Limited access to food and physiological trade-offs in a long-distance migrant shorebird. I. Energy metabolism, behavior, and body-mass regulation

Physiological and Biochemical Zoology

Volumn 82, Issue 5, 2009, Pages 549-560

  Vézina, Franĉois ^a,c   Petit, Magali ^a   Buehler, Deborah M ^b   Dekinga, Anne ^a   Piersma, Theunis ^a,b  

^a ROYAL NETHERLANDS INSTITUTE FOR SEA RESEARCH   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c UNIVERSITÉ DU QUÉBEC À RIMOUSKI   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BODY MASS; FEEDING BEHAVIOR; FOOD AVAILABILITY; FOOD INTAKE; FOOD LIMITATION; METABOLISM; MIGRATORY SPECIES; MUSCLE; TRADE-OFF; WADER;

ACUTE PHASE RESPONSE; ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIRD DISEASE; BODY WEIGHT; CHARADRIIFORMES; ENERGY METABOLISM; FEMALE; FLYING; FOOD; HISTOLOGY; IMMUNOLOGY; MALE; PHYSIOLOGY; THERMOREGULATION;

ACUTE-PHASE REACTION; ANIMALS; BEHAVIOR, ANIMAL; BIRD DISEASES; BODY TEMPERATURE REGULATION; BODY WEIGHT; CHARADRIIFORMES; ENERGY METABOLISM; FEMALE; FLIGHT, ANIMAL; FOOD; MALE;

AVES; CALIDRIS CANUTUS;

EID: 70350148541     PISSN: 15222152     EISSN: None     Source Type: Journal    
DOI: 10.1086/603644     Document Type: Article

References (67)

1. Baker A.J., T. Piersma, and A.D. Greenslade. 1999. Molecular vs. phenotypic sexing in red knots. Condor 101:887-893.
2. Bautista L.M., J. Tinbergen, P. Wiersma, and A. Kacelnik. 1998. Optimal foraging and beyond: how starlings cope with changes in food availability. Am Nat 152:543-561.
3. Bech C. and K.E. Praesteng. 2004. Thermoregulatory use of heat increment of feeding in the tawny owl (Strix aluco). J Therm Biol 29:649-654.
4. Blem C.R. 1976. Pattern of lipid storage and utilization in birds. Am Zool 16:671-684.
5. 1990. Avian energy storage. Curr Ornithol 7:59-113.
6. Bruinzeel L.W. and T. Piersma. 1998. Cost reduction in the cold, heat generated by terrestrial locomotion partly substitutes for thermoregulation costs in knots Calidris canutus. Ibis 140:323-328.
7. Buehler D.M., F. Encinas-Viso, M. Petit, F. Vézina, B.I. Tieleman, and T. Piersma. 2009. Limited access to food and physiological trade-offs in a long-distance migrant shorebird. II. Constitutive immune function and the acute-phase response. Physiol Biochem Zool 82:561-571.
8. Butte N.F., W.W. Wong, M.S. Treuth, K.J. Ellis, and E.O. Smith. 2004. Energy requirements during pregnancy based on total energy expenditure and energy deposition. Am J Clin Nutr 79:1078-1087.
9. Chappell M.A., G.C. Bachman, and K.A. Hammond. 1997. The heat increment of feeding in house wren chicks, magnitude, duration, and substitution for thermostatic costs. J Comp Physiol 167:313-318.
10. Davidson N.C., P.R. Evans, and J.D. Uttley. 1986a.Geographical variation of protein reserves in birds: the pectoral muscle mass of dunlins in winter. J Zool (Lond) 208:125-133.
11. Davidson N.C., J.D. Uttley, and P.R. Evans. 1986b. Geographic variation in the lean mass of dunlins wintering in Britain. Ardea 74:191-198.
12. Deerenberg C., G.J.F. Overkamp, G.H. Visser, and S. Daan. 1998. Compensation in resting metabolism for experimentally increased activity. J Comp Physiol B 168:507-512.
13. Dekinga, A., M.W. Dietz, A. Koolhaas, and T. Piersma. 2001. Time course and reversibility of changes in the gizzards of red knots alternately eating hard and soft food. J Exp Biol 204:2167-2173.
14. Dietz M.W., A. Dekinga, T. Piersma, and S. Verhulst. 1999. Estimating organ size in small migrating shorebirds with ultrasonography, an intercalibration exercise. Physiol Biochem Zool 72:28-37.
15. Dietz M.W., T. Piersma, A. Hedenstrom, and M. Brugge. 2007. Intraspecific variation in avian pectoral muscle mass, constraints on maintaining manoeuvrability with increasing body mass. Funct Ecol 21:317-326.
16. Doherty P.F. and T.C. Grubb. 2002. Survivorship of permanentresident birds in a fragmented forested landscape. Ecology 83:844-857.
17. 2003. Relationship of nutritional condition of permanent- resident woodland birds with woodlot area, supplemental food, and snow cover. Auk 120:331-336.
18. Drent R.H. and S. Daan. 1980. The prudent parent, energetic adjustments in avian breeding. Ardea 68:225-252.
19. Ettinger A.O. and J.R. King. 1980. Time and energy budgets of the willow flycatcher (Empidonax traillii) during the breeding season. Auk 97:533-546.
20. Freeman S. and W.M. Jackson. 1990. Univariate metrics are not adequate to measure avian body size. Auk 107:69-74.
21. Gessaman J.A. and K.A. Nagy. 1988. Energy-metabolism: errors in gas-exchange conversion factors. Physiol Zool 61:507-513.
22. Graf R., S. Krishna, and H.C. Heller. 1989. Regulated nocturnal hypothermia induced in pigeons by food deprivation. Am J Physiol 256:R733-R738.
23. Kelly J.P., N. Warnock, G.W. Page, and W.W. Weathers. 2002. Effects of weather on daily body mass regulation in wintering dunlin. J Exp Biol 205:109-120.
24. Ketterson E.D. and J.R. King. 1977. Metabolic and behavioral responses to fasting in the white-crowned sparrow (Zonotrichia leucophris gambelii). Physiol Zool 50:115-129.
25. King J.R. 1972. Adaptive periodic fat storage by birds. Proc Fifteenth Int Ornithol Congr 200-217.
26. Laurila M., T. Pilto, and E. Hohtola. 2005. Testing the flexibility of fasting-induced hypometabolism in birds, effect of photoperiod and repeated food deprivations. J Therm Biol 30: 131-138.
27. Lehikoinen E. 1987. Seasonality of the daily weight cycle in wintering passerines and its consequences. Ornis Scand 18: 216-226.
28. Lessells C.M. and P.T. Boag. 1987. Unrepeatable repeatabilities, a common mistake. Auk 104:116-121.
29. LindströmÅ., A. Kvist, T. Piersma, A. Dekinga, and M.W. Dietz. 2000. Avian pectoral muscle size rapidly tracks body mass changes during flight, fasting and fuelling. J Exp Biol 203: 913-919.
30. MacArthur R.A. and K.L. Campbell. 1994. Heat increment of feeding and its thermoregulatory benefit in the muskrat (Ondatra zibethicus). J Comp Physiol B 164:141-146.
31. Masman D., M. Gordijn, S. Daan, and C. Dijkstra. 1986. Ecological energetics of the kestrel, field estimates of energy intake throughout the year. Ardea 74:24-39.
32. Merom K., S. Quader, and Y. Yom-Tov. 2005. The winter fattening model: a test at low latitude using the clamorousreed- warbler. Ibis 147:680-687.
33. Morrison R.I.G., N.C. Davidson, and J.R. Wilson. 2007. Survival of the fattest, body stores on migration and survival in red knots Calidris canutus islandica. J Avian Biol 38:479-487.
34. Nudds R.L. and D.M. Bryant. 2001. Exercise training lowers the resting metabolic rate of zebra finches, Taeniopygia guttata. Funct Ecol 15:458-464.
35. Packard G.C. and T.J. Boardman. 1988. The misuse of ratio, indices, and percentages in ecophysiological research. Physiol Zool 61:1-9.
36. 1999 The use of percentages and size-specific indices to normalize physiological data for variation in body size, wasted time, wasted effort? Comp Biochem Physiol A 122: 37-44.
37. Piersma T. 2002. Energetic bottlenecks and other design constraints in avian annual cycles. Integr Comp Biol 42:51-67.
38. 2007. Using the power of comparison to explain habitat use and migration strategies of shorebirds worldwide. J Ornithol 148:S45-S59.
39. Piersma T., N. Cadée, and S. Daan. 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.
40. Piersma T. and J. Drent. 2003. Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228- 233.
41. Piersma T., J.A. Gessaman, A. Dekinga, and G.H. Visser. 2004. Gizzard and other lean mass components increase, yet basal metabolic rates decrease, when red knots Calidris canutus are shifted from soft to hard-shelled food. J Avian Biol 35:99- 104.
42. Piersma T., A. Koolhaas, A. Dekinga, and E. Gwinner. 2000. Red blood cell and white blood cell counts in sandpipers (Philomachus pugnax, Calidris canutus): effect of captivity, season, nutritional status, and frequent bleeding. Can J Zool 78:1349-1355.
43. Poppitt S.D., J.R. Speakman, and P.A. Racey. 1993. The energetics of reproduction in the common shrew (Sorex araneus), a comparison of indirect calorimetry and the doubly labeled water method. Physiol Zool 66:964-982.
44. Rashotte M.E. and D. Henderson. 1988. Coping with rising food costs in a closed economy: feeding-behavior and nocturnal hypothermia in pigeons. J Exp Anal Behav 50:441- 456.
45. Rashotte M.E., S. Saarela, R.P. Henderson, and E. Hohtola. 1999. Shivering and digestion-related thermogenesis in pigeons during dark phase. Am J Physiol 277:R1579-R1587.
46. Reneerkens J., T. Piersma, and M. Ramenofsky. 2002. An experimental test of the relationship between temporal variability of feeding opportunities and baseline levels of corticosterone in a shorebird. J Exp Zool 293:81-88.
47. Rising J.D. and K.M. Somers. 1989. The measurement of overall body size in birds. Auk 106:666-674.
48. Robin J.-P., Y. Handrich, Y. Cherel, and Y. Le Maho. 1989. Energy saving during breeding and molt in birds. Pp. 293- 304 in C. Bech and R.E. Reinertsen, eds. Physiology of Cold Adaptation in Birds. Plenum, New York.
49. Schmidt-Nielsen K. 1990. Animal Physiology: Adaptation and Environment. Cambridge University Press, Cambridge.
50. Secor S.M. and J. Diamond. 1998. A vertebrate model of extreme physiological regulation. Nature 395:659-662.
51. Selman C. and P.R. Evans. 2005. Alterations in tissue aerobic capacity may play a role in premigratory fattening shorebirds. Biol Lett 1:101-104.
52. Senar J.C. and J. Pascual. 1997. Keel and tarsus length may provide a good predictor of avian body size. Ardea 85:269- 274.
53. Shapiro C.J. and W.W. Weathers. 1981. Metabolic and behavioral responses of American kestrels to food deprivation. Comp Biochem Physiol 68:111-114.
54. Speakman J.R., A. Gidney, J. Bett, I.P. Mitchell, and M.S. Johnson. 2001. Limits to sustained energy intake. IV. Effect of variation in food quality on lactating mice Mus musculus. J Exp Biol 204:1957-1965.
55. Tiebout H.M. 1991. Daytime energy management by tropical hummingbirds: responses to foraging constraint. Ecology 72: 839-851.
56. Vaanholt L.M., B. Jong, T. Garland, S. Daan, and G.H. Visser. 2007. Behavioral and physiological responses to increased foraging effort in male mice. J Exp Biol 210:2013-2024.
57. van Gils, J.A., A. Dekinga, B. Spaans, W.K. Vahl, and T. Piersma. 2005. Digestive bottleneck affects foraging decisions in red knots Calidris canutus. II. Patch choice and length of working day. J Anim Ecol 74:102-130.
58. van Gils, J.A., B. Spaans, A. Dekinga, and T. Piersma. 2006. Foraging in a tidally structured environment by red knots (Calidris canutus): ideal, but not free. Ecology 87:1189-1202.
59. Vézina F., K.M. Jalvingh, A. Dekinga, and T. Piersma. 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.
60. 2007. Thermogenic side effects to migratory predisposition in shorebirds. Am J Physiol 292:R1287-R1297.
61. Vézina F. and T.D. Williams. 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.
62. Weathers W.W. and K.A. Sullivan. 1993. Seasonal patterns of time and energy allocation by birds. Physiol Zool 66:511- 536.
63. Wiersma P. and T. Piersma. 1994. Effects of microhabitat, flocking, climate and migratory goal on energy-expenditure in the annual cycle of red knots. Condor 96:257-279.
64. Wiersma P., H.M. Salomons, and S. Verhulst. 2005. Metabolic adjustments to increasing foraging costs of starlings in a closed economy. J Exp Biol 208:4099-4108.
65. Wiersma P. and S. Verhulst. 2005. Effects of intake rate on energy expenditure, somatic repair and reproduction of zebra finches. J Exp Biol 208:4091-4098.
66. Wikelski M. and R.E. Ricklefs. 2001. The physiology of life histories. Trends Ecol Evol 16:479-481.
67. Zwarts L., J.B. Hulscher, K. Koopman, and P.M. Zegers. 1996. Short-term variation in the body weight of oystercatchers Haematopus ostralegus: effect of available feeding time by day and night, temperature and wind force. Ardea 84A:357-372.