Discovery of a secular trend in Cayo Santiago macaque reproduction

Abstract

Reproductive synchrony and the consequent clustering of births are hypothesized to be regulated by seasonal changes in rainfall and food availability. Such climate-related seasonality is, however, questionable in tropical populations occupying temporally invariant habitats year round. Using the long-term data of the Cayo Santiago rhesus macaques from 1973 to 2013, this study distinguishes synchrony (a greater than chance clustering of births) from seasonality (a cluster of births during a period of the year when abiotic conditions are favorable) and shows that females are highly synchronized (>72% of births in a 3-month period) but the effects of environmental zeitgebers on reproduction are overridden by biological factors. Specifically, biotic and abiotic factors including (i) loss of immature offspring; (ii) population density; (iii) age at delivery; (iv) rainfall; and (v) changes in colony management were modeled in relation to the annual onset of births and the median birth date. Females experiencing loss of immature offspring had an interbirth interval of <365 days in average and the proportion of these females increased up to 48% due to changes in colony management overtime, although reproductive synchrony increased with increasing population density. A secular trend in both the onset of births and the median date of birth is documented and the model predicts that the median birth date will advance across all calendar-based seasons by 2050. The secular trend in reproduction appears to be triggered by changes in the age at delivery of females, the absence of physiological constraints from maternal investment due to offspring loss, shorter interbirth interval, and a higher degree of coordination due to increasing population density. This study challenges the reproductive phenology previously described for rhesus macaques highlighting the importance of long-term studies in addressing the ultimate causes of reproductive synchrony.

Keywords: Macaca mulatta; interbirth interval; lactational anovulation; reproductive phenology; seasonal reproduction; synchronization.

Fig. 1.

Temporal advance in the onset of birth season (A) and median birth date (B) of Cayo Santiago rhesus macaques from 1973 (season 1) to 2013 (season 41).

Fig. 2.

Median interbirth interval of Cayo Santiago females giving birth in consecutive years during two periods of different culling strategies; from 1973 to 1996 entire social groups were culled, 1996–2013 culling was targeted to immature individuals mostly.

Fig. 3.

Interbirth interval of Cayo Santiago females giving birth during consecutive seasons but experiencing loss of an immature offspring (death or culling) versus females with no loss of offspring.

Fig. 4.

Degree of synchrony of reproduction among Cayo Santiago females. Degree of synchrony was estimated by calculating the percentage of births during each season occurring within three months.

Fig. 5.

Predicted time of the population’s median birth date to advance a full 12-months period.