Scaling of swim speed in breath-hold divers

Journal of Animal Ecology

Volumn 80, Issue 1, 2011, Pages 57-68

  Watanabe, Yuuki Y ^a   Sato, Katsufumi ^b   Watanuki, Yutaka ^c   Takahashi, Akinori ^a   Mitani, Yoko ^c   Amano, Masao ^d   Aoki, Kagari ^b   Narazaki, Tomoko ^b   Iwata, Takashi ^a   Minamikawa, Shingo ^e   Miyazaki, Nobuyuki ^b  

^a NATIONAL INSTITUTE OF POLAR RESEARCH   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d NAGASAKI UNIVERSITY   (Japan)

^e NATIONAL RESEARCH INSTITUTE OF FAR SEAS FISHERIES   (Japan)

Author keywords

Biomechanics; Cost of transport; Data logger; Phylogenetically independent contrast

Indexed keywords

BIOMECHANICS; BIRD; CAPTIVE POPULATION; ECTOTHERMY; INSTRUMENTATION; MAMMAL; PHYLOGENETICS; REYNOLDS NUMBER; STATISTICAL ANALYSIS; SWIMMING BEHAVIOR; TURBULENT FLOW; TURTLE;

ANIMAL; ARTICLE; BASAL METABOLIC RATE; BIRD; BODY SIZE; DIVING; GENETICS; HUMAN; MAMMAL; PHYLOGENY; PHYSIOLOGY; SWIMMING; THERMOREGULATION; TURTLE;

ANIMALS; BASAL METABOLISM; BIRDS; BODY SIZE; BODY TEMPERATURE REGULATION; DIVING; HUMANS; MAMMALS; PHYLOGENY; SWIMMING; TURTLES;

ANIMALIA; AVES; MAMMALIA; TESTUDINES;

EID: 78650025183     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/j.1365-2656.2010.01760.x     Document Type: Article

References (91)

1. Akamatsu, T., Wang, D., Wang, K., Wei, Z., Zhao, Q. & Naito, Y. (2002) Diving behaviour of freshwater finless porpoises (Neophocaena phocaenoides) in an oxbow of the Yangtze River, China. ICES Journal of Marine Science, 59, 438-443.
2. Akamatsu, T., Wang, D., Wang, K. & Naito, Y. (2005) Biosonar behaviour of free-ranging porpoises. Proceedings of the Royal Society B: Biological Sciences, 272, 797-801.
3. Amano, M. & Yoshioka, M. (2003) Sperm whale diving behavior monitored using a suction-cup-attached TDR tag. Marine Ecology Progress Series, 258, 291-295.
4. Baker, A.J., Pereira, S.L., Haddrath, O.P. & Edge, K.-A. (2006) Multiple gene evidence for expansion of extant penguins out of Antarctica due to global cooling. Proceedings of the Royal Society B: Biological Sciences, 273, 11-17.
5. Bethge, P., Nicol, S., Culik, B.M. & Wilson, R.P. (1997) Diving behaviour and energetics in breeding little penguins (Eudyptula minor). Journal of Zoology, 242, 483-502.
6. Blackwell, S.B., Haverl, C.A., Le Boeuf, B.J. & Costa, D.P. (1999) A method for calibrating swim-speed recorders. Marine Mammal Science, 15, 894-905.
7. Bowen, B.W., Nelson, W.S. & Avise, J.C. (1993) A molecular phylogeny for marine turtles: trait mapping, rate assessment, and conservation relevance. Proceedings of the National Academy of Sciences, 90, 5574-5577.
8. Boyd, I.L. & Croxall, J.P. (1996) Dive durations in pinnipeds and seabirds. Canadian Journal of Zoology, 74, 1696-1705.
9. Boyd, I.L., Reid, K. & Bevan, R.M. (1995) Swimming speed and allocation of time during the dive cycle in Antarctic fur seals. Animal Behaviour, 50, 769-784.
10. Butler, P.J. & Jones, D.R. (1997) Physiology of diving of birds and mammals. Physiological Reviews, 77, 837-899.
11. Costa, D.P., Gales, N.J. & Goebel, M.E. (2001) Aerobic dive limit: how often does it occur in nature? Comparative Biochemistry and Physiology, Part A, 129, 771-783.
12. Crocker, D.E., Gales, N.J. & Costa, D.P. (2001) Swimming speed and foraging strategies of New Zealand sea lions (Phocarctos hookeri). Journal of Zoology, 254, 267-277.
13. Culik, B.M., Wilson, R.P. & Bannasch, R. (1994) Underwater swimming at low energetic cost by pygoscelid penguins. Journal of Experimental Biology, 197, 65-78.
14. Dial, K.P., Greene, E. & Irschick, D.J. (2008) Allometry of behavior. Trends in Ecology & Evolution, 23, 394-401.
15. Felsenstein, J. (1985) Phylogenies and the comparative method. American Naturalist, 125, 1-15.
16. Fish, F.E. (1996) Transitions from drag-based to lift-based propulsion in mammalian swimming. Integrative and Comparative Biology, 36, 628-641.
17. Friesen, V.L., Baker, A.J. & Piatt, J.F. (1996) Phylogenetic relationships within the Alcidae (Charadriiformes: Aves) inferred from total molecular evidence. Molecular Biology and Evolution, 13, 359-367.
18. Gallon, S.L., Sparling, C.E., Georges, J.-Y., Fedak, M.A., Biuw, M. & Thompson, D. (2007) How fast does a seal swim? Variations in swimming behaviour under differing foraging conditions. Journal of Experimental Biology, 210, 3285-3294.
19. Garland Jr, T., Bennett, A.F. & Rezende, E.L. (2005) Phylogenetic approaches in comparative physiology. Journal of Experimental Biology, 208, 3015-3035.
20. Garland Jr, T., Harvey, P.H. & Ives, A.R. (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology, 41, 18-32.
21. Garland Jr, T. & Ives, A.R. (2000) Using the past to predict the present: confidence intervals for regression equations in phylogenetic comparative methods. American Naturalist, 155, 346-364.
22. Garland Jr, T., Dickerman, A.W., Janis, C.M. & Jones, J.A. (1993) Phylogenetic analysis of covariance by computer simulation. Systematic Biology, 42, 265-292.
23. Goldbogen, J.A., Calambokidis, J., Shadwick, R.E., Oleson, E.M., McDonald, M.A. & Hildebrand, J.A. (2006) Kinematics of foraging dives and lunge-feeding in fin whales. Journal of Experimental Biology, 209, 1231-1244.
24. Goldbogen, J.A., Calambokidis, J., Croll, D.A., Harvey, J.T., Newton, K.M., Oleson, E.M., Schorr, G. & Shadwick, R.E. (2008) Foraging behavior of humpback whales: kinematic and respiratory patterns suggest a high cost for a lunge. Journal of Experimental Biology, 211, 3712-3719.
25. Grafen, A. (1989) The phylogenetic regression. Philosophical Transactions of the Royal Society of London B, 326, 119-157.
26. Grémillet, D., Kuntz, G., Woakes, A.J., Gilbert, C., Robin, J.-P., Le Maho, Y. & Butler, P.J. (2005) 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.
27. Halsey, L.G., Butler, P.J. & Blackburn, T.M. (2006) A phylogenetic analysis of the allometry of diving. American Naturalist, 167, 276-287.
28. Handrich, Y., Bevan, R.M., Charrassin, J.-B., Butler, P.J., Pütz, K., Woakes, A.J., Lage, J. & Le Maho, Y. (1997) Hypothermia in foraging king penguins. Nature, 388, 64-67.
29. Hansen, E.A. & Ricklefs, R.E. (2004) Foraging by deep-diving birds is not constrained by an aerobic diving limit: a model of avian depth dependent diving metabolic rate. American Naturalist, 163, 358-374.
30. Hedenstrom, A. & Alerstam, T. (1995) Optimal flight speed of birds. Philosophical Transactions of the Royal Society of London B, 348, 471-487.
31. Hind, A. & Gurney, W.S.C. (1997) The metabolic cost of swimming in marine homeotherms. Journal of Experimental Biology, 200, 531-542.
32. Hindell, M.A., Lea, M.-A., Morrice, M.G. & MacMahon, C.R. (2000) Metabolic limits on dive duration and swimming speed in the southern elephant seal Mirounga leonina. Physiological and Biochemical Zoology, 73, 790-798.
33. Hoerner, S.F. (1965) Fluid Dynamic Drag: Practical Information on Aerodynamic Drag and Hydrodynamic Resistance. Hoerner Fluid Dynamics, New Jersey.
34. Hooker, S.K., Miller, P.J.O., Johnson, M.P., Cox, O.P. & Boyd, I.L. (2005) Ascent exhalations of Antarctic fur seals: a behavioural adaptation for breath-hold diving? Proceedings of the Royal Society B: Biological Sciences, 272, 355-363.
35. Del Hoyo, J., Elliott, A. & Sargatal, J. (1992) Handbook of the Birds of the World. Vol. 1 Lynx Edicions, Barcelona.
36. Del Hoyo, J., Elliott, A. & Sargatal, J. (1996) Handbook of the Birds of the World. Vol. 3. Lynx Edicions, Barcelona.
37. Kooyman, G.L. (1989) Diverse Divers: Physiology and Behavior. Springer-Verlag, Berlin.
38. Kooyman, G.L. & Ponganis, P.J. (1998) The physiological basis of diving to depth: birds and mammals. Annual Review of Physiology, 60, 19-32.
39. Krafft, B.A., Lydersen, C., Kovacs, K.M., Gjertz, I. & Haug, T. (2000) Diving behaviour of lactating bearded seals (Erignathus barbatus) in the Svalbard area. Canadian Journal of Zoology, 78, 1408-1418.
40. De Leeuw, J.J., Butler, P.J., Woakes, A.J. & Zegwaard, F. (1998) Body cooling and its energetic implications for feeding and diving of tufted ducks. Physiological and Biochemical Zoology, 71, 720-730.
41. Lesage, V., Hammill, M.O. & Kovacs, K.M. (1999) Functional classification of harbor seal (Phoca vitulina) dives using depth profiles, swimming velocity, and an index of foraging success. Canadian Journal of Zoology, 77, 74-87.
42. Lockyer, C. (1976) Body weights of some species of large whales. ICES Journal of Marine Science, 36, 259-273.
43. Luna-Jorquera, G. & Culik, B.M. (1999) Diving behaviour of Humboldt penguins Spheniscus humboldti in northern Chile. Marine Ornithology, 27, 67-76.
44. Maddison, W.P. & Maddison, D.R. (2009) Mesquite: a modular system for evolutionary analysis. Version 2.7.
45. Midford, P.E., Garland Jr, T. & Maddison, W.P.(2003) PDAP Package.
46. Miller, P.J.O., Johnson, M.P., Tyack, P.L. & Terray, E.A. (2004) Swimming gaits, passive drag and buoyancy of diving sperm whales Physeter macrocephalus. Journal of Experimental Biology, 207, 1953-1967.
47. Minamikawa, S. (2003) How is the optimal diving speed of animals settled? Science Journal KAGAKU, 73, 54-55. (in Japanese).
48. Narazaki, T., Sato, K., Abernathy, K.J., Marshall, G.J. & Miyazaki, N. (2009) Sea turtles compensate deflection of heading at the sea surface during directional travel. Journal of Experimental Biology, 212, 4019-4026.
49. Nikaido, M., Hamilton, H., Makino, H., Sasaki, T., Takahashi, K., Goto, M., Kanda, N., Pastene, L.A. & Okada, N. (2006) Baleen whale phylogeny and a past extensive radiation event revealed by SINE insertion analysis. Molecular Biology and Evolution, 23, 866-873.
50. Otani, S., Naito, Y., Kato, A. & Kawamura, A. (2000) Diving behavior and swimming speed of a free-ranging harbor porpoise, Phocoena phocoena. Marine Mammal Science, 16, 811-814.
51. Packard, G.C. & Boardman, T.J. (1999) The use of percentages and size-specific indices to normalize physiological data for variation in body size: wasted time, wasted effort? Comparative Biochemistry and Physiology A - Molecular and Integrative Physiology, 122, 37-44.
52. Pagel, M.D. (1992) A method for the analysis of comparative data. Journal of Theoretical Biology, 156, 431-442.
53. Pennycuick, C. J. (2008) Modelling the Flying Bird. Academic Press, London.
54. Ponganis, P.J., Ponganis, E.P., Ponganis, K.V., Kooyman, G.L., Gentry, R.L. & Trillmich, F. (1990) Swimming velocity in otariids. Canadian Journal of Zoology, 68, 2105-2112.
55. Ponganis, P.J., Gentry, R.L., Ponganis, E.P. & Ponganis, K.V. (1992) Analysis of swim velocities during deep and shallow dives of two northern fur seals, Callorhinus ursinus. Marine Mammal Science, 8, 69-75.
56. Radl, A. & Culik, B.M. (1999) Foraging behaviour and reproductive success in Magellanic penguins (Spheniscus magellanicus): a comparative study of two colonies in southern Chile. Marine Biology, 133, 381-393.
57. Ribak, G., Weihs, D. & Arad, Z. (2004) How do cormorants counter buoyancy during submerged swimming? Journal of Experimental Biology, 207, 2101-2114.
58. Ribak, G., Weihs, D. & Arad, Z. (2005) Submerged swimming of the great cormorant Phalacrocorax carbo sinensis is a variant of the burst-and-glide gait. Journal of Experimental Biology, 208, 3835-3849.
59. Ropert-Coudert, Y., Grémillet, D. & Kato, A. (2006) Swim speeds of free-ranging great cormorants. Marine Biology, 149, 415-422.
60. Rosen, D.A.S. & Trites, A.W. (2002) Cost of transport in Steller sea lions, Eumetopias jubatus. Marine Mammal Science, 18, 513-524.
61. Sato, K., Naito, Y., Kato, A., Niizuma, Y., Watanuki, Y., Charrassin, J.B., Bost, C.-A., Handrich, Y. & Le Maho, Y. (2002) Buoyancy and maximal diving depth in penguins do they control inhaling air volume? Journal of Experimental Biology, 205, 1189-1197.
62. Sato, K., Mitani, Y., Cameron, M.F., Siniff, D.B. & Naito, Y. (2003) Factors affecting stroking patterns and body angle in diving Weddell seals under natural conditions. Journal of Experimental Biology, 206, 1461-1470.
63. Sato, K., Charrassin, J.B., Bost, C.-A. & Naito, Y. (2004) Why do macaroni penguins choose shallow body angles that result in longer descent and ascent durations? Journal of Experimental Biology, 207, 4057-4065.
64. Sato, K., Watanuki, Y., Takahashi, A., Miller, P.J.O., Tanaka, H., Kawabe, R., Ponganis, P.J., Handrich, Y., Akamatsu, T., Watanabe, Y., Mitani, Y., Costa, D.P., Bost, C.-A., Aoki, K., Amano, M., Trathan, P., Shapiro, A. & Naito, Y. (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: Biological Sciences, 274, 471-477.
65. Sato, K., Shiomi, K., Watanabe, Y., Watanuki, Y., Takahashi, A. & Ponganis, P.J. (2010) Scaling of swim speed and stroke frequency in geometrically similar penguins: they swim optimally to minimize cost of transport. Proceedings of the Royal Society B: Biological Sciences, 277, 707-714.
66. Savage, V.M., Gillooly, J.F., Woodruff, W.H., West, G.B., Allen, A.P., Enquist, B.J. & Brown, J.H. (2004) The predominance of quarter-power scaling in biology. Functional Ecology, 18, 257-282.
67. Schmidt-Nielsen, K. (1972) Locomotion: energy cost of swimming, flying, and running. Science, 177, 222-228.
68. Schmidt-Nielsen, K. (1984) Scaling: Why is Animal Size so Important?. Cambridge University Press, Cambridge.
69. Schreer, J.F. & Kovacs, K.M. (1997) Allometry of diving capacity in air-breathing vertebrates. Canadian Journal of Zoology, 75, 339-358.
70. Siegel-Causey, D. (1988) Phylogeny of the Phalacrocoracidae. Condor, 90, 885-905.
71. Thompson, D., Hiby, A.R. & Fedak, M.A. (1993) How fast should I swim? Behavioural implications of diving physiology. Symposia of the Zoological Society of London, 66, 349-368.
72. Trites, A.W. & Pauly, D. (1998) Estimating mean body masses of marine mammals from maximum body lengths. Canian Jounal of Zoology, 76, 886-896.
73. Videler, J.J. & Nolet, B.A. (1990) Costs of swimming measured at optimum speed: scale effects, differences between swimming styles, taxonomic groups and submerged and surface swimming. Comparative Biochemistry and Physiology, Part A, 97, 91-99.
74. Vogel, S. (1994) Life in Moving Fluids: the Physical Biology of Flow, 2nd edn. Princeton University Press, Princeton.
75. Watanabe, Y., Mitani, Y., Sato, K., Cameron, M.F. & Naito, Y. (2003) Dive depths of Weddell seals in relation to vertical prey distribution as estimated by image data. Marine Ecology Progress Series, 252, 283-288.
76. Watanabe, Y., Baranov, E.A., Sato, K., Naito, Y. & Miyazaki, N. (2004) Foraging tactics of Baikal seals differ between day and night. Marine Ecology Progress Series, 279, 283-289.
77. Watanabe, Y., Baranov, E.A., Sato, K., Naito, Y. & Miyazaki, N. (2006) Body density affects stroke patterns in Baikal seals. Journal of Experimental Biology, 209, 3269-3280.
78. Watanuki, Y. & Burger, A.E. (1999) Body mass and dive duration in alcids and penguins. Canadian Journal of Zoology, 77, 1838-1842.
79. Watanuki, Y., Niizuma, Y., Gabrielsen, G.W., Sato, K. & Naito, Y. (2003) Stroke and glide of wing-propelled divers: deep diving seabirds adjust surge frequency to buoyancy change with depth. Proceedings of the Royal Society B: Biological Sciences, 270, 483-488.
80. Watanuki, Y., Takahashi, A., Daunt, F., Wanless, S., Harris, M., Sato, K. & Naito, Y. (2005) Regulation of stroke and glide in a foot-propelled avian diver. Journal of Experimental Biology, 208, 2207-2216.
81. Watanuki, Y., Wanless, S., Harris, M., Lovvorn, J.R., Miyazaki, M., Tanaka, H. & Sato, K. (2006) Swim speeds and stroke patterns in wing-propelled divers: a comparison among alcids and a penguin. Journal of Experimental Biology, 209, 1217-1230.
82. Webb, P.W., Kostecki, P.T. & Stevens, E.D. (1984) The effect of size and swimming speed on locomotory kinematics of rainbow trout. Journal of Experimental Biology, 109, 77-95.
83. Williams, T.D. (1995) The Penguins Spheniscidae. Oxford University Press, Oxford.
84. Williams, T.M. (1999) The evolution of cost efficient swimming in marine mammals: limits to energetic optimization. Philosophical Transactions of the Royal Society of London B, 354, 193-201.
85. Williams, T.M. & Kooyman, G.L. (1985) Swimming performance and hydrodynamic characterastics of harbor seals Phoca vitulina. Physiological Zoology, 58, 576-589.
86. Williams, T.M., Davis, R.W., Fuiman, L.A., Francis, J., Le Boeuf, B.J., Horning, M., Calambokidis, J. & Croll, D.A. (2000) Sink or swim: strategies for cost-efficient diving by marine mammals. Science, 288, 133-136.
87. Wilson, R.P., Ropert-Coudert, Y. & Kato, A. (2002) Rush and grab strategies in foraging marine endotherms: the case for haste in penguins. Animal Behaviour, 63, 85-95.
88. Wilson, R.P., Hustler, K., Ryan, P.G., Burger, A.E. & Noldeke, E.C. (1992) Diving birds in cold water: do Archimedes and Boyle determine energetic costs? American Naturalist, 140, 179-200.
89. Wynen, L.P., Goldsworthy, S.D., Insley, S.J., Adams, M., Bickham, J.W., Francis, J., Gallo, J.P., Hoelzel, A.R., Majluf, P., White, R.W.G. & Slade, R. (2001) Phylogenetic relationships within the eared seals (Otariidae: Carnivora): implications for the historical biogeography of the family. Molecular Phylogenetics and Evolution, 21, 270-284.
90. Zamparo, P., Pendergast, D.R., Termin, B. & Minetti, A.E. (2002) How fins affect the economy and efficiency of human swimming. Journal of Experimental Biology, 205, 2665-2676.
91. Zar, J.H. (1999). Biostatistical Analysis, 4th edn. Prentice Hall, Upper Saddle River, NJ.