Sexual maturation and seasonal changes in reproductive phenomena of male Japanese monkeys (Macaca fuscata) at Takasakiyama

The authors examined testis tissues and blood which were collected from free-ranging Japanese monkeys of the Takasakiyama troop during four periods in 1971 (mating season: late January-early February; early birth season: June; late birth season: August; and intermediate season between birth season and mating season: October), and studied their sexual maturation and seasonal changes in reproductive phenomena. Results of observations on the testis and plasma testosterone concentration were in agreement with each other. Except in a few cases, the testis was infantile until October at 4 years old and developed rapidly during the following two months, and spermatogenesis started in the mating season at 4 years old (in exceptional cases, it started one year earlier). After the following two-year process of sexual maturation, monkeys attained full maturation in the mating season at 6 years old. For seasonal changes in reproductive phenomena also, results of observations on the testis and the plasma testosterone were in agreement with each other. Activity of the testis repeated an annual cycle of being maximal in the mating season, regressing in the birth season, and redeveloping toward the following mating season. Such seasonal changes were noticeably observed with 4- to 6-year-old animals, which are in the process of sexual maturation.     

Serum dehydroepiandrosterone sulfate concentrations across the life span of laboratory-housed rhesus monkeys

Cross-sectional studies of humans have shown that dehydroepiandrosterone sulfate (DHEAS) peaks shortly after sexual maturation and declines thereafter, suggesting that the progressive reduction in DHEAS may play a role in the aging process and in the development of age-related morbidity. The present study examines changes in DHEAS concentrations across the life span of rhesus monkeys as part of the development of this primate model for studies of aging. Serum concentrations of DHEAS were measured in 792 laboratory-housed rhesus monkeys (Macaca mulatta) aged 0.5-36 years (527 females, 265 males). DHEAS concentrations in all monkeys were used to formulate an equation that describes two levels of decline of DHEAS with age. The most rapid decline occurs from infancy until approximately 5 years of age. The decline then occurs gradually with increasing age. There were no signs of an andrenarche just prior to sexual maturation, as is seen in humans or the great apes. This equation can be used to predict the expected mean serum DHEAS concentration and normal ranges of male or female rhesus monkeys at any age greater than 5 months.     

Normal hematologic values in the cynomolgus monkeys aged from 1 to 18 years

Normal hematological values including erythrocyte count (RBC), hematocrit value (Ht), hemoglobin concentration (Hb), total leucocyte count (WBC), and differential leucocyte count were determined with 206 healthy cynomolgus monkeys (Macaca fascicularis) aged in 1 to 18 years. These animals were born and reared at Tsukuba Primate Center for Medical Science, NIH, Japan. Additionally, 32 cynomolgus monkeys of wild origin estimated to be 5 or more years old were examined for their hematology. The presence or absence of sex- and age-related differences in the values was statistically analysed. As regards infant and juvenile monkeys, there were no significant differences in RBC, Ht and Hb between males and females. However, these values became significantly larger in males than in females after sexual maturation. Lymphocyte count was larger than neutrophil count until 3 to 4 years of age after birth, but this relation was inverted in adult monkeys aged more than 5 years. Segmentation of the nucleus was a prominent finding in neutrophils. Neither sex- nor age-related difference in the number of nuclear segmentation was noted.     

Intertroop relationships among Japanese monkeys

Intertroop relationships among Japanese monkeys, which have been paid only scant attention for the past 20 years, are examined from several points of view. Japanese monkey troops are generally distributed in such a way as to concentrate locally, that is, to form a local concentration of troops (LCT). About 20% of the nomadic ranges of the troops within LCT's overlap; but in their natural state, they seldom approach but rather to avoid one another. From observations of intertroop encounters at Takasakiyama, where three troops are provisionized and use the same feeding place, it has been found that there exists a dominant-subordinate relationship among troops, that monkeys of each troop have a clear consciousness of belonging to their troop, and that monkeys of different troops rate one another on the basis of their capability. The frequency of male transfer between troops within LCT's is by far higher than between LCT's. In Japanese monkey society, a troop only is a social unit and a social order higher than a troop is not seen; however, it is not impossible to consider an LCT a consanguineally connected group by reason of the transfer of males among the troops within it.     

Fetal and infant head circumference sexual dimorphism in primates

Studies have shown that after controlling for the effects of body size on brain size, the brains of adult humans, rhesus monkeys, and chimpanzees differ in relative size, where males have a greater volume of cerebral tissue than females. We assess whether head circumference sexual dimorphism is present during early development by evaluating sex differences in relative head circumference in living fetuses and infants within the first year of life. Head circumference is used as a proxy for brain size in the fetus and infant. Femur length is used as a proxy for body length in the fetus. Ultrasonography was used to obtain fetal measures, and anthropometry was used to obtain postnatal measures in humans, rhesus monkeys, baboons, and common marmosets. We show that statistically significant but low levels of head circumference sexual dimorphism are present in humans, rhesus monkeys, and baboons in early life. On average, males have head circumferences about 2% larger than females of comparable femur/body length in humans, rhesus monkeys, and baboons. No evidence for head circumference sexual dimorphism in the common marmoset was found. Dimorphism was present across all body size ranges. We suggest that head circumference sexual dimorphism emerges largely postnatally and increases throughout maturation, particularly in humans who reach adult dimorphism values greater than the monkeys. We suggest that brain dimorphism is not likely to impose an additional energetic burden to the gestating or lactating mother. Finally, some of the problems with ascribing functional significance to brain size sexual dimorphism are discussed, and the energetic implications for brain size sexual dimorphism in infancy are assessed.     

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, growth and feeding in the ballan wrasse Labrus bergylta Ascanius 1767

A study of the age, growth and feeding of the protogynous wrasse Labrus bergylta (Teleostei: Labridae) was made on 25 male and 316 female specimens taken from the southern coasts of the Isle of Man from October 1972 to October 1974. Age determination and back-calculations for length were made from the opercular bones. The oldest male and female specimens were 29 and 25 years old respectively. The growth curves showed only a slight increase in growth rate after sexual inversion, and a pattern of slow irregular increase, with no pronounced levelling off in old fish. The time of sexual inversion varied widely: intersexual specimens of 5 and 14 years were found. The youngest functional male was 6 years old. The weight/length relationships of males and females were very similar and the following equation, derived from all individuals, was used to calculate weights for age utilizing the back-calculated lengths:
The mouth, pharyngeal teeth and gut length to fish length ratio (0.622) suggested an omnivorous diet. Analysis of gut contents confirmed this, with decapod Crustacea, isopods and molluscs the dominant food items. There were seasonal changes in feeding intensity and composition of the diet, related to temperature changes, onshore-offshore migration patterns, availability of food items, and changes in habitat associated with maturation.     

Assessing the Occurrence of Sexual Segregation in Spider Monkeys (Ateles geoffroyi yucatanensis), Its Mechanisms and Function

Sexual segregation is a recognized dimension of the socioecology of many vertebrates, but it has not been systematically examined in primates. We investigated temporal patterns of sexual segregation in spider monkeys (Ateles geoffroyi yucatanensis) using a test that distinguishes sexual segregation from aggregation and random association between the sexes. We further investigated how sexual segregation varies over time as a function of food availability, and then tested other possible factors that might be causally linked to sexual segregation in spider monkeys. We predicted that male philopatry and cooperative territorial defence leads to sexual dimorphism in behavior, which in turn creates different optimal energetic requirements for males and females as reflected in differing activity budgets and diet. We investigated sexual segregation in a group of 33–35 spider monkeys at Runaway Creek Nature Reserve in Belize over 23 mo in 2008–2009. We used the sex compositions of subgroups recorded in scan samples to test the occurrence of sexual segregation at monthly and biweekly time scales.We found that males and females were significantly segregated in 15 out of the 23 mo of the study, and that periods of nonsegregation coincided with months of low food availability. The sexes differed significantly in activity and diet; males spent more time traveling, and less time resting and feeding than females, and they had a higher proportion of ripe fruits in their diets than did females. We propose that sexual segregation in spider monkeys is primarily a form of social segregation that results from males and females pursuing optimal dietary and behavioral strategies to satisfy sex-specific energetic demands. We further suggest that sexual segregation represents an important constraint on fission–fusion dynamics that should be considered when assessing the potential for variability in subgroup composition.     

Effect of restriction in daily feeding periods on reproduction in the female rat

Effects of restriction in daily feeding periods (2, 4, 8 and 12 hrs) imposed in 21 days old rats for 9 weeks were studied on the food intake, body growth, onset of puberty, reproductive cyclicity and ovarian functions. Control rats were feeding for 24 hrs ad lib. Though the restriction in feeding periods had no effect on the daily food intake but body growth was significantly reduced. Restricted feeding for 2, 4 and 8 hrs daily resulted in the delay in the onset of puberty, inhibition of oestrous cyclicity, reduction in ovarian weights, reduced growth, increased atresia of antral follicles and cessation of ovulation. The rats fed for 12 hrs daily, though weighed less but exhibited all the above mentioned reproductive functions similar to those of controls. The results have revealed that the restriction in feeding time induces nutritional deficiency, causing delay in sexual maturation and inhibition of ovarian functions.     

Intraspecies variation in dominance style of Macaca fuscata

Knowledge of intraspecific variation is important to test the evolutionary basis of covariation in primate social systems, yet few reports have focused on it, even in the best-studied species of the Macaca genus. We conducted a comparative study of the dominance styles among three provisioned, free-ranging groups of Japanese macaques at Shodoshima Island, Takasakiyama Mountain and Shiga Heights, and collected standard data on aggressive and affiliative behavior during a period of 5 years. Our data in the Takasakiyama and Shiga groups support previous studies showing that Japanese macaques typically have despotic social relations; nevertheless, our data in the Shodoshima group are inconsistent with the norm. The social traits of Shodoshima monkeys suggested that: (1) their dominance style is neither despotic nor tolerant but is intermediate between the two traits; (2) some measures of dominance style, e.g., frequency and duration of social interactions, covary as a set of tolerant traits in Shodoshima monkeys. This study suggests broad intraspecific variation of dominance style in Japanese macaques as can be seen in some other primate species.     

Sexual Maturation of Female Japanese Macaques Under Poor Nutritional Conditions and Food-Enhanced Perineal Swelling in the Koshima Troop

Provisioned food was severely restricted for 5 years, from 1972 until June 1977, in the insular Koshima troop of Japanese macaques. The monkeys experienced very poor nutritional conditions during this period. The feeding policy was changed in 1977 and food conditions improved, but only in summer. A remarkable consequence of intensive provisioning in summer was the occurrence of perineal swelling in many young females outside of the mating season. Females that matured during the period of poor food conditions showed an extraordinary delay in primiparity and exhibited conspicuous perineal swelling in the summer of 1977. Researchers studied the development of perineal swelling under standard conditions of constant provisioning from 1990 to 1995. First perineal swelling appeared at 5 years of age under standard conditions but appeared at 8 years of age under poor food conditions. The extraordinary delay in primiparity did not occur among females that were 6 years old when food conditions were improved in summer. We deduced that female Japanese macaques have a critical age of 5 to 6 years for sexual maturation. If the critical age is exceeded under poor food conditions, sexual maturation is hard to achieve even with improvements in food conditions. Seasonal changes in the incidence of perineal swelling were related to the period of high body weight. Rapid improvements in food conditions probably caused perineal swelling and activated sex hormones in female Koshima Japanese macaques.     

提高实验猴繁殖率的综合措施

实验猴繁殖率的高低直接影响实验猴养殖企业的经济效益。本文借鉴本中心多年实验猴繁育经验,总结了一套较为完备的提高实验猴繁殖率的措施,内容涵盖实验猴繁殖特性、种公猴选种、繁殖猴分群及梯度饲养、孕猴用药、母猴产后护理、仔猴补饲及断奶、繁殖猴饲料搭配等各方面。这些措施应用于实践后,实验猴繁殖率可保持在较高水平并逐年提高。我们认为这些措施可在其它实验猴养殖企业推广应用。     

The mating brain: early maturing sneaker males maintain investment into the brain also under fast body growth in Atlantic salmon (Salmo salar)

It has been suggested that mating behaviours require high levels of cognitive ability. However, since investment into mating and the brain both are costly features, their relationship is likely characterized by energetic trade-offs. Empirical data on the subject remains equivocal. We investigated if early sexual maturation was associated with brain development in Atlantic salmon (Salmo salar), in which males can either stay in the river and sexually mature at a small size (sneaker males) or migrate to the sea and delay sexual maturation until they have grown much larger (anadromous males). Specifically, we tested how sexual maturation may induce plastic changes in brain development by rearing juveniles on either natural or ad libitum feeding levels. After their first season we compared brain size and brain region volumes across both types of male mating tactics and females. Body growth increased greatly across both male mating tactics and females during ad libitum feeding as compared to natural feeding levels. However, despite similar relative increases in body size, early maturing sneaker males maintained larger relative brain size during ad libitum feeding levels as compared to anadromous males and females. We also detected several differences in the relative size of separate brain regions across feeding treatments, sexes and mating strategies. For instance, the relative size of the cognitive centre of the brain, the telencephalon, was largest in sneaker males. Our data support that a large relative brain size is maintained in individuals that start reproduction early also during fast body growth. We propose that the cognitive demands during complex mating behaviours maintain a high level of investment into brain development in reproducing individuals.     

Determination of growth and maturation in the common frog, Rana temporaria, by skeletochronology

Growth and maturation in a Swiss population of Rana temporaria were studied in 1983 and 1984 by means of skeletochronology. Resting line (growth ring) diameters were used to back-calculate individual body sizes in previous years; these permitted establishment of an average growth curve and determination of individual ages and sizes at first reproduction. Growth was rapid up to maturation, but continued thereafter at a decreased rate. Males were larger than females at age two but females grew faster thereafter, causing sexual dimorphism in adult body sizes. Body size distributions for both years and for frogs recaptured and first captured in 1984 were established. Growth in immatures was positively, but in adults negatively correlated with body size, with considerable variation at all sizes. Individual adult sizes were positively correlated with body sizes at the end of the first year. Average individual age at first reproduction was 2.8 years in males and 3.1 years in females (range in both sexes two to four years). There is no evidence for a two-year-cycle of reproduction.     

Sexual maturation among members of a transported troop of Japanese macaques (Macaca fuscata)

Data on the sexual maturation of a transported natural troop of Japanese macaques were collected during the 1973–74 and 1974–75 breeding seasons. Analysis of the data revealed that the sexual maturation of many monkeys was delayed one to two years. It is suggested that the delay of sexual maturation is related to a failure of the pubescent-aged monkeys to attain appropriate weight levels after transportation. This study was partially supported by a University of Oregon, Department of Anthropology PHS Biomedical Science Grant 50-262-1112.     

Ontogeny of sexual dimorphism in the Long-tailed Manakin Chiroxiphia linearis: long maturation of display trait morphology

Males of dimorphic species often show ornaments that are thought to have evolved through female choice or/and male–male competition. The sexual differentiation of similar morphologies occurs during ontogeny, resulting in differential sex and age-specific selection. The Long-tailed Manakin is a dimorphic species with a highly skewed mating system, the males of which delay plumage maturation over 3 to 4 years. We describe ontogenetic changes in feather morphology in this species through sexual maturity. Males showed a significant increase in length of the central rectrices with age, hence their degree of sexual dimorphism increased from zero in 1-year-old males to 189.5% in adults. In contrast, male tail length decreased with age. Wing length did not vary significantly with age, but females had relatively longer wings than males. Wing loading was greater in females and decreased with age in males. In adults, rectrix length was positively correlated with testis volume, supporting the hypothesis that secondary sexual characters can signal the condition of primary sexual characters. Rectrix length showed positive allometry with body size in males less than 4 years old, whereas older males showed negative allometry and females showed isometry. Wing area and wing loading shifted from negative to positive allometry in males of 2 to 3 years of age. Changes in male morphology during ontogeny in the Long-tailed Manakin appeared to be associated with their specific display behaviours. Age-related changes in allometric growth of rectrices in the Long-tailed Manakin suggested that young males invest disproportionately more in the length of this trait relative to their body size. This investment could act as a signal of competitive ability to move status position in their orderly queue.     

布氏田鼠标志种群的繁殖参数

采用标志重捕和染色观测法跟踪了内蒙古典型草原区布氏田鼠野外种群,按绝对时间年龄研究其种群繁殖参数。结果3表明：4－5月份出生的雄鼠能在当年达到性成熟,性成熟发育历期约为1．5个月,6月后出生的雄鼠当年达不到性成熟。在达到性成熟的当年雄鼠中,多数个体再度转入性休止期,其平均繁殖结束时间要林越冬雄鼠早1个月,而越冬雄鼠则在整个繁殖期保持性活动状态。雌鼠性成熟发育历期约为1个月,首次产仔时间约为2月龄。雌鼠在一年中的产仔窝数与其年龄有关;越冬鼠能产3－4窝,4月份出生的雌鼠能产2－3窝,5月份出生的雌鼠当年能产1－2窝,6月份出生的雌鼠能产0－1窝,7月份之后出生雌鼠当年不参加繁殖,在自然条件下,布氏田鼠一年中最多能产4窝。     

Night observations of free-ranging Rhesus monkeys

The nocturnal distribution and behavior of individually marked Macaca mulatta were studied at the La Parguera, Puerto Rico, colony of the Caribbean Primate Research Center. The new image intensifier was used successfully to identify 399 monkeys in 185 sleeping clusters. Monkeys moved into mangrove trees close to favorite feeding areas usually 35 minutes after sunset. The group condensed to less than one-half the daytime spread, vocalizations increased and grooming ceased. Movements and vocalizations ceased several hours after sunset, although bursts of activity occurred throughout the night. Activity resumed 40 minutes before sunrise. Activity was higher during full moon, when I observed feeding, play and sexual behavior. Fights at night were twice as frequent during the breeding season. Monkeys slept in clusters of one to four, 58% of which were of two. Sixty-three percent were composed of maternal relatives, 33% were mother-infant pairs. Mature males clustered with non-related males, slept alone or with females (in the breeding season). Yearlings slept with their mothers or with older siblings. Distribution of monkeys in a group at night reflects daytime associations.     

Gustatory adaptation affects sexual maturation in male German cockroaches,Blattella germanica

Adaptations to hazardous environmental factors are essential for survival, although they may be maladaptive in conditions where the hazard is absent. In German cockroach (Blattella germanica L.) populations, glucose aversion has evolved rapidly in response to glucose‐containing insecticidal baits, but little is known about the consequences of this behaviour in the absence of bait. In the present study, glucose‐averse (GA) and wild‐type (WT) male German cockroaches are restricted to a range of nutritionally defined diets containing either glucose or fructose as the sole carbohydrate source, and time to first expression of courtship is measured by stimulating the male antennae daily with isolated antennae from receptive, 6‐day‐old females. Glucose‐averse males that are restricted to glucose‐containing diets mature their courtship responses significantly later than GA males restricted to fructose‐containing diets, whereas there is no difference in maturation of courtship responses between GA males restricted to fructose‐containing diets and WT males restricted to diets containing either sugar type. Glucose‐averse males furthermore respond later to GA female antennae than to WT female antennae, all from 6‐day‐old females. This suggests that GA females are less sexually stimulating, and the results are also consistent with earlier findings showing that GA females contain less developed oocytes than WT females at this age. These findings demonstrate that an adaptive gustatory mutation conferring protection from a toxin may have comparatively detrimental effects under conditions where the toxin has vanished, both by delaying female sexual maturation and signalling and by delaying male sexual maturation and courtship under conditions where glucose is a major energy source.     

Development from birth to sexual maturity in a semi-free-ranging colony of mandrills (Mandrillus sphinx) in Gabon.

This report presents information collected over 7 years (1983-1990) in Gabon, on a breeding group of 14, increasing to 45, mandrills maintained in a rainforest enclosure. Under these conditions, a seasonal cycle of mating (June-October) and birth (January-May) occurred. Females began to exhibit sexual skin swellings at age 2.75-4.5 years (3.6 +/- 0.6 years, mean +/- SD; n = 10) and first delivered offspring when 3.25-5.5 years old (4.4 +/- 0.8 years; n = 9). Gestation periods ranged from 152 to 176 days (167 +/- 9 days; n = 6 accurately dated pregnancies) and interbirth intervals from 11 to 15 months (12.4 +/- 1.3 months; n = 15). Females could reproduce 2 years before attaining adult body weight (10-15 kg) and complete dental eruption by 5.0-5.5 years. Males, by contrast, developed more slowly, reaching adult body weight (30-35 kg) and testicular volume (volume of left testis: 25-30 ml) at 8 years. Consistently high circulating testosterone concentrations (8.17 +/- 2.0 ng ml-1) could be measured by 9 years of age. Fully developed males exhibited fatting of the rump and flanks, as well as striking sexual skin coloration and an active sternal cutaneous gland; little expression of these features was evident during pubertal development. Marked individual age differences occurred with regard to the onset and complete development of these features, suggesting possible interactions between social environment and physical maturation.