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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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References

  • Amthor H, Huang R, McKinnell I, Christ B, Kambadur R, Sharma M, Patel K (2002) The regulation and action of myostatin as a negative regulator of muscle development during avian embryogenesis. Dev Biol 251:241–257

    Article  PubMed  CAS  Google Scholar 

  • Barske J, Fusani L, Wikelski M, Feng NY, Santos M, Schlinger B (2014) Energetics of the acrobatic courtship in male golden-collared manakins (Manacus vitellinus). Proc Roy Soc B 281:20132482

    Article  CAS  Google Scholar 

  • Bauchinger U, Keil J, McKinney RA, Starck JM, McWilliams SR (2010) Exposure to cold but not exercise increases carbon turnover rates in specific tissues of a passerine. J Exp Biol 213:526–534

    Article  PubMed  CAS  Google Scholar 

  • Bish LT, Morine KJ, Sleeper MM, Sweeney HL (2010) Myostatin is upregulated following stress in an Erk-dependent manner and negatively regulates cardiomyocyte growth in culture and in a mouse model. PLoS One 5:e10230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bozinovic F, Sabat P (2010) On the intraspecific variability in basal metabolism and the food habits hypothesis in birds. Curr Zool 56:759–766

    Google Scholar 

  • Bryant DM, Newton AV (1994) Metabolic costs of dominance in dippers Cinclus cinclus. Anim Behav 48:447–455

    Article  Google Scholar 

  • Cadée N, Piersma T, Daan S (1996) Endogenous circannual rhythmicity in a non-passerine migrant, the knot Calidris canutus. Ardea 84:75–84

    Google Scholar 

  • Callis TE, Pandya K, Seok HY, Tang R-H, Tatsuguchi M, Huang Z-P, Chen J-F, Deng Z, Gunn B, Shumate J, Willis MS, Selzman CH, Wang D-Z (2009) MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Invest 119:2772–2786

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carey C, Dawson WR (1999) A search for environmental cues used by birds in survival of cold winters. Curr Ornithol 15:1–31

    Article  Google Scholar 

  • Carmeli E, Moas M, Lennon S, Powers SK (2005) High intensity exercise increases expression of matrix metalloproteinases in fast skeletal muscle fibers. Exp Physiol 90(4):613–619

    Article  PubMed  CAS  Google Scholar 

  • Clavijo-Baquet S, Bozinovic F (2012) Testing the fitness consequences of the thermoregulatory and parental care models for the origin of endothermy. PLoS One 7:e37069

    Article  CAS  Google Scholar 

  • Dawson WR, Marsh RL, Yacoe ME (1983) Metabolic adjustments of small passerine birds for migration and cold. Am J Physiol 245:R755–R767

    PubMed  CAS  Google Scholar 

  • Ekman J (1990) Alliance in winter flocks of willow tits - effects of rank on survival and reproductive success in male-female associations. Behav Ecol 26:239–245

    Google Scholar 

  • Gabriel JE, Alvares LE, Gobet MC, de Paz CCP, Packer IU, Macari M, Coutinho LL (2003) Expression of MyoD, myogenin, myostatin and Hsp70 transcripts in chicken embryos submitted to mild heat or cold. J Therm Biol 28:261–269

    Article  CAS  Google Scholar 

  • Guernec A, Berri C, Chevalier B, Wacrenier-Cere N, Le Bihan-Duval E, Duclos MJ (2003) Muscle development, insulin-like growth factor-I and myostatin mRNA levels in chickens selected for increased breast muscle yield. Growth Horm IGF Res 13:8–18

    Article  PubMed  CAS  Google Scholar 

  • Hayes JP, O’Connor CS (1999) Natural selection on thermogenic capacity of high-altitude deer mice. Evolution 53:1280–1287

    Article  Google Scholar 

  • Heldin C-H, Miyazono K, ten Dijke P (1997) TGF-β signaling from cell membrane to nucleus through SMAD proteins. Nature 390:465–471

    Article  PubMed  CAS  Google Scholar 

  • Hogstad O (1987) It is expensive to be dominant. Auk 104:333–336

    Google Scholar 

  • Huang K-L, Wang J-W, Han C-C, Liu H-H, Li L, Dai F, Pan Z, Xu F, He H, Xu H (2011) Developmental expression and alternative splicing of the duck myostatin gene. Comp Biochem Physiol Part D 6:238–243

    CAS  Google Scholar 

  • Huet C, Li Z-F, Liu H-Z, Black RA, Galliano M-F, Engvall E (2001) Skeletal muscle cell hypertrophy induced by inhibitors of metalloproteinases; myostatin as a potential mediator. Am J Physiol 281:C1624–C1634

    CAS  Google Scholar 

  • Ijiri D, Miura M, Kanai Y, Hirabayashi M (2009) Increased mass of slow-type skeletal muscles and depressed myostatin gene expression in cold-tolerant chicks. Zool Sci 26:277–283

    Article  PubMed  CAS  Google Scholar 

  • Jenni-Eiermann S, Jenni L, Smith S, Constantini D (2014) Oxidative stress in endurance flight: an unconsidered factor in bird migration. PLoS One 9:e97650

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Johnson BD, Padilla J, Wallace JP (2012) The exercise dose affects oxidative stress and brachial artery flow-mediated dilation in trained men. Eur J Appl Physiol 112:33–42

    Article  PubMed  CAS  Google Scholar 

  • Kim YS, Bobbili NK, Paek KS, Jin HJ (2006) Production of a monoclonal anti-myostatin antibody and the effects of in ovo administration of the antibody on posthatch broiler growth and muscle mass. Poultry Sci 85:1062–1071

    Article  CAS  Google Scholar 

  • Kim YS, Kim KH, Kim CJ (2012) Production of bioactive extracellular domain of pig and chicken activin type IIB receptors in Pichia pastoris. Process Biochem 47:139–146

    Article  CAS  Google Scholar 

  • King MO, Zhang Y, Carter T, Johnson J, Harmon E, Swanson DL (2015) Phenotypic flexibility of skeletal muscle and heart masses and expression of myostatin and tolloid–like proteinases in migrating passerine birds. J Comp Physiol B 185. doi:10.1007/s00360-015-0887-7

  • Kocamis H, McFarland D, Killefer J (2001) Temporal expression of growth factor genes during myogenesis in satellite cells derived from biceps femoris and pectoralis major muscles of the chicken. J Cell Physiol 186:146–152

    Article  PubMed  CAS  Google Scholar 

  • LeBrasseur NK, Schelhorn TM, Bernardo BL, Cosgrove PG, Loria PM, Brown TA (2009) Myostatin inhibition enhances the effects of exercise on performance and metabolic outcomes in aged mice. J Gerontol 64A:940–948

    Article  CAS  Google Scholar 

  • Lee S-J (2004) Regulation of muscle mass by myostatin. Annual Rev Cell Dev Biol 20:61–86

    Article  CAS  Google Scholar 

  • Lee S-J (2008) Genetic analysis of the role of proteolysis in the activation of latent myostatin. PLoS One 3:e1628

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lewden A, Petit A, Vézina F (2012) Dominant black-capped chickadees pay no maintenance energy costs for their wintering status and are not better at enduring cold than subordinate individuals. J Comp Physiol B 182:381–392

    Article  PubMed  Google Scholar 

  • Lewden A, Petit M, Milbergue M, Orio S, Vézina F (2014) Evidence of facultative daytime hypothermia in a small passerine wintering at northern latitudes. Ibis 156:321–329

    Article  Google Scholar 

  • Liknes ET, Swanson DL (2011) Phenotypic flexibility of body composition associated with seasonal acclimatization of passerine birds. J Therm Biol 36:363–370

    Article  Google Scholar 

  • Liknes ET, Scott SM, Swanson DL (2002) Seasonal acclimatization in the American goldfinch revisited: to what extent to metabolic rates vary seasonally? Condor 104:548–557

    Article  Google Scholar 

  • Liu H-H, Wang J-W, Yu H-Y, Zhang R-P, Chen X, Jin H-B, Dai F, Li L, Xu F (2012) Injection of duck recombinant follistatin fusion protein into duck muscle tissues stimulates satellite cell proliferation and muscle fiber hypertrophy. Appl Microbiol Biotechnol 94:1255–1263

    Article  PubMed  CAS  Google Scholar 

  • Maldonado K, Cavieres G, Veloso C, Canals M, Sabat P (2009) Physiological responses in rufous-collared sparrows to thermal acclimation and seasonal acclimatization. J Comp Physiol B 179:335–343

    Article  PubMed  Google Scholar 

  • Marsh RL, Dawson WR (1989) Avian adjustments to cold. In: Wang LCH (ed) Advances in comparative and environmental physiology 4: animal adaptation to cold. Springer, New York, pp 205–253

    Chapter  Google Scholar 

  • McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R (2003) Myostatin negatively regulates satellite cell activation and self-renewal. J Cell Biol 162:1135–1147

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McFarland DC, Velleman SG, Pesall JE, Liu C (2006) Effect of myostatin on turkey myogenic satellite cells and embryonic myoblasts. Comp Biochem Physiol Part A 144:501–508

    Article  CAS  Google Scholar 

  • McFarland DC, Velleman SG, Pesall JE, Liu C (2007) The role of myostatin in chicken (Gallus domesticus) myogenic satellite cell proliferation and differentiation. Gen Comp Endocr 151:351–357

    Article  PubMed  CAS  Google Scholar 

  • McKechnie AE (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B 178:235–247

    Article  PubMed  Google Scholar 

  • McKechnie AE, Swanson DL (2010) Sources and significance of variation in basal, summit and maximal metabolic rates in birds. Curr Zool 56:741–758

    Google Scholar 

  • Miyazawa K, Shinozaki M, Hara T, Furuya T, Miyazono K (2002) Two major Smad pathways in TGF-β superfamily signaling. Genes Cells 7:1191–1204

    Article  PubMed  CAS  Google Scholar 

  • Morissette MR, Cook SA, Foo SY, McKoy G, Ashida N, Novikov M, Scherrer-Crosbie M, Li L, Matsui T, Brooks G, Rosenzweig A (2006) Myostatin regulates cardiomyocyte growth through modulation of Akt signaling. Circ Res 99:15–24

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mosher DS, Quignon P, Bustamante CD, Sutter NB, Mellersh C, Parker HG, Ostrander EA (2007) A mutation in the myostatin gene increases muscle mass and enhances racing performance in heterozygote dogs. PLoS Genet 5:e79

    Article  CAS  Google Scholar 

  • Mott I, Ivarie R (2002) Expression of myostatin is not altered in lines of poultry exhibiting myofiber hyper- and hypoplasia. Poult Sci 81:799–804

    Article  PubMed  CAS  Google Scholar 

  • Otter K, Chruszcz B, Ratcliffe L (1997) Honest advertisement and song output during the dawn chorus of black-capped chickadees. Behav Ecol 8:167–173

    Article  Google Scholar 

  • Parker L, McGuckin TA, Leicht AS (2014) Influence of exercise intensity on systemic oxidative stress and antioxidant capacity. Clin Physiol Funct Imaging 34:377–383

    Article  PubMed  CAS  Google Scholar 

  • Petit M, Vézina F (2014a) Reaction norms in natural conditions: how does metabolic performance respond to weather variations in a small endotherm facing cold environments? PLoS One 9:e113617

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Petit M, Vézina F (2014b) Phenotype manipulations confirm the role of pectoral muscles and haematocrit in avian maximal thermogenic capacity. J Exp Biol 217:824–830

    Article  PubMed  Google Scholar 

  • Petit M, Lewden A, Vézina F (2013) Intra-seasonal flexibility in avian metabolic performance highlights the uncoupling of basal metabolic rate and thermogenic capacity. PLoS One 8:e68292

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Petit M, Lewden A, Vézina F (2014) How does flexibility in body composition relate to seasonal changes in metabolic performance in a small passerine wintering at a northern latitude? Physiol Biochem Zool 87:539–549

    Article  PubMed  Google Scholar 

  • Piersma T (2002) When a year takes 18 months: evidence for a strong circannual clock in a shorebird. Naturwissenschaften 89:278–279

    Article  PubMed  CAS  Google Scholar 

  • Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233

    Article  Google Scholar 

  • Piersma T, van Gils J (2011) The flexible phenotype: a body-centred integration of ecology, physiology, and behavior. Oxford University Press, Oxford

    Google Scholar 

  • Pigliucci M (2001) Phenotypic plasticity: beyond nature and nurture. Johns Hopkins University Press, Baltimore

    Google Scholar 

  • Price ER, Bauchinger U, Zajac DM, Cerasale DJ, McFarlan JT, Gerson AR, McWilliams SR, Guglielmo CG (2011) Migration- and exercise-induced changes to flight muscle size in migratory birds and association with IGF1 and myostatin mRNA expression. J Exp Biol 214:2823–2831

    Article  PubMed  CAS  Google Scholar 

  • Rodgers BD, Garikipati DK (2008) Clinical, agricultural and evolutionary biology of myostatin: a comparative review. Endocr Rev 29:513–534

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roskaft E, Jarvi T, Bakken M, Bech C, Reinertsen RE (1986) The relationship between social status and resting metabolic rate in great tits (Parus major) and pied flycatchers (Ficedula hypoleuca). Anim Behav 34:838–842

    Article  Google Scholar 

  • Sears MW, Hayes JP, O’Connor CS, Geluso K, Sedinger JS (2006) Individual variation in thermogenic capacity affects above-ground activity of high-altitude deer mice. Funct Ecol 20:97–104

    Article  Google Scholar 

  • Sgueo C, Wells ME, Russell DE, Schaeffer PJ (2012) Acclimatization of seasonal energetics in northern cardinals (Cardinalis cardinalis) through plasticity of metabolic rates and ceilings. J Exp Biol 215:2418–2424

    Article  PubMed  Google Scholar 

  • Stager M, Swanson DL, Cheviron Z (2015) Regulatory mechanisms of metabolic flexibility in the dark–eyed junco (Junco hyemalis). J Exp Biol 218 (in press). doi:10.1242/jeb.113472

  • Steiger SS, Kelley JP, Cochran WW, Wikelski M (2009) Low metabolism and inactive lifestyle of a tropical rain forest bird investigated via heart-rate telemetry. Physiol Biochem Zool 82:580–589

    Article  PubMed  Google Scholar 

  • Swanson DL (1990) Seasonal variation in cold hardiness and peak rates of cold-induced thermogenesis in the dark-eyed junco (Junco hyemalis). Auk 107:561–566

    Google Scholar 

  • Swanson DL (2001) Are summit metabolism and thermogenic endurance correlated in winter-acclimatized passerine birds. J Comp Physiol B 171:475–481

    Article  PubMed  CAS  Google Scholar 

  • Swanson DL, Liknes ET (2006) A comparative analysis of thermogenic capacity and cold tolerance in small birds. J Exp Biol 209:466-474

    Article  PubMed  Google Scholar 

  • Swanson DL (2010) Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr Ornithol 17:75–129

    Google Scholar 

  • Swanson DL, Garland T Jr (2009) The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions. Evolution 63:184–194

    Article  PubMed  CAS  Google Scholar 

  • Swanson DL, Merkord CL (2013) Seasonal phenotypic flexibility of flight muscle size in small birds: a comparison of ultrasonography and tissue mass measurements. J Ornithol 154:119–127

    Article  Google Scholar 

  • Swanson DL, Olmstead KL (1999) Evidence for a proximate influence of winter temperature on metabolism in passerine birds. Physiol Biochem Zool 72:566–575

    Article  PubMed  CAS  Google Scholar 

  • Swanson DL, Sabirzhanov B, VandeZande A, Clark TG (2009) Seasonal variation of myostatin gene expression in pectoralis muscle of house sparrows (Passer domesticus) is consistent with a role in regulating thermogenic capacity and cold tolerance. Physiol Biochem Zool 82:121–128

    Article  PubMed  CAS  Google Scholar 

  • Swanson DL, Zhang Y, King MO (2013) Individual variation in thermogenic capacity is correlated with flight muscle size but not cellular metabolic capacity in American goldfinches, Spinus tristis. Physiol Biochem Zool 86:421–431

    Article  PubMed  Google Scholar 

  • Swanson DL, Zhang Y, Liu J-S, Merkord CL, King MO (2014a) Relative roles of temperature and photoperiod as drivers of metabolic flexibility in dark-eyed juncos. J Exp Biol 217:866–875

    Article  PubMed  CAS  Google Scholar 

  • Swanson DL, Zhang Y, King MO (2014b) Mechanistic drivers of flexibility in summit metabolic rates of small birds. PLoS One 9:e101577

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Swanson DL, King MO, Harmon E (2014c) Seasonal variation in pectoralis muscle and heart myostatin and tolloid-like proteins in small birds: a regulatory role for seasonal phenotypic flexibility? J Comp Physiol B 184:249–258

    Article  PubMed  CAS  Google Scholar 

  • Tieleman BI, Williams JB, Bloomer P (2003) Adaptation of metabolism and evaporative water loss along an aridity gradient. Proc Roy Soc Lond B 270:207–214

    Article  Google Scholar 

  • Tieleman BI, Dijkstra TH, Lasky JR, Mauck RA, Visser GH, Williams JB (2006) Physiological and behavioural correlates of life-history variation: a comparison between tropical and temperate zone House Wrens. Funct Ecol 20:491–499

    Article  Google Scholar 

  • van de Ven TMFN, Mzilikazi M, McKechnie AE (2013) Phenotypic flexibility in body mass, basal metabolic rate and summit metabolism in southern red bishops (Euplectes orix): responses to short term thermal acclimation. Comp Biochem Physiol Part A 165:319–327

    Article  CAS  Google Scholar 

  • Vézina F, Salvante K (2010) Behavioral and physiological flexibility are used by birds to manage energy and support investment in the early stages of reproduction. Cur Zool 56:767–792

    Google Scholar 

  • Vézina F, Thomas DW (2000) Social status does not affect resting metabolic rate in wintering dark-eyed junco (Junco hyemalis). Physiol Biochem Zool 73:231–236

    Article  PubMed  Google Scholar 

  • Vézina F, Jalvingh KM, Dekinga A, Piersma T (2006) Acclimation to different thermal conditions in a northerly wintering shorebird is driven by body mass-related changes in organ size. J Exp Biol 209:3141–3154

    Article  PubMed  Google Scholar 

  • Vézina F, Jalvingh KM, Dekinga A, Piersma T (2007) Thermogenic side effects to migratory disposition in shorebirds. Am J Physiol Regul Integr Comp Physiol 292:1287–1297

    Article  CAS  Google Scholar 

  • Vézina F, Dekinga A, Piersma T (2011) Shorebirds’ seasonal adjustments in thermogenic capacity are reflected by changes in body mass: how preprogrammed and instantaneous acclimation work together. Integr Comp Biol 51:394–408

    Article  PubMed  Google Scholar 

  • Wagner DN, Mineo PM, Sgueo C, Wikelski M, Schaeffer PJ (2013) Does low daily energy expenditure drive low metabolic capacity in the tropical robin, Turdus grayi? J Comp Physiol B 183:833–841

    Article  PubMed  CAS  Google Scholar 

  • Welle S, Bhatt K, Pinkert CA, Tawil R, Thornton CA (2007) Muscle growth after postdevelopmental myostatin gene knockout. Am J Physiol Endocrinol Metab 292:E985–E991

    Article  PubMed  CAS  Google Scholar 

  • Whittemore L-A, Song K, Li X, Aghajanian J, Davies M, Girgenrath S, Hill JJ, Jalenak M, Kelley P, Knight A, Maylor R, O’Hara D, Pearson A, Quazi A, Ryerson S, Tan X-Y, Tomlinson KN, Veldman GM, Widom A, Wright JF, Wudyka S, Zhao L, Wolfman NM (2003) Inhibition of myostatin in adult mice increases skeletal muscle mass and strength. Biochem Biophys Res Comm 300:965–971

    Article  PubMed  CAS  Google Scholar 

  • Wiersma P, Nowak B, Williams JB (2012) Small organ size contributes to the slow pace of life in tropical birds. J Exp Biol 215:1662–1669

    Article  PubMed  Google Scholar 

  • Wolfman NM, McPherron AC, Pappano WN, Davies MV, Song K, Tomlinson KN, Wright JF, Zhao L, Sebald SM, Greenspan DS, Lee S-J (2003) Activation of latent myostatin by the BMP-1/tolloid family of metalloproteinases. Proc Natl Acad Sci USA 100:15842–15846

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Swanson DL (2014) Cold and exercise training produce similar Increases in maximal metabolic output in house sparrows. Integr Comp Biol 54[Suppl 1]:e233

    Google Scholar 

  • Zub K, Borowski Z, Szafranska PA, Wieczorek M, Kanoarzewski M (2014) Lower body mass and higher metabolic rate enhance winter survival in root voles, Microtus oeconomus. Biol J Linn Soc 113:297–309

    Article  Google Scholar 

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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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  1. David L. Swanson
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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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