Brief Communication: Growth Velocity and Weaning dN “Dips” During Ontogeny in Macaca mulatta

OBJECTIVES: A “dip” in the stable nitrogen isotope ratios (dN) of subadults in the late weaning/early post-weaning phase of growth and development has been observed. Speculatively, this is the mechanism of positive nitrogen balance operating among rapidly growing subadults. An alternate hypothesis for dN dips is that during weaning, subadults eat lower-N foods than adults. METHODS: This study explores the role of positive nitrogen balance in affecting dN variation of growing subadults by comparing growth velocity with stable carbon isotope (dC) and dN ratios of blood serum from captive rhesus macaques (Macaca mulatta) (n514) with controlled diets during the first 10 months of life. RESULTS: During the first six months, dN values are inversely correlated with growth in some of the anthropometrics (weight and sagittal circumference). Dips in some infants’ dN values below their mothers’ values are observed at the end of the weaning period. However, during this time frame, dN values of the infants are not correlated with anthropometric indices. Serum stable isotope ratios of lactating and non-lactating adult females differ significantly. CONCLUSIONS: Growth in body mass and size explains some of the variation in infant dN values, but are not responsible for dips in the late weaning/early post-weaning phase. It is advised that future research evaluate the extent to which growth in other body systems affects nitrogen balance and dN dips during ontogeny, and expand on isotopic differences between lactating and non-lactating females. Am J Phys Anthropol 157:347–357, 2015. VC 2015 Wiley Periodicals, Inc. Weaning is a risky period during ontogeny, during which an infant is exposed to a new pathogen environment, and is simultaneously withdrawn from the nutritional benefits of breast milk, including enhanced resistance to infection (L€onnerdal, 2003). In addition to risks posed in early childhood, weaning also is associated with a wide range of later-life health outcomes (Cunningham, 1995; Miller, 2014). Human beings mitigate the risks of weaning via cultural practices such as prolonged nursing, introducing select weaning foods intended to buffer the transition, and enlisting social support (Gray, 1996; McDade and Worthman, 1998; Piperata, 2009), as well as through biological adaptation, for example, through the deposition of fat reserves during gestation and early infancy (Kuzawa et al., 2007; Miller, 2014). Understanding the weaning process, and how humans culturally and physiologically mitigate the risks of weaning, are basic elements in understanding the success and biocultural diversity of our species. Weaning behaviors may be assessed using stable carbon and nitrogen isotope ratios (dC and dN) from osseous or soft tissues, which is possible because dC and dN values are high among breastfeeding infants and decline as weaning progresses. This decline represents a drop in an infant’s trophic position, as breast milk composes less of the infant’s diet (Fogel et al., 1989; Fuller et al., 2006; Newsome et al., 2006; Reitsema, 2012; Romek et al., 2013). In addition to reflecting diet, including breastfeeding, stable isotope ratios of consumer tissues reflect physiological states associated with pregnancy and lactation. Catabolism of endogenous tissue reserves as in wasting (Fuller et al., 2005; Hatch, 2012; Hobson et al., 1993) or as is the case for income breeders who draw off endogenous reserves to meet the reproductive demands (Hinde et al., 2009; Sare et al., 2005) and protein synthesis during fasting in anabolic states (Lee et al., 2012), leads to higher dN values in an organism’s tissues. Rapid growth and weight gain, as in pregnancy or during early post-natal infant growth, can lead to lower tissue dN values in a consumer by inducing a state of positive nitrogen balance (Fuller et al., 2004). These physiological effects are independent of dietary dN values (for a review, see Reitsema, 2013). Nitrogen balance refers to the balance between nitrogen consumed with protein, nitrogen needed and used for tissue building and maintenance, and nitrogen in excess of biological demands that is excreted as waste. The stable isotope composition (the relative abundance of the heavier isotope N and Abbreviations: dC, carbon isotope; dN, nitrogen isotope Grant sponsor: University of Georgia Joshua Laerm Award; Grant number: R21HD 075264-02; Grant sponsor: Yerkes NPRC operating support from the Office of the Director, NIH; Grant num-