Journal of Ornithology

, Volume 156, Supplement 1, pp 367–376 | Cite as

Global patterns of seasonal acclimatization in avian resting metabolic rates

  • Andrew E. McKechnie
  • Matthew J. Noakes
  • Ben Smit
Review

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 (Msum) 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 Msum 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.

Keywords

Acclimatization Basal metabolic rate Latitude Subtropics Summit metabolism 

References

  1. Anderson KJ, Jetz W (2005) The broad-scale ecology of energy expenditure of endotherms. Ecol Lett 8:310–318CrossRefGoogle Scholar
  2. Arens JR, Cooper SJ (2005) Metabolic and ventilatory acclimatization to cold stress in House Sparrows (Passer domesticus). Physiol Biochem Zool 78(4):579–589PubMedCrossRefGoogle Scholar
  3. Blomberg SP, Garland T, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57(4):717–745PubMedCrossRefGoogle Scholar
  4. Bush NG, Brown M, Downs CT (2008) Seasonal effects on thermoregulatory responses of the Rock Kestrel, Falco rupicolis. J Therm Biol 33(7):404–412CrossRefGoogle Scholar
  5. Careau V, Thomas D, Humphries MM, Réale D (2008) Energy metabolism and animal personality. Oikos 117(5):641–653CrossRefGoogle Scholar
  6. Chamane S, Downs CT (2009) Seasonal effects on metabolism and thermoregulation abilities of the red-winged starling (Onychognathus morio). J Therm Biol 34:337–341CrossRefGoogle Scholar
  7. Cooper SJ (2000) Seasonal energetics of mountain chickadees and juniper titmice. Condor 102(3):635–644CrossRefGoogle Scholar
  8. Cooper SJ (2002) Seasonal metabolic acclimatization in mountain chickadees and juniper titmice. Physiol Biochem Zool 75(4):386–395PubMedCrossRefGoogle Scholar
  9. Cooper SJ, Swanson DL (1994) Seasonal acclimatization of thermoregulation in the black-capped chickadee. Condor 96:638–646CrossRefGoogle Scholar
  10. Dawson WR, Carey C (1976) Seasonal acclimation to temperature in Cardueline finches. J Comp Physiol 112:317–333CrossRefGoogle Scholar
  11. Dawson WR, Buttemer WA, Carey C (1985) A reexamination of the metabolic response of house finches to temperature. Condor 87:424–427CrossRefGoogle Scholar
  12. Doucette LI, Geiser F (2008) Seasonal variation in thermal energetics of the Australian owlet-nightjar (Aegotheles cristatus). Comp Biochem Physiol A 151:615–620CrossRefGoogle Scholar
  13. 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 37:144–150CrossRefGoogle Scholar
  14. 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 320:1763–1768PubMedCrossRefGoogle Scholar
  15. Hart JS (1962) Seasonal acclimatization in four species of small wild birds. Physiol Zool 35:224–236Google Scholar
  16. Jetz W, Thomas GE, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491:444–448PubMedCrossRefGoogle Scholar
  17. 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):279–288CrossRefGoogle Scholar
  18. Liknes ET, Scott SM, Swanson DL (2002) Seasonal acclimatization in the American Goldfinch revisited: to what extent do metabolic rates vary seasonally? Condor 104:548–557CrossRefGoogle Scholar
  19. 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 54:23–30CrossRefGoogle Scholar
  20. 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):190–199CrossRefGoogle Scholar
  21. Lindsay CV, Downs CT, Brown M (2009b) Physiological variation in amethyst sunbirds (Chalcomitra amethystina) over an altitudinal gradient in winter. J Exp Biol 212:483–493PubMedCrossRefGoogle Scholar
  22. 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 Google Scholar
  23. Lovegrove BG (2000) The zoogeography of mammalian basal metabolic rate. Am Nat 156(2):201–219PubMedCrossRefGoogle Scholar
  24. 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 169:453–460PubMedCrossRefGoogle Scholar
  25. 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 181:1075–1087PubMedCrossRefGoogle Scholar
  26. Maddison WP, Maddison DR (2011) Mesquite: a modular system for evolutionary analysis. Version 2.75 http://mesquiteproject.org
  27. Maddocks TA, Geiser F (2000) Seasonal variations in thermal energetics of Australian silvereyes (Zosterops lateralis). J Zool Lond 252(3):327–333CrossRefGoogle Scholar
  28. 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):335–343PubMedCrossRefGoogle Scholar
  29. McKechnie AE (2008) Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J Comp Physiol B 178:235–247PubMedCrossRefGoogle Scholar
  30. Merola-Zwartjes M, Ligon JD (2000) Ecological energetics of the Puerto Rican tody: heterothermy, torpor and intra-island variation. Ecology 81(4):990–1002CrossRefGoogle Scholar
  31. 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 217:1363–1369PubMedCrossRefGoogle Scholar
  32. Montgomerie R, Lyon B, Holder K (2001) Dirty ptarmigan: behavioral modification of conspicuous male plumage. Behav Ecol 12(4):429–438CrossRefGoogle Scholar
  33. 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):100–104CrossRefGoogle Scholar
  34. O’Connor TP (1995) Metabolic characteristics and body composition in house finches: effects of seasonal acclimatization. J Comp Physiol B 165:298–305CrossRefGoogle Scholar
  35. O’Connor TP (1996) Geographic variation in metabolic seasonal acclimatization in house finches. Condor 98:371–381CrossRefGoogle Scholar
  36. 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 3:145–151Google Scholar
  37. 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):289–290CrossRefGoogle Scholar
  38. 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):e113617PubMedPubMedCentralCrossRefGoogle Scholar
  39. Pohl H (1971) Seasonal variation in metabolic functions of bramblings. Ibis 113:185–193CrossRefGoogle Scholar
  40. 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:851–867CrossRefGoogle Scholar
  41. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  42. 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):1047–1071CrossRefGoogle Scholar
  43. 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
  44. Rising JD, Hudson JW (1974) Seasonal variation in the metabolism and thyroid activity of the black-capped chickadee (Parus atricapillus). Condor 76:198–203CrossRefGoogle Scholar
  45. 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 165:366–376CrossRefGoogle Scholar
  46. 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 215:2418–2424PubMedCrossRefGoogle Scholar
  47. Sharbaugh SM (2001) Seasonal acclimatization to extreme climatic conditions by black-capped chickadees (Poecile atricapilla) in interior Alaska (64ºN). Physiol Biochem Zool 74(4):568–575PubMedCrossRefGoogle Scholar
  48. 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 24:330–339CrossRefGoogle Scholar
  49. Smith CC, Reichman OJ (1984) The evolution of food caching by birds and mammals. Annu Rev Ecol Syst 15:329–351CrossRefGoogle Scholar
  50. Southwick EE (1980) Seasonal thermoregulatory adjustments in white-crowned sparrows. Auk 97:76–85Google Scholar
  51. Swanson DL (1990) Seasonal variation in cold hardiness and peak rates of cold-induced thermogenesis in the dark-eyed junco (Junco hyemalis). Auk 107:561–566Google Scholar
  52. Swanson DL (1991) Seasonal adjustments in metabolism and insulation in the Dark-eyed Junco. Condor 93:538–545CrossRefGoogle Scholar
  53. Swanson DL (2010) Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr Ornithol 17:75–129Google Scholar
  54. Swanson DL, Garland T (2009) The evolution of high summit metabolism and cold tolerance in birds and its impact on present-day distributions. Evolution 63:184–194PubMedCrossRefGoogle Scholar
  55. Swanson DL, Liknes ET (2006) A comparative analysis of thermogenic capacity and cold tolerance in small birds. J Exp Biol 209:466–474PubMedCrossRefGoogle Scholar
  56. Swanson DL, Olmstead KL (1999) Evidence for a proximate influence of winter temperatures on metabolism in passerine birds. Physiol Biochem Zool 72(5):566–575PubMedCrossRefGoogle Scholar
  57. Swanson DL, Weinacht DP (1997) Seasonal effects on metabolism and thermoregulation in northern bobwhite. Condor 99:478–489CrossRefGoogle Scholar
  58. 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):19–26PubMedCrossRefGoogle Scholar
  59. Weathers WW, Caccamise DF (1978) Seasonal acclimatization to temperature in monk parakeets. Oecologia 35:173–183CrossRefGoogle Scholar
  60. Wells ME, Schaeffer PJ (2012) Seasonality of peak metabolic rate in non-migrant tropical birds. J Avian Biol 43:481–485CrossRefGoogle Scholar
  61. Wiersma P, Chappell MA, Williams JB (2007a) Cold- and exercise-induced peak metabolic rates in tropical birds. Proc Natl Acad Sci USA 104(52):20866–20871PubMedPubMedCentralCrossRefGoogle Scholar
  62. 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):9340–9345PubMedPubMedCentralCrossRefGoogle Scholar
  63. Wijnandts H (1984) Ecological energetics of the long-eared owl (Asio otus). Ardea 72:1–92Google Scholar
  64. 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 36:167–172CrossRefGoogle Scholar
  65. Withers PC (1992) Comparative animal physiology. Saunders College Publishing, Fort WorthGoogle Scholar
  66. 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 33:315–319CrossRefGoogle Scholar
  67. 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):519–525CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2015

Authors and Affiliations

  • Andrew E. McKechnie
    • 1
  • Matthew J. Noakes
    • 1
  • Ben Smit
    • 2
  1. 1.DST-NRF Centre of Excellence at the Percy FitzPatrick Institute, Department of Zoology and EntomologyUniversity of PretoriaHatfieldSouth Africa
  2. 2.Centre for African Conservation Ecology, Department of ZoologyNelson Mandela Metropolitan UniversityPort ElizabethSouth Africa

Personalised recommendations