Comparison of behavioral sequence of copulation between chimpanzees and bonobos

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.     

Do bonobos copulate more frequently and promiscuously than chimpanzees?

The copulatory activities of bonobos (Pan paniscus) of Wamba, Zaire, were compared with those of chimpanzees (P. troglodytes schweinfurthii) of Mahale, Tanzania. The copulation rates of adult male bonobos were equal to or lower than those of adult male chimpanzees. The copulation rates of adult female bonobos were approximately equal to those of adult female chimpanzees who were in maximal genital swelling, but it should be much higher than those of the adult female chimpanzees throughout the birth interval. The copulation rates of adolescent male bonobos were lower than those of adolescent male chimpanzees, whereas the copulation rates of adolescent female bonobos were much higher than those of adolescent female chimpanzees. It was suggested that the bonobos of Wamba did not copulate more promiscuously than did the chimpanzees of Mahale. The female bonobos may show “receptivity”, whereas female chimpanzees may show rather “proceptivity”.     

Plasticity in courtship and sneaking behaviors depending on tail length in the male guppy, <Emphasis Type="Italic">Poecilia reticulata</Emphasis>

Male guppies Poecilia reticulata exhibit two types of mating behavior, i.e., courtship displays for cooperative copulation and sneaking attempts for forced copulation. The frequencies of the two male mating behaviors are influenced by tail length. Males possessing long tails exhibit courtship displays less frequently and sneaking attempts more frequently than those possessing short tails, even though they have similar total lengths. To examine whether these male behavioral tendencies depending on tail length are genetically controlled or are determined by tail length per se, tail length manipulation was conducted. The tail lengths of males that had previously possessed longer tails were surgically shortened to a greater degree than those of their counterparts that had previously possessed shorter tails. Although the frequencies of the mating behaviors exhibited by the latter males did not apparently change, the former males clearly increased the frequency of courtship displays and decreased that of sneaking attempts following tail shortening. These results indicate that males adjust the frequencies of the two mating behaviors according to their tail length. Since females avoid cooperative mating with males possessing long tails, the change in mating behavioral patterns by males depending on their tail length may increase their mating opportunities.     

Female reproductive cycles and the sexual behavior of moor macaques (Macaca maurus) in their natural habitat,South Sulawesi,Indonesia

The female reproductive cycles and sexual behavior of moor macaques (Macaca maurus) were studied in their natural habitat. Female moor macaques showed repeated perineal swelling. The average cycle length was 36.2 days and the mean duration of swelling was 11.9 days. The estimated duration of gestation in two observed cases was 175 and 176 days, respectively. Females did not exhibit post-conception sexual swelling. Males appeared to ejaculate in multi-mounts. Serial mounting by the alpha male was concentrated on swelling females, while second- and third-ranking males sometimes mounted non-swelling females in series.     

Female bonobos use copulation calls as social signals

During mating events, females of many primate species produce loud and distinct vocalizations known as 'copulation calls'. The adaptive significance of these signals is considered to be in promoting the caller's direct reproductive success. Here, we investigated copulation calling in bonobos (Pan paniscus), a species in which females produce these vocalizations during sexual interactions with partners of both sexes. Females were more likely to call when mating with males than with females. We also observed a positive relationship between the likelihood of calling and partner rank, regardless of partner sex. Sexual activity generally increased with swelling size (an indicator of reproductive state) and, during their peak swelling, females called more with male than with female partners. Female bonobos are unusual among the non-human primates in terms of their heightened socio-sexuality. Our results suggest that in this species, copulation calls have undergone an evolutionary transition from a purely reproductive to a more general social function, reflecting the intrinsic evolutionary links between vocal behaviour and social cognition.     

Female sexual behavior, but not sex skin swelling, reliably indicates the timing of the fertile phase in wild long-tailed macaques (Macaca fascicularis)

The extent to which catharrine primate males are able to discern the fertile phase during the female ovarian cycle under natural conditions is still debated. In a recent study, we showed that wild male long-tailed macaques are able to detect the fertile phase, but the cues males used to assess female reproductive status remained unclear. In the present study, we tested female sex skin swelling and specific female behaviors for their reliability in signaling the fertile phase, as determined by measurement of fecal estrogens (E) and progestogens (P) during nine ovulatory cycles in seven free-ranging females. We found that changes in sex skin swellings showed a significant positive correlation to the E/P ratio, but swelling size did not significantly differ between cycle phases. In contrast, the frequency of two of the tested female behaviors, namely initiation of sexual interactions and reaching back for the male during copulation, was not only correlated with female reproductive hormones, but was significantly elevated during the fertile phase compared to nonfertile phases of the cycle. We thus conclude that female sex skin swelling does not reliably indicate the timing of the fertile phase in long-tailed macaques, whereas certain female behaviors do. Since cycles differed considerably in the number of males with which females had sexual interactions as well as in the number of sexual interactions with dominant males, the signaling character of these specific female behaviors appears to be robust against inconsistencies in these social variables. Female behavior might therefore play an important role in the recognition of the fertile phase by male macaques under natural conditions.     

The Structure of Bonobo Copulation Calls During Reproductive and Non‐Reproductive Sex

Copulation calls in primates are usually identified as sexually selected signals that promote the reproductive success of the caller. In this study, we investigated the acoustic structure of copulation calls in bonobos (Pan paniscus), a great ape known for its heightened socio‐sexuality. Throughout their cycles, females engage in sexual relations with both males and other females and produce copulation calls with both partners. We found that calls produced during sexual interactions with male and female partners could not be reliably distinguished in terms of their acoustic structure, despite major differences in mating behaviour and social context. Call structure was equally unaffected by the size of a female’s sexual swelling and by the rank of her mating partner. Rank of the partner did affect call delivery although only with male, but not female partners. The only strong effect on call structure was because of caller identity, suggesting that these signals primarily function to broadcast individual identity during sexual interactions. This primarily social use of an evolved reproductive signal is consistent with a broader trend seen in this species, namely a transition of sexual behaviour to social functions.     

Context and Development of Sexual Behavior of Wild Bonobos (Pan paniscus) at Wamba, Zaire

I studied sexual behavior of immature bonobos (Pan paniscus) in a wild group living at Wamba, Zaire, with special reference to its development. Even immature individuals under 1 year old performed sexual behavior. Sexual behavior occurred in almost all age–sex combinations, except between immature and mature females. Based on analyses of behavioral pattern and context, I classified sexual behavior involving immature individuals into three categories. (1) Genital contact between immature individuals was observed during play, and was performed by males more frequently than by females. This sexual behavior shared many traits with that of other great apes. (2) Copulation-like genital contact was observed between immature males and mature females. Its frequency increased with the immature male's age; it developed into copulation in adulthood. (3) Genital contact used to regulate interindividual relationships. This behavior, which is unique to bonobos, was absent among infants. It developed between late juvenile and early adolescent periods in association with changes in social circumstances.     

Male mating strategies and reproductive constraints in a group of wild tufted capuchin monkeys (Cebus apella nigritus)

Tufted capuchin monkeys (Cebus apella) provide an extreme example of active female sexual solicitation of males. In spite of being targeted by females for sex, males may delay copulation for hours or days. Data were collected on the sexual interactions in one wild capuchin group at the Estação Biológica de Caratinga in Brazil from September 1996 to August 1997. All successful conceptions during this year occurred in the dry season, yet sexual behavior was observed during 9 months of the year. This study tested whether male sexual response to female proceptivity was seasonally‐mediated. Male consortship participation, solicitation of females, latency to copulation, and copulation frequency were compared between fertile and nonconceptive females. Seasonal patterns in copulation interference, mating style, and alternative mating strategies were also examined. Thirty‐two copulations were observed. The alpha male was solicited for significantly more consortship days per female, but his mating success, in terms of copulation frequency, did not differ from that of two other adult males in the group. In the dry season, when the females were fertile, the males showed increased contest competition for mates, a higher frequency of alternative mating strategies against copulation interference, and increased monitoring of the females' condition. However, contrary to expectations, the alpha male's latency to copulation was significantly longer in the fertile season than in the nonconceptive months, and no males were observed to mate more than one time per day, even at the conceptive peak. Male mating strategies were affected by both season and rank, and there was evidence for reproductive constraints on males throughout the year. Limited male ejaculatory capacity and male choice in the timing of copulations within female proceptive phases may both be important factors in driving the sexual dynamics of this species. Am. J. Primatol. 67:313–328, 2005. © 2005 Wiley‐Liss, Inc.     

Nonconceptive Sexual Behavior in Bonobos and Capuchins

Sexual behavior by infecundable females, and by same-sex and adult-immature dyads, occurs in wild and captive bonobos (Pan paniscus). Proposed functions of these behaviors, in social primates generally, include practice, paternity confusion, exchange, and communication as well as appeasement. We used this framework to interpret and to compare observations of sexual behavior in a captive bonobo group and a wild white-faced capuchin (Cebus capucinus) group. In both species, (a) sexual behavior was no more frequent in cycling females than in pregnant or lactating females and (b) same-sex and adult-immature dyads engaged in as much mounting or genitogenital contact as adult heterosexual dyads did. The species differed in that (a) bonobos engaged in sexual behavior 65 times as frequently as capuchins, (b) only bonobos engaged in sexual contact other than ventrodorsal mounting during focal observation, and (c) bonobo sexual contact was concentrated most heavily in socially tense situations in adult female–female dyads, whereas capuchin sexual contact was concentrated most heavily in socially tense situations in adult male–male dyads. These data and published literature indicate that (a) practice sex occurs in both species, (b) paternity confusion may be a current function of C. capucinus nonconceptive sex, (c) exchange sex remains undemonstrated in capuchins, and (d) communication sex is more important to members of the transferring sex—female bonobos and male capuchins—than to members of the philopatric sex.     

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 competition in a group of captive bonobos (Pan paniscus)

We describe the occurrence of sexual competition, expressed as harassment of sexual interactions in a captive group of bonobos. We monitored all aggressive and pestering interventions during sexual interactions of three captive adult females, one adolescent, and three adult males. The study period covered two complete menstrual cycles for each female, with continuous daily observations. There was relatively little overt sexual competition by the males, in analogy with other studies. Most male interventions occurred towards interactions with the alfa female. The alfa female performed the most intense and the highest number of interventions towards the sexual interactions of the other females. The data provide evidence for female intra-sexual competition in this female dominant species.     

Mating behaviors of the proboscis monkey (Nasalis larvatus)

The mating behaviors of the proboscis monkey were observed in a riverine forest along a tributary of the Kinabatangan River, Sabah, Malaysia, for a period of 30 months. Solicitation for copulation was initiated frequently by males and occasionally by females. Most copulations involved only one mount; however, some multiple-mount copulations were observed and a maximum of six mounts per copulation were recorded. The mean duration of mounts was about 27 sec. Nonsexual mounts (female-female, female-juvenile/infant, juvenile-juvenile, and juvenile-infant) were also observed. Female-female mounts occurred shortly after failed solicitations toward males were observed. Harassment by juveniles and/or infants was observed during copulation; however, these harassments apparently did not interfere with copulation. Sexual swelling was evident in 77.4% of copulating females, with copulating subadult females showing the most distinct swelling.     

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.     

Effects of male group size,parity, and cycle stage on female chimpanzee copulation rates at Ngogo,Kibale National Park,Uganda

Chimpanzees have complex and variable mating strategies, but most copulations occur when females with full sexual swellings are in parties with multiple males and mate with most or all of those males. Daily copulation rates for fully swollen females vary at different times of a female’s cycle, among females, and across communities and populations. Variation in female age, parity, and cycle stage underlie some of this variation, but possible demographic effects on copulation rates have not been systematically investigated. Demographic variation can affect many aspects of behavior and ecology, including the frequency and success of different mating tactics. Analysis of data from the unusually large chimpanzee community at Ngogo produces two results that are consistent with the hypothesis that demographic variation affects female copulation rates. Copulation rates were high compared with those reported from other research sites, where females had fewer potential mates available. Daily copulation rates of fully swollen females were also positively related to the number of males with whom they associated. Ngogo data also re-confirm results from other studies, of both wild and captive populations, showing that female copulation rates increase during periovulatory periods. This is consistent with the hypothesis that sexual swellings and extended receptivity and proceptivity help to protect females against infanticide by helping to ensure they mate with all potential sires. As at some other sites, parous females at Ngogo copulated at higher rates than nulliparous females. Possible effects of demography on sexual behavior should be considered in assessments of differences between chimpanzees and bonobos and of variation across chimpanzee populations.     

What Females Tell Males About Their Reproductive Status: Are Morphological and Behavioural Cues Reliable Signals of Ovulation in Bonobos (Pan paniscus)?

In many Old World primate species, female attractivity increases during the tumescent phase of the sexual swelling for a period that lasts considerably longer than oestrus‐related attractivity in other mammals. We examined the reliability of the swelling as an indicator of ovulation in captive bonobos, a species with a long and variable phase of maximum tumescence. Using a combined approach of (1) observations of sexual behaviour, (2) visual scoring of the sexual swelling and (3) analysis of faecal progestin to assess the timing of ovulation during 23 ovulatory cycles of eight adult females, we found that in 30% of these cycles the presumed day of ovulation did not fall within the period of maximum tumescence. When ovulation did occur during maximum swelling, it was more closely related to the end rather than the onset of the maximum swelling period. However, the pattern of sexual swelling was not a reliable indicator of ovulation. In addition, sexual behaviour of both sexes increased in frequency with the degree of the swelling but not around the time of ovulation. We conclude that swellings in bonobos provide honest information on the probability of ovulation, but not its exact timing, and that therefore the `obvious ovulation'‐hypothesis cannot explain the function of sexual swellings in bonobos.     

Female Goldeneye Ducks (Bucephala clangula) Do Not Discriminate among Male Precopulatory Display Patterns

Female goldeneyes remain motionless on the surface of the water while single males circle them performing a series of highly stereotyped displays. After performing between eight and 90 of these displays the male either copulates or attempts to copulate with the female. However, females allow only 58% of males to mount them, while rejecting 42%. We have examined 804 of these precopulatory sequences containing 11,841 actions in an effort to determine why females find some display sequences of males unsuitable, while others are accepted. Males have an extraordinarily varied sequence of actions, and sequence variation leading to successful and unsuccessful copulation attempts was similar. Most surprising was the tendency of males to eliminate one of the five actions, whether in successful or unsuccessful attempts. As unlikely as we think it might be as the result of natural selection, the only statistically significant difference we found between successful and unsuccessful attempts was the reduction in the frequency of expression of one or more of the behaviors in successful attempts. These observations, coupled with the large variation seen in most sequences, suggest that there is not a correct sequence, or even a correct set of actions leading to copulation. The male must, however, perform goldeneye species-specific precopulatory behavior as performed by adult males, although it apparently can be performed in a wide variety of patterns.     

A comparison of the mating behavior of adolescent and adult female rhesus macaques (Macaca mulatta)

This study compares adult and adolescent female rhesus macaques with regard to (1) characteristics of their copulatory partners, (2) their proceptive behaviors, and (3) adult male behaviors toward them during estrus. We conducted focal follows of 24 adolescent and 65 adult free-ranging estrous female rhesus macaques on Cayo Santiago during two mating seasons. Compared to adult females, adolescents presented sexually to males at higher rates; copulated more frequently with rankless young male, and extra-group males; and, in one of two mating seasons, were ignored more frequently by males to whom they presented sexually. Adolescents tended to copulate with ranked, resident males at higher frequencies on days when the operational sex ratio (adult males:estrous adult females) was high. Males directed “muzzle-up” signals to adolescents at lower rates than to adults in one of two mating seasons, although this effect vanished when males who might have fathered adolescent females were excluded from analysis. Adolescents did not differ consistently from adults in strength of the correlation between proximity maintenance (dyadic Hinde's Index) and copulation rate, or in approach rate to males. Adolescent females, relative to adult females, presented sexually more to rankless young males, but did not present more to ranked, resident males. Both proximate (e.g. endocrine) and ultimate (e.g. differential fecundity; female-female mate competition) explanations may account for the reported differences between adult and adolescent female rhesus macaque sexuality.     

Social and menstrual cycle phase influences on the behavior of group-housed Cebus apella

This study examined sexual and other social behavior in relation to menstrual cycle phase in four mixed-sex social groups of Cebus apella. Groups consisted of two adult males and either six or nine adult females. Menstrual cycles of high (rank 1–2) and low (rank 3–7) dominance-rank females from each group were monitored via vaginal swabs, and correlated with data collected from ongoing behavioral observations. Only cycles bounded by positive detection of menstrual blood were included in this analysis (n = 15 females, 182 cycles; mean ± s.d., cycle length = 20.8 ± 1.2 days). Rates of copulation and female solicitation of males varied significantly with cycle phase, with highest rates at midcycle. While total rates of solicitation and copulation did not vary with female dominance rank, copulation rates with the dominant male were significantly greater for high ranking females than for low ranking ones. Variance observed in affiliative and agonistic behaviors, including those with males, was attributable to female rank rather than cycle phase. Females and males were also observed attempting to interfere with copulations of lower ranking same-sex individuals. Although further study, particularly of wild populations, is needed, these results indicate that female-female reproductive competition should be included as a component of the capuchin breeding system. As in other primate species, both social and hormone-related factors influence the sexual behavior of Cebus apella. © 1995 Wiley-Liss, Inc.     

The effects of sexual experience and female receptivity on courtship-rape decisions in male guppies, Poecilia reticulata (Pisces: Poeciliidae)

This paper examines the effects of prior sexual experience and of female receptivity on the probability that male guppies will court females with high or low intensity displays or attempt rape. There were no differences in behaviour between males with a history of high copulation success and those with low copulation success. Males with receptive females exhibited higher levels of high intensity displays and fewer rape attempts than males with unreceptive females, regardless of prior experience. The results are discussed in terms of sexual selection and the selective advantage of behavioural plasticity in which different sexual behaviour patterns are chosen with respect to the probability of a successful mating at a given time.