Annual cycles of metabolic rate are genetically determined but can be shifted by phenotypic flexibility

Journal of Experimental Biology

Volumn 215, Issue 19, 2012, Pages 3459-3466

  Versteegh, M A ^a   Helm, B ^b,c   Gwinner, E ^b   Tieleman, B I ^a,b  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b MAX PLANCK INSTITUTE FOR ORNITHOLOGY   (Germany)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Annual cycle; Birds; Common garden; Metabolic rate; Temperature

Indexed keywords

ANIMAL; ARTICLE; BASAL METABOLIC RATE; BODY WEIGHT; GENETICS; HYBRIDIZATION; PHENOTYPE; PHYSIOLOGY; SEASON; SONGBIRD; SPECIES DIFFERENCE; TEMPERATURE;

ANIMALS; BASAL METABOLISM; BODY WEIGHT; HYBRIDIZATION, GENETIC; PASSERIFORMES; PHENOTYPE; SEASONS; SPECIES SPECIFICITY; TEMPERATURE;

AVES; SAXICOLA TORQUATA;

EID: 84866244913     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.073445     Document Type: Article

References (68)

1. Ambrose, S. J. and Bradshaw, S. D. (1988). The water and electrolyte metabolism of free-rangeing and captive white-browed scrubwrens, sericornis frontalis (acanthizidae), from arid, semi-arid and mesic environments. Aust. J. Zool. 36, 29-51.
2. Bauchinger, U., Wohlmann, A. and Biebach, H. (2005). Flexible remodeling of organ size during spring migration of the garden warbler (Sylvia borin). Zoology 108, 97-106.
3. Broggi, J., Hohtola, E., Koivalu, K., Orell, M., Thomson, R. L. and Nilsson, J.-Å. (2007). Sources of variation in winter basal metabolic rate in the great tit. Funct. Ecol. 21, 528-533.
4. Bush, N. G., Brown, M. and Downs, C. T. (2008). Seasonal effects on thermoregulatory responses of the rock kestrel, Falco rupicolis. J. Therm. Biol. 33, 404-412.
5. Chamane, S. C. and Downs, C. T. (2009). Seasonal effects on metabolism and thermoregulation abilities of the red-winged starling (Onychognathus morio). J. Therm. Biol. 34, 337-341.
6. Cooper, S. J. (2000). Seasonal energetics of mountain chickadees and juniper titmice. Condor 102, 635-644.
7. Cooper, S. J. and Swanson, D. L. (1994). Seassonal acclimatization of thermoregulation in the black-capped chickadee. Condor 96, 638-646.
8. Daan, S., Masman, D. and Groenewold, A. (1990). Avian basal metabolic rates: their association with body composition and energy expenditure in nature. Am. J. Physiol. 259, R333-R340.
9. Dawson, W. (2003). Plasticity in avian responses to thermal challenges - an essay in honor of Jacob Marder. Isr. J. Zool. 49, 95-109.
10. Deerenberg, C., Overkamp, G. J. F., Visser, G. H. and Daan, S. (1998). Compensation in resting metabolism for experimentally increased activity. J. Comp. Physiol. B 168, 507-512.
11. Dietz, M. W., Daan, S. and Masman, D. (1992). Energy requirements for molt in the kestrel Falco tinnunculus. Physiol. Zool. 65, 1217-1235.
12. Dietz, M. W., Piersma, T. and Dekinga, A. (1999). Body-building without power training: endogenously regulated pectoral muscle hypertrophy in confined shorebirds. J. Exp. Biol. 202, 2831-2837.
13. Dittami, J. P. and Gwinner, E. (1985). Annual cycles in the African stonechat, Saxicola torquata axillaris, and their relationship to environmental factors. J. Zool. 207, 357-370.
14. Doucette, L. I. and Geiser, F. (2008). Seasonal variation in thermal energetics of the Australian owlet-nightjar (Aegotheles cristatus). Comp. Biochem. Physiol. 151A, 615-620.
15. Flinks, H. and Pfeifer, F. (1987). Brutzeit, Gelegegröße und Bruterfolg beim Schwarzkehlchen (Saxicola torquata). Charadrius 23, 128-140.
16. Gessaman, J. A. (1987). Energetics. In Raptor Management Techniques Manual. National Wildlife Federation Scientific and Technical Series, pp. 289-320. Washington, DC: National Wildlife Federation Scientific and Technical Series.
17. Gwinner, E. (1996). Circadian and circannual programmes in avian migration. J. Exp. Biol. 199, 39-48.
18. Gwinner, E., Neusser, V., and Schmidt, E. (1987). Haltung, Zucht und Eiaufzucht Afrikanischer und Europäischer Schwarzkehlchen Saxicola torquata. Gefederte Welt, 111, 118-120.
19. Gwinner, E., König, S. and Haley, C. (1995a). Genetic and environmental factors influencing clutch size in equatorial and temperate zone stonechats (Saxicola torquata axillaris and S. t. rubicola): An experimental study. Auk 112, 748-755.
20. Gwinner, E., König, S. and Zeman, M. (1995b). Endogenous gonadal, LH and molt rhythms in tropical stonechats: effect of pair bond on period, amplitude, and pattern of circannual cycles. J. Comp. Physiol. 177, 73-79.
21. Hahn, T. P. and MacDougall-Shackleton, S. A. (2008). Adaptive specialization, conditional plasticity and phylogenetic history in the reproductive cue response systems of birds. Philos. Trans. R. Soc. Lond. B 363, 267-286.
22. Helm, B. (2009). Geographically distinct reproductive schedules in a changing world: costly implications in captive stonechats. Integr. Comp. Biol. 49, 563-579.
23. Helm, B., Gwinner, E. and Trost, L. (2005). Flexible seasonal timing and migratory behavior: results from stonechat breeding programs. Ann. N. Y. Acad. Sci. 1046, 216-227.
24. Helm, B., Fiedler, W. and Callion, J. (2006). Movements of European stonechats Saxicola torquata according to ringing recoveries. Ardea 94, 33-44.
25. Helm, B., Schwabl, I. and Gwinner, E. (2009). Circannual basis of geographically distinct bird schedules. J. Exp. Biol. 212, 1259-1269.
26. Hume, I. D. and Biebach, H. (1996). Digestive tract function in the long-distance migratory garden warbler, Sylvia borin. J. Comp. Physiol. B 166, 388-395.
27. Kersten, M., Bruinzeel, L. W., Wiersma, P. and Piersma, T. (1998). Reduced basal metabolic rate of migratory waders wintering in coastal Africa. Ardea 86, 71-80.
28. King, J. R. (1974). Seasonal allocation of time and energy resources in birds. In Avian Energetics (ed. R. A. Paynter), pp. 4-85. Cambridge, MA: Nutall Ornithology Club.
29. Klaassen, M. (1995). Moult and basal metabolic costs in males of two subspecies of stonechats: the European Saxicola torquata rubicula and the East African S. t. axillaris. Oecologia 104, 424-432.
30. König, S. and Gwinner, E. (1995). Frequency and timing of successive broods in captive African and European stonechats Saxicola torquata axillaris and S. t. rubicola. J. Avian Biol. 26, 247-254.
31. Kvist, A. and Lindström, Å. (2001). Basal metabolic rate in migratory waders: intraindividual, intraspecific, interspecific and seasonal variation. Funct. Ecol. 15, 465-473.
32. Lindström, Å. (1997). Basal metabolic rates of migrating waders in the Eurasian Arctic. J. Avian Biol. 28, 87-92.
33. Lindström, Å., Visser, G. H. and Daan, S. (1993). The energetic cost of feather synthesis is proportional to basal metabolic rate. Physiol. Zool. 66, 490-510.
34. Looney, S. W. and Stanley, W. B. (1989). Exploratory repeated measures analysis for 2 or more groups - review and update. Am. Stat. 43, 220-225.
35. Maddocks, T. A. and Geiser, F. (2000). Seasonal variations in thermal energetics of Australian silvereyes (Zosterops lateralis). J. Zool. (Lond.) 252, 327-333.
36. Maldonado, K. E., Cavieres, G., Veloso, C., Canals, M. and Sabat, P. (2009). Physiological responses in rufous-collared sparrows to thermal acclimation and seasonal acclimatization. J. Comp. Physiol. B 179, 335-343.
37. McKechnie, A. E. (2008). Phenotypic flexibility in basal metabolic rate and the changing view of avian physiological diversity: a review. J. Comp. Physiol. B 178, 235-247.
38. McNab, B. K. (1988). Food habits and the basal rate of metabolism in birds. Oecologia 77, 343-349.
39. Mueller, P. and Diamond, J. (2001). Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proc. Biol. Sci. 98, 12550-12554.
40. Nilsson, J.-A. (2002). Metabolic consequences of hard work. Proc. Biol. Sci. 269, 1735-1739.
41. Nudds, R. L. and Bryant, D. M. (2001). Exercise training lowers the resting metabolic rate of zebra finches, Taeniopygia guttata. Funct. Ecol. 15, 458-464.
42. Pearson, D. J. and Lack, P. C. (1992). Migration patterns and habitat use by passerine and near-passerine migrant birds in eastern Africa. Ibis 134, 89-98.
43. Piersma, T. and Drent, J. (2003). Phenotypic flexibility and the evolution of organismal design. Trends Ecol. Evol. 18, 228-233.
44. Piersma, T., Cadée, N. and Daan, S. (1995). Seasonality in basal metabolic rate and thermal conductance in a long-distance migrant shorebird, the knot (Calidris canutus). J. Comp. Physiol. B 165, 37-45.
45. Piersma, T., Bruinzeel, L., Drent, R., Kersten, M., VanderMeer, J. and Wiersma, P. (1996). Variability in basal metabolic rate of a long-distance migrant shorebird (red knot, Calidris canutus) reflects shifts in organ sizes. Physiol. Zool. 69, 191-217.
46. Piersma, T., Gudmundsson, G. A. and Lilliendahl, K. (1999). Rapid changes in the size of different functional organ and muscle groups during refueling in a longdistance migrating shorebird. Physiol. Biochem. Zool. 72, 405-415.
47. R Development Core Team (2010). R: a language and environment for statistical computing. Available at: http://www.R-project.org.
48. Raess, M. (2008). Continental efforts: migration speed in spring and autumn in an inner-Asian migrant. J. Avian Biol. 39, 13-18.
49. Ricklefs, R. E. and Wikelski, M. (2002). The physiology/life-history nexus. Trends Ecol. Evol. 17, 462-468.
50. Schaub, M. and Jenni, L. (2000). Body mass of six long-distance migrant passerine species along the autumn migration route. J. Ornithol. 141, 441-460.
51. Smit, B. and McKechnie, A. E. (2010). Avian seasonal metabolic variation in a subtropical desert: basal metabolic rates are lower in winter than in summer. Funct. Ecol. 24, 330-339.
52. Speakman, J. R. (2005). Body size, energy metabolism and lifespan. J. Exp. Biol. 208, 1717-1730.
53. Swanson, D. L. (2010). Seasonal metabolic variation in birds: functional and mechanistic correlates, Chap. 3. In Current Ornithology, Vol. 17 (ed. Thompson, C. F.), pp. 75-129. New York: Springer.
54. Swanson, D. L. and Dean, K. L. (1999). Migration-induced variation in thermogenic capacity in migratory passerines. J. Avian Biol. 30, 245.
55. Swanson, D. L. and Olmstead, K. L. (1999). Evidence for a proximate influence of winter temperature on metabolism in passerine birds. Physiol. Biochem. Zool. 72, 566-575.
56. Tieleman, B. I. (2007). Differences in the physiological responses to temperature among stonechats from three populations reared in a common environment. Comp. Biochem. Physiol. 146A, 194-199.
57. Tieleman, B. I., Williams, J. B., Buschur, M. E. and Brown, C. R. (2003). Phenotypic variation of larks along an aridity gradient: are desert birds more flexible? Ecology 84, 1800-1815.
58. Tieleman, B. I., Dijkstra, T. H., Klasing, K. C., Visser, G. H. and Williams, J. B. (2008). Effects of experimentally increased costs of activity during reproduction on parental investment and self-maintenance in tropical house wrens. Behav. Ecol. 19, 949-959.
59. Tieleman, B. I., Versteegh, M. A., Fries, A., Helm, B., Dingemanse, N. J., Gibbs, H. L. and Williams, J. B. (2009a). Genetic modulation of energy metabolism in birds through mitochondrial function. Proc. Biol. Sci. 276, 1685-1693.
60. Tieleman, B., Versteegh, M., Helm, B. and Dingemanse, N. (2009b). Quantitative genetics parameters show partial independent evolutionary potential for body mass and metabolism in stonechats from different populations. J. Zool. (Lond.) 279, 129-136.
61. Turesson, G. (1922). The genotypical response of the plant species to the habitat. Hereditas 3, 211-350.
62. Urquhart, E. (2002). Stonechats. A Guide to the Genus Saxicola. London: Christoffer Helm.
63. Versteegh, M. A., Helm, B., Dingemanse, N. J. and Tieleman, B. I. (2008). Repeatability and individual correlates of basal metabolic rate and total evaporative water loss in birds: a case study in European stonechats. Comp. Biochem. Physiol. 150A, 452-457.
64. Vézina, F. and Williams, T. D. (2005). Interaction between organ mass and citrate synthase activity as an indicator of tissue maximal oxidative capacity in breeding European starlings: implications for metabolic rate and organ mass relationships. Funct. Ecol. 19, 119-128.
65. Vézina, F., Jalvingh, K. M., Dekinga, A. and Piersma, T. (2007). Thermogenic side effects to migratory predisposition in shorebirds. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R1287-R1297.
66. Vézina, F., Dekinga, A. and 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.
67. Wikelski, M., Spinney, L., Schelsky, W., Scheuerlein, A. and Gwinner, E. (2003). Slow pace of life in tropical sedentary birds: a common-garden experiment on four stonechat populations from different latitudes. Proc. Biol. Sci. 270, 2383-2388.
68. Zheng, W.-H., Li, M., Liu, J.-S. and Shao, S.-L. (2008). Seasonal acclimatization of metabolism in Eurasian tree sparrows (Passer montanus). Comp. Biochem. Physiol. 151A, 519-525.