Journal of Ornithology

, Volume 154, Issue 1, pp 119–127 | Cite as

Seasonal phenotypic flexibility of flight muscle size in small birds: a comparison of ultrasonography and tissue mass measurements

Original Article


Changes in flight muscle size are important mediators of phenotypic flexibility in birds, so the ability to track such changes over time in individual birds is a valuable tool for investigating phenotypic flexibility. Ultrasonography has been used to track changes in flight muscle size in shorebirds, but has not been previously used to track such changes in small birds, despite variation in flight muscle size being an important contributor to phenotypic flexibility in these birds. One prominent avian example of phenotypic flexibility is the seasonal phenotypes of small birds in response to climatic variation. The winter phenotype in these birds is characterized by increases in organismal metabolic rates and pectoralis muscle mass. We measured seasonal flight muscle size in House Sparrows (Passer domesticus, 25–30 g) using both ultrasonography and wet muscle mass and tested the correlation between ultrasonographic measures of breast muscle thickness and muscle mass. We further tested whether ultrasonographic measures of muscle thickness were sufficiently precise to detect seasonal variation in flight muscle mass. Muscle mass was significantly and positively associated with ultrasonographic measurements of breast muscle thickness for short-axis (SA), long-axis (LA), and combined SA and LA measurements. Breast muscle mass was significantly greater in winter than in summer (17.5 %) and muscle thickness also increased significantly in winter for both SA (9.1 %) and LA (7.5 %) measures. Thus, these data confirm that winter elevations of flight muscle mass consistently contribute to the winter phenotype in House Sparrows and that ultrasonography is effective in detecting seasonal changes in muscle mass in small birds.


Phenotypic flexibility Pectoralis Acclimatization Winter Ultrasonography House Sparrow 


Jahreszeitliche phänotypische Flexibilität in der Größe der Flugmuskulatur bei kleinen Vögeln: Ein Vergleich von Maßen anhand von Ultraschall und Gewebegewicht

Veränderungen der Flugmuskulatur von Vögeln sind wichtige Mediatoren phänotypischer Flexibilität. Von daher ist die Möglichkeit, derartige zeitliche Veränderungen in individuellen Vögeln zu messen ein sehr hilfreich um phänotypische Flexibilität zu untersuchen. Mittels Ultraschalls können Veränderungen in der Flugmuskulatur von Seevögeln gemessen werden. Diese Methode wurde jedoch bis jetzt noch nicht in Singvögeln genutzt, und das obwohl Variation in der Größe von Flugmuskeln in diesen Arten ein wichtiger Indikator von phänotypischer Flexibilität ist. Ein bekanntes Beispiel von phänotypischer Flexibilität in der Ornithologie sind die saisonalen Veränderungen von Phänotypen kleiner Vögel als Reaktion auf Klimavariation. Die winterlichen Phänotypen dieser Vögel sind durch einen Anstieg physiologischer Umsatzraten und des Gewichtes des Pectoralis Muskels geprägt. Wir haben die saisonale Größe der Flugmuskulatur in Haussperlingen (Passer domesticus, 25–30 g) mittels Ultraschalls sowie durch Bestimmung der Dicke und des Nassgewichtes, sowie die Korrelation zwischen beiden bestimmt. Ferner haben wir untersucht ob die Ultraschallmessung der Dicke der Muskeln die saisonale Veränderung in der Masse der Flugmuskeln vorhersagen kann. Muskelmasse war signifikant positiv mit den Ultraschallmaßen short-axis (SA), long-axis (LA) und einer Kombination von SA und LA assoziiert. Die Masse des Brustmuskels war im Winter signifikant höher als im Sommer (17.5 %). Ebenso nahm die Dicke der Muskeln während des Winters zu (SA: 9.1 %, LS: 7.5 %). Unsere Daten unterstützen dass die Zunahme der Flugmuskulatur während des Winters konsistent zum Winterphänotyp von Haussperlingen beitragen, und ferner, dass Ultraschall ausreichend effektiv ist um saisonale Veränderungen in der Muskelmasse kleiner Vögel zu detektieren.


  1. Arens JR, Cooper SJ (2005) Metabolic and ventilatory acclimatization to cold stress in house sparrows (Passer domesticus). Physiol Biochem Zool 78:579–589PubMedCrossRefGoogle Scholar
  2. Baggott GK (1975) Moult, flight muscle “hypertrophy” and premigratory lipid deposition of the juvenile Willow warbler, Phylloscopus trochilus. J Zool 175:299–314Google Scholar
  3. Bairlein F (1995) Manual of field methods ESF (
  4. Bauchinger U, McWilliams SR, Kolb H, Popenko VM, Price ER, Biebach H (2011) Flight muscle shape reliably predicts flight muscle mass of migratory songbirds: a new tool for field ornithologists. J Ornithol 152:507–514CrossRefGoogle Scholar
  5. Carrascal LM, Senar JC, Mozetich I, Uribe F, Domènech J (1998) Interactions among environmental stress, body condition, nutritional status, and dominance in great tits. Auk 115:727–738CrossRefGoogle Scholar
  6. Constantini D, Cardinale M, Carere C (2007) Oxidative damage and anti-oxidant capacity in two migratory bird species at a stop-over site. Comp Biochem Physiol C 144:363–371Google Scholar
  7. Cooper SJ (2002) Seasonal metabolic acclimatization in mountain chickadees and juniper titmice. Physiol Biochem Zool 75:386–395PubMedCrossRefGoogle Scholar
  8. Dawson WR, O’Connor TP (1996) Energetic features of avian thermoregulatory responses. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman & Hall, New York, pp 85–124CrossRefGoogle Scholar
  9. Dietz MW, Dekinga A, Piersma T, Verhulst S (1999) Estimating organ size in small migrating shorebirds with ultrasonography: an intercalibration exercise. Physiol Biochem Zool 72:28–37PubMedCrossRefGoogle Scholar
  10. Engstrand SM, Bryant DM (2002) A trade-off between clutch size and incubation efficiency in the barn swallow Hirundo rustica. Funct Ecol 16:782–791CrossRefGoogle Scholar
  11. Evans PR, Davidson NC, Uttley JD, Evans RD (1992) Premigratory hypertrophy of flight muscles: an ultrastructural study. Ornis Scand 23:238–243CrossRefGoogle Scholar
  12. Gosler AG, Harper DGC (2000) Assessing the heritability of body condition in birds: a challenge exemplified by the great tit, Parus major L. (Aves). Biol J Linn Soc 71:103–117CrossRefGoogle Scholar
  13. Guglielmo CG, Williams TD (2003) Phenotypic flexibility of body composition in relation to migratory state, age and sex in the western sandpiper. Physiol Biochem Zool 76:84–98Google Scholar
  14. Hart JS (1962) Seasonal acclimatization in four species of small wild birds. Physiol Zool 35:224–236Google Scholar
  15. Hohtola E (1982) Thermal and electromyographic correlates of shivering thermogenesis in the pigeon. Comp Biochem Physiol 73A:159–166CrossRefGoogle Scholar
  16. Köver G, Romvari R, Horn P, Berenyi E, Jensen JF, Sørensen P (1998) In vivo assessment of breast muscle, abdominal fat and total fat volume in meat-type chickens by magnetic resonance imaging. Acta Vet Hungar 46:135–144Google Scholar
  17. Landys-Ciannelli MM, Piersma T, Jukema J (2003) Strategic size changes of internal organs and muscle tissue in the Bar-tailed Godwit during fat storage on a spring stopover site. Funct Ecol 17:151–159Google Scholar
  18. Lessels CM, Boag PT (1987) Unreapeatable repeatabilities: a common mistake. Auk 104:116–121Google Scholar
  19. Liknes ET, Swanson DL (2011) Phenotypic flexibility of body composition associated with seasonal acclimatization of passerine birds. J Therm Biol 36:363–370CrossRefGoogle Scholar
  20. Lindström Å, Kvist A, Piersma T, Dekinga A, Dietz M (2000) Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J Exp Biol 203:913–919PubMedGoogle Scholar
  21. Marjoniemi K, Hohtola E (1999) Shivering thermogenesis in leg and breast muscles of Galliform chicks and nestlings of the domestic pigeon. Physiol Biochem Zool 72:484–492PubMedCrossRefGoogle Scholar
  22. Marsh RL (1984) Adaptations of the Gray Catbird Dumetella carolinensis to long-distance migration: flight muscle hypertrophy associated with elevated body mass. Physiol Zool 57:105–117Google Scholar
  23. 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 205–253CrossRefGoogle Scholar
  24. McKechnie AE, Swanson DL (2010) Sources and significance of variation in basal, summit and maximal metabolic rates in birds. Curr Zool 56:741–758Google Scholar
  25. Newton SF (1993) Body condition of a small passerine bird: ultrasonic assessment and significance in overwinter survival. J Zool Lond 229:561–580CrossRefGoogle Scholar
  26. O’Connor TP (1995) Metabolic characteristics and body composition in house finches: effects of seasonal acclimatization. J Comp Physiol B 165:298–305CrossRefGoogle Scholar
  27. Piersma T, Dietz MW (2007) Twofold seasonal variation in the supposedly constant, species-specific ratio of upstroke to downstroke flight muscles in red knots Calidris canutus. J Avian Biol 38:536–540Google Scholar
  28. Piersma T, van Gils JA (2011) The flexible phenotype: a body-centred integration of ecology, physiology, and behavior. Oxford University Press, OxfordGoogle Scholar
  29. Piersma T, Gudmundsson GA, Lilliendahl K (1999) Rapid changes in the size of different functional organ and muscle groups during refueling in a long-distance migrating shorebird. Physiol Biochem Zool 72:405–415PubMedCrossRefGoogle Scholar
  30. Potti J, Moreno J, Merino S, Frias O, Rodriquez R (1999) Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca. Oecologia 120:1–8CrossRefGoogle Scholar
  31. Pyle P (1997) Identification guide to North American birds. Slate Creek Press, Bolinas, California, USA, Part I. Columbidae to PloceidaeGoogle Scholar
  32. Rae LR, Mitchell GW, Mauck RA, Guglielmo CG, Norris DR (2009) Radio transmitters do not affect the body condition of savannah sparrows during the fall premigratory period. J Field Ornithol 80:419–426CrossRefGoogle Scholar
  33. Senar JC, Conroy MJ, Carrascal LM, Domènech J, Mozetich I, Uribe F (1999) Identifying sources of heterogeneity in capture probabilities: an example using the Great Tit Parus major. Bird Study 46(suppl.):S248–S252Google Scholar
  34. Senar JC, Domènech J, Uribe F (2002) Great Tits (Parus major) reduce body mass in response to wing area reduction: a field experiment. Behav Ecol 13:725-727Google Scholar
  35. Swanson DL (1991) Substrate metabolism under cold stress in seasonally acclimatized dark-eyed juncos. Physiol Zool 64:1578–1592Google Scholar
  36. Swanson DL (2001) Are summit metabolism and thermogenic endurance correlated in winter acclimatized passerine birds? J Comp Physiol B 171:475–481PubMedCrossRefGoogle Scholar
  37. Swanson DL (2010) Seasonal metabolic variation in birds: functional and mechanistic correlates. Curr Ornithol 17:75–129Google Scholar
  38. Swanson DL, Liknes ET (2006) A comparative analysis of thermogenic capacity and cold tolerance in small birds. J Exp Bio. 209:466–474CrossRefGoogle Scholar
  39. Tallman DT, Swanson DL, Palmer JS (2002) Birds of South Dakota, 3rd edn. South Dakota Ornithologists’ Union, AberdeenGoogle Scholar
  40. Vézina F, Williams TD (2003) Plasticity in body composition in breeding birds: what drives the metabolic costs of egg production? Physiol Biochem Zool 76:716–773PubMedCrossRefGoogle Scholar
  41. Vézina F, Williams TD (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 19:119–128CrossRefGoogle Scholar
  42. 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 209:3141–3154PubMedCrossRefGoogle Scholar
  43. Vézina F, Jalvingh KM, Dekinga A, Piersma T (2007) Thermogenic side effects to migratory disposition in shorebirds. Am J Physiol Regul Integr Comp Physiol 292:1287–1297CrossRefGoogle Scholar
  44. 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 51:394–408PubMedCrossRefGoogle Scholar
  45. Ward S (1996) Energy expenditure of female barn swallows Hirundo rustica during egg formation. Physiol Zool 69:930–951Google Scholar
  46. Winkler DW, Allen PE (1995) Effects of handicapping on female condition and reproduction in tree swallows (Tachycineta bicolor). Auk 112:737–747Google Scholar
  47. Winkler DW, Allen PE (1996) The seasonal decline in tree swallow clutch size: physiological constraint or strategic adjustment? Ecology 77:922–932CrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of South DakotaVermillionUSA

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