Energetics at the urban edge: Environmental and individual predictors of urinary C-peptide levels in wild chacma baboons (Papio ursinus)

Fürtbauer, Ines; Christensen, Christa Lykke; Bracken, Anna M.; O’Riain, M. Justin; Heistermann, Michael; King, Andrew J.

doi:10.1016/j.yhbeh.2020.104846

Cited by 14 publications

(31 citation statements)

References 95 publications

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“…Levels of uCP were the highest during gestation, especially in late gestation, in line with results in other primate species (bonobos (Pan paniscus): Nurmi et al 2018; chacma baboons (Papio ursinus): Fürtbauer et al 2020). Elevated uCP levels during gestation can reflect maternal insulin resistance induced by a shift in maternal energy metabolism from carbohydrate to lipid oxidation (Cianni et al 2003).…”

Section: Gestationsupporting

confidence: 81%

“…uCP levels in early lactating females were unexpectedly similar to NGNL females (as found in Grueter et al 2014;Cano-Huertes et al 2017;Bergstrom et al 2020;Fürtbauer et al 2020), suggesting that females of these two reproductive stages-who have similar energy intake and a carbohydrate-rich diet-have similar energy balance, although early lactating females have substantial energy expenses. Some studies have shown that even under favorable nutritional conditions, uCP levels still decrease in situations of high energy expenditure requiring a rapid and immediate energy supply, such as in a period of infection or mating (Emery Thompson et al 2009;Higham et al 2011b).…”

Section: Lactationmentioning

confidence: 53%

“…Frozen samples were thawed at room temperature and we assessed urinary C-peptide of insulin (uCP) via enzyme immunoassay using a commercial C-Peptide ELISA kit from IBL International GmbH Hamburg, Germany (RE 53,011), which has been validated and used successfully for uCP measurements in other macaques (Girard-Buttoz et al 2011Higham et al 2011a, b), as well as baboons (Fürtbauer et al 2020).…”

Section: Urinary C-peptide Analysismentioning

confidence: 99%

“…The energetic costs of female reproduction are reflected physiologically and can be assessed from concentrations of urinary C-peptide of insulin (uCP), a non-invasive marker of energy balance in primates (Sherry and Ellison 2007;Deschner et al 2008;Emery et al 2008;Girard-Buttoz et al 2011;Fürtbauer et al 2020). The C-peptide originates from the pancreas where it is cleaved from the inactive proinsulin and released into the bloodstream together with active insulin.…”

Section: Introductionmentioning

confidence: 99%

“…Thus, measuring C-peptide concentration in urine provides an indirect assessment of insulin production (Melani et al 1970;Meistas et al 1982). The few studies linking uCP and female reproduction in primates found uCP levels to be unchanged across the reproductive cycle (Grueter et al 2014;Bergstrom et al 2020), higher during gestation (McCabe and Emery Thompson 2013;Nurmi et al 2018;Fürtbauer et al 2020), or lower during lactation (Ellison and Valeggia 2003;Emery Thompson et al 2012). Female energy balance, therefore, seems to be affected differentially by reproductive states across species.…”

Section: Introductionmentioning

confidence: 99%

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The effect of reproductive state on activity budget, feeding behavior, and urinary C-peptide levels in wild female Assamese macaques

Touitou

Heistermann

Schülke

et al. 2021

Behav Ecol Sociobiol

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The source of maternal energy supporting reproduction (i.e., stored or incoming) is an important factor determining different breeding strategies (capital, income or mixed) in female mammals. Key periods of energy storage and allocation might induce behavioral and physiological shifts in females, and investigating their distribution throughout reproduction helps in determining vulnerable phases shaping female reproductive success. Here, we examined the effects of reproductive state on activity budget, feeding behavior, and urinary C-peptide (uCP) levels, a physiological marker of energy balance, in 43 wild female Assamese macaques (Macaca assamensis). Over a 13-month study period, we collected 96,266 instantaneous records of activity and 905 urine samples. We found that early lactating females and non-gestating–non-lactating females follow an energy-saving strategy consisting of resting more at the expense of feeding and consuming mostly fruits which contributed to enhancing their energy intake and feeding efficiency. We found an opposite pattern in gestating and late lactating females who feed more at the expense of resting and consume mostly seeds, providing a fiber-rich diet. Storing food into cheek pouches increased throughout gestation while it decreased all along with lactation. Lastly, we found the highest uCP levels during late gestation. Our results reflect different feeding adaptations in response to the energetic costs of reproduction and suggest a critical role of fat accumulation before conception and metabolizing fat during gestation and lactation. Overall, our study provides an integrative picture of the energetics of reproduction in a seasonal species and contributes to our understanding of the diversity of behavioral and physiological adaptations shaping female reproductive success. Significance statement To offset their substantial energetic investment in reproduction, mammalian females may modify their behavior and the way they extract energy from their environment. In addition, as a result of heightened energy expenditure, female reproduction might trigger physiological shifts. To date, most studies investigated the energetic costs of female reproduction using either a behavioral or a physiological approach. To arrive at a more comprehensive picture, we combined behavioral data with a physiological marker of energy balance, i.e., urinary C-peptide, in a seasonal primate species in its natural habitat. Our results indicate that throughout the reproductive cycle, behavioral and physiological adaptations operate concomitantly, inducing modifications in female activity budget, feeding behavior, and suggesting shifts in fat use. Overall, our results illustrate the relevance of combining data on behavior and hormones to investigate breeding strategies in coping with the energetic costs of reproduction.

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Section: Gestationsupporting

confidence: 81%

Section: Lactationmentioning

confidence: 53%

Section: Urinary C-peptide Analysismentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The effect of reproductive state on activity budget, feeding behavior, and urinary C-peptide levels in wild female Assamese macaques

Touitou

Heistermann

Schülke

et al. 2021

Behav Ecol Sociobiol

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Minimally invasive biomarkers in human and non‐human primate evolutionary biology: Tools for understanding variation and adaptation

Urlacher

Kim

Luan

et al. 2022

American J Hum Biol

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Background: The use of minimally invasive biomarkers (MIBsphysiological biomarkers obtained from minimally invasive sample types) has expanded rapidly in science and medicine over the past several decades. The MIB approach is a methodological strength in the field of human and non-human primate evolutionary biology (HEB). Among humans and our closest relatives, MIBs provide unique opportunities to document phenotypic variation and to operationalize evolutionary hypotheses.Aims: This paper overviews the use of MIBs in HEB. Our objectives are to (1) highlight key research topics which successfully implement MIBs,(2) identify promising yet under-investigated areas of MIB application, and(3) discuss current challenges in MIB research, with suggestions for advancing the field.

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Urinary C‐peptide and total triiodothyronine as energetic biomarkers for studies of lemurs

Beeby,

Baden,

Higham

2023

American J Primatol

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Measuring energy balance and energy metabolism can provide crucial information for understanding the ecological and behavioral drivers of an animal's energetic and physiological condition. Both urinary C‐peptide (uCP) of insulin and urinary total triiodothyronine (uTT3) have been validated as noninvasive biomarkers of energy balance and metabolic activity in haplorrhine primates. This study attempts to validate uCP and uTT3 measures in strepsirrhines, a phylogenetically distinct primate clade, using the ruffed lemur (genus Varecia) as a model. We experimentally manipulated the diet of captive black‐and‐white (Varecia variegata) and red (Varecia rubra) ruffed lemurs at Duke Lemur Center across a 4‐week period. We collected urine samples from subjects (n = 5) each day during 1 week of control diet, 2 weeks of calorie‐restricted diet and 1 week of refeeding, designed to temporarily reduce energy balance and metabolism. We also tested the outcome of filter paper as a storage method by comparing to controls (frozen at −20°C) to assess its suitability for studies of wild populations. We successfully measured uCP and uTT3 levels in frozen urine samples using commercial enzyme immunoassay kits and found that both biomarkers were excreted at lower concentrations (C‐peptide: 1.35 ng/mL, 54% reduction; TT3: 1.5 ng/mL, 37.5% reduction) during calorie‐restricted periods compared to normal diet periods. Filter paper recovery for uCP was 19%, though values were significantly positively correlated with frozen control samples. uTT3 could not be recovered at measurable concentrations using filter paper. These methods enable noninvasive measurement of energetic conditions in wild strepsirrhines and subsequent assessment of relationships between energy balance and numerous socioecological drivers in primate populations.

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Energetics at the urban edge: Environmental and individual predictors of urinary C-peptide levels in wild chacma baboons (Papio ursinus)

Cited by 14 publications

References 95 publications

The effect of reproductive state on activity budget, feeding behavior, and urinary C-peptide levels in wild female Assamese macaques

The effect of reproductive state on activity budget, feeding behavior, and urinary C-peptide levels in wild female Assamese macaques

Minimally invasive biomarkers in human and non‐human primate evolutionary biology: Tools for understanding variation and adaptation

Urinary C‐peptide and total triiodothyronine as energetic biomarkers for studies of lemurs

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