Estrogen and Progestogen Correlates of the Structure of Female Copulation Calls in Semi-Free-Ranging Barbary Macaques (Macaca sylvanus)

Abstract

Females of many Old World primates produce conspicuous vocalizations in combination with copulations. Indirect evidence exists that in Barbary macaques (Macaca sylvanus), the structure of these copulation calls is related to changes in reproductive hormone levels. However, the structure of these calls does not vary significantly around the timing of ovulation when estrogen and progestogen levels show marked changes. We here aimed to clarify this paradox by investigating how the steroid hormones estrogen and progesterone are related to changes in the acoustic structure of copulation calls. We collected data on semi-free-ranging Barbary macaques in Gibraltar and at La Forêt des Singes in Rocamadour, France. We determined estrogen and progestogen concentrations from fecal samples and combined them with a fine-grained structural analysis of female copulation calls (N = 775 calls of 11 females). Our analysis indicates a time lag of 3 d between changes in fecal hormone levels, adjusted for the excretion lag time, and in the acoustic structure of copulation calls. Specifically, we found that estrogen increased the duration and frequency of the calls, whereas progestogen had an antagonistic effect. Importantly, however, variation in acoustic variables did not track short-term changes such as the peak in estrogen occurring around the timing of ovulation. Taken together, our results help to explain why female Barbary macaque copulation calls are related to changes in hormone levels but fail to indicate the fertile phase.

Fig. 1

(a) Waveform and (b) spectrogram of a female Barbary macaque copulation call. The single units making up the call (panted grunts) are clearly visible.

Fig. 2

Representative pattern of estrogen (E_total) and progestogen (5-P-3OH) levels, and the time course of call duration (mean ± SD of the females recorded calls at a particular day) during the conception and postconception cycles of female JU (mating season 03/04). The occurrence of a value for call duration also indicates the occurrence of a copulation call on this particular day. The figure includes the 3-d time lag of the hormonal effect on copulation call occurrence and length, i.e., the acoustic data are shifted 3 d backwards.