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Environmental, ecological and mechanistic drivers of avian seasonal metabolic flexibility in response to cold winters

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Abstract

Small birds inhabiting regions with cold winter climates show seasonally flexible metabolic phenotypes, with the winter phenotype characterized by increments of summit metabolic rate (Msum) and cold tolerance. In the study reported here, we focused on variations in Msum as a metric of metabolic performance because it is positively correlated with cold tolerance in birds and positively related to overwinter survival in small mammals, although the latter has yet to be demonstrated in birds. Temperature appears to be a prominent driver of seasonal metabolic phenotypes in birds, as evidenced by the correlation between inter- and intra-seasonal variation in Msum and temperature variation, by recent temperature variables serving as better predictors of Msum variation than long-term climate variables, and by the induction of Msum variation by experimental cold exposure. In contrast, photoperiod and social status do not appear to be prominent drivers of metabolic flexibility in birds studied to date. Because skeletal muscle is the primary thermogenic tissue in birds, studies of the mechanistic underpinnings of metabolic flexibility have focused on skeletal muscles, particularly flight muscles. At the level of the skeletal muscle, two potential mechanisms exist for increasing thermogenic capacity, namely, muscle hypertrophy and elevated cellular metabolic intensity. Correlative studies suggest consistent winter increments in flight muscle size, with a potential regulatory role for the muscle growth inhibitor myostatin. Recent experimental studies in small birds, including modification of flight costs, cold acclimation, and exercise training, also suggest that muscle size is an important driver of metabolic flexibility in birds. Therefore, the focus of our study was on the seasonal regulation of muscle size and its contribution to metabolic flexibility. Future studies should address fitness consequences of Msum variation, the relative roles of muscle hypertrophy, and other factors (e.g., oxygen and substrate transport, cellular metabolic intensity) promoting Msum variation, as well as the molecular mechanisms underlying seasonal phenotypes.

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Acknowledgments

DLS was supported by the U.S. National Science Foundation IOS-1021218 and the University of South Dakota. FV was supported by a Discovery grant 9045333 from the Natural Sciences and Engineering Research Council of Canada as well as a Nouveaux Chercheurs grant 132032 from the Fonds de Recherche du Québec sur la nature et les technologies. We thank the many postdoctoral fellows, graduate students, and undergraduate students who contributed substantially to this work, and M. Petit for providing Black-capped Chickadee data for Figs. 2, 3 and 4. We also thank two anonymous reviewers for the constructive comments on an earlier version of the manuscript.

Compliance with ethical standards

All applicable international, national and/or institutional guidelines for the care and use of animals were followed. DLS collected birds for these studies under active State and Federal (United States Fish and Wildlife Service, MB758442) scientific collecting permits, and all studies were approved by the University of South Dakota Institutional Animal Care and Use Committee. All bird manipulations by FV were approved by the animal care committee of the Université du Québec à Rimouski and have been conducted under scientific and banding permits from Environment Canada—Canadian wildlife service.

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Authors and Affiliations

  1. Department of Biology, University of South Dakota, Vermillion, SD, USA

    David L. Swanson

  2. Département de Biologie, Chimie et Géographie, Université du Québec à Rimouski, Rimouski, QC, Canada

    François Vézina

  3. Groupe de recherche sur les environnements nordiques BORÉAS, Rimouski, QC, Canada

    François Vézina

  4. Centre d’Études Nordiques Québec, Quebec City, QC, Canada

    François Vézina

  5. Centre de la Science de la Biodiversité du Québec, Montreal, QC, Canada

    François Vézina

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Correspondence to David L. Swanson.

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Communicated by E. Matthysen.

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Swanson, D.L., Vézina, F. Environmental, ecological and mechanistic drivers of avian seasonal metabolic flexibility in response to cold winters. J Ornithol 156 (Suppl 1), 377–388 (2015). https://doi.org/10.1007/s10336-015-1192-7

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