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.     

Hormone profiles and reproductive characteristics in wild female Japanese macaques (Macaca fuscata)

In this study we investigated the reproductive characteristics of wild female Japanese macaques (Macaca fuscata fuscata) in 2 nonconsecutive years using noninvasive methods to monitor physiological events. We detected ovulation dates and ascertained conceptions from fecal hormone profiles. First ovulations occurred from middle October to early November in 1997, and from middle to late November in 1999. Most females conceived during their first ovarian cycle. On average, postconception bleeding occurred 18.4 days after ovulation, and menstruation occurred 13.7 days after ovulation. The average gestation length was 176.3 days. The average degree of facial redness and the percentage of females that copulated synchronously changed across the ovarian cycle and peaked in the periovulatory period. Although prolonged periods of postconception copulation have been reported in previous studies, they did not occur in this study, which suggests that such behavior may not be a species-typical characteristic. Female fertility varied between the 2 years. The copulation rates of females with no infant <1 year of age were 100% (14/14) in 1997 and 45.5% (5/11) in 1999. The ovulation rates of the female subjects that we chose for hormonal assays were 100% (9/9) in 1997 and 50.0% (3/6) in 1999. Th conception rates of these selected females were 100% (9/9) in 1997 and 16.7% (1/6) in 1999. The birth rates (the number of females that delivered divided by the total number of adult females in the troop) were 73.3% (11/15) in 1998 and 6.7% (1/15) in 2000. The modified birth rates (the number of females that delivered /the number of adult females with no infant <1 year of age) x 100 were 78.6% (11/14) in 1998 and 9.1% (1/11) in 2000.     

Reproductive seasonality in wild northern pig-tailed macaques (Macaca leonina)

Primates - Macaque reproductive patterns range from strictly seasonal breeding to non-seasonal breeding, but factors explaining this variation are not fully understood. Valid reproductive...     

Lifetime reproductive success in female Japanese macaques

Lifetime reproductive success, measured by the number of offspring surviving to age five, varied from 0 to 10 in a group of 33 provisioned female Japanese macaques. Of the three contributors to reproductive success, the number of reproductive years, fecundity per year and survivorship of offspring to reproductive age, the first accounted for two-thirds of the variation. Fecundity per year and survivorship were negatively correlated, indicating reproductive costs of reducing interbirth interval. No other demographic measure used, nor the behavioral measure 'dominance rank', significantly correlated with lifetime reproductive success or its components. Age-specific changes in fecundity and infant survival were not found for this sample, neither could cessation of reproduction, even in very old females, be demonstrated.     

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.     

Seasonal variation and sex differences in the nutritional status in two local populations of wild Japanese macaques

Seasonal variations and sex differences in the nutritional status in two local populations of wild Japanese macaques (Macaca fuscata fuscata) were examined. It was hypothesized that the ecological condition and/or reproductive strategies of each sex determine the nutritional condition and its seasonal fluctuation in each sex. Morphometric measures such as body mass, thoracic and femoris circumferences, skinfold thickness in four places (triceps, biceps femoris, subscapular, and abdomen), and wet mass of mesenteric and omental fat were used for comparisons between sexes, seasons, and populations. Animals of the Shimane population were larger than those of the Boso population in most morphometric measures, abdominal skinfold, and mesenteric and omental fat mass, suggesting environmental and/or genetic differences in the two populations. Females of both populations had larger skinfolds and mesenteric and omental fat mass than males, indicating that females had more fat than males. Females showed seasonality in most measures, having two peaks of body mass, thoracic and femoris circumferences, abdominal skinfold, and mesenteric and omental fat masses in early spring and late fall. In contrast, males exhibited no clear seasonal variations for most measurements, except for biceps femoris and subscapular skinfolds, which showed peaks in summer. Most morphometric measurements significantly correlated to each other, particularly in females, but most skinfolds had no correlation with other measurements. These findings suggest that sexual dimorphism in body composition and its fluctuation may be affected by the different reproductive strategies of males and females.     

Frog- and lizard-eating behaviour of wild Japanese macaques in Yakushima,Japan

Frog- and lizard-eating and related behaviours were observed on eight occasions in two troops of wild Japanese macaques (Macaca fuscata yakui) in Yakushima, between March 1984 and April 1989. In each case, the first animal seen handling the prey was an adult. Juveniles showed interest in the prey, sniffed or mouthed it in three cases, and ate discarded parts of it in another. In the three cases where capture was observed, detection of the prey appeared to be fortuitous. Four monkeys ate leaves after eating meat. Those leaves identified were of species not commonly eaten. Though invertebrate-eating is common and widespread among Japanese macaques, the consumption of vertebrates is rare. The possibility that these behaviours represent a local tradition among the Yakushima macaques is discussed.     

Troop extinction and fusion in wild Japanese macaques of Yakushima Island,Japan

A wild Japanese macaque troop decreased in size because the birth rate dropped and infant mortality increased. In the 1989 mating season, the last male left the troop, and the remaining two females joined a neighboring troop. Thus, the troop ceased to exist as an independent troop. A lower limit to troop size may exist, below which a troop cannot effectively defend its range, forcing the females to join a larger troop. © 1994 Wiley-Liss, Inc.     

Reciprocation and interchange in wild Japanese macaques: grooming, cofeeding, and agonistic support

Social primates spend a significant proportion of their time exchanging grooming with their group companions. Although grooming is mainly exchanged in kind, given its hygienic and tension-reducing functions, it is still debated whether grooming also provides some social benefits, such as preferential access to resources (e.g., food or mating partners). In this study we analyzed grooming distribution among wild female Japanese macaques living in two groups on Yakushima. We tested the tendency of monkeys to reciprocate the amount of grooming received, and to direct their grooming up the hierarchy. Then we analyzed the relation of grooming to three of its possible benefits: reduced aggression, increased tolerance over food, and agonistic support against a male aggressor. The data were analyzed by means of row-wise matrix correlations. Grooming was highly reciprocated (i.e., exchanged in kind) and directed up the hierarchy in both the study groups. No significant relationship was found between grooming and aggression. Conversely, grooming favored tolerance over food, since it was positively correlated with presence on the same food patch, close proximity, and close approaches (both within 1 m) during feeding. Grooming was also positively related to agonistic support against adult males, although this relationship became nonsignificant when we controlled for kinship. Although these results are not definitive, they suggest that monkeys may derive various social benefits from grooming. This conclusion is supported by the fact that in various primate species animals tend to prefer high-ranking individuals as grooming partners.     

Otter scent signals age, sex, and reproductive status

Scent is used across taxa to communicate information about signaler identity. Eurasian otters Lutra lutra are mainly solitary and thought to use scent as their primary means of communication. Little is known, however, about what information otters communicate through scent or what social function this performs. Headspace solid-phase microextraction and gas chromatography-mass spectrometry were used to sample and analyze volatile organic compounds from anal scent gland secretion from 158 otters of differing sex, age, and female reproductive status. Univariate and multivariate differences were clear between adult and juvenile otters. Complex sex differences were apparent in adult otters but not in younger individuals, suggesting the use of this scent secretion in mate attraction. The scent of pregnant and lactating females was highly differentiated from male and juvenile scent, but anecdotal reports suggest females avoid communication during these times.     

Changes in ovarian morphology and hormone concentrations associated with reproductive seasonality in wild large Japanese field mice (Apodemus speciosus)

Wild large Japanese field mice (Apodemus speciosus) responses to cyclic seasonal changes are associated with physiological and behavioral changes. However, the detailed regulation of oogenesis in the ovary during the seasonal reproductive cycle in wild large Japanese field mice has not been studied. We assessed the dynamics and changes in ovarian morphology and hormone concentrations associated with reproductive seasonality throughout the year. The stages of the ovarian morphological breeding cycle of wild large Japanese field mice were classified as breeding, transition, and non-breeding periods during the annual reproductive cycle. Measurement of blood estradiol concentrations throughout the year showed that the levels in September and October were higher than those in other months. It is presumed that follicle development starts from a blood estradiol concentration of 38.4 ± 27.1 pg/mL, which marks a shift from the transitional season to the breeding season, followed by the transition to the non-breeding season at 26.1 ± 11.6 pg/mL. These results suggest that seasonal follicle development in wild rodents is correlated with estradiol regulation. We consider this species to be an alternative animal model for studying seasonal reproductive changes and the effects of environmental changes.     

Candidate genes underlying heritable differences in reproductive seasonality between wild and domestic rabbits

Reproductive seasonality is a trait that often differs between domestic animals and their wild ancestors, with domestic animals showing prolonged or even continuous breeding seasons. However, the genetic basis underlying this trait is still poorly understood for most species, and because environmental factors and resource availability are known to play an important role in determining breeding seasons, it is also not clear in most cases to what extent this phenotypic shift is determined by the more lenient captive conditions or by genetic factors. Here, using animals resulting from an initial cross between wild and domestic rabbits followed by two consecutive backcrosses (BC1 and BC2) to wild rabbits, we evaluated the yearly distribution of births for the different generations. Similar to domestic rabbits, F1 animals could be bred all year round but BC1 and BC2 animals showed a progressive and significant reduction in the span of the breeding season, providing experimental evidence that reduced seasonal breeding in domestic rabbits has a clear genetic component and is not a simple by‐product of rearing conditions. We then took advantage of a recently published genome‐wide scan of selection in the domesticated lineage and searched for candidate genes potentially associated with this phenotypic shift. Candidate genes located within regions targeted by selection include well‐known examples of genes controlling clock functions (CRY1 and NR3C1) and reproduction (PRLR).     

Testing for links between face color and age,dominance status,parity, weight,and intestinal nematode infection in a sample of female Japanese macaques

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.     

Nursing behaviour of bighorn sheep: correlates of ewe age,parasitism, lamb age,birthdate and sex

The nursing behaviour of marked bighorn ewes, Ovis canadensis, and their lambs was observed in Alberta, Canada, for 2 years. Suckle duration decreased as lambs grew older. Nursing behaviour in midlactation was correlated with maternal condition; young ewes, ewes with high faecal counts of lungworm (Protostrongylus spp.) larvae, and ewes whose lambs were born late allowed shorter suckles and were less likely to nuzzle their lamb's rump during a suckle. Sons did not appear to receive more milk than daughters. Suckle duration in mid-lactation was correlated with survival for female lambs but not for males. Lambs born late were disadvantaged, probably because nutritious forage was accessible to their mothers only in early lactation.     

Sex-biased parasitism,seasonality and sexual size dimorphism in desert rodents

We investigated seasonality of gender differences in the patterns of flea infestation in nine rodent species to test if sex-biased parasitism in terms of mean abundance, species richness, prevalence and the level of aggregation (a) varies among hosts and between seasons, and (b) is linked to sexual size dimorphism. Sexual size differences were significant in both summer and winter in Acomys cahirinus, Gerbillus pyramidum and Meriones crassus, and in winter only in Acomys russatus, Gerbillus dasyurus, Gerbillus nanus and Sekeetamys calurus. Sexual size dimorphism was male biased except for A. russatus in which it was female biased. Manifestation of sexual differences in flea infestation was different among hosts between seasons. A significant effect of sex on mean flea abundance was found in six hosts, on mean flea species richness in five hosts and on prevalence in two hosts. Male-biased parasitism was found in summer in one host only and in winter in five hosts. Female-biased parasitism occurred in winter in A. russatus. Gender differences in the slopes of the regressions of log-transformed variances against log-transformed mean abundances occurred in three hosts. No relationship was found between sexual size dimorphism and any parasitological parameter in any season using both conventional regressions and the method of independent contrasts. Our results suggest that sex-biased parasitism is a complicated phenomenon that involves several different mechanisms.     

Climate and reproductive seasonality in two free-ranging island populations of rhesus macaques (Macaca mulatto)

We gathered data over a 3-year period (1988–1990) on two free-ranging, island populations of rhesus macaques (Macaca mulatta)to test hypotheses concerning birth seasonal asynchrony and the relationship between climate and reproductive seasonality. Rhesus macaques from Kashmir, India, were translocated to Key Lois in 1973 and from Key Lois to Raccoon Key in 1978. Both sites are low-lying mangrove islands in the Florida Keys. Floral diversity and abundance are greater on Raccoon Key than on Key Lois. Average maximal and minimal temperatures per month did not vary significantly between Raccoon Key and Key Lois over the 3-year period. Average minimal temperatures per month on Key Lois, but not Raccoon Key, varied significantly between years. There were no significant variations in either the amount or the dates of rainfall over the 3-year period for the study area. A combined total of 1524 births was recorded for Raccoon Key (N = 879) and Key Lois (N =645). The birth season on Raccoon Key began 6 weeks earlier than on Key Lois. Births were associated with warmer, rainier months on both islands. Conceptions were associated with cooler, drier months at both study sites. No significant correlations were found between the date of the onset of the summer rains and either median conception or median birth dates on Raccoon Key or Key Lois. Our results do not substantiate the hypothesis that the onset of rainfall, within the temporal period set by photoperiod, regulates seasonal reproduction in rhesus macaques. We suggest that reproductive seasonality in the study populations may be influenced by a variety of factors.     

Changes in testicular and nipple volume related to age and seasonality in Japanese macaques (Macaca fuscata), especially in the pre- and post-pubertal periods

We investigated, longitudinally and cross-sectionally, age and seasonal change in both the testis and nipple volume of Japanese macaques (Macaca fuscata) in relation to concentration profiles of gonadal steroids: testosterone (T) in males and progesterone (P) in females. Testicular volume (TV) and nipple volume (NV) showed rapid growth at puberty, 4.5 and 3.5 years of age in males and females, respectively, but in both sexes there were precocious individuals. The testis as a whole matures at about 10 years of age. TV change is closely related to T concentration profile. The pattern of TV change is composed of maturation and seasonal effects, with individual variation evident mainly in the latter. Some individuals show a simple pattern consisting of one peak in the breeding season (from summer to winter) and one trough in the non-breeding season. Other individuals exhibit a more complicated pattern composed of two or more peaks and troughs before and during the breeding season. The nipple matures at about 7 years but it is difficult to determine the exact maturational age as there are many confounding factors relating to NV. NV shows seasonal fluctuations similar to that of TV. Many animals have periods of substantial growth whereas others do not. The NV in adults from 10 to 25 years does not appear to change much with age, but animals older than 25 years of age have significantly smaller nipples. Seasonal fluctuation in NV mirrors that of the P level. Considered to be controlled by estrogen and P, the NV is a good indicator of the physiological status of reproduction, with its peak about 2 weeks earlier than that of P, that is, at the mid-follicular phase. NV and P level show a similar pattern in pregnancy; from conception, indicated by a P peak, NV and P concentration first decrease, then they increase until peri-parturition and slowly decrease again until the next breeding season.This revised version was published online in April 2005 with corrections to the cover date of the issue.