Perception of female reproductive state from vocal cues in a mammal species

Abstract

While acoustic signalling by males is known to a¡ect male^male competition, mate attraction and the timing of ovulation, the extent to which sexual selection has shaped the evolution of female acoustic signals is poorly understood. Among mammals, experimental evidence indicates that females attract mating partners by using olfactory and visual signals to advertise their reproductive state. Whether or not males ascertain female reproductive state from vocal signals has, however, never been systematically tested. In this study, we use playbacks of recorded vocalizations to demonstrate that male Barbary macaques, Macaca sylvanus, can discriminate between female copulation calls given at di¡erent stages of the oestrous cycle, responding more strongly to those given around the time when conception is most likely to occur. Acoustic analysis suggests that the mean dominant frequency of call units and a number of temporal parameters could provide males with the information necessary to discern the proximity of ovulation in this way. Our results provide the ¢rst experimental evidence that the calls of female mammals may contain information on reproductive state, which males can perceive and use in such a way as to increase their reproductive success.

The evolution of female copulation calls in primates: a review and a new model

“…Swelling size did affect, however, other acoustic parameters such as the number of call units in a call, rate of call unit delivery and mean call unit duration. Using a playback experiment, Semple (1998b) showed that Barbary macaque (Macaca sylvanus) males responded more strongly to the copulation calls given near ovulation than to the calls recorded in other stages of the cycle (see also Semple and McComb 2000). Taken together, these findings suggest that females may advertise their fertility through the rate or the acoustic structure of their copulation calls.…”

“…In macaques and baboons these vocalizations attract the attention of other males, who often approach and investigate the calling female (van Noordwijk 1985;. Playback experiments conducted by Semple (1998b;Semple and McComb 2000) with Barbary macaques showed that males respond to hearing copulation calls of estrous females by looking towards the loudspeaker and approaching. Moreover, Semple (1998b) showed that females were mated more quickly following the playback of their copulation call than following the playback of a control stimulus.…”

Evidence for tactical concealment in a wild primate

“…The clear flexibility in vocal behaviour depending on distance to the leader male suggests, however, that vocalization rates do not simply decrease with a low-ranked partner or between individuals with weak social bonds (that is, the follower and unit females 35 ). Additionally, the acoustic properties of copulation calls themselves may be indicative of social status, similar to those of other primates 51,52 . Experimental work is needed to fully understand the function of copulation calls in geladas.…”

“…Male copulation calls may be a potential indicator of ejaculation 42 , but we found no indication that ejaculation was absent in silent copulations. Alternatively, both sexes' copulation calls may indicate fertility and rank 51,52 or function to strengthen the pair bond between the partners 47,53 , as they occur during-not after-mounting and ejaculation. The clear flexibility in vocal behaviour depending on distance to the leader male suggests, however, that vocalization rates do not simply decrease with a low-ranked partner or between individuals with weak social bonds (that is, the follower and unit females 35 ).…”

“…Because female primates' copulation vocalizations may vary with the phases of their oestrous cycles 51 , we attempted to control for the possible influence of reproductive state on female geladas' vocal behaviour. In the absence of complete hormonal records for all females within this dataset, we controlled for oestrous state by examining the vocal behaviour of females that mated with multiple males on any given day.…”