Demography and reproductive parameters of a free-ranging group of Japanese macaques (Macaca fuscata) at Katsuyama

Demographic and reproductive data were analyzed for a period of 28 years in the females of a free-ranging group of Japanese macaques at Katsuyama, Okayama Prefecture, Japan. The overall mean, age-specific fecundity rates were 5.43% for 4-year-olds and 41.86% for 5-year-olds, increasing to a peak of 66.67% for 13-year-olds. Fecundity remained relatively high (52.31–54.24%) in 16–19-year-olds, but decreased sharply (45.45–17.86%) in 20–23-year-olds, and became very low in 24–26-year-olds. Females aged 27 years or more did not produce infants. The average age at first birth was 5.41 years. Births peaked in mid-May. The timing of the first births each year remained essentially unchanged during the study period, whereas the timing of the median and last births shifted towards the later part of the season. The mean interbirth interval for all females was 1.56 years. The value was 1.54 years for multiparous females and 1.29 years for females following infant loss. These intervals were significantly shorter than those for primiparous females, and females with surviving infants. The overall mean infant mortality within the first year of life was 10.2%. The value was 8.6% for 10–14-year-olds, and 7.5% for 15–19-year-olds. The timing of birth differed among the four female matrilineal dominance rank-classes. The female fecundity rates increased as a function of matrilineal dominance rank. It is suggested that all demographic and reproductive data should be analyzed in detail with respect to the group's history.     

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.     

A preliminary study on hair length in the Japanese monkey (Macaca fuscata fuscata)

The hair length of Japanese monkeys was investigated. The hair of the Japanese monkey is long on the back and the lateral side of the upper arm and short on the back of the hand. There was variation in the length of hairs in the same region of the body. The distribution of hair length approximated to a normal curve and did not display any marked bias or skewness. The increase in length of hairs was remarkable from 0 to 1 year of age, and then continued at a constant rate. Sex differences in hair length were not so remarkable at any age.     

Characteristics of serial cross-sections of hairs of the Japanese monkey (Macaca fuscata fuscata)

The characteristics of serial cross-sections of hairs collected from an adult male Japanese monkey were investigated. Cross-sections were made of five to eight pieces per hair. The shapes of the cross-sections were elliptical or rounded on the whole. The fibre indices of the sections ranged from 83 to 100. In particular, those of proximal (basal) sections were close to 100. The hair diameter was 86.4 μ at maximum and 27.2 μ at minimum. A tendency was observed for the longer hairs to have thicker diameters. The changes in thickness along the fibre shaft were slightly different in relation to hair length. The thickest point was at around the middle of the fibre in the intermediate hair, somewhat towards the top of the central part in the long hair, and somewhat towards the base in the short hair. The hair of the Japanese monkey, however, was considered to be scanty in changes along the fibre shaft in comparison with many other animals. Medullae could scarcely be seen in the short hair and in the terminal and proximal sections of all hairs. Their shapes in cross-section were not uniform and rough at the margins. The fibre-medulla indices were generally less than 30 and smaller than those of many other mammals. Pigmentary granules were observed in all sections examined. The granules were black-grey in sections of the black-grey coloured part and yellow in the yellowish sections. They were dense in distal sections and scarce in sections close to the base. The cross-sectional appearance of the thickest part of the long hair was considered to be useful for hair identification, since it was good in pigmentation and medullation and relatively small fibre index.     

Development of co-feeding relationships in immature free-ranging Japanese monkeys (Macaca fuscata fuscata)

The co-feeding relationships of immature Japanese monkeys in the provisioned situation were studied. The most frequent co-feeders for immature females were diversified as compared to those for immature males. The number of immature females who showed strong co-feeding relationships with their mothers gradually decreased with age in both high- and middle/low-ranking matrilines, but the percent decrease was greater for middle/low-ranking immatures. Almost all immature females who displayed strong co-feeding relationships with adult males were from middle/low-ranking matrilines. Strong co-feeding relationships with mothers among immature males from high-ranking matrilines remained until 4 years of age. In contrast, strong co-feeding relationships with mothers among middle/low-ranking immature males decreased rapidly in the first year of life, and most 1- to 4-year-olds showed no strong co-feeding relationships with other group members. It is considered that middle/low-ranking mothers may not provide their immatures with a secure base for obtaining food in the provisioned situation.     

A case of diverticular disease of the colon in a Japanese monkey (Macaca fuscata)

Diverticular disease of the colon was detected in a female Japanese monkey by X-ray examination. The monkey was 15 years old and had been kept under captive conditions for nine years. Lack of appetite and activity, and constipation were observed. The monkey was given fiber-rich vegetables and wild plants, and its appetite and activity then improved. Based on a consideration of various factors, it is suggested that one possible cause of the diverticulosis in this case was a low dietary fiber intake.     

Successful artificial insemination for indoor breeding in the Japanese monkey (Macaca fuscata) and the cynomolgus monkey (Macaca fascicularis)

Methods of artificial insemination (AI) for indoor breeding in the Japanese monkey and the Cynomolgus monkey were investigated. For the Japanese monkey AI was carried out in six females during the winter mating season and in six females during the summer non-mating season. During the mating season, semen was inseminated near ovulation time in natural menstrual cycles. In the mating season study, three females inseminated at the uterine cavity became pregnant. Three inseminated at the cervical canal failed to become pregnant. For the non-mating season study, ovulation was induced artificially by PMSG and hCG and AI was carried out near the induced ovulation time. In the non-mating season, no animals became pregnant. Of four Cynomolgus monkeys used, pregnancy occurred in two animals inseminated near ovulation time in natural menstrual cycles. AI occurred at the uterine cavity in one and cervical canal in the other. In both species ovulation was verified by laparoscopy. Semen was collected by penile electro-stimulation then diluted to 2.5 to 5.0×10⁷/ml with Whitten's medium. Diluted semen of 0.2l was inseminated at the uterine cavity or cervical canal. Our results indicate the usefulness of vaginal AI as a method of artificial indoor breeding.     

Use of a mirror to direct their responses in Japanese monkeys (Macaca fuscata fuscata)

Two male Japanese monkeys used a mirror to inspect an object attached to their bodies but not directly visible. These monkeys had been trained previously to use a mirror to guide their hand to a target. In Experiment 1 their behavior in the presence of a mirror was observed. In Experiment 2 the monkeys used the mirror to locate a picture projected on a screen to the left or right rear side of the cage. In Experiment 3 the monkeys used a mirror to observe and finally grasp an object attached behind their heads. Two monkeys who were not trained to use a mirror to obtain an otherwise hidden object did not show such behavior.     

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.     

Copulatory behavior unaccompanied by ovulation in the Japanese monkey (Macaca fuscata)

Copulatory behavior unrelated to conception is sometimes observed in some non-human primates including the Japanese monkey. In the present study, the authors examined whether a mature follicle or a newly formed fresh corpus luteum was observed in the ovaries of female Japanese monkeys which displayed the copulatory behavior unrelated to conception. Post-conception copulatory behaviors were observed in three out of four females usually kept in individual cages in an air-conditioned room, and in two out of three females without infants kept in an outdoor group cage. However, neither a mature Graafian follicle nor a fresh corpus luteum formed newly after conception was observed in any of these females by laparoscopic examinations conducted immediately after termination of the copulatory behavior. In females with infants born in the preceding birth season, copulatory behaviors were observed in three out of four females kept in the outdoor group cage, and in two out of four females in a free-ranging troop. Ovulation was confirmed in one case out of the three kept in the outdoor group cage, but neither a mature follicle nor a newly formed corpus luteum was observed in the remaining four females. These findings suggest that copulatory behavior in the Japanese monkey is not always controlled by the development of a follicle or ovulation in the ovary.     

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.     

Differences in hair density of Japanese monkeys (Macaca fuscata fuscata) with locality and age

The hair density of free-ranging Japanese monkeys (Macaca fuscata fuscata) living in three different areas was investigated. The Japanese monkeys had thicker hair than other macaques. The hair density in the Japanese monkeys varied with locality: the northern monkeys had thicker hair than the southern ones. The density did not vary markedly with age up to 3 years of age, but then decreased gradually up to adult age (≧7 years old). The remarkable growth of the trunk suggested that the total number of hairs increased with age, especially during the period as a juvenile.     

Socioecological Context of Parturition in Wild Japanese Macaques (Macaca fuscata) on Yakushima Island

Female primates may adopt special feeding, foraging, and social strategies around the time of giving birth. We observed 8 females during the prepartum period, the day of birth, and the postpartum period in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. We collected data on their activity budgets, quantitative feeding and foraging behavior, and on female-male interactions. On the day of birth, females spent less time moving and feeding, and more time resting relative to other periods. Overall dietary diversity as well as arthropod foraging also decreased on the day of birth. Females fed mostly on mature leaves, new leaves and shoots during prepartum periods but mostly on fruit during postpartum periods. Decreased feeding on leaves and increased feeding on fruit probably changed as a result of seasonal availability, independently of parturition. Feeding on flowers, fungi and other items remained constant over all periparturitional periods. On the day of birth, new mothers had fewer social interactions with males and spent more time out of proximity with other adults than in other periods. Females rejected grooming presentations from males, groomed less with males, spent less time 3 m of males, and received less aggression from males on the day of birth. In the postpartum period, interactions with males returned to prepartum values. Grooming with females did not differ across the three periods. These results suggest that interactions with males may be costly for females on the day of birth.     

Digging and eating of underground plant-parts by wild Japanese monkeys (Macaca fuscata)

It has been reported that Japanese monkeys pull out and eat underground parts of plants, but they do so only a little and occasionally. The authors observed that wild Japanese monkeys in the mountains area near Hinohara Village ate underground plant-parts as one of the main components of their diet and they spent a lot of time digging for them. From information obtained from local old people, it appears that they have exhibited this behavior for many years as part of their feeding repertoire.     

Object manipulation in a captive troop of Japanese monkeys (Macaca fuscata): A developmental analysis

A captive troop of Japanese monkeys (Macaca fuscata) was presented with a nylon rope, a wooden cube, and an iron tube, and their subsequent manipulations were observed in detail. In total, 202 manipulation patterns were distinguished on the basis of three components: the actions performed, body-parts used, and relations to other objects. The developmental changes in these modes of manipulation were analyzed cross-sectionally, revealing four characteristics: (1) the most manipulative members of the troop were those aged 2–3 and 4–6 years old; (2) most of the manipulatory repertoire appeared by 4–6 years old; (3) actions such as Roll, Rub, and Slide and the use of bodyparts continued to increase in variety until 4–6 years old, while the variety of other actions showed plateaus after 2–3 years old or an earlier age; and (4) secondary manipulations appeared at 1 year old and continued to increase in variety even after 4–6 years old.     

Recognition of facial expressions in a Japanese monkey (Macaca fuscata) and humans (Homo sapiens)

Recognition of facial expressions by a Japanese monkey and two humans was studied. The monkey subject matched 20 photographs of monkey facial expressions and 20 photographs of human facial expressions. Humans sorted the same pictures. Matching accuracy by the monkey was about 80% correct for both human and monkey facial expressions. The confusion matrices of those facial expressions were analyzed by a multi-dimensional scaling procedure (MDSCAL). The resulting MDS plots suggested that the important cues in recognizing facial expressions of monkeys were “thrusting the mouth” and ‘raising the eyebrows.” Comparison of the MDS plots by the monkey subject with those by human subjects suggested that the monkey categorized the human “happiness” faces. This may suggest that the monkey has an ability to recognize human smile face even though it is learned. However, the monkey did not differentiate the human “anger/disgust” faces from the human “sad” faces, while human subjects clearly did. This may correlate with the lack of eyebrow movement in monkeys.     

Measurement of serum IgE antibodies against Japanese cedar pollen (Cryptomeria japonica) in Japanese monkeys (Macaca fuscata) with pollinosis.

IgE antibodies against allergens of Japanese cedar (Cryptomeria japonica, CJ) pollen in the serum of seven Japanese monkeys (Macaca fuscata) with pollinosis were measured by fluorometric indirect enzyme-linked immunosorbent assay (ELISA). All of the monkeys were found to have specific IgE to the crude pollen antigen. The specific IgE levels were well correlated with those determined by the Pharmacia CAP system. IgE antibodies were then assayed with two kinds of purified allergens (Cry j I and Cry j II) by the ELISA. We found that five monkeys had specific IgE to both allergens, although the other two had IgE only to Cry j I or Cry j II; there is different immune responsiveness to the two major allergens in the monkeys.     

Hepatic neuroendocrine carcinoma in a Japanese macaque (Macaca fuscata)

Primary neuroendocrine neoplasm of the liver is extremely rare in both humans and non‐human primates. The present report describes the clinical and pathological findings of an aged Japanese macaque (Macaca fuscata) with hepatic neuroendocrine carcinoma. To our knowledge, this is the first report of hepatic neuroendocrine neoplasm in macaques.     

Immobilization with a single dose of ketamine hydrochloride and a combination of xylazine hydrochloride-ketamine hydrochloride and antagonism by yohimbine hydrochloride in the Japanese monkey (Macaca fuscata)

Forty-nine free-ranging Japanese monkeys (Macaca fuscata) were immobilized with 4.3–15.6 mg/kg (mean±S.D.=10.0±2.5 mg/kg) of ketamine hydrochloride (HCl), and 27 Japanese monkeys kept in enclosures were immobilized with a combination of 0.8–1.4 mg/kg (1.0±0.2 mg/kg) of xylazine HCl and 4.0–7.1 mg/kg (5.0±0.6 mg/kg) of ketamine HCl. In the xylazine HCl-ketamine HCl combination, good myorelaxation was induced. The mean induction times for the single dosage of ketamine HCl and the xylazine HCl-ketamine HCl combination were 2.8±1.5 min and 6.9±4.4 min, respectively. The mean immobilization times with the single dosage of ketamine HCl and the xylazine HCl-ketamine HCl combination were 39.3±16.5 min and 58.8±34.2 min, respectively. A half dose of ketamine HCl in combination with xylazine HCl could also immobilize Japanese monkeys successfully. Administrations of 0.5 mg/kg i.v. and 1.0 mg/kg i.m. of yohimbine HCl as an antagonist to xylazine HCl at 30 min after the induction reduced the immobilization time to 31.4±0.5 min and 49.0±22.1 min, respectively. Yohimbine HCl appears to be an effective antagonist to combination anesthesia by xylazine HCl-ketamine HCl in the Japanese monkey.