To develop effective conservation and management actions, it is important to examine anthropogenic disturbance patterns and their impact on wildlife. We examined variation in the behavioral and physiological stress response of the Critically Endangered Mexican mantled howler monkeys Alouatta palliata mexicana in relation to two types of anthropogenic disturbance, habitat spatial patterns and presence of humans or their livestock (noise and presence nearby primates). We studied four groups (42 individuals) in two forest fragments at the Los Tuxtlas Biosphere Reserve for a total of 1100 observation hours, during which we recorded the howler monkeys’ vocalizations, locomotion and vigilance. We additionally collected fecal samples to determine the concentrations of glucocorticoid metabolites (fGCM). Howler monkeys vocalized less and moved more when in more spatially disturbed locations and when exposed more time to nearby noise but spent less time in locomotion when humans were present. fGCM were only related to human presence, suggesting that habitat spatial patterns are less of a challenge than human presence. This may be related to the generally unpredictable nature of the latter. Although our study does not allow determining whether the behavioral and physiological responses of howler monkeys to disturbance are costly, from a conservation standpoint it may be more prudent to assume that they are and design strategies to mitigate them. In this sense, actions aimed at reducing anthropogenic noise could benefit the conservation of Mexican mantled howler monkeys.
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.
To date, no study has investigated how human disturbance affects the size of the behavioral repertoire of a species. The aim of the present study is to illustrate how measurement of behavioral diversity assists in documenting biodiversity loss, demonstrating that human disturbance has a negative effect on behavioral diversity. We studied the social interaction repertoire of 41 adult black howler monkeys (Alouatta pigra) belonging to 10 groups living in different habitats in Campeche (Mexico), and related repertoire size to a proxy of human-induced habitat disturbance, habitat size. The social interaction repertoire of groups living in habitats with higher human-induced disturbance included lower number of behavioral types, and in particular, fewer energy-demanding behaviors. Thus, in addition to a loss in biodiversity, measured through organismal diversity, the disturbance of black howler monkeys' habitats is accompanied by a loss in behavioral diversity. We believe that the study of behavioral diversity as an element of biodiversity will become an increasingly important research topic, as it will improve our understanding of the behavioral strategies displayed by wildlife facing anthropogenic disturbance.
Allostatic load refers to the wear and tear of the organism associated with the repeated activation of mechanisms that allow for homeostasis. Although allostasis (i.e., maintaining stability through change) is achieved through the orchestration of multiple systems, assessments of allostatic load in wildlife have usually relied on the measurement of single or few physiological mediators. In the present study, we aimed at constructing an allostatic load index (ALI) for male mantled howler monkeys (Alouatta palliata) based on seven physiological mediators (C-peptide, triiodothyronine, glucocorticoids, testosterone, amount of activity, foraging effort, and participation in agonistic interactions). We then examined if variation in this ALI was associated with social, ecological, and abiotic challenges. For five years, we studied ten adult males belonging to two groups. We assessed physiological mediators via behavioral observations (3,364 hours of samplings), and both urine (1,500 assayed samples) and fecal (1,500 assayed samples) sampling. We calculated an ALI based on mediator specific risk scores. Seasonality, encounters with extragroup males, mating, and centrality were positively related with male allostatic load, though only the first two had significant effects on ALI. ALI reflected the physiological and behavioral responses of males to social, ecological, and abiotic challenges. It remains for future research to determine if the observed trends correspond to normal fluctuations in mechanisms that allow male mantled howler monkeys to cope with their environment.
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