Physiological responses to food deprivation in the house sparrow, a species not adapted to prolonged fasting

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 303, Issue 5, 2012, Pages

  Khalilieh, Anton ^a   McCue, Marshall D ^b   Pinshow, Berry ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b ST MARY'S UNIVERSITY   (United States)

Author keywords

13CO2; Blood metabolites; Breath testing; Fasting; House sparrow; Stable isotopes; Starvation

Indexed keywords

3 HYDROXYBUTYRIC ACID; CARBOHYDRATE; CARBON 13; CARBON DIOXIDE; GLUCOSE; GLYCINE; LIPID; PALMITIC ACID; PROTEIN; TRIACYLGLYCEROL;

ADAPTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD LEVEL; BREATH ANALYSIS; CONTROLLED STUDY; DIET RESTRICTION; FEMALE; FOOD DEPRIVATION; MALE; NONHUMAN; OXIDATION; PRIORITY JOURNAL; SPARROW; SPECIES DIFFERENCE; SUBSPECIES;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BREATH TESTS; CARBON ISOTOPES; FASTING; FOOD DEPRIVATION; GLUCOSE; GLYCINE; LIPID METABOLISM; SPARROWS; TIME FACTORS;

EID: 84865770473     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00076.2012     Document Type: Article

References (67)

1. Allen WV. Biochemical aspects of lipid storage and utilization in animals. Am Zool 16: 631-647, 1976.
2. Alonso-Alvarez C, Ferrer M. A biochemical study of fasting, subfeeding, and recovery processes in yellow-legged gulls. Physiol Biochem Zool 74: 703-713, 2001.
3. Amat JA, Hortas F, Arroyo GM, Rendon MA, Ramirez JM, Rendon- Martos M, Perez-Hurtado A, Garrido A. Interannual variations in feeding frequencies and food quality of greater flamingo chicks (Phoenicopterus roseus): evidence from plasma chemistry and effects on body condition. Comp Biochem Physiol A 147: 569-576, 2007.
4. Anderson TR. Biology of the Ubiquitous House Sparrow: From Genes to Populations. Oxford, UK: Oxford University Press, 2006.
5. Battley PF, Dietz MW, Piersma T, Dekinga A, Tang SX, Hulsman K. 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, 2001.
6. Bauchinger U, Biebach H. Differential catabolism of muscle protein in Garden Warblers (Sylvia borin): flight and leg muscle act as a protein source during long distance migration. J Comp Physiol B 171: 293-301, 2001.
7. Blem CR. Avian energy storage. Current Ornithol 7: 59-113, 1990.
8. Blem CR. Geographic variation in the bioenergetics of the house sparrow. Ornithol Monogr 14: 96-121, 1973.
9. Booth AM, Minot EO, Fordham RA, Imber MJ. Co-ordinated food provisioning in the little shearwater Puffinus assimilis haurakiensis: a previously undescribed foraging strategy in the Procellariidae. Ibis 142: 145-146, 2000.
10. Bos C, Metges CC, Gaudichon C, Petze KJ, Pueyo ME, Morens C, Everwand J, Benamouzig R, Tome D. Postprandial kinetics of dietary amino acids are the main determinant of their metabolism after soy or milk protein ingestion in humans. J Nutr 133: 1308-1315, 2003.
11. Burlington RF, Klain GJ. Gluconeogenesis during hibernation and arousal from hibernation. Comp Biochem Physiol 22: 701-708, 1967.
12. Buyse J, Geypens B, Malheiros RD, Moraes VM, Swennen Q, Decuypere E. Assessment of age-related glucose oxidation rates of broiler chickens by using stable isotopes. Life Sci 75: 2245-2255, 2004.
13. Caloin M. Modeling of lipid and protein depletion during total starvation. Am J Physiol Endocrinol Metab 287: E790-E798, 2004.
14. Castellini MA, Rea LD. The biochemistry of natural fasting at its limits. Experientia 48: 575-582, 1992.
15. Chaurand T, Weimerskirch H. The regular alternation of short and long foraging trips in the blue petrel Halobaena caerulea - a previously undescribed strategy of food provisioning in a pelagic seabird. J Anim Ecol 63: 275-282, 1994.
16. Cherel Y, LeMaho Y. Five months of fasting in king penguin chicks: body mass loss and fuel metabolism. Am J Physiol Regul Integr Comp Physiol 249: R387-R392, 1985.
17. Cherel Y, Robin JP, Heitz A, Calgari C, LeMaho Y. Relationships between lipid availability and protein-utilization during prolonged fasting. J Comp Physiol B 162: 305-313, 1992.
18. Cherel Y, Robin JP, LeMaho Y. Physiology and biochemistry of long-term fasting in birds. Can J Zool 66: 159-166, 1988.
19. Craig H. Isotopic standards for carbon and oxygen and correction factors for mass-spectrometric analysis of carbon dioxide. Geochim Cosmochim Ac 12: 133, 1957.
20. Dawson WR, Yacoe ME, Marsh RL. Metabolic adjustments of small passerine birds for migration and cold. Am J Physiol Regul Integr Comp Physiol 245: R755-R767, 1983.
21. Dugan PJ, Evans PR, Goodyer LR, Davidson NC. Winter fat reserves in shorebirds- disturbance of regulated levels by severe weather conditions. Ibis 123: 359-363, 1981.
22. Frick NT, Bystriansky JS, Ip YK, Chew SF, Ballantyne JS. Carbohydrate and amino acid metabolism in fasting and aestivating African lungfish (Protopterus dolloi). Comp Biochem Physiol A 151: 85-92, 2008.
23. Gjedde A, Crone C. Induction processes in blood-brain transfer of ketone-bodies during starvation. Am J Physiol 229: 1165-1169, 1975.
24. Goodman M. Protein sparing in skeletal-muscle during prolonged starvation- dependence on lipid fuel availability. Diabetes 36: 14, 1987.
25. Hamer KC, Nicholson LW, Hill JK, Wooller RD, Bradley JS. Nestling obesity in procellariiform seabirds: temporal and stochastic variation in provisioning and growth of short-tailed shearwaters Puffinus tenuirostris. Oecologia (Berl) 112: 4-11, 1997.
26. Hedenstrom A. Extreme endurance migration: what is the limit to non-stop flight? PLoS Biol 8: 2010.
27. Hervant F, Mathieu J, Barre H, Simon K, Pinon C. Comparative study on the behavioral, ventilatory, and respiratory responses of hypogean and epigean crustaceans to long-term starvation and subsequent feeding. Comp Biochem Physiol A 118: 1277-1283, 1997.
28. Hervant F, Renault D. Long-term fasting and realimentation in hypogean and epigean isopods: a proposed adaptive strategy for groundwater organisms. J Exp Biol 205: 2079-2087, 2002.
29. Hudson JW, Kimzey AL. Temperature regulation and metabolic rhythms in populations of the house sparrow, Passer domesticus. Comp Biochem Physiol 17: 203-217, 1966.
30. Jenni-Eiermann S, Jenni L. Metabolic responses to flight and fasting in night-migrating passerines. J Comp Physiol B 161: 465-474, 1991.
31. Jenni-Eiermann S, Jenni L. Plasma metabolite levels predict individual body-mass changes in a small long-distance migrant, the garden-warbler. Auk 111: 888-899, 1994.
32. Jenni-Eiermann S, Jenni L. What can plasma metabolites tell us about the metabolism, physiological state and condition of individual birds? An overview. Biol Cons Fauna 312-319, 1998.
33. Jenni-Eiermann S, Jenni L, Piersma T. Plasma metabolites reflect seasonally changing metabolic processes in a long-distance migrant shorebird (Calidris canutus). Zoology 105: 239-246, 2002.
34. Jenni L, Jenni-Eiermann S. Fuel supply and metabolic constraints in migrating birds. J Comp Physiol B 29: 521-528, 1998.
35. Jenni L, Schaub M. Behavioural and physiological reactions to environmental variation in bird migration: a review. In: Avian Migration, edited by Berthold P, Gwinner E, and Sonneenschein E. New York: Springer- Verlag, 2003, p. 155-171.
36. Karasov WH, Pinshow B. Changes in lean mass and in organs of nutrient assimilation in a long-distance passerine migrant at a springtime stopover site. Phys Zool 71: 435-448, 1998.
37. Klaassen M, Biebach H. Energetics of fattening and starvation in the long-distance migratory garden warbler, Sylvia borin, during the migratory phase. J Comp Physiol B 164: 362-371, 1994.
38. Klaassen M, Lindstrom A, Zijlstra R. Composition of fuel stores and digestive limitations to fuel deposition rate in the long-distance migratory thrush nightingale, Luscinia luscinia. Physiol Zool 70: 125-133, 1997.
39. Le Maho Y. Metabolic adaptations to long-term fasting in antarctic Penguins and Domestic Geese. J Therm Biol 8: 91-96, 1983.
40. Le Maho Y, Vankha HV, Koubi H, Dewasmes G, Girard J, Ferre P, Cagnard M. Body-composition, energy-expenditure, and plasma metabolites in long-term fasting geese. Am J Physiol Endocrinol Metab 241: E342-E354, 1981.
41. Lehikoinen E. Winter Ecology of Passerines: Significance of Weight and Size. Report Number 14. Department of Biology, University of Turku, Turku, Finland, 1986.
42. Lighton J. Measuring Metabolic Rates: a Manual for Scientists. Oxford, UK: Oxford University Press, 2008.
43. Lima SL. Predation risk and unpredictable feeding conditions: determinants of body mass in birds. Ecology 67: 377-385, 1986.
44. Masoro EJ. Physiological Chemistry of Lipids in Mammals. Philadelphia, PA: Saunders, 1968.
45. McCarthy MD, Benner R, Lee C, Fogel ML. Amino acid nitrogen isotopic fractionation patterns as indicators of heterotrophy in plankton, particulate, and dissolved organic matter. Geochim Cosmochim Ac 71: 4727-4744, 2007.
46. McCue MD. Starvation physiology: Reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A 156: 1-18, 2010.
47. McCue MD. Tracking the oxidative and nonoxidative fates of isotopically labeled nutrients in animals. Bioscience 61: 217-230, 2011.
48. McCue MD, Amitai O, Khozin-Goldberg I, McWilliams SR, Pinshow B. Effect of dietary fatty acid composition on fatty acid profiles of polar and neutral lipid tissue fractions in zebra finches, Taeniopygia guttata. Comp Biochem Physiol A 154: 165-172, 2009.
49. McCue MD, McWilliams SR, Pinshow B. Ontogeny and nutritional status influence oxidative kinetics of nutrients and whole-animal bioenergetics in zebra finches, Taeniopygia guttata: new applications for 13C breath testing. Physiol Biochem Zool 84: 32-42, 2011.
50. McCue MD, Sivan O, McWilliams SR, Pinshow B. Tracking the oxidative kinetics of carbohydrates, amino acids and fatty acids in the house sparrow using exhaled 13CO2. J Exp Biol 213: 782-789, 2010.
51. McCue MD, Smith A, McKinney R, Rewald B, Pinshow B, McWilliams SR. A mass balance approach to identify and compare differential routing of 13C-labeled carbohydrates, lipids, and proteins in vivo. Physiol Biocheml Zool 84: 506-513, 2011.
52. Miles JM, Haymond MW, Gerich JE. Suppression of glucose-production and stimulation of insulin-secretion by physiological concentrations of ketone-bodies in man. J Clin Endocrinol Metab 52: 34-37, 1981.
53. Mrosovsky N, Sherry D. Animal anorexias. Science 207: 837-842, 1980.
54. Navarro I, Gutierrez J. Fasting and starvation. In: In Biochemistry and Molecular Biology of Fishes, edited by Hochachka PW, and Mommsen WTP. Amsterdam: Elsevier Science, 1995, p. 393-434.
55. Peroni O, Large V, Beylot M. Measuring gluconeogenesis with 2-C-13 glycerol and mass isotopomer distribution analysis of glucose. Am J Physiol Endocrinol Metab 269: E516-E523, 1995.
56. Piersma T. Why marathon migrants get away with high metabolic ceilings: towards an ecology of physiological restraint. J Exp Biol 214: 295-302, 2011.
57. Piersma T, Jukema J. Budgeting the flight of a long-distance migrant - changes in nutrient reserve levels of bar-tailed godwits at successive spring staging sites. Ardea 78: 315-337, 1990.
58. Richdale LE. Biology of the sooty shearwater Puffinus griseus. Proc Zool Soc Lond 141: 141-117, 1963.
59. Robinson AM, Williamson DH. Physiological roles of ketone-bodies as substrates and signals in mammalian-tissues. Physiol Rev 60: 143-187, 1980.
60. Schaub M, Jenni L. Fuel deposition of three passerine bird species along the migration route. Oecologia (Berl) 122: 306-317, 2000.
61. Sokoloff L. Metabolism of ketone bodies in the brain. Annu Rev Med 24: 271-280, 1973.
62. Tabiri HY, Bertolo RFP, Ball RO, Korver DR. Development of the indicator amino acid oxidation technique in chickens: Calibration of oxidation system and determination of bicarbonate retention factor. Poult Sci 81: 1020-1025, 2002.
63. Thouzeau C, Robin JP, Le Maho Y, Handrich Y. Body reserve dynamics and energetics of barn owls during fasting in the cold. J Comp Physiol B 169: 612-620, 1999.
64. Vandenheuvel FA. Structure of membranes and role of lipids therein. Adv Lipid Res 9: 161-248, 1971.
65. Vezina F, Williams TD. The metabolic cost of egg production is repeatable. J Exp Biol 208: 2533-2538, 2005.
66. Wang T, Hung CCY, Randall DJ. The comparative physiology of food deprivation: From feast to famine. Annu Rev Physiol 68: 223-251, 2006.
67. Weber JM. The physiology of long-distance migration: extending the limits of endurance metabolism. J Exp Biol 212: 593-597, 2009.