Energetic consequences of seasonal breeding in female Japanese macaques (Macaca fuscata)

Japanese macaques inhabit a relatively cold environment and females of this species could have developed strategies of energy economy to face the sometimes-harsh seasonal conditions of temperate climates, as well as reproductive costs, and thus regulate their energy balance. Here, we explore the relationship between nutritional status, body composition, seasonality, and reproductive status using isotope-labeled water, anthropometric measurements, and leptin assays from 14 captive female Japanese macaques. Our results indicated that body mass provided the best predictor of fat-free mass and fat mass. These females varied in estimated percent body fat between 8 and 25% (18% on average at the beginning of the mating season and 13% during the birth season). Higher body mass and body fat content were observed at the beginning of the mating season, which supports the hypothesis that individual females need to attain a sufficient physical condition to cover energy costs associated with mating activity, and to survive under severe ecological conditions in winter with high thermoregulatory costs. We found a relationship between conception rates and energetic condition or body fat, with females that conceived during one mating season being fatter after the end of their previous mating season. Together, these results suggest that, even in captive settings with constant food availability, seasonal breeding entails relatively high energy costs, and that females with higher energy status could invest more in reproductive activities and could afford to reproduce more rapidly.     

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.     

Female mating strategy in an enclosed group of Japanese macaques

Female Japanese macaques (Macaca fuscata) are noted for mating with multiple males and for their ability to exert mate choice. In a captive group of Japanese macaques housed at the Primate Research Institute of Kyoto University, Japan, behavioral and endocrine data were combined to examine female mating strategies. During one breeding season, daily behavioral observations were conducted on females who exhibited copulatory behavior. Blood was collected from females twice weekly and their ovulatory periods estimated by analyzing hormone profiles. Females began mating shortly before ovulation, peaked at ovulation, and continued receiving ejaculations for up to ten weeks after conception. Females were more responsible than males for inbreeding avoidance with matrilineal kin. Males sometimes approached females from their own matriline, but females avoided such males and expressed mate choice behavior preferentially toward non-matrilineal males. Over the entire mating season, females did not choose non-matrilineal males on the basis of displays, dominance rank, age, weight, or weight change during the mating season. When females were likely to conceive, however, they expressed mate choice behavior toward males who displayed most frequently. Female mating strategy may include both mate choice at ovulation and other, non-procreative functions.     

Female sexual behavior in the absence of male-male competition in captive Japanese macaques (Macaca fuscata)

A captive group of Japanese macaques (Macaca fuscata). consisting of one adult male and three adult females, was observed for 88 hr during the 1988 mating season. We focused on the group's sexual activities because understanding how social dynamics affect reproductive behavior may enhance our ability to establish self-sustaining captive populations. The adult male exhibited distinct preferences in copulation partners, although all females were receptive and cycled during the study period. The dominant female participated in the most copulations and successfully harassed and disrupted copulations between the male and the other females. The alpha female, therefore, actively constrained the formation of mating pairs. Further, the male did not consort with his year-round female grooming partner. This female, the least dominant member of the group, engaged in the most autosexual and homosexual behavior. Birth season data show that only the dominant female bore offspring. This study emphasizes the influence of social dynamics on a group's reproductive potential and suggests an alternative means by which females can influence consort formation.     

Aggression in adult male primates: A comparison of confined Japanese macaques and free-ranging olive baboons

The frequencies and types of adult male aggressive behavior of confined Japanese macaques (Macaca fuscata)and free-ranging olive baboons (Papio anubis)were compared. The baboons, which do not have a mating season, were more aggressive to conspecific males than were the macaques during their nonmating season. The baboons also solicited aid during aggressive encounters more frequently than the macaques. However, during their mating season, the macaques were more aggressive to conspecific females than were the baboons. The macaques were also involved in more triadic sequences of aggression, and the frequency of occurrence of these patterns supported Chase’s theory of dominance hierarchy formation and maintenance. The differences in aggressive behavior appeared to be related to the seasonal reproductive cycle of the macaques.     

Seasonal changes in spermatogenic cell degeneration in the seminiferous epithelium of adult Japanese macaques (Macaca fuscata fuscata)

The degenerating pattern of spermatogenic cells in the seminiferous tubule of Japanese macaques was studied to clarify a relationship between seasonal changes of reproductive performances and cytological findings in the Japanese macaque. For light microscopy, testis samples were obtained from five adult animals by biopsy in April (nonmating season) and October (mating season). For electron microscopy, specimens from four additional macaques were used. Degenerating cells were found in all steps of spermatogenesis. In stages I to V of the cycle of the seminiferous epithelium, morphologically atypical pachytene spermatocytes were observed in 14.7 and 10.0% of the cells in the nonmating and mating seasons, respectively, although the difference in percentage was not significant. Mature spermatids with atypical features in those stages occupied 59.6% of the cells in the nonmating season, which significantly decreased to 34.1% in the mating season. These results imply that the seasonal change of sperm production is related, at least in part, to the process of degeneration of the spermatogenic cells in this species.     

Effect of Dominance,Reproductive State,and Group Size on Body Mass in Macaca radiata

Body mass can impact reproductive performance in males and females. In nonhuman primates the relationship is often mediated by dominance. We measured body mass monthly in a provisioned group of bonnet macaques (Macaca radiata) living at a Hindu temple. We also measured body mass on 3 occasions in a wild population of bonnet macaques. In the temple group, females that reproduced lost body mass, while females that did not reproduce gained body mass. Mass loss among females occurred primarily while they were nursing. Adult males from the temple group lost mass during the mating season and gained it during the non-mating season. Subadult males experienced less seasonal variation in body mass. Body mass and changes in mass were not related to dominance rank in either the temple or the forest group. Furthermore, maternal dominance rank did not affect infant mass. Females from the smallest forest group weighed significantly less than females from the two larger forest groups, which suggests intergroup competition in the population. Body mass was not related to dominance rank in a straightforward manner but may indirectly affect reproductive performance. The pattern of body mass change suggests that the period of lactation is critical for females and endurance rivalry is an important form of competition among males.     

Measuring temperament in rhesus macaques: consistency and change in emotionality over time

This study of rhesus macaques (Macaca mulatta) investigated whether individual differences in emotionality, as measured by scratching frequencies, are stable over time and across seasons. Five adult females living in captive social groups were observed during two consecutive birth seasons and five females during the birth and the mating season. Scratching frequencies were higher during the birth than during the mating season, suggesting that the presence of infants was associated with elevated emotionality. Individual differences in scratching frequencies remained stable across two consecutive birth seasons, but there was no significant correlation between scratching frequencies in the birth and in the mating season. These findings suggest that, under certain circumstances, individual differences in emotionality are consistent over time and that scratching may be used as a non-invasive indicator of temperament.     

The role of nutrition, body condition and lactation on calving success in muskoxen

Relationships between nutrition, body weight (BW), body condition score (BCS) and fertility were explored in 11 captive female muskoxen between 1988–1994. In 1987, six adult female muskoxen were allocated to high plane (HP) or low plane (LP) nutritional treatments (HP n = 3; LP n = 3), which were maintained year-round through spring 1995 (HP n = 6; LP n = 5). Treatment group size fluctuated annually. Age, lactation status, calving date and calf birth weight were recorded for each cow. Body weight was measured weekly and BCS measured bi-weekly throughout the mating season from 1 August to 31 October. Sixty-one complete observations of BW and BCS in autumn, lactation status and calving success were collected. Body weight and BCS differed significantly ( t -test) with pregnancy ( P < 0.001) and nutritional treatment ( P < 0.001). A significant logistic regression model was generated for the relationship between BW in October and pregnancy ( P < 0.001). When BCS each month was combined with BW in October, BCS in September was the most significant variable ( P < 0.001) and the only one to enter the model. Neither lactational status nor year, in combination or alone, was significant. Both BW in autumn (176 kg provides a 50% probability of a female calving the following spring) and BCS (score of six provides a 50% probability of successful calving) can be useful predictors of fertility in muskoxen. The ability of muskoxen to make significant gains in weight and body condition in autumn may represent a nutritional control point regulating reproduction in this species.     

Seasonal Variation in Female Mate Choice and Operational Sex Ratio in Wild Populations of an Annual Fish,Austrolebias reicherti

The intensity of mating competition and the potential benefits for female of mating with certain males can be influenced by several extrinsic factors, such that behavioral decisions can be highly context-dependent. Short-lived species with a single reproductive season are a unique model to study context-sensitive mating decisions. Through exhaustive sampling in the field and simultaneous choice tests in the laboratory, we evaluated operational sex ratio (OSR) and female mate choice at the beginning and end of the reproductive season in the annual killifish Austrolebias reicherti. We found seasonal change in both OSR and female mate choice. At the start of the reproductive season the OSR did not deviate from parity, and females preferred larger males. Later in the reproductive season, while the proportion of males in the ponds decreased, females became unselective with respect to male size. The particular biological cycle of annual killifish, where both life expectancy and mating opportunities decline sharply over a short timescale, could account for the seasonal change in female choice. Reduction in choosiness could arise from diminished reproductive prospects due to a decline in male availability. Moreover, as the end of the season approaches, any benefits of choosiness are presumably reduced: a female’s fitness will be higher if she mates with any male than if she forgoes reproduction and dies. Future work will disentangle the mechanisms underlying seasonal changes in mating preferences, notably direct responses to demographic factors, environmental cues, or intrinsic changes during development.     

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.     

Female reproductive parameters and fruit availability: factors determining onset of estrus in Japanese macaques

This study examined the onset of estrus, nutritional conditions during the mating season, and female reproductive parameters in a troop of unprovisioned Japanese macaques (Macaca fuscata fuscata). The mean interbirth interval (IBI) was 25.1 mo, suggesting a 2-yr birth cycle. The mean IBI following the death of an infant before the mating season was only 19.8 mo, whereas the mean IBI was 27.8 mo when the infant survived. Estrus occurred during the time of the greatest food quality, in the autumn (i.e., mating season). A female whose infant did not survive the mating season tended to come into estrus more readily than one with a surviving infant. Only one of the 19 females whose infants survived came into estrus, whereas 43 of the 58 (74.1%) females whose infants did not survive came into estrus. Fruit conditions during the mating season each year were evaluated by the seed crop of the two species (Fagus crenata and Zelkova serrata) that constituted the main food source for the macaques; fruiting levels were classified as "high-fruit" or "low-fruit." Females came into estrus more often during high-fruit mating seasons than during low-fruit mating seasons: 36 (97.3%) of 37 females came into estrus during high-fruit mating seasons, whereas eight (20%) of 40 females came into estrus during low-fruit mating seasons. Although females came into estrus under both high- and low-fruit conditions during the mating season, estrus seldom occurred when females had a surviving infant, and it appears that the absence of a surviving infant is an almost essential variable for the onset of estrus. When females with a surviving infant were excluded from the analysis because they were unlikely to come into estrus, all 35 remaining females (100%) came into estrus during high-fruit mating seasons, whereas only eight (34.8%) of 23 females came into estrus during low-fruit mating seasons. Therefore, the onset of estrus is strongly affected not only by the survival of infants through the mating season, but also by fruiting conditions, especially the availability of high-quality food.     

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.     

Affiliative relations among male Japanese macaques (Macaca fuscata yakui) within and outside a troop on Yakushima Island

Male Japanese macaques (Macaca fuscata yakui) in a troop on Yakushima Island frequently groom other males. However, previous studies have not compared the social relations of troop males to those of non-troop males. I followed all troop males and non-troop males in and near a troop during a mating season and during the following non-mating season and recorded their neighbors, grooming, and agonistic interactions. Comparisons of the social relations of troop males and non-troop males with other troop members revealed that grooming and agonistic interactions with females during the mating season were similar between troop and non-troop males. However, troop males groomed each other more often and had fewer agonistic interactions among themselves than did non-troop males. Compared to what occurred in the mating season, troop males groomed females less often and exchanged grooming bouts more often with other troop males during the non-mating season. One non-troop male groomed females more frequently than did any troop male in both seasons, and this male groomed troop males more frequently than did any troop male in the non-mating season. This male immigrated into the troop during the following mating season. Regardless of their competition with respect to reproduction, male Japanese macaques on Yakushima Island maintain affiliative relations, probably to cooperatively defend fertile females from non-troop males.     

Seasonal Effects on Reconciliation in Macaca fuscata yakui

Dietary composition may have profound effects on the activity budgets, level of food competition, and social behavior of a species. Similarly, in seasonally breeding species, the mating season is a period in which competition for mating partners increases, affecting amicable social interactions among group members. We analyzed the importance of the mating season and of seasonal variations in dietary composition and food competition on reconciliation in wild female Japanese macaques (Macaca fuscata yakui) on Yakushima Island, Japan. Yakushima macaques are appropriate subjects because they are seasonal breeders and their dietary composition significantly changes among the seasons. Though large differences occurred between the summer months and the winter and early spring months in activity budgets and the consumption of the main food sources, i.e., fruits, seeds, and leaves, the level of food competition and conciliatory tendency remained unaffected. Conversely, conciliatory tendency is significantly lower during the mating season than in the nonmating season. Moreover, conciliatory tendency is lower when 1 or both female opponents is in estrous than when they are not. Thus the mating season has profound effects on reconciliation, whereas seasonal changes in activity budgets and dietary composition do not. The detrimental effects of the mating season on female social relationships and reconciliation may be due to the importance of female competition for access to male partners in multimale, multifemale societies.     

Adolescent growth and development in Japanese macaques (Macaca fuscata): Punctuated adolescent growth spurt by season

Adolescent growth of Japanese macaques (Macaca fuscata) was studied. Their growth is composed both of a seasonal cycle of acceleration and deceleration and of linear increases. There is a major growth spurt in linear dimension and body weight at the beginning of the breeding season of the third and fourth year of life in females and males respectively, when they mature reproductively. They show additional accelerated growth in the following year(s). These growth spurts, in total, are considered to correspond with the adolescent growth spurt in humans. Adolescent growth of Japanese macaques is characterized by a punctuation by slower growth and a later start, which is considered to be the product of adaptation to a strongly seasonal environment.     

Seasonality, sociality, and reproduction: Long-term stressors of ring-tailed lemurs (Lemur catta)

Fecal glucocorticoid (fGC) concentrations are reliable, non-invasive indices of physiological stress that provide insight into an animal's energetic and social demands. To better characterize the long-term stressors in adult members of a female-dominant, seasonally breeding species - the ring-tailed lemur (Lemur catta) - we first validated fecal samples against serum samples and then examined the relationship between fGC concentrations and seasonal, social, demographic, genetic, and reproductive variables. Between 1999 and 2006, we collected 1386 fecal samples from 32 adult, semi-free-ranging animals of both sexes. In males and non-pregnant, non-lactating females, fGC concentrations were significantly elevated during the breeding season, specifically during periods surrounding known conceptions. Moreover, group composition (e.g., multi-male versus one-male) significantly predicted the fGC concentrations of males and females in all reproductive states. In particular, the social instability introduced by intra-male competition likely created a stressor for all animals. We found no relationship, however, between fGC and the sex, age, or heterozygosity of animals. In reproducing females, fGC concentrations were significantly greater during lactation than during the pre-breeding period. During pregnancy, fGC concentrations were elevated in mid-ranking dams, relative to dominant or subordinate dams, and significantly greater during the third trimester than during the first or second trimesters. Thus, in the absence of nutritional stressors, social dominance was a relatively poor predictor of fGC in this female-dominant species. Instead, the animals were maximally challenged by their social circumstances and reproductive events—males by competition for mating opportunities and females by late-term gestation and lactation.     

Application of paternity discrimination by DNA polymorphism to the analysis of the social behavior of primates

Paternity in many primate species cannot be established reliably on behavioral grounds. For instance, Japanese macaques (Macaca fuscata) have a multi-male group structure and promiscuous mating patterns. On the other hand, accurate evaluation of male reproductive success is needed to analyze primate behavior. DNA finger-printing techniques were applied to 2 captive groups of Japanese macaques in the Primate Research Institute of Kyoto University for identification of paternity. Also, mating behavior of a captive group was observed in order to compare the reproductive success of each male with that expected on the basis of his observed mating activity. The number of offspring of full adult males was not related to their social rank although the number of copulations with ejaculation was highly correlated with their social rank. Monitoring of the female sexual cycles from the plasma profiles of gonadotropins and ovarian hormones suggested that males could not choose females at days of ovulation. The results of two-free-ranging wild troops, like those of the captive groups, indicated that high-ranking males could not monopolize the paternity of offspring. The results of paternity discrimination in Japanese macaques were compared with results from patas monkeys (Erythrocebus patas) in a discussion of social structure and male reproductive success. Some aspects of polymorphism detection techniques are also discussed.     

Plasma cholesterol levels in free-ranging macaques compared with captive macaques and humans

Plasma total cholesterol in free-ranging Japanese macaques (Macaca fuscata) on Koshima islet and in free-ranging long-tailed macaques (Macaca fascicularis) at Pangandaran in Indonesia was found to occur at very low levels compared with captive macaques and humans. Although total cholesterol levels in captive macaques were lower than humans, differences in HDL cholesterol levels were only small. In both sexes of wild and captive Japanese macaques, total cholesterol levels decreased from birth through to young adulthood but then increased in adult females of the captive group. In contrast, the value for adult females of the wild troop remained at a low level. Low TCH levels in adult females of the wild Japanese macaque troop may be due to a low energy intake and may have caused a delay in the onset of sexual maturation. Plasma TCH levels increased with the addition of 0.1% dietary cholesterol over six weeks in captive long-tailed macaques. That the cholesterol value after six weeks was dependent on cholesterol levels prior to supplementation indicates that captive macaques are slightly saturated with cholesterol.     

Age and sex differences in the impact of seasonal energy stress among Andean agriculturalists

It has been widely argued that children and females are most severely affected during periods of food scarcity. This proposition is tested using dietary and anthropometric data from the Andean community of Nuñoa, Peru. Contrary to expectation, children (ages 12 years and under) are relatively protected from seasonal food scarcity while adults experience severe caloric stress. Anthropometric measures of nutritional status corroborate the dietary analysis, indicating significantly better nutritional status in children. Sex differences in dietary adequacy are not evident. Adult males, however, have significantly poorer measures of nutritional status than adult females. These differences in dietary adequacy and nutritional status reflect adaptations to marked seasonality in work demands and energy availability.