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

Abstract

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.

Metabolic strategies in wild male Barbary macaques: evidence from faecal measurement of thyroid hormone

“…In the mating season itself, increased T3 levels were linked to increases in intensity of mating activity, and to temperature and rainfall. Mating activity is highly energetically demanding in polygynous male primates [15], and Barbary macaque males mate at high rates and experience intense intra-sexual competition during the mating season [16]. An increase in BMR could therefore benefit males by increasing their aerobic capacity [17].…”

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

“…Most studies described a relation between ovarian steroids and female behaviors [Aujard et al, 1998;Engelhardt et al, 2005] or male sexual interest [Aujard et al, 1998;Engelhardt et al, 2004Engelhardt et al, , 2005Gesquiere et al, 2007;Heistermann et al, 2008;Zumpe & Michael, 1996], whereas other studies showed that there was no relationship between hormonal levels and female's proceptivity and attractivity [Brauch et al, 2007;Higham et al, 2009]. Further studies are therefore required to clarify this issue and understand the reasons why the link between sexual behaviors and hormonal levels may be lost.…”

“…Cycles in which more than one sample was missing around the significant PdG rise were excluded from analysis, and only cycles in which PdG levels remained elevated for at least 2-3 consecutive days were included in the analysis. Based on the time lag between ovulation and the postovulatory rise in fecal PdG excretion of 2-3 days in macaques [Shideler et al, 1993], we determined for each cycle a 2-day window (days-2/-3 relative to the defined rise) in which ovulation was most likely [Heistermann et al, 2008]. The periovulatory period, or fertile window, was then considered to be the time block covering these 2 days plus three preceding days to account for sperm life span in the female tract, as shown by Wilcox et al [1995] in humans.…”

“…There are various cues of proceptivity and attractivity that males may use to detect female fertility status and therefore allocate their mating effort throughout a female's ovarian cycle. Given the causal relationship between estrogen peak and ovulation, several estrogen-related cues were suggested as signals conveying information on the timing of the fertile phase (see Heistermann et al, 2008 for further details). Foremost among these are female behaviors, visual cues (sexual swellings), vocalizations, and olfactory cues (sexual pheromones).…”

Multimodal Sexual Signaling and Mating Behavior in Olive Baboons (Papio anubis)

“…The periovulatory period, or fertile window, was then considered to be the time block covering the 2 days before detumescence (D0) plus the three preceding days in order to account for the life span of sperm in the female tract [humans, Wilcox et al, 1995]. The fertile phase was then defined as a period of 5 days (D-1 to D-5) [e.g., Barelli et al, 2007;Brauch et al, 2007;Engelhardt et al, 2004;Heistermann et al, 2008], the period preceding this phase (D-6 to D-10) was taken to represent the prefertile phase (5 days) while the 5 days following the fertile phase were defined as postfertile phase (D0 to Dþ4). We only used data collected during this 15-day period in analyses.…”