Retardation of bone development in the Koshima troop of Japanese macaques

Retardation of bone development was observed in the Koshima troop of free ranging Japanese macaques. In the control group, epiphyseal unions of appendicular long bones generally started to close at about 4 yrs of age and were completed at about 8 or 9 yrs of age. Limb bone unions of the Koshima troop, however, started to close at about 9 yrs of age and completely closed at about 15 yrs of age. In the epiphyseal unions of trunk and girdle bones, the Koshima troop again showed a retardation of closure compared with the control group. Until long bones reached their full length, that is, until about 15 yrs of age, their size was small in the Koshima troop compared with the control group, though the sample size of the Koshima troop was small. After 15 yrs of age, however, many osteometrical measurements of the Koshima troop were nearly the same as controls. A prolonged growing duration compensated for the slow growth and allowed them to become as large as controls. This prolongation may be an adaptation in response to small size during the developmental period. In some parts of the body, however, Koshima macaques failed to reach the adult size of controls. Males were less likely than females to reach full size. Causes of the retardation and small size in the Koshima troop are discussed, but they remain open to further studies.     

Vertebral age changes in Japanese macaques

This study deals with maturation and aging of the vertebrae in Japanese macaques (Macaca fuscata fuscata) of known chronological age. The samples used were 103 skeletons of captive raised Japanese macaques varying in age from 6-23 years. Epiphyseal union between the vertebral body and the epiphyseal disk (epiphyseal ring, annular epiphysis) and degenerative changes of the vertebrae were macroscopically examined. It was revealed that vertebral epiphyseal union develops comparatively rapidly in the sacral and cervical vertebrae, moderately in the lumbar vertebrae, and slowly in the thoracic vertebrae. It was found that, as a central tendency, the vertebral epiphyseal union begins at about 6 years of age, progresses lineally in proportion to age, and completes at about 23 years of age. However, considerable variation in developmental states of union was observed among individuals of the same age. Concerning vertebral degenerative changes, few were observed among the present samples. Compared with the other primates with regard to the timing of vertebral maturation, shortening of duration of maturation was found among humans. Human vertebrae may have become an early-maturing organ in order to sustain the increased loading that is accompanied by the adoption of habitual erect posture and bipedal locomotion.     

Somatometrical features of Japanese monkeys in the Koshima islet: In viewpoint of somatometry,growth, and sexual maturation

The Japanese monkeys inhabiting Koshima islet were investigated morphologically, and compared with those living in other areas of Japan. The morphological features of the Koshima monkeys are thought to reflect many interrelated factors. Their body size is the smallest inMacaca fuscata fuscata. The lower latitude and the warmer winter of the islet represent the major factors in this small body size. Another physical characteristic is their longer limbs, which may be related to the same environmental factors. The adult males of the Koshima troop show the widest variation, while the variation in the adult females is the narrowest, among the troops ofMacaca fuscata examined. This may be explained either by sexually differentiated growth, that is, males continue to grow considerably after 8 years of age, whereas females do not; or by isolation, that is, males sometimes immigrate into or emigrate from the islet, whereas almost of all the females remain there. It was found that the influence of food limitations on body weight depends on sex and age; babies and juveniles, and adult males did not lose their body weight, but monkeys aged from 3 to 7 years and adult females had lost much weight compared to those of the same ages and sexes measured in 1963 (feeding was not limited). This fact may support the idea of “sex-age-class selection” proposed byMori (1979), but the weight loss pattern could be explained by changes of body composition with growth. The growth of the anterior trunk length, too, was restrained. Sexual maturation in males was delayed by at least one year.     

Reproduction of wild Japanese macaque females of Yakushima and Kinkazan Islands: A preliminary report

Wild Japanese macaque females of the Yakushima and Kinkazan populations exhibited similar reproductive features. (1) Births/female/year (BR: 0.27–0.35) was lower than those of provisioned troops, but (2) infant mortality (IM: 0.23–0.25) was higher than those of provisioned troops. (3) The interbirth interval (IBI) following the death of infants was 1.5–1.6 years, shorter than that following surviving infants (2.2–2.4 yrs). (4) Birth sex ratio (BSR) did not differ from 1∶1. There was no consistent correlation between (5) female age and IM, (6) maternal rank and offspring BSR, or (7) maternal rank and reproductive success. On the other hand, (8) BR of Yakushima females was significantly lower than that of Kinkazan females. In particular, (9) Yakushima females stopped reproduction earlier than Kinkazan females, although (10) the first birth of Yakushima females was about one year earlier than Kinkazan females. (11) BR exhibited a humped curve against female age in Yakushima, but it was uncertain whether old-aged females of Kinkazan exhibited a post-reproductive life span (PRLS). (12) The survivorship for female juveniles was lower than that for male juveniles in Yakushima, whereas the survivorship for male juveniles was lower than that for female juveniles in Kinkazan. These data may indicate that Yakushima females more severely compete for resources than Kinkazan females, because of high population density, whereas the population density of Kinkazan might be limited by climate (e.g. heavy snow) rather than density dependent ecological effects.     

Epiphyseal union and dental eruption in Macaca mulatta

Age of dental eruption and epiphyseal fusion is estimated for the permanent dentition and long bone epiphyses of rhesus macaques (Macaca mulatta), with 299 skeletons of individuals with known age of death, from the Cayo Santiago skeletal collection. Epiphyses at a given joint tend to fuse at the same time. While males and females tend to have the same pattern of epiphyseal fusion, females' epiphyses fuse earlier than those of males, espeically at the elbow and knee joints. The order of epiphyseal fusion in rhesus macaques follows the general primate pattern. Times of dental eruption for males and females are generally the same, except for the relatively late eruption of the canine in the males. The order of eruption follows a common primate pattern (dm2?M1?I1?I2?M2?(P3,P4)?C?M3). Multiple regressions were calculated in order to allow determination of developmental state, or predictions of chronological age, from epiphyseal fusion and/or dental eruption scores in juvenile rhesus macaques. Standard deviations of residuals from these regressions indicate considerable variation in developmental state among aminals of the same chronological age. The lack of correlation between residuals from the separate skeletal and dental regressions, indicates that skeletal and dental development are largely independent.     

Inter-male associations in a wild Japanese macaque troop on Yakushima Island,Japan

Adult male association and its annual change were studied in a wild population of Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Unlike many other Japanese macaque troops, adult troop males frequently maintained proximity and exchanged grooming with one another in both the mating and non-mating seasons, and the dominance relationship rarely appeared in such inter-male associations. The few cases of agonistic interactions occurred mostly when estrous females or food resources were immediately concerned. Although troop males were very intolerant to newly appeared solitary males (new males) during the mating season, close associations were formed between troop males and new males as soon as the mating season terminated. The consort of new males and lower-ranking troop males with estrous females was frequently disturbed, but these males could copulate no less frequently than higher-ranking males. A comparison among macaque species suggests the existence of two forms of inter-male association: (1) the frequent association based on the symmetrical exchange of social behaviors; and (2) the infrequent and asymmetrical association related to the dominance relationship. The form of inter-male association seems to be influenced by whether or not males can keep close associations with females throughout the year.     

Life history variables of wild troops of formosan macaques (Macaca cyclopis) in Kenting,Taiwan

A study on population dynamics of wild Formosan macaques (Macaca cyclopis) in Kenting, southern Taiwan, was conducted from March 1985 to August 1990. At first, only one monkey troop was studied. It fissioned in 1987 and both of the daughter troops have been observed since then. Total number of animals increased from 10 to 29 over the years, but the sizes of individual troops have never been more than 20. Seasonality in breeding has been detected: copulations were concentrated in the period from November to January and 75% of all the 28 births occurred between April and June. Time of birth by parous females without offspring from the preceding year was earlier than that of lactating females. Young females gave their first births at 4 or 5 years of age. Total birth rate over the study period was 0.8 infant per female per year. Hunting was the main cause of death while natural mortality rate was low for the animals. There was only one adult male in each troop for most of the time. Troop males in the two daughter troops have been replaced two or three times in the three years by some solitary males that moved around in the area. The reproductive parameters of Formosan macaques in Kenting were found to be more similar to that of rhesus monkeys than to Japanese macaques. And a case of higher reproductive success in a high-ranking matriline was reported.     

Growth of wild and laboratory born chimpanzees

The skeletal remains of a wild juvenile chimpanzee,Pan troglodytes verus, of known chronological age are measured and found to be smaller than laboratory born and fed juveniles of the same age. Other wild born immature skeletal materials of all the three subspecies ofPan troglodytes, including both known and estimated chronological ages, are also smaller than laboratory born chimpanzees when comparisons are made on corresponding age groups. Differences between wild and laboratory born chimpanzees are larger in the limb bones than in the cranium. Limb bones of laboratory individuals grow earlier than those of wild ones regardless of subspecies. Small limb bone size of wild chimpanzees is discussed in terms of life processes.     

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.     

Age estimation from stages of union of the vertebral epiphyses of the ribs

This study attempts to fill a persistent gap in the literature by documenting the timing of epiphyseal union at the vertebral end of the ribs in a sample of modern Portuguese skeletons. The skeletal remains of 53 females and 45 males, between the ages of 11 and 30, were taken from the Lisbon documented skeletal collection. Individuals in the sample have been previously described as being representative of a middle‐to‐low socioeconomic segment of the early 20th century Lisbon population. Three anatomical locations were examined for epiphyseal union: the head, the articular tubercle and the nonarticular tubercle. The first epiphysis to show partial union is that of the nonarticular tubercle (females, 11–19 years; males, 11–19 years), followed by the epiphysis of the articular tubercle (females, 11–20 years; males, 16–20 years), and finally by the head epiphysis (females, 15–24 years; males, 16–22 years), which can still show incomplete epiphyseal closure at 25 and 24 years for females and males, respectively. A trend for earlier female maturation was observed, but the statistical tests only confirmed this result for some ribs and age groups. No directional asymmetry was found, but a significant fluctuating asymmetry was observed in all three epiphyses. A preliminary analysis showed that the asymmetric group of individuals in the study sample includes all the rural‐to‐urban migrants, relative to the symmetric group. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Influence of artificial food supply on population parameters and dispersal in the Hakone T troop of Japanese macaques

A free-ranging troop of Japanese monkeys was observed for seven years from April 1971 to March 1978 in the Hakone area, Kanagawa Prefecture, Japan. This troop was fed artificially between 1956 and 1977. The artificial food supply was reduced by about half after 1974. The troop-size fluctuated around 100 between 1971 and 1974, but fell drastically from 91 in 1975 to 58 in 1978. Population parameters were compared between the two periods of 1971–1974 and 1975–1977. Clear differences between the two periods were found in primiparous age, ratio of non-natal resident males to all resident males, ratio of newcomers to non-natal resident males, age-specific disappearance rate, and proportion of deserters observed in the study area. A correlation existed between the number of males and females of 5 or more years of age in the troop. The numbers in the three age-sex groups (natal males, non-natal males, and females of 5 or more years of age in the troop) were closely connected with one another. The scarcity of food supply may have caused not only males but also females to disperse. The drastic decrease in troop-size after 1974 could be based on the disappearance of adult females. The cause of the dispersal of young males and adult females could have been mutual competition among the troop members for food, and that in adult males could have been competition for females.     

Age structure and body size of the Chuanxi Tree Frog Hyla annectans chuanxiensis from two different elevations in Sichuan (China)

Age, body size, and growth patterns in the subtropical anuran Hyla annectans chuanxiensis from high (Dengchigou Protection Station) and low (Lingguan Town) elevations in Baoxing County of Sichuan province (China) were described using skeletochronology. Females were significantly older than males at the low-elevation site, but there was no significant difference between the sexes at the high-elevation site. Age at sexual maturity of both males and females was 2 years at the high-elevation site, whereas males matured at 1 year and females at 2 years at the low-elevation site. Males and females from the low-elevation population reached a maximum age of 3 and 4 years, respectively, whereas males and females from the high-elevation population reached a maximum age of 4 and 5 years, respectively. At both sites, females were significantly larger than males. Females and males from the high-elevation population were larger than individuals from the low-elevation population. When the effect of age was controlled, the differences in body size of the two populations were significant only for females. Von Bertalanffy growth curves indicated that the growth rates in males was greater than in females in both populations. They also showed that the growth of both sexes slowed at an earlier age in the low-elevation population than in the high-elevation population. The findings suggest that age is a major factor underlying body size patterns for both sexes, but that the elevation of the locality affects the body size of females.     

Reproductive biology of rhesus and Japanese macaques

This paper offers a comparison of the reproductive biology of the Japanese macaques of Arashiyama, Japan and the free-ranging rhesus macaques of Silver Springs, Florida, U.S.A. The data indicate that rhesus macaques of Silver Springs have a higher reproductive rate than the Japanese macaques of Arashiyama. The reproducive rate of the rhesus monkeys over three birth seasons is 82% and that for the Japanese macaque is 53%. The higher reproductive rate of rhesus monkeys is accomplished through an earlier onset of sexual maturation (4 and 5 years for the rhesus and 5 and 6 years for the Japanese monkeys) and a shorter interbirth interval (14.27±5.54 months for rhesus and 18.00±6.57 months for Japanese monkeys). It is suggested that, because of the relatively harsh winters experienced by Japanese macaques, the slower reproductive rate of the Japanese monkeys has been selected for in order to enable females to lengthen the time in which maternal care is extended to their offspring.     

The growth pattern of chimpanzees: Somatic growth and reproductive maturation inPan troglodytes

Growth of chimpanzees reared at the Kumamoto Primates Park of Sanwa Kagaku Kenkyusho Co. Ltd. was studied cross-sectionally from the viewpoints of somatic growth and reproductive maturation. Distance and velocity curves were expressed using spline function method. Males showed adolescent growth acceleration in body weight, with a peak at 7.86 yrs of age, but not in trunk length. Females showed continuous rapid growth from mid-juvenile to adolescent phase in both body weight and trunk length, but no isolated adolescent spurt. The Sanwa chimpanzees matured at about 12.5 yrs of age for females and 15.0 yrs for males. The mean adult weights and trunk lengths were 53.2 kg and 507.8 mm for males and 42.7 kg and 481.6 mm for females. The Sanwa chimpanzees had similar growth patterns to those of the Yerkes chimpanzees, although they showed a slight delay in infancy, and a higher growth rate from the early juvenile phase onwards. Growth patterns in these two laboratories may be regarded as “normative” for laboratory-reared chimpanzees. They matured earlier than wild chimpanzees by more than two years. The major reason for the retarded maturation in wild chimpanzees is the delay of growth from infant to the early juvenile phases (0–4 yrs of age), probably owing to a limited nutritional supply from the mother. Development of the testes comprised three phases: slow growth from infant to juvenile (until 6.4 yrs); rapid growth around adolescence (until 9.2 yrs); and adult (mean testicular volume, 187 cm³). Setting the nutritional standard at 2,000–2,600 Cal/day (= Kcal/day) per adult, calories were considered for captive chimpanzees in each age class.     

Epiphyseal union at the innominate and lower limb in a modern Portuguese skeletal sample, and age estimation in adolescent and young adult male and female skeletons

This study documents the timing of epiphyseal union at the innominate, femur, tibia, and fibula in a sample of modern Portuguese skeletons. The sample was taken from the Lisbon documented skeletal collection and it is comprised of 57 females and 49 males between the ages of 9 and 25. Individuals are mostly representative of the middle-to-low socioeconomic segment of the early 20th century Lisbon population. A total of 18 anatomical locations were examined for epiphyseal union using a three-stage scheme: 1) no union; 2) partial union; and 3) completed union, all traces of fusion having disappeared. Results show that females are ahead of males by 1-2 years and provide similar age ranges for the stages of union than previous studies. Some variations between studies can be explained by methodological differences between dry bone and radiographic observations. However, a review of the literature indicates that socioeconomic status of a given population seems to be of decisive importance to the rate of ossification and most of the differences in skeletal maturation across studies and populations can probably be ascribed to different levels of social and economic development of the societies in which the individuals lived. Although the effects of socioeconomic status in skeletal maturation are greater during childhood than in adolescence, as to make the timing of epiphyseal union a reliable estimate of age at death, they are not negligible and age estimates should take into account the likely socioeconomic status of the individual, whose remains are under examination.     

Behavior, Diet, and Movements of the Sulawesi Crested Black Macaque (Macaca nigra)

We present the first field study of activity budgets, diet and ranging patterns of the Sulawesi crested black macaque, Macaca nigra, one of seven macaque species endemic to Sulawesi, Indonesia. We studied three crested macaque groups, ranging in size from 50 to 97 individuals, for 18 months in the Tangkoko-DuaSudara Nature Reserve, North Sulawesi. They spent 59% of the day moving and procuring food, especially fruits, and 41% of the day resting and socializing. Their diet is composed of more than 145 species of fruit (66% of observed feeding bouts), vegetative material (2.5%), invertebrates (31.5%), and occasional vertebrate prey. Group differences were more pronounced than seasonal or diurnal differences. Specifically, the largest group moved farther during the day, moved at a faster and more uniform rate, ate less fruit, rested more, and socialized less than the smaller groups did. The largest group had the largest home range, but it included less primary forest and more disturbed habitat than the ranges of smaller groups. There are individual differences in activity budgets of adult males and females in time spent moving, resting, feeding, and socializing that may reflect differences in reproductive strategies of males versus females. The behavior of large juveniles is more similar to that of adults than to that of small juveniles. Daily movements and use of home range are correlated with diet. Macaques moved shorter distances as the proportion of time spent feeding on fruit increased, and the top four dietary items accounted for most of the variance in entry into hectare blocks of home range.     

Age-related and individual differences of reproductive success in male and female barbary macaques (Macaca sylvanus)

Age-related and individual differences in longterm reproductive success were analyzed in two social groups of free-ranging Barbary macaques. Maternity data were obtained from continuous birth records and paternity was determined with oligonucleotide-fingerprinting. The fathers of 246 of 286 investigated individuals could be identified. They were born during a 14-year period and represented 73 and 34% of all known offspring from the females of the study groups B/F and C, respectively. Only these infants were considered when comparing male reproductive success with that of females. The necessary adjustment of the female data resulted in small deviations from the true values in one group, but substantially increased individual differences in female fertility in the second group. Subadult males, 4.5 – 6.5 yrs old, had a much lower reproductive success than adult males (7.5 – 25 yrs old) and same-aged females. Reproductive success of adult males was not significantly affected by age, while females invariably ceased reproduction during the first half of the third decade of life. Males were more likely than females to leave no offspring, unless they survived 9 – 10 yrs of age. The number of years with breeding opportunities was important for male reproductive success but less significant than that for females. Reproductive success of several males during the 14-year study period was similar to or even exceeded that possible for a female in her whole lifetime. Variance of male reproductive success significantly exceeded that of females in both study groups.     

Differential effects of kinship,dominance, and the mating season on female allogrooming in a captive group ofMacaca fuscata

An analysis of allogrooming (total times spent grooming individual partners) of 8 sexually mature females (3–12 years of age) in a captive group of 17 Japanese macaques, shows that during the nonmating season, grooming distributions were characterized by high proportions of grooming given to family members and/or higher ranking nonkin. During the mating season, all eight females showed significant shifts in their grooming distributions, and four females showed significant shifts in grooming between their nonestrous and estrous periods (defined behaviorally). Fox six of eight females, mating season grooming was characterized by either high proportions of grooming given to family members and/or heterosexual and homosexual partners. It was found that within dyadic sexual relationships, dominants gave more grooming to subordinates than the former received, in contrast to a reversal of this pattern in the majority of these same dyads during the nonmating season. This is interpreted as one short-term function of grooming: a dominant asymmetrically grooms a subordinate sexual partner to maintain proximity with (or reduce tension in) the latter. The two remaining focal females (middle ranking, nulliparous) differed from the other females in that they shifted their mating season grooming to subordinate nonkin, despite the lack of evidence that this was a result of sexual interactions, patterns of partner availability, competition, patterns of grooming reciprocity, or agonistic alliance support. From these results, it is suggested that in some contexts, grooming of subordinate nonkin may function to reduce tension in thegroomer. In the Japanese macaque, this latter possibility and the asymmetric grooming of subordinate homosexual partners may prove to be exceptions to the general rule that female cercopithecine grooming of nonkin flows up the dominance hierarchy.     

Changes of dominance rank,age, and tenure of wild Japanese macaque males in the Kinkazan a troop during seven years

Male age-rank and tenure-rank relationships were studied for seven years in unprovisioned Japanese macaque (Macaca fuscata fuscata) troop on Kinkazan Island, Japan. Males whose estimated ages were between 15 and 19 yr old monopolized the highest ranks, while older males whose estimated ages were ≥ 20 yr old tended to decline in rank, resulting in a humped age-rank curve. The ranks of males tended to rise as their tenure in the troop increased. The departure of higher-ranking males was the social mechanism for changes in rank, suggesting that the disappearance of higher-ranking males plays an important role in determining rank dominance.     

Non-metric skeletal age changes in the Darajani baboon

Dental attrition, cranial suture closure, and epiphyseal union are compared as indicators of relative age in baboons, Papio cynocephalus (Linnaeus, 1776). Tooth destruction from wear is extreme. Such destruction is certainly a factor of vital importance to feral baboons and may limit life span. As cusps wear away, they form selenes of dentine and enamel which are effective grinding surfaces. In conditions of extreme wear, functional fourth molars may be quite beneficial. Vault sutures of females remain active longer than those of males. In contrast, most other cranial sutures and sites of epiphyseal activity mature earlier in the female than in males. Attrition scores in this sample are as useful as assessments of closure or epiphyseal union to determine the relative position of an individual in an age sequence. The most reliable estimates rely on all three sources.