Female reproductive energetics in mantled howler monkeys (Alouatta palliata): A follow‐up study

Abstract

Objective: Reproduction entails several challenges to primate females, among which energetic costs are remarkable at certain stages of the reproductive cycle. Still, females may use behavioral and physiological strategies to cope with those challenges. We had previously reported covariation between female energetic condition through the reproductive cycle and time-budget adjustments in mantled howler monkeys (Alouatta palliata). Accordingly, we suggested that behavioral flexibility allowed coping with the energetic challenges of reproduction. Subsequent evidence from the same population, however, suggested otherwise, so we performed a follow-up study on the variation in female reproductive energetics based on a larger sample of females. Methods: We studied 48 free-ranging adult females at Los Tuxtlas (Mexico). We assessed energy balance via urinary C-peptide concentrations (2717 urine samples), behavioral energy intake and expenditure (5728 sampling hours), and physiological energy expenditure via fecal triiodothyronine metabolites (fTH3; 3138 fecal samples). Results: We found that energy balance varied among reproductive states: (a) cycling was a period of low C-peptide concentrations; (b) the highest C-peptide concentrations occurred during gestation; and (c) the beginning of lactation marked a notable decrease in C-peptide concentrations, which then improved at mid-lactation to again decline at lactation offset. These peaks and valleys in energy balance did not seem to be associated with variation in energy acquisition but were rather mirrored by activity levels and fTH3 during lactation. Discussion: Energy balance was not preserved through the reproductive cycle, supporting previous contentions that the reproductive performance of female man-Ariadna R. Negrín and Pedro A. D. Dias contributed equally to this study.

Correlates of hormonal modulation in mantled howler monkey males,Alouatta palliata

“…Mantled howler monkeys travel slowly and infrequently when ambient temperature is low (Ceccarelli et al, 2019), and during the dry season, they travel for longer periods than at other times (G omez-Espinosa et al, 2014). Most conceptions and weaning of offspring occur in the late dry-early wet seasons (Crist obal-Azkarate et al, 2017), although female energy balance does not seem to be affected by fluctuation in energy intake (Rangel-Negrín et al, 2021). This possibly reflects the fact that variation in fruit availability (the main source of energy in mantled howler monkeys' diet) is relatively low and there are fruiting trees during the entire year (Cano-Huertes et al, 2017).…”

The influence of anthropogenic noise on the behavior of male mantled howler monkeys

“…We identified the study subjects by the natural markings in their fur and a variety of other physical traits, including scars, broken fingers, and facial features. Given that the reproductive state affects the behavior of female mantled howler monkeys (e.g., females are more active at lactation onset than at other states: Rangel‐Negrín et al, 2021), in this study we concentrated on the 16 adult males residing in the five study groups.…”

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

“…Supporting comparative evidence linking urinary Cpeptide levels with reproductive function is now also available from wild chimpanzees (Emery , chacma baboons (Papio ursinus : Fürtbauer et al, 2020), and howler monkeys (Alouatta palliata: Rangel-Negrin et al, 2021). The role of resource availability in moderating rapid recovery of postpartum C-peptide levels and ovulation among humans (Valeggia & Ellison, 2004), for example, has now also been demonstrated among chimpanzees living with varying food resources (Emery .…”

“…The role of resource availability in moderating rapid recovery of postpartum C‐peptide levels and ovulation among humans (Valeggia & Ellison, 2004 ), for example, has now also been demonstrated among chimpanzees living with varying food resources (Emery Thompson et al, 2012 ). Highlighting the importance of variation in energy expenditure—as well as energy intake—in this energy balance pathway, the dynamics of postpartum urinary C‐peptide levels have also been found to map onto the dynamic costs of milk production and infant transport and vigilance activities among NHPs (Emery Thompson et al, 2012 ; Rangel‐Negrin et al, 2021 ). The interesting finding that C‐peptide levels are greatest during gestation among humans and many NHPs (Fürtbauer et al, 2020 ; Rangel‐Negrin et al, 2021 ) has led to the hypothesis that primates have evolved a conservative pregnancy metabolic strategy to prepare for the heightened challenges of lactation (Dufour & Sauther, 2002 ; Fürtbauer et al, 2020 ).…”