Sexual swelling,receptivity, and grouping of wild pygmy chimpanzee females at Wamba,Zaïre

The sexual swelling and copulatory behavior of ten pygmy chimpanzee (Pan paniscus) females in a wild group were studied at Wamba, Republic of Zaïre. Since the maximum size of the sexual skin revealed great individual variations depending on age and adolescent females showed little cyclic fluctuation in size, the sexual swelling was measured according to its firmness which periodically fluctuated in all age classes. The duration of maximum swelling and the cycle length were longer inP. paniscus than inP. troglodytes. Although pregnant females and those with newborn infants were sexually inactive, females with infants older than 3 years copulated as frequently as those without dependent infants. Contrary to previous reports on the sexuality ofP. paniscus, copulation was mostly restricted to the maximum swelling phase. All females were usually found in a large mixed party containing both sexes and offspring, regardless of their sexual receptivity.     

Factors Affecting Proximity Among Members of a Wild Group of Moor Macaques During Feeding,Moving, and Resting

We studied the effects of kinship, age, sex, and other factors on patterns of spatial proximity among group members in a wild group of moor macaques (Macaca maurus) in Sulawesi, Indonesia. We assessed the importance of each factor via multiple linear regression analyses. Moor macaques stay close to their matrilineal relatives more frequently when the group moves or rests than when they feed. Subjects of similar age, sex, or rank tended to stay close to each other. Females were in the proximity of females with newborn infants regardless of the phase of activity of the group. Kinship may have less effect on proximity during feeding in moor macaques than in Japanese macaques. Weak effects of kinship during feeding may result from weak contest competition for food within the group.     

Initial calcification of the upper permanent incisor in Japanese macaques

Fifteen laboratory-born Japanese macaques,Macaca fuscata (Blyth, 1875), were examined radiographically for the timing of initial crown calcification of the permanent upper first incisors. The mean age of initial calcification was 199.8 days in females and 204.7 days in males; the sexual difference was significant (p<.05). Precocious incisor calcification in females inM. fuscata resembles that inM. nemestrina andHomo sapiens.     

Intergroup encounters in wild moor macaques (<Emphasis Type="Italic">Macaca maurus</Emphasis>)

We studied intergroup encounters among moor macaques at the Karaenta Nature Reserve, South Sulawesi, Indonesia. Group B has been observed on the basis of individual identification since 1988. We analyzed 85 encounters between members of Group B and members of neighboring groups from September 1990 to November 1998. The average frequency of intergroup encounters was 0.035/hour. Neither the presence of females in estrus nor rainfall had an effect on encounter frequency. Behaviors of moor macaques during intergroup encounters differed from those of Japanese macaques. In moor macaques, no intergroup interactions with body contact were observed during encounters, and females never directed aggression toward members of different groups. The present study did not confirm the prediction of the model ofvan Schaik (1989). Extension of the existing models is required to explain the difference in female dominance styles among macaques by socioecological factors.     

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.     

Functional significance of behavioral,morphological, and endocrine correlates across the ovarian cycle in semifree ranging female Tonkean macaques

The role of sexual displays in mating strategies and their reliability in indicating the time of ovulation has given rise to multiple explanations in nonhuman primates. In order to discriminate among hypotheses, socio-sexual behaviors were recorded in a semifree ranging group of Tonkean macaques (Macaca tonkeana), together with sexual skin swelling volumes and measurements of urinary concentrations of estrone conjugates and pregnanediol glucuronide. A clear preovulatory peak of urinary estrogen levels occurred 2 days before a defined rise in pregnanediol glucuronide concentrations, indicating that both hormones pointed out the female's ovulatory period. The concept of estrus rightly could be applied to female Tonkean macaques since fluctuations in estrogen levels correlated with cyclic changes in genital swelling sizes and rates of female behavioral attractivity and proceptivity. Males proved to be capable of recognizing the optimal conception period as judged from the occurrence of maximal rates of following behavior, serial matings, and ejaculations during the peri-ovulatory phase. During this time, males succeeded in maintaining exclusive and enduring associations with females. However, consortships occurred precociously, with males starting to affiliate with females, follow, and mount them 1 week before the presumed time of ovulation. These long-lasting consortships appear to be a consequence of the female extended follicular phase. This presumably sexually selected character allowed females to extend conspicuous sexual displays: genital swelling and utterance of an estrous call, which might attract males' attention and arouse them. With regard to female mating tactics, the combination of reliably indicating the time of ovulation to the male and durable periods of competitor exclusion led to reject explanations assuming manipulation about paternity or long-lasting intermale competition incitement in Tonkean macaques. Competition for mates between females also turned out to be an irrelevant factor as it was very low in the species. We conclude that the main function of sexual displays is to herald the approach of ovulation toward available mates. Am. J. Primatol. 46:285–309, 1998. © 1998 Wiley-Liss, Inc.     

The evolution of “egalitarian” and “despotic” social systems among macaques

Recent studies of captive macaques have revealed considerable inter-species differences in dominance styles among females. In “egalitarian” species such as stumptail (Macaca arctoides) or tonkean macaques (M. tonkeana), social interactions are more symmetrical and less kin-biased than in “despotic” species such as Japanese (M. fuscata) or rhesus macaques (M. mulatta). Field observations of moor macaques (M. maurus), close relatives of tonkean macaques, suggest that tolerance during feeding characterizes their egalitarian dominance style in the natural habitat. Although it has been proposed that communal defense against other groups may be the main selective force in the evolution of egalitarian dominance style among females, few field data support this prediction. A game theory analysis showed that both an “egalitarian” strategy and a “despotic” strategy are possible evolutionarily stable strategies (ESS) under certain conditions. The difference in dominance styles might reflect the difference in ESS. This means that an egalitarian dominance style can emerge without strong between-group contest competition. A phylogenetic comparison among macaques suggests that despotic dominance styles very likely evolved from egalitarian dominance styles. In the future, primate socioecological studies should pay more attention to the evolutionary history of each species.     

Extended postpregnancy estrous cycles in fernale lion-tailed macaques

Past studies of female primate reproduction have focused on regularly cycling females, and thus the reproductive characteristics of females in other reproductive states (e.g., pregnant, or lactating) have rarely been investigated. In this study, data were collected on estrous swellings and sexual and proceptive behavior in six female lion-tailed macaques during recovery from lactational amenorrhea for the first three to five postpregnancy cycles. For these females, the length of the first lactational recovery swelling cycle averaged 81 days, nearly three times the length of cycles exhibited by nonparturient, isosexually housed females Actual swelling durations were also nearly three times the length of those seen in nonlactating females, and occupied a larger proportion of the cycle For most females, cycle duration and sexual and proceptive behavior declined progressively over successive cycles. The alpha female in each group accounted for the majority of copulations in the first three cycles, and this effect was pronounced in the first cycle. Extended postpregnancy cycles in this species may be related to female reproductive competition and /or a tactic to attract extra-group males. © 1993 Wiley-Liss, Inc.     

Responses to animal stimulus photographs in stumptailed macaques (Macaca arctoides)

Interest in their animate environment was studied in a captive group of 11 stumptailed macaques (Macaca arctoides). Subjects were shown projected photographic slides, most of which showed a single individual primate or non-primate. The measure of interest was the duration of viewing. Results showed that adult females exhibited more interest towards stumptailed macaques versus other macaques species, and towards adult females carrying infants versus adult females alone. Data concerning non-primates showed that subjects were especially interested by photographs of felids; this effect was partly due to the presence of two frontal and conspicuous eyes in felids.     

Female sexual behavior and sexual swelling size as potential cues for males to discern the female fertile phase in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although female catarrhine primates show cyclic changes in sexual behavior and sexual swellings, the value of these sexual signals in providing information to males about timing of the fertile phase is largely unclear. Recently, we have shown that in Barbary macaques, males receive information from females which enables them to discern the fertile phase and to focus their reproductive effort accordingly. Here, we investigate the nature of the cues being used by examining female sexual behavior and the size of sexual swelling as potential indicators of the fertile phase. We collected behavioral data and quantified swelling size using digital images of 11 females of the Gibraltar Barbary macaque population and related the data to the time of ovulation and the fertile phase as determined from fecal hormone analysis. We found that rates of female sexual behaviors were not correlated with female estrogen levels and did not significantly differ between the fertile and non-fertile phases of the cycle. In contrast, swelling size was significantly correlated with female estrogen levels and increased predictably towards ovulation with size being maximal during the fertile phase. Moreover, frequencies of male ejaculatory copulations showed a strong positive correlation with swelling size and highest rates were found during maximum swelling. Our data provide strong evidence that female Barbary macaques honestly signal the probability of fertility through sexual swelling and that males apparently use this information to time their mating activities. Honest advertising of the fertile phase might be part of a female strategy to manipulate male mating behavior for their own advantage, such as ensure fertilization with high quality sperm or influence paternity outcome.     

Social and seasonal influences on the reproductive cycle in female mandrills (Mandrillus sphinx)

We present 12 years of perineal swelling data for a semifree-ranging colony of mandrills (Mandrillus sphinx), and evaluate the influence of rank, parity, and seasonality on reproductive parameters. Female sexual swellings showed a seasonal pattern, with August the median month of ovulation. Overlapping periovulatory periods did not decrease the likelihood of conception. Females showed their first genital swelling at age 3.6 years (n = 28; range, 3.2-4.6 years), and higher-ranking females experienced their first swelling earlier than low-ranking females. Median postpartum amenorrhea (PPA) duration was 208 days (n = 92; range, 74-538 days). PPA was longer in primiparous females than in multiparous females, but PPA duration was unrelated to female rank. Median follicular phase duration was 24 days for the first cycle after parturition (n = 84; range, 12-40 days), shortening to 17 days in subsequent cycles (n = 55; range, 6-39 days). The follicular phase was longer in nulliparous females than in parous females, but was unrelated to female rank. Median cycle length (from one sexual swelling breakdown to the next) was 38 days (n = 57; range, 18-108 days). Eighty-seven percent of conceptions occurred within two cycles, and half of the nulliparous females conceived during their first swelling cycle. Lower-ranking females were more likely to require more cycles to conceive than higher-ranking females. The cycling phase was significantly longer in nulliparous females than in parous females, and was also significantly longer in lower-ranking females than in higher-ranking females. We discuss the influence of provisioning on female reproductive parameters, the influence of parity and rank on the different phases of the interbirth interval, and the evolution of long and variable follicular phases in mandrills.     

Sexual size dimorphism,growth, and maturity of the fluvial eight-barbel loach in the Kako River,Japan

The maturation and growth pattern of the fluvial eight-barbel loach Lefua sp. (Japanese name: nagare-hotoke-dojo), an endangered species, was investigated using an individual identification-recapture method from 1995 to 1998 in an upper reach of a headwater tributary of the Kako River, Hyogo Prefecture, Japan. Based on observations of the gonads through the abdominal skin, the loach was estimated to breed mostly from May to July. All the males matured by age 1⁺, and all the females matured by age 2⁺. Gamete release in all individuals of both males and females was predicted from recaptured loaches during each breeding season. The standard length of mature females was significantly larger than that of males, showing sexual size dimorphism (SSD). The maximum sizes recorded were 75.4 mm SL for females and 61.2 mm SL for males. Both males and females of immature specimens grew mainly from May to November, including the breeding season, with no significant differences in growth rates between them. After sexual maturity, both males and females grew mainly from July to October (or November), after the breeding season, and the females exhibited higher growth rates than males. Therefore, SSD of the species seems to be attributable to the different growth rates after maturity. The longevity of the loach was estimated to exceed ten years based on individual growth patterns of various sizes during the survey period. It is likely that the loach has an iteroparous life history, breeding every year, and moderate growth rates after maturity.     

The Influence of Age,Sex, and Rank on Yawning Behavior in Two Species of Macaques (Macaca fascicularis and M. fuscata)

Yawning behavior was studied in two species of macaques: the long-tailed macaque (Macaca fascicularis) and the Japanese macaque (M. fuscata). Japanese macaques yawned much more than long-tailed macaques. Age, sex, and dominance rank exerted different effects on yawning in the two species. In the long-tailed macaques, sex differences in frequency of yawning emerged only after sexual maturity; yawning rates increased significantly in both males and females as they reached sexual maturity; and, among males, dominance rank was positively correlated with frequency of yawning. Differently, in the Japanese macaques, males, both mature and immature, yawned more than same-aged females; sexual maturity was associated with an increase in yawning in males only; and male rank did not correlate with the frequency of yawning. Regardless of interspecific differences, the overall results supported only in part the finding that, in Old World monkeys, yawning is largely influenced by plasma concentrations of androgens. There was evidence that social factors were also important in influencing the age-sex class distribution of yawning.     

Social relationships between adult male and female rhesus macaques: 1. Sexual consortships

The sexual relationships of 15 adult male rhesus macaques (Macaca mulatta), of one social group in the Cayo Santiago colony, Puerto Rico, were studied during the 1981 mating season. Two criteria were used to determine whether or not a focal male was in consort in a given 20-min observational sample. One hundred and thirty-two consortships were recorded. The distribution and duration of all consortships, and the distribution of those consortships that coincided with the estimated time of conception, were positively correlated with male dominance rank and length of tenure. Correlations with dominance were stronger than those with tenure. Older females had more consortships with focal males than younger females. There was no relationship between female rank and the distribution of consortships. Consortships did not give exclusive access to receptive females although they may do in feral situations. Males were primarily responsible for maintaining proximity in about two thirds of consortships. The four top-ranking males were primarily responsible in all but one of their consortships. Almost all of those in which the female was primarily responsible involved younger, slightly lower-ranking males. This pattern may have resulted from the females being attracted to the latter males although other interpretations are possible. The partner who was primarily responsible for maintaining proximity also tended to be the predominant groomer, supporting the view that grooming plays a role in the maintenance of sexual consortships. Almost a third of consortships were with females who had conceived, suggesting that males could not accurately assess female reproductive state. Consortships maintained by the male were longer than those maintained by the female. Males may try to increase their chances of fertilising a female by prolonging the consortship. High-ranking males may have been more successful at this, resulting in the positive correlation between male dominance rank and consortship duration.     

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.     

A morphometric analysis of the Japanese macaque (Macaca fuscata) mandibular cheek teeth from the Torihama Shell-midden, Early Jomon Period, Fukui Prefecture, Japan

We quantitatively examined the differences in the size and proportion of the Japanese macaque (Macaca fuscata) by comparing the Early Jomon specimens from Torihama shell-midden, Fukui Prefecture and modern specimens from Fukui Prefecture. The purpose of this study was to explore the temporal change in the proportion and size of teeth of the Japanese macaques based on the quantified data. The result of measurements of lower premolars and molars demonstrated that sexual dimorphism was evident only among the modern specimens where the females were significantly smaller than males. The size of male Torihama specimens was within the range of the modern population, whereas the size of the female Torihama specimens was significantly larger than the modern female population. The proportional pattern of premolars and molars for male and female Torihama specimens also differed. The results may suggest a possible difference in the degree of size reduction between males and females since the last glacial period.Morphometric analysis of mandibular cheek teeth from Torihama Shell-midden     

Frequent harassment of mounting after a takeover of a group of moor macaques (Macaca maurus)

Harassment behavior during mounting was observed in a group of moor macaques (Macaca maurus) in Sulawesi, Indonesia. During the study periods in 1994 and 1995, most harassment was performed by juveniles less than 5 years old. No harassment by adult females was observed. Mounting by the α-male, who had newly immigrated to the group, was harassed more frequently than that by the β-male in 1994. In 1995, the frequency of harassment during mounting by the α-male was low as compared with that in 1994. In the case of the new α-male, harassment occurred more frequently during mounting with sexually tumescent females than during mounting with detumescent females. Harassment was rarely observed during mounting by natal males of the group. Many hypotheses have been proposed to explain harassment of mounting in primates. The present results offer support for the following two hypotheses: (1) harassment is an attempt to establish a social bond between the performer and the mounting individuals; or (2) harassment occurs in response to mounting by unfamiliar males.     

Quantitative aspects of the effect of mating on readiness to lay in the Australian sheep blowfly,Lucilia cuprina

Virgin females of Lucilia cuprinararely lay eggs, whereas mated females do so readily. This effect of mating is due entirely to increased readiness to lay, and not to any effect on ovarian development. An investigation was made of how readiness to lay was affected by matings which differed in terms of the male's chemical and mechanical contribution. Individual males were mated, during 1 day, to a succession of females whose readiness to lay was determined 1 or 8 days after mating. On both days, the proportion of females laying was inversely related to the number of females with which the male had previously mated. A high proportion of females that had mated with previously unmated or oncemated males laid at both 1 and 8 days after mating. However, this proportion tended to decline between day 1 and day 8 in females that had mated with males with two or more previous matings, and this effect was most evident in females mated with males that had previously mated with four or more females. When matings were manually terminated as soon as coupling had occurred, the proportion laying remained as low as in virgins. This proportion progressively increased as mating duration increased from 2 to 6 min. The proportion that laid after mating terminated at 6 or 8 min was as high as that for females from full-term matings (mean duration, 12.5 min). The results are generally similar to those obtained in parallel experiments on the effect of mating on sexual receptivity in this species and, therefore, indicate that the physiological bases for the two effects of mating might be the same.     

Female reproductive signaling, and male mating behavior, in the olive baboon

Baboon sexual swellings are among the largest and most colorful signals displayed by any mammal, and many baboon studies have shown an association between sexual swellings and both female and male sexual behavior. However, the extent to which female behavior and sexual swellings combine to signal the timing of ovulation and the fertile period to males, and the extent to which males use these and other signals when determining patterns of mating behavior, remain key topics of research. Here we assess the social and sexual behavior of both female and male olive baboons with respect to detailed measures of swelling size made from digital photographs, measures of fecal progestogen and estrogen levels, and estimates of the timing of ovulation and the fertile period based on those levels. Female aggression and grooming behavior were unrelated to fecal progestogen and estrogen levels, but there were some significant relationships between these hormonal measures and presenting behaviors. Measures of female behavior collected during the study did not appear to reveal the timing of ovulation or the fertile period. Male consortship behavior was closely tied to fine-scale changes in sexual swelling size, but copulation behavior was not. Copulation behavior of consorting males was, however, linked to the timing of both ovulation and the fertile period, suggesting that males did have knowledge about these timings. Together these results suggest that males used fine-scale swelling size changes when deciding when to consort, but that consorting males did not use fine-scale swelling size changes in deciding when to copulate. We propose that swelling size may advertise the period during which males should consort with females, with other signals available only from closer inspection then used by consorting males to assess the timing of the fertile period more accurately. An important implication of this interpretation is that different males may have access to different signals of ovulation at any one time. Such a system would allow females to offer different males different information simultaneously, perhaps offering a solution to the ‘female dilemma’ of how females can simultaneously assure and confuse paternity in multi-male societies.     

Sexual behavior in brown capuchins ( Cebus apella )

We observed sexual behavior patterns in two captive groups of Cebus apella.We obtained data on intersexual solicitations and intersexual competition. The length of proceptivity cycles by females averaged 18.8 ± 1.2 days; this corresponds with published reports of physiological measures of ovulatory cycles. Females initiated sexual interactions with males significantly more than males initiated interactions with females, and female solicitations increased in frequency over the duration of displayed periods of proceptivity. In contrast, male solicitations of females were infrequent and did not change significantly throughout female proceptive phases. Each female solicited the same male throughout a given proceptive phase. We observed no evidence of male-male or female-female competition. Males seem to respond to female sexual behavior directed toward them, rather than initiating sexual interactions themselves. Even so, male sexual interactions with females followed only a small proportion of solicitations.