Crossref journal-article
The Company of Biologists
Journal of Experimental Biology (237)
Abstract

SUMMARYFish larvae, like most adult fish, undulate their bodies to propel themselves. A detailed kinematic study of the larval body wave is a prerequisite to formulate a set of functional requirements that the locomotor system must fulfil to generate the observed swimming kinematics. Lateral displacement and curvature profiles were obtained for zebrafish (Danio rerio) larvae at 2–21 days post-fertilisation for three swimming behaviours (cyclic swimming, slow starts and fast startle responses) using high-speed video. During cyclic swimming, fish larvae maintain tail beat frequencies of up to 100 Hz. The corresponding longitudinal strains, estimated from the peak curvatures of the midline, reach up to 0.19 in superficial tissue. The strain rate can reach 120 s–1. The wave of curvature travels along the body at a near-constant rate. Posterior to the stiff head, body-lengthspecific curvature is high and rises gently along the entire trunk to a maximum value of 6. Burst-and-coast swimming generates similar peak curvatures to cyclic swimming, but curvature rises more steeply from head to tail. Fish larvae exhibit phase shifts of 57–63°between the wave of lateral displacement and the wave of curvature, resulting in a 1:1.2 ratio of body wave length to curvature wave length. During C-starts, muscle strain can reach 0.19 and superficial longitudinal strain rates approach 30 s–1. Fish larvae do not initiate their escape response with a standing wave of curvature, although their C-starts approach a standing wave as the larvae grow older. The performance demands derived from swimming kinematics suggest that larval axial muscles have very short contraction cycles (10 ms), experience considerable strains (up to 0.2)and strain rates (up to 30 s–1 in white muscle fibres) yet are able to power swimming for several seconds.

Bibliography

Müller, U. K., & van Leeuwen, J. L. (2004). Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development. Journal of Experimental Biology, 207(5), 853–868.

Authors 2
  1. Ulrike K. Müller (first)
  2. Johan L. van Leeuwen (additional)
References 38 Referenced 207
  1. Askew, G. N. and Marsh, R. L. (2001). The mechanical power output of the pectoralis muscle of blue-breasted quail(Coturnix chinensis): the in vivo length cycle and its implications for muscle performance. J. Exp. Biol.204,3587-3600. (10.1242/jeb.204.21.3587)
  2. Bainbridge, R. (1958). The speed of swimming of fish as related to size and to the frequency and amplitude of the tail beat. J. Exp. Biol.35,109-133. (10.1242/jeb.35.1.109)
  3. Blight, A. R. (1977). The muscular control of vertebrate swimming movements. Biol. Rev.52,181-218. (10.1111/j.1469-185X.1977.tb01349.x)
  4. Brokaw, C. J. (1965). Non-sinusoidal bending waves of sperm flagella. J. Exp. Biol.43,155-169. (10.1242/jeb.43.1.155)
  5. Budick, S. A. and O'Malley, D. M. (2000). Locomotor repertoire of larval zebrafish: swimming, turning and prey capture. J. Exp. Biol.203,2565-2579. (10.1242/jeb.203.17.2565)
  6. Buss, R. R. and Drapeau, P. (2001). Synaptic drive to motoneurons during fictive swimming in developing zebrafish. J. Neurophysiol.86,197-210. (10.1152/jn.2001.86.1.197)
  7. Ellerby, D. J. and Altringham, J. D. (2001). Spatial variation in fast muscle function of the rainbow trout Oncorhynchus mykiss during fast-starts and sprinting. J. Exp. Biol.204,2239-2250. (10.1242/jeb.204.13.2239)
  8. Fuiman, L. A. (1986). Burst swimming performance of larval zebra danios and the effects of diel temperature fluctuations. Trans. Am. Fish. Soc.115,143-148. (10.1577/1548-8659(1986)115<143:BPOLZD>2.0.CO;2)
  9. Fuiman, L. A. and Webb, P. W. (1988). Ontogeny of routine swimming activity and performance in zebra danios (Teleostei:Cyprinidae). Anim. Behav.36,250-261. (10.1016/S0003-3472(88)80268-9)
  10. Jayne, B. C. and Lauder, G. V. (1993). Red and white muscle activity and kinematics of the escape response of the blue-gill sunfish during swimming activity. J. Comp. Physiol. A173,495-508.
  11. Gemballa, S. and Vogel, F. (2002). Spatial arrangement of white muscle fibres and myoseptal tendons in fishes. Comp. Biochem. Physiol. A133,1013-1037. (10.1016/S1095-6433(02)00186-1)
  12. Gray, J. (1933). Studies of animal locomotion. I. The movement of fish with special reference to the eel. J. Exp. Biol.10,88-104.
  13. 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. (10.1242/jeb.201.10.1659)
  14. Hess, F. and Videler, J. J. (1984). Fast continuous swimming of saithe (Pollachius virens): a dynamic analysis of bending moments and muscle power. J. Exp. Biol.109,229-251. (10.1242/jeb.109.1.229)
  15. Johnston, I. A., van Leeuwen, J. L., Davies, M. L. F. and Beddow, T. (1995). How fish power predatory fast-starts. J. Exp. Biol.198,1851-1861. (10.1242/jeb.198.9.1851)
  16. 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.198,243-256. (10.1006/jtbi.1998.0696)
  17. Lipschutz, M. M. (1969). Theory and Problems of Differential Geometry. Schaum's Outline Series. New York: McGraw-Hill.
  18. Lowe, C. P. (2003). Dynamics of filaments:modelling the dynamics of driven microfilaments. Proc. R. Soc. Lond. B358,1543-1550.
  19. McHenry, M. J., Pell, C. A. and Long, J. H.(1995). Mechanical control of swimming speed: stiffness and axial wave form in undulatory fish models. J. Exp. Biol.198,2293-2305. (10.1242/jeb.198.11.2293)
  20. McHenry, M. J. (2003). Mechanisms of helical swimming: asymmetries in the morphology, movement and mechanics of larvae of ascidian Distaplia occidentalis.J. Exp. Biol.204,2959-2973.
  21. Müller, U. K., Smit, J., Stamhuis, E. J. and Videler, J. J. (2000). How the body contributes to the wake in undulatory fish swimming: flow fields of a swimming eel (Anguilla anguilla). J. Exp. Biol.204,2751-2762.
  22. Osse, J. W. M. and van den Boogaart, J. G. M.(1999). Dynamic morphology of fish larvae, structural implications of friction forces in swimming, feeding and ventilation. J. Fish Biol.55,156-174.
  23. Rome, L. C. and Lindstedt, S. L. (1998). The quest for speed: muscles built for high-frequency contractions. News Physiol. Sci.13,261-268. (10.1152/physiologyonline.1998.13.6.261)
  24. Shadwick, R. E., Katz, S. L., Korsmeyer, K. E., Knower, T. and Covell, J. W. (1999). Muscle dynamics in skipjack tuna:timing of red muscle shorting in relation to activation and body curvature during steady swimming. J. Exp. Biol.202,2139-2150. (10.1242/jeb.202.16.2139)
  25. Spierts, I. L. Y. and van Leeuwen, J. L.(1999). Kinematics and muscle dynamics of C- and S-starts of carp(Cyprinus carpio L.). J. Exp. Biol.202,393-406. (10.1242/jeb.202.4.393)
  26. Triller, A., Rostaing, P., Korn, H. and Legendre, P.(1997). Morphofunctional evidence for mature synaptic contacts on the Mauthner cell of 52-hour-old zebrafish larvae. Neuroscience80,133-145. (10.1016/S0306-4522(97)00092-4)
  27. 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 L.) recruitment and normalised power output during swimming in different modes. J. Zool. Lond.220,123-145.
  28. van Raamsdonk, W., Pool, C. W. and te Kronnie, G.(1978). Differentiation of muscle fiber types in the teleost Brachydanio rerio.Anat. Embryol.153,137-155. (10.1007/BF00343370)
  29. Videler, J. J. (1993). Fish Swimming. London: Chapman and Hall. (10.1007/978-94-011-1580-3)
  30. Videler, J. J. and Hess, F. (1984). Fast continuous swimming of two pelagic predators, saithe (Pollachius virens) and mackerel (Scomber scombrus): a kinematic analysis. J. Exp. Biol.109,209-228. (10.1242/jeb.109.1.209)
  31. Wakeling, J. M. and Johnston, I. A. (1998). Muscle power output limits fast-start performance in fish. J. Exp. Biol.201,1505-1526. (10.1242/jeb.201.10.1505)
  32. Wakeling, J. M., Kemp, K. M. and Johnston, I. A.(1999). The biomechanics of fast-starts during ontogeny in the common carp Cyprinus carpio.J. Exp. Biol.202,3057-3067. (10.1242/jeb.202.22.3057)
  33. Wassersug, R. J. and von Seckendorf Hoff, K.(1985). The kinematics of swimming in anuran larvae. J. Exp. Biol.119,1-30. (10.1242/jeb.119.1.1)
  34. Weihs, D. (1980). Energetic significance of changes in swimming modes during growth in larval anchovy, Engraulis mordax.Fish. Bull.77,597-604.
  35. Webb, P. W. and Weihs, D. (1986). Functional locomotor morphology of early life history stages of fishes. Trans. Am. Fish. Soc.115,115-127. (10.1577/1548-8659(1986)115<115:FLMOEL>2.0.CO;2)
  36. Woledge, R. C., Curtin, N. A. and Homsher, E.(1985). Energetic of Aspects of Muscle Contraction. London: Academic Press.
  37. Woltring, H. J. (1986). A Fortran package for generalised, cross-validatory spline smoothing and differentiation. Adv. Eng. Software8,104-113. (10.1016/0141-1195(86)90098-7)
  38. Young, I. S. and Rome, L. S. (2001). Mutually exclusive muscle designs: the power output of locomotory and sonic muscles of the oyster toadfish (Opsanus tau). Proc. R. Soc. Lond. B268,1965-1970. (10.1098/rspb.2001.1731)
Dates
Type When
Created 21 years, 7 months ago (Jan. 27, 2004, 5:15 p.m.)
Deposited 1 year, 7 months ago (Jan. 11, 2024, 8:48 p.m.)
Indexed 4 weeks, 1 day ago (Aug. 7, 2025, 4:53 a.m.)
Issued 21 years, 6 months ago (Feb. 15, 2004)
Published 21 years, 6 months ago (Feb. 15, 2004)
Published Print 21 years, 6 months ago (Feb. 15, 2004)
Funders 0

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@article{Mu_ller_2004, title={Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development}, volume={207}, ISSN={0022-0949}, url={http://dx.doi.org/10.1242/jeb.00821}, DOI={10.1242/jeb.00821}, number={5}, journal={Journal of Experimental Biology}, publisher={The Company of Biologists}, author={Müller, Ulrike K. and van Leeuwen, Johan L.}, year={2004}, month=feb, pages={853–868} }