Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys

In many primates species, female sexual attractivity is influenced by behavioral cues as well as by nonbehavioral cues (i.e., visual-morphological or chemical signals). Both kinds of cues are usually related to the ovarian cycle and female hormonal state. Female tufted capuchins (Cebus apella) lack any external morphological change in relation to the ovarian cycle and evidence of scent-marking behavior has never been reported. In addition, tufted capuchin males do not routinely investigate the female's body or urine. Instead, capuchin females are extremely active in sexually soliciting the male(s) and their courtship toward them involves a rich behavioral repertoire. In the present study we defined female tufted capuchin proceptivity and investigated its relationship with female reproductive state. Ovarian hormones were measured in urine and fecal samples from four captive females in order to (a) assess their reliability for monitoring female ovarian function and (b) provide information on the timing of the component cycle phases and in particular the periovulatory phase. Measurements of urinary and fecal progestin metabolites provided the best indicator of ovarian cyclicity and for timing of the periovulatory phase. Through a multivariate analysis of the behavioral data set we distinguished four behaviors (eyebrow raising with vocalization, touching-and-running, nuzzling and head cocking) which showed a marked cyclicity (21.3 days) that matched that of urinary progesterone (21.9 days). Data showed that each period of proceptive behaviors was 2.7 +/- 0.8 days long and the day of a defined luteal phase rise in urinary progesterone levels was markedly shifted toward the end of this period. Furthermore, the ejaculations observed always occurred within proceptive periods. The results clearly indicate that female behavior is a good indicator of the periovulatory phase and can enhance female attractivity.     

Loss of oestrus, concealed ovulation and paternity confusion in free-ranging Hanuman langurs.

Ovarian cycles in catarrhine primates are uniquely characterized by prolonged periods of sexual activity in which the timings of ovulation and copulation do not necessarily correspond. According to current hypotheses of primate social evolution, extended sexuality in multi-male groups might represent part of a female strategy to confuse paternity in order to reduce the risk of infanticide by males. We test this hypothesis by examining mating behaviour in relation to timing of ovulation and paternity outcome in a multi-male group of free-living Hanuman langurs. Using faecal progestogen measurements, we first document that female langurs have extended receptive periods in which the timing of ovulation is highly variable. Next, we demonstrate the capacity for paternity confusion by showing that ovulation is concealed from males and that copulations progressively decline throughout the receptive phase. Finally, we demonstrate multiple paternity, and show that despite a high degree of monopolization of receptive females by the dominant male, non-dominant males father a substantial proportion of offspring. We believe that this is the first direct evidence that extended periods of sexual activity in catarrhine primates may have evolved as a female strategy to confuse paternity.     

Concealed fertility and extended female sexuality in a non-human primate (Macaca assamensis)

In numerous primates living in mixed-sex groups, females display probabilistic cues of fertility to simultaneously concentrate paternity to dominant males while diluting it amongst others as a means to reduce the risk of infanticide and to increase male care for offspring. A few species, however, lack these cues and potentially conceal fertility from males; yet, to date, little is known about mating patterns and their underlying proximate mechanisms in such species. Here, we investigated mating activity and sexual consortships relative to female reproductive state in wild Assamese macaques (Macaca assamensis), a species where females lack prominent anogenital swellings and copulation calls. During two mating seasons (2837 contact hours) we recorded sexual and social behaviors, sexual consortships, and collected 1178 fecal samples (n = 15 females) which were analyzed for progestogen concentrations to assess female reproductive state and to determine the timing of ovulation and conception. Although mostly conceiving in their first ovarian cycle, females were sexually receptive throughout the entire 4-month mating season, and within-cycle mating frequencies were not increased during fertile phases. Dominant males did not monopolize fertile matings, and consortships by high-ranking males lasted for long periods, which were not exclusively linked to female fertile phases. Furthermore, females copulated promiscuously but not randomly, i.e. for almost every female, matings were concentrated to a certain male, irrespective of male rank. Collectively, we demonstrate that fertility is undisclosed to males. The extreme extended female sexuality facilitated by concealed fertility may allow females to create differentiated mating relationships within a promiscuous mating system. Our study provides important new insight into the plasticity of female sexuality in non-human primates.     

Analysis of tufted capuchin (Cebus apella) courtship and sexual behavior repertoire: changes throughout the female cycle and female interindividual differences

Sexual solicitations and initiative (proceptivity, sensu Beach [1976] Horm Behav 7:105-138) are important components of the sexuality of females of many primate species. In the tufted capuchin (Cebus apella), female proceptivity characterizes the species' mating system. In study 1, we defined and discussed 20 behavioral patterns based on the observation of 6 females and 5 males living in two social groups. In study 2, each behavior, including mounting activity, was quantitatively assessed during the periovulatory and nonperiovulatory cycle phases of 4 females, detected on the basis of urinary progestin levels (N = 20 ovulatory cycles, 5 for each female); moreover, we monitored changes in females' social interactions (agonism, grooming activity, and play). Nine of the behaviors typically used by the female during courtship and in sexual interactions showed a dramatic increase during the periovulatory phase. Though males mounted females at an apparently higher rate during the periovulatory than the nonperiovulatory phase, the difference was not significant. However, when adult male mounting is separated into those which occur within play and nonplay contexts, there is a significant periovulatory phase effect for mounts not associated with play. Females groomed adult males at the same rate throughout the cycle. Agonism and play did not show any phase effect; however, females' avoidance of adult males significantly increased during the periovulatory phase. Finally, each female made a statistically different use of the behavioral repertoire by performing some behaviors more than others. This variability among females during courtship calls for further research into whether it affects mating success.     

Juggling priorities: female mating tactics in Phayre's leaf monkeys

Extended sexual receptivity in primates is thought to facilitate paternity confusion, thus decreasing the risk of infanticide. However, females might also provide some indication of ovulation to attract preferred males during fertile periods. We examined female mate preferences across defined receptive periods (N = 59) in a group of wild Phayre's leaf monkeys (Trachypithecus phayrei crepusculus) at Phu Khieo Wildlife Sanctuary (February-September 2006; 2,603 contact hours). The group contained seven cycling adult females and three reproductively active males (one adult and two adolescents). We predicted that females would prefer the adult male during periovulatory (POP) receptive periods, but the adolescent males during nonperiovulatory (NPOP) and postconceptive (PC) periods. We collected focal and ad libitum data on sexual and agonistic behaviors to determine female preferences and male awareness of female fertility. We also determined the degree of mating overlap to assess if males were capable of monopolizing females. Our results indicate that females were more frequently proceptive and receptive toward the adult male during POP. By contrast, females were more proceptive and receptive toward one of the adolescent males during PC periods, but rarely interacted with the other adolescent. Patterns of attractivity and agonism across receptive periods suggested that the adult male could detect fertility, while the preferred adolescent could not. Finally, we found a high degree of overlap in total receptive period days, but a low degree of overlap in POP receptive days, suggesting that the adult male might have monopolized females, especially since he seemed to be aware of female fertility. Although these results suggest that females provide some information on ovulation, they also suggest that females attempt to confuse paternity, perhaps capitalizing on male differences in the ability to detect fertility.     

Relationship between ovarian cycle phase and sexual behavior in female Japanese macaques (Macaca fuscata)

We conducted behavioral observations simultaneously with fecal sample collection on eight nonlactating females 2-3 times per week, October 1997-March 1998, to examine the relationship between ovarian hormones and the sexual behavior of female Japanese macaques (Macaca fuscata) during the mating season. We analyzed samples by enzyme immunoassay for fecal hormone levels. Hormone profiles of estrone-glucuronide (E1) and pregnanediol-glucuronide (PdG) were used to separate ovarian cycles into three phases (follicular, periovulatory, and luteal). Hormonal profiles indicate average cycle lengths of 27.6 +/- 4.2 days (+/- SD; n = 26). Average lengths of the luteal and follicular phases were 12.3 +/- 3.8 days (+/- SD) and 8.3 +/- 3.4 days (+/- SD), respectively. We observed female Japanese macaques engaging in sexual activity throughout the ovarian cycle, with the highest rates occurring during the follicular and periovulatory phases as compared to the luteal phase. The attractivity of female Japanese macaques increased significantly during the follicular and periovulatory phases of the ovarian cycle, when E1 levels are peaking and PdG levels drop to baseline. In addition, females displayed a significant increase in proceptive behavior during the follicular and periovulatory phases. Grooming bouts, as well as proximity between female and male macaques, also increased significantly during the follicular and periovulatory phases. We conclude that fluctuating levels of ovarian hormones in different phases of the cycle are significantly associated with variable rates of copulatory and pericopulatory behaviors in these Japanese macaque females.     

Relationship between sexual interactions and the timing of the fertile phase in captive female Japanese macaques (Macaca fuscata)

Japanese macaques live in multi‐male/multi‐female social groups in which competition between males, female mate choice, and alternative male mating strategies are important determinants of mating and reproductive success. However, the extent to which adult males rely on female behavior to make their mating decisions as well as the effect of social rank on mating success are not clear as results are inconclusive, varying from study to study. In this study, we combined behavioral and endocrine data of 14 female Japanese macaques to examine the relationship between ovarian cycle phase and frequency of sexual behaviors, and to investigate how social rank influences sexual behavior in this species. We found that there was no increase in female proceptive behaviors during the fertile phase of the ovarian cycle, suggesting that female behaviors did not clearly signal the probability of conception. In spite of that, the frequencies of ejaculatory copulations were highest during this phase, indicating that the attractivity of females increased significantly during the period with higher probability of conception. Males, and especially the highest ranking male, were able to discriminate females nearing ovulation and to concentrate their mating effort, implying that the timing of ovulation was not concealed from them. The α male seemed able to monopolize most female matings, which is probably due in part to the low number of females simultaneously ovulating and to the limited number of inconspicuous places that the lower ranking males have to mate with females and avoid α male aggression. All together, these results suggest that different males may have access to different signals of ovulation and/or are differentially restrained as to how they can act on that information. The exact nature of the estrogen‐related cues males use to recognize female reproductive status, and to what extent males use them warrants further investigation. Am. J. Primatol. 71:868–879, 2009. © 2009 Wiley‐Liss, Inc.     

What Hanuman langur males know about female reproductive status

In species with a high risk of infanticide, a conflict of interest exists between the sexes over the amount of paternity information that is available to males. While females are expected to keep males unaware of their reproductive status in order to confuse paternity, selection should favor those male traits that enhance the males' assessment of female status and consequently of paternity probability. In Hanuman langurs (Semnopithecus entellus), a species that is extremely vulnerable to infanticide, females have been shown to successfully conceal the exact timing of ovulation from males--perhaps because they exhibit no sexual swelling and mate during all reproductive phases, including gestation. Nevertheless, it remains unclear whether males have hitherto unrecognized information about females' reproductive condition on a broader level that could still enhance male reproductive success. We investigated male assessment of female reproductive states in a population of wild Hanuman langurs as indicated by changes in male behavior, such as rates of copulations, anogenital inspections, and consortships, in relation to different female receptive periods (pregnant, fertile-nonconceptional, and conceptional). Our data indicate that males were able to discern qualitatively distinct reproductive states. Males were more interested in fertile than pregnant females, as indicated by higher copulation rates. Based on consortships, males distinguished fertile from nonfertile phases, as well as fertile, nonconceptional receptive periods from conceptional ones. Hanuman langur males are thus not as unaware of female reproductive condition as previously thought, supporting the idea of an ongoing battle of the sexes over paternity information. However, granting some knowledge while at the same time concealing the exact day of ovulation may also reflect a pure female strategy of balancing paternity concentration with paternity confusion, which is the most likely strategy in this system with high infanticide risk and male defense of infants.     

Female Barbary macaque (Macaca sylvanus) copulation calls do not reveal the fertile phase but influence mating outcome

In a number of primate species, females utter loud and distinctive calls during mating. Here we aim to clarify the information content and function of Barbary macaque (Macaca sylvanus) copulation calls by testing (i) whether or not copulation calls advertise the female fertile phase and (ii) whether and how copulation calls influence male ejaculatory behaviour. In order to do this, we combined hormone measurements with acoustic analysis and behavioural observations. In contrast to a previous study implying that the structure of copulation calls indicates the timing of the fertile phase, our results, using objective endocrine criteria for assessing ovulation, provide evidence that the structure of copulation calls of female Barbary macaques does not reveal the timing of the fertile phase. More importantly, females seem to influence the likelihood of ejaculation by calling versus remaining silent and by adjusting the timing of call onset. Females make use of this ability to influence mating outcome to ensure ejaculatory matings with almost all males in the group. In addition, calls given during ejaculatory copulations differ from those during non-ejaculatory copulations, providing information about mating outcome for listeners. We conclude that in this species, copulation calls apparently serve to enhance sperm competition and maximize paternity confusion.     

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.     

Female Mate Preferences Among Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park, Uganda

Studies of reproduction among chimpanzees traditionally have focused on the mating strategies of males. However, less is known about the mating strategies of female chimpanzees and whether they demonstrate mate choice. I investigated sexual behavior and female mate preference in the chimpanzees of the Kanyawara community. To estimate mate preferences, I analyzed female proceptivity and resistance rates of 6 estrous females toward a total of 13 males as well as male solicitation and aggression rates toward females. Males solicited some females more often than others for mating and preferred them throughout estrus, not only during the periovulatory period (POP), when conception was most likely. In contrast, though females had strong mate preferences in both non-POP and POP, their mate preferences were not consistent between the 2 phases. The shift in mate preferences is evidence of a promiscuous yet tactical mating strategy to confuse paternity. Further, females were more proceptive and generally less resistant toward eschewed males in non-POP and more proceptive and less resistant toward preferred males in POP. Hence, the results indicate that females attempted to mate selectively during the fertile phase. Kanyawara female chimpanzees appear to change their mating strategies and selectivity during estrus and thus may pursue a mixed reproductive strategy. The tactic may allow females to deceive males, indicating that promiscuity among chimpanzee females may be more strategic than previously thought.     

Sociosexual behavior, male mating tactics, and the reproductive cycle of giraffe Giraffa camelopardalis

Female distribution exerts a major impact on male mating tactics. Giraffe cows have a reproductive cycle, and a social system, that should favor a male roaming reproductive tactic. We conducted a 2-year study of female Rothschild's giraffe (G. c. rothschildi) reproductive endocrinology in order to characterize attributes of the reproductive cycle and investigate how female endocrine and behavioral cues influence mating activity. We used non-invasive fecal steroid methods to determine reproductive state among females residing in a herd in a large outdoor enclosure. We found that females had an estrous cycle of 14.7 days and that they regularly had multiple ovarian cycles prior to conception. Adult males were more likely to associate with, and sexually investigate, females when they were cycling than when they were either pregnant or acyclic. During the estrous cycle, male-female proximity and sociosexual behavior were more pronounced during the probable fertile phase than the rest of the cycle. Sexual activity between giraffe coincided with the periovulatory period, with male interest in females peaking during the fertile window in the absence of proceptive behavior by females. We conclude that males detect reliable cues revealing female reproductive status and partition their reproductive effort in response to such cues. We propose that male giraffe adopt a roaming reproductive strategy with their large size, enabling them to search for and mate guard fertile females while minimizing metabolic costs.     

Do males time their mate-guarding effort with the fertile phase in order to secure fertilisation in Cayo Santiago rhesus macaques?

In contrast to most mammalian species, female sexual activity is not limited to the fertile phase of the ovarian cycle in anthropoid primates, which has long been proposed to conceal the timing of ovulation to males. It is now generally believed that females are still most attractive during the fertile phase, leading to high-ranking males successfully mate-guarding them specifically during this period. While studies conducted in species exhibiting exaggerated sexual swellings (probabilistic signal of the fertile phase) have generally supported this hypothesis, mixed support comes from others. Here, we investigated whether high-ranking males timed mate-guarding effort towards female fertile phases in rhesus macaques (Macaca mulatta). In this species, adult females do not exhibit sexual swellings, but undergo facial skin colour variation, an alternative oestrogen-dependent graded-signal of female reproductive status. We collected behavioural, hormonal and genetic paternity data during two mating seasons for one group of the free-ranging population of Cayo Santiago. Our results show that mate-guarding by top-ranking males did not completely cover the entire female fertile phase and that this tactic accounted for only 30-40% of all fertilisations observed. Males tended to prolong mate-guarding into the luteal phase (null probability of fertilisation), which mirrors the pattern of male attraction to female facial colour reported in an earlier study. These findings suggest that males may have limited knowledge regarding the exact timing of females' fertile phase in rhesus macaques, which presumably allows females to gain more control over reproduction relative to other anthropoid primate species.     

Female ovarian cycle phase affects the timing of male sexual activity in free-ranging Barbary macaques (Macaca sylvanus) of Gibraltar

Although all macaques have a multimale multifemale mating system, the degree of promiscuity shown by the Barbary macaque is considered to be extreme in terms of both mating frequency and number of mating partners. How mating activity is distributed throughout the female menstrual cycle and whether or not copulations are concentrated around the fertile phase as in other members of the genus is, however, not known. To examine this, we collected data on rates of copulation throughout 29 ovarian cycles from 13 free-ranging females of the Gibraltar Barbary macaque population and related them to the time of ovulation and the female fertile phase as determined from fecal hormone analysis. In addition, patterns of male inspection of females and time spent in consortship, both indicators of female attractivity, were also analyzed. The results indicate that both mating behavior and female attractivity vary predictably with ovarian cycle stage. Rates of copulation were found to increase toward the time of ovulation, with a distinct peak of ejaculatory (but not non-ejaculatory) copulations occurring in the fertile phase. Additionally, we show that frequency of inspection of females by males and time spent in consortship were also highest during the fertile phase and that ejaculatory copulations and male pericopulatory behaviors were significantly correlated with levels of female sex hormones. Our findings indicate that the Barbary macaque shows a mating pattern during the cycle similar to that described for other members of the genus. More importantly, however, our study provides clear evidence that despite an extreme degree of promiscuity Barbary macaque males concentrate their reproductive effort to the fertile phase, implying that they are able to discern this period and that thus timing of ovulation is not concealed from them. Estrogen-related cues appear to be involved in the process of recognition of female reproductive status by males, but the exact nature of these cues and how male Barbary macaques use them remains to be clarified.     

Assessment of female reproductive status by male longtailed macaques, Macaca fascicularis, under natural conditions

Recent theories on primate sexual selection have paid increasing attention to the importance of reproductive strategies of females living in multimale groups. However, the extent to which females are able effectively to conceal or advertise the time of ovulation as part of these strategies remains unclear. Few studies have investigated the ability of males to discern female reproductive status under natural conditions, and none has taken into account differences in male rank, and thus ability to gain access to females or cues. We tested male assessment of a female's fertile phase under natural conditions in longtailed macaques. We used timing of mate guarding by dominant males and the response of subordinate males towards the repeated playback of a female copulation call to measure male interest in females throughout the ovarian cycle. Relating the degree of male interest to female reproductive status, as determined noninvasively by faecal hormone analysis, we found that interest in females shown by both dominant and subordinate males was strongest during and around the fertile phase. Our results also indicate that males were better able to recognize the fertile period in conception than in nonconception cycles. Furthermore, our finding of a strong positive relation between male interest and female oestrogen levels in all cycles indicates that at least some of the cues used by males to assess female reproductive status are oestrogen related.     

Menstrual cycle patterns of hormones and sexual behavior in gorillas

Oppositely sexed pairs of gorillas were tested behaviorally during the menstrual cycle to determine the relationship between hormone concentrations of the female and the frequency of sexual activity by the pair. Five females were tested individually during two cycles with each of two males, but serum samples for hormone assay were obtained from each female only during the first cycle of testing. There was no clear relationship between hormones and behavior for the single cycle in which the serum samples were obtained, with the exception that no copulations occurred after the early luteal phase, when progesterone was greater than 5 ng/ml. Normalized behavioral data from all four test cycles for all pairs suggested that female-solicited copulations were restricted primarily to the periovulatory period. Male sexual initiative (by one of the males) accounted for most copulations temporally dissociated from the periovulatory period. Normalized hormone data for all of the females suggested that (1) attractivity was associated with estradiol concentrations during the follicular phase, (2) proceptivity with estradiol and testosterone at midcycle, whereas (3) receptivity was not associated with hormone patterns or cycle phase. The data suggest that hormones are one of several variables that contribute to the regulation of sexual behavior in gorillas.     

Do male paternity guards ensure female fidelity in a duetting fairy-wren?

Most socially monogamous bird species engage in extra-pair mating,and consequently males may adopt various behavioral strategiesto guard paternity. However, the relationship between mate guardingand extra-pair paternity is unclear: low levels of extra-pairpaternity can be associated either with no mate guarding orwith intense mate guarding. We investigate paternity guardsin the purple-crowned fairy-wren (Malurus coronatus), a duettingspecies where extra-pair paternity is rare. This species isunusual in a genus known for extremely high levels of extra-pairmating. We examine the behavioral interactions between the sexesunderlying these low rates of extra-pair paternity and showthat male purple-crowned fairy-wrens do not use frequent copulationor courtship feeding to assure paternity or guard females acousticallyby duetting. Males maintain close proximity to females bothwhen they are fertile and when they are not breeding and donot invest in courtship displays to extra-pair females. Consistentwith predictions of theoretical models, low extra-pair paternityin this species may be related to female fidelity rather thanmale paternity assurance strategies, but short-term removalof males would be necessary to test this experimentally.     

A Comparison of Female Mating Strategies in <Emphasis Type="Italic">Pan troglodytes</Emphasis> and <Emphasis Type="Italic">Pongo</Emphasis> spp.

Orangutans and chimpanzees differ in many aspects of their mating and social systems. Nevertheless, because both great apes require enormous maternal investment in offspring and because female reproductive potential is limited, female orangutans and chimpanzees should be selective of their mates, yet expected to exhibit anti-infanticide strategies such as mating with multiple males. We review and compare mating patterns in orangutans and chimpanzees to understand how these critical pressures are filtered through the different demands of the socioecology of each species. We highlight the variation in female mating behavior as a function of the proximity of ovulation. We conclude that both genera pursue tactics for paternity confusion by mating with multiple males and by mating cooperatively or even proceptively with nonpreferred partners when conception is unlikely. Mating selectivity is suggested by variation in proceptive behavior toward particular partners and by increased resistance of nonpreferred partners during the periovulatory period. Thus, data for both species support a mixed mating strategy whereby females shift their mating behavior in accordance with ovulatory status to accommodate the competing demands of mate selectivity and paternity confusion.     

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.     

Estrous asynchrony causes low birth rates in wild female chimpanzees

Estrous cycle asynchrony likely functions to elevate individual females' sexual attractiveness during female mate choice. Female chimpanzees show physiological estrus as anogenital swelling. Copulations are concentrated during the period of maximal tumescence, which is called the estrous period. A group of female chimpanzees in Mahale Mountains National Park, Tanzania, was shown to display asynchrony in both maximal tumescence and periovulatory periods. We tested the hypothesis that females establish asynchronous maximal tumescence or periovulatory periods with respect to other females to increase copulation frequency and birth opportunities (Hypothesis 1). We analyzed differences in birth rates between four asynchronous years and five nonasynchronous years. Counter to Hypothesis 1, females in periovulatory periods during asynchronous years showed significantly lower birth rates than those in nonasynchronous years. In addition, periovulatory females copulated more frequently on days on which no other female in a periovulatory period was present. These results suggest that birth rates tend to decrease when females experience nonoverlapping ovulation cycles, although copulation frequency is high. Such a decrease in the birth rate may have resulted from the cost associated with multiple copulations. We tested two other hypotheses: paternity confusion (Hypothesis 2) and sperm competition (Hypothesis 3). Both of these hypotheses were partially supported. The highest‐ranking male most effectively monopolized access to receptive females when relatively few other males and receptive females from the party (or subgroup) were present. The viability of Hypotheses 2 and 3 requires that dominant males are able to hinder a female from mating with other males. Given that the male‐biased operational sex ratio created by female asynchrony is likely to reduce the efficiency of mate guarding by dominant males, an asynchronous female may gain a fitness benefit by increasing the probability of mating with at least one male who produces superior sperm. Am. J. Primatol. 73:180–188, 2011. © 2010 Wiley‐Liss, Inc.