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

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

Seasonal variation in fecal testosterone levels in free-ranging male Japanese macaques

Seasonal variation in fecal testosterone levels in free-ranging male Japanese macaques (Macaca fuscata) was examined with reference to their dominance rank and age class. Six adult (>or=7 years old, three higher-ranking and three lower-ranking) and four adolescent (5-6 years old, two higher-ranking and two lower-ranking) males were selected as target animals. Fecal samples of these males were collected during the first 3-5 days of each month and analyzed by the method developed by Barrett et al. [Primates 43:29-39, 2002 b]. Testosterone levels varied significantly across the 12 months, and were highest in the early and middle parts of the mating season (i.e., October and November). Higher-ranking adult males displayed a peak testosterone level in October, whereas lower-ranking adults had no clear peak in the mating season. Such a difference in testosterone peaks in males could provide higher-ranking males more opportunities to fertilize females at first ovulation in the mating season than lower-ranking males.     

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.     

Do males have a better chance of mating when the number of estrous females is equal to or greater than the males' ordinal rank? Testing the hypothesis in Japanese macaques

This study was designed to test the hypothesis that male primates in multi-male/multi-female social groups with a clear male dominance hierarchy have a better chance of mating when the number of estrous females is equal to or greater than, as opposed to less than, the males' ordinal rank. I studied a Japanese macaque (Macaca fuscata fuscata) troop during mating seasons from 1992 to 1995. The mean daily operational sex ratio (OSR; the number of estrous females per troop male), which was calculated on observation days, was 0.21, 1.9, 0.48, and 3.1 in 1992-1995, respectively. Overall, focal animal sampling of males yielded 118 male-day records. The male-day records for each male were divided into the two estrous female number conditions: 1) the male-day records when the number of estrous females was equal to or greater than the male's ordinal rank, and 2) the male-day records when the number of estrous females was less than the male's ordinal rank. In the 1993 and 1995 mating seasons, when the number of estrous females was equal to or greater than the ordinal rank of each male, all of the males were observed mating. Conversely, when the number of estrous females was less than the ordinal rank of some male, they were not observed mating in the 1992 and 1994 mating seasons. The percentage for each male across each male's total mating opportunity was <20% when the number of estrous females was less than the male's ordinal rank. By contrast, the percentage for each male across each male's total mating opportunity exceeded 45% when the number of estrous females was equal to or greater than the male's ordinal rank, except for one male. Of all the male-day records for males observed mating with ejaculation, 41 were obtained when the number of estrous females was equal to or greater than the male's rank; conversely, only three records were obtained when the number of estrous females was less than the male's ordinal rank. Therefore, it appears that males have a better chance of mating when the number of estrous females is equal to or greater than the males' ordinal rank, as opposed to when the number is less than their ordinal rank.     

Reproductive synchrony in captive macaques

Captive bonnet macaques housed at the California Primate Research Center reproduce seasonally. The chances of producing surviving infants were substantially reduced among females who conceived at the peak of the mating season compared with females whose conceptions were more isolated in time. Primiparous females and low ranking females were most consistently affected by the extent of reproductive synchrony. Behavioral data suggest that harassment of conceiving and pregnant females may have contributed to the correlation between the extent of reproductive synchrony and infant mortality as the levels of aggression toward females were highest during the months in which conceptions were most common.     

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.     

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.     

Homosexual incest avoidance among females in captive Japanese macaques

This paper reports a systematic pattern of homosexual incest avoidance among females in a captive group of Japanese macaques (Macaca fuscata) culled from the Arashiyama-West troop known for its high rates of female homosexuality. The study group included three matrilines and two generations. Between eight and 11 females were sexually active over four consecutive mating seasons, and all engaged in both heterosexual and homosexual activity. While all females performed homosexual acts with almost all possible non-kin partners, they systematically avoided homosexual interactions with their mother, daughters, and sisters. This pattern could not be explained either in terms of kin not being simultaneously in estrus, kin avoiding affiliative interactions in general, or non-kin utilizing the tension-reducing effect of estrus to affiliate exclusively with each other. In contrast to homosexual females, heterosexual pairs of relatives (brother-sister, mother-son) were sometimes incestuous. Assuming that female homosexuality expresses the reproductive strategy of females unconstrained by male influence, the present results point to the strong tendency of females to avoid incest and suggest that males are primarily responsible for the reported exceptions to incest avoidance.     

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.     

The reproductive biology of a free-ranging troop of Japanese monkeys

Quantitative data on the reproductive biology of Japanese monkeys (Macaca fuscata), especially of females, are reported here. Arashiyama B troop shows stable annual breeding periodicity, and has mating seasons between October and March. In mating seasons, females show estrus with rather consistent cyclicity, and are in estrus for a total of 35 days on an average. The mean length of estrous cycle is 34 days. Although most females show estrus inter-menstrually, some show peri-menstrually; i.e., estrus does not always synchronize strictly with ovulation. Pubescent females between 3.5 and 6.5 years show estrus, but with low sexual activity. Middle-aged females between 7.5 and 16.5 years show high sexual activity with high conception rate. Old-aged females over 17.5 years show low sexual activity. Females with surviving infants have lower sexual activity than those without infants. There is found no significant correlation between female's ranking and sexual activity. This study was financed partly by the Cooperative Research Fund of the Primate Research Institute, Kyoto University.     

Neonatal abandonment in Japanese macaques

This study analyzed long-term demographic data relative to a captive colony of Japanese macaques (Macaca fuscata) in order to evaluate factors predicting increased probability of infant neonatal abandonment. Overall, 7.7% of liveborn infants were abandoned at birth. Probability of abandonment was significantly increased in primiparous and, to a lesser extent, low-ranking mothers. Primiparous mothers abandoned about 40% of their infants at birth. Mother age and infant sex had no independent effects on the probability of neonatal abandonment. Primiparous mothers that did not abandon their infants suffered increased infant mortality and showed longer interbirth intervals compared to same-age multiparous mothers. These results are partially consistent with adaptive hypotheses predicting maternal divestment under unfavorable conditions, and with proximate explanations linking abandonment to inexperience and stress.     

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.     

Mating Tactics in Response to Costs Incurred by Mating with Multiple Males in Wild Female Japanese Macaques

We investigated the costs of mating with multiple males in terms of feeding time, traveling distances, sexual proceptivity, and male aggression, for wild female (Macaca fuscata yakui) on Yakushima Island, Japan. We analyzed all-day focal sampling data from 7 females during the mating season (Sept.-Nov. 1996). On days when estrous females copulated with multiple males, they decreased their feeding time to half that of anestrous days, traveled longer distances, showed more proceptive sexual behaviors and received more aggression from subordinate males than on days when they copulated with only the 1st-ranking male. On days when females copulated with only the 1st-ranking male, they showed no difference in feeding time with that of anestrous days, and expended less effort than the above mating pattern because of short traveling distances, diminished sexual proceptivity and a lower frequency of aggression received. The results suggest that the costs of estrous vary according to female sexual proceptivity and the number and social status of mating partners. Female Japanese macaques exhibit a mixed mating strategy over prolonged estrous periods, which may provide females with opportunities to maximize the benefits of copulating with multiple males and to minimize the costs of estrus by mating with only the 1st-ranking male. During an estrous cycle, females may be adjusting efforts for reproduction and survival; i.e., mating vs. feeding.     

Demography and life history of Thomas langurs (Presbytis thomasi)

Life history data from wild primate populations are necessary to explain variation in primate social systems and explain differences between primates and other mammals. Here we report life history data from a 12.5-year study on wild Thomas langurs. Mean age at first reproduction was 5.4 years and the sex ratio at birth was even. The mean interbirth interval (IBI) after a surviving infant was 26.8 mo, after nonsurviving infants 17.7 mo, and combined 22.0 mo. Mean annual birth rate of adult females was 0.44, while reaching a peak at 6 years of age and showing no decrease with age. Mortality was highest during the first year of life (48.0% for males and 43.0% for females) and consistently higher for males than females. The oldest female observed during the study was estimated to be 20 years of age, whereas the oldest male disappeared at age 13 years, indicating that males die at a much earlier age than females. A Leslie matrix based on these estimates yielded a growth rate of 1.01, which is comparable to the nonsignificant increase in density indicated by our long-term field data. A comparison with life history data for sympatric frugivorous primates suggests that folivory might be associated with faster life history.     

Sources of variation in interbirth intervals among captive bonnet macaques (Macaca radiata)

Female fitness is a function of variation in the length of females' reproductive careers, the viability of their offspring, and the frequency with which they give birth. Infant loss shortens interbirth intervals in most primate species, but we know considerably less about other factors that contribute to variation in the length of interbirth intervals within groups. In one large captive group of bonnet macaques, maternal parity, age, experience, family size, and recent reproductive history are all associated with variation in the length of intervals that follow the birth of surviving infants. Primiparous females have the longest interbirth intervals, while multiparous females who have produced surviving infants in the past and have raised their last infant successfully have the shortest interbirth intervals. Infant sex and maternal rank have no direct effect upon the length of interbirth intervals. One of the underlying causes of variation in the length of interbirth intervals after surviving births seems to be variation in the timing of conceptions among females. Females who conceive early in the mating season tend to have shorter interbirth intervals than other females. However, females who are multiparous, experienced, and have recently raised infants have late conceptions and short interbirth intervals.     

Long-term variation in fruiting and the food habits of wild Japanese macaques on Kinkazan Island, northern Japan

We studied the relationship between the food habits of Japanese macaques (Macaca fuscata) and the availability of nuts (Fagus crenata, Zelkova serrata, Carpinus spp., and Torreya nucifera) on Kinkazan Island, northern Japan, from 1997 to 2005 to examine the long-term variations in both food habits and availability. The food habits of the monkeys showed clear seasonal changes: the staple foods were woody leaves and flowers in spring (May and June), woody leaves and seeds or fruits other than nuts in summer (July and August), nuts and seeds or fruits other than nuts in fall (September-November), and herbaceous plants in winter (December-April). The availability of nuts, combinations of masting species, and energy production varied among years. Food habits varied among years, but the magnitude of variability of food habits differed among seasons, with large variability during summer and winter, and small variability in spring. Food availability was poor in summer and winter, but in several years the monkeys were able to consume nuts during those seasons. We emphasize the importance of conducting long-term studies on both food availability and the food habits of animals in the temperate zone.     

Reproductive patterns in pygmy lorises (Nycticebus pygmaeus): Behavioral and physiological correlates of gonadal activity

The purpose of this study was to evaluate behavioral and physiological parameters of reproduction in a breeding colony of pygmy lorises. To this end, nine male and eight female adult pygmy lorises were kept under natural lighting conditions and monitored through five consecutive breeding seasons. Behavioral data were collected continuously throughout the year on all loris pairs. Behaviors associated with estrogen peaks in females included approaches, leaves, and lunges by females. Whistles were more frequent during estrus, but there was high inter‐individual variability. Males responded to estrous females by persistent following. There was a higher percentage of births in pairs that were together for more than 30 days before onset of estrus, compared with pairs that were put together when females came into estrus. However, these results may have been influenced by factors such as previous familiarity and social compatibility. Fecal testosterone levels were measured using radioimmunoassays and correlated with estrogen peaks and labial swelling of the females. The data showed an annual rhythm in testosterone that was consistent with a July–August mating season. Captive births were significantly higher during January–April than they were during any other months of the year. The earliest testosterone peak in a juvenile male was detected at 58 weeks, while the youngest male to sire offspring was 73 weeks of age at the time of the conception. Zoo Biol 22:15–32, 2003. © 2003 Wiley‐Liss, Inc.     

Reproductive patterns and birth seasonality in a South-American breeding colony of common marmosets,Callithrix jacchus

We analyzed data on captive-born and wild-caught females housed under natural conditions in a colony located in northeastern Brazil. No differences in reproductive performance were found between captive-born and wild-caught females. Twins were the most frequent litter size, followed by triplets and singletons. No parity effect was observed, with similar infant survival for nulliparous and multiparous females. No significant departures in sex ratio were detected for births and mortality of the male and female infants. The age of the females at the time of pairing showed a negative correlation with pairing-parturition length, but did not affect infant survival. The prolongation in pairing-parturition interval (PPI) and interbirth interval (IBI) was related to birth seasonality. The births were clustered in the second half of the dry season and the beginning of the wet season (November–March), and the time of pairing and the time of infant birth influenced the PPI and IBI, respectively. The use of outdoor cages, which allowed the animals to be aware of the seasonal variations in photo-period and rainfall seems to be sufficient to time the reproductive activity, even when the animals are maintained on a constant food supply.     

Preliminary observations on sexual behavior and the mating system in free-ranging lesser galagos. (Galago moholi)

Sexual and associated patterns of behavior of lesser galagos (Galago moholi) were recorded during an 18-month study conducted at the Nylsvley Nature Reserve in South Africa. Animals were trapped and fitted with radio transmitter belts in order to monitor nocturnal activities during twice-yearly mating seasons. Most copulations occurred during the last week in May, while a subsidiary (post-partum) mating season occurred in late September-early October. Females came into estrus sequentially during the May season. Adult males exhibited increase in body weight and testes volume during the mating season, changes which were most pronounced among the larger males (> 226 g). Larger males also had the greatest mating success, initiating 88% of observed copulations. Sixty-seven percent of matings involved more than one male copulating with the same female during her estrus, which lasted 1-3 days. Mounts were prolonged (range 2-53 min, mean 9.0 min) and males copulated repeatedly (2-5 times) with the same partner during a single night. These observations of sexual behavior and of large relative testes size in free-ranging lesser galagos are consistent with the occurrence of a dispersed mating system involving sperm competition in this nocturnal prosimian species.