Extent of phenotypic flexibility during long-distance flight is determined by tissue-specific turnover rates: A new hypothesis

Journal of Avian Biology

Volumn 41, Issue 6, 2010, Pages 603-608

  Bauchinger, Ulf ^a   McWilliams, Scott R ^a  

^a UNIVERSITY OF RHODE ISLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIRD; FLIGHT BEHAVIOR; FUNCTIONAL MORPHOLOGY; HYPOTHESIS TESTING; MAGNITUDE; MIGRATORY BEHAVIOR; PHENOTYPIC PLASTICITY; PROTEIN;

AVES;

EID: 78649787862     PISSN: 09088857     EISSN: 1600048X     Source Type: Journal    
DOI: 10.1111/j.1600-048X.2010.05137.x     Document Type: Article

References (53)

1. Alexander, P. A. and Goldspink, G. 1977. Mechanics and Energetics of Animal Locomotion. Chapman and Hall, London.
2. Battley, P. F. and Piersma, T. 2005. Adaptive interplay between feeding ecology and features of the digestive tract in birds. - In: Starck, J. M. and Wang, T. (eds), Physiological and ecological adaptations to feeding in vertebrates. Science Publishers, USA, pp. 201-228.
3. Battley, P. F., Dietz, M. W., Piersma, T., Dekinga, A., Tang, S. X. and 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.
4. Battley, P. F., Piersma, T., Dietz, M. W., Tang, S. X., Dekinga, A. and Hulsman ., K. 2000. Empirical evidence for differential organ reductions during trans-oceanic bird flight. Proc. R. Soc. B 267: 191-195.
5. Bauchinger, U. and Biebach, H. 1998. The role of protein during migration in passerine birds. Proceedings of the first European Ornithological Congress, Bologna, Italy. Biologia e Conservatione della Fauna 102: 299-305.
6. Bauchinger, U. and Biebach, H. 2005. Phenotypic flexibility of skeletal muscles during long-distance migration of garden warblers: muscle changes are differentially related to body mass. Ann. N. Y. Acad. Sci. 1046: 271-281.
7. Bauchinger, U. and McWilliams, S. R. 2009. Carbon turnover in tissues of a passerine bird: allometry, isotopic clocks, and phenotypic flexibility in organ size. Physiol. Biochem. Zool. 82: 787-797.
8. Bauchinger, U., Keil, J., McKinney, R. A., Starck, J. M. and McWilliams, S. R. 2010. Exposure to cold but not exercise increases carbon turnover rates in specific tissues of a passerine. J. Exp. Biol. 213: 526-534.
9. Bauchinger, U., Wohlmann, A. and Biebach, B. 2005. Flexible remodeling of organ size during spring migration of the garden warbler (Sylvia borin). Zoology 108: 97-106.
10. Carleton, S. A. and Martinez del Rio, C. 2005. The effect of cold-induced increased metabolic rate on the rate of C-13 and N-15 incorporation in house sparrows (Passer domesticus). Oecologia 144: 226-232.
11. Carleton, S. A., Kelly, L., Anderson-Sprecher, R. and Martinez del Rio, C. 2008. Should we use one-, or multi-compartment models to describe 13C incorporation into animal tissues?. Rapid Com. Mass. Spec. 22: 1-7.
12. Cherel, Y. and Groscolas, R. 1999. Relationship between nutrient utilization in long-term fasting birds and mammals. - In: Adams, N. J. and Slotow, R. H. (eds), Proceedings of the 22nd International Congress of Ornithology, pp. 17-34 (Bird Life, Johannesburg, South Africa).
13. Dekinga, A., Dietz, M. W., Koolhaas, A. and Piersma, T. 2001. Time course and reversibility of changes in the gizzard of Red Knots alternately eating hard and soft food. J. Exp. Biol. 204: 2167-2173.
14. Diamond, J. and Hammond, K. A. 1992. The matches, achieved by natural selection, between biological capacities and their natural loads. Experentia 48: 551-557.
15. Dietz, M. W., Piersma, T., Hedenström, A. and Brugge, M. 2007. Intraspecific variation in avian pectoral muscle mass: constraints on maintaining manoeuvrability with increasing body mass. Funct. Ecol. 21: 317-326.
16. Gaunt, A. S., Hikida, R. S., Jehl, J. R. and Fenbert, L. 1990. Rapid atrophy and hypertrophy of an avian flight muscle. Auk 107: 649-659.
17. Hammond, K. A. and Diamond, J. 1997. Maximal sustained energy budgets in humans and animals. Nature 386: 457-462.
18. Hobson, K. A. and Clark, R. G. 1992. Assessing avian diets using stable isotopes. 2. Factors influencing diet-tissue fractionation. Condor 94: 189-197.
19. Hume, I. D., Bieglbock, C., Ruf, T., Frey-Roos, F., Bruns, U. and Arnold, W. 2002. Seasonal changes in morphology and function of the gastrointestinal tract of free-living alpine marmots (Marmota marmota). J. Comp. Physiol. 172: 197-207.
20. Hume, I.D. and Biebach, H. 1996. Digestive tract function in the long-distance migratory garden warbler, Sylvia borin. J. Comp. Physiol. B 166: 388-395.
21. Jehl, J. R. 1997. Cyclical changes in body composition in the annual cycle and migration of the eared grebe Podiceps nigricollis. J. Avian Biol. 28: 132-142.
22. Jenni, L. and Jenni-Eiermann, S. 1998. Fuel supply and metabolic constraints in migrating birds. J. Avian Biol. 29: 521-528.
23. Jenni-Eiermann, S. and Jenni, L. 1991. Metabolic responses to flight and fasting in night-migrating passerines. J. Comp. Physiol. B 61: 465-474.
24. Karasov, W. H. 1996. Digestive plasticity in avian energetics and feeding ecology. - In: Carey, C. (ed.), Avian energetics and nutritional ecology. Chapman and Hall, New York.
25. Karasov, W. H. and 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: 435-448.
26. Karasov, W. H., Pinshow, B., Starck, J. M. and Afik, D. 2004. Anatomical and histological changes in the alimentary tract of migrating blackcaps (Sylvia atricapilla): A comparison among fed, fasted, food-restricted, and refed birds. Physiol. Biochem. Zool. 77: 149-160.
27. Kersten, M. and Visser ., W. 1996. The rate of food processing in the oystercatcher: food intake and energy expenditure constrained by a digestive bottleneck. Funct. Ecol. 10: 440-448.
28. Klaassen, M. 1996. Metabolic constraints on long-distance migration in birds. J. Exp. Biol. 199: 57-64.
29. Klaassen, M., Kvist, A. and Lindström, Å. 2000. Flight costs and fuel composition of a bird migrating in a wind tunnel. Condor 102: 444-451.
30. Landys-Ciannelli, M. M., Piersma, T. and Jukema, J. 2003. Strategic size changes of internal organs and muscle tissue in bar-tailed godwit during fat storage on a spring stopover site. Funct. Ecol. 17: 151-179.
31. Lindström, Å., Kvist, A., Piersma, T., Dekinga, A. and Dietz, M. W. 2000. Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J Exp. Biol. 203: 913-919.
32. Marsh, R. L. 1984. Adaptations of the gray catbird Dumetella carolinensis to long-distance migration: flight muscle hypertrophy associated with elevated body mass. Physiol. Zool. 57: 105-117.
33. Martinez del Rio, C., Wolf, N., Carleton, S.A. and Gannes, L. Z. 2009. Isotopic ecology ten years after a call for more laboratory experiments. Biol. Rev. 84: 91-111.
34. McWilliams, S. R. and Karasov, W. H. 2005. Migration takes guts. Digestive physiology of migratory birds and ist ecological significance. - In: Mara, P. and Greenberg, R. (eds), Birds of Two Worlds. The Ecology and Evolution of Migration. Johns Hopkins University Press, Baltimore.
35. Piersma, T. 1990. Pre-migratory "fattening" usually involves more than the deposition of fat alone. Ring. Migr. 11: 113-115.
36. Piersma, T. 2002. Energetic bottlenecks and other design constraints in avian annual cycles. Integ. Comp. Biol. 42: 51-67.
37. Piersma, T. 1998. Phenotypic flexibility during migration:optimization of organ size contingent on risk and rewards of fueling and flight?. J. Avian. Biol. 29: 511-520.
38. Piersma, T. and Drent, J. 2003. Phenotypic flexibility and the evolution of organismal design. TREE 18: 228-233.
39. Piersma, T. and Lindström, Å. 1997. Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol. Evol. 12: 134-138.
40. Piersma, T., Gudmundsson, G. A. and Lilliendahl, K. 1999. Rapid changes in the size of different functional organ and muscle groups during refuelling in a long-distance migrating shorebird. Physiol. Biochem. Zool. 72: 405-415.
41. Pigliucci, M. 1996. How organisms respond to environmental changes: From phenotypes to molecules (and vice versa). Trends Ecol. Evol. 11: 168-173.
42. Portugal, S. J., Thorpe, S. K. S., Green, J. A., Myatt, J. P. and Butler, P. 2009. Testing the use/disuse hypothesis: pectoral and leg muscle changes in captive barnacle geese Branta leucopsis during wing moult. J. Exp. Biol. 212: 2403-2410.
43. Post, D. M., Layman, C. A., Arrington, D. A., Takimoto, G., Quattrochi, J. and Montaña, C. G. 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179-189.
44. Schwilch, R., Grattarola, A., Spina, F. and Jenni, L. 2002. Protein loss during long-distance migratory flight in passerine birds: adaptation and constraint. J. Exp. Biol. 205: 687-695.
45. Secor, S. M. and Diamond, J. 1998. A vertebrate model of extreme physiological regulation. Nature 395: 659-662.
46. Stearns, S. C. 1989. The evolutionary significance of phenotypic plasticity. Bioscience 39: 436-445.
47. Swick, R. W. and Benevenga, N. J. 1976. Labile protein reserves and protein turnover. J. Dairy Sci. 60: 505-515.
48. Thouzeau, C., Robin, J.-P., Le Maho, Y. and Handrich, Y. 1999. Body reserve dynamics and energetics of barn owls during fasting in the cold. J. Comp. Physiol. 169: 612-620.
49. Travis, J. 1994. Evaluating the adaptive role of morphological plasticity. - In: Wainwright, P. C and Reilly, S. M. (eds), Ecological morphology. The University of Chicago Press.
50. Van Den Hout, P. J., Piersma, T., Dekinga, A., Lubbe, S. K. and Visser, G. H. 2006. Ruddy turnstones Arenaria interpres rapidly build pectoral muscles after a raptor scare. J. Avian Biol. 37: 425-430.
51. Van Gils, J. A., Piersma, T., Dekinga, A. and Battley, P. F. 2006. Modelling phenotypic flexibility: an optimality analysis of gizzard size in red knots (Calidris canutus). Ardea 94: 409-420.
52. Waterlow, J. C. 1999. The mysteries of nitrogen balance. Nutr. Res. Rev. 12: 25-54.
53. Wolf, N., Carleton, S. A. and Martinez del Rio, C. 2009. Ten years of experimental animal isotopic ecology. Funct. Ecol. 23: 17-26.