Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees

Abstract

C-peptide of insulin presents a promising new tool for behavioral ecologists that allows for regular, noninvasive assessment of energetic condition in wild animals. C-peptide is produced on an equimolar basis with insulin, thus is indicative of the body's response to available glucose and, with repeated measurement, provides a biomarker of energy balance. As yet, few studies have validated the efficacy of C-peptide for monitoring energy balance in wild animals. Here, we assess seasonal and interindividual variation in urinary C-peptide concentrations of East African chimpanzees (Pan troglodytes schweinfurthii). We assayed 519 urine samples from 13 adult male chimpanzees in the Kanyawara community of Kibale National Park, Uganda. Cpeptide levels were significantly predicted by the total amount of fruit and the amount of preferred fruit in the diet. However, chimpanzees had very low C-peptide titers during an epidemic of severe respiratory illness, despite highly favorable feeding conditions. Kanyawara males had significantly lower C-peptide levels than males at Ngogo, a nearby chimpanzee community occupying a more productive habitat. Among Kanyawara males, low-ranking males had consistently higher C-peptide levels than dominant males. While counterintuitive, this result supports previous findings of costs associated with dominance in male chimpanzees. Our preliminary investigations demonstrate that C-peptide has wide applications in field research, providing an accessible tool for evaluating seasonal and individual variation in energetic condition, as well as the costs of processes such as immune function and reproduction.

The context of female dispersal in Kanyawara chimpanzees

“…However, it is possible that the emigration patterns we observed were directly related not to dietary quality, but to a correlated variable such as the changing size or composition of social parties (Chapman et al, 1994;Hashimoto et al, 2003; Emery Thompson & Wrangham, 2006) (Anderson et al, 2006;Emery Thompson & Wrangham, 2008). While we found a strong significant pattern, we hope in the future to corroborate these data with a more sensitive measure of individual energetic condition (Emery Thompson et al, 2009). …”

“…We calculated the percentage of observations in which chimpanzees ate fruit as a proportion of all observations in which chimpanzees fed. At Kanyawara, this measure of dietary quality is significantly correlated with fruit availability estimates obtained from phenological transects (Wrangham et al, 1991(Wrangham et al, , 1996Sherry, 2002) and with biomarkers of chimpanzee energetic condition (C-peptide of insulin, Emery Thompson et al, 2009).…”

Seasonal Variation in Physiology Challenges the Notion of Chimpanzees (Pan troglodytes verus) as a Forest-Adapted Species

“…Typically used as a measure of urinary concentration (Anestis et al, 2009), we employed the byproduct creatinine as a marker of an individual's hydration status. C-peptide, a peptide of insulin and therefore indicative of an individual's metabolic status, has recently been demonstrated to be a suitable biomarker for monitoring energetic status, especially in non-invasive studies of wild primates (Sherry and Ellison, 2007;Emery Thompson and Knott, 2008;Emery Thompson et al, 2009, 2016GirardButtoz et al, 2011;McCabe et al, 2013;Grueter et al, 2014;Surbeck et al, 2015). Lastly, although cortisol variation is a nonspecific measure of general physiological stress (Beehner and Bergman, 2017), we mirror other vertebrate research (Christison and Johnson, 1972;El-Halawani et al, 1973;Edens and Siegel, 1975;Harikai et al, 2003;Beehner and Bergman, 2017;Wessling et al, 2018), which has linked cortisol response to thermal challenges.…”

Faster reproductive rates trade off against offspring growth in wild chimpanzees

“…39). C-peptide is a well-validated marker of energy balance in primates (55)(56)(57)(58)(59). In lactating mothers, it is a useful tool to assess the metabolic load of milk production relative to the total energy budget (39,55,60).…”