Heterothermy in small, migrating passerine birds during stopover: Use of hypothermia at rest accelerates fuel accumulation

Journal of Experimental Biology

Volumn 212, Issue 19, 2009, Pages 3068-3075

  Wojciechowski, Michał S ^a   Pinshow, Berry ^b  

^a NICOLAUS COPERNICUS UNIVERSITY   (Poland)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Heterothermy; Hypothermia; Migration; Passerine bird; Stopover; Sylvia atricapilla

Indexed keywords

ANIMAL; ARTICLE; BODY SIZE; BODY TEMPERATURE; ENERGY METABOLISM; FEMALE; HISTOLOGY; MALE; PHYSIOLOGY; POPULATION MIGRATION; SONGBIRD; TEMPERATURE; THERMOREGULATION;

ANIMAL MIGRATION; ANIMALS; BODY SIZE; BODY TEMPERATURE; BODY TEMPERATURE REGULATION; ENERGY METABOLISM; FEMALE; MALE; PASSERIFORMES; TEMPERATURE;

ANIMALIA; AVES; PASSERIFORMES; SYLVIA ATRICAPILLA;

EID: 70349117231     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.033001     Document Type: Article

References (62)

1. Bairlein, F. (2002). How to get fat: nutritional mechanisms of seasonal fat accumulation In migratory songbirds. Naturwissenschaften 89, 1-10.
2. 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. (Pubitemid 32501232)
3. Bauchinger, U., Wohlmann, A. and Biebach, H. (2005). Flexible remodeling of organ size during spring migration of the garden warbler (Sylvia boriri). Zoology 108, 97-106. (Pubitemid 40793379)
4. Berthold, P. (1996). Control of Bird Migration. London: Chapman & Hall.
5. Bicudo, J., Vianna, C. R. and Chaui-Berlinck, J. G. (2001). Thermogenesls in birds. Biosci. Rep. 21, 181-188.
6. Biebach, H. (1996). Energetics of winter and migratory fattening. In Avian Energetics and Nutritional Ecology (ed. C. Carey), pp. 280-323. New York: Chapman & Hall.
7. Biebach, H., Friedrich, W. and Heine, G. (1986). Interaction of body mass, fat, foraging and stopover period In trans-Sahara migrating passerine birds. Oecologia 69, 370-379. (Pubitemid 18282952)
8. Biebach, H., Biebach, I., Friedrich, W., Heine, G., Partecke, J. and Schmidl, D. (2000). Strategics of passerine migration across the Mediterranean Sea and the Sahara Desert: a radar study. Ibis 142, 623-634. (Pubitemid 30778700)
9. Boix-Hinzen, C. and Lovegrove, B. G. (1998). Circadian metabolic and thermoregulatory patterns of red-billed woodhoopoes (Phoeniculus purpureus): the influence of huddling. J. Zool. Lond. 244, 33-41. (Pubitemid 28161477)
10. Bowlin, M. S., Cochran, W. W. and Wikelski, M. C. (2005). Blotelemetry of New World thrushes during migration: physiology, energetics and orientation in the wild. Integr. Comp. Biol. 45, 295-304.
11. Butler, P. J. and Woakes, A. J. (2001). Seasonal hypothermia In a large migrating bird: saving energy for fat deposition? J. Exp. Biol. 204, 1361-1367.
12. Carmi, N., Pinshow, B., Porter, W. P. and Jaeger, J. (1992). Water and energy limitations on flight duration in small migrating birds. Auk 109, 268-276.
13. Carpenter, F. L. and Hixon, M. A. (1988). A new function for torpor-fat conservation in a wild migrant hummingbird. Condor 90, 373-378.
14. Chaplin, S. B. (1982). The energetic significance of huddling behavior In common bushtits (Psaltriparus minimus). Auk 99, 424-430.
15. Cramp, S. (1992). The Birds of the Western Palearctic, vol.6. Oxford: Oxford University Press.
16. Dawson, W. R. and Whittow, G. C. (2000). Regulation of body temperature. In Sturkie's Avian Physiology (ed. G. C. Whittow), pp. 343-390. New York: Academic Press.
17. Du Plessis, M. A. and Williams, J. B. (1994). Communal cavity roosting in green woodhoopoes - consequences for energy-expenditure and the seasonal pattern of mortality. Auk 111, 292-299.
18. Gannes, L. Z. (2002). Mass change pattern of blackcaps refueling during spring migration: evidence for physiological limitations to food assimilation. Condor 104, 231-239.
19. Geiser, F., Goodship, N. and Pavey, C. R. (2002). Was basking important In the evolution of mammalian endothermy? Naturwissenschaften 89, 412-414. (Pubitemid 35192095)
20. Gosier, A. G., Greenwood, J. J. D., Baker, J. K. and Davidson, N. C. (1998). The field determination of body size and condition In passerines: a report to the British Ringing Committee. Bird Study 45, 92-103.
21. Graf, R., Krishna, S. and Heller, H. C. (1989). Regulated nocturnal hypothermia induced in pigeons by food deprivation. Am. J. Physiol. 256, R733-R738. (Pubitemid 19086524)
22. Gwinner, E., Biebach, H. and Vonkries, I. (1985). Food availability affects migratory restlessness In caged garden warblers (Sylvia borin). Naturwissenschaften 72, 51-52.
23. Hedenström, A. and Alerstam, T. (1997). Optimum fuel loads in migratory birds: distinguishing between time and energy minimization. J. Theor. Biol. 189, 227-234. (Pubitemid 28039531)
24. Heinrich, B. (2003). Overnighting of golden-crowned kinglets during winter. Wilson Bull. 115, 113-114.
25. Hieben, S. (1993). Seasonal-changes in body-mass and use of torpor In a migratory hummingbird. Auk 110, 787-797.
26. Hohtola, E., Hissa, R., Pyörnilä, A., Rintamäki, H. and Saarela, S. (1991). Nocturnal hypothermia In fasting Japanese quail: the effect of ambient temperature. Physiol. Behav. 49, 563-567.
27. 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.
28. Humphries, M. M., Thomas, D. W. and Kramer, D. L. (2003). The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol. Biochem. Zool. 76, 165-179.
29. IUPS Thermal Commission (2001). Glossary of terms for thermal physiology. Jpn. J. Physiol. 51, 245-280.
30. Jefimow, M., Wojciechowski, M., Masuda, A. and Oishi, T. (2004). Correlation between torpor frequency and capacity for non-shivering thermogenesls in the Siberian hamster (Phodopus sungorus). J. Therm. Biol. 29, 641-647. (Pubitemid 39311192)
31. 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. (Pubitemid 28314384)
32. Karasov, W. H. and Pinshow, B. (2000). Test for physiological limitation to nutrient assimilation in a long-distance passerine migrant at a springtime stopover site. Physiol. Biochem. Zool. 73, 335-343.
33. Karasov, W. H., Pinshow, B., Starek, 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. Zoom, 149-160. (Pubitemid 38504372)
34. Klaassen, M. and 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, 362-371. (Pubitemid 2141844)
35. 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.
36. Krementz, D. G. and Pendleton, G. W. (1990). Fat scoring: sources of variability. Condor 92, 500-507.
37. Le Maho, Y. (1977). Emperor penguin strategy to live and breed in cold. Am. Sci. 65, 680-693.
38. Marom, S., Korine, C., Wojciechowski, M. S. and Pinshow, B. (2006). Energy metabolism and evaporative water loss in two desert-dwelling, sympatric microchiropteran species. Physiol. Biochem. Zool. 79, 965-976.
39. McKechnie, A. E. and Lovegrove, B. G. (2001). Thermoregulation and the energetic significance of clustering behavior In the white-backed mouseblrd (Colius colius). Physiol. Biochem. Zool. 74, 238-249.
40. McKechnie, A. E. and Lovegrove, B. G. (2002). Avian facultative hypothermic responses: a review. Condor 104, 705-724.
41. McKechnie, A. E. and Lovegrove, B. G. (2003). Facultative hypothermic responses in an Afrotroplcal arid-zone passerine, the red-headed finch (Amadina erythrocephala). J. Comp. Physiol. B 173, 339-346.
42. McKechnie, A. E. and Wolf, B. O. (2004). The energetics of the rewarmlng phase of avian torpor. In Life in the Cold: Evolution, Mechanisms, Adaptation and Application (Biological Papers of the University of Alaska 27) (ed. B. M. Barnes and H. V. Carey), pp. 265-273. Fairbanks, AK: Institute of Arctic Biology, University of Alaska.
43. McKechnie, A. E., Körtner, G. and Lovegrove, B. G. (2006). Thermoregulation under semi-natural conditions In specked mousebirds: the role of communal roosting. Afr. Zool. 41, 155-163. (Pubitemid 44734158)
44. McKechnie, A. E., Ashdown, R. A. M., Christian, M. B. and Brigham, R. M. (2007). Torpor in an African caprimulgid, the freckled nightjar Caprimulgus tristigma. J. Avian Biol. 38, 261-266.
45. McWilliams, S. R., Guglielmo, C., Pierce, B. and Klaassen, M. (2004). Flying, fasting, and feeding In birds during migration: a nutritional and physiological ecology perspective. J. Avian Biol. 35, 377-393. (Pubitemid 39275400)
46. Moreau, R. E. (1972). The Palearctic African Bird Migration Systems. London: Academic Press.
47. Pennycuick, C. J. and Battley, P. F. (2003). Burning the engine: a time-marching computation of fat and protein consumption In a 5420-km non-stop flight by great knots, Calidris tenuirostris. Oikos 103, 323-332.
48. Pinshow, B., Fedak, M. A., Battles, D. R. and Schmidt-Nielsen, K. (1976). Energy expenditure for thermoregulation and locomotion In emperor penguins. Am. J. Physiol. 231, 903-912.
49. Prinzinger, R., Preßmar, A. and Schleucher, E. (1991). Body temperature In birds. Comp. Biochem. Physiol. 99A, 499-506.
50. Reinertsen, R. E. (1996). Physiological and ecological aspects of hypothermia. In Avian Energetics and Nutritional Ecology (ed. C. Carey), pp. 125-157. New York: Chapman & Hall.
51. Schaub, M. and Jenni, L. (2000). Body mass of six long-distance migrant passerine species along the autumn migration route. J. Omithol. 141, 441-460. (Pubitemid 30813842)
52. Schleucher, E. (2004). Torpor In birds: taxonomy, energetics, and ecology. Physiol. Biochem. Zool. 77, 942-949.
53. Schleucher, E. and Prinzinger, R. (2006). Heterothermla and torpor in birds: highly specialized physiological ability or just deep "nocturnal hypothermia"? The limitations of terminology. Acta Zool. Sin. 52 Suppl., 393-396.
54. Smith, S. M. (1972). Roosting aggregations of bushtits In response to cold temperatures. Condor 74, 478-479.
55. Speakman, J. R. and Rowland, A. (1999). Preparing for inactivity: how Insectivorous bats deposit a fat store for hibernation. Proc. Nutr. Soc. 58, 123-131.
56. Steen, J. (1958). Climatic adaptation in some small northern birds. Ecology 39, 625-629.
57. Tracy, C. R., Wojciechowski, M. S., McWhorter, T. J., Yosef, R., Karasov, W. H. and Pinshow, B. (2005). Carbohydrate absorption In migrating blackcaps, upon arrival and after refeedlng, at a stopover in southern Israel, lntegr. Comp. Biol. 45, 1085.
58. Welton, N. J., Houston, A. I., Ekman, J. and McNamara, J. M. (2002). A dynamic model of hypothermia as an adaptive response by small birds to winter conditions. Acta Biotheor. 50, 39-56. (Pubitemid 34231303)
59. Wikelski, M., Tarlow, E. M., Raim, A., Diehl, R. H., Larkin, R. P. and Visser, G. H. (2003). Costs of migration In free-flying songbirds. Nature 423, 704.
60. Wingfield, J. C, Schwabl, H. and Mattocks, P. W., Jr (1990). Endocrine mechanisms of migration. In Bird Migration: Physiology and Ecophysiology (ed. E. Gwinner), pp. 233-256. Berlin: Springer-Verlag.
61. Wojciechowski, M., Yosef, R. and Pinshow, B. (2005). Body composition of small migrating birds at a stopover site In southern Israel, integr. Comp. Biol. 44, 666.
62. Wojciechowski, M. S., Jefimow, M. and Pinshow, B. (2008). Blackcaps huddle at night at migratory stopovers. In Hypometabolism in Animals: Torpor, Hibernation and Cryobiology (ed. B. G. Lovegrove and A. E. McKechnie), pp. 405-414. University of KwaZulu-Natal, Pietermarltzburg: Interpak Books.