Seasonal energetic stress in a tropical forest primate: proximate causes and evolutionary implications.

Steffen Foerster,Steven L Monfort,Marina Cords,Antje Engelhardt

doi:10.1371/journal.pone.0050108

Abstract

Animals facing seasonal variation in food availability experience selective pressures that favor behavioral adjustments such as migration, changes in activity, or shifts in diet. Eclectic omnivores such as many primates can process low-quality fallback food when preferred food is unavailable. Such dietary flexibility, however, may be insufficient to eliminate constraints on reproduction even for species that live in relatively permissive environments, such as moist tropical forests. Focusing on a forest-dwelling primate with a flexible diet (Cercopithecus mitis) we investigated whether females experience seasonal energetic stress and how it may relate to reproductive seasonality. We used fecal glucocorticoids (fGCs) as an indicator of energetic stress, controlling for the potentially confounding effects of social interactions and reproductive state. We modeled within-female fGC variation with General Linear Mixed Models, evaluating changes in feeding behavior and food availability as main effects. Regardless of reproductive state, fGCs increased when females shifted their diet towards fallback foods (mature leaves and other non-preferred items) and when they spent more time feeding, while fGCs decreased with feeding time on preferred items (insects, fruits, young leaves) and with the availability of young leaves. Changes in fruit availability had no general effects on fGCs, likely because fruits were sought out regardless of availability. As predicted, females in the energetically demanding stages of late pregnancy and early lactation showed greater increases in fGCs between periods of low versus high availability of fruits and young leaves than females in other reproductive states. Potential social stressors had no measurable effects on fGCs. Preliminary evidence suggests that seasonal energetic stress may affect the timing of infant independence from mothers and contribute to unusually long inter-birth intervals compared to closely related species of similar body size. Our findings highlight how the study of stress responses can provide insights into the proximate control of reproductive strategies.

Highlights

Despite minimal seasonal variation in day length and temperature, most tropical habitats experience seasonal fluctuation in rainfall that mediates changes in food availability for many animals
Many primates are known especially for having evolved considerable dietary flexibility, most likely as a response to the challenge of environmental seasonality [7]. They are able to cope with periods of food shortage by exploiting alternative, nonpreferred items, known as fallback foods [8], which are often lower than preferred foods in usable energy content and/or higher in plant secondary compounds
Ripe fruit and young leaf availability were both negatively correlated with the time spent feeding on mature leaves and other food items, indicating that mature leaves and other food items can be considered non-preferred fallback foods [8]

Summary

Introduction

Despite minimal seasonal variation in day length and temperature, most tropical habitats experience seasonal fluctuation in rainfall that mediates changes in food availability for many animals. These environmental changes require behavioral and physiological adaptations to minimize negative effects on fitness [1,2]. Many primates are known especially for having evolved considerable dietary flexibility, most likely as a response to the challenge of environmental seasonality [7] They are able to cope with periods of food shortage by exploiting alternative, nonpreferred items, known as fallback foods [8], which are often lower than preferred foods in usable energy content and/or higher in plant secondary compounds. They have not been well studied in other mammals, the importance of fallback foods for primates has led researchers to view them as a driving force in the evolution of life histories, anatomy and behavior [9]

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Conclusion