Advertisement

Locomotion

  • Randall W. Davis
Chapter

Abstract

The convergent evolution of a fusiform body shape in aquatic vertebrates decreases drag resulting from the greater density and viscosity of water compared to air. There are two types of drag: pressure drag and friction drag. Pressure drag is greatly reduced by a streamlined or fusiform body shape. Total drag increases with body mass for marine mammals primarily due to friction drag. Active drag of a free-swimming animal is generally assumed to be ~threefold greater than passive drag. The most derived and efficient modes of aquatic locomotion include pelvic oscillation (seals and walruses), pectoral oscillation (sea lions and fur seals), and caudal oscillation (Cetacea and Sirenia). The power generated by the contracting muscles is translated into the power associated with locomotion (thrust × velocity). The energetic cost of swimming in these species is probably 1.6- to 2.6-fold greater than resting metabolism at routine swim speeds. The average minimum cost of transport (COT) for five marine mammal species is similar to the predicted mean minimum COT of quadrupedal running mammals with the same body masses. Despite differences in size, feeding ecology, and diving behavior, the routine swim speeds of most marine mammals fall in the range of 1–3 m s−1.

Keywords

Locomotion Drag Thrust Energetics Cost of transport Speed Buoyancy 

References

  1. Adachi T, Maresh JL, Robinson PW, Peterson SH, Costa DP, Naito Y, Watanabe YY, Takahashi A (2014) The foraging benefits of being fat in a highly migratory marine mammal. Proc R Soc B 281:2014–2120CrossRefGoogle Scholar
  2. Ahlborn BK, Blake RW, Chan KHS (2009) Optimal fineness ratio for minimum drag in large whales. Can J Zool 87:124–131CrossRefGoogle Scholar
  3. Aoki K, Watanabe YY, Crocker DE, Robinson PW, Biuw M, Costa DP, Miyazaki N, Fedak MA, Miller PJO (2011) Northern elephant seals adjust gliding and stroking patterns with changes in buoyancy: validation of at-sea metrics of body density. J Exp Biol 214:2973–2987PubMedCrossRefPubMedCentralGoogle Scholar
  4. Au D, Weihs D (1980) At high speeds dolphins save energy by leaping. Nature 284:548–550CrossRefGoogle Scholar
  5. Beck CA, Bowen WD, Iverson SJ (2000) Seasonal changes in buoyancy and diving behaviour of adult grey seals. J Exp Biol 203:2323–2330.PubMedPubMedCentralGoogle Scholar
  6. Bodkin JL, Esslinger GG, Monson DH (2004) Foraging depths of sea otters and implications to coastal marine communities. Mar Mamm Sci 20:305–321CrossRefGoogle Scholar
  7. Boyd IL, Reid K, Bevan RM (1995) Swimming speed and allocation of time during the dive cycle in Antarctic fur seals. Anim Behav 50:769–784CrossRefGoogle Scholar
  8. Castellini MA, Kooyman GL, Ponganis PJ (1992) Metabolic rates of freely diving Weddell seals: correlations with oxygen stores, swim velocity and diving duration. J Exp Biol 165:181–194PubMedGoogle Scholar
  9. Cortez M, Wolt R, Davis RW (2016) Development of an altricial mammal at sea I: activity budgets of female sea otters and their pups in Simpson Bay, Alaska. J Exp Mar Biol Ecol 481:71–80CrossRefGoogle Scholar
  10. Costa DP, Kooyman GL (1982) Oxygen consumption, thermoregulation, and the effect of fur oiling and washing on the sea otter, Enhydra lutris. Can J Zool 60:2761–2767CrossRefGoogle Scholar
  11. Costa DP, Le Boeuf BJ, Huntley AC, Ortiz CL (1986) The energetics of lactation in the northern elephant seal, Mirounga angustirostris. J Zool Lond 209:21–33CrossRefGoogle Scholar
  12. Crocker DE (1995) Reproductive effort and fasting physiology of female northern elephant seals. Ph.D. Thesis, University of California, Santa CruzGoogle Scholar
  13. Crocker DE, Le Boeuf BJ, Costa DP (1997) Drift diving in female northern elephant seals: implications for food processing. Can J Zool 75:27–39CrossRefGoogle Scholar
  14. Dassis M, Rodríguez D, Leno EN, Davis RW (2012) Submerged swimming and resting metabolic rates in southern sea lions. J Exp Mar Biol Ecol 432(433):106–112CrossRefGoogle Scholar
  15. Davis RW, Weihs D (2007) Locomotion in deep diving elephant seals: physical and physiological constraints. Philos Trans R Soc Lond B Biol Sci 362:2141–2150PubMedPubMedCentralCrossRefGoogle Scholar
  16. Davis RW, Castellini MA, Kooyman GL, Maue R (1983) Renal glomerular filtration rate and hepatic blood flow during voluntary dives in Weddell seals. Am J Phys 245:R743–R748Google Scholar
  17. Davis RW, Williams TM, Kooyman GL (1985) Swimming metabolism of yearling and adult harbor seals Phoca vitulina. Physiol Zool 58:590–596CrossRefGoogle Scholar
  18. Davis RW, Fuiman L, Williams TM, Le Boeuf BJ (2001) Three-dimensional movements and swimming activity of a female northern elephant seal. Comp Biochem Physiol A Mol Integr Physiol 129:759–770PubMedCrossRefPubMedCentralGoogle Scholar
  19. Davis RW, Madden K, Fuiman LA, Williams TM (2013) Classification and behavior of free-ranging Weddell seal dives based on three-dimensional movements and video-recorded observations. Deep-Sea Res II 88:65–77CrossRefGoogle Scholar
  20. Domning DP, de Buffrenil V (1991) Hydrostasis in the Sirenia: quantitative data and functional interpretations. Mar Mamm Sci 7:331–368CrossRefGoogle Scholar
  21. Feldkamp SD (1987a) Swimming in the California sea lion: morphometrics, drag and energetics. J Exp Biol 131:117–135PubMedPubMedCentralGoogle Scholar
  22. Feldkamp SD (1987b) Fore flipper propulsion in the California sea lion, Zalophus californianus. J Zool (Lond) 212:43–57CrossRefGoogle Scholar
  23. Fish FE (1996) Transitions from drag-based to lift-based propulsion in mammalian swimming. Am Zool 36:628–641CrossRefGoogle Scholar
  24. Fish FE (1998) Comparative kinematics and hydrodynamics of odontocete cetaceans: morphological and ecological correlates with swimming performance. J Exp Biol 201:2867–2877PubMedPubMedCentralGoogle Scholar
  25. Fish FE (2000) Biomechanics and energetics in aquatic and semiaquatic mammals: Platypus to whale. Physiol Biochem Zool 73:683–698PubMedCrossRefPubMedCentralGoogle Scholar
  26. Fish FE (2002) Balancing requirements for stability and maneuverability in cetaceans. Integr Comp Biol 42:85–93PubMedCrossRefPubMedCentralGoogle Scholar
  27. Fish FE, Innes S, Ronald K (1988) Kinematics and estimated thrust production of swimming harp and ringed seals. J Exp Biol 137:157–173PubMedPubMedCentralGoogle Scholar
  28. Fish FE, Howie LE, Murray MM (2008) Hydrodynamic flow control in marine mammals. Integr Comp Biol 211:1859–1867Google Scholar
  29. Fish FE, Legac P, Williams TM, Wei T (2014) Measurement of hydrodynamic force generation by swimming dolphins using bubble DPIV. J Exp Biol 217:252–260PubMedCrossRefPubMedCentralGoogle Scholar
  30. Garrett JK, Fish FE (2015) Kinematics of terrestrial locomotion in harbor seals and grey seals: importance of spinal flexion by amphibious phocids. Mar Mamm Sci 31:459–478CrossRefGoogle Scholar
  31. Hertel H (1966) Structure form and movement. Reinhold, New YorkGoogle Scholar
  32. Hindell MA, Slip DJ, Burton HR (1991) The diving behaviour of adult male and female southern elephant seals, Miroungu leonina (Pinnipedia: Phocidae). Aust J Zool 39:595–619CrossRefGoogle Scholar
  33. Hoyt DF, Taylor CR (1981) Gait and the energetics of locomotion in horses. Nat Lond 292:239–240CrossRefGoogle Scholar
  34. Kenyon KW (1969) The sea otter in the eastern Pacific ocean. North Am Fauna 68:1–352CrossRefGoogle Scholar
  35. Kojeszewski T, Fish FE (2007) Swimming kinematics of the Florida manatee (Trichechus manatus latirostris): hydrodynamic analysis of an undulatory mammalian swimmer. J Exp Biol 210:2411–2418PubMedCrossRefPubMedCentralGoogle Scholar
  36. Kooyman GL (1973) Respiratory adaptions in marine mammals. Integr Comp Biol 13:457–468Google Scholar
  37. Kooyman GL, Kerem DH, Campbell WB, Wright JJ (1973) Pulmonary gas exchange in freely diving Weddell seals, Leptonychotes weddelli. Respir Physiol 17:283–290PubMedCrossRefPubMedCentralGoogle Scholar
  38. Le Boeuf BJ, Costa DP, Huntley AC, Feldkamp SD (1988) Continuous, deep diving in female northern elephant seals, Mirounga angustirostris. Can J Zool 66:446–458CrossRefGoogle Scholar
  39. Le Boeuf BJ, Naito Y, Asaga T, Crocker D, Costa DP (1992) Swim speed in a female northern elephant seal: metabolic and foraging implications. Can J Zool 70:786–795CrossRefGoogle Scholar
  40. Liwanag HE, Berta A, Costa DP, Abney M, Williams TM (2012) Morphological and thermal properties of mammalian insulation: the evolution of fur for aquatic living. Biol J Linn Soc 106:926–939CrossRefGoogle Scholar
  41. Madden KM, Fuiman LA, Williams TM, Davis RW (2008) Identification of foraging dives in free-ranging Weddell seals Leptonychotes weddellii: confirmation using video records. Mar Ecol Prog Ser 365:263–275CrossRefGoogle Scholar
  42. McGovern KA, Rodríguez DH, Lewis MN, Davis RW (2019) Classification and behavior of free-ranging southern elephant seal dives based on three-dimensional movements and video-recorded observations. Mar Ecol Prog Ser 620:215–232CrossRefGoogle Scholar
  43. McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol A Mol Integr Physiol 151:5–28PubMedCrossRefPubMedCentralGoogle Scholar
  44. Miller PJO, Johnson MP, Tyack PL, Terray EA (2004) Swimming gaits, passive drag and buoyancy of diving sperm whales Physeter macrocephalus. J Exp Biol 207:1953–1967PubMedCrossRefPubMedCentralGoogle Scholar
  45. Miller PJO, Biuw M, Watanabe YY, Thompson D, Fedak MA (2012) Sink fast and swim harder! Round-trip cost-of-transport for buoyant divers. J Exp Biol 215:3622–3630PubMedCrossRefPubMedCentralGoogle Scholar
  46. Mitani Y, Andrews RD, Sato K, Kato A, Naito Y, Costa DP (2010) Three-dimensional resting behaviour of northern elephant seals: drifting like a falling leaf. Biol Lett 6:163–166PubMedCrossRefPubMedCentralGoogle Scholar
  47. Nowacek DP, Johnson MP, Tyack PL, Shorter KA, McLellan W, Pabst DA (2001) Buoyant balaenids: the ups and downs of buoyancy in right whales. Proc R Soc Lond B 268:1811–1816CrossRefGoogle Scholar
  48. Otani S, Naito Y, Kato A, Kawamura A (2000) Diving behavior and swimming speed of a free-ranging harbor porpoise, Phocoena phocoena. Mar Mamm Sci 16:811–814CrossRefGoogle Scholar
  49. Otani S, Naito Y, Kato A, Kawamura A (2001) Oxygen consumption and swim speed of the harbor porpoise Phocoena phocoena. Fisheries Sci 67:894–898CrossRefGoogle Scholar
  50. Pennycuick CJ (1975) On the running of the gnu (Connochaetes taurinus) and other animals. J Exp Biol 63:775–799Google Scholar
  51. Ponganis PJ, Ponganis EP, Ponganis KV, Kooyman GL (1990a) Swimming velocities in otariids. Can J Zool 68:2105–2112CrossRefGoogle Scholar
  52. Ponganis PJ, Kooyman GL, Zornow MH, Castellini MA, Croll DA (1990b) Cardiac output and stroke volume in swimming harbor seals. J Comp Physiol B 160:473–482PubMedCrossRefGoogle Scholar
  53. Ponganis PJ, Kooyman GL, Zornow MH (1991) Cardiac output in swimming California sea lions, Zalophus californianus. Physiol Zool 64:1296–1306CrossRefGoogle Scholar
  54. Richard G, Vacquié-Garcia J, Jouma’a J, Picard B, Génin A, Arnould JPY, Bailleul F, Guinet C (2014) Variation in body condition during the post-moult foraging trip of southern elephant seals and its consequences on diving behaviour. J Exp Biol 217:2609–2619PubMedCrossRefGoogle Scholar
  55. Rohr J, Latz MI, Fallon S, Nauen JC, Hendricks E (1998) Experimental approaches towards interpreting dolphin stimulated bioluminescence. J Exp Biol 201:1447–1460PubMedPubMedCentralGoogle Scholar
  56. Rohr JJ, Fish FE, Gilpatrick JW (2002) Maximum swim speeds of captive and free ranging delphinids. Mar Mamm Sci 18:1–19CrossRefGoogle Scholar
  57. Sato K, Mitani Y, Cameron MF, Siniff DB, Naito Y (2003) Factors affecting stroking patterns and body angle in diving Weddell seals under natural conditions. J Exp Biol 20:1461–1470CrossRefGoogle Scholar
  58. Schmidt-Nielsen K (1997) Animal physiology. Cambridge University Press, Cambridge, p 617Google Scholar
  59. Skrovan RC, Williams TM, Berry PS, Moore PW, Davis RW (1999) The diving physiology of bottlenose dolphins (Tursiops truncatus). II. Biomechanics and changes in buoyancy at depth. J Exp Biol 202:2749–2761PubMedPubMedCentralGoogle Scholar
  60. Stahl WR (1967) Scaling of respiratory variables in mammals. J Appl Physiol 22:453–460.PubMedCrossRefPubMedCentralGoogle Scholar
  61. Tarasoff FJ, Kooyman GL (1973) Observations on the anatomy of the respiratory system of the river otter, sea otter and harp seal. I. The topography, weight and measurements of the lungs. Can J Zool 51:163–170PubMedCrossRefPubMedCentralGoogle Scholar
  62. Taylor CR, Schmidt-Nielsen K, Raab JL (1970) Scaling of energetic cost of running to body size in mammals. Am J Physiol 219:1104–1107PubMedCrossRefPubMedCentralGoogle Scholar
  63. Taylor CR, Karas RH, Weibel ER, Hoppler H (1987) Adaptive variation in the mammalian respiratory system in relation to energetic demand. II. Reaching the limits to oxygen flow. Respir Physiol 69:7–26CrossRefGoogle Scholar
  64. Tinker MT, Costa DP, Estes JA, Wieringa N (2007) Individual dietary specialization and dive behaviour in the California sea otter: using archival time-depth data to detect alternative foraging strategies. Deep-Sea Res II 54:330–342CrossRefGoogle Scholar
  65. van der Hoop JM, Fahlman A, Hurst T, Rocho-Levine J, Shorter AK, Petrov V, Moore MJ (2014) Bottlenose dolphins modify behavior to reduce metabolic effect of tag attachment. J Exp Biol 217:4229–4236PubMedCrossRefPubMedCentralGoogle Scholar
  66. Vogel S (1994) Life in moving fluids. Princeton University Press, Princeton, p 488Google Scholar
  67. Watanabe Y, Baranov EA, Sato K, Naito Y, Miyazaki N (2006) Body density affects stroke patterns in Baikal seals. J Exp Biol 209:3269–3280PubMedCrossRefPubMedCentralGoogle Scholar
  68. Watanabe YY, Sato K, Watanuki Y, Takahashi A, Mitani Y, Amano M, Aoki К, Narazaki T, Takashi I, Minamikawa S Miyazaki N (2011) Scaling of swim speed in breath-hold divers. J Animal Eco l 80:57–68CrossRefGoogle Scholar
  69. Webb PM, Crocker DE, Blackwell SB, Costa DP, Le Boeuf BJ (1998) Effects of buoyancy on the diving behavior of northern elephant seals. J Exp Biol 201:2349–2358PubMedPubMedCentralGoogle Scholar
  70. Weber P, Howle LE, Murray MM, Reidenberg JS, Fish FE (2014) Hydrodynamic performance of the flippers of large-bodied cetaceans in relation to locomotor ecology. Mar Mamm Sci 30:413–432CrossRefGoogle Scholar
  71. Weihs D (1974) Energetic advantages of burst swimming of fish. J Theor Biol 48:215–229PubMedCrossRefPubMedCentralGoogle Scholar
  72. Weihs D (2002) Dynamics of dolphin porpoising revisited. Integr Comp Biol 42:1071–1078PubMedCrossRefPubMedCentralGoogle Scholar
  73. Wickler SJ, Hoyt DF, Cogger EA, Hirschbeini MH (2000) Preferred speed and cost of transport: the effect of incline. J Exp Biol 203:2195–2200PubMedPubMedCentralGoogle Scholar
  74. Williams TD, Allen DD, Groff JM, Glass RL (1992) An analysis of California sea otter (Enhydra lutris) pelage and integument. Mar Mamm Sci 8:1–18CrossRefGoogle Scholar
  75. Williams TM (1989) Swimming by sea otters: adaptations for low energetic cost locomotion. J Comp Physiol A 164:815–824PubMedCrossRefPubMedCentralGoogle Scholar
  76. Williams TM (1999) The evolution of cost efficient swimming in marine mammals: limits to energetic optimization. Phil Trans R Soc B 354:193–201.CrossRefGoogle Scholar
  77. Williams TM, Davis RW, Fuiman L, Francis J, Le Boeuf BJ, Horning M, Calambokidis J, Croll DA (2000) Sink or swim: strategies for cost-efficient diving by marine mammals. Science 288:133–136PubMedCrossRefPubMedCentralGoogle Scholar
  78. Williams TM, Friedl AW, Fong ML, Yamada RM, Sedivy P, Haun JE (1992) Travel at low energetic cost by swimming and wave-riding bottlenose dolphins. Nature 355:821–823PubMedCrossRefPubMedCentralGoogle Scholar
  79. Williams TM, Friedl WA, Haun JE (1993) The physiology of bottlenose dolphins (Tursiops truncatus): heart rate, metabolic rate and plasma lactate concentration during exercise. J Exp Biol 179:31–46PubMedPubMedCentralGoogle Scholar
  80. Williams TM, Fuiman LA, Horning M, Davis RW (2004) The cost of foraging by a marine predator, the Weddell seal Leptonychotes weddellii: pricing by the stroke. J Exp Biol 207:973–982PubMedCrossRefPubMedCentralGoogle Scholar
  81. Williams TM, Kastelein RA, Davis RW, Thomas JA (1988) The effects of oil contamination and cleaning on sea otters I: thermoregulatory implications based on pelt studies. Can J Zool 66:2776–2781CrossRefGoogle Scholar
  82. Williams TM, Kooyman GL (1985) Swimming performance and hydrodynamic characteristics of harbor seals Phoca vitulina. Physiol Zool 58:576–589CrossRefGoogle Scholar
  83. Williams TM, Kooyman GL, Croll DA (1991) The effect of submergence on heart rate and oxygen consumption of swimming seals and sea lions. J Comp Physiol B 160:637–644PubMedCrossRefPubMedCentralGoogle Scholar
  84. Williams TM, Worthy GAJ (2002) Anatomy and physiology: the challenge of aquatic living. In: Hoelzel R (ed) Marine mammal biology: an evolutionary approach. Blackwell Science, Oxford, pp 73–97Google Scholar
  85. Williams TM, Kendall TL, Richter BP, Ribeiro-French CR, John JS, Odell KL, Losch BA, Feuerbach DA, Stamper MA (2017) Swimming and diving energetics in dolphins: a stroke-by-stroke analysis for predicting the cost of flight responses in wild odontocetes. J Exp Biol 220:1135–1145.PubMedCrossRefPubMedCentralGoogle Scholar
  86. Wolt R, Gelwick FP, Weltz F, Davis RW (2012) Foraging behavior and prey preference of sea otters (Enhydra lutris kenyoni) in a predominantly soft sediment habitat in Alaska. Mamm Biol 77:271–280CrossRefGoogle Scholar
  87. Worthy GAJ, Innes S, Braune BM, Stewart REA (1987) Rapid acclimation of cetaceans to an open-system respirometer. In: Huntley AC, Costa DP, Worthy GAJ, Castellini MA (eds) Approaches to marine mammal energetics. Sp Pub Soc Mar Mamm No. 1. Allen Press, Lawrence, Kansas, pp 115–126Google Scholar
  88. Würsig B, Würsig M (1979) Behavior and ecology of the bottlenose dolphin, Tursiops truncatus, in the South Atlantic. Fish Bull 77:399–412Google Scholar
  89. Würsig B, Würsig M (1980) Behavior and ecology of the dusky dolphin, Lagenorhynchus obscurus, in the South Atlantic. Fish Bull 77:871–890Google Scholar
  90. Yazdi P, Kilian A, Culik BM (1999) Energy expenditure of swimming bottlenose dolphins (Tursiops truncatus). Mar Biol 134:601–607CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Randall W. Davis
    • 1
  1. 1.Marine BiologyTexas A&M UniversityGalvestonUSA

Personalised recommendations