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

Abstract

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 alpha 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 alpha 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.

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

“…This is a similar situation to that found in populations where female breeding is highly a seasonal (e.g., crested macaques: Engelhardt et al unpublished data) or where group sizes are small (e.g., West African olive baboons: Higham et al, 2009b). Moreover, we might expect that the strength of male-male competition should be stronger in captivity than in free-ranging conditions [see Garcia et al, 2009], with dominant males being better able to monopolize fertile females under captive conditions, especially because captivity might not allow many sneak copulations for subordinate males. We should therefore have expected an increase in the monopolization of fertile females by the dominant male in this captive context.…”

“…Males tended to bias their sexual behaviors toward high-ranking females [Garcia et al, 2009;Muller et al, 2006;Proctor et al, 2011;Zumpe and Michael, 1996], suggesting that female mating success was dominance-rank related. As visual, auditory and olfactory cues were not found to convey information about female characteristics, we suggest that males could use behavioral cues to discriminate among females based on rank differences.…”

“…likely [Daspre et al, 2009;Deschner et al, 2004;Engelhardt et al, 2004;Garcia et al, 2009;Gesquiere et al, 2007;Higham et al, 2009a;Thompson and Wrangham, 2008] suggesting that they are able to make mating decisions based on the discrimination of fertility differences within female reproductive cycles. However, the signals and cues available to males for their mating decisions, and the relative reliability of these, are still poorly understood.…”

“…They are predicted to discriminate in mating decisions based on fertility differences between females (if fertility changes with reproductive history or social parameters such as age and social rank, for instance), with males biasing their sexual behaviors particularly towards highranking and older females [Garcia et al, 2009;Muller et al, 2006;Proctor et al, 2011]. Discriminating between high/low rank females or aged/young females may, however, only be relevant when both types of females are simultaneously available.…”

“…Female behavior has been related to the timing of ovulation in some species [e.g., humans: Bullivant et al, 2004;capuchins: Carosi and Visalberghi, 2002;long-tailed macaques: Engelhardt et al, 2005], although such relationships may not be universal [e.g., Barbary macaques: Brauch et al, 2007; Japanese macaques : Garcia et al, 2009;olive baboons: Higham et al, 2009a]. In primate species with a conspicuous sexual swelling whose size is correlated with the underlying probability of ovulation, such as baboons [Daspre et al, 2009;Gesquiere et al, 2007;Higham et al, 2008a], female proceptive behavior can be predicted to be more weakly linked to ovarian cycle stage.…”