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

Abstract

Abstract 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.

Abstract 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.