Characteristic pattern of monoaminergic nerve fibers in the pineal organ of the monkey,Macaca fuscata

Summary Monoaminergic nerve fibers were studied in the pineal organ of the monkey, Macaca fuscata, by use of fluorescence and immunohistochemical procedures. Abundant formations of noradrenergic nerve fibers were observed in the pineal organ. They entered the parenchyma in the form of several coarse bundles via the capsule in the distal portion of the organ and spread throughout the organ after branching into smaller units. The density of the autonomic innervation decreased gradually toward the proximal portion of the organ. In the distal portion, numerous nerve fibers formed perivascular plexuses around the blood vessels and some fibers ran as bundles unrelated to the blood vessels in the stroma. Fine varicose fibers and bundles derived from these plexuses penetrated among the pinealocytes. However, only a few intraparenchymal fluorescent fibers were detected in the proximal third of the gland. With the use of serotonin antiserum serotonin-immunoreactive nerve fibers were clearly restricted to the ventroproximal part of the pineal organ. Although the somata of the pinealocytes showed intense immunoreactivity, their processes were not stained. In one exceptional case, clusters of pinealocytes displaying very intense immunoreactivity were found in an area extending from the distal margin of the ventral portion of the pineal stalk to the proximal portion of the pineal organ proper; these cells were bipolar or multipolar and endowed with well-stained processes.     

A cytogenetic study on congenital limb malformations in the Japanese monkey (Macaca fuscata)

A cytogenetic investigation was performed on 88 Japanese monkeys (Macaca fuscata) with abnormal limbs from 11 free-ranging provisioned troops including nine individuals with abnormalities indistinguishable as to whether they were congenital or injurious. All of the monkeys with abnormal limbs including the nine questionable individuals had the same karyotypes as those of normal individuals. The chromosome number was 42, consisting of 20 bi-arm autosome pairs and a submetacentric X-chromosome and Y-chromosome. The ninth chromosome pair, which was the only chromosome pair with remarkable secondary constriction, displayed length polymorphism of the centromeric C-band and secondary constriction in both deformed and normal monkeys. These kinds of variants have also been commonly found in other monkey species, which have almost the same karyotype as the Japanese monkey and have not been reported to show frequent occurrence of limb malformation. We concluded therefore that chromosomal abnormalities could be excluded from the main causal factors for limb malformations of the Japanese monkey.     

Behavior of Japanese monkey (Macaca fuscata) mothers and neonates at parturition

Parturitional behavior in 12 caged Macaca fuscatawas analyzed. Wild-caught mothers showed adequate maternal behaviors immediately following the neonate’s expulsion. Parity differences existed in the behaviors; primiparae were more idiosyncratic than were multiparae. Among multiparae, those with two or more offspring were uniformly adequate, but those with a single birth experience varied in the adequacy of the maternal care they provided at parturition. Mothers embraced and licked their neonates and had ventroventral contact with them frequently immediately after parturition but decreased these behaviors after expulsion of the placenta. In contrast, mothers showed allogrooming after consuming the placenta. Placentophagy was correlated with the level of orality represented by maternal licking behaviors. An isolation-reared primipara reacted to her newborn in a basically negative manner, although she showed little actual aggression. She showed a rapid shift in her negative behavior during the immediate postpartum period. This mother’s newborn sought contact with her, indicating the neonate’s active role in establishing a stable mother-neonate bond.     

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.     

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.     

Discrimination of mother by infant among Japanese Macaques (Macaca fuscata)

Experiments on five mother-infant pairs of Japanese monkeys (Macaca fuscata)living together in a captive group were conducted during the first 12 weeks after birth in order to assess the time at which infants begin to discriminate their own mothers from other adult females. After removal from their social group, infants exposed to their mothers and three unfamiliar adult females at a distance of 150 cm failed to orient visually toward their mothers. However, when the infants were allowed to approach the four females, they responded preferentially to their mothers during the third month of life. We concluded that by 8–12 weeks of age, infant Japanese macaques are able to discriminate between their mothers and other adult females.     

CRF-immunoreactive nerve fibers in the circumventricular organs of the monkey,Macaca fuscata

Summary The occurrence of CRF (corticotropin-releasing factor)-immunoreactive nerve fibers in the circumventricular organs of adult male monkeys, Macaca fuscata, was studied on serially sectioned brains, by means of the peroxidase-antiperoxidase technique in combination with a highly specific and sensitive CRF antiserum. CRF-containing nerve fibers were found in high concentrations in the infundibulum and, in addition, in small numbers in the posterior lobe, organum vasculosum laminae terminalis, subfornical organ, and area postrema; they were missing in the pineal body and the subcommissural organ. The CRF immunoreactive nerve fibers distributed in these organs were located in the proximity of the blood vessels.Supported by a grant (No. 56440022) from the Ministry of Education, Science, and Culture, Japan     

Pattern of synaptic connections in the pineal organ of the ayu,Plecoglossus altivelis (Teleostei)

Summary Synaptic connections were studied by means of electron microscopy in the sensory pineal organ of the ayu, Plecoglossus altivelis, a highly photosensitive teleost species. Three types of specific contacts were observed in the pineal end-vesicle: 1) symmetrically organized gap junctions between the basal processes of adjacent photoreceptor cells; 2) sensory synapses endowed with synaptic ribbons, formed by basal processes of photoreceptor cells and dendrites of pineal neurons; 3) conventional synapses between pineal neurons, containing both clear and dense-core vesicles at the presynaptic site. Based on these findings, the following interpretations are given: (i) The gap junctions may be involved in an enhancement of electric communication and signal encoding between pineal photoreceptor cells. (ii) The sensory synapses transmit photic signals from the photoreceptor cells to pineal nerve cells. (iii) The conventional synapses are assumed to be involved in a lateral interaction and/or summation of information in the sensory pineal organ. A concept of synaptic relationships among the sensory and neuronal elements in the pineal organ of the ayu is presented.Fellow of the Alexander von Humboldt Foundation, Federal Republic of Germany     

Immunohistochemical demonstration of serotonin-containing nerve fibers in the hypothalamus of the monkey,Macaca fuscata

Summary The distributional pattern of serotonin-containing nerve fibers in the hypothalamus of the monkey (Macaca fuscata) was analyzed with the use of the peroxidaseantiperoxidase method in conjunction with a highly sensitive and specific anti-serotonin serum. The highest concentrations of serotonin-immunoreactive varicose fibers were found in the nucleus praeopticus medialis, nucleus ventromedialis hypothalami, and the complex of mammillary nuclei (nucleus praemamillaris, supramamillaris, mamillaris medialis et lateralis). However, the nucleus suprachiasmaticus, where numerous serotoninergic fibers have been reported to occur in the rat, appeared to be almost devoid of these fibers. The infundibular stalk, and the intermediate and posterior lobes of the pituitary contained considerable numbers of immunoreactive fibers. The present study provides a morphological basis for possible clarification of the influence of serotoninergic projections on various neuroendocrine mechanisms in primates. Furthermore, an attempt was made to clarify the differences and similarities concerning the distributional patterns of serotoninergic nerve fibers within the monkey hypothalamus in contrast to the rat hypothalamus.Supported by grants (No. 56440022, 57214028) from the Ministry of Education, Science and Culture, Japan     

A further food-washing tradition in Japanese macaques (Macaca fuscata)

A case of food-washing tradition is reported in a captive group of Japanese macaques. Two techniques are employed, with one or both hands being used to wash food under water flowing from watering spouts. Processes of diffusion of the behaviour in the group follow the patterns previously described by Japanese scientists observing this species. It is suggested that development of such a behaviour could be related to particular environmental conditions.     

Hierarchy,kinship and social interaction among Japanese monkeys (Macaca fuscata)

The study reports the relationship between hierarchy, genetic relatedness and social interaction in captive Japanese macaques. Grooming and proximity were found to be positively related to both dominance rank and degrees of relatedness. Ranks also positively correlated with threats while no relationship was observed between genetic relationships and agonistic interactions. The removal of a-male tightened the male hierarchy while the female hierarchy became relatively loose. Affiliative behaviour became more correlated with ranks than degrees of genetic relatedness. In the absence of α-male, the next dominant male avoided involvement in either agonistic or afliliative interactions with reintroduced animals and group females.     

Suppressed copulatory behavior and ovarian function in lactating Japanese monkeys (Macaca fuscata fuscata) during the mating season

The influence of lactation on copulatory behaviors and ovarian functions was studied in Japanese monkeys (Macaca fuscata fuscata) during the mating season. Three lactating females were housed in an outdoor group cage with their infants, and three nonlactating females were housed in an adjacent outdoor cage. They were mated by introduction of one of four rotationally chosen males into the females' cage, for two hours three times a week; the occurrence of ejaculatory copulations was recorded. Blood samples were collected on each observation day, and plasma levels of estradiol, progesterone, and luteinizing hormone (LH) were measured by specific radioimmunoassays. In nonlactating females, plasma estradiol increased during the transition into the mating season, and rose to levels over 90 pg/ml for the first time on about 50 days before the first ovulation. Shortly after plasma estradiol exceeded 90 pg/ml in the nonlactating females, the onset of ejaculatory copulations occurred. They received ejaculations continuously up to the early ovarian luteal phase. On the other hand, in lactating females, there were lower levels of plasma estradiol (below 90 pg/ml) during the transition into the mating season, and they received no ejaculation during that period. Two of the three lactating females ovulated only once, and they received ejaculations only during the periovulatory period, coinciding with the rise of their plasma estradiol levels over 90 pg/ml. The remaining lactating female remained anovulatory and received no ejaculation throughout the entire mating season. These results have demonstrated that the low sexual activity of lactating females is clearly correlated with low levels of plasma estradiol due to suppressed ovarian function.     

Sexual strategies of female Japanese macaques (Macaca fuscata)

Evidence is reviewed that female Japanese macaques have multiple male mating partners when they are available and show a preference for mating with sexually unfamiliar males. Several lines of evidence suggest that this aspect of female sexual behavior results in the offspring of an individual female being sired by more than one male thereby maintaining the genetic diversity of the troop. Evidence is presented in this paper that a decrease in the number of adult troop males and a lack of extra-troop migrant males in the Arashiyama West troop of Japanese macaques following transplantation to a ranch in south Texas had consequences for the sexual behavior of the females.     

Measuring male-female relationships during the mating season in wild Japanese macaques (Macaca fuscata yakui)

Heterosexual relationships during one mating season were examined in a wild troop of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Validation tests of putative mate choice behaviors demonstrated that female initiation and maintenance of proximity, female lookback at the male, and sexual presents to the male, were associated with increased mating. Male grooming the female was also associated with increased mating. Ten dyadic social behaviors were subject to principal components analysis to empirically define behavioral dimensions of male-female relationships. The analysis yielded four relationship dimensions: ‘Mutual Choice and Male Coercion,’ ‘Female Choice’ (two types), and ‘Mutual Choice’ Dyads tended to be characterized by more than one dimension. The results suggested that females sought matings with multiple males of various dominance ranks. Female relationships with high ranking males contained elements of male coercion and mate guarding, however, because these males attempted to inhibit females from mating with lower ranking males. The correlation between each relationship dimension and mating success depended, in part, on the dominance rank of males. Relationships involving high ranking males, which were most likely to contain elements of male coercion and mate guarding, were associated with mating success. Relationships involving low ranking males, which usually lacked such coercive elements. were less strongly correlated with mating success. These results, obtained from a wild troop, are compared to those previously obtained in captive and provisioned groups of Japanese macaques.     

Decision making in grooming by Japanese macaques (Macaca fuscata)

I analyzed the temporal organization of individual Japanese macaques’ (Macaca fuscata) grooming sequences in 14 mothers and 13 offspring of different age/sex classes and 4 nonkin females. I hypothesized that preceding grooming affects subsequent grooming by the same individual. Grooming bouts were likely to be terminated as the bouts became longer when females groomed nonrelatives. Moreover, the duration of first bouts was longer than that of following bouts. These effects were also seen in grooming of mothers by their offspring > 1 year old and that of adult and adolescent female offspring by their mothers. In contrast, neither the duration of first bouts nor the number of preceding bouts had much effect on the occurrence or duration of subsequent bouts in any subject.     

Hb Izu (Macaca)β83 (EF 7) Gly→Cys: The major hemoglobin of the Japanese monkey (Macaca fuscata) in a troop at Shimokita,the northernmost limit of its habitat

A hemoglobin variant was discovered in Japanese monkeys (Macaca fuscata) of the Wakinosawa A-1 troop of the Shimokita peninsula, the northernmost limit of this species' habitat. The variant was characterized by slow migration on starch gel electrophoresis due to its polymerizing nature. Structural analysis revealed that Gly at the 83rd amino acid residue of theβ chain was substituted by Cys, and the variant was identified as Hb Izu (Macaca). The gene frequency of the variant was extremely high, at 85.7%, and much higher than the 21.3% obtained for the troops of the Izu peninsula. The genotypic frequencies in the troops of both the Izu and Shimokita peninsulas agreed with expectations as calculated from the Hardy-Weinberg equilibrium.     

Environmental temperature and reproductive seasonality in Japanese macaques (Macaca fuscata)

This study demonstrates that the reproductive seasonality ofMacaca fuscata seems to be more affected by environmental temperature than by photoperiod. Mean conception dates for 25 groups of Japanese macaques species did not correlate with latitude. Instead, they were positively related to mean fall and winter temperatures and negatively related to the magnitude of the decrease in the mean temperature from summer to fall. Evidence from transplanted groups supports the hypothesis that environmental temperature is a decisive factor in determining the timing of mating activities of Japanese macaques. These results are also consistent with the concept that, in temperate zones, environmental temperature is probably the best indicator of local climatic characteristics.     

Comparison between the diameter of hair cross-sections and the thickness of the enclosed hairs in Japanese monkeys (Macaca fuscata fuscata)

The thickness of hairs from Japanese monkeys was measured by enclosing the hairs on slide glasses with balsam. Nine monkeys were used for the study. Forty to 69 hairs from the back were examined per head. High correlations between the thickness of the enclosed hairs and the diameter of cross-sections were obtained in all monkeys. In the Japanese monkey, therefore, it is considered possible to utilize enclosed hairs for measuring the thickness without preparing cross-sections. Moreover, the medullae of which the air layers are strongly related to thermoregulation, were readily observed in the enclosed hairs.     

How social relationships influence a monkey's choice of feeding sites in the troop of Japanese macaques (Macaca fuscata fuscata) on Koshima islet

When the individual Japanese macaques of the Koshima troop feed on natural food, they usually feed alone. In situations where animals usually feed without other animals, there is a possibility that subordinate animals may avoid feeding sites at which dominant animals are feeding. This paper examines whether social relationships such as kinship or dominance exert any influence on an animal's choice of feeding sites, by analyzing episodes in which an animal approached and climbed into a tree where other animals were. As a result, it was found that social relationships did not influence whether an animal climbed into a tree where other animals were feeding, and that no particular age-sex pair co-fed. Agonistic interactions frequently occurred when the inter-individual distance was less than 1 m. From these findings, the feeding sites were divided into two spaces: (1) a tolerance feeding space, and (2) an intolerance feeding space. It is presumed that animals can feed without entering others' intolerance feeding spaces when food is abundant, as it was in the present study period. Thus social relationships do not influence an animal's choice of feeding sites in such a situation.     

Lactation in the Japanese monkey (Macaca fuscata): Yield and composition of milk and nipple preference of young

Changes in the yield and chemical composition of milk, together with those in the nipple preferences and suckling behavior of infants, were followed in three lactating Japanese monkeys rearing single infants under laboratory conditions at monthly intervals for six months after their paturition. Milk accumulating in the mammary glands during a 4-hr separation of the infant was collected by milking under anesthesia with the aid of a physiological dose of oxytocin. The stage of full lactation appeared to last for about two or three months after parturition. The milk at this stage contained 14.0% of total solids, 4.2% of lipids, 1.6% of proteins, and 6.2% of lactose, and the concentrations of Na, Cl, and K in the milk water were 7.4, 15.1, and 5.9 mM, respectively. From the 9th or 13th week of lactation onwards, according to the individual, the milk composition changed appreciably and the time during which the young left hold of the mother's nipple also increased. The weaning of young in the Japanese monkey appears to begin during the 3rd or 4th month of age. The milk production then wanes and almost ceases by the end of the 6th month. The nipple preference of the young was generally established completely by the 3rd, or the 8th at latest, week of age. However, no difference in either the yield or composition of the milk secreted was found between the mammary glands of the preferred and non-preferred sides. Without regard to the apparent nipple preference, infants seem to ingest milk from the mother's breasts of both sides. Accurate estimation of the rate of milk production could not be achieved, but the rate was expected to be 150–200 g/day at the height of lactation based on the relation between the mother's body weight and the milk production rates of other primate species. A disparity was noted between the observed and estimated values for the milk yield, and a diurnal fluctuation in the milk secretion of the Japanese monkey was inferred. This study was conducted through the official system of the Primate Research Institute, Kyoto University, for cooperative research work with other institutions.