Advertisement

Moult-related reduction of aerobic scope in passerine birds

  • William A. ButtemerEmail author
  • Silke Bauer
  • Tamara Emmenegger
  • Dimitar Dimitrov
  • Strahil Peev
  • Steffen Hahn
Original Paper

Abstract

It is well established that the nutrient and energy requirements of birds increase substantially during moult, but it is not known if these increased demands affect their aerobic capacity. We quantified the absolute aerobic scope of house and Spanish sparrows, Passer domesticus and P. hispaniolensis, respectively, before and during sequential stages of their moult period. The absolute aerobic scope (AAS) is the difference between maximum metabolic rate (MMR) during peak locomotor activities and minimum resting metabolic rate (RMRmin), thus representing the amount of aerobic power above that committed to maintenance needs available for other activities. As expected, RMRmin increased over the moult period by up to 40 and 63% in house and Spanish sparrows, respectively. Surprisingly, the maximum metabolic rates also decreased during moult in both species, declining as much as 25 and 38% compared with pre-moult values of house and Spanish sparrows, respectively. The concurrent changes in RMRmin and MMR during moult resulted in significant decreases in AAS, being up to 32 and 47% lower than pre-moult levels of house and Spanish sparrows, respectively, during moult stages having substantial feather replacement. We argue that the combination of reduced flight efficiency due to loss of wing feathers and reduced aerobic capacity places moulting birds at greater risk of predation. Such performance constraints likely contribute to most birds temporally separating moult from annual events requiring peak physiological capacity such as breeding and migration.

Keywords

Avian moult energetics Aerobic scope Resting metabolic rate Maximum metabolic rate Passer domesticus Passer hispaniolensis 

Notes

Acknowledgements

We thank Pavel Zehtindjiev for facilitating our research at Kalimok Station and Martin Marinov, Katrina Ivanova, and Mihaela Ilieva for animal care assistance, and the four anonymous reviewers for their constructive comments. All experimental procedures were carried out under the permission and guidelines of the Bulgarian Academy of Sciences and the Bulgarian Ministry of Environment and Waters (no. 627/30.03.2015). All birds were released at the end of study. This study is report No. 65 of the Biological Experimental Station ‘Kalimok’.

Author contributions

SH, SB and WAB developed the conceptual framework and analysed the data. SH, TE and WAB made metabolic measurements. SH, SB and WAB wrote the manuscript. DD, SP, SH, TE and WAB captured birds and made morphological measurements.

Funding

This study was supported by the Swiss National Science Foundation (31003A_160265) to S.B. and S.H.

Compliance with ethical standards

Conflict of interest

All authors discussed and approved the manuscript and have no competing interests.

References

  1. Alonso JC (1984) Zur Mauser Spanischer Weiden- und Haussperlinge (Passer hispaniolensis und domesticus). J Orn 125:209–223CrossRefGoogle Scholar
  2. Bishop CM (1999) The maximum oxygen consumption and aerobic scope of birds and mammals: getting to the heart of the matter. Proc R Soc Lond B 266:2275–2281CrossRefGoogle Scholar
  3. Bortolotti GR, Blas J, Negro JJ, Tella JL (2006) A complex plumage pattern as an honest social signal. Anim Behav 72:423–430CrossRefGoogle Scholar
  4. Brett JR (1972) The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Resp Physiol 14:151–170CrossRefGoogle Scholar
  5. Buttemer WA, Hayworth AM, Weathers WW, Nagy KA (1986) Time-budget estimates of avian energy expenditure: Physiological and meteorological considerations. Physiol Zool 59:131–149CrossRefGoogle Scholar
  6. Buttemer WA, Warne S, Bech C, Astheimer LB (2008) Testosterone effects on avian basal metabolic rate and aerobic performance: facts and artefacts. Comp Biochem Physiol 150A:304–310Google Scholar
  7. Careau V, Hoye BJ, O’Dwyer TW, Buttemer WA (2014) Among- and within-individual correlations between basal and maximal metabolic rates in birds. J Exp Biol 217:3593–3596CrossRefGoogle Scholar
  8. Chai P, Dudley R (1999) Maximum flight performance of hummingbirds: capacities, constraints, and trade-offs. Am Nat 153:398–411Google Scholar
  9. Chappell MA, Bech C, Buttemer WA (1999) The relationship of central and peripheral organ masses to aerobic performance variation in house sparrows. J Exp Biol 202:2269–2279Google Scholar
  10. Chappell MA, Savard J-F, Siani J, Coleman SW, Keagy J, Borgia G (2011) Aerobic capacity in wild satin bowerbirds: repeatability and effects of age, sex and condition. J Exp Biol 214:3186–3196CrossRefGoogle Scholar
  11. Dawson A (2006) Control of molt in birds: Association with prolactin and regression in starlings. Gen Comp Endocrinol 147:314–322CrossRefGoogle Scholar
  12. Dawson A, Sharp PJ (1998) The role of prolactin in the development of reproductive photorefractoriness and postnuptial molt in the European starling (Sturnus vulgaris). Endocrinol 139:485–490CrossRefGoogle Scholar
  13. de la Hera I, Hedenstrom A, Pérez-Tris J, Tellería JL (2010) Variation in the mechanical properties of flight feathers of the blackcap Sylvia atricapilla in relation to migration. J Avian Biol 41:342–347CrossRefGoogle Scholar
  14. DesRochers DW, Reed JM, Awerman J, Kluge JA, Wilkinson J, van Griethuijsen LI, Aman J, Romero LM (2009) Exogenous and endogenous corticosterone alter feather quality. Comp Biochem Physiol 152A:46–52CrossRefGoogle Scholar
  15. Dietz MW, Daan S, Masman D (1992) Energy requirements for molt in the kestrel Falco tinnunculus. Physiol Zool 65:1217–1235CrossRefGoogle Scholar
  16. Eck S, Fiebig J, Fiedler W, Heynen I, Nicolai B, Töpfer T, van den Elzen R, Winkler R, Woog F (2011) Vögel vermessen/measuring birds. Deutsche Ornithologen-Gesellschaft. Christ Media Natur, MindenGoogle Scholar
  17. Fitzpatrick S (1998) Colour schemes for birds: structural coloration and signals of quality in feathers. Ann Zool Fenn 35:67–77Google Scholar
  18. Geluso K, Hayes JP (1999) Effects of dietary quality on basal metabolic rate and internal morphology of European starlings (Sturnus vulgaris). Physiol Biochem Zool 72:189–197CrossRefGoogle Scholar
  19. Hahn S, Dimitrov D, Emmenegger T, Ilieva M, Peev S, Zehtindjiev P, Briedis M (2019) Migration, wing morphometry and wing moult in Spanish and house sparrows from the eastern Balkan Peninsula. J Ornithol 160:271–274CrossRefGoogle Scholar
  20. Hayashi K, Kirihara D, Tomita Y (1991) Effects of hypo- and hyperthyroidism on the rates of muscle protein synthesis and breakdown in cockerels. Anim Sci Technol (Jpn) 62:109–113Google Scholar
  21. Hayashi K, Kuroki H, Kamizono T, Ohtsuka A (2009) Comparison of the effects of thyroxine and triiodothyronine on heat production and skeletal muscle breakdown in chicken. J Poult Sci 46:212–216CrossRefGoogle Scholar
  22. Heise CC, Rimmer CC (2000) Definitive prebasic molt of gray catbirds at two sites in New England. Condor 102:894–904CrossRefGoogle Scholar
  23. Hill RW (1972) Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J Appl Physiol 33(2):261–263CrossRefGoogle Scholar
  24. Hinds DS, Baudinette RV, Macmillen RE, Halpern EA (1993) Maximum metabolism and the aerobic factorial scope of endotherms. J Exp Biol 182:41–56Google Scholar
  25. Hoye BJ, Buttemer WA (2011) Inexplicable inefficiency of avian molt? Insights from an opportunistically breeding arid-zone species, Lichenostomus penicillatus. PLoS One 6(2):e16230CrossRefGoogle Scholar
  26. Hudson JW, Kimzey SL (1966) Temperature regulation and metabolic rhythms in populations of the house sparrow, Passer domesticus. Comp Biochem Physiol 17:203–217CrossRefGoogle Scholar
  27. Hulbert AJ, Else PL (2004) Basal metabolic rate: History, composition, regulation, and usefulness. Physiol Biochem Zool 77:869–876CrossRefGoogle Scholar
  28. Jenni-Eiermann S, Jenni L, Piersma T (2002) Temporal uncoupling of thyroid hormones in red knots: T3 peaks in cold weather, T4 during moult. J Ornithol 143:331–340CrossRefGoogle Scholar
  29. Killen SS, Mitchell MD, Rummer JL, Chivers DP, Ferrari MCO, Meekan MG, McCormick MI (2014) Aerobic scope predicts dominance during early life in a tropical damselfish. Funct Ecol 28:1367–1376CrossRefGoogle Scholar
  30. 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 104:424–432CrossRefGoogle Scholar
  31. Lasiewski RC (1963) Oxygen consumption of torpid, resting, active, and flying hummingbirds. Physiol Zool 36:122–140CrossRefGoogle Scholar
  32. Lindström Å, Visser GH, Daan S (1993) The energetic cost of feather synthesis is proportional to metabolic rate. Physiol Zool 66:490–510CrossRefGoogle Scholar
  33. Marras S, Claireaux G, McKenzie DJ, Nelson JA (2010) Individual variation and repeatability in aerobic and anaerobic swimming performance of European seabass, Dicentrarchus labrax. J Exp Biol 213:26–32CrossRefGoogle Scholar
  34. McKechnie AE, Swanson DL (2010) Sources and significance of variation in basal, summit and maximal metabolic rate in birds. Curr Zool 56:741–758Google Scholar
  35. McKittrick J, Chen P-Y, Bodde SG, Yang W (2012) The structure, functions, and mechanical properties of keratin. JOM 64:449–468CrossRefGoogle Scholar
  36. McNabb FMA (2007) The hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction. Crit Rev Toxicol 37:163–193CrossRefGoogle Scholar
  37. Murphy EC (1985) Bergmanns’s rule, seasonality, and geographic variation in body size of house sparrows. Evolution 39:1327–1334CrossRefGoogle Scholar
  38. Murphy ME (1996) Energetics and nutrition of molt. In: Carey C (ed) Avian energetics and nutritional ecology. Plenum Press, New York, pp 158–198CrossRefGoogle Scholar
  39. Murphy ME, King JR, Lu J (1988) Malnutrition during the postnuptial molt of white-crowned sparrows: feather growth and quality. Can J Zool 66:1403–1413CrossRefGoogle Scholar
  40. Neufer PD (1989) The effect of detraining and reduced training on the physiological adaptations to aerobic exercise training. Sports Med 8:302–321CrossRefGoogle Scholar
  41. Newton I (1966) The moult of the bullfinch Pyrrhula pyrrhula. Ibis 108:41–67CrossRefGoogle Scholar
  42. Nilsson J-A, Svensson E (1996) The cost of reproduction: a new link between current reproductive effort and future reproductive success. Proc R Soc Lond B 263:711–714CrossRefGoogle Scholar
  43. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing.Vienna, Austria. https://www.R-project.org/. Accessed 23 Jan 2019
  44. Rolfe DFS, Brown GC (1997) Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol Rev 77:731–758CrossRefGoogle Scholar
  45. Schieltz PC, Murphy ME (1997) The contribution of insulation changes to the energy cost of avian molt. Can J Zool 75(3):396–400CrossRefGoogle Scholar
  46. Schleussner G, Dittami JP, Gwinner E (1985) Testosterone implants affect molt in male European starlings, Sturnus vulgaris. Physiol Zool 58:597–604CrossRefGoogle Scholar
  47. Smith JP (1982) Changes in blood levels of thyroid hormones in two species of passerine birds. Condor 84:160–167CrossRefGoogle Scholar
  48. Taruscio TG, Murphy ME (1995) 3-Methylhistidine excretion by molting and non-molting sparrows. Comp Biochem Physiol 111A:397–403CrossRefGoogle Scholar
  49. Taylor CR, Maloiy GMO, Weibel ER, Langman VA, Kamau JMZ (1980) Design of the mammalian respiratory system. III. Maximum aerobic capacity to body mass: wild and domestic mammals. Resp Physiol 44:25–37CrossRefGoogle Scholar
  50. Torre-Bueno JR, Larochelle J (1978) The metabolic cost of flight in unrestrained birds. J Exp Biol 75:223–229Google Scholar
  51. Tucker V (1968) Respiratory exchange and evaporative water loss in the flying budgerigar. J Exp Biol 48:67–87Google Scholar
  52. Turček FJ (1966) On plumage quality in birds. Ekologia Polska 14:617–633Google Scholar
  53. Vega Rivera JH, McShea WJ, Rappole JH, Haas CA (1998) Pattern and chronology of prebasic molt for the wood thrush and its relation to reproduction and migration departure. Wilson Bull 110:384–392Google Scholar
  54. Vezina F, Gustowska A, Jalvingh KM, Chastel O, Piersma T (2009) Hormonal consequences and thermoregulatory consequences of molting on metabolic rate in a northerly wintering shorebird. Physiol Zool 82:129–142CrossRefGoogle Scholar
  55. Weber TP, Borgudd J, Hedenström A, Persson K, Sandberg G (2004) Resistance of flight feathers to mechanical fatigue covaries with moult strategy in two warbler species. Biol Lett 1:27–30CrossRefGoogle Scholar
  56. Wingfield JC (2008) Organisation of vertebrate annual cycles: implications for control mechanisms. Philos Trans R Soc Lond Ser B Biol Sci 363:425–441CrossRefGoogle Scholar
  57. Zeidler K (1966) Untersuchungen über Flügelbefiederung und Mauser des Haussperlings (Passer domesticus L.). J Ornithol 107:113–153CrossRefGoogle Scholar
  58. Zhang Y, Eyster K, Liu J-S, Swanson DL (2015) Cross-training in birds: cold and exercise training produce similar changes in maximal metabolic output, muscle masses and myostatin expression in house sparrows (Passer domesticus). J Exp Biol 218:2190–2200CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of WollongongWollongongAustralia
  2. 2.Department of Bird MigrationSwiss Ornithological InstituteSempachSwitzerland
  3. 3.Institute of Biodiversity and Ecosystem ResearchBulgarian Academy of SciencesSofiaBulgaria

Personalised recommendations