Abstract
The adjustment of resting metabolic rates represents an important component of avian seasonal acclimatization, with recent studies revealing substantial differences between summer and winter in birds from a wide range of latitudes. We compared seasonal variation in basal metabolic rate (BMR) and summit metabolism (M sum) between temperate and tropical/subtropical latitudes, and examined correlations with latitude and temperature. The direction and magnitude of seasonal adjustments in BMR are broadly related to temperature and latitude, but are significantly more variable among tropical and subtropical species compared to those inhabiting temperate zones. Winter adjustments in BMR among subtropical species, when expressed relative to summer values, range from decreases of approximately 35 % to increases of more than 60 %, whereas the majority of temperate-zone species show increases in BMR during winter. Relatively few seasonal M sum data exist for tropical/subtropical species, but those that are available involve responses ranging from winter decreases to increases of similar magnitude to those characteristic of many temperate-zone species. Recent studies also highlight the substantial variation in seasonal adjustments that may occur within species, and reiterate the need for further investigations of the relative roles of environmental variables such as temperature and food availability as determinants of seasonal metabolic variation.
Similar content being viewed by others
References
Anderson KJ, Jetz W (2005) The broad-scale ecology of energy expenditure of endotherms. Ecol Lett 8:310–318
Arens JR, Cooper SJ (2005) Metabolic and ventilatory acclimatization to cold stress in House Sparrows (Passer domesticus). Physiol Biochem Zool 78(4):579–589
Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745
Bush NG, Brown M, Downs CT (2008) Seasonal effects on thermoregulatory responses of the Rock Kestrel, Falco rupicolis. J Therm Biol 33(7):404–412
Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117(5):641–653
Chamane S, Downs CT (2009) Seasonal effects on metabolism and thermoregulation abilities of the red-winged starling (Onychognathus morio). J Therm Biol 34:337–341
Cooper SJ (2000) Seasonal energetics of mountain chickadees and juniper titmice. Condor 102(3):635–644
Cooper SJ (2002) Seasonal metabolic acclimatization in mountain chickadees and juniper titmice. Physiol Biochem Zool 75(4):386–395
Cooper SJ, Swanson DL (1994) Seasonal acclimatization of thermoregulation in the black-capped chickadee. Condor 96:638–646
Dawson WR, Carey C (1976) Seasonal acclimation to temperature in Cardueline finches. J Comp Physiol 112:317–333
Dawson WR, Buttemer WA, Carey C (1985) A reexamination of the metabolic response of house finches to temperature. Condor 87:424–427
Doucette LI, Geiser F (2008) Seasonal variation in thermal energetics of the Australian owlet-nightjar (Aegotheles cristatus). Comp Biochem Physiol A 151:615–620
Downs CT, Zungu MM, Brown M (2012) Seasonal effects on thermoregulatory abilities of the Wahlberg’s epauletted fruit bat (Epomophorus wahlbergi) in KwaZulu-Natal, South Africa. J Therm Biol 37:144–150
Hackett SJ, Kimball RT, Reddy S, Bowie RCK, Braun EL, Braun MJ, Chojnowski JL, Cox WA, Han K-L, Harshman J, Huddleston CJ, Marks BD, Miglia KJ, Moore WS, Sheldon FH, Steadman DW, Witt CC, Yuri T (2008) A phylogenomic study of birds reveals their evolutionary history. Science 320:1763–1768
Hart JS (1962) Seasonal acclimatization in four species of small wild birds. Physiol Zool 35:224–236
Jetz W, Thomas GE, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491:444–448
Liknes ET, Swanson DL (1996) Seasonal variation in cold tolerance, basal metabolic rate, and maximal capacity for thermogenesis in white-breasted nuthatches Sitta carolinensis and downy woodpeckers Picoides pubescens, two unrelated arboreal temperate residents. J Avian Biol 27(4):279–288
Liknes ET, Scott SM, Swanson DL (2002) Seasonal acclimatization in the American Goldfinch revisited: to what extent do metabolic rates vary seasonally? Condor 104:548–557
Lill A, Box J, Baldwin J (2006) Do metabolism and contour plumage insulation vary in response to seasonal energy bottlenecks in superb fairy-wrens? Aust J Zool 54:23–30
Lindsay CV, Downs CT, Brown M (2009a) Physiological variation in amethyst sunbirds (Chalcomitra amethystina) over an altitudinal gradient in summer. J Therm Biol 34(4):190–199
Lindsay CV, Downs CT, Brown M (2009b) Physiological variation in amethyst sunbirds (Chalcomitra amethystina) over an altitudinal gradient in winter. J Exp Biol 212:483–493
Londoño GA, Chappell MA, del Rosario Castañeda M, Jankowski JE, Robinson SK (in press) Basal metabolism in tropical birds: latitude, altitude, and the “pace of life”. Funct Ecol
Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156(2):201–219
Lovegrove BG, Lawes MJ, Roxburgh L (1999) Confirmation of plesiomorphic daily torpor in mammals: the round-eared elephant shrew Macroscelides proboscideus (Macroscelidea). J Comp Physiol B 169:453–460
Lovegrove BG, Perrin MR, Brown M (2011) The allometry of parrot BMR: seasonal data for the greater vasa parrot, Coracopsis vasa, from Madagascar. J Comp Physiol B 181:1075–1087
Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75 http://mesquiteproject.org
Maddocks TA, Geiser F (2000) Seasonal variations in thermal energetics of Australian silvereyes (Zosterops lateralis). J Zool Lond 252(3):327–333
Maldonado KE, 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(3):335–343
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
Merola-Zwartjes M, Ligon JD (2000) Ecological energetics of the Puerto Rican tody: heterothermy, torpor and intra-island variation. Ecology 81(4):990–1002
Minnaar IA, Bennett NC, Chimimba CT, McKechnie AE (2014) Summit metabolism and metabolic expansibility in Wahlberg’s epauletted fruit bats (Epomophorus wahlbergi): seasonal acclimatisation and effects of captivity. J Exp Biol 217:1363–1369
Montgomerie R, Lyon B, Holder K (2001) Dirty ptarmigan: behavioral modification of conspicuous male plumage. Behav Ecol 12(4):429–438
Nzama SN, Downs CT, Brown M (2010) Seasonal variation in the metabolism–temperature relation of House Sparrows (Passer domesticus) in KwaZulu-Natal, South Africa. J Therm Biol 35(2):100–104
O’Connor TP (1995) Metabolic characteristics and body composition in house finches: effects of seasonal acclimatization. J Comp Physiol B 165:298–305
O’Connor TP (1996) Geographic variation in metabolic seasonal acclimatization in house finches. Condor 98:371–381
Orme D, Freckleton RP, Petzoldt T, Fritz S, Isaac N, W P (2013) Caper: comparative analyses of phylogenetics and evolution in R. Methods Ecol Evol 3:145–151
Paradis E, Bolker B, Claude J, Cuong H, Desper R, Du-rand B, Dutheil J, Gascuel O, Heibl C, Lawson D, Lefort V, Legendre P, Lemon J, Noel Y, Nylander J, Opgen-Rhein R, Popescu A-A, Schliep K, Strimmer K, De Vienne D (2013) Ape: analyses of phylogenetics and evolution. Bioinformatics 20(2):289–290
Petit M, Vezina F (2014) Reaction norms in natural conditions: how does metabolic performance respond to weather variations in a small endotherm facing cold environments? PLoS OME 9(11):e113617
Pohl H (1971) Seasonal variation in metabolic functions of bramblings. Ibis 113:185–193
Pohl H, West GC (1973) Daily and seasonal variation in metabolic response to cold during rest and exercise in the common redpoll. Comp Biochem Physiol 45A:851–867
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147(6):1047–1071
Rising J (2011) Dark-eyed Junco (Junco hyemalis). In: del Hoyo J, Elliot A, Sargatal J, Christie DA, de Juana E (eds) Handbook of the birds of the world alive, vol http://www.hbw.com/node/61909. Lynx, Barcelona
Rising JD, Hudson JW (1974) Seasonal variation in the metabolism and thyroid activity of the black-capped chickadee (Parus atricapillus). Condor 76:198–203
Saarela S, Klapper B, Heldmaier G (1995) Daily rhythm of oxygen consumption and thermoregulatory responses in some European winter- or summer-acclimatized finches at different ambient temperatures. J Comp Physiol B 165:366–376
Sgueo C, Wells ME, Russel DA, 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
Sharbaugh SM (2001) Seasonal acclimatization to extreme climatic conditions by black-capped chickadees (Poecile atricapilla) in interior Alaska (64ºN). Physiol Biochem Zool 74(4):568–575
Smit B, McKechnie AE (2010) Avian seasonal metabolic variation in a subtropical desert: basal metabolic rates are lower in winter than in summer. Funct Ecol 24:330–339
Smith CC, Reichman OJ (1984) The evolution of food caching by birds and mammals. Annu Rev Ecol Syst 15:329–351
Southwick EE (1980) Seasonal thermoregulatory adjustments in white-crowned sparrows. Auk 97:76–85
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
Swanson DL (1991) Seasonal adjustments in metabolism and insulation in the Dark-eyed Junco. Condor 93:538–545
Swanson DL (2010) Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr Ornithol 17:75–129
Swanson DL, Garland T (2009) The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions. Evolution 63:184–194
Swanson DL, Liknes ET (2006) A comparative analysis of thermogenic capacity and cold tolerance in small birds. J Exp Biol 209:466–474
Swanson DL, Olmstead KL (1999) Evidence for a proximate influence of winter temperatures on metabolism in passerine birds. Physiol Biochem Zool 72(5):566–575
Swanson DL, Weinacht DP (1997) Seasonal effects on metabolism and thermoregulation in northern bobwhite. Condor 99:478–489
van de Ven TMFN, Mzilikazi N, McKechnie AE (2013) Seasonal metabolic variation in two populations of an Afrotropical euplectid bird. Physiol Biochem Zool 86(1):19–26
Weathers WW, Caccamise DF (1978) Seasonal acclimatization to temperature in monk parakeets. Oecologia 35:173–183
Wells ME, Schaeffer PJ (2012) Seasonality of peak metabolic rate in non-migrant tropical birds. J Avian Biol 43:481–485
Wiersma P, Chappell MA, Williams JB (2007a) Cold- and exercise-induced peak metabolic rates in tropical birds. Proc Natl Acad Sci USA 104(52):20866–20871
Wiersma P, Muñoz-Garcia A, Walker A, Williams JB (2007b) Tropical birds have a slow pace of life. Proc Natl Acad Sci USA 104(22):9340–9345
Wijnandts H (1984) Ecological energetics of the long-eared owl (Asio otus). Ardea 72:1–92
Wilson A-L, Brown M, Downs CT (2011) Seasonal variation in metabolic rate of a medium-sized frugivore, the Knysna Turaco (Tauraco corythaix). J Therm Biol 36:167–172
Withers PC (1992) Comparative animal physiology. Saunders College Publishing, Fort Worth
Zheng W-H, Liu J-S, Jiang X-H, Fang Y-Y, Zhang G-K (2008a) Seasonal variation on metabolism and thermoregulation in Chinese bulbul. J Therm Biol 33:315–319
Zheng W-H, Ming L, Liu J-S, Shao S-L (2008b) Seasonal acclimatization of metabolism in Eurasian tree sparrows (Passer montanus). Comp Biochem Physiol A 151(4):519–525
Acknowledgments
We thank David Swanson and François Vézina for organizing an exceptionally interesting and enjoyable symposium, and the International Ornithological Congress for a travel grant to A.E.M. Two anonymous reviewers provided insightful comments that greatly improved the quality of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by E. Matthysen.
Rights and permissions
About this article
Cite this article
McKechnie, A.E., Noakes, M.J. & Smit, B. Global patterns of seasonal acclimatization in avian resting metabolic rates. J Ornithol 156 (Suppl 1), 367–376 (2015). https://doi.org/10.1007/s10336-015-1186-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-015-1186-5