This study provides detailed information about reproductive hormone levels–urinary E1 and Pd–the timing of ovulation, and associated swelling patterns in wild female bonobos. Assessment of sexual swelling patterns revealed that the duration of females’ MSPs was highly variable. Furthermore, there was high variability in the timing of ovulation relative to the onset of the MSP, with ovulation occurring outside of the MSP in almost one third of the ovulatory cycles. Since ovulation did not occur in an additional eight swelling cycles, ovulation occurred during the MSP in only 52.9 % of the analysed cycles. These findings resulted in a very low probability of ovulation occurring on any particular day of a female’s MSP, suggesting that the sexual swellings of wild bonobos are a poor indicator of the timing of ovulation within cycles, and do not always signal fecundity across cycles.

Female dominance rank was not found to have a significant effect on the ISI duration, the MSP duration, the occurrence of ovulation, or the timing of ovulation. Some studies suggested that lower-ranking females may experience suppressed reproductive functioning due to harassment from higher-ranking individuals [92]. If social subordination inhibits the oestrogen-induced surge in luteinising hormone, this can result in anovulatory cycles or premature termination of menstrual cycles [101]. However, aggressive interactions between females are relatively infrequent in bonobos [63, 102]. Dominant females show tolerance toward lower-ranking females, and conflicts are often resolved in non-agonistic ways without overt aggression. Additionally, since several females shared the same dominance rank in our study (Table 1), there was not a steep dominance hierarchy among the females. Access to food resources and the nutritional status of female primates can influence their reproductive hormone levels [103, 104], fecundity (e.g., [105]), and the size and duration of sexual swellings [30]. However, differences in energetic condition and access to resources may be mitigated by the tolerant nature of bonobos [106], and by reduced levels of feeding competition compared to other species [107] (but see [108]). The relationship between feeding ecology and female rank in bonobos remains an area for future investigation.

Duration of the interswelling interval (ISI) and the interovulatory interval (IOI)

The mean duration of ovarian cycles for females in this community, determined from the ISI and the IOI, is within the range previously reported for the intermenstrual interval of bonobos in captivity (\( \overline{X} \) = 33.8–49 days) [52, 57, 58, 109–111] and in the wild (\( \overline{X} \) = 42 days) [59]. Differences in cycle duration are likely due to variability in follicular phase duration, as has been found in other studies [52, 112], and as can be inferred from the relatively constant duration of the luteal phase found in our study. Several factors including lactation [52, 113], dominance rank [91], and age [112, 114] have been found to influence duration of the follicular phase. More specifically, mean cycle duration was significantly longer for low-ranking gelada baboons [92] and for lactating captive bonobos [53]. Although there was considerable interindividual and intraindividual variation in our study, dominance rank and reproductive state did not have a significant effect on the ISI duration. The observed variation in the ISI duration merits further investigation.

There was less variability in the IOI compared to the ISI. This suggests that ovulation may be relatively stable temporally, while the onset of the MSP, and swelling patterns in general, vary according to external influences (e.g., social or ecological factors) or due to physiological factors. For example, the consumption of plant steroids can influence endogenous hormone levels [115] and resulted in the suppression of sexual swellings in wild baboons [116]. In other studies, elevated cortisol levels were linked to extended cycle lengths [117] and reproductive suppression [118, 119]. If the IOI remains constant across multiple cycles, variability in the timing of ovulation relative to the MSP might be caused by variability in the onset and duration of the MSP. Accurate assessment of this phenomenon would require the collection of multiple consecutive cycles from the same female.

High variability in the duration of the maximum swelling phase (MSP)

The mean MSP duration (\( \overline{X} \) ± SD = 10.6 ± 6.8 days) was shorter in the Luikotale community compared to wild bonobos at Wamba (\( \overline{X} \) = 14.6 days [59]) and bonobos in captivity (\( \overline{X} \) = 16.0 ± 6.8 days [53]; \( \overline{X} \) = 11.5 days [52]). This could be due in part to our conservative estimate of the MSP duration when there was a sample gap of one day at the onset or end of the MSP. Additionally, studies show that captive primates who are well-nourished and have improved nutritional condition, compared to their wild counterparts, have enhanced reproductive and hormonal functioning [104, 120]. A shorter mean duration of the MSP could be caused by fluctuations in food availability and energetic costs. These fluctuations are likely higher for bonobos in the wild, compared to bonobos in captivity or at research sites during periods when they were provisioned with food [59].

Although there was considerable variation in the MSP duration of the Luikotale bonobos (range: 1–31 days), this finding corroborates other studies of captive bonobos, MSP range: 4–26 days [52] and 3–30 days [53], as well as a study of wild bonobos which reported a MSP range of 3–22 days [59]. The variability in MSP duration for bonobos exceeds the variability found in populations of wild chimpanzees at Taï National Park, Côte d’Ivoire (\( \overline{X} \) = 10.9 days, range: 6–18 days, [16]), at Mahale (\( \overline{X} \) = 11.3 days, range: 5.0–14.0 days, [121]), and at Gombe (\( \overline{X} \) = 9.6 days, range: 7–17 days, [122]).

Consistent with Reichert et al. [53], neither female parity nor reproductive state had a significant effect on the MSP duration. This finding differs from several other species of nonhuman primates, including some populations of chimpanzees, where nulliparous females often have longer MSPs compared to parous females [95, 123]. At Luikotale, females’ MSPs generally increased in duration as time since parturition increased; however, the number of days since parturition did not have a statistically significant effect on MSP duration. Shorter MSPs following parturition could be caused by the energetic demands of lactation [124] and an associated decrease in ovarian steroid production [99]. However, some of our females had swelling cycles with prolonged MSPs while lactating. Contrary to similar studies on other species of nonhuman primates [16, 38], we found that MSP duration did not vary significantly between individuals. This may be due to the large intraindividual variability in MSP duration across different cycles of some females. High intraindividual and interindividual variability in MSP duration contribute to bonobo sexual swellings being less precise signals of ovulation, and render it difficult for male bonobos to predict the timing of ovulation.

Anovulatory swelling cycles in wild bonobos

There are only a few cases of anovulatory cycles in nonhuman primates reported in the literature [52, 125, 126]. During our study, we observed eight swelling cycles with no indication that ovulation occurred, yet females displayed sexual swellings with MSPs that resembled patterns of normal, ovulatory cycles (see Fig. 6 and Additional file 3: Table S8). Generally, changes in the size of female sexual swellings are regulated by oestradiol and progesterone [41, 43]. In the absence of a pronounced pre-ovulatory rise in oestrogen, swelling tumescence may result from changes in oestrogen and progestin receptor concentration in the sexual skin [127], in combination with small fluctuations in oestrogen and progesterone levels. In comparison to other species which do not display sexual swellings decoupled from ovulatory cycles, the receptor sensitivity and density of bonobo sexual swellings may be different, or may fluctuate in a different way in relation to hormone excretion. Furthermore, it is possible that oestrogen is metabolised at or near oestrogen receptors in target tissues, e.g., in female sexual swellings, but that this metabolism is not reflected in urinary measurements of oestrogen metabolites [128].

In addition to bonobo sexual swellings being a relatively weak intracycle signal of the fecund phase, the presence of tumescent sexual swellings when females are not ovulating exemplifies the low intercycle reliability of this signal across the interbirth interval. As reported in other studies [62, 65], females displayed maximally tumescent sexual swellings during periods of gestation. They also displayed MSPs as early as three months (this study) to eight months [62] following parturition, during which time ovulation is unlikely. These findings parallel studies that found that female primates displayed situation-dependent sexual swellings during certain events, e.g., encounters with strange males or group takeovers by a new male [47, 129]. Other researchers have proposed that sexual swellings may function as a social passport during intergroup transfer and immigration to enhance social integration of females [130–132]. Since young, nulliparous females often do not give birth for several years after immigration, it is possible that they are displaying sexual swelling cycles during this time without ovulating, or that the quality of these cycles is not sufficient for conception. Females may display maximally tumescent swellings which are decoupled from ovulation during these situations to appear receptive and attractive to males [133]. If tumescent sexual swellings are perceived to signal female fecundity and the ability to conceive, they could facilitate social interactions and integration with both males and females, e.g., mothers of potential male mating partners. Furthermore, sexual swellings decoupled from ovulation may be used in a strategic way by females with young, dependent offspring, enabling females to appear sexually attractive and receptive to males without incurring the risk of conceiving. Given these potential social functions of sexual swellings, it is possible that sexual swellings during periods of low or zero fecundity may not have been selected against, as they might facilitate female immigration and social interactions.

High variability in the timing of ovulation results in low predictability of ovulation and fecundity

Previous studies spanning several species of primates (e.g., Macaca nigra, Papio cynocephalus: reviewed in [28]; Pan troglodytes spp: [16, 134, 135]) reported some variation in the temporal relation between ovulation and sexual swellings; however, ovulation almost always occurred during the second half of the MSP. A study on captive bonobos found greater variability in the timing of ovulation relative to patterns of sexual swelling; however, the variability was limited to the second half of the MSP and post-detumescence [53]. Our results from wild bonobos show even more variability in the timing of ovulation, with ovulation occurring before, after, or on almost any day of the MSP. Given that ovulation occurred during the MSP in only 52.9 % of the analysed swelling cycles, female bonobos appear to be an extreme example of variability in the timing of ovulation relative to the sexual swelling signal. If we conceptualise the signal reliability of sexual swellings as a continuum, species with swellings that reliably or accurately signal the timing of ovulation would be distributed at one end of the continuum. Our findings suggest that wild bonobos occupy a position towards the opposite end of the continuum, where sexual swellings indicate ovulation with much less reliability and accuracy than in other species.

Consequently, the day-specific probabilities of ovulation and fecundity for female bonobos were very low, especially when compared to the same probabilities in female Western chimpanzees at Taï [16] (Fig. 7b). At its highest calculated value (0.24), the probability of a female bonobo being fecund, i.e., able to conceive, was two and a half times lower than in other species of primates, e.g., Pan troglodytes verus: 0.64 [16] and Hylobates lar: 0.73 [38]. The low predictability of ovulation in wild bonobos may hinder male mate guarding of females, especially when several females display MSPs simultaneously [133, 136]. Overlap in females’ MSPs often occurs in bonobos due to the lengthy duration of the MSP within a cycle and the high number of swelling cycles within interbirth intervals of females. Reproductive synchrony and temporal overlap in female receptivity or oestrous have been found to inhibit male monopolisation potential in other species [137, 138], and may affect male mating strategies in bonobos as well.

Broader Implications

In species where the timing of ovulation within a cycle can be more accurately predicted, males may be able to mate guard and monopolise fecund females during days when they are able to conceive. In a number of primate species, mate guarding is often used as a form of indirect sexual coercion by males [139] to constrain with whom a female can mate, and thereby ensure that the mate-guarding male sires a female’s offspring. In communities of chimpanzees where ovulation usually occurs near the end of the MSP and is thus relatively predictable, some studies found high frequencies of male-male mate competition and corresponding high levels of testosterone in high-ranking males when females exhibited MSPs (e.g., [140] but see [141]).

Given the low predictability of ovulation and fecundity in wild bonobos based on sexual swelling patterns alone, males may have to attend to other cues and signals to correctly pinpoint a female’s fecund phase and time their mating efforts effectively. Chemosignals [142–144], behavioural cues [125], and vocal cues [145, 146] may play ancillary roles in signalling female fecundity in bonobos, as has been found in other species. If males are using other signals and focussing their mating efforts accordingly, this may offer one explanation as to why a high proportion of copulations are observed outside the MSP in bonobos, compared to other species [58, 60, 147]. Our results show that ovulation occurred outside the MSP in over 30 % of the ovulatory cycles we analysed. If males are able to detect ovulation by behavioural, olfactory, or other signals, this could cause males to solicit females outside the MSP and result in a weaker correlation between male solicitations and the MSP.

When ovulation is not tightly linked to the MSP, and if males are not able to discern and predict the window of fecundity in a female’s cycle using other signals, then it is more difficult and costly for a male to monopolise a female over a long period of time [148]. The costs associated with mate guarding a female throughout an extended MSP may outweigh the benefits [30]. Consequently, the high degree of uncertainty in bonobo sexual swellings may constrain or eliminate mate guarding by males. This might have resulted in male bonobos adopting alternative mating strategies to increase their mating success, e.g., deferring to females in feeding contexts, grooming females, or being perpetually willing to copulate with females. Accordingly, alternative mating strategies may lead to males investing more into affiliative relationships with females [149] rather than competing with other males for mating opportunities. In support of this theory, a recent study in this community found that high-ranking male bonobos with the highest mating success did not have elevated levels of testosterone during periods of mate competition [68]. In contrast to many communities of chimpanzees, these results suggest that male bonobos are not using intrasexual aggression to compete over potentially fecund females.

By displaying tumescent sexual swellings during extended periods of time, female bonobos may prolong the period during which they are attractive to males, and thereby increase their ability to confuse paternity [150]. Furthermore, if high costs associated with mate guarding and aggressing females lead to a decrease in these behaviours by males, females may be less constrained in expressing female mate choice compared to other species [151]. If female bonobos can manipulate male mating strategies or benefit from having sexual swellings that are less reliable and of longer duration, then one might ask why female chimpanzees do not have sexual swellings similar to those of female bonobos? The cost-of-sexual-attraction hypothesis may offer one explanation [107]. This hypothesis posits that the intensity of female sexual attractiveness, exhibited via sexual swellings, is primarily driven by levels of within-group scramble competition. If ranging in large groups and maintaining sexual swellings is costly for females due to low food availability, insufficient food between fruit trees, e.g., terrestrial herbaceous vegetation, or anthropogenic disturbances, then females might intensify their sexual attractiveness during shorter periods of time [152]. This, in turn, could lead to elevated levels of sexual coercion by males [153]. On the other hand, a low cost of grouping could lead to a lower intensity of sexual attractiveness, i.e., longer MSPs, and could increase the number of cycles per conception, resulting in a lower level of sexual coercion and more social benefits for females. Although this hypothesis seems plausible, ecological data to support it are still lacking. Empirical data pertaining to the quality and quantity of available food resources and the cost of grouping in wild bonobos will contribute to understanding how sexual swellings affect ranging and behaviour patterns in bonobos versus chimpanzees.

The extent to which male bonobos attend to female sexual swellings and use these signals to time their mating efforts and strategies remain to be investigated. Further study will assess whether there is evidence of female mate choice in wild bonobos, whether females modify their mating strategies across the ovarian cycle, and to what extent sexual swellings serve other social functions in this species.