Reproductive seasonality in two sympatric primates (Ateles belzebuth and Lagothrix lagotricha poeppigii) from Amazonian Ecuador

Abstract

With their large body size and “slow” life histories, atelin primates are thought to follow a risk‐averse breeding strategy, similar to capital breeders, in which they accumulate energy reserves in anticipation of future reproductive events such as gestation and lactation. However, given the paucity of longitudinal data from wild populations, few studies to date have been able to compare the timing of reproductive events (e.g., copulations, conceptions, and births) in relation to shifting resource availability over multiple years. We examined the reproductive patterns of two atelin species—white‐bellied spider monkeys (Ateles belzebuth) and lowland woolly monkeys (Lagothrix lagotricha poeppigii)—in relation to habitat‐wide estimates of fruit availability at the Tiputini Biodiversity Station (TBS) in Amazonian Ecuador. Our sample included 4 years of data on births (N = 36) and copulations (N = 170) for Lagothrix, 10 years of data on births (N = 35) and copulations (N = 74) for Ateles, and 7 years of data on ripe fruit availability. Reproductive events were distinctly seasonal. For both species, births were concentrated between May and September, a time period in which ripe fruit was relatively scarce, while inferred conceptions occurred between September and January, when ripe fruit availability was increasing and maintained at high‐levels throughout the forest. Interannual variation in births was relatively stable, except for in 2016 when twice as many infants were born following a strong El Niño event that may have led to unusually high levels of fruit productivity during the 2015 breeding season. Although copulations were observed year‐round, an overwhelming majority (>90% for Lagothrix and >80% for Ateles) took place between August and February when females were most likely to conceive. Collectively, these data follow the reproductive patterns observed in other atelin primates, and, as proposed by others, suggest that atelins may follow a risk‐averse breeding strategy.

Reproductive endocrinology of wild female woolly monkeys (Lagothrix lagotricha poeppigii) during puberty, ovarian cyclicity, and pregnancy

“…Vertical green lines indicate the date they were last seen ranging with other individuals in their respective focal groups (G and C). Vertical dashed black lines represent estimated ovulation dates higher number of infants were born after El Niño years, when the forest was most productive and when females were potentially in better body condition to conceive (Ellis et al, 2021). Given the potential influence of body condition on female reproduction in this population, the timing of conception relative to food availability may be a crucial factor for reproducing successfully.…”

“…Additionally, despite the fact that copulations have been observed year-round in multiple populations of several different woolly monkey subspecies (Di Fiore & Fleischer, 2005;Ellis et al, 2021;Nishimura, 2003;Stevenson, 2002), woolly monkeys display seasonality in their birthing patterns (Ellis et al, 2021), suggesting that females may still be sexually active during non-conceptive periods.…”

“…Here, we present a study of female reproductive endocrinology in wild woolly monkeys (genus Lagothrix ) living in a lowland rainforest site in the Amazon rainforest. While woolly monkey reproductive patterns have been previously described from behavioral observations in both captive (Mack & Kakfa, 1978; Mooney & Lee, 1999; Williams, 1967) and wild populations (Ellis et al, 2021; Nishimura, 2003), no study has yet examined endocrine aspects of their reproductive biology. Indeed, woolly monkeys are the only group in the family Atelidae (i.e., howler monkeys, spider monkeys, woolly monkeys, and muriquis) whose female reproductive endocrinology has not been studied (Ziegler et al, 2009).…”

“…Additionally, despite the fact that copulations have been observed year‐round in multiple populations of several different woolly monkey subspecies (Di Fiore & Fleischer, 2005; Ellis et al, 2021; Nishimura, 2003; Stevenson, 2002), woolly monkeys display seasonality in their birthing patterns (Ellis et al, 2021), suggesting that females may still be sexually active during non‐conceptive periods. Furthermore, given that female woolly monkeys lack conspicuous visual signs of ovulation (Di Fiore et al, 2011), it is challenging for researchers to determine whether observed mating patterns correspond to female fertility (e.g., in respect to either the timing of ovulation within cycles or to ovarian cycling during the mating season).…”

A 24-Year Record of Female Reproductive Dynamics in Two Sympatric Mouse Lemur Species in Northwestern Madagascar

“…The main proximate trigger of seasonal reproduction is day length (i.e., photoperiod) (Perret & Aujard, 2001). Nonetheless, some reproductive variation can be explained by changes in environmental factors, such as climate (temperature, rainfall) or resource availability, or by internal factors such as body condition and age (Brockman & van Schaik, 2005;Ellis et al, 2021;Fernandez-Duque et al, 2002;Huang et al, 2012;Savini et al, 2008;Stone & Ruivo, 2020).…”