copulate during the OC cycles, albeit at reduced rates, whereas the less compatible and less frequently copulating pairs ceased copulating altogether when the female received the OC. There was no independent effect of the OC on ejaculation per se. Both male and female sexual initiative were reduced in the OC cycles, but female responsiveness to male sexual solicitations and direct copulatory attempts were not affected. Data indicate that despite generally adverse effects of the OC on certain physiological and behavioral dimensions of sexuality, social factors ultimately determined the degree of response to the OC.(ABSTRACT TRUNCATED AT 250 WORDS)

Spermatogenesis and hormone levels in rhesus macaques inoculated with simian immunodeficiency virus.

The presence of sperm in testicular tissue of rhesus macaques that died as a result of infection with simian immunodeficiency virus (SIV) was related to age and body weight. Depressed testosterone levels were not associated with elevated LH levels. The data suggest that azoospermia in the SIV-infected macaques was due to cachexia and not a direct effect of virus on the testis, supporting a similar hypothesis regarding azoospermia in men infected with human immunodeficiency virus.

Serum and urinary concentrations of sex hormones and genital swelling during the menstrual cycle of the gibbon.

The relationship between sex hormone concentrations and female genital swelling during the menstrual cycle in the monogamous gibbon was comparable with that of polygamous female primates, such as the chimpanzee, which live in multimale groups and have larger swellings. The data, therefore, support the hypothesis proposed by C. R. Carpenter more than 50 years ago, that the gibbon's genital swelling, like that of other female primates, reflects basic physiological processes associated with progress of the menstrual cycle. Genital swelling increased during the follicular phase with increasing concentrations of oestradiol and oestrone glucuronide, reached maximal swelling in association with the mid-cycle peaks in the oestrogens and LH and began detumescence with the initial increases in progesterone during the luteal phase. The data also suggest that the menstrual cycle of the gibbon is shorter than previously reported, since cycles of 19-22 days exhibited hormone patterns that are consistent with ovulation. The genital swelling of the female gibbon is a useful marker for monitoring progress of the menstrual cycle and the presumptive time of ovulation.

Testicle size of orang-utans in relation to body size.

Few data are available for assessing the relative testicle size of orang-utans, Pongo pygmaeus, so measures were obtained for 31 individuals of varying age. It was shown that the volume of the testicles, calculated from in situ measures of testicle length and breadth, closely approximates testicle weight when multiplied by the specific gravity of solid tissue. Growth curves for body weight and data published for wild specimens were evaluated to obtain the weight most characteristic of male Pongo, and the ratio of testicle weight to body weight was calculated. The mean ratio for individuals with fully adult stature is 0.034, similar to but smaller than that of humans at about 0.050, and larger than the ratios reported for 5 gorillas at 0.013. The testicles mature faster than the body, however, so the mean ratio for young adult orang-utans is about 0.056 and resembles the ratio for humans more closely than the full adults. The differences between the ratios for a monogamous gibbon species, orang-utans, and humans is accounted for when testicle size relative to the weight of the female is considered. This is consistent with a sperm dilution effect produced by variation in the size of the female reproductive tract. The small relative testicle size of the gorilla is anomalous and requires verification as does the application of female size to scale the testicles.

Hormone levels and anogenital swelling of female chimpanzees as a function of estrogen dosage in a combined oral contraceptive.

A combined oral contraceptive consisting of ethinyl estradiol (EE2) in three dosages (50, 100, and 400 micrograms) and norethindrone (0.5 mg) was given to female chimpanzees to determine the effect on endogenous sex hormone levels and anogenital swelling. Serum levels of EE2 increased with increasing dosages of EE2, estradiol decreased, and luteinizing hormone, progesterone and testosterone were maintained at approximately midfollicular phase levels. Urinary levels of EE2 glucuronide increased with the increasing dosages of EE2, whereas estrone and pregnanediol glucuronide were essentially undetectable. The cyclic increase in female anogenital swelling was abolished when the norethindrone was combined with 50 micrograms of EE2 and relatively constant and low levels of swelling were recorded. Relatively constant but successively higher levels of swelling were recorded when the norethindrone was combined with the higher dosages of EE2. These effects of oral contraceptives on female genital tissues are relevant to our laboratory studies of sexual behavior in chimpanzees given oral contraceptives and could also have implications for women taking oral contraceptives.

Genital swelling in females of the monogamous gibbon, Hylobates (H.) lar.

Cyclical changes in the vulvae of five adult lar gibbons (Hylobates [H.] lar) were studied and compared with those of eight lowland gorillas. The results reveal that the gibbons have relatively conspicuous and specialized sexual swellings that alter shape and appearance during the ovarian cycle. At maximum extent, the genital swellings of gorillas are relatively and absolutely smaller than those of gibbons, and lack the distinctive coloration seen in the genital swellings of the smaller apes. We conclude that the female gibbon's sexual swelling is a far more conspicuous and effective signal of estrus status than that of the gorilla, and that this is not explicable in terms of allometry. Previous investigators have pointed to one-male mating systems, monogamous pair-bonding, or an arboreal habitat as reasons that some primates should have less conspicuous signals of estrus than others. Our findings for the gibbon are the reverse of these predictions, and indicate that sexual selection other than by intermale competition for estrous females is implicated in the ultimate causation of the gibbon's swelling. The adaptive value and significance of the female gibbon's sexual signals remain unclear, however.

The external genitalia of female gibbons, Hylobates (H.) lar.

The external genitalia of one perimenarcheal and five adult female white handed-gibbons (Hylobates (H.) lar) were examined to clarify their gross anatomy. It was found that the vulval structures were complex and exhibited inter-individual variation in arrangement. This complexity appears to result from an ontogenetic process by which the tissues of the vaginal rim (the labia minora) bud-off and extrude extensions toward the vagina immediately prior and subsequent to menarche. Two of these lobular structures surround the urethral meatus and constitute a urethral eminence. The tissues of the vulva, excluding the clitoris with associated prepuce and frenulum and vestigial labia majora, undergo cycles of tumescence and detumescence during intermenstrual intervals. The complex form of the external genitalia and the presence of a swelling cycle are unusual for a monogamous species, are contrary to current applications of sexual selection theory, and raise questions about the significance of mate choice in hominoid evolution.

Behavioral responsiveness to strangers in young chimpanzees (Pan troglodytes).

Earlier studies of responses of primate infants to strangers were frequently confounded with separation from the attachment figure and/or removal to an unfamiliar setting. In the present study, young chimpanzees were tested in a familiar setting with a human female caretaker who served as an attachment figure. Two strangers were introduced: a human female, approximately the size of the caretaker, who refrained from initiating interactions and a larger human male, who repeatedly approached and initiated contact with the subjects. A somewhat more intense response was elicited by the larger, more assertive male stranger, but neither stranger elicited severe distress. The behavior of the chimpanzees is better described as wary, rather than fearful. These results may be attributable to the continued presence of the caretaker in contrast to previous studies reporting severe distress to strangers when chimpanzees are tested alone. A wariness of strangers in nursery-reared chimpanzees may develop by 6 months of age and may diminish somewhat by 2 years of age under the conditions of this study.

Sexual aggression in the great apes.

Species-typical frequencies of copulation during the menstrual cycle differ among common chimpanzee, orang-utan, and gorilla, but all three species exhibit a midcycle enhancement associated with estrus. Thus, in the natural habitat, chimpanzees mate for 10-14 days, orang-utans for 5-6 days, and gorillas for 2-3 days. In traditional laboratory pair-tests, however, conducted in a single cage with both animals freely accessible to each other, all three species of great apes copulate more frequently than the species-typical pattern. In all three species, moreover, the increased copulation appears to result from increased male sexual initiative (aggression), male dominance over females, and the inability of the female to avoid or escape from the male within the limited spatial conditions of the free-access test. This interpretation is supported by studies using restricted-access tests in which females control sexual access. These data suggest that male sexual aggression in our closest biological affiliates commonly occurs when females are rendered vulnerable to the male by the absence of the normal social constraints and spatial prerogatives typical of the natural habitat. The possible implications of this interpretation for a biological perspective on human sexual aggression are considered.

Hormones and behavior of prepubertal and peripubertal chimpanzees.

Twenty-one chimpanzees ranging in age from 2.9 to 9.2 years at the midpoint of a study consisting of five 4-week blocks were studied behaviorally in four groups of five or six animals per group, balanced for age and sex. Blood samples for radioimmunoassay of follicle-stimulating hormone (FSH), luteinizing hormone, 17 beta-estradiol, testosterone, dehydroepiandrosterone (DHA), DHA sulfate (DHAS), and cortisol were obtained once each 4-week block. Sex differences were found only in the categories of play duration and initiative and genital inspection, all of which were greater for the males. Several categories (6) of play and other affiliative behaviors were negatively correlated with age and/or body weight for the males, whereas fewer of those categories (2) were so correlated in the females. Hierarchical behavior, genital inspection, solitary behavior other than play, and autogrooming were all positively correlated with age and/or body weight for the males, and only autogrooming for the females. FSH and testosterone levels and testicular volume were positively correlated with age and body weight in the males, whereas for the females cortisol was negatively correlated with body weight and only FSH and the ratios of DHA and DHAS to cortisol were positively correlated with age and/or body weight. Most of the behaviors that were significantly correlated with age and body weight for the males were also correlated in the same direction with FSH and testosterone levels and testicular volume, but not with DHA or DHAS levels. The data are consistent with the view that testosterone, but not the adrenal androgens DHA and DHAS, contributed to the behavioral development of the males. There were few significant correlations between hormones and behavior for the females and interpretation is not clear. The absence of age-related increases in DHA and DHAS of both the males and females, in contrast to the pattern of FSH (and testosterone for the males), supports the growing consensus that adrenarche and puberty are independent developmental processes. The absence of any strong correlations between behavior and levels of the adrenal androgens in either the males or females suggests that adrenarche per se is not a significant event in the behavioral development of chimpanzees.

Sex-related behavior of immature wild mountain gorillas.

Sex-related behavior in immature wild mountain gorillas consisted primarily of genital stimulating episodes in which one animal thrusted against the body of another. Whereas the immature males used the D-V position predominantly, a single immature female that performed as an actor used the V-V position exclusively. All episodes of genital stimulating behavior originated in the context of play and most actors were older (and larger) than recipients of such behavior. The data support the findings of earlier research but suggest that genital stimulating behavior among immature gorillas occurs more frequently than previously thought. These results in conjunction with comparable data on pygmy and common chimpanzees and orangutans suggest that genital-stimulating behavior by immature individuals is a species-typical phenomenon in the behavioral development of the great apes.

Behavioral responsiveness of young chimpanzees (Pan troglodytes) to a novel environment.

Behavioral responsiveness to a novel environment was documented in 22 chimpanzees grouped according to age; 6-months, 1-year, 2-years and 5-years. An attachment figure, a human caretaker, accompanied each subject during the 15-min test sessions so as to preclude confounding of responses to novelty with separation responses. Extreme distress reported previously for chimpanzees and human children when tested alone in a novel situation was rarely observed in these tests when an attachment figure was present. Stereotyped rocking, an indication of mild distress occurred more frequently in the younger animals. Younger animals engaged in distal visual exploration of the environment while remaining close to the attachment figure, whereas the older animals locomoted more frequently and explored the environment directly with their hands. Repeated exposure to the environment reduced the differences among the 6-month, 1-year and 2-year groups. The 6-month group, however, continued to locomote least and least frequently engaged in tactile exploration. These data on chimpanzees resemble data on human children which suggest that an attachment figure: attenuates the distress exhibited by young individuals of these species when exposed to novel stimuli, and thereby provides a secure base which supports the exploration of novel stimuli, a prerequisite to behavioral adaptation.

Hormone responses to clomiphene citrate in young chimpanzees.

The responses of gonadotropin and gonadal steroids to the administration of clomiphene citrate were studied in male and female chimpanzees, aged 3.6 to 9.9 years. Follicle-stimulating hormone (FSH) was significantly reduced after treatment in the prepubertal females (n = 4) and in early pubertal males (n = 2) but not in prepubertal males (n = 5). FSH was unchanged or increased in early pubertal females (n = 2) and late pubertal males (n = 2). There was no consistent response to treatment with clomiphene citrate by luteinizing hormone (LH) in either males or females, nor by 17 beta-estradiol in the females. Testosterone levels were reduced in the early pubertal males only. These results support the hypothesis that negative feedback by gonadal steroids is operative in prepubertal chimpanzees and that puberty is accompanied by a reduction in the sensitivity to such feedback.

[Hormonal and compartmental correlates during adrenarche in the chimpanzee]. / Corrélations hormonales et comportementales au cours de l'adrénarche chez le Chimpanzé.

Ten male and eleven female Chimpanzees from three to nine years of age were studied to establish possible correlations between behavioral changes and hormonal changes peculiar to adrenarche and the pre-puberty period. Most of the thirteen behaviors studied varied with age, body weight and hormones. For the males, the correlations were significant statistically for age, weight and plasma concentration of testosterone and of FSH. The correlations for the females were more often not significant statistically. In ten out of the thirteen behaviors for the female, however, the correlations with the sulfate of plasma dehydroepiandrosterone were in the same direction as those observed for the males with testosterone.

Luteinizing hormone and gonadal steroid levels during the menstrual cycle of orangutans.

Serum luteinizing hormone (LH), progesterone, 17 beta-estradiol, and testosterone were measured during a single cycle each of five female orangutans, and urinary LH was measured in four of those cycles. Midcycle peaks in LH and luteal phase elevations in progesterone (5.7-13.8 ng/ml) suggested that the cycles were ovulatory. 17 beta-Estradiol was elevated at midcycle (163-318 pg/ml) and during the luteal phase (56-136 pg/ml) and testosterone was also elevated at midcycle (143-580 pg/ml). These hormone patterns in the orangutans closely resemble those for chimpanzees, gorillas, and human females.