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Fluctuations in daily energy intake do not cause physiological stress in a Neotropical primate living in a seasonal forest

  • Physiological ecology - original research
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Abstract

Animals may face periods of nutritional stress due to short-term food shortage and/or low energy consumption associated with seasonal fluctuations in resource availability. We tested the hypothesis that periods of restricted macronutrient and energy intake result in energy deficits and physiological stress in wild black howler monkeys (Alouatta pigra) inhabiting seasonal tropical semi-deciduous forests. We conducted full-day follows of focal animals recording feeding rates, time spent feeding, and total amount of food ingested. We carried out nutritional analysis of foods collected from feeding trees and calculated the daily nutrient and energy intake of each focal individual. Fecal glucocorticoid metabolites (fGCM) of focal animals were used as an indicator of physiological stress. We found that fluctuations in daily energy intake across seasons did not have significant effects on fGCM of individuals. However, protein intake was negatively associated with fGCM, highlighting the interplay among macronutrients, metabolism, and the endocrine system. Fecal glucocorticoid metabolites were also positively related to fruit availability, but this relationship was most likely due to social stress associated with intergroup encounters and resource defense that occurred when preferred trees were fruiting. Behavioral strategies such as dietary shifts and nutrient mixing, and metabolic adaptations such as low energy expenditure allowed individuals to fulfill their minimum energy requirements even during periods of decreased resource availability and intake. The present study suggests that seasonal variations in food, macronutrient, and energy acquisition may have limited physiological costs for animals that exploit different types of plant resources such as howler monkeys.

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Acknowledgments

We thank Fabian Leendertz, Tom Gillespie, Paul Garber, and Alejandro Estrada for their support and assistance during the howler monkey darting and marking procedures; our volunteer field assistants for their help in collecting the data; Jessica Rothman for welcoming us to conduct nutritional analyses in her lab; and Edith Klobetz-Rassam for help with the fGCM analysis. We are grateful to INIFAP and SEMARNAT, Mexico for granting permission to conduct field research. We thank NSF-DDIG (grant BCS 1128821); the International Primatological Society; Sigma Xi Grants-in-Aid of Research; Scott Neotropical Fund-Cleveland Metroparks Zoo; Lewis and Clark Fund-American Philosophical Society; IdeaWild; and the Department of Anthropology, the Graduate College, and the Earth and Society Initiative for Disease Emergence of University of Illinois for several grants awarded to purchase equipment, carry out laboratory analyses, and conduct field research. The authors declare that they have no conflict of interest.

Author contribution statement

RMM and NR formulated the idea, collected and analyzed the data, and wrote the manuscript; RP provided funding and technical support for hormone analyses, and wrote the manuscript.

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Authors and Affiliations

  1. Department of Anthropology, University of Illinois at Urbana-Champaign, Champaign, USA

    Rodolfo Martínez-Mota & Nicoletta Righini

  2. Red de Manejo Biorracional de Plagas y Vectores, Instituto de Ecología, A.C, Xalapa, Veracruz, Mexico

    Nicoletta Righini

  3. Department of Biomedical Sciences, University of Veterinary Medicine, Vienna, Austria

    Rupert Palme

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  1. Rodolfo Martínez-Mota
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  2. Nicoletta Righini
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  3. Rupert Palme
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Correspondence to Nicoletta Righini.

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Communicated by Hannu J. Ylonen.

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Martínez-Mota, R., Righini, N. & Palme, R. Fluctuations in daily energy intake do not cause physiological stress in a Neotropical primate living in a seasonal forest. Oecologia 182, 973–984 (2016). https://doi.org/10.1007/s00442-016-3739-6

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