Tomoo Enomoto

On social preference in sexual behavior of Japanese monkeys (Macaca fuscata)

Sexual interaction patterns between both sexes in a Japanese monkey troop were classified into eight types by taking approach, following and stability of mounting series as indicators. Analysis of these types in pairs in several types of social relation demonstrated the structure of social preference for the sexual partner as follows: (1) pairs in grooming, genealogical or protecting-depending relations tend to show few sexual interactions between each other; (2) the males of the pair in co-walking or co-eating relations behaves actively to the female, but, in the typical case, the female refuses her partner; and (3) both sexes of the pair in the chasing relation show the most active interactions including ejaculation.

Habitat Use and Ranging of Wild Bonobos (Pan paniscus) at Wamba

The relationship between vegetation and ranging patterns of wild bonobos at Wamba, Democratic Republic of the Congo, was examined. Via Landsat data, we distinguished three types of vegetation—dry forest, swamp forest, and disturbed forest—at Wamba. The home ranges of the study groups changed considerably from year to year, due mainly to intergroup relationships. The population density of each group varied between 1.4 and 2.5 individuals per km2and was lowest during a period of population increase. Home ranges consisted mainly of dry forest. The bonobos used dry forest more frequently than the other forest types, though they also used swamp and disturbed forest almost every day. The latter types of forest seemed to be important resources for the bonobos, owing to the abundant herbaceous plants that are rich in protein and constantly available. The bonobos tended to use dry forest more frequently in the rainy season than in the relatively dry season, probably because the favored fruits in the dry forest were mostly available in the rainy season. There was no seasonal difference in the size of the daily ranging area.

Social play and sexual behavior of the bonobo (Pan paniscus) with special reference to flexibility

The social play behavior of the bonobo, or pygmy chimpanzee, was studied in a provisioned group at Wamba, Zaire. Ethograms of the play behavior among young, between mothers and their offspring, alloparental care, play-like sexual behavior, and play among adults are presented with descriptions of specific episodes. Between juveniles, rough-and-tumble play was predominant. Sexual behavior was sometimes inserted within the play context, and playful copulation and variously modified sexual behaviors were also observed. Although the patterns of paternal care of the adult male bonobos were not so different from those reported for the chimpanzee, they characteristically included activities with sexual elements. Play behavior among adults could be detected, and some play functioned resolve tensions among them. It is suggested that because play is functionless in a direct way, it appears to create flexibility in adult behavior, and that the self-handicapping characteristically observed in play possibly promotes reciprocal interactions based on an equality principle.

Male aggression and the sexual behavior of Japanese monkeys

The factors that regulate male aggressive behavior towards females during the mating season and their relationship to the sexual behavior of Japanese monkeys were investigated. Observations were made on the Shiga A troop in Nagano Prefecture for 132 days during both the non-mating and mating seasons in three successive years. As a result, chasing towards females was observed in males older than 4 years. The frequencies of this type of behavior increased in the mating season. The chasing rank of the individual males did not correlate with the male dominance rank but with the tree-shaking rank. Chasing was directed not only at estrous females but also at non-estrous females. Pairs of both sexes in which chasing was observed, tended to have sexual interactions. Both hormonal and social factors should be considered in the regulation of chasing. The role of aggression in the formation of new male-female bonds in discussed.

Longitudinal studies on annual changes in plasma testosterone, body weight and spermatogenesis in adult Japanese mankeys (Macaca fuscata fuscata) under laboratory conditions

The present study was undertaken to clarify the annual changes in testicular function of Japanese monkeys under laboratory conditions. Five adult males were kept in an air-conditioned room with artificial 12/12 hr lighting. Measurements of body weight and blood sampling were conducted monthly for 13 months. The concentrations of plasma testosterone were determined by radio-immunoassay. The testicular size was measured and testicular tissues taken by biopsy were examined histologically at the four seasons. The body weight and plasma testosterone levels showed coincidental annual changes with a peak in September and a nadir in March or May. The percentage of seminiferous tubules including pachytene spermatocytes and the number of pachytene spermatocytes in tubular cross-sections were significantly increased in both the autumn and winter and decreased in the spring. Electron microscopically, the seasonal change was reflected in an increased size of fat granules in Sertoli cells in the breeding season.

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.

A comparative study on testicular microstructure and relative sperm production in gorillas, chimpanzees, and orangutans

We performed histological analyses for comparing testicular microstructure between the gorilla, chimpanzee, and orangutan. Testicular samples were obtained by autopsy or biopsy from 10 gorillas, 11 chimpanzees, and 7 orangutans from several zoos and institutes. The seminiferous epithelia were thick in the chimpanzee and orangutan but thin in the gorilla. Leydig cells in the interstitial tissue were abundant in the gorilla. The acrosomic system was extremely well developed in the orangutans. Our study reveals that the cycle of seminiferous epithelium in orangutan testis can be divided into ten stages, whereas that in human, chimpanzee, and gorilla testes can be divided into only six stages. Phylogenetic analyses of the number of divisions may indicate that the seminiferous epithelium of our common ancestor has changed since the orangutan diverged from it. Furthermore, we performed comparative analyses of testicular microstructure to estimate relative sperm production among these three animals, and proposed a new indicator (namely the spermatogenic index, SI) closely related to sperm production. The SI indicated that a chimpanzee usually produces about 223 times more sperm than a gorilla and about 14 times more than an orangutan. Our data demonstrate the significance of the SI for estimating sperm production, thus aiding our understanding of the reproductive strategy as well as testis weight and relative testis size in investigated primates. Am. J. Primatol. 73: 570‐577, 2011.

Observation on the cycle of the seminiferous epithelium in the Japanese macaque (Macaca fuscata) using semithin sections

The stages of the cycle of the seminiferous epithelium in the Japanese macaque are investigated using testes fixed by a mixture of formaldehyde and glutaraldehyde containing picric acid and embedded in a methacrylate resin, Quetol 523M. Sections, 1.0–2.0 µm in thickness, were cut with glass knives and stained with periodic acid-Schiff (PAS) and hematoxylin. Sections from such resin blocks illustrated cellular detail without structural distortion during the polymerization process. Furthermore, staining affinity with PAS and hematoxylin was excellent. In stained sections, typical germ cell associations were described, based on the nuclear morphology of type A (dark and pale) spermatogonium, type B spermatogonium, various developmental stages of primary spermatocytes during meiosis, and the development of the acrosomic system. In the Japanese macaque, two different steps of spermatids (steps 3 and 4) were constantly seen in the same area of the tubular epithelium during stage III. Therefore, a classification into ten stages is proposed for the cycle in this species. Additional characteristics are described based on the observation of the seminiferous epithelium using semithin sections.

Seasonal changes in the spermatogenic epithelium of adult Japanese macaques (Macaca fuscata fuscata)

A histological study was undertaken to clarify seasonal changes in the spermatogenic epithelium of Japanese macaques. Testicular tissue samples were excised by biopsies from five adult laboratory-maintained males in mating and non-mating seasons. The samples were fixed with Bouins solution, embedded in paraffin, and stained with PAS and hematoxylin. Microscopic observations on cross-sections of seminiferous tubules revealed that the seminiferous epithelium in the mating season was thicker than in the non-mating season. PAS-stained granules were found in some of the dark A-type spermatogonia, which significantly increased in the non-mating season. Spermatids of the steps preceding the appearance of the acrosomic cap in stages I to III were observed significantly more often than those in the step coinciding with the formation of the acrosomic cap in stage IV. In stage I, the ratio of mature spermatids or spermatozoa to immature spermatids in the mating season was higher than that in the non-mating season. These findings suggest that spermiogenesis, as well as spermatocytogenesis, is inhibited in the non-mating season.

Seasonal changes in spermatogenic cell degeneration in the seminiferous epithelium of adult Japanese macaques (Macaca fuscata fuscata)

The degenerating pattern of spermatogenic cells in the seminiferous tubule of Japanese macaques was studied to clarify a relationship between seasonal changes of reproductive performances and cytological findings in the Japanese macaque. For light microscopy, testis samples were obtained from five adult animals by biopsy in April (nonmating season) and October (mating season). For electron microscopy, specimens from four additional macaques were used. Degenerating cells were found in all steps of spermatogenesis. In stages I to V of the cycle of the seminiferous epithelium, morphologically atypical pachytene spermatocytes were observed in 14.7 and 10.0% of the cells in the nonmating and mating seasons, respectively, although the difference in percentage was not significant. Mature spermatids with atypical features in those stages occupied 59.6% of the cells in the nonmating season, which significantly decreased to 34.1% in the mating season. These results imply that the seasonal change of sperm production is related, at least in part, to the process of degeneration of the spermatogenic cells in this species.