Kinematic analysis of swimming ontogeny in seabass (Dicentrarchus labrax)

Damien Olivier; Quentin Mauguit; Nicolas Vandewalle; Eric Parmentier

doi:10.26496/bjz.2013.125

Authors

Damien Olivier Laboratoire de Morphologie Fonctionnelle et Evolutive, Allée de la chimie, 3 Bât B6 Université de Liège, B-4000 Liège, Belgium
Quentin Mauguit Laboratoire de Morphologie Fonctionnelle et Evolutive, Allée de la chimie, 3 Bât B6 Université de Liège, B-4000 Liège, Belgium
Nicolas Vandewalle GRASP, Institut de Physique, Bât. B5a, Université de Liège, B-4000 Liège, Belgium
Eric Parmentier Laboratoire de Morphologie Fonctionnelle et Evolutive, Allée de la chimie, 3 Bât B6 Université de Liège, B-4000 Liège, Belgium

DOI:

https://doi.org/10.26496/bjz.2013.125

Keywords:

swimming, ontogeny, body-caudal locomotion, Strouhal number, larvae

Abstract

Swimming has been investigated in multiple species, but few studies consider the establishment of swimming through ontogeny. This study describes the establishment of cyclical swimming in Dicentrachus labrax, a marine fish from cold, temperate waters. The data were compared with results from previous studies on two subtropical freshwater catfish species (Clarias gariepinus and Corydoras aeneus). The three species have different modes of locomotion each during their adult stage (anguilliform, subacarangiform and carangiform). The swimming of Dicentrarchus labrax was recorded with a high-speed video camera (500 fps) from 0 to 288 hours and from 960 to 2496 hours post-hatching. Three indices, i.e. coefficient of determination (r²), coefficient of variation (CV), and Strouhal number (St), were used to investigate the establishment and efficiency of swimming. Important differences in the timing of swimming establishment were observed between the seabass and the two catfish species. The two catfish species display a sine-shaped swimming mode immediately or soon after hatching, and the efficiency of movement substantially improves during the first days of life. For seabass, however, establishment of swimming is slower during the same developmental period. These differences may be related to a faster developmental rate in the catfishes that allows them to swim rapidly in an intermediate regime flow and to develop the required morphology to establish efficient movements earlier.

References

Bagarinao T (1986). Yolk resorption, onset of feeding and survival potential of larvae of three tropical marine fish species reared in the hatchery. Marine Biology, 91: 449-459. https://doi.org/1007/BF00392595

Batty RS (1981). Locomotion of plaice larvae. Symposia of the Zoological Society of London, 48: 53-69.

Batty RS (1984). Development of swimming movements and musculature of larval herring (Clupea harengus). Journal of Experimental Biology, 110: 217-229.

Burgess W (1992). Colored atlas of miniature catfish. Every species of Corydoras, Brochis and Aspidoras. T.F.H. Publications, Inc., Neptune City, New Jersey (USA).

Blaxter JHS (1969). Development eggs and larvae. In: W. Hoar & D. Randall (eds), Fish Physiology, Elsevier, 3: 177-252.

Boeuf G & Payan, P (2001). How should salinity influence fish growth? Comparative Biochemistry and Physiology Part C, 130: 41-423.

Borazjani I & Sotiropoulos F (2008). Numerical investigation of the hydrodynamics of carangiform swimming in the transitional and inertial flow regimes. Journal of Experimental Biology, 211(10): 1541-1558. https://doi.org/10.1242/jeb.015644

Borazjani I & Sotiropoulos F (2009). Numerical investigation of the hydrodynamics of anguilliform swimming in the transitional and inertial flow regimes. Journal of Experimental Biology, 212(4): 576-592. https://doi.org/10.1242/jeb.025007.

Breder CM (1926). The locomotion of fishes. Zoologica, 4: 159-256.

Budick S A & O’Malley DM (2000). Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. Journal of Experimental Biology, 203: 2565-2579.

Danos N (2012). Locomotor development of zebrafish (Danio rerio) under novel hydrodynamic conditions. Journal of Experimental Zoology, 317:117–126.

Fontaine E, Lentink D, Kranenbarg S, Müller UK, Van Leeuwen JL, Barr A H & Burdick JW (2008). Automated visual tracking for studying the ontogeny of zebrafish swimming. Journal of Experimental Biology, 211(8): 1305-1316. https://doi.org/10.1242/jeb.010272

Fuiman L A & Webb PW (1988). Ontogeny of routine swiming activity and performance in zebra danios (Teleostei, Cyprinidae). Animal Behaviour, 36(1): 250-261. https://doi.org/10.1016/S00033472(88)80268-9

Gray J (1933). Studies in animal locomotion: I. The movement of fish with special reference to the eel. Journal of Experimental Biology, 10: 88-104.

Gray J & Hancock GJ (1955). The propulsion of sea-urchin spermatozoa. Journal of Experimental Biology 32: 775-801.

Hale M E (1999). Locomotor mechanics during early life history: Effects of size and ontogeny on fast-start performance of salmonid fishes. Journal of Experimental Biology, 202(11): 1465-1479.

Herskin J & Steffensen JF (1998). Energy savings in sea bass swimming in a school: measurements of tail beat frequency and oxygen consumption at different swimming speeds. Journal of Fish Biology, 53: 366-376.

Horner AM & Jayne BC (2008). The effects of viscosity on the axial motor pattern and kinematics of the African lungfish (Protoptetus annectens) during lateral undulatory swimming. The journal of Experimental Biology, 211: 1612-1622. https://doi.org/10.1242/jeb.013029

Lauder GV (1989). Caudal Fin Locomotion in Ray-Finned Fishes: Historical and Functional Analyses . American Zoologist, 29: 85-102.

Lauder GV (2000). Function of the Caudal Fin During Locomotion in Fishes: Kinematics, Flow Visualisation, and Evolutionary Patterns. American Zoologist, 40: 101-122.

Lauder GV (2006). Hydrodynamics of undulatory propulsion. In: E. Shadwick & GV Lauder (eds), Fish Biomechanics, Elsevier, New York: 425-468.

Lighthill MJ (1969). Hydromechanics of aquatic animal propulsion. Annual Review of Fluid Mechanics, 1(1): 413-446. https://doi.org/10.1146/annurev.fl.01.0110169.002213

Lindsey CC (1978). Form function and locomotory habits in fish. In: W. Hoar & D. Randall (eds), Fish Physiology, Academic Press, New York, 7: 1-100.

Long JH, Mc Henry MJ & Boetticher NC (1994). Undulatory swimming: How traveling waves are produced and modulated in sunfish (Lepomis gibbosus). Journal of Experimental Biology, 192(1): 129-145.

Mauguit Q, Genotte V, Becco C, Baras E, Vandewalle N & Vandewalle P (2010a). Ontogeny of swimming movements in the Catfish Clarias gariepinus. The Open Fish Science Journal, 3: 16-29. https://doi.org/ 10.2174/1874401X01003010016

Mauguit Q, Olivier D, Vandewalle N & Vandewalle P (2010b). Ontogeny of swimming movements in bronze corydoras (Corydoras aeneus). Canadian Journal of Zoology, 88: 378-389. https://doi.org/10.1139/Z10-012

McHenry MJ & Lauder GV (2005). The mechanical scaling of coasting in zebrafish (Danio rerio). Journal of Experimental Biology, 208 (12): 2289-2301. https://doi.org/10.1242/jeb.01642

McHenry MJ, Pell CA & Long JH (1995). Mechanical control of swimming speed-stiffness and axial wave-form in undalating fish models. Journal of Experimental Biology, 198(11): 2293-2305.

Mclain DH (1974). Drawing counturs from arbitrary data points. Computer Journal, 17: 318-324.

Müller UK & Videler JJ (1996). Inertia as a ‘safe harbour’: Do fish larvae increase length growth to escape viscous drag? Reviews in Fish Biology and Fisheries, 6: 353-360.

Müller UK & Van Leeuwen JL (2004). Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development. Journal of Experimental Biology, 207(5): 853-868. https://doi.org/10.1242/jeb.00821

Müller UK, Van Den Boogaart JGM & Van Leeuwen JL (2008). Flow patterns of larval fish: undulatory swimming in the intermediate flow regime. Journal of Experimental Biology, 211(2): 196-205. https://doi.org/110.1242/jeb.005629. 10.1242/jeb.005629

Osse JWM (1990). Form changes in fish larvae in relation to changing demands of function. Netherlands Journal of Zoology, 40(1): 362-385. https://doi.org/10.1163/156854289X00354

Osse JWM & Van Den Boogaart JGM (2000). Body size and swimming types in carp larvae; effects of being small. Netherlands Journal of Zoology, 50 (2): 233-244.

Palomares MLD (1991). La consommatíon de nourriture chez les poissons: étude comparative, mise au point d’un modèle prédictif et application à l’étude des réseaux trophiques. Ph D Thesis, Institut National Polytechnique, Toulouse.

Pickett GD & Pawson MG (1994). Seabass biology, exploitation and conservation. Chapman and Hall, Fish and Fisheries, 12.

Taylor GK, Nudds RL & Thomas ALR (2003). Flying and swimming animals cruise at a Strouhal number tuned for high power efficiency. Nature, 425(6959): 707-711. https://doi.org/710.1038/nature02000.

Teugels, G. (1986). A systematic revision of the African species of the genus Clarias (Pisces: Clariidae). Annales Musee Royal de l’Afrique Centrale, 247: 199-247.

Thorsen DH, Cassidy JJ & Hale ME (2004). Swimming of larval zebrafish: fin-axis coordination and implications for function and neural control. Journal of Experimental Biology, 207(24): 4175-4183. https://doi.org/10.1242/jeb.01285

Tytell ED (2004). The hydrodynamics of eel swimming II. Effect of swimming speed. Journal of Experimental Biology, 207(19): 3265-3279. http://dx.doi/org/10.1242/jeb.01139

Videler JJ (1981). Swimming movements, body structure and propulsion in cod Gadus morhua. Symposia of the Zoological Society of London, 48: 1-27.

Videler JJ (1993). Fish swimming. Chapman and Hall, London.

Videler (2011). An opinion paper: emphasis on white muscle development and growth to improve farmed fish flesh quality. Fish Physiology and Biochemistry, 37: 337-343. https://doi.org/10.1007/s10695-011-9501-4

Webb PW (1984). Form and function in fish swimming. Scientific American, 251: 72-82.

Webb PW & Weihs D (1986). Functional locomotor morphology of early life history stages of fishes. Transactions of the American Fisheries Society, 115(1): 115-127.