Metabolic rate throughout the annual cycle reveals the demands of an Arctic existence in Great Cormorants

Ecology

Volumn 92, Issue 2, 2011, Pages 475-486

  White, Craig R ^a,b   Grémillet, David ^c,d   Green, Jonathan A ^e   Martin, Graham R ^a   Butler, Patrick J ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c CNRS   (France)

^d UNIVERSITY OF CAPE TOWN   (South Africa)

^e UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Arctic; Basal metabolic rate; Catch per unit effort; CPUE; Daily energy expenditure; Day length; Diving depths; Field metabolic rate; Foraging efficiency; Great Cormorant; Greenland; Phalacrocorax carbo; Seasonal variation

Indexed keywords

ABUNDANCE; AIR TEMPERATURE; ANNUAL CYCLE; CATCH PER UNIT EFFORT; DAY LENGTH; ENDOTHERMY; FORAGING BEHAVIOR; FORAGING EFFICIENCY; METABOLISM; PHYSIOLOGY; POLAR REGION; SEABIRD; SEASONAL VARIATION; TEMPORAL VARIATION; WATER TEMPERATURE;

ANIMAL; ARCTIC; ARTICLE; BIRD; ECOSYSTEM; ENERGY METABOLISM; METABOLISM; PHYSIOLOGY; TIME;

ANIMALS; ARCTIC REGIONS; BIRDS; ECOSYSTEM; ENERGY METABOLISM; TIME FACTORS;

ARCTIC;

ANIMALIA; AVES; PHALACROCORACIDAE; PHALACROCORAX CARBO;

EID: 79955546706     PISSN: 00129658     EISSN: None     Source Type: Journal    
DOI: 10.1890/09-1951.1     Document Type: Article

References (77)

1. Allen, C. W. 1973. Astrophysical quantities. Third edition. Athlone Press, Canberra, Australia.
2. Ancel, A., L. N. Starke, P. J. Ponganis, R. van Dam, and G. L. Kooyman. 2000. Energetics of surface swimming in Brant's cormorants (Phalacrocorax penicillatus Brant). Journal of Experimental Biology 203:3727-3731. (Pubitemid 32097356)
3. Andersen, S. M., J. Teilmann, P. B. Harders, E. H. Hansen, and D. Hjøllund. 2007. Diet of harbour seals and great cormorants in Limfjord, Denmark: interspecific competition and interaction with fishery. ICES Journal of Marine Science 64:1235-1245.
4. Anderson, K. J., and W. Jetz. 2005. The broad-scale ecology of energy expenditure of endotherms. Ecology Letters 8:310-318. (Pubitemid 40393916)
5. Barlow, K. E., and J. P. Croxall. 2002. Provisioning behaviour of macaroni penguins Eudyptes chrysolophus. Ibis 144:248-258. (Pubitemid 34805440)
6. Bevan, R. M., I. L. Boyd, P. J. Butler, K. Reid, A. J. Woakes, and J. P. Croxall. 1997. Heart rates and abdominal temperatures of free ranging south georgian shags, Phalacrocorax georgianus. Journal of Experimental Biology 200: 661-675. (Pubitemid 27134176)
7. Brugger, K. E. 1993. Digestibiligy of three fish species by Double-crested Cormorants. Condor 95:25-32.
8. Burnham, K. P., and D. R. Anderson. 2001. Kullback-Leibler information as a basis for strong inference in ecological studies. Wildlife Research 28:111-119. (Pubitemid 32614554)
9. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Second edition. Springer-Verlag, New York, New York, USA.
10. Butler, P. J., J. A. Green, I. L. Boyd, and J. R. Speakman. 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. (Pubitemid 38504280)
11. Carscadden, J. E., W. A. Montevecchi, G. K. Davoren, and B. S. Nakashima. 2002. Trophic relationships among capelin (Mallotus villosus) and seabirds in a changing ecosystem. ICES Journal of Marine Science 59:1027-1033. (Pubitemid 35241000)
12. Chappell, M. A., K. R. Morgan, S. L. Souza, and T. L. Bucher. 1989. Convection and thermoregulation in two Antarctic seabirds. Journal of Comparative Physiology B 159:313-322.
13. Chiaradia, A., Y. Ropert-Coudert, A. Kato, and T. Mattern. and Yorke. 2007. Diving behaviour of little penguins from four colonies across their whole distribution range: bathymetry affecting diving effort and fledging success. Marine Biology 151:1535-1542. (Pubitemid 46682929)
14. Cook, T., Y. Cherel, C.-A. Bost, and Y. Tremblay. 2007. Chickrearing Crozet shags (Phalacrocorax melanogenis) display sex-specific foraging behaviour. Antarctic Science 19:55-63. (Pubitemid 46662192)
15. Cook, T. R., A. Kato, H. Tanaka, Y. Ropert-Coudert, and C.-A. Bost. 2010. Buoyancy under control: underwater locomotor performance in a deep diving seabird suggests respiratory strategies for reducing foraging effort. PLoS ONE 5(3):e9839. [doi: 10.1371/journal.pone.0009839]
16. Croxall, J. P., and G. S. Lishman. 1987. The food and feeding ecology of penguins. Pages 101-131 in J. P. Croxall, editor. Seabirds: feeding ecology and role in marine ecosystems. Cambridge University Press, Cambridge, UK.
17. Drent, R. H., and S. Daan. 1980. The prudent parent: energetic adjustments in avian breeding. Ardea 68:225-252.
18. Dunn, E. H. 1975. Caloric intake of nestling double-crested Cormorants. Auk 92:553-565.
19. Ellis, H. I., and G. W. Gabrielsen. 2002. Energetics of freeranging seabirds. Pages 359-407 in E. A. Schreiber and J. Burger, editors. The biology of marine birds. CRC Press, Boca Raton, Florida, USA.
20. Enstipp, M. R., F. Daunt, S. Wanless, E. M. Humphries, K. C. Hamer, and D. Grémillet. 2006a. Foraging energetics of North Sea birds confronted with fluctuating prey availability. Pages 191-210 in I. Boyd, S. Wanless, and C. J. Camphuysen, editors. Top predators in marine ecosystems: their role in monitoring and management. Cambridge University Press, Cambridge, UK.
21. Enstipp, M. R., D. Grémillet, and D. R. Jones. 2006b. The effects of depth, temperature and food ingestion on the foraging energetics of a diving endotherm, the double-crested cormorant (Phalacrocorax auritus). Journal of Experimental Biology 209:845-859.
22. Enstipp, M. R., D. Grémillet, and D. R. Jones. 2007a. Investigating the functional link between prey abundance and seabird predatory performance. Marine Ecology Progress Series 331:267-279. (Pubitemid 46408736)
23. Enstipp, M. R., D. Grémillet, and S.-H. Lorentsen. 2005. Energetic costs of diving and thermal status in European shags (Phalacrocorax aristotelis). Journal of Experimental Biology 208:3451-3461. (Pubitemid 41463267)
24. Enstipp, M. R., D. R. Jones, S.-H. Lorentsen, and D. Grémillet. 2007b. Energetic costs of diving and prey-capture capabilities in cormorants and shags (Phalacrocoracidae) underline their unique adaptation to the aquatic environment. Journal of Ornithology 148:S593-S600. (Pubitemid 350238512)
25. Friis-Rødel, E., and P. Kanneworff. 2002. A review of capelin (Mallotus villosus) in Greenland waters. ICES Journal of Marine Science 59:860-896.
26. Green, J. A., I. L. Boyd, A. J. Woakes, C. J. Green, and P. J. Butler. 2005. Do seasonal changes in metabolic rate facilitate changes in diving behaviour? Journal of Experimental Biology 208:2581-2593. (Pubitemid 41080429)
27. Green, J. A., I. L. Boyd, A. J. Woakes, N. L. Warren, and P. J. Butler. 2009. Evaluating the prudence of parents: daily energy expenditure throughout the annual cycle of a freeranging bird. Journal of Avian Biology 40:529-538.
28. Green, J. A., J. L. Tanton, A. J. Woakes, I. L. Boyd, and P. J. Butler. 2004. Effects of long-term implanted data loggers on macaroni penguins Eudyptes chrysolophus. Journal of Avian Biology 35:370-376. (Pubitemid 39027102)
29. Grémillet, D. 1997. Catch per unit effort, foraging efficiency, and parental investment in breeding great cormorants (Phalacrocorax carbo carbo). ICES Journal of Marine Science 54:635-644. (Pubitemid 28309959)
30. Grémillet, D., C. Chauvin, R. P. Wilson, Y. Le Maho, and S. Wanless. 2005a. Unusual feather structure allows partial plumage wettability in diving great cormorants. Journal of Avian Biology 36:57-63. (Pubitemid 40199372)
31. Grémillet, D., G. Kuntz, F. Delbart, M. Mellet, A. Kato, J.-P. Robin, P.-E. Chaillon, J.-P. Gendner, S.-H. Lorentsen, and Y. Le Maho. 2004. Linking the foraging performance of a marine predator to local prey abundance. Functional Ecology 18:793-801. (Pubitemid 40033220)
32. Grémillet, D., G. Kuntz, C. Gilbert, A. J. Woakes, P. J. Butler, and Y. Le Maho. 2005b. Cormorants dive through the Polar night. Biology Letters 1:469-471. (Pubitemid 41796597)
33. Grémillet, D., G. Kuntz, A. J. Woakes, C. Gilbert, J.-P. Robin, Y. Le Maho, and P. J. Butler. 2005c. Year-round recordings of behavioural and physiological parameters reveal the survival strategy of a poorly insulated diving endotherm during the Arctic winter. Journal of Experimental Biology 208:4231-4241. (Pubitemid 41789749)
34. Grémillet, D., S. Storch, and G. Peters. 2000. Determining food requirements in marine top predators: a comparison of three independent techniques in Great Cormorants, Phalacrocorax carbo carbo. Canadian Journal of Zoology 78:1567-1579.
35. Grémillet, D., S. Wanless, D. N. Carss, D. Linton, M. P. Harris, J. R. Speakman, and Y. Le Maho. 2001. Foraging energetics of arctic cormorants and the evolution of diving birds. Ecology Letters 4:180-184. (Pubitemid 32516070)
36. Grémillet, D., and R. P. Wilson. 1999. A life in the fast lane: energetics and foraging strategies of the great cormorant. Behavioral Ecology 10:516-524.
37. Grémillet, D., R. P. Wilson, S. Storch, and Y. Gary. 1999. Three-dimensional space utilization by a marine predator. Marine Ecology Progress Series 183:263-273. (Pubitemid 29355182)
38. Grémillet, D., G. Wright, A. Lauder, D. N. Carss, and S. Wanless. 2003. Modelling the daily food requirements of wintering great cormorants: a bioenergetic tool for wildlife management. Journal of Applied Ecology 40:266-277. (Pubitemid 36524546)
39. Guillemette, M., A. J. Woakes, A. Flagstad, and P. J. Butler. 2002. Effects of data-loggers implanted for a full year in female common eiders. Condor 104:448-452. (Pubitemid 34489983)
40. Halsey, L. G., C. R. White, M. R. Enstipp, D. R. Jones, G. R. Martin, and P. J. Butler. 2007. When cormorants go fishing: the differing costs of hunting for sessile and motile prey. Biology Letters 3:574-576.
41. Heide-Jørgensen, M. P., K. L. Laidre, M. L. Logsdon, and T. G. Nielsen. 2007. Springtime coupling between chlorophyll a, sea ice and sea surface temperature in Disko Bay, West Greenland. Progress in Oceanography 73:79-95. (Pubitemid 46436111)
42. Jobling, M., and A. Breiby. 1986. The use and abuse of fish otoliths in studies of feeding habits of marine piscivores. Sarsia 71:265-274.
43. Johansen, R., R. T. Barrett, and T. Pedersen. 2001. Foraging strategies of Great Cormorants Phalacrocorax carbo carbo wintering north of the Arctic Circle. Bird Study 48:59-67. (Pubitemid 32663089)
44. Keller, T. M., and G. H. Visser. 1999. Daily energy expenditure of great cormorants Phalacrocorax carbo sinensis wintering at Lake Chiemsee, southern Germany. Ardea 87:61-69. (Pubitemid 29492462)
45. Kooyman, G. L., Y. Cherel, Y. Le Maho, J. P. Croxall, P. H. Thorson, V. Ridoux, and C. A. Kooyman. 1992. Diving behavior and energetics during foraging cycles in King Penguins. Ecological Monographs 62:143-163.
46. Martin, G. R., C. R. White, and P. J. Butler. 2008. Vision and the foraging technique of great cormorants Phalacrocorax carbo: pursuit or close-quarter foraging? Ibis 150:485-494.
47. McKechnie, A. E., and B. O. Wolf. 2004. The allometry of avian basal metabolic rate: Good predictions need good data. Physiological and Biochemical Zoology 77:502-521. (Pubitemid 39098537)
48. Merkel, F. R., A. Mosbech, D. Boertmann, and L. Grøndhal. 2002. Winter seabird distribution and abundance off southwestern Greenland, 1999. Polar Research 21:17-36. (Pubitemid 34757947)
49. Methven, D. A., R. L. Haedrich, and G. A. Rose. 2001. The fish assemblage of a Newfoundland estuary: diel, monthly and annual variation. Estuarine, Coastal and Shelf Science 52: 669-687. (Pubitemid 32760260)
50. Nagy, K. A., I. A. Girard, and T. K. Brown. 1999. Energetics of free-ranging mammals, reptiles and birds. Annual Review of Nutrition 19:247-277. (Pubitemid 29380604)
51. Nagy, K. A., W. R. Siegfried, and R. P. Wilson. 1984. Energy utilization by free-ranging Jackass Penguins, Spheniscus demersus. Ecology 65:1648-1655. (Pubitemid 16277203)
52. Nickell, L. A., and M. D. J. Sayer. 1998. Occurrence and activity of mobile macrofauna on a sublittoral reef: diel and seasonal variation. Journal of the Marine Biological Association of the United Kingdom 78:1061-1082. (Pubitemid 29038474)
53. Norderhaug, K. N., H. Christie, J. H. Fossa? , and S. Fredriksen. 2005. Fish-macrofauna interactions in a kelp (Laminaria hyperborea) forest. Journal of the Marine Biological Association of the United Kingdom 85:1279-1286. (Pubitemid 41432770)
54. Pelletier, D., M. Guillemette, J.-M. Grandbois, and P. J. Butler. 2008. To fly or not to fly: high flight costs in a large sea duck do not imply an expensive lifestyle. Proceedings of the Royal Society B 275:2117-2124.
55. Phillips, R. A., J. R. D. Silk, and J. P. Croxall. 2005. Foraging and provisioning strategies of the light-mantled sooty albatross at South Georgia: competition and co-existence with sympatric pelagic predators. Marine Ecology Progress Series 285:259-270. (Pubitemid 40263263)
56. Platteeuw, M., and M. R. Van Eerden. 1995. Time and energy constraints of fishing behaviour in breeding cormorants Phalacrocorax carbo sinensis at Lake Ijsselmeer, The Netherlands. Ardea 83:223-234. (Pubitemid 26451393)
57. Rezende, E. L., D. L. Swanson, F. F. Novoa, and F. Bozinovic. 2002. Passerines versus nonpasserines: So far, no statistical differences in the scaling of avian energetics. Journal of Experimental Biology 205:101-107. (Pubitemid 34861263)
58. Ricklefs, R. E., M. Konarzewski, and S. Daan. 1996. The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. American Naturalist 147: 1047-1071.
59. Schmid, D., D. Grémillet, and B. M. Culik. 1995. Energetics of underwater swimming in the great cormorant (Phalacrocorax carbo sinensis). Marine Biology 123:875-881. (Pubitemid 27140842)
60. Schmidt-Nielsen, K. 1997. Animal physiology: adaptation and environment. Cambridge University Press, Cambridge, UK.
61. Shepard, E. L. C., R. P. Wilson, F. Quintana, A. G. Laich, and D. W. Forman. 2009. Pushed for time or saving on fuel: finescale energy budgets shed light on currencies in a diving bird. Proceedings of the Royal Society B 276:3149-3155.
62. Stephenson, R., P. J. Butler, and A. J. Woakes. 1986. Diving behaviour and heart rate in tufted ducks (Aythya fuligula). Journal of Experimental Biology 126:341-359.
63. Swanson, D. L., and E. T. Liknes. 2006. A comparative analysis of thermogenic capacity and cold tolerance in small birds. Journal of Experimental Biology 209:466-474.
64. Swanson, D. L., and K. L. Olmstead. 1999. Evidence for a proximate influence of winter temperature on metabolism in passerine birds. Physiological and Biochemical Zoology 72: 566-575.
65. van Tets, G. F. 1976. Australasia and the origin of shags and cormorants, Phalacrocoracidae. Pages 121-124 in H. J. Frith and J. H. Calaby, editors. Proceedings of the 16th International Ornithological Congress, Canberra, Australia. Australian Academy of Science, Canberra, Australia.
66. Wanless, S., S. K. Finney, M. P. Harris, and D. J. McCafferty. 1999. Effect of the diel light cycle on the diving behaviour of two bottom feeding marine birds: the blue-eyed shag Phalacrocorax atriceps and the European shag P. aristotelis. Marine Ecology Progress Series 188:219-224.
67. Wes?awski, J. M., M. Zajaczkowski, S. Kwaśniewski, J. Jezierski, and W. Moskal. 1988. Seasonality in an Arctic fjord ecosystem: Hornsund, Spitsbergen. Polar Research 6: 185-189. (Pubitemid 19324518)
68. White, C. R., T. M. Blackburn, G. R. Martin, and P. J. Butler. 2007a. Basal metabolic rate of birds is associated with habitat temperature and precipitation, not primary productivity. Proceedings of the Royal Society B 274:287-293. (Pubitemid 47055487)
69. White, C. R., P. J. Butler, D. Grémillet, and G. R. Martin. 2008a. Behavioural strategies of predation in cormorants Phalacrocoracidae foraging under challenging light conditions. Ibis 150(Special Issue 1):231-239.
70. White, C. R., N. Day, P. J. Butler, and G. R. Martin. 2007b. Vision and foraging in cormorants: more like herons than hawks. PLoS ONE 2:e639. [doi: 610.1371/journal.pone. 0000639]
71. White, C. R., G. R. Martin, and P. J. Butler. 2008b. Wingspreading, wing-drying and food-warming in great cormorants Phalacrocorax carbo. Journal of Avian Biology 39:576-578.
72. Wilson, R. P. 2004. Reconstructing the past using futuristic developments: trends and perspectives in logger technology for penguins. Memoirs of National Institute of Polar Research Special Issue 58:34-49.
73. Wilson, R. P., and D. Grémillet. 1996. Body temperatures of free-living African penguins (Spheniscus demersus) and bank cormorants (Phalacrocorax neglectus). Journal of Experimental Biology 199:2215-2223. (Pubitemid 27011447)
74. Wilson, R. P., K. Hustler, P. G. Ryan, A. E. Burger, and E. C. Nöldeke. 1992. Diving birds in cold water: do Archimedes and Boyle determine energetic costs? American Naturalist 140:179-200. (Pubitemid 23395794)
75. Wilson, R. P., A. Steinfurth, Y. Ropert-Coudert, A. Kato, and M. Kurita. 2002. Lip-reading in remote subjects: an attempt to quantify and separate ingestion, breathing and vocalization in free-living animals using penguins as a model. Marine Biology 140:17-27. (Pubitemid 36064150)
76. Wilson, R. P., C. R. White, F. Quintana, L. G. Halsey, N. Liebsch, G. R. Martin, and P. J. Butler. 2006. Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. Journal of Animal Ecology 75:1081-1090. (Pubitemid 44175175)
77. World Clock. 2009. (http://www.timeanddate.com/worldclock/astronomy.html)