Muscle dynamics in skipjack tuna: Timing of red muscle shortening in relation to activation and body curvature during steady swimming

Journal of Experimental Biology

Volumn 202, Issue 16, 1999, Pages 2139-2150

  Shadwick, Robert E ^a   Katz, Stephen L ^a,c   Korsmeyer, Keith E ^a,d   Knower, Torre ^a   Covell, James W ^b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c DUKE UNIVERSITY   (United States)

^d HAWAII PACIFIC UNIVERSITY   (United States)

Author keywords

Electromyography; Katsuwonus pelamis; Muscle activation; Muscle strain; Red muscle; Sonomicrometry; Swimming; Tuna

Indexed keywords

KATSUWONUS PELAMIS; PELAMIS; SCOMBRIDAE; SCOMBRIDAE GEN. SP.; VERTEBRATA;

EID: 0032828766     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Alexander, R. McN. and Bennet-Clark, H. C. (1977). Storage of elastic strain energy in muscle and other tissues. Nature 265, 114-117.
2. Altringham, J. D. and Block, B. A. (1997). Why do tuna maintain elevated slow muscle temperatures? Power output of muscle isolated from endothermic and ectothermic fish. J. Exp. Biol. 200, 2617-2627.
3. Altringham, J. D. and Johnston, I. A. (1990). Modelling muscle power output in a swimming fish. J. Exp. Biol. 148, 395-402.
4. Altringham, J. D., Wardle, C. S. and Smith, C. I. (1993). Myotomal muscle function at different locations in the body of a swimming fish. J. Exp. Biol. 182, 191-206.
5. Bone, Q. (1978). Locomotor muscle. In Fish Physiology, vol. VII (ed. W. S. Hoar and D. J. Randall), pp. 361-424. New York: Academic Press.
6. Brill, R. W. (1996). Selective advantages conferred by the high performance physiology of tunas, billfishes and dolphin fish. Comp. Biochem. Physiol. 113A, 3-15.
7. Brill, R. W. and Dizon, A. E. (1979). Red and white muscle fibre activity in swimming skipjack tuna, Katsuwonus pelamis (L.). J. Fish Biol. 15, 679-685.
8. Cheng, J.-Y., Pedley, T. J. and Altringham, J. D. (1998). A continuous dynamic beam model for swimming fish. Phil. Trans. R. Soc. Lond. B 353, 981-997.
9. Coughlin, D. J. and Rome, L. C. (1996). The roles of pink and red muscle in powering steady swimming in scup, Stenotomus chrysops. Am. Zool. 36, 666-677.
10. Coughlin, D. J., Valdes, L. and Rome, L. C. (1996). Muscle length changes during swimming in scup: sonomicrometry verifies the anatomical high-speed cine technique. J. Exp. Biol. 199, 459-463.
11. Covell, J. W., Smith, M., Harper, D. G. and Blake, R. W. (1991). Skeletal muscle deformation in the lateral muscle of the intact rainbow trout Oncorhynchus mykiss during fast start maneuvers. J. Exp. Biol. 156, 453-466.
12. Dewar, H. and Graham, J. B. (1994a). Studies of tropical tuna swimming performance in a large water tunnel. I. Energetics. J. Exp. Biol. 192, 13-31.
13. Dewar, H. and Graham, J. B. (1994b). Studies of tropical tuna swimming performance in a large water tunnel. III. Kinematics. J. Exp. Biol. 192, 45-59.
14. Dizon, A. E. and Brill, R. W. (1979). Thermoregulation in tunas. Am. Zool. 19, 249-265.
15. Fierstine, H. L. and Walters, V. (1968). Studies in locomotion and anatomy of scombroid fishes. Mem. S. Calif. Acad. Sci. 6, 1-31.
16. Franklin, C. E. and Johnston, I. A. (1997). Muscle power output during escape responses in an Antarctic fish. J. Exp. Biol. 200, 703-712.
17. Gillis, G. B. (1998). Neuromuscular control of anguilliform locomotion: patterns of red and white muscle activity during swimming in the American eel Aguilla rostrata. J. Exp. Biol. 201, 3245-3256.
18. Graham, J. B., Koehrn, F. J. and Dickson, K. A. (1983). Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion and endothermy. Can. J. Zool. 61, 2087-2096.
19. Hammond, L., Altringham, J. D. and Wardle, C. S. (1998) Myotomal slow muscle function of rainbow trout Oncorhynchus mykiss during steady swimming. J. Exp. Biol. 201, 1659-1671.
20. Hess, F. and Videler, J. J. (1984). Fast continuous swimming of saithe (Pollachius virens): a dynamic analysis of bending movements and muscle power. J. Exp. Biol. 109, 229-251.
21. Hunter, J. R. and Zweifel, J. R. (1971). Swimming speed, tail beat frequency, tail beat amplitude and size in jack mackerel, Trachurus symmetricus and other fishes. Fish. Bull. Fish Wildl. Serv. US 69, 253-266.
22. Jayne, B. C. and Lauder, G. V. (1995). Speed effects on midline kinematics during steady undulatory swimming of largemouth bass Micropterus salmoides. J. Exp. Biol. 198, 585-602.
23. Johnson, T. P. and Johnston, I. A. (1991). Power output of fish muscle fibres performing oscillatory work: effects of acute and seasonal temperature change. J. Exp. Biol. 157, 409-423.
24. Johnson, T. P., Syme, D. A., Jayne, B. C. and Lauder, G. V. (1994). Modeling red muscle power output during steady and unsteady swimming in largemouth bass. Am. J. Physiol. 36, R481-R488.
25. Johnston, I. A., Franklin, C. E. and Johnson, T. P. (1993). Recruitment patterns and contractile properties of fast muscle fibres isolated from rostral and caudal myotomes of the short-horned sculpin. J. Exp. Biol. 185, 251-265.
26. Joseph, J., Klawe, W. and Murphy, P. (1988). Tuna and Billfish. Fish Without a Country. La Jolla, CA: Inter-American Tropical Tuna Commission.
27. Kafuku, T. (1950). Red muscles in fishes. I. Comparative anatomy of the scombroid fishes of Japan. Jap. J. Ichthyol 1, 89-100.
28. Katz, S. L. and Shadwick, R. E. (1998). Curvature of swimming fish midlines as an index of muscle strain suggests swimming muscle produces net positive work. J. Theor. Biol. 193, 243-256.
29. Katz, S. L., Shadwick, R. E. and Rapoport, H. S. (1999). Muscle strain histories in swimming milkfish in steady and sprinting gaits. J. Exp. Biol. 202, 529-541.
30. Kirkpatrick, S. W., Covell, J. W. and Friedman, W. F. (1973). A new technique for the continuous assessment of fetal and neonatal cardiac performance. Am. J. Obstet. Gynec. 116, 963-972.
31. Kishinouye, K. (1923). Contributions to the comparative study of the so-called scombroid fishes. J. Coll. Agric Imper. Univ. Tokyo 8, 293-475.
32. Knower, T. (1998). Biomechanics of thunniform swimming. PhD thesis, University of California, San Diego.
33. Knower, T., Shadwick, R. E., Katz, S. L., Graham, J. B. and Wardle, C. S. (1999). Red muscle activation patterns in yellowfin (Thunnus albacares) and skipjack (Katsuwonas pelamis) tunas during steady swimming. J. Exp. Biol. 202, 2127-2138.
34. Korsmeyer, K. E., Lai, N. C., Shadwick, R. E. and Graham, J. B. (1997). Heart rate and stroke volume contributions to cardiac output in swimming yellowfin tuna: response to exercise and temperature. J. Exp. Biol. 200, 1975-1986.
35. Lighthill, M. J. (1970). Aquatic animal propulsion of high hydromechanical efficiency. J. Fluid Mech. 44, 265-301.
36. Long, J. H., Jr (1998). Muscles, elastic energy and the dynamics of body stiffness in swimming eels. Am. Zool. 38, 771-792.
37. Long, J. H., Jr and Nipper, K. S. (1996). The importance of body stiffness in undulatory propulsion. Am. Zool. 36, 678-694.
38. Lowe, C. G. (1996). Kinematics and critical swimming speed of juvenile scalloped hammerhead sharks. J. Exp. Biol. 199, 2605-2610.
39. Magnuson, J. J. (1978). Locomotion in scombrid fishes: hydrodynamics, morphology, and behavior. In Fish Physiology. Locomotion, vol. VII (ed. W. S. Hoar and D. J. Randall), pp. 239-313. New York: Academic Press.
40. Rayner, M. D. and Keenan, M. J. (1967). Role of red and white muscles in the swimming of skipjack tuna. Nature 214, 392-393.
41. Rome, L. C. and Sosnicki, A. A. (1991). Myofilament overlap in swimming carp. II. Sarcomere length changes during swimming. Am. J. Physiol. 260, C289-C296.
42. Rome, L. C. and Swank, D. (1992). The influence of temperature on power output of scup red muscle during cyclic length changes. J. Exp. Biol. 171, 261-282.
43. Rome, L. C., Swank, D. and Corda, D. (1993). How fish power swimming. Science 261, 340-343.
44. Shadwick, R. E., Knower, T. and Fonseca, M. (1992). The mechanical organization of muscle and tendon in yellowfin tuna. Am. Zool. 32, 159A.
45. Shadwick, R. E., Steffensen, J. F., Katz, S. L. and Knower, T. (1998). Muscle dynamics in fish during steady swimming. Am. Zool. 38, 755-770.
46. Tang, J. and Wardle, C. S. (1992). Power output of two sizes of Atlantic salmon (Salmo salar) at their maximum sustained swimming speeds. J. Exp. Biol. 166, 33-46.
47. van Leeuwen, J. L. (1995). The action of muscles in swimming fish. Exp. Physiol. 80, 177-191.
48. van Leeuwen, J. L., Lankheet, M. J. M., Akster, H. A. and Osse, J. W. M. (1990). Function of red axial muscles of carp (Cyprinus carpio): recruitment and normalized power output during swimming in different modes. J. Zool., Lond. 220, 123-145.
49. Videler, J. J. (1993). Fish Swimming. London: Chapman & Hall.
50. Wainwright, S. A. (1983). To bend a fish. In Fish Biomechanics (ed. P. W. Webb and D. Weihs), pp. 68-91. New York: Praeger Publ.
51. Wakeling, J. M. and Johnston, I. A. (1998). Muscle power output limits fast-start performance in fish. J. Exp. Biol. 201, 1505-1526.
52. Wakeling, J. M. and Johnston, I. A. (1999). White muscle strain in the common carp and red to white muscle gearing ratios in fish. J. Exp. Biol. 202, 521-528.
53. Wardle, C. S. and Videler, J. J. (1993). The timing of the electromyogram in the lateral myotomes of mackerel and saithe at different swimming speeds. J. Fish Biol. 42, 347-359.
54. Wardle, C. S. and Videler, J. J. (1994). The timing of lateral muscle strain and EMG activity in different species of steadily swimming fish. In Mechanics and Physiology of Animal Swimming (ed. L. Maddock, Q. Bone and J. M. V. Rayner), pp. 111-118. Cambridge: Cambridge University Press.
55. Wardle, C. S., Videler, J. J. and Altringham, J. D. (1995). Tuning in to fish swimming waves: body form, swimming mode and muscle function. J. Exp. Biol. 198, 1629-1636.
56. Wardle, C. S., Videler, J. J., Arimoto, T., Franco, J. M. and He, P. (1989). The muscle twitch and the maximum swimming speed of giant bluefin tuna, Thunnus thynnus L. J. Fish Biol. 35, 129-137.
57. Webb, P. W., Kostecki, P. T. and Stevens, E. D. (1984) The effect of size and swimming speed on locomotor kinematics of rainbow trout. J. Exp. Biol. 109, 77-95.
58. Westneat, M. W., Hoese, W., Pell, C. A. and Wainwright, S. A. (1993). The horizontal septum mechanisms of force transfer in locomotion of scombrid fishes Scombridae Perciformes. J. Morph. 217, 183-204.
59. Williams, T. L., Grillner, S., Smoljaninov, V. V., Wallen, P., Kashin, S. and Rossignol, S. (1989). Locomotion in lamprey and trout: the relative timing of activation and movement. J. Exp. Biol. 143, 559-566.