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.     

Direct measurements of urinary estrone conjugates during the normal menstrual cycle of the gorilla (Gorilla gorilla)

A direct immunoassay for urinary estrone conjugates (estrone sulfate and estrone glucuronide) was used to assess the preovulatory estrogen rise in normal gorilla menstrual cycles. Immunoreactive estrone conjugates in samples concomitantly assessed for total estrogen immunoreactivity reflected similar profiles throughout the cycle; however, the speed and resolution of the direct assay for conjugates indicate this method to be more accurate in monitoring ovulation than the measurement of total immunoreactive estrogens. In a single conceptive ovarian cycle, urinary estrone conjugate continued to rise in the luteal phase, indicating that this test may also be useful for detecting early pregnancy. The application of this technique provides clear profile of ovarian function in gorillas as well as in other primate species.     

Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla)

We explored two hypotheses related to potential differences between sexes in dispersal behaviour in western lowland gorillas (Gorilla gorilla gorilla). Direct observations suggest that immature females have more opportunities to move between breeding groups than immature males. The distribution of kin dyadic relationships within and between groups does not, however, support this hypothesis. At larger geographical scales, dispersal is likely to be easier for males than females because of the solitary phase most blackbacks experience before founding their own breeding group. However, previous work indicates that males settle preferentially close to male kin. By specifically tracing female and male lineages with mitochondrial and Y-chromosomal genetic markers, we found that male gorillas in the 6000 km2 area we surveyed form a single population whereas females are restricted to the individual sites we sampled and do not freely move around this area. These differences are more correctly described as differences in dispersal distances, rather than differences in dispersal rates between sexes (both sexes emigrate from their natal group in this species). Differences in resource competition and dispersal costs between female and male gorillas are compatible with the observed pattern, but more work is needed to understand if these ultimate causes are responsible for sex-biased dispersal distances in western lowland gorillas.     

Growth and feeding relationships of a hand-reared lowland gorilla infant (Gorilla g gorilla)

A captive-born female lowland gorilla that was being hand-reared by a group of surrogate mothers in a public zoo was observed for her first 6 mo. Caloric intake and weight gain, along with feeding bias of surrogate mothers, were examined. Caloric intake was highest during early morning and late at night. The weekly caloric intake and weight gain fluctuated with no established pattern. Although the gorilla's caloric intake did not increase with age, her total weight increased with a slower growth rate in the latter part of the study period, indicating a decreased caloric intake/weight ratio. It became evident that each surrogate exhibited an “overfeeding” and “underfeeding” tendency; calories given by the surrogates varied considerably, reflecting the interaction between the infant and the surrogates.     

Urinary steroid evaluations to monitor ovarian function in exotic ungulates: III. Estrone sulfate and pregnanediol-3-glucuronide excretion in the Indian rhinoceros (Rhinoceros unicornis)

A study was undertaken to identify urinary estrogen and progesterone metabolites in the female Indian rhinoceros (Rhinoceros unicornis). Measurements of these metabolites were then used to monitor ovarian function and establish normal levels and patterns of steroid excretion during the estrous cycle and pregnancy. Urine samples were analyzed for estrone sulfate and pregnanediol-3-glucuronide (PDG) by direct radioimmunoassays. Both hormones produced discrete profiles reflecting ovarian activity in nonconceptive cycles. The estrous cycle was observed to be 48 days (range 39–64) with a mean follicular phase of 14.8 days (range 13–19), followed by a mean luteal phase of 19 days (range 17–21). Of the single gestation monitored, PDG levels rose above luteal phase levels by the third month after breeding and remained elevated throughout gestation. The combined estrogen and progesterone metabolite profiles present a complete evaluation of ovarian steriod production in the mature female Indian rhinoceros.     

Spatial memory and foraging competition in captive western lowland gorillas (Gorilla gorilla gorilla)

Spatial memory and foraging competition were investigated in three mother/offspring pairs of western lowland gorillas,Gorilla gorilla gorilla, using a naturalistic foraging task at the Toronto Zoo. Sixteen permanent food sites were placed throughout the animals’ enclosures. All of the sites were baited and a pair of animals was free to visit the sites and collect the food. Five of the subjects collected the food with accuracy better than chance. Most of the subjects visited the sites using a pattern, and for half the subjects this was one of adjacency. The high accuracy of five of the subjects and the lack of a consistent adjacency pattern suggest that the animals did in fact use spatial memory. Furthermore, the gorillas tended to avoid visiting food sites that had been previously depleted by their partner. They also appeared to split their search of the enclosures, each visiting only a proportion of the food sites. This indicated that the animals were competing and altering their foraging behaviour based on the behaviour of their partner. Therefore, accuracy was recalculated to take this into account. When the sites depleted by either animal in a pair during a given trial were worked into the accuracy calculations for individual animals, three of the animals still maintained accuracy above chance. This suggests that the animals were not only able to remember which sites they had depleted, but those sites depleted by their foraging partner as well.     

Urinary steroid evaluations to monitor ovarian function in exotic ungulates: V. Estrogen and pregnanediol-3-glucuronide excretion in the black rhinoceros (Diceros bicornis)

A study of female black rhinoceros (Diceros bicomis) urinary steroid and steroid metabolite excretion was performed to determine if techniques useful for monitoring reproductive events in the Indian rhinoceros (Rhinoceros unicornis) could be utilized to evaluate the black rhinoceros. Urine samples from 19 zoo-held black rhinoceros were analyzed for estrogen, estrone conjugates (EC), and pregnanediol-3-glucuronide (PDG) content by direct radioimmunoassays. Estrogen analysis revealed that >95% of the estrogens present in female black rhinoceros urine are conjugated, with estrone and estradiol accounting for virtually all of these estrogens. There is no observable difference in the amount of estrogen present in estrus; postestrus; and early-, mid-, and late-gestation urine samples. Analysis of serial urine samples for EC failed to reveal any discernible levels or patterns which reflected reproductive status. Neither nonpregnant nor early-gestational female black rhinoceros' urine samples contained detectable amounts of PDG. Urinary PDG concentrations became measurable in midgestation (9–12 months prior to parturition) and rose steadily throughout the remainder of gestation. PDG levels declined sharply and became nondetectable 1 day postpartum. Though a wide range in PDG levels was observed among individual pregnant animals, each female consistently excreted increasing amounts of PDG through latter pregnancy.     

The development of infant play in a captive group of lowland gorillas (Gorilla gorilla gorilla)

Three infant gorillas born at the Yerkes Regional Primate Research Center of Emory University were studied during their first year and one-half of life for various aspects of behavior, including solitary and social play, using both focal animal and one-zero sampling. The appearance of play in these infants followed a developmental trend, beginning with mother-infant play, and followed by solitary play, and then social play among peers. Mothers were initially very vigilant, repeatedly interrupting infant peer play bouts, this relaxing toward the end of the first year. Evidence for a possible sex difference in active social play is presented.     

Several examinations on the reproductive status of lowland gorillas (Gorilla g. gorilla) at Hannover Zoo

There as been no reproduction within the Hannover Zoo's gorilla group, although several adult females and a silverback male have been living together for a prolonged period. Therefore, the sexual cycle of three adult females was examined by means of total urinary estrogen excretion, measurement of the urogenital cleft length, ovulation detection with the help of the Subhuman-Primate-Pregnancy Test (SPPT), measurement of basal body temperature, semiquantitative blood tests to detect menstruation, and observation of sexual behavior. Fertility status of the silverback male was examined by means of behavioral observation, rectal probe ejaculation (RPE), and testicular biopsy. Sexual cyclicity was demonstrable in two females, whereas the third had an irregular occurrence of estrogen peaks and her menstruation and sexual behavior did not show normal cyclicity. The male's infertility was characterized by absence of any sexual behavior, azoospermia in repeated RPE, unsuccessful treatment with clomiphene, and atrophy of seminiferous tubules in the extirpated tissue. Several factors, such as vitamin E deficiency, humoral dysregulation, testicular hypoxy, and spermatogenic arrest, caused through stress due to inadequate shelter systems, are discussed hypothetically in regard to their possible etiological relevance with respect to infertility in this species. In many cases infertility in the gorilla male is presumably based on a polyfactoral etiology. Analysis of urinary hormone levels in parallel with behavioral studies is still to be tested as a practical method of gaining information on the puberty development of adolescent males and on the fertility status of adult males under zoo conditions.     

Timing of surgery during the menstrual cycle and prognosis of breast cancer

There are conflicting reports on the differential effect of surgery performed during the two phases of the menstrual cycle, namely, follicular and luteal, and prognosis of operable breast cancer. A statistical meta-analysis of the published evidence suggests a modest survival benefit of 15+/-4% when the operation is performed during the luteal phase. Further research in this area might provide a novel avenue to understand the natural history of breast cancer. A spin off from these studies might be the understanding of the importance of events that occur at the time of surgery in determining long term prognosis.     

Reproduction in the vervet monkey (Cercopithecus aethiops): II. Annual menstrual patterns and seasonality

Menstrual patterns and progesterone levels were monitored for 5 years from a cohort of 28 female vervet monkeys that were individually caged indoors. Three distinct cycle types (short, normal, and prolonged) were defined according to cycle length. Mean length of the normal cycle (32.5 days) and menses duration (4.8 days) are in agreement with previous reports. Prolonged cycles (> 50 days) contributed 20% of the total, with a decreased incidence during the natural peak breeding period. Weekly progesterone measurements indicated that many prolonged cycles were associated with an extended luteal phase, while others were probably due to lack of ovulation. From these data it would appear that the vervet monkey, although not strongly seasonal, does favor a particular time of year for breeding in a colony housed indoors.     

Behavioral responses of an infant gorilla to maternal separation in a captive social group of lowland gorillas (Gorilla gorilla gorilla)

The present report describes behavioral reactions of a 33-month-old female infant gorilla to maternal separation in a captive social group whose composition is similar to that of wild groups. The infant gorilla responded differently to two types of maternal separation. When she remained alone for a few hours, she cried repeatedly and moved restlessly, indicating protest. Upon reunion and also for a few days thereafter, an intensification of the mother-infant relationship occurred. On the other hand, when she was separated from her mother but remained with the other group members for nine days, she did not display any behaviors that could be characterized as protest, but rather showed clear behavioral depression. During the 9-day separation period, she hardly played with other group members but she developed affiliative relationships with the leading male. After the reunion from the 9-day separation, she spent as much time near her mother as before separation and played with other infants at a level similar to that before separation, while she sometimes displayed behavioral patterns demanding the maintenance of physical contact with her mother. The present findings are compared with other reports in great apes and human children.     

ORIGINAL ARTICLE: Medical and surgical management of reproductive neoplasia in two western lowland gorillas (Gorilla gorilla gorilla)

Background Reports of female reproductive tract neoplasia are infrequent in great apes. Methods Two captive‐born, female western lowland gorillas (Gorilla gorilla gorilla) housed at the North Carolina Zoological Park were diagnosed with reproductive neoplasia. Results The first gorilla had uterine endometrial thickening and uterine fibroids diagnosed during a routine annual examination. Subsequently, the animal underwent several uterine curettage procedures in an attempt to debulk the uterine mass. Biopsy results indicated uterine adenocarcinoma. The animal was treated with an ovariohysterectomy followed by a combination of megestrol acetate and medroxyprogesterone acetate. The second gorilla was diagnosed with squamous cell carcinoma of the vagina, cervix, and uterus after presenting for intermittent vaginal bleeding of 1‐month duration. This animal underwent palliative radiation therapy, receiving two rounds of radiation treatment 8 weeks apart. Conclusions The following report describes the diagnosis and management of the two cases.     

Serum levels of gonadotropins and gonadal steroids,including testosterone,during the menstrual cycle of the chimpanzee (Pan troglodytes)

The objective of this study was to expand the data on menstrual cycle serum hormone patterns in female common chimpanzees, both in terms of the number of cycles analyzed and by the addition of data on testosterone levels. Samples were obtained from 11 unanesthetized animals trained for conscious blood withdrawal. LH, FSH, 17β-estradiol (E₂), progesterone (P), and testosterone (T) were measured by radioimmunoassay, genital swelling was recorded, and menstrual blood was noted. Concurrent midcycle elevations in LH and FSH and luteal phase elevations in progesterone suggested that the cycles were ovulatory. Detumescence of genital swelling occurred about 3 days after the midcycle LH peak, 1 day after the luteal phase nadir in E₂, and 1 day after P levels exceeded 5 ng/ml. These relationships provide further support for the use of genital swelling in monitoring progress of the menstrual cycle. The hormone patterns in the chimpanzees closely resembled those of the human females, but E₂ and T levels were higher. The levels of E₂ and T were higher and the midcycle elevation in T was broader in the chimpanzee than in gorillas and orangutans. This is of interest because E₂ and T are implicated in the regulation of mating, and chimpanzees mate over a greater portion of the cycle than the other apes. These data indicate the need for further study of hormonal contributions to the different patterns of mating in the great apes. They also support the use of the female common chimpanzee as a model for the human female in endocrine studies of the menstrual cycle.     

Deception and hiding in captive lowland gorillas (Gorilla gorilla gorilla)

Deception and hiding are described for a group of captive lowland gorillas comprising two adult males, one female, and her infant. The males repeatedly interacted with the infant, and their interest was repeatedly thwarted by the mother. As in other social situations in which one animal controls access to an object desired by another, deceit was used to thwart the other's control. Either one or both males at times concealed their actions toward the infant, inhibited their attention to the infant, created a neutral image to get the infant, or interacted with the infant to tease the mother.