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

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.

Personality as a Predictor of Time-Activity Budget in Lion-Tailed Macaques (Macaca silenus)

“…Additionally, we found that the only lactating female (Rajaja) spent most of the time resting. This is in line with previous studies that showed lactating females rest more at the cost of foraging and feeding as an energy-saving strategy [ 15 , 85 ]. However, our study only contained a single lactating female, and removing her from the sample did not significantly affect the time-activity budget, therefore conclusions should be taken with caution.…”

“…Moreover, we examined the individual variation in behavioural states using goodness of fit chi-square tests. Analyses were also run without the lactating female in the sample since lactation may impact the time-activity budget, favouring resting over foraging as an energy-saving strategy [ 15 ]. We assessed whether potential differences in the time-activity budget were due to individual variation rather than differences in reproductive state.…”

“…The existing research focused primarily on group or species-level time-activity budgets (e.g., [ 15 , 16 , 17 , 18 ]), while little information exists at the individual level. Variations in individual time-activity budgets have been reported in social species, indicating differences in fitness; however, the underlying mechanisms are still poorly understood (see [ 19 ]).…”

Growth trajectories of wild Assamese macaques (Macaca assamensis) determined from parallel laser photogrammetry

“…and the habitat comprises mainly hill and dry evergreen forest (Borries et al 2002). The study population is frugivorous with the main part of their plant diet comprising fruit, pulp, and seeds, and a considerable part of their feeding time budget devoted to slow and low intake foraging for animal matter (Schülke et al 2011;Heesen et al 2013;Touitou et al 2021a). Individuals measured for this study lived in four neighboring social groups with overlapping home-ranges.…”

“…Reproduction was seasonal with 79% of 201 births recorded between 2006 and 2019 occurring in the 3 months from April through June (Touitou et al 2021a;unpubl. data).…”