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 Bouin's 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.     

Parasite changes and their influence on the body weight of Japanese monkeys (Macaca fuscata fuscata) of the Koshima troop

The incidence of eggs in individual feces (percentage of infected animals) and the EPG (eggs per gram of feces) of gastrointestinal nematodes for individually discriminated Japanese monkeys of the Koshima troop were investigated monthly from October 1974 to June 1979. Eggs of four nematode species,Oesophagostomum aculeatum, Trichuris trichiura, Streptopharagus pigmentatus andStrongyloides fülleborni, were frequently found; a few cestode segments ofBertiella spp. were occasionally found.S. fülleborni had a high incidence (100%) in young monkeys, suggesting that its incidence might vary with the monkeys' age. Seasonal changes in the incidence and EPG of each parasite were observed. The monkeys were treated with the anthelmintic thiabendazole once a month from May to July, 1975. Thiabendazole exerted an excellent effect onS. pigmentatus andS. fülleborni, and a lesser effect onO. aculeatum. Decreases in parasites caused by either seasonal changes and/or the anthelmintic treatment did not produce an increase in the monkeys' body weight, indicating that body weight is more affected by food intake or some factors other than parasitic infections. It is suggested that field anthelmintic treatment on wild monkeys should be conducted with the greatest care, since reinfection can occur immediately after such treatment.     

Age gradations in vocalization and body weight in Japanese monkeys (Macaca fuscata)

449 syllables in 174 food calls of Japanese monkeys of various ages were analyzed spectrographically. The fundamental frequency bands were divided into 55 frequency modulation patterns. The percentage of harsh syllables changed with age class among adults. Although the duration of syllables did not change with age, the maximum fundamental frequency and the minimum fundamental frequency showed age-related changes. Both were distinctly decreased by 6-8 years of age and thereafter the decline was far more gradual. Body weight also increased up to 6 years of age for females and 8 years for males, thereafter stabilizing for both sexes. The matching in age-related changes between fundamental frequency and body weight indicates that it is increase in size of the vocal folds with physical growth that lowers the fundamental frequency.     

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.     

Age changes in plasma IGF-1 concentration in free-ranging Japanese macaques (Macaca fuscata)

To obtain fundamental data on the endocrine background for the wild Japanese macaque (Macaca fuscata) growth profiles, we have measured plasma insulin-like growth factor 1 (IGF-1) concentrations of free-ranging and open-enclosed Japanese macaques from five different regions in their habitat. General features of the IGF-1 levels in those troops were: 1) an age-dependent increase in the young macaques and 2) distinctively higher values among several adult females. The age changes in IGF-1 levels during the adolescent period in the free-ranging Japanese macaques were similar to those in the caged Japanese macaques.     

Annual changes in hair length of the Japanese monkey (Macaca fuscata fuscata)

The hair length of Japanese monkeys was investigated for a period of one year and the molting phenomenon was clarified. Nine monkeys were employed in the study. The molting of the Japanese monkey was found to be of a seasonal type and occurred once during the year. The molting continued for one to four months in each monkey. The hair of the Japanese monkeys was wholly replaced during the period from April to August. The hair length was thus short in summer, and long in winter. Hair replacement in pregnant females began after parturition and was generally later than that in other individuals. During molting, both new and old hairs could be observed simultaneously in the same region of the body. The hair replacement ended around summer when the hair became the shortest. The new hairs continued to grow after molting and became the longest towards autumn or winter. Thus, the summer coat and the winter coat were essentially the same in the Japanese monkey. Such annual changes in the hair of the Japanese monkey were considered to be suitable for the climate of Japan.     

Ecological studies of reproduction in Japanese monkeys (Macaca fuscata)

Birth data of 25 troops of Japanese monkeys, which range over major areas in Japan between lat. 31°22 N. and 41°15 N., show significant differences in the timing of the birth season among different troops. The difference seems regional to some extent. Correlations between the timing of the birth season of the troop and various environmental factors—latitude, rainfall, temperature, social factors and so on, were examined, and it was suggested that the effect of environmental factors are complex and not always direct, and that the threshold value of each factor in causing the onset of the copulatory season might vary by troops. The difference in the timing of the birth season among different troops has not yet been sufficiently explained by a simple correlation with environmental conditions.While troops with large numbers of birth show annual uniform monthly distribution patterns of births, those with a smaller number of births show more fluctuations in the monthly distribution pattern of births from year to year. However, all the births in the latter come within a range of about four months, which is fixed for each troop.     

Plasma testosterone and male dominance in a Japanese macaque (Macaca fuscata) troop compared with repeated measures of testosterone in laboratory males

Plasma testosterone levels measured by radioimmunoassay did not correlate with dominance rank or aggressive behavior in 21 adult males of a natural troop of Japanese macaques (Macaca fuscata). The data were replicated during two consecutive breeding seasons. Levels of male dominance and aggressive behavior were highly correlated from year to year, but testosterone levels of individual males were not. Nor were individual levels of testosterone correlated in five laboratory males sampled every 15 min over a 2-hr period. These laboratory males showed multiple, apparently random peaks but the mean testosterone level of 11.73 ng/ml did not vary significantly throughout the 120 min that were studied. By demonstrating that the stress of blood collection did not depress plasma testosterone titers in laboratory males, these data validated the method used in the study of the natural troop.     

Mirror guided behavior in Japanese monkeys (Macaca fuscata fuscata)

Two male Japanese monkeys were trained to use a mirror to reach an object that could not be seen directly. Training to use a mirror in this way proceeded, step-by-step, from reaching a piece of apple to key-tracking. In Experiment 1 the monkeys were trained to use the mirror to locate a desired object, a piece of apple in a box facing the mirror, which could be seen only by looking into the mirror. The apple, once located, however, could be grasped without further reference to the mirror. This behavior is referred to as mirror mediated object discrimination. In subsequent experiments the monkeys could not reach the goal object except by observing it and his hand movement in the mirror. In Experiment 2 the target was a piece of apple visible in the mirror, in Experiment 3 an illuminated key and in Experiment 4 a series of keys which were illuminated sequentially. Mirror guided behavior such as shown in Experiment 2, 3, and 4 has not previously been demonstrated in monkeys.     

Disability, compensatory behavior, and innovation in free-ranging adult female Japanese macaques (Macaca fuscata)

Little is known about consequences of disability in nonhuman primates, yet individuals with disabilities can reveal much about behavioral flexibility, innovation, and the capabilities of a species. The Macaca fuscata population surrounding the Awajishima Monkey Center has experienced high rates of congenital limb malformation for at least 40 years, creating a unique opportunity to examine consequences of physical impairment in situ, in a relatively large sample of free-ranging adult monkeys. Here we present behavioral data on 11 disabled adult females and 12 nondisabled controls from 279 hours of randomly ordered 30-minute focal animal follows collected during May-August in 2005, 2006, and 2007. We quantified numerous statistically significant disability-related behavioral differences among females. Disabled females spent less time begging for peanuts from tourists, and employed a behavioral variant of such peanut begging; they had a lower frequency of hand use in grooming and compensated with increased direct use of the mouth or a two-arm pinch technique; and they had a higher frequency of self-scratching, and more use of feet in self-scratching. Self-scratching against substrates was almost exclusively a disability associated behavior. Two females used habitual bipedalism. These differences not withstanding, disabled females behaved similarly to controls in many respects: overall reliance on provisioned and wild foods, time spent feeding, and feeding efficiency did not differ among females, and there was no time difference in behavior performed arboreally or terrestrially. Disabled adult females were able to compensate behaviorally to perform social and life-sustaining activities, modifying existing behaviors to suit their individual physical situations and, occasionally, inventing new ways of doing things.     

Dermal melanocytosis in Japanese monkeys (Macaca fuscata)

The skin of Japanese monkeys (Macaca fuscata) shows diffuse discolorations resembling human dermal melanocytosis. Very few laboratory animals have melanocytes in the dermis. The purpose of this study was to clarify the dermatologic characteristics of Japanese monkeys in terms of gross appearance, skin color, and histopathologic findings. A colorimeter was used to record the skin colors of pigmented and nonpigmented sites. Tissue specimens obtained from both types of sites were examined histopathologically. All animals examined had pigmented sites on their bodies, and the discolorations extended over 25% to 33% of the body surface. The colorimeter could detect differences in skin color due to dermal melanocytosis. All parameters of the colorimetric systems used (Yxy, L*a*b*, and L*C*h* systems) demonstrated significant differences between pigmented and nonpigmented sites. In pigmented sites, the epidermis lacked melanocytes, but the dermis had numerous melanocytes with abundant melanin. Activated melanocytes with well-developed dendrites were distributed throughout the upper part of the dermal layer. Melanocytes were not arranged in clusters, and elastic and collagen fibers in the dermis showed no histological abnormalities. Nonpigmented sites lacked melanin granules in both the epidermis and dermis. This study revealed that gross dermal melanocytosis correlated well with colorimetric results and histopathologic findings. These findings suggest that the pigmentation of Japanese monkeys is equivalent to dermal melanocytosis in humans, to the end that Japanese monkeys may be a useful animal model for investigating dermal melanogenesis.     

Sweating in the Japanese macaque (Macaca fuscata)

The sweating rates on the palms and chests of three adult male Japanese macaques were measured by the CaCl₂ method at temperatures of 20–40°C. Rectal and skin temperatures on the palms and chests were also measured by means of copper-constantan thermocouples every minute. As ambient temperature was raised from 20°C to 40°C over a one-hour period, the sweating rates on the palms gradually increased and reached a certain plateau level in 30 to 40 minutes, but the sweating rates on the chests, on the other hand, were very low. A good correlation existed between the skin temperatures and the sweating rates on the palms as well as the skin temperatures and the sweating rates on the chests.     

Age-related differences in social grooming among adult female Japanese monkeys ( Macaca fuscata)

The present study investigated the influence of dominance rank in combination with kinship on age-related differences in social grooming among adult females in a free-ranging group of Japanese monkeys (Macaca fuscata). Eighty-three adult females were divided into six sub-groups according to age-class (younger: 5–9 years old; middle: 10–14 years old; older: 15–22 years old) and dominance rank (high and low rank). The ratio of the number of unrelated females that each female groomed to the total number of available unrelated females and grooming bouts which she gave to unrelated females decreased with increasing age for both high- and low-ranking females, whereas age did not appear to affect corresponding values for related females. On the other hand, compared with low-ranking females, high-ranking females of all age-classes received grooming more often from a larger number of unrelated females. Moreover, older females of low rank received grooming less often from a smaller number of unrelated females than younger females of low rank. These results indicate that with increasing age females are more likely to concentrate on related females when they have grooming interactions with other females. This tendency seems to be more apparent for low-ranking females. Moreover, the present findings also indicate that older high-ranking females could maintain their social attractiveness as high as younger high-ranking females.     

Fecal testosterone immunoreactivity as a non-invasive index of functional testosterone dynamics in male Japanese macaques (Macaca fuscata)

Validation of a simple method for the extraction and quantification of testosterone (T) from the excreta of male Japanese macaques (Macaca fuscata) is presented. Radioimmunoassay of paired fecal and serum samples collected from four intact sexually mature males during the breeding season provided profiles that were significantly correlated when samples were offset by approximately 48 hr. Additionally, no significant differences were observed in the pattern of temporal variation of T levels in serum and feces. Two castrated males were injected with radioinert T, and the patterns of excretion were observed by analysis of serial fecal and urine samples. Approximately 48 hr after the steroid was administered, a significant peak in the average fecal T levels was apparent. The injection event was also registered in the urine of both males, although qualitative differences were observed. These data suggest that measures of fecal T provide a reliable and non-invasive means of assessing gonadal function in this species. As the analysis of hormone levels in feces allows for frequent, stress-free sampling with minimal disruption, this method should be preferred in long-term orin situ applications requiring endocrine monitoring.     

Snowball construction by a feral troop of Japanese macaques (Macaca fuscata) living under seminatural conditions

Feral Japanese macaques (Macaca fuscata) living under seminatural conditions in Oregon constructed several large snowballs in their two-acre corral. This behavior did not involve the basic reward systems connected with agonistic or feeding behavior which are most commonly associated with tool-using in nonhuman primates.     

Self-wrist biting in Arashiyama-B troop of Japanese monkeys (Macaca fuscata fuscata)

Self-wrist biting in the Arashiyama-B troop of Japanese monkeys was observed during a nearly 4-year study. In all, six monkeys were seen performing this behavioural pattern. Medium ranking monkeys belonging to the age class 2–7 years performed this behavioural pattern most frequently. A slight tendency for the diffusion of this behaviour along kinship lines was also observed.