Journal of Ornithology

, 147:531 | Cite as

Effect of endurance flight on haematocrit in migrating birds

  • Lukas Jenni
  • Susanne Müller
  • Fernando Spina
  • Anders Kvist
  • Åke Lindström
Original Article


The effects of an endurance flight on the haematocrit, the percentage of packed red blood cells per blood volume, were examined within the framework of six possible factors explaining possible changes in the haematocrit. Two approaches were adopted: (1) the haematocrit was studied in four species of passerine birds which landed on an Italian island after having crossed the Mediterranean Sea on their spring migration in a non-stop flight; (2) the haematocrit was evaluated in six individual red knots after a flight of 1, 2, 4 and 10 h in a wind tunnel and the data thus obtained compared with data on resting birds with or without food. In the four passerine species, the haematocrit decreased from 51% in fat birds to 48% in lean birds. In lean birds, the haematocrit dropped from 48% in birds with well-developed breast muscles to 36% in birds with emaciated breast muscles. In the red knots, the haematocrit was dependent on body mass in flying and resting birds. The haematocrit decreased from about 51% pre-flight to about 49% within 1 h of flight and remained at this level for up to 10 h of flight. Taking the results from the passerines and the red knots together, it seems that the haematocrit drops by a few percentage points within 1 h after the onset of flight, decreases very slowly with decreasing body mass and decreases more steeply in very lean birds having entered stage III of fasting. This indicates that dehydration is not an underlying factor in decreased haematocrit because if this were the case we would expect an increase with endurance flight. We found no effect of the presence of blood parasites on haematocrit. With the onset of flight, haemodilution may be adaptive, because it reduces blood viscosity and, thereby, energy expenditure by the heart, or it may be a sign of water conservation as an insurance against the risk of dehydration during long non-stop flights. During endurance flight, a reduction in the haematocrit may be adaptive, in that oxygen delivery capacity is adjusted to the decreased oxygen needs as body mass decreases. A decreasing haematocrit would also allow birds to reduce heart beat frequency and/or heart size, because blood viscosity decreases disproportionally with decreasing haematocrit. However, when energy stores are about to come to an end and birds increase protein breakdown, the haematocrit decreases even further, and birds probably become anaemic due to a reduced erythropoiesis.


Bird migration Blood parasites Energy stores Fasting Haematocrit Haemoconcentration Haemodilution Wind tunnel 



We thank Y. Endriss, Swiss Tropical Institute, Basel, for introducing SM into the art of making blood smears, for providing a working place and for much helpful advice. The wind tunnel study was supported by a PIONIER grant to Theunis Piersma from the Netherlands Organization for Scientific Research (NWO), and by grants from the Crafoord Foundation and the Swedish Natural Science Research Council (to ÅL), Knut and Alice Wallenberg Foundation (to Thomas Alerstam), and the Swedish Council for Planning and Coordination of Research (to Thomas Alerstam and ÅL). Bernard Spaans, Anita Koolhaas, Anne Dekinga, Maurine W. Dietz, Martin Green, Mikael Rosén, Anders Hedenström and Anders Forslid kindly helped with practical matters. The wind tunnel work was carried out under license from the Lund/Malmö Ethical Committee (no. M161-97). We are indebted to P.J. Butler, M. Landys-Ciannelli and R.L. Holberton for helpful comments on an earlier version.


  1. Åstrand P-O, Rodahl K (1986) Textbook of work physiology, physiological bases of exercise. McGraw-Hill, New YorkGoogle Scholar
  2. Bairlein F (1995) Manual of field methods. European-African Songbird migration network. Institut für Vogelkunde, WilhelmshavenGoogle Scholar
  3. Bairlein F, Totzke U (1992) New aspects on migratory physiology of trans-Saharan passerine migrants. Ornis Scand 23:244–250Google Scholar
  4. 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 Roy Soc Lond B 267:191–195CrossRefGoogle Scholar
  5. Bell DJ, Bird TP, McIndoe WM (1965) Changes in erythrocyte levels and the mean corpuscular haemoglobin concentration in hens during the laying cycle. Comp Biochem Physiol 14:83–100PubMedCrossRefGoogle Scholar
  6. Biebach H (1998) Phenotypic organ flexibility in Garden Warblers Sylvia borin during long-distance migration. J Avian Biol 29:529–535Google Scholar
  7. Boismenu C, Gauthier G, Larochelle J (1992) Physiology of prolonged fasting in greater snow geese (Chen caerulescens atlantica). Auk 109:511–521Google Scholar
  8. Butler PJ, Woakes AJ (1990) The physiology of bird flight. In: Gwinner E (eds) Bird migration. Springer, Berlin Heidelberg New York, pp 300–318Google Scholar
  9. Butler PJ, Woakes AJ, Bishop CM (1998) Behaviour and physiology of Svalbard Barnacle Geese Branta leucopsis during their autumn migration. J Avian Biol 29:536–545Google Scholar
  10. Carmi N, Pinshow B, Horowitz M, Bernstein MH (1993) Birds conserve plasma volume during thermal and flight-incurred dehydration. Physiol Zool 66:829–846Google Scholar
  11. Carmi N, Pinshow B, Horowitz M (1994) Plasma volume conservation in pigeons: effects of air temperature during dehydration. Am J Physiol 267:R1449–R1453PubMedGoogle Scholar
  12. Cherel Y, Le Maho Y (1985) Five months of fasting in king penguin chicks: body mass loss and fuel metabolism. Am J Physiol 249:R387–R392PubMedGoogle Scholar
  13. Cherel Y, Leloup J, Le Maho Y (1988a) Fasting in king penguin. II. Hormonal and metabolic changes during molt. Am J Physiol 254:R178–R184Google Scholar
  14. Cherel Y, Robin JP, Le Maho Y (1988b) Physiology and biochemistry of long-term fasting in birds. Can J Zool 66:159–166CrossRefGoogle Scholar
  15. Collodel L, Favretto G, Caenaro G, Teodori T, Mazzon D, Stritoni P, Piccoli A, Nieri A (1997) Changes in hematocrit and plasma viscosity during maximal aerobic exercise. Med Sport 50:385–390Google Scholar
  16. Cooper JE, Anwar MA (2001) Blood parasites of birds: a plea for more cautious terminology. Ibis 143:149–150Google Scholar
  17. Dawson RD, Bortolotti GR (1997) Variation in hematocrit and total plasma proteins of nestling American kestrels (Falco sparverius) in the wild. Comp Biochem Physiol 117A:383–390CrossRefGoogle Scholar
  18. Dein J (1986) Hematology. In: Harrison GJ, Harrison WR (eds) Clinical avian medicine. Saunders, London, pp 174–191Google Scholar
  19. Driedzic WR, Crowe HL, Hicklin PW, Sephton DH (1993) Adaptation in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can J Zool 71:1602–1608CrossRefGoogle Scholar
  20. Ernst E, Daburger L, Saradeth T (1991) The kinetics of blood rheology during and after prolonged standardized exercise. Clin Hemorheol 11:429–439Google Scholar
  21. Gillen CM, Lee R, Mack GW, Tomaselli CM, Nishiyasu T, Nadel ER (1991) Plasma volume expansion in humans after a singly intense exercise protocol. J Appl Physiol 71:1914–1920PubMedGoogle Scholar
  22. Harrison MH (1985) Effects of thermal stress and exercise on blood volume in humans. Physiol Rev 65:149–209PubMedGoogle Scholar
  23. Jenni L, Jenni-Eiermann S, Spina F, Schwabl H (2000) Regulation of protein breakdown and adrenocortical response to stress in birds during migratory flight. Am J Physiol 278:R1182–R1189Google Scholar
  24. Jenni-Eiermann S, Jenni L (1992) High plasma triglyceride levels in small birds during migratory flight: a new pathway for fuel supply during endurance locomotion at very high mass-specific metabolic rates? Physiol Zool 65:112–123Google Scholar
  25. Jenni-Eiermann S, Jenni L, Kvist A, Lindström Å, Piersma T, Visser GH (2002) Fuel use and metabolic response to endurance exercise: a wind tunnel study of a long-distance migrant shorebird. J Exp Biol 205:2453–2460PubMedGoogle Scholar
  26. Jones PJ (1983) Haematocrit values of breeding Red-billed queleas Quelea quelea (Aves: Ploceidae) in relation to body condition and thymus activity. J Zool 201:217–222CrossRefGoogle Scholar
  27. Kaiser A (1993) A new multi-category classification of subcutaneous fat deposits of songbirds. J Field Ornithol 64:246–255Google Scholar
  28. Kvist A, Lindström Å (2003) Gluttony in migratory waders—unprecedented energy assimilation rates in vertebrates. Oikos 103:397–402CrossRefGoogle Scholar
  29. Kvist A, Lindström Å, Green M, Piersma T, Visser GH (2001) Carrying large fuel loads during sustained bird flight is cheaper than expected. Nature 413:730–732PubMedCrossRefGoogle Scholar
  30. Landys MM, Piersma T, Visser GH, Jukema J, Wijker A (2000) Water balance during real and simulated long-distance migratory flight in the Bar-tailed Godwit. Condor 102:645–652CrossRefGoogle Scholar
  31. Landys-Ciannelli MM, Jukema J, Piersma T (2002) Blood parameter changes during stopover in a long-distance migratory shorebird, the Bar-tailed Godwit Limosa lapponica taymyrensis. J Avian Biol 33:451–455CrossRefGoogle Scholar
  32. 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 17:151–159CrossRefGoogle Scholar
  33. Le Maho Y, Vu Van Kha H, Koubi H, Dewasmes G, Girard J, Ferré P, Cagnard M (1981) Body composition, energy expenditure, and plasma metabolites in long-term fasting geese. Am J Physiol 241:E342–E354PubMedGoogle Scholar
  34. Lindström Å, Piersma T (1993) Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135:70–78Google Scholar
  35. Lindström Å, Kvist A, Piersma T, Dekinga A, Dietz MW (2000) Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J Exp Biol 203:913–919PubMedGoogle Scholar
  36. Lundgren BO, Kiessling KH (1985) Seasonal variation in catabolic enzyme activities in breast muscle of some migratory birds. Oecologia 66:468–471CrossRefGoogle Scholar
  37. Merilä J, Svensson E (1995) Fat reserves and health state in migrant Goldcrest (Regulus regulus). Funct Ecol 9:842–848CrossRefGoogle Scholar
  38. Morton ML (1994) Hematocrits in montane sparrows in relation to reproductive schedule. Condor 96:119–126Google Scholar
  39. Neuhaus D, Fedde MR, Gaehtgens P (1992) Changes in hemorheology in the racing greyhound as related to oxygen delivery. Eur J Appl Physiol Occup Physiol 65:278–285PubMedCrossRefGoogle Scholar
  40. O’Toole ML, Douglas PS, Hiller WDB, Laird RH (1999) Hematocrits of triathletes: is monitoring useful? Med Sci Sports Exerc 31:372–377PubMedCrossRefGoogle Scholar
  41. Ots I, Murumägi A, Horak P (1998) Haematological health state indices of reproducing Great Tits: methodology and sources of natural variation. Funct Ecol 12:700–707CrossRefGoogle Scholar
  42. Patterson HD, Thompson R (1971) Recovery of interblock information when block sizes are unequal. Biometrika 58:545–554CrossRefGoogle Scholar
  43. Pennycuick CJ (1998) Computer simulation of fat and muscle burn in long-distance bird migration. J Theor Biol 191:47–61PubMedCrossRefGoogle Scholar
  44. Piersma T, Everaarts JM, Jukema J (1996) Build-up of red blood cells in refuelling Bar-tailed Godwits in relation to individual migratory quality. Condor 98:363–370Google Scholar
  45. Piersma T, Koolhaas A, Dekinga A, Gwinner E (2000) Red blood cell and white blood cell counts in sandpipers (Philomachus pugnax, Calidris canutus): effects of captivity, season, nutritional status, and frequent bleedings. Can J Zool 78:1349–1355CrossRefGoogle Scholar
  46. Pilastro A, Spina F (1997) Ecological and morphological correlates of residual fat reserves in passerine migrants at their spring arrival in southern Europe. J Avian Biol 28:309–318Google Scholar
  47. Prinzinger R, Misovic A (1994) Vogelblut – eine allometrische Übersicht der Bestandteile. J Ornithol 135:133–165CrossRefGoogle Scholar
  48. 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
  49. Smith FM, West NH, Jones DR (2000) The cardiovascular system. In: Whittow GC (eds) Avian physiology. Academic, San Diego, pp 141–231Google Scholar
  50. Svensson E, Merilä J (1996) Molt and migratory condition in Blue Tits: a serological study. Condor 98:825–831Google Scholar
  51. Vleck CM, Priedkalns J (1985) Reproduction in zebra finches: hormone levels and effect of dehydration. Condor 87:37–46Google Scholar
  52. Wingfield JC, Schwabl H, Mattocks PW Jr (1990) Endocrine mechanisms of migration. In: Gwinner E (eds) Bird migration. Springer, Berlin Heidelberg New York, pp 232–256Google Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2006

Authors and Affiliations

  • Lukas Jenni
    • 1
  • Susanne Müller
    • 1
    • 4
  • Fernando Spina
    • 2
  • Anders Kvist
    • 3
  • Åke Lindström
    • 3
  1. 1.Swiss Ornithological InstituteSempachSwitzerland
  2. 2.Istituto Nazionale per la Fauna SelvaticaBolognaItaly
  3. 3.Department of Animal EcologyLundSweden
  4. 4.ArlesheimSwitzerland

Personalised recommendations