Journal of Comparative Physiology B

, Volume 181, Issue 3, pp 413–421 | Cite as

Quantitative magnetic resonance analysis and a morphometric predictive model reveal lean body mass changes in migrating Nearctic–Neotropical passerines

Original Paper

Abstract

Most studies of lean mass dynamics in free-living passerine birds have focused on Old World species at geographical barriers where they are challenged to make the longest non-stop flight of their migration. We examined lean mass variation in New World passerines in an area where the distribution of stopover habitat does not require flights to exceed more than a few hours and most migrants stop flying well before fat stores near exhaustion. We used either quantitative magnetic resonance (QMR) analysis or a morphometric model to measure or estimate, respectively, the fat and lean body mass of migrants during stopovers in New York, USA. With these data, we examined (1) variance in total body mass explained by lean body mass, (2) hourly rates of fat and lean body mass change in single-capture birds, and (3) net changes in fat and lean mass in recaptured birds. Lean mass contributed to 50% of the variation in total body mass among white-throated sparrows Zonotrichia albicollis and hermit thrushes Catharus guttatus. Lean mass of refueling gray catbirds Dumetella carolinensis and white-throated sparrows, respectively, increased 1.123 and 0.320 g h−1. Lean mass of ovenbirds Seiurus aurocapillus accounted for an estimated 33–40% of hourly gains in total body mass. On average 35% of the total mass gained among recaptured birds was lean mass. Substantial changes in passerine lean mass are not limited to times when birds are forced to make long, non-stop flights across barriers. Protein usage during migration is common across broad taxonomic groups, migration systems, and migration strategies.

Keywords

Protein catabolism Stopover refueling Nearctic–neotropical migrant Urban habitat Body composition 

References

  1. Åkesson S, Karlsson L, Pettersson J (1992) Body composition and migration strategies: a comparison between robins (Erithacus rubecula) from two stop-over sites in Sweden. Vogelwarte 36:188–195Google Scholar
  2. Bauchinger U, Biebach H (1998) The role of protein during migration in passerine birds. Biol Conserv Fauna 102:299–305Google Scholar
  3. 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 1046:271–281PubMedCrossRefGoogle Scholar
  4. Bauchinger U, McWilliams S (2009) Carbon turnover in tissues of a passerine bird: allometry, isotopic clocks, and phenotypic flexibility in organ size. Physiol Biochem Zool 82:787–797PubMedCrossRefGoogle Scholar
  5. Bauchinger U, Wohlmann A, Biebach H (2005) Flexible remodeling of organ size during spring migration of the garden warbler (Sylvia borin). Zool 108:97–106CrossRefGoogle Scholar
  6. 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, pp 269–280Google Scholar
  7. Bonter DN, Donovan TM, Brooks EW (2007) Daily mass changes in landbirds during migration stopover on the south shore of Lake Ontario. Auk 124:122–133CrossRefGoogle Scholar
  8. Carlisle JD, Kaltenecker GS, Swanson DL (2005) Stopover ecology of autumn landbird migrants in the Boise foothills of southwestern Idaho. Condor 107:244–258CrossRefGoogle Scholar
  9. Carpenter FL, Hixon MA, Beuchat CA, Russell RW, Paton DC (1993) Biphasic mass gain in migrant hummingbirds: body composition changes, torpor, and ecological significance. Ecology 74:1173–1182CrossRefGoogle Scholar
  10. Cimprich DA, Moore FR (1995) Grey Catbird (Dumetella carolinensis). In: Poole A, Gill F (eds) The birds of North America, No. 167. Academy of Natural Sciences, PhiladelphiaGoogle Scholar
  11. Craves JA (2009) A fifteen year study of fall stopover patterns of Catharus thrushes at an inland, urban site. Wilson J Ornithol 121:112–118CrossRefGoogle Scholar
  12. DeCandido R, Allen D (2005) First confirmed nesting of the Pine Warbler (Dendroica pinus) in New York City. Kingbird 55:328–334Google Scholar
  13. Deerenberg C, Biebach H, Bauchinger U (2002) Spleen size variation during long distance migration in a passerine. Avian Sci 2:217–226Google Scholar
  14. Dunn EH (2000) Temporal and spatial patterns in daily mass gain of Magnolia Warblers during migratory stopover. Auk 117:12–21CrossRefGoogle Scholar
  15. Dunn EH (2001) Mass change during migration stopover: a comparison of species groups and sites. J Field Ornithol 72:419–432Google Scholar
  16. Falls JB, Kopachena JG (2010) White-throated sparrow (Zonotrichia albicolis). In: Poole A, Gill F (eds) The birds of North America, No. 167. Academy of Natural Sciences, PhiladelphiaGoogle Scholar
  17. Fowle M, Kerlinger P (2001) The New York City Audubon Society guide to finding birds in the metropolitan area. Cornell University Press, New YorkGoogle Scholar
  18. Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82:1473–1483CrossRefGoogle Scholar
  19. Guglielmo CG (2010) Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr Comp Biol 50:336–345CrossRefGoogle Scholar
  20. Hume ID, Biebach H (1996) Digestive tract function in the long-distance migratory Garden Warbler, Sylvia borin. J Comp Physiol B 166:388–395CrossRefGoogle Scholar
  21. Jenni L, Jenni-Eiermann S (1992) Metabolic patterns of feeding, overnight fasted and flying night migrants during autumn migration. Ornis Scand 23:251–259CrossRefGoogle Scholar
  22. Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528CrossRefGoogle 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 Regulatory Integr Comp Physiol 278:1182–1189Google Scholar
  24. Jenni-Eiermann S, Jenni L (1991) Metabolic responses to flight and fasting in night migrating passerines. J Comp Physiol B 161:465–474CrossRefGoogle Scholar
  25. Jones PW, Donovan TM (1996) Hermit thrush (Catharus guttatus). In: Poole A, Gill F (eds) The birds of North America, No. 261. Academy of Natural Sciences, Philadelphia, PennsylvaniaGoogle Scholar
  26. Jones AS, Johnson MS, Nagy TR (2009) Validation of quantitative magnetic resonance for the determination of body composition of mice. Int J Body Compos Res 7:67–72PubMedGoogle Scholar
  27. Karasov WH (1990) Digestion in birds: chemical and physiological determinants and ecological implications. Stud Avian Biol 13:391–415Google Scholar
  28. 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 71:435–448PubMedCrossRefGoogle Scholar
  29. Klaassen M, Biebach H (1994) Energetics of fattening and starvation in the long-distance migratory garden warbler, Sylvia borin, during the migratory phase. J Comp Physiol B 164:362–371CrossRefGoogle Scholar
  30. Klaassen M, Kvist A, Lindström Å (2000) Flight costs and fuel composition of a bird migrating in a wind tunnel. Condor 102:444–451CrossRefGoogle Scholar
  31. 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
  32. Levey DJ, Karasov WH (1994) Gut passage of insects by European starlings and comparison with other species. Auk 111:478–481Google Scholar
  33. Lindström Å, Piersma T (1993) Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135:70–87CrossRefGoogle Scholar
  34. Lindström Å, Klaassen M, Kvist A (1999) Variation in energy intake and basal metabolic rate of a bird migrating in a wind tunnel. Funct Ecol 13:352–359CrossRefGoogle Scholar
  35. 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
  36. Marsh RL (1983) Adaptations of the Gray Catbird Dumetella carolinensis to long distance migration: energy stores and substrate concentrations in plasma. Auk 100:170–179Google Scholar
  37. McGuire LP, CG Guglielmo (in press) Quantitative magnetic resonance: a rapid, noninvasive body composition analysis technique for live and salvaged bats. J MammalGoogle Scholar
  38. Mehlman DW, Mabey SE, Ewert DN, Duncan C, Abel B, Cimprich D, Sutter RD, Woodrey MS (2005) Conserving stopover sites for forest-dwelling migratory landbirds. Auk 122:1281–1290CrossRefGoogle Scholar
  39. Mittelbach M, Crewdson M (1998) Wild New York: a guide to the wildlife, wild places, and natural phenomena of New York City. Random House, New YorkGoogle Scholar
  40. Moore FR, Gauthreaux SA, Kerlinger P, Simons TR (1995) Habitat requirements during migration: important link in conservation. In: Martin TE, Finch DM (eds) Ecology and management of Neotropical migratory birds: a synthesis and review of critical issues. Oxford University Press, New York, pp 121–144Google Scholar
  41. Nixon JP, Zhang M, Wang C, Kuskowski MA, Novak CM, Levine JA, Billington CJ, Kotz CM (2010) Evaluation of quantitative magnetic resonance imaging system for whole body composition analysis in rodents. Obesity 18:1652–1659PubMedCrossRefGoogle Scholar
  42. Odum EP, Rogers DT, Hicks DL (1964) Homeostasis of nonfat components of migrating birds. Science 143:1037–1039PubMedCrossRefGoogle Scholar
  43. Peig J, Green AJ (2009) New perspectives for estimating body condition fro mass/length data: the scaled index as an alternative method. Oikos 118:1883–1891CrossRefGoogle Scholar
  44. Pennycuick CR (1998) Computer simulation of fat and muscle burn in long-distance bird migration. J Theor Biol 191:47–61PubMedCrossRefGoogle Scholar
  45. Piersma T (1990) Pre-migratory “fattening” involves more than fat alone. Ringing Migr 11:113–115Google Scholar
  46. Piersma T, Gill RE Jr (1998) Guts don’t fly: small digestive organs in obese bar-tailed godwits. Auk 115:196–203Google Scholar
  47. Piersma T, Jukema J (1990) Budgeting the flight of a long-distance migrant: changes in nutrient reserve levels of bar-tailed godwits at successive spring staging sites. Ardea 78:315–337Google Scholar
  48. Piersma T, Van Brederode NE (1990) The estimation of fat reserves in coastal waders before their departure from nrthwest Africa in spring. Ardea 78:221–236Google Scholar
  49. 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. Phsiol Biochem Zool 72:405–415CrossRefGoogle Scholar
  50. 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
  51. Seewagen CL (2008a) Lipid content of Nearctic-Neotropical migratory passerines killed during stopovers in a New York City park. Northeast Nat 15:87–96CrossRefGoogle Scholar
  52. Seewagen CL (2008b) An evaluation of condition indices and predictive models for non-invasive estimates of lipid mass of migrating Common Yellowthroats, Ovenbirds and Swainson’s Thrushes. J Field Ornithol 79:80–86CrossRefGoogle Scholar
  53. Seewagen CL, Guglielmo CG (2010) Effects of fat and lean body mass on migratory landbird stopover duration. Wilson J Ornithol 122:82–87CrossRefGoogle Scholar
  54. Seewagen CL, Slayton EJ (2008) Mass changes of migratory landbirds during stopovers in a New York City park. Wilson J Ornithol 120:296–303CrossRefGoogle Scholar
  55. Seewagen CL, Slayton EJ, Guglielmo CG (2010) Passerine migrant stopover duration and spatial behaviour at an urban stopover site. Acta Oecolo 36:484–492Google Scholar
  56. Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. WH Freeman and Company, San FranciscoGoogle Scholar
  57. Swanson DL, Carlisle HA, Liknes ET (2003) Abundance and richness of Neotropical migrants during stopover at farmstead woodlots and associated habitats in southeastern South Dakota. Am Midland Nat 149:176–191CrossRefGoogle Scholar
  58. Taicher GZ, Tinsley FC, Reiderman A, Heiman ML (2003) Quantitative magnetic resonance (QMR) method for bone and whole-body-composition analysis. Analyt Bioanalyt Chem 377:990–1002CrossRefGoogle Scholar
  59. Tankersley Jr R, Orvis K (2003) Modeling the geography of migratory pathways and stopover habitats for Neotropical migratory birds. Cons Ecol 7:7Google Scholar
  60. Tinsley FC, Taicher GZ, Heiman ML (2004) Evaluation of a quantitative magnetic resonance method for mouse whole body composition analysis. Obes Res 12:150–160PubMedCrossRefGoogle Scholar
  61. van der Meer J, Piersma T (1994) Physiologically inspired regression models for estimating and predicting nutrient stores and their composition in birds. Physiol Zool 67:305–329Google Scholar
  62. Van Horn MA, Donovan TM (1994) Ovenbird (Seiurus aurocapillus). In: Poole A, Gill F (eds) The birds of North America, No. 182. Academy of Natural Sciences, PhiladelphiaGoogle Scholar
  63. Warton DI, Wright IJ, Falster DS, Westoby M (2006) Bivariate line-fitting methods for allometry. Biol Rev 81:259–291PubMedCrossRefGoogle Scholar
  64. Wirestam R, Fagerlund T, Rosèn M, Hedenström A (2008) Magnetic resonance imaging for noninvasive analysis of fat storage in migratory birds. Auk 125:965–971CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  1. 1.Department of Biology, Advanced Facility for Avian ResearchUniversity of Western OntarioLondonCanada
  2. 2.Department of OrnithologyWildlife Conservation SocietyBronxUSA

Personalised recommendations