Inter‐individual variation in weaning among rhesus macaques (Macaca mulatta): Serum stable isotope indicators of suckling duration and lactation

Abstract

Weaning is a transition in early development with major implications for infant survival and well-being, and for maternal lifetime reproductive success. The particular strategy a primate mother adopts in rearing her offspring represents a negotiation between her ability to invest and her need to invest, and can be considered adaptive and influenced by biological and social factors. Any investigation into how and why maternal weaning strategies differ among non-human primates is limited by the precision of the measurement tool used to assess infants' weaning ages. Stable carbon and nitrogen isotope analysis of soft tissues (e.g., hair, nails, feces, urine, blood) offers an objective means of monitoring the weaning status of infants. In this study, we assess stable isotope ratios in blood serum from 14 captive rhesus macaque dyads (Macaca mulatta) at infant ages 2, 5, 6, 7, 8, and 10 months to estimate the timing of weaning events. Male infants wean earlier than female infants. Infants with the lowest birth weights wean latest. Most infants wean upon reaching 2.5 times their birth weights, sooner than when weaning elsewhere has been predicted for captive cercopithecine primates. The longest weaning periods (ca. 10 months) are observed among infants of small mothers. The shortest weaning period, between 2 and 5 months, was among the lowest ranking dyad. Parity and mothers' ages had no discernible effect on the timing of weaning events. The stable carbon and nitrogen isotope values of dams during lactation are significantly different than those of a non-lactating adult female outgroup, raising questions about the suitability and selection of adult comparative baselines in studies where lactating mothers cannot be sampled longitudinally (e.g., bioarchaeology; paleontology). Am. J. Primatol. 78:1113-1134, 2016. © 2015 Wiley Periodicals, Inc.

Age at reproductive debut: Developmental predictors and consequences for lactation, infant mass, and subsequent reproduction in rhesus macaques (Macaca mulatta)

“…More recent studies revealed that sustained positive energy balance influences resumption of estrous (baboon: Rosetta et al, 2011; chimpanzee: Emery Thompson et al, 2012; human: Valeggia and Ellison, 2009). The better ability of typical breeders to provide higher AME likely supported faster infant growth (Hinde et al, 2009) and earlier attainment of weaning thresholds (Lee et al, 1991; Lee, 1996; Reitsema et al 2015). These factors, combined with the peak timing of parturition, afforded typical breeders the capacity for somatic recovery to conceive during the subsequent breeding season.…”

A novel fecal stable isotope approach to determine the timing of age‐related feeding transitions in wild infant chimpanzees

“…Stable carbon and nitrogen isotope analyses of keratin, collagen, blood, urine, and feces have been used to assess the diets of primates in the wild and in captivity (e.g., Gorilla beringei : Blumenthal, Chritz, Rothman, & Cerling, ; Papio ursinus : Codron et al, ; Lemur catta : Loudon, Sponheimer, Sauther, & Cuozzo, ; Pan paniscus : Oelze et al, ; Pan troglodytes : Loudon, Sandberg, Wrangham, Fahey, & Sponheimer, ; Schoeninger, Moore, & Sept, ; Schoeninger, Most, Moore, & Somerville, ). Numerous human studies, particularly those using bone collagen from the archaeological record, and several nonhuman primate studies have used stable carbon and nitrogen isotopes to assess the diets of infants and estimate weaning status (e.g., humans: Fogel, Tuross, & Owsley, ; Fuller, Fuller, Harris, & Hedges, ; Herring, Saunders, & Katzenberg, ; Katzenberg, Herring, & Saunders, ; Katzenberg & Pfeiffer, ; Katzenberg, Saunders, & Fitzgerald, ; Richards, Mays, & Fuller, ; Tsutaya & Yoneda, ; Waters‐Rist, Bazaliiskii, Weber, & Katzenberg, ; nonhuman primates: Fahy et al, ; Humphrey, Dirks, Dean, & Jeffries, ; Oelze, ; Reitsema, ; Reitsema & Muir, ; Reitsema, Partrick, & Muir, ). Stable isotopes in feces were used in only one primate study to track the diet of a captive langur infant (Reitsema, ).…”

Alloparenting is associated with reduced maternal lactation effort and faster weaning in wild chimpanzees

“…Inter-individual variation in weaning age occurs at Ngogo [46], as in other mammals (e.g. primates: mountain gorillas, Gorilla beringei beringei  [63]; humans, H. sapiens  [64,65]; rhesus macaques, M. mulatta  [51]; eastern chimpanzees, P. t. schweinfurthii  [52]; non-primates: northern fur seals, Ca. ursinus ; California sea lions, Z. californianus  [48]; beluga whales, D. leucas  [49]; Steller sea lions, E. jubatus  [50]).…”