Journal of Comparative Physiology B

, Volume 185, Issue 7, pp 797–810 | Cite as

Migration-induced variation of fatty acid transporters and cellular metabolic intensity in passerine birds

  • Yufeng Zhang
  • Marisa O. King
  • Erin Harmon
  • Kathleen Eyster
  • David L. Swanson
Original Paper

Abstract

Because lipids are the main fuel supporting avian endurance activity, lipid transport and oxidation capacities may increase during migration. We measured enzyme activities, mRNA expression and protein levels in pectoralis and heart for several key steps of lipid transport and catabolism pathways to investigate whether these pathways were upregulated during migration. We used yellow-rumped (Setophaga coronata) and yellow (S. petechia) warblers and warbling vireos (Vireo gilvus) as study species because they all show migration-induced increases in organismal metabolic capacities. For yellow-rumped warblers, β-hydroxyacyl CoA-dehydrogenase (HOAD) activities and fatty acid transporter mRNA and/or protein levels were higher during spring than fall in pectoralis and heart, except that fatty acid translocase (FAT/CD36) protein levels showed the opposite pattern in heart. Lipid transporter protein levels, but not mRNA expression, in pectoralis and heart of warbling vireos were higher either during spring or fall than summer, but this was not true for HOAD activities. For yellow warblers, pectoralis, but not heart, protein levels of lipid transporters were upregulated during migration relative to summer, but this pattern was not evident for mRNA expression or HOAD activity. Finally, muscle and heart citrate synthase and carnitine palmitoyl transferase activities showed little seasonal variation for any species. These data suggest that pectoralis and heart lipid transport and catabolism capacities are often, but not universally, important correlates of elevated organismal metabolic capacity during migration. In contrast, migration-induced variation in cellular metabolic intensity and mitochondrial membrane transport are apparently not common correlates of the migratory phenotype in passerines.

Keywords

Lipid transport Phenotypic flexibility Migration Pectoralis Heart Birds 

References

  1. Battley PF, Dietz MW, Piersma T, Dekinga A, Tang S, Hulsman K (2001) Is long-distance bird flight equivalent to a high-energy fast? Body composition changes in freely migrating and captive fasting great knots. Physiol Biochem Zool 74:435–449. doi:10.1086/320432 CrossRefPubMedGoogle Scholar
  2. Bonen A et al (2003) Plasmalemmal fatty acid transport is regulated in heart and skeletal muscle by contraction, insulin and leptin, and in obesity and diabetes. Acta Physiol Scand 178:347–356. doi:10.1046/j.1365-201X.2003.01157.x CrossRefPubMedGoogle Scholar
  3. Bonen A, Chabowski A, Luiken JJ, Glatz JF (2007) Is membrane transport of FFA mediated by lipid, protein, or both? Mechanisms and regulation of protein-mediated cellular fatty acid uptake: molecular, biochemical, and physiological evidence. Physiology (Bethesda) 22:15–29Google Scholar
  4. Borgmann KL, Pearson SF, Levey DJ, Greenberg CH, Stouffer P (2004) Wintering yellow-rumped warblers (Dendroica coronata) track manipulated abundance of Myrica cerifera fruits. Auk 121:74–87CrossRefGoogle Scholar
  5. Burelle Y et al (2004) Regular exercise is associated with a protective metabolic phenotype in the rat heart. Am J Physiol Heart Circ Physiol 287:H1055–H1063. doi:10.1152/ajpheart.00925.2003 CrossRefPubMedGoogle Scholar
  6. Campbell SE, Febbraio MA (2001) Effect of ovarian hormones on mitochondrial enzyme activity in the fat oxidation pathway of skeletal muscle. Am J Physiol 281:E803–E808Google Scholar
  7. Chabowski A, Górski J, Bonen A (2006) Regulation of fatty acid transport: from transcriptional to posttranscriptional effects. Naunyn Schmiedebergs Arch Pharmacol 373:259–263CrossRefPubMedGoogle Scholar
  8. Clarke DC et al (2004) Overexpression of membrane-associated fatty acid binding protein (FABPpm) in vivo increases fatty acid sarcolemmal transport and metabolism. Physiol Genomics 17:31–37. doi:10.1152/physiolgenomics.00190.2003 CrossRefPubMedGoogle Scholar
  9. Corder K, Schaeffer P (2015) Summit metabolic rate exhibits phenotypic flexibility with migration, but not latitude in a neotropical migrant, Parkesia noveboracensis. J Ornithol 156:547–550. doi:10.1007/s10336-015-1157-x CrossRefGoogle Scholar
  10. Dawson WR, Marsh RL, Yacoe ME (1983) Metabolic adjustments of small passerine birds for migration and cold. Am J Physiol 245:755–767Google Scholar
  11. deGraw W, Kern M, King J (1979) Seasonal changes in the blood composition of captive and free-living white-crowned sparrows. J Comp Physiol 129:151–162. doi:10.1007/BF00798180 CrossRefGoogle Scholar
  12. Driedzic WR, Crowe HL, Hicklin PW, Sephton DH (1993) Adaptations in pectoralis muscle, heart mass, and energy metabolism during premigratory fattening in semipalmated sandpipers (Calidris pusilla). Can J Zool 71:1602–1608. doi:10.1139/z93-226 CrossRefGoogle Scholar
  13. Evans PR, Davidson NC, Uttley JD, Evans RD (1992) Premigratory hypertrophy of flight muscles: an ultrastructural study. Ornis Scand 23:238–243. doi:10.2307/3676644 CrossRefGoogle Scholar
  14. Glatz JF, Luiken JJ, Bonen A (2010) Membrane fatty acid transporters as regulators of lipid metabolism: implications for metabolic disease. Physiol Rev 90:367–417. doi:10.1152/physrev.00003.2009 CrossRefPubMedGoogle Scholar
  15. Grubbs FE (1950) Sample criteria for testing outlying observations. Ann Math Stat: 27–58Google Scholar
  16. Guglielmo CG (2010) Move that fatty acid: fuel selection and transport in migratory birds and bats. Integr Comp Biol 50:336–345. doi:10.1093/icb/icq097 CrossRefPubMedGoogle Scholar
  17. Guglielmo CG, Haunerland NH, Williams TD (1998) Fatty acid binding protein, a major protein in the flight muscle of migrating western sandpipers. Comp Biochem Physiol B 119:549–555. doi:10.1016/S0305-0491(98)00016-9 CrossRefPubMedGoogle Scholar
  18. Guglielmo CG, Haunerland NH, Hochachka PW, Williams TD (2002) Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird. Am J Physiol 282:R1405–R1413. doi:10.1152/ajpregu.00267.2001 Google Scholar
  19. Guzmán M, Saborido A, Castro J, Molano F, Megias A (1991) Treatment with anabolic steroids increases the activity of the mitochondrial outer carnitine palmitoyltransferase in rat liver and fast-twitch muscle. Biochem Pharm 41:833–835. doi:10.1016/0006-2952(91)90088-M CrossRefPubMedGoogle Scholar
  20. Hajri T, Han XX, Bonen A, Abumrad NA (2002) Defective fatty acid uptake modulates insulin responsiveness and metabolic responses to diet in CD36-null mice. J Clin Invest 109:1381–1389. doi:10.1172/jci14596 PubMedCentralCrossRefPubMedGoogle Scholar
  21. Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528. doi:10.2307/3677171 CrossRefGoogle Scholar
  22. Kiens B (2006) Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev 86:205–243. doi:10.1152/physrev.00023.2004 CrossRefPubMedGoogle Scholar
  23. King M, Zhang Y, Carter T, Johnson J, Harmon E, Swanson D (2015) Phenotypic flexibility of skeletal muscle and heart masses and expression of myostatin and tolloid-like proteinases in migrating passerine birds. J Comp Physiol B 185(3):333–342. doi:10.1007/s00360-015-0887-7 CrossRefPubMedGoogle Scholar
  24. Liknes ET, Swanson DL (2011) Phenotypic flexibility in passerine birds: seasonal variation of aerobic enzyme activities in skeletal muscle. J Therm Biol 36:430–436. doi:10.1016/j.jtherbio.2011.07.011 CrossRefGoogle Scholar
  25. Liknes ET, Scott SM, Swanson DL (2002) Seasonal acclimatization in the american goldfinch revisited: to what extent do metabolic rates vary seasonally? The Condor 104:548–557. doi:10.2307/1370735 CrossRefGoogle Scholar
  26. Liknes ET, Guglielmo CG, Swanson DL (2014) Phenotypic flexibility in passerine birds: seasonal variation in fuel storage, mobilization and transport. Comp Biochem Physiol B 174:1–10. doi:10.1016/j.cbpa.2014.03.017 CrossRefGoogle Scholar
  27. Lindström Å (1997) Basal metabolic rates of migrating waders in the Eurasian arctic. J Avian Biol 28:87–92. doi:10.2307/3677098 CrossRefGoogle Scholar
  28. Liu M, Swanson DL (2014) Physiological evidence that anthropogenic woodlots can substitute for native riparian woodlands as stopover habitat for migrant birds. Physiol Biochem Zool 87:183–195. doi:10.1086/671746 CrossRefPubMedGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative pcr and the 2−ΔΔct method. Methods 25:402–408. doi:10.1006/meth.2001.1262 CrossRefPubMedGoogle Scholar
  30. Luiken JFP, Coort SM, Koonen DY, van der Horst D, Bonen A, Zorzano A, Glatz JC (2004) Regulation of cardiac long-chain fatty acid and glucose uptake by translocation of substrate transporters. Pflügers Archiv 448:1–15. doi:10.1007/s00424-003-1199-4 CrossRefPubMedGoogle Scholar
  31. Lundgren BO (1988) Catabolic enzyme activities in the pectoralis muscle of migratory and non-migratory goldcrests, great tits, and yellowhammers. Ornis Scand 19:190–194. doi:10.2307/3676557 CrossRefGoogle Scholar
  32. Lundgren BO, Kiessling K-H (1985) Seasonal variation in catabolic enzyme activities in breast muscle of some migratory birds. Oecologia 66:468–471. doi:10.2307/4217656 CrossRefGoogle Scholar
  33. Lundgren BO, Kiessling K-H (1986) Catabolic enzyme activities in the pectoralis muscle of premigratory and migratory juvenile reed warblers Acrocephalus scirpaceus (Herm.). Oecologia 68:529–532. doi:10.2307/4217878 CrossRefGoogle Scholar
  34. Marsh RL (1981) Catabolic enzyme activities in relation to premigratory fattening and muscle hypertrophy in the gray catbird (Dumetella carolinensis). J Comp Physiol B 141:417–423. doi:10.1007/BF01101461 CrossRefGoogle Scholar
  35. Marsh RL, Dawson WR (1982) Substrate metabolism in seasonally acclimatized American goldfinches. Am J Physiol 242:R563–R569PubMedGoogle Scholar
  36. McFarlan JT, Bonen A, Guglielmo CG (2009) Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichia albicollis). J Exp Biol 212:2934–2940. doi:10.1242/jeb.031682 CrossRefPubMedGoogle Scholar
  37. McWilliams SR, Guglielmo C, Pierce B, Klaassen M (2004) Flying, fasting, and feeding in birds during migration: a nutritional and physiological ecology perspective. J Avian Biol 35:377–393. doi:10.1111/j.0908-8857.2004.03378.x CrossRefGoogle Scholar
  38. Pelsers MM, Butler PJ, Bishop CM, Glatz JF (1999) Fatty acid binding protein in heart and skeletal muscles of the migratory barnacle goose throughout development. Am J Physiol 276:R637–R643PubMedGoogle Scholar
  39. Piersma T (1998) Phenotypic flexibility during migration: optimization of organ size contingent on the risks and rewards of fueling and flight? J Avian Biol 29:511–520. doi:10.2307/3677170 CrossRefGoogle Scholar
  40. Piersma T, Cadée N, Daan S (1995) Seasonality in basal metabolic rate and thermal conductance in a long-distance migrant shorebird, the knot (Calidris canutus). J Comp Physiol B 165:37–45. doi:10.1007/BF00264684 CrossRefGoogle Scholar
  41. 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 98:363–370. doi:10.2307/1369154 CrossRefGoogle Scholar
  42. Place AR, Stiles EW (1992) Living off the wax of the land: bayberries and yellow-rumped warblers. Auk: 334–345Google Scholar
  43. Pownall HJ, Hamilton JA (2003) Energy translocation across cell membranes and membrane models. Acta Physiol Scand 178:357–365. doi:10.1046/j.1365-201X.2003.01154.x CrossRefPubMedGoogle Scholar
  44. Pravenec M et al (2003) Transgenic expression of CD36 in the spontaneously hypertensive rat is associated with amelioration of metabolic disturbances but has no effect on hypertension. Physiol Res 52:681–688PubMedGoogle Scholar
  45. Price ER, McFarlan JT, Guglielmo CG (2010) Preparing for migration? The effects of photoperiod and exercise on muscle oxidative enzymes, lipid transporters, and phospholipids in white-crowned sparrows. Physiol Biochem Zool 83:252–262. doi:10.1086/605394 CrossRefPubMedGoogle Scholar
  46. Price ER, Staples JF, Milligan CL, Guglielmo CG (2011) Carnitine palmitoyl transferase activity and whole muscle oxidation rates vary with fatty acid substrate in avian flight muscles. J Comp Physiol B 181:565–573. doi:10.1007/s00360-010-0542-2 PubMedGoogle Scholar
  47. Ramakers C, Ruijter JM, Deprez RHL, Moorman AFM (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66. doi:10.1016/S0304-3940(02)01423-4 CrossRefPubMedGoogle Scholar
  48. Ramenofsky M (1990) Fat storage and fat metabolism in relation to migration. In: Gwinner E (ed) Bird migration. Springer, Berlin, pp 214–231. doi:10.1007/978-3-642-74542-3_15 CrossRefGoogle Scholar
  49. Seewagen CL, Guglielmo CG, Morbey YE (2013) Stopover refueling rate underlies protandry and seasonal variation in migration timing of songbirds. Behav Ecol 24:634–642. doi:10.1093/beheco/ars225 CrossRefGoogle Scholar
  50. Smith JP, Achua JK, Summers TR, Ronan PJ, Summers CH (2014) Neuropeptide S and BDNF gene expression in the amygdala are influenced by social decision-making under stress. Front Behav Neurosci 8:121. doi:10.3389/fnbeh.2014.00121 PubMedCentralPubMedGoogle Scholar
  51. Srivastava S, Rani S, Kumar V (2014) Photoperiodic induction of pre-migratory phenotype in a migratory songbird: identification of metabolic proteins in flight muscles. J Comp Physiol B 184:741–751. doi:10.1007/s00360-014-0827-y CrossRefPubMedGoogle Scholar
  52. Swanson DL (1995) Seasonal variation in thermogenic capacity of migratory warbling vireos. Auk 112:870–877. doi:10.2307/4089019 CrossRefGoogle Scholar
  53. Swanson DL (2010) Seasonal metabolic variation in birds: functional and mechanistic correlates. In: Thompson CF (ed) Current ornithology, vol 17. Springer, New York, pp 75–129. doi:10.1007/978-1-4419-6421-2_3 Google Scholar
  54. Swanson DL, Dean KL (1999) Migration-induced variation in thermogenic capacity in migratory passerines. J Avian Biol 30:245–254. doi:10.2307/3677350 CrossRefGoogle Scholar
  55. Swanson DL, Zhang Y, Liu J-S, Merkord CL, King MO (2014) Relative roles of temperature and photoperiod as drivers of metabolic flexibility in dark-eyed juncos. J Exp Biol 217:866–875. doi:10.1242/jeb.096677 CrossRefPubMedGoogle Scholar
  56. Tallman DT, Swanson DL, Palmer JS (2002) Birds of South Dakota, 3rd edn. South Dakota Ornithologists’ Union, AberdeenGoogle Scholar
  57. Terrill SB, Ohmart RD (1984) Facultative extension of fall migration by yellow-rumped warblers (Dendroica coronata). Auk 101:427–438. doi:10.2307/4086595 Google Scholar
  58. Thompson JN, Willson MF (1979) Evolution of temperate fruit/bird interactions: phenological strategies. Evolution: 973–982Google Scholar
  59. Thorne RF, Ralston KJ, de Bock CE, Mhaidat NM, Zhang XD, Boyd AW, Burns GF (2010) Palmitoylation of CD36/FAT regulates the rate of its post-transcriptional processing in the endoplasmic reticulum. Biochim Biophys Acta 1803:1298–1307. doi:10.1016/j.bbamcr.2010.07.002 CrossRefPubMedGoogle Scholar
  60. van Breda E, Keizer H, Vork M, Surtel DM, de Jong Y, van der Vusse G, Glatz JC (1992) Modulation of fatty-acid-binding protein content of rat heart and skeletal muscle by endurance training and testosterone treatment. Pflügers Archiv 421:274–279. doi:10.1007/BF00374838 CrossRefPubMedGoogle Scholar
  61. 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 19:119–128. doi:10.1111/j.0269-8463.2005.00942.x CrossRefGoogle Scholar
  62. 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 209:3141–3154. doi:10.1242/jeb.02338 CrossRefPubMedGoogle Scholar
  63. Weber TP, Piersma T (1996) Basal metabolic rate and the mass of tissues differing in metabolic scope: migration-related covariation between individual knots Calidris canutus. J Avian Biol 27:215–224. doi:10.2307/3677225 CrossRefGoogle Scholar
  64. Zajac DM, Cerasale DJ, Landman S, Guglielmo CG (2011) Behavioral and physiological effects of photoperiod-induced migratory state and leptin on Zonotrichia albicollis: II. Effects on fatty acid metabolism. Gen Comp Endocrinol 174:269–275. doi:10.1016/j.ygcen.2011.08.024 CrossRefPubMedGoogle Scholar
  65. Zhang Y, King MO, Harmon E, Swanson DL (2015) Summer-to-winter phenotypic flexibility of fatty acid transport and catabolism in small birds. Physiol Biochem Zool (in press) Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Yufeng Zhang
    • 1
  • Marisa O. King
    • 1
  • Erin Harmon
    • 1
    • 3
  • Kathleen Eyster
    • 2
  • David L. Swanson
    • 1
  1. 1.Department of BiologyUniversity of South DakotaVermillionUSA
  2. 2.Division of Basic Biomedical SciencesSanford School of Medicine, University of South DakotaVermillionUSA
  3. 3.Cardiovascular Research InstituteSanford Research/University of South DakotaSioux FallsUSA

Personalised recommendations