Migratory body mass increase in Northern Wheatears (Oenanthe oenanthe) is the accumulation of fat as proven by quantitative magnetic resonance

  • Natalie A. KelseyEmail author
  • Franz Bairlein
Original Article


Migratory birds need energy-rich fuel which is primarily gained through fattening. However, it is also hypothesised that birds store excess lean mass as an additional energy reserve during migration. Until now, changes in the fat of live birds could only be determined indirectly through the change in body mass and fat score. Recently, the full-body scanner EchoMRI™ using quantitative magnetic resonance has become available making quick and precise measurements of whole-body compositions of live birds (i.e., fat, lean and water mass) possible without sedating the birds. In this study, the EchoMRI™ was applied on Northern Wheatears Oenanthe oenanthe hatched and reared in captivity during their first autumn migration stage. Results demonstrated that pre-migratory increase in body mass is primarily due to the fattening of the birds, while additional lean mass was not stored.


Body composition Migratory bird Oenanthe oenanthe EchoMRI™ QMR Body mass gain 


Für ihre jährlichen Flüge benötigen Zugvögel energiereichen Treibstoff, der hauptsächlich in Form von Fett angelegt wird. Jedoch wird vermutet, dass auch die Muskelmasse als zusätzliche Energiereserve während des Vogelzuges zunimmt. Bis jetzt war die Bestimmung des Fettgehaltes an lebenden Vögeln nur indirekt anhand der Körpermasse und des Fettscores möglich. Doch seit kurzem erlaubt der Ganzkörperscanner EchoMRI™ mittels quantitativer Magnetresonanz (engl. quantitative magnetic resonance QMR) die Körperzusammensetzung lebender Vögel (d.h. Fett-, Muskelmasse, Wassergehalt) schnell und präzise zu bestimmen, ohne dass die Tiere dafür sediert werden müssen. In dieser Studie wurde mittels des EchoMRI™ der Verlauf der Körperzusammensetzung an in Gefangenschaft aufgezogenen Steinschmätzern Oenanthe oenanthe während ihrer ersten herbstlichen Zugphase untersucht. Die Ergebnisse zeigten, dass die Gewichtszunahme vor der Zugphase hauptsächlich aus Fett besteht und Muskelmasse nicht als zusätzliche Energiereserve angesetzt wurde.



We are grateful to Ulrich Meyer and Adolf Völk for animal husbandry and to Heiko Schmaljohann and Arndt Wellbrock for kindly advising us in the statistical analysis.


Funding was provided by the Ministry for Science and Culture of Lower Saxony (Grant No. 74ZN1477).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Animal housing was approved by Zweckverband Veterinäramt JadeWeser (42508-Te) and supervised by the institute’s Animal Welfare Committee.

Supplementary material

10336_2018_1621_MOESM1_ESM.pdf (449 kb)
Supplementary material 1 (PDF 448 kb)


  1. Bairlein F (1986) Ein standardisiertes Futter für ERnährungsuntersuchungen an omnivoren Kleinvögeln. J Ornithol 127:338–340CrossRefGoogle Scholar
  2. Bairlein F (1991) Body mass of Garden Warblers (Sylvia borin) on migration: a review of field data. Vogelwarte 36:48–61Google Scholar
  3. Bairlein F, Gwinner E (1994) Nutritional mechanisms and temporal control of migratory energy accumulation in birds. Annu Rev Nutr 14:187–215CrossRefGoogle Scholar
  4. Bairlein F, Norris DR, Nagel R, Bulte M, Voigt CC, Fox JW, Hussell DJT, Schmaljohann H (2012) Cross-hemisphere migration of a 25 g songbird. Biol Lett 8:505–507CrossRefGoogle Scholar
  5. Bairlein F, Dierschke V, Delingat J, Eikenaar C, Maggini I, Bulte M, Schmaljohann H (2013) Revealing the control of migratory fuelling. An integrated approach combining laboratory and field studies in Northern Wheatears Oenanthe oenanthe. Curr Zool 59:381–392CrossRefGoogle Scholar
  6. Bairlein F, Dierschke J, Dierschke V, Salewski V, Geiter O, Hüppop K, Köppen U, Fiedler W (2014) Atlas des Vogelzuges. Ringfunde deutscher Brut- und Gastvögel. Aula-Verlag, WiebelsheimGoogle Scholar
  7. Bairlein F, Fritz J, Scope A, Schwendenwein I, Stanclova G, van Dijk G, Meijer HAJ, Verhulst S, Dittami J (2015) Energy expenditure and metabolic changes of free-flying migrating Northern Bald Ibis. PLoS ONE 10:e0134433CrossRefGoogle Scholar
  8. Bartoń K (2018) R Package ‘MuMIn’m. Version 1(42):1Google Scholar
  9. Battley PF, Piersma T, Dietz MW, Tang S, Dekinga A, Hulsman K (2000) Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc Royal Soc London B 267:191–195CrossRefGoogle Scholar
  10. Bauchinger U, Biebach H (2005) Phenotypic flexibility of skeletal muscles during long-distance migration of Garden Warblers: muscle changes are differentially related to body mass. Ann NY Acad Sci 1046:271–281CrossRefGoogle Scholar
  11. Bauchinger U, Wohlmann A, Biebach H (2005) Flexible remodelling of organ size during spring migration of the garden warbler (Sylvia borin). Zoology 108:97–106CrossRefGoogle Scholar
  12. Berthold P (1996) Control of bird migration. Chapman & Hall, LondonGoogle Scholar
  13. Bezzel E, Prinzinger R (1990) Ornithologie. Ulmer, StuttgartGoogle Scholar
  14. Biebach H, Bauchinger U (2003) Energetic savings by organ adjustment during long migratory flights in Garden Warblers (Sylvia borin). In: Berthold P, Gwinner E, Sonnenschein E (eds) Avian migration. Springer, Berlin Heidelberg, pp 269–280CrossRefGoogle Scholar
  15. Blem CR (1976) Patterns of lipid storage and utilization in birds. Am Zool 16:671–684CrossRefGoogle Scholar
  16. Bryant DM, Hails CJ (1983) Energetics and growth patterns of three tropical bird species. Auk 100:425–439Google Scholar
  17. Bulte M, Bairlein F (2013) Endogenous control of migratory behavior in Alaskan Northern Wheatears Oenanthe oeananthe. J Ornithol 154:567–570CrossRefGoogle Scholar
  18. Bulte M, McLaren JD, Bairlein F, Bouten W, Schmaljohann H, Shamoun-Baranes J (2014) Can wheatears weather the Atlantic? Modeling nonstop trans-Atlantic flights of a small migratory songbird. Auk 11:363–370CrossRefGoogle Scholar
  19. Chilgren JD (1977) Body composition of captive White-crowned Sparrows during postnuptial Molt. Auk 94:677–688CrossRefGoogle Scholar
  20. Condor P (1989) The wheatear. Christoph Helm, LondonGoogle Scholar
  21. Connell CE, Odum EP, Kale H (1960) Fat-free weights of birds. Auk 77:1–9CrossRefGoogle Scholar
  22. Conway CJ, Eddleman WR, Simpson KL (1994) Evaluation of lipid indices of the wood thrush. Condor 96:783–790CrossRefGoogle Scholar
  23. Delingat J, Dierschke V, Schmaljohann H, Bairlein F (2009) Diurnal patterns of body mass change during stopover in a migrating songbird, the northern wheatear Oenanthe oenanthe. J Avian Biol 40:625–634CrossRefGoogle Scholar
  24. Dierschke V, Delingat J (2001) Stopover behavior and departure decision of northern wheatears, Oenanthe oenanthe, facing different onward non-stop flight distances. Behav Ecol Sociobiol 50:535–545CrossRefGoogle Scholar
  25. Dierschke V, Mendel B, Schmaljohann H (2005) Differential timing of spring migration in northern wheatears Oenanthe oenanthe: hurried males or weak females? Behav Ecol Sociobiol 57:470–480CrossRefGoogle Scholar
  26. Dierschke J, Dierschke V, Hüppop O, Jachmann KF (2011) Die Vogelwelt der Insel Helgoland. OAG Helgoland, HelgolandGoogle Scholar
  27. Dobush GR, Ankney D, Krementz DG (1985) The effect of apparatus, extraction time, and solvent type on lipid extractions of snow geese. Can J Zool 63:1917–1920CrossRefGoogle Scholar
  28. Dumont ER (2010) Bone density and the lightweight skeletons of birds. Proc Biol Sci 277:2193–2198CrossRefGoogle Scholar
  29. EchoMRI (2016) EchoMRI™ - Corporation Pte Ltd., Body Composition Analysis. Version 2016. Accessed 14 December 2016
  30. Eikenaar C, Klinner T, de Lille T, Bairlein F, Schmaljohann H (2014) Fuel loss and flexible fuel deposition rates in a long-distance migrant. Behav Ecol Sociobiol 68:1465–1471CrossRefGoogle Scholar
  31. Evans PR, Davidson NC, Uttley JD, Evans RD (1992) Premigratory hypertrophy of flight muscles: an ultrastructural study. Ornis Scandinavica 23:238–243CrossRefGoogle Scholar
  32. Fry CH, Ferguson-Lees IJ, Dowsett RJ (1972) Flight muscle hypertrophy and ecophysiological variation of Yellow wagtail Motacilla flava races at Lake Chad. J Zool Lond 167:293–306CrossRefGoogle Scholar
  33. Gerson AR, Guglielmo CG (2011) Flight at low ambient humidity increases protein catabolism in migratory birds. Science 333:1434–1436CrossRefGoogle Scholar
  34. Gerson AR, Guglielmo CG (2013) Energetics and metabolite profiles during early flight in American robins (Turdus Migratorius). J Camp Physiol B 183:983–991CrossRefGoogle Scholar
  35. Guglielmo CG, Williams TD (2003) Phenotypic flexibility of body composition in relation to migratory state, age, and sex in the Western Sandpiper (Calidris mauri). Physiol Biochem Zool 76:84–98CrossRefGoogle Scholar
  36. Guglielmo CG, McGuire LP, Gerson AR, Seewagen CL (2011) Simple, rapid, and non-invasive measurement of fat, lean, and total water masses of live birds using quantitative magnetic resonance. J Ornithol 152:75–85CrossRefGoogle Scholar
  37. Gwinner E (1996) Circadian and circannual programmes in avian migration. J Exp Biol 199:39–48PubMedGoogle Scholar
  38. Harber MP, Konopka AR, Undem MK, Hinkley JM, Minchev K, Kaminsky LA, Trappe TA, Trappe S (2012) Aerobic exercise training induces skeletal muscle hypertrophy and age-dependent adaptations in myofiber function in young and older men. J Appl Physiol 113:1495–1504CrossRefGoogle Scholar
  39. Hedenström A, Fagerlund T, Rosen M, Wirestam R (2009) Magnetic resonance imaging versus chemical fat extraction in small passerine, the willow warbler Phylloscopus trochilus: a fat-score based statistical comparison. J Avian Biol 40:457–460CrossRefGoogle Scholar
  40. Hicks DL (1976) Adipose tissue composition and cell size in fall migratory thrushes (Turdidae). Condor 69:387–399CrossRefGoogle Scholar
  41. Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528CrossRefGoogle Scholar
  42. Kaiser A (1992) Fat deposition and theoretical flight range of small autumn migrants in southern Germany. Bird Study 39:96–110CrossRefGoogle Scholar
  43. Kaiser A (1993) A new multi-category classification of subcutaneous fat deposits of songbirds. J Field Ornithol 64:246–255Google Scholar
  44. Karasov WH (1990) Digestion in birds: chemical and physiological determinants and ecological implications. Stud Avian Biol 13:391–415Google Scholar
  45. Karasov WH, Pinshow B (1998) Changes in lean mass and in organs of nutrient assimilation in a long-distance passerine migrant at a springtime stopover site. Physiol Zool 71:435–448CrossRefGoogle Scholar
  46. Kennedy LV, Morbey YE, Mackenzie SA, Taylor PD, Guglielmo CG (2017) A field test of the effects of body composition analysis by quantitative magnetic resonance on songbird stopover behaviour. J Ornithol 158:593–601CrossRefGoogle Scholar
  47. Klaassen M (1996) Metabolic constraints on long-distance migration in birds. J Exp Biol 199:57–64PubMedGoogle Scholar
  48. Klaassen M, Lindström Å, Zijlstra R (1997) Composition of fuel stores and digestive limitations to fuel deposition rate in the long-distance migratory Thrush Nightingale, Luscinia luscinia. Physiol Zool 70:125–133CrossRefGoogle Scholar
  49. Krementz DG, Pendleton GW (1990) Fat scoring. Sources of variability. Condor 92:500–507CrossRefGoogle Scholar
  50. Lindström Å, Piersma T (1993) Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135:70–78CrossRefGoogle Scholar
  51. Maggini I, Bairlein F (2010) Endogenous rhythms of seasonal migratory body mass changes and nocturnal restlessness in different populations of Northern Wheatear Oenanthe oenanthe. J Biol Rhythms 25:268–276CrossRefGoogle Scholar
  52. Maggini I, Bulte M, Bairlein F (2017) Endogenous control of fuelling in a migratory songbird. Sci Nat 104:93CrossRefGoogle Scholar
  53. McWilliams SR, Whitman M (2013) Non-destructive techniques to assess body composition of birds: a review and validation study. J Ornithol 154:597–618CrossRefGoogle Scholar
  54. Meijer T, Möhring FJ, Trillmich F (1994) Annual and daily variation in body mass and fat of Starlings Sturnus vulgaris. J Avian Biol 25:98–104CrossRefGoogle Scholar
  55. Newton I (2007) The migration ecology of birds. Elsevier Science & Technology, LondonGoogle Scholar
  56. Odum EP (1960) Lipid deposition in nocturnal migrant birds. In: Proceedings of XII international ornithological congress, pp 563–576Google Scholar
  57. Odum EP, Connell CE (1956) Lipid levels in migrating birds. Science 123:892–894CrossRefGoogle Scholar
  58. Odum EP, Connell CE, Stoddard HL (1961) Flight energy and estimated flight ranges of some migratory birds. Auk 78:515–527CrossRefGoogle Scholar
  59. Odum EP, Rogers DT, Hicks DL (1964) Homeostasis of the nonfat components of migrating birds. Science 143:1037–1039CrossRefGoogle Scholar
  60. Piersma T (1990) Pre-migratory “fattening” usually involves more than the deposition of fat alone. Ringing Migr 11:113–115CrossRefGoogle Scholar
  61. Pond CM (1978) Morphological aspects and the ecological and mechanical consequences of fat deposition in wild vertebrates. Annu Rev Ecol Evol Syst 9:519–570CrossRefGoogle Scholar
  62. R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Accessed 14 December 2016
  63. Schmaljohann H, Becker PJJ, Karaardic H, Liechti F, Naef-Daenzer B, Grande C (2011) Nocturnal exploratory flights, departure time, and direction in a migratory songbird. J Ornithol 152:439–452CrossRefGoogle Scholar
  64. Schwilch R, Grattarola A, Spina F, Jenni L (2002) Protein loss during long-distance migratory flight in passerine birds: adaptation and constraint. J Exp Biol 205:687–695PubMedGoogle Scholar
  65. Seewagen CL, Guglielmo CG (2011) Quantitative magnetic resonance analysis and a morphometric predictive model reveal lean body mass changes in migrating Nearctic-Neotropical passerines. J Comp Physiol B 181:413–421CrossRefGoogle Scholar
  66. Seynnes OR, de Boer M, Narici MV (2007) Early skeletal muscle hypertrophy and architectural changes in response to high-intensity resistance training. J Appl Physiol 102:368–373CrossRefGoogle Scholar
  67. Taicher GZ, Tinsley FC, Reidermann A, Heiman ML (2003) Quantitative magnetic resonance (QMR) method for bone and whole-body-composition analysis. Anal Bioanal Chem 377:990–1002CrossRefGoogle Scholar
  68. Tinsley FC, Taicher GZ, Heiman ML (2004) Evaluation of a quantitative magnetic resonance method for mouse whole body composition analysis. Obesity 12:150–160CrossRefGoogle Scholar
  69. Wikelski M, Tarlow EM, Raim A, Diehl RH, Larkin RP, Visser GH (2003) Costs of migration in free-flying songbirds. Nature 423:704CrossRefGoogle Scholar

Copyright information

© Deutsche Ornithologen-Gesellschaft e.V. 2019

Authors and Affiliations

  1. 1.Institute of Avian Research ‘Vogelwarte Helgoland’WilhelmshavenGermany

Personalised recommendations