Daily energy expenditure increases in response to low nutritional stress in an Arctic-breeding seabird with no effect on mortality

Functional Ecology

Volumn 23, Issue 6, 2009, Pages 1081-1090

  Welcker, Jorg ^a,b   Harding, Ann M A ^c,d   Kitaysky, Alexander S ^e   Speakman, John R ^f   Gabrielsen, Geir W ^a  

^a NORWEGIAN POLAR INSTITUTE   (Norway)

^b UNIVERSITY OF TROMSØ   (Norway)

^c ALASKA PACIFIC UNIVERSITY   (United States)

^d UNIVERSITY OF LEEDS   (United Kingdom)

^e UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^f UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

Body mass; Doubly labelled water; Fitness; Little auk; Parental effort; Survival

Indexed keywords

BIOENERGETICS; BODY MASS; BREEDING POPULATION; CONCENTRATION (COMPOSITION); FITNESS; HORMONE; MORTALITY; NUTRIENT LIMITATION; PARENTAL CARE; PHYSIOLOGICAL RESPONSE; PLASMA; REPRODUCTIVE SUCCESS; SEABIRD; SURVIVAL;

ALLE ALLE; ANIMALIA; PINGUINUS;

EID: 70449386867     PISSN: 02698463     EISSN: 13652435     Source Type: Journal    
DOI: 10.1111/j.1365-2435.2009.01585.x     Document Type: Article

References (80)

1. Amat, J.A., Visser, G.H., Perez-Hurtado, A. Arroyo, G.M. (2000) Brood desertion by female shorebirds: a test of the differential parental capacity hypothesis on Kentish plovers. Proceedings of the Royal Society of London Series B-Biological Sciences, 267, 2171 2176.
2. Auel, H., Harjes, M., Da Rocha, R., Stubing, D. Hagen, W. (2002) Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biology, 25, 374 383.
3. Beckman, K.B. Ames, B.N. (1998) The free radical theory of aging matures. Physiological Reviews, 78, 547 581.
4. Berteaux, D., Thomas, D.W., Bergeron, J.M. Lapierre, H. (1996) Repeatability of daily field metabolic rate in female meadow voles (Microtus pennsylvanicus). Functional Ecology, 10, 751 759.
5. Brand, M.D. (2000) Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Experimental Gerontology, 35, 811 820.
6. Brown, C.R., Brown, M.B. Brazeal, K.R. (2008) Familiarity with breeding habitat improves daily survival in colonial cliff swallows. Animal Behaviour, 76, 1201 1210.
7. Brown, J.H., Gillooly, J.F., Allen, A.P., Savage, V.M. West, G.B. (2004) Toward a metabolic theory of ecology. Ecology, 85, 1771 1789.
8. Bryant, D.M. (1991) Constraints on energy expenditure by birds. Acta XX Congressus Internationalis Ornithologici, IV, 1989 2001.
9. Bryant, D.M. (1997) Energy expenditure in wild birds. Proceedings of the Nutrition Society, 56, 1025 1039.
10. Bryant, D.M. Tatner, P. (1988) The costs of brood provisioning: effects of brood size and food supply. Acta XIX Congressus Internationalis Ornithologici, V, 364 379.
11. Butler, P.J., Green, J.A., Boyd, I.L. Speakman, J.R. (2004) Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Functional Ecology, 18, 168 183.
12. Cairns, D.K. (1987) Seabirds as indicators of marine food supplies. Biological Oceanography, 5, 261 267.
13. Chaurand, T. Weimerskirch, H. (1994) The regular alternation of short and long foraging trips in the Blue Petrel Halobaena caerulea: a previously undescribed strategy of food provsioning in a pelagic seabird. Journal of Animal Ecology, 63, 275 282.
14. Clinchy, M., Zanette, L., Boonstra, R., Wingfield, J.C. Smith, J.N.M. (2004) Balancing food and predator pressure induces chronic stress in songbirds. Proceedings of the Royal Society of London Series B-Biological Sciences, 271, 2473 2479.
15. Daan, S., Deerenberg, C. Dijkstra, C. (1996) Increased daily work precipitates natural death in the kestrel. Journal of Animal Ecology, 65, 539 544.
16. Dale, K., Falk-Petersen, S., Hop, H. Fevolden, S.E. (2006) Population dynamics and body composition of the Arctic hyperiid amphipod Themisto libellula in Svalbard fjords. Polar Biology, 29, 1063 1070.
17. Deerenberg, C., Pen, I., Dijkstra, C., Arkies, B.J., Visser, G.H. Daan, S. (1995) Parental energy-expenditure in relation to manipulated brood size in the european kestrel Falco tinnunculus. Zoology-Analysis of Complex Systems, 99, 39 48.
18. Falk-Petersen, S. (1981) Ecological investigations on the zooplankton community of Balsfjorden, northern Norway: seasonal changes in body weight and the main biochemical composition of Thysanoessa inermis (Kroyer), Thysanoessa raschii (M.Sars), and Meganyctiphanes norvegica (M.Sars) in relation to environmental factors. Journal of Experimental Marine Biology and Ecology, 49, 103 120.
19. Fridolfsson, A.K. Ellegren, H. (1999) A simple and universal method for molecular sexing of non-ratite birds. Journal of Avian Biology, 30, 116 121.
20. Furness, R.W. Bryant, D.M. (1996) Effect of wind on field metabolic rates of breeding Northern Fulmars. Ecology, 77, 1181 1188.
21. Fyhn, M., Gabrielsen, G.W., Nordoy, E.S., Moe, B., Langseth, I. Bech, C. (2001) Individual variation in field metabolic rate of kittiwakes (Rissa tridactyla) during the chick-rearing period. Physiological and Biochemical Zoology, 74, 343 355.
22. Gabrielsen, G.W., Taylor, J.R.E., Konarzewski, M. Mehlum, F. (1991) Field and laboratory metabolism and thermoregulation in Dovekies (Alle alle). Auk, 108, 71 78.
23. Gessaman, J.A. Nagy, K.A. (1988) Energy metabolism: errors in gas-exchange conversion factors. Physiological Zoology, 61, 507 513.
24. Golet, G.H., Schmutz, J.A., Irons, D.B. Estes, J.A. (2004) Determinants of reproductive costs in the long-lived Black-legged Kittiwake: a multiyear experiment. Ecological Monographs, 74, 353 372.
25. Gorman, M.L., Mills, M.G., Raath, J.P. Speakman, J.R. (1998) High hunting costs make African wild dogs vulnerable to kleptoparasitism by hyaenas. Nature, 391, 479 481.
26. Hamer, K.C., Monaghan, P., Uttley, J.D., Walton, P. Burns, M.D. (1993) The influence of food-supply on the breeding ecology of kittiwakes Rissa tridactyla in Shetland. Ibis, 135, 255 263.
27. Harding, A.M.A., Van Pelt, T.I., Lifjeld, J.T. Mehlum, F. (2004) Sex differences in Little Auk Alle alle parental care: transition from biparental to paternal-only care. Ibis, 146, 642 651.
28. Harding, A.M.A., Egevang, C., Walkusz, W., Merkel, F., Blanc, S. Grémillet, D. (2009a) Estimating prey capture rates of a planktivorous seabird, the little auk (Alle alle), using diet, diving behaviour, and energy consumption. Polar Biology, doi :.
29. Harding, A.M.A., Kitaysky, A.S., Hall, M.E., Welcker, J., Karnovsky, N.J., Talbot, S.L., Hamer, K.C. Grémillet, D. (2009b) Flexibility in the parental effort of an Arctic-breeding seabird. Functional Ecology, 23, 348 358.
30. Harman, D. (1956) Aging: a theory based on free radical and radiation chemistry. Journal of Gerontology, 11, 298 300.
31. Jakubas, D. Wojczulanis, K. (2007) Predicting the sex of Dovekies by discriminant analysis. Waterbirds, 30, 92 96.
32. Jodice, P.G.R., Roby, D.D., Suryan, R.M., Irons, D.B., Turco, K.R., Brown, E.D., Thedinga, J.F. Visser, G.H. (2006) Increased energy expenditure by a seabird in response to higher food abundance. Marine Ecology Progress Series, 306, 283 293.
33. Karnovsky, N.J., Kwasniewski, S., Weslawski, J.M., Walkusz, W. Beszczynska-Moller, A. (2003) Foraging behavior of Little Auks in a heterogeneous environment. Marine Ecology-Progress Series, 253, 289 303.
34. Kitaysky, A.S., Piatt, J.F. Wingfield, J.C. (2007) Stress hormones link food availability and population processes in seabirds. Marine Ecology-Progress Series, 352, 245 258.
35. Kitaysky, A.S., Wingfield, J.C. Piatt, J.F. (1999b) Dynamics of food availability, body condition and physiological stress response in breeding Black-legged Kittiwakes. Functional Ecology, 13, 577 584.
36. Kitaysky, A.S., Piatt, J.F., Wingfield, J.C. Romano, M. (1999a) The adrenocortical stress-response of Black-legged Kittiwake chicks in relation to dietary restrictions. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 169, 303 310.
37. Kitaysky, A.S., Hunt, G.L., Flint, E.N., Rubega, M.A. Decker, M.B. (2000) Resource allocation in breeding seabirds: responses to fluctuations in their food supply. Marine Ecology-Progress Series, 206, 283 296.
38. Kitaysky, A.S., Kitaiskaia, E.V., Wingfield, J.C. Piatt, J.F. (2001) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology, 171, 701 709.
39. Kitaysky, A.S., Kitaiskaia, E., Piatt, J. Wingfield, J.C. (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Hormones and Behavior, 43, 140 149.
40. Kitaysky, A.S., Romano, M.D., Piatt, J.F., Wingfield, J.C. Kikuchi, M. (2005) The adrenocortical response of tufted puffin chicks to nutritional deficits. Hormones and Behavior, 47, 606 619.
41. Lifson, N. McClintock, R. (1966) Theory of use of turnover rates of body water for measuring energy and material balance. Journal of Theoretical Biology, 12, 46 74.
42. Lynn, S.E., Breuner, C.W. Wingfield, J.C. (2003) Short-term fasting affects locomotor activity, corticosterone, and corticosterone binding globulin in a migratory songbird. Hormones and Behavior, 43, 150 157.
43. Mehlum, F. Gabrielsen, G.W. (1993) The diet of high-arctic seabirds in coastal and ice-covered, pelagic areas near the Svalbard archipelago. Polar Research, 12, 1 20.
44. 18O) Method: A Guide to its use. UCLA Publication, University of California, Los Angeles.
45. Nagy, K.A., Girard, I.A. Brown, T.K. (1999) Energetics of free-ranging mammals, reptiles, and birds. Annual Review of Nutrition, 19, 247 277.
46. Pedersen, C.E. Falk, K. (2001) Chick diet of dovekies Alle alle in Northwest Greenland. Polar Biology, 24, 53 58.
47. Pravosudov, V.V., Kitaysky, A.S., Wingfield, J.C. Clayton, N.S. (2001) Long-term unpredictable foraging conditions and physiological stress response in mountain chickadees (Poecile gambeli). General and Comparative Endocrinology, 123, 324 331.
48. R Development Core Team (2008) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL http://www.R-project.org.
49. Romero, L.M. Reed, J.M. (2005) Collecting baseline corticosterone samples in the field: is under 3 min good enough? Comparative Biochemistry and Physiology a-Molecular & Integrative Physiology, 140, 73 79.
50. Schoech, S.J., Bowman, R. Reynolds, S.J. (2004) Food supplementation and possible mechanisms underlying early breeding in the Florida Scrub-Jay (Aphelocoma coerulescens). Hormones and Behavior, 46, 565 573.
51. Scott, C.L., Kwasniewski, S., Falk-Petersen, S. Sargent, J.R. (2000) Lipids and life strategies of Calanus finmarchicus, Calanus glacialis and Calanus hyperboreus in late autumn, Kongsfjorden, Svalbard. Polar Biology, 23, 510 516.
52. Selman, C., Mclaren, J.S., Collins, A.R., Duthie, G.G. Speakman, J.R. (2008) The impact of experimentally elevated energy expenditure on oxidative stress and lifespan in the short-tailed field vole Microtus agrestis. Proceedings of the Royal Society B-Biological Sciences, 275, 1907 1916.
53. Speakman, J.R. (1993) How should we calculate CO2 production in doubly labelled water studies of animals. Functional Ecology, 7, 746 750.
54. Speakman, J.R. (1997) Doubly Labelled Water - Theory and Practice. Chapman & Hall, London.
55. Speakman, J.R. (2000) The cost of living: Field metabolic rates of small mammals. Advances in Ecological Research, 30, 177 297.
56. Speakman, J.R. (2005) Body size, energy metabolism and lifespan. Journal of Experimental Biology, 208, 1717 1730.
57. Speakman, J.R. (2008) The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society B-Biological Sciences, 363, 375 398.
58. Speakman, J.R. Krol, B. (2005) Comparison of different approaches for the calculation of energy expenditure using doubly labeled water in a small mammal. Physiological and Biochemical Zoology, 78, 650 667.
59. Speakman, J.R. Racey, P.A. (1987) The equilibrium concentration of O-18 in body-water: implications for the accuracy of the doubly-labeled water technique and a potential new method of measuring RQ in free-living animals. Journal of Theoretical Biology, 127, 79 95.
60. Speakman, J.R. Racey, P.A. (1988) Consequences of non steady-state CO2 production for accuracy of the doubly labeled water technique: the importance of recapture interval. Comparative Biochemistry and Physiology a-Physiology, 90, 337 340.
61. Speakman, J.R., Nagy, K.A., Masman, D., Mook, W.G., Poppitt, S.D., Strathearn, G.E. Racey, P.A. (1990) Interlaboratory comparison of different analytical techniques for the determination of O-18 abundance. Analytical Chemistry, 62, 703 708.
62. Speakman, J.R., Racey, P.A., Haim, A., Webb, P.I., Ellison, G.T.H. Skinner, J.D. (1994) Interindividual and intraindividual variation in daily energy expenditure of the pouched mouse (Saccostomus campestris). Functional Ecology, 8, 336 342.
63. Speakman, J.R., Ergon, T., Cavanagh, R., Reid, K., Scantlebury, D.M. Lambin, X. (2003) Resting and daily energy expenditures of free-living field voles are positively correlated but reflect extrinsic rather than intrinsic effects. Proceedings of the National Academy of Sciences of the United States of America, 100, 14057 14062.
64. Speakman, J.R., Talbot, D.A., Selman, C., Snart, S., Mclaren, J.S., Redman, P., Krol, E., Jackson, D.M., Johnson, M.S. Brand, M.D. (2004) Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell, 3, 87 95.
65. Steen, H., Vogedes, D., Broms, F., Falk-Petersen, S. Berge, J. (2007) Little Auks (Alle alle) breeding in a High Arctic fjord system: bimodal foraging strategies as a response to poor food quality? Polar Research, 26, 118 125.
66. Stempniewicz, L. (2001) Alle alle Little Auk. The Journal of the Birds of the Western Palearctic. BWP Update, vol. 3, pp. 175 201. Oxford University Press, Oxford.
67. Thomas, D.W., Blondel, J., Perret, P., Lambrechts, M.M. Speakman, J.R. (2001) Energetic and fitness costs of mismatching resource supply and demand in seasonally breeding birds. Science, 291, 2598 2600.
68. Timofeev, S.F. (2006) Euphausiid biomass in the Arctic Ocean. Crustaceana, 79, 157 165.
69. Tinbergen, J.M. Dietz, M.W. (1994) Parental energy expenditure during brood rearing in the great tit (Parus major) in relation to body mass, temperature, food availability and clutch size. Functional Ecology, 8, 563 572.
70. Uttley, J.D., Walton, P., Monaghan, P. Austin, G. (1994) The effects of food abundance on breeding performance and adult time budgets of guillemots Uria aalge. Ibis, 136, 205 213.
71. Van Trigt, R., Kerstel, E.R.T., Neubert, R.E.M., Meijer, H.A.J., Mclean, M. Visser, G.H. (2002) Validation of the DLW method in Japanese quail at different water fluxes using laser and IRMS. Journal of Applied Physiology, 93, 2147 2154.
72. Visser, G.H. Schekkerman, H. (1999) Validation of the doubly labeled water method in growing precocial birds: The importance of assumptions concerning evaporative water loss. Physiological and Biochemical Zoology, 72, 740 749.
73. Weathers, W.W., Hodum, P.J. Blakesley, J.A. (2001) Thermal ecology and ecological energetics of California Spotted Owls. Condor, 103, 678 690.
74. Webster, M.D. Weathers, W.W. (1989) Validation of single-sample doubly labeled water method. American Journal of Physiology, 256, R572 R576.
75. Weimerskirch, H. (1998) How can a pelagic seabird provision its chick when relying on a distant food resource? Cyclic attendance at the colony, foraging decision and body condition in Sooty Shearwaters Journal of Animal Ecology, 67, 99 109.
76. Weimerskirch, H., Ancel, A., Caloin, M., Zahariev, A., Spagiari, J., Kersten, M. Chastel, O. (2003) Foraging efficiency and adjustment of energy expenditure in a pelagic seabird provisioning its chick. Journal of Animal Ecology, 72, 500 508.
77. Welcker, J., Harding, A.M.A., Karnovsky, N.J., Steen, H., Strøm, H. Gabrielsen, G.W. (in press) Flexibility in the bimodal foraging strategy of a high Arctic alcid, the Little Auk Alle alle. Journal of Avian Biology.
78. Werner, I. Auel, H. (2005) Seasonal variability in abundance, respiration and lipid composition of Arctic under-ice amphipods. Marine Ecology-Progress Series, 292, 251 262.
79. Wingfield, J.C., Ramos-Fernandez, G., La Mora, A.N.D. Drummond, H. (1999) The effects of an "El Nino" southern oscillation event on reproduction in male and female blue-footed boobies, Sula nebouxii. General and Comparative Endocrinology, 114, 163 172.
80. Wolf, T.J. Schmid-Hempel, P. (1989) Extra loads and foraging life-span in honeybee workers. Journal of Animal Ecology, 58, 943 954.