Age-related variation in energy expenditure in a long-lived bird within the envelope of an energy ceiling

Journal of Animal Ecology

Volumn 83, Issue 1, 2014, Pages 136-146

  Elliott, Kyle H ^a   Le Vaillant, Maryline ^b,c,d   Kato, Akiko ^b,c   Gaston, Anthony J ^e   Ropert Coudert, Yan ^b,c   Hare, James F ^a   Speakman, John R ^f,g   Croll, Donald ^h  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c CNRS   (France)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e ENVIRONMENT CANADA   (Canada)

^f UNIVERSITY OF ABERDEEN   (United Kingdom)

^g INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

^h UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Device effects; Doubly labelled water; Energy ceiling; Extrinsic limitation; Intrinsic limitation; Repeatability; Thick billed murre; Uria lomvia

Indexed keywords

AGE STRUCTURE; BIRD; ENERGY BUDGET; FITNESS; HANDICAP PRINCIPLE; LIFE HISTORY TRAIT; REPRODUCTIVE COST; TRADE-OFF; WILD POPULATION;

ANIMALIA; AVES; LARIDAE; URIA LOMVIA;

AGING; ANIMAL; ARTICLE; BIOLOGICAL MODEL; CHARADRIIFORMES; DEVICE EFFECTS; DOUBLY LABELLED WATER; ECOSYSTEM; ENERGY CEILING; ENERGY METABOLISM; EXTRINSIC LIMITATION; INTRINSIC LIMITATION; META ANALYSIS; PHYSIOLOGY; REPEATABILITY; THICK-BILLED MURRE; URIA LOMVIA;

DEVICE EFFECTS; DOUBLY LABELLED WATER; ENERGY CEILING; EXTRINSIC LIMITATION; INTRINSIC LIMITATION; REPEATABILITY; THICK-BILLED MURRE; URIA LOMVIA;

AGING; ANIMALS; CHARADRIIFORMES; ECOSYSTEM; ENERGY METABOLISM; MODELS, BIOLOGICAL;

EID: 84890799361     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12126     Document Type: Article

References (88)

1. Angelier, F., Moe, B., Weimerskirch, H. & Chastel, O. (2007) Age-specific reproductive success in a long-lived bird: do older parents resist stress better? Journal of Animal Ecology, 76, 1181-1191.
2. Ballance, L.G., Ainley, D.A., Ballard, G. & Barton, K. (2009) An energetic correlate between colony size and foraging effort in seabirds, with an example of the Adélie penguin, Pygoscelis adeliae. Journal of Avian Biology, 40, 279-288.
3. Beaulieu, M., Reichert, S., Le Maho, Y., Ancel, A. & Criscuolo, F. (2011) Oxidative status and telomere length in a long-lived bird facing a costly reproductive event. Functional Ecology, 25, 577-585.
4. Bech, C., Langseth, I., Moe, B., Fyhn, M. & Gabrielsen, G.W. (2002) The energy economy of the arctic-breeding kittiwake (Rissa tridactyla): a review. Comparative Biochemistry and Physiology A, 133, 765-770.
5. Berteaux, D., Masseboeuf, F., Bonzom, J.-M., Bergeron, J.-M., Thomas, D.W. & Lapierre, H. (1996b) Effect of carrying a radiocollar on expenditure of energy by meadow voles. Journal of Mammalogy, 77, 359-363.
6. Bókony, V., Lendvai, A.Z., Liker, A., Angelier, F., Wingfield, J.C. & Chastel, O. (2009) Stress response and the value of reproduction: are birds prudent parents? American Naturalist, 173, 589-598.
7. Crome, F.H.J. (1975) Notes of the breeding of the purple crowned pigeon. Emu, 75, 172-174.
8. Culik, B.M. & Wilson, R.P. (1991) Field metabolic rates of instrumented Adélie penguins using doubly-labelled water. Journal of Comparative Physiology B, 162, 567-673.
9. Culik, B.M. & Wilson, R.P. (1992) Swimming energetics and performance of instrumented Adélie penguins (Pygoscelis adeliae). Journal of Experimental Biology, 148, 355-368.
10. Daan, S., Deerenberg, C. & Dijkstra, C. (1996) Increased daily work precipitates natural death in the kestrel. Journal of Animal Ecology, 65, 539-544.
11. Drent, R.H. & Daan, S. (1980) The prudent parent-energetic adjustments in avian breeding. Ardea, 68, 225-252.
12. Elliott, K.H., Crump, D. & Gaston, A.J. (2010) Sex-specific behaviour by a monomorphic seabird represents risk partitioning. Behavioral Ecology, 21, 1024-1032.
13. Elliott, K.H., Davoren, G.K. & Gaston, A.J. (2007) The influence of buoyancy and drag on the dive behaviour of an Arctic seabird, the thick-billed murre. Canadian Journal of Zoology, 85, 352-361.
14. Elliott, K.H., Davoren, G.K. & Gaston, A.J. (2008) Sources of bias in observations of murre provisioning behaviour. Journal of Field Ornithology, 79, 298-307.
15. Elliott, K.H., Woo, K.J. & Gaston, A.J. (2010) Specialization in murres: the story of eight specialists. Waterbirds, 32, 491-506.
16. Elliott, K.H., Woo, K.J., Gaston, A.J., Benvenuti, S., Dall'Antonia, L. & Davoren, G.K. (2009) Central-place foraging in an Arctic seabird provides evidence for Storer-Ashmole's halo. Auk, 126, 613-625.
17. Elliott, K.H., McFarlane-Tranquilla, L., Burke, C.M., Hedd, A., Montevecchi, W.A. & Anderson, W.G. (2012) Year-long deployments of small geolocators increase corticosterone levels in murres. Marine Ecology Progress Series, 466, 1-7.
18. Elliott, K.H., Le Vaillant, M., Kato, A., Speakman, J.R. & Ropert-Coudert, Y. (2013a) Accelerometry predicts daily energy expenditure in a bird with high activity levels. Biology Letters, 9, 20120919.
19. Elliott, K.H., Ricklefs, R.E., Gaston, A.J., Hatch, S.A., Speakman, J.R. & Davoren, G.K. (2013b) High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins. Proceedings of the National Academy of Sciences, 110, 9380-9384.
20. Gales, R., Williams, C. & Ritz, D. (1990) Foraging behaviour of the little penguin, Eudyptula minor: initial results and assessment of instrument effect. Journal of Zoology, 220, 61-85.
21. Gaston, A.J. & Elliott, K.H. (2012) Effects of climate-influenced parasitism, predation and predator-predator interactions on reproduction and survival of an Arctic marine bird. Arctic, 66, 43-51.
22. Gaston, A.J. & Hipfner, J.M. (2006) Breeding Brunnich's Guillemots balance maintenance of body condition against investment in chick growth. Ibis, 148, 106-113.
23. Gessaman, J.A. & Nagy, K.A. (1988) Transmitter loads affect the flight speed and metabolism of homing pigeons. Condor, 90, 662-668.
24. Godfrey, J.D., Bryant, D.M. & Williams, M.J. (2003) Radio-telemetry increases free-living energy costs in the endangered takahe Prophyrio mantelli. Biological Conservation, 114, 35-38.
25. Green, J.A., Boyd, I.L., Woakes, A.J., Warren, N.L. & Butler, P.J. (2009) Evaluating the prudence of parents: daily energy expenditure throughout the annual cycle of a free-ranging bird, the macaroni penguin Eudyptes chrysolophus. Journal of Avian Biology, 40, 529-538.
26. Guillemette, M. (1998) The effect of time and digestion constraints in common eiders while feeding and diving over blue mussel beds. Functional Ecology, 12, 123-131.
27. Hammond, K.A. & Diamond, J. (1997) Maximal sustained energy budgets in humans and animals. Nature, 386, 457-462.
28. Hansen, E.S. (2003) Ecophysiological constraints on energy provisioning rate by seabird parents. Diss. University of Missouri, St. Louis, MO.
29. Harding, A.M.A., Kitaysky, A.S., Hall, M.E., Welcker, J., Karnovsky, N.J., Talbot, S.L. et al. (2009) Flexibility in the parental effort of an Arctic-breeding seabird. Functional Ecology, 23, 348-358.
30. Heath, J.P., Gilchrist, H.G. & Ydenberg, R.C. (2010) Interactions between rate processes with different time scales explain counterintuitive foraging patterns of arctic wintering eiders. Proceedings of the Royal Society B, 277, 3179-3186.
31. Hernández, F., Arredondo, J.A., Hernández, F., Hewitt, D.G., DeMaso, S.J. & Bingham, R.L. (2004) Effects of radiotransmitters on body mass, feed consumption, and energy expenditure of northern bobwhites. Wildlife Society Bulletin, 32, 394-400.
32. Houston, A.I., Thompson, W.A. & Gaston, A.J. (1996) An analysis of the "intermediate" nestling growth strategy in the Alcidae: a time and energy budget model of a parent thick-billed murre. Functional Ecology, 10, 432-439.
33. Jackson, D.M., Trayhurn, P. & Speakman, J.R. (2001) Associations between energetics and over-winter survival in the short-tailed field vole Microtus agrestis. Journal of Animal Ecology, 70, 633-640.
34. Jacobs, S.R., Elliott, K.H. & Gaston, A.J. (2013) Parents are a drag: long-lived birds share the cost of increased foraging effort with their offspring, but males pass on more of the costs than females. PLoS ONE, 8, e54594.
35. Jacobs, S.R., Edwards, D., Ringrose, J., Elliott, K.H., Weber, J.-M. & Gaston, A.J. (2011) Changes in body composition during breeding: reproductive strategies of three seabird species under poor environmental conditions. Comparative Biochemistry and Physiology B, 158, 77-82.
36. Jacobs, S.R., Elliott, K.H., Guigueno, M.F., Redman, P., Speakman, J.R., Gaston, A.J. et al. (2012) Non-lethal measures of seabird body condition. Physiological and Biochemical Zoology, 85, 85-95.
37. Jodice, P.G., Roby, D.D., Hatch, S.A., Gill, V.A., Lanctot, R.B. & Visser, G.H. (2002) Does food availability affect energy expenditure rates of nesting seabirds? A supplemental-feeding experiment with black-legged kittiwakes (Rissa tridactyla). Canadian Journal of Zoology, 80, 214-222.
38. Jodice, P.G.R., Roby, D.D., Suryan, R.M., Irons, D.B., Turco, K.R., Brown, E.D. et al. (2006) Increased energy expenditure by a seabird in response to higher food abundance. Marine Ecology Progress Series, 306, 283-293.
39. Kenward, R.E. & Sibly, R.M. (1977) A woodpigeon (Columba palumbus) feeding preference explained by digestive bottleneck. Journal of Applied Ecology, 14, 815-826.
40. 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.
41. Klaassen, M., Becker, P.H. & Wagener, M. (1992) Transmitter loads do not affect the daily energy expenditure of nesting common terns. Journal of Field Ornithology, 63, 181-185.
42. Kleiber, M. (1975) The Fire of Life. Robert E. Krieger Publishing Company, Malabar, FL.
43. Król, E., Murphy, M. & Speakman, J.R. (2007) Limits to sustained energy intake. X. Effects of fur removal on reproductive performance in laboratory mice. Journal of Experimental Biology, 210, 4233-4243.
44. Kvist, A., Lindström, Å., Green, M., Piersma, T. & Visser, G.H. (2001) Carrying large fuel loads during sustained flight is cheaper than expected. Nature, 413, 730-732.
45. Leclaire, S., Bourret, V., Wagner, R.H., Hatch, S.A., Helfenstein, F., Chastel, O. et al. (2011) Behavioral and physiological responses to male handicap in chick-rearing black-legged kittiwakes. Behavioral Ecology, 22, 1156-1165.
46. Lessells, C.M. & Boag, P.T. (1987) Unrepeatable repeatabilities: a common mistake. Auk, 104, 116-121.
47. Manini, T.M., Everhart, J.E., Patel, K.V., Schoeller, D.A., Colbert, L.H., Visser, M. et al. (2006) Daily activity energy expenditure and mortality among older adults. JAMA, 296, 171-179.
48. Mauck, R.A. & Grubb, T.C. (1995) Petrel parents shunt all experimentally increased reproductive costs to their offspring. Animal Behaviour, 49, 999-1008.
49. Methling, C., Tudorache, C., Skov, P.V. & Steffensen, J.F. (2011) Pop up satellite tags impair swimming performance and energetics of the European eel (Anguilla anguilla). PLoS ONE, 6, e20797.
50. Moreno, J., Merino, S., Potti, J., de Leon, A. & Rodriguez, R. (1999) Maternal energy expenditure does not change with flight costs or food availability in the pied flycatcher (Ficedula hypoleuca): costs and benefits for nestlings. Behavioral Ecology and Sociobiology, 46, 244-251.
51. Nagy, K.A., Siegfried, W.R. & Wilson, R.P. (1984) Energy utilization by free-ranging jackass penguins, Spheniscus demersus. Ecology, 65, 1648-1655.
52. Nudds, R.L. & Bryant, D.M. (2002) Consequences of load carrying by birds during short flights are found to be behavioral and not energetic. American Journal of Physiology-Regulatory Physiology, 283, R249-R256.
53. Paredes, R., Jones, I.L. & Boness, D.J. (2005) Reduced parental care, compensatory behaviour and reproductive costs of thick-billed murres equipped with data loggers. Animal Behaviour, 69, 197-208.
54. Pennycuick, C.J., Schaffner, F.C., Fuller, M.R., Obrecht, H.H. & Sternberg, L. (1990) Foraging flights of the white-tailed tropicbird (Phaethon lepturus): radiotracking and doubly-labelled water. Colonial Waterbirds, 30, 96-102.
55. Pennycuick, C.J., Fast, P.L.F., Ballerstädt, N. & Rattenborg, N. (2012) The effect of an external transmitter on the drag coefficient of a bird's body, and hence on migration range, and energy reserves after migration. Journal of Ornithology, 153, 633-644.
56. Peterson, C.C., Nagy, K.A. & Diamond, J. (1990) Sustained metabolic scope. Proceedings of the National Academy of Sciences USA, 87, 2324-2328.
57. Pontzer, H., Raichlen, D.A., Wood, B.M., Mabulla, A.Z.P., Racette, S.B. & Marlowe, F.W. (2012) Hunter-gatherer energetics and human obesity. PLoS ONE, 7, e40503.
58. Ricklefs, R.E., Konarzewski, M. & Daan, S. (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. American Naturalist, 147, 1047-1071.
59. Roby, D.D. & Ricklefs, R.E. (1986) Energy expenditure in adult least auklets and diving petrels during the chick-rearing period. Physiological Zoology, 59, 661-678.
60. Ropert-Coudert, Y., Wilson, R.P., Yoda, K. & Kato, A. (2007) Assessing performance constraints in penguins with externally-attached devices. Marine Ecology Progress Series, 333, 281-289.
61. Ropert-Coudert, Y., Kato, A., Poulin, N. & Grémillet, D. (2009) Leg-attached data-loggers do not modify the diving performances of a foot-propelled seabird. Journal of Zoology, 279, 294-297.
62. Saether, B.E., Andersen, R. & Pedersen, H.C. (1993) Regulation of parental effort in a long-lived seabird: an experimental manipulation of the cost of reproduction in the Antarctic petrel, Thalassoica antarctica. Behavioral Ecology and Sociobiology, 33, 147-150.
63. Sato, K., Watanuki, Y., Takahashi, A., Miller, P.J.O., Tanaka, H., Kawabe, R. et al. (2007) Stroke frequency, but not swimming speed, is related to body size in free-ranging seabirds, pinnipeds and cetaceans. Proceedings of the Royal Society B, 274, 471-477.
64. Schmidt-Wellenburg, C.A., Engel, S. & Visser, G.H. (2008) Energy expenditure during flight in relation to body mass: effects of natural increases in mass and artificial load in rose coloured starlings. Journal of Comparative Physiology B, 178, 767-777.
65. Sealy, S.G. (1973) The adaptive significance of post-hatching developmental patterns and growth rates in the Alcidae. Ornis Scandinavica, 4, 113-121.
66. Sedinger, J.S., White, R.G. & Hauer, W.E. (1990) Effects of carrying radio transmitters on energy expenditure of Pacific black brant. Journal of Wildlife Management, 54, 42-45.
67. Selman, C., Blount, J.D., Nussey, D.H. & Speakman, J.R. (2012) Oxidative damage, ageing, and life-history evolution: where now? Trends in Ecology & Evolution, 27, 570-577.
68. Shaffer, S.A. (2011) A review of seabird energetic using the doubly labelled water method. Comparative Biochemistry and Physiology A, 158, 315-322.
69. Shirai, M., Ito, M., Yoda, K. & Niizuma, Y. (2012) Applicability of the doubly-labelled water method to the rhinoceros auklet, Cerorhinca monocerata. Biology Open, 1, 1141-1145.
70. Speakman, J.R. (1997) Doubly-Labelled Water: Theory and Practice. Chapman & Hall, London.
71. Speakman, J.R. (2000) The cost of living: field metabolic rates of small mammals. Advances in Ecological Research, 30, 177-297.
72. Speakman, J.R. (2008) The physiological costs of reproduction in small mammals. Philosophical Transactions of the Royal Society B, 363, 375-398.
73. Speakman, J.R. & Krol, E. (2005) Validation of the doubly-labelled water method in a small mammal. Physiological and Biochemical Zoology, 78, 650-667.
74. Speakman, J.R. & Król, E. (2010) Maximum heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. Journal of Animal Ecology, 79, 726-746.
75. 2 production for accuracy of the doubly labeled water technique - the importance of recapture interval. Comparative Biochemistry and Physiology A-Physiology, 90, 337-340.
76. Speakman, J.R., Ergon, T., Cavanagh, R., Reid, K., Scantlebury, D.M. & Lambin, X. (2003) Resting and daily energy expenditure of free-living field voles are positively correlated but reflect extrinsic rather than intrinsic effects. Proceedings of the National Academy of Sciences, 100, 14057-14062.
77. Steinhausen, M.F., Andersen, N.G. & Steffensen, J.F. (2006) The effect of external dummy transmitters on oxygen consumption and performance of swimming Atlantic cod. Journal of Fish Biology, 69, 951-956.
78. 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.
79. Tieleman, B.I., Dijkstra, T.H., Klasing, K.C., Visser, G.H. & Williams, J.B. (2008) Effects of experimentally increased costs of activity during reproduction on parental investment and self-maintenance in tropical house wrens. Behavioral Ecology, 19, 949-959.
80. 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.
81. Tinbergen, J.M. & Verhulst, S. (2000) A fixed energetic ceiling to parental effort in the great tit? Journal of Animal Ecology, 69, 323-334.
82. Vandenabeele, S.P., Shepard, E.L., Grogan, A. & Wilson, R.P. (2012) When three per cent may not be three per cent: device-equipped seabirds experience variable flight constraints. Marine Biology, 159, 1-14.
83. Watanuki, Y., Wanless, S., Harris, M., Lovvorn, J.R., Miyazaki, M., Tanaka, H. et al. (2006) Swim speeds and stroke patterns in wing-propelled divers: a comparison among alcids and a penguin. Journal of Experimental Biology, 209, 1217-1230.
84. Welcker, J., Harding, A.M.A., Kitaysky, A.S., Speakman, J.R. & Gabrielsen, G.W. (2009) Daily energy expenditure increases in response to low nutritional stress in an Arctic-breeding seabird with no effect on mortality. Functional Ecology, 23, 1081-1090.
85. Welcker, J., Moe, B., Bech, C., Fyhn, M., Schultner, J., Speakman, J.R. et al. (2010) Evidence for an intrinsic energetic ceiling in free-ranging kittiwakes Rissa tridactyla. Journal of Animal Ecology, 78, 205-213.
86. Wolf, T.J. & Schmid-Hempel, P. (1989) Extra loads and foraging life-span in honeybee workers. Journal of Animal Ecology, 58, 943-954.
87. Woo, K.J., Elliott, K.H., Davidson, M., Gaston, A.J. & Davoren, G.K. (2008) Individual specialization by a generalist marine predator reflects specialization in foraging behaviour. Journal of Animal Ecology, 77, 1082-1091.
88. Ydenberg, R.C. (1989) Growth-mortality trade-offs and the evolution of juvenile life histories in the Alcidae. Ecology, 70, 1494-1506.