Swimming performance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae) Swimming performance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae) II. Kinematics

SUMMARY The swimming kinematics of the eastern Pacific bonito Sarda chiliensis at a range of sustained speeds were analyzed to test the hypothesis that the bonito's swimming mode differs from the thunniform locomotor mode of tunas. Eight bonito (fork length FL 47.5±2.1 cm, mass 1.25±0.15 kg) (mean ± s.d.) swam at speeds of 50–130 cm s-1 at 18±2°C in the same temperature-controlled water tunnel that was used in previous studies of tunas. Kinematics variables, quantified from 60 Hz video recordings and analyzed using a computerized, two-dimensional motion analysis system, were compared with published data for similar sized tunas at comparable speeds. Bonito tailbeat frequency, tailbeat amplitude and stride length all increased significantly with speed. Neither yaw (6.0±0.6%FL) nor propulsive wavelength (120±65% fish total length) varied with speed, and there were no mass or body-length effects on the kinematics variables for the size range of bonitos used. Relative to similar sized yellowfin (Thunnus albacares) and skipjack (Katsuwonus pelamis) tunas at similar speeds, the bonito has a lower tailbeat frequency, a higher yaw and a greater stride length. The lateral displacement and bending angle of each intervertebral joint during a complete tailbeat cycle were determined for the bonito at a swimming speed of 90 cm s-1. The pattern of mean maximum lateral displacement (zmax) and mean maximum bending angle (βmax) along the body in the bonito differed from that of both chub mackerel Scomber japonicus and kawakawa tuna Euthynnus affinis; zmax was highest in the bonito. This study verifies that S. chiliensis is a carangiform swimmer and supports the hypothesis that the thunniform locomotor mode is a derived tuna characteristic associated with changes in this group's myotomal architecture. The finding that yaw and zmax were greater in the bonito than in both mackerels and tunas suggests that swimming kinematics in the bonito is not intermediate between that of tunas and mackerels, as would be predicted on the basis of morphological characteristics.

[1]  M. Lighthill Hydromechanics of Aquatic Animal Propulsion , 1969 .

[2]  P. Bushnell,et al.  Cardiovascular and respiratory physiology of tuna: adaptations for support of exceptionally high metabolic rates , 1994, Environmental Biology of Fishes.

[3]  Imants G. Priede,et al.  Metabolic Scope in Fishes , 1985 .

[4]  W. H. Neill,et al.  Respiration rates and low-oxygen tolerance limits in skipjack tuna , 2013 .

[5]  J. Graham,et al.  Anatomical and physiological specializations for endothermy , 2001 .

[6]  A. Blight THE MUSCULAR CONTROL OF VERTEBRATE SWIMMING MOVEMENTS , 1977 .

[7]  B. Nolet,et al.  Costs of swimming measured at optimum speed: scale effects, differences between swimming styles, taxonomic groups and submerged and surface swimming. , 1990, Comparative biochemistry and physiology. A, Comparative physiology.

[8]  J. Gray Studies in Animal Locomotion , 1936 .

[9]  C. Milligan,et al.  LACTATE METABOLISM IN RAINBOW TROUT , 1993 .

[10]  Jennifer C. Nauen,et al.  Locomotion in scombrid fishes: morphology and kinematics of the finlets of the chub mackerel Scomber japonicus. , 2000, The Journal of experimental biology.

[11]  J. J. Videler Fish Swimming Movements: a Study of One Element of Behaviour , 1984 .

[12]  J. M. Donley,et al.  Swimming kinematics of juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). , 2000, The Journal of experimental biology.

[13]  M. Lucas,et al.  AN ANNULAR RESPIROMETER FOR MEASURING AEROBIC METABOLIC RATES OF LARGE, SCHOOLING FISHES , 1993 .

[14]  J. Magnuson COMPARATIVE STUDY OF ADAPTATIONS FOR CONTINUOUS SWIMMING AND HYDROSTATIC EQUILIBRIUM OF SCOMBROID AND XIPHOID FISHES , 1973 .

[15]  F. Koehrn,et al.  Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion and endothermy , 1983 .

[16]  P. Webb Hydrodynamics and Energetics of Fish Propulsion , 1975 .

[17]  T. Lowe,et al.  Gill and intestinal Na+-K+ ATPase activity, and estimated maximal osmoregulatory costs, in three high-energy-demand teleosts: yellowfin tuna (Thunnus albacares), skipjack tuna (Katsuwonus pelamis), and dolphin fish (Coryphaena hippurus) , 2001 .

[18]  Harry L. Fierstine,et al.  Studies in locomotion and anatomy of scombroid fishes , 1968 .

[19]  Graham,et al.  Red muscle activation patterns in yellowfin (Thunnus albacares) and skipjack (Katsuwonus pelamis) tunas during steady swimming. , 1999, The Journal of experimental biology.

[20]  J. Gray,et al.  Studies in Animal Locomotion: I. The Movement of Fish with Special Reference to the Eel , 1933 .

[21]  V. Tucker The energetic cost of moving about. , 1975, American Scientist.

[22]  Brian Blanksby,et al.  Swimming , 2002, Clinics in sports medicine.

[23]  J. Sibert,et al.  THE SPAWNING FREQUENCY OF SKIPJACK TUNA, KATSUWONUS PELAMIS, FROM THE SOUTH PACIFIC , 1986 .

[24]  J. Finnerty,et al.  Endothermy in fishes: a phylogenetic analysis of constraints, predispositions, and selection pressures , 1994, Environmental Biology of Fishes.

[25]  L. Fuiman,et al.  What a drag it is getting cold: partitioning the physical and physiological effects of temperature on fish swimming , 1997, The Journal of experimental biology.

[26]  J. Teal,et al.  Heat conservation in tuna fish muscle. , 1966, Proceedings of the National Academy of Sciences of the United States of America.

[27]  H. Dewar,et al.  ASPECTS OF SHARK SWIMMING PERFORMANCE DETERMINED USING A LARGE WATER TUNNEL , 1990 .

[28]  John J. Videler,et al.  Fast Continuous Swimming of Two Pelagic Predators, Saithe (Pollachius Virens) and Mackerel (Scomber Scombrus): a Kinematic Analysis , 1984 .

[29]  Graham,et al.  STUDIES OF TROPICAL TUNA SWIMMING PERFORMANCE IN A LARGE WATER TUNNEL - KINEMATICS , 1994, The Journal of experimental biology.

[30]  S. Perry,et al.  Effects of Exhausting Exercise on Acid-Base Regulation in Skipjack Tuna (Katsuwonus pelamis) Blood , 1985, Physiological Zoology.

[31]  D. Weihs Hydromechanics of Fish Schooling , 1973, Nature.

[32]  J. Graham Heat exchnage in the black skipjack, and the blood-gas relationship of warm-bodied fishes. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[33]  C. Milligan,et al.  Metabolic recovery from exhaustive exercise in rainbow trout , 1996 .

[34]  R. Shadwick,et al.  Muscle Dynamics in Fish During Steady Swimming , 1998 .

[35]  Robert E. Shadwick,et al.  8. Swimming and muscle function , 2001 .

[36]  J. Roberts Active branchial and ram gill ventilation in fishes. , 1975, The Biological bulletin.

[37]  I. Johnston,et al.  Thermal dependence of contractile properties of single skinned muscle fibres from Antarctic and various warm water marine fishes including Skipjack Tuna (Katsuwonus pelamis) and Kawakawa (Euthynnus affinis) , 2004, Journal of Comparative Physiology B.

[38]  Kenneth D. Lawson,et al.  Warm-Bodied Fish , 1971 .

[39]  Richard W. Brill,et al.  The cardiovascular system of tunas , 2001 .

[40]  John J. Magnuson,et al.  4 - Locomotion by Scombrid Fishes: Hydromechanics, Morphology, and Behavior , 1978 .

[41]  J. Graham,et al.  Water-tunnel studies of heat balance in swimming mako sharks. , 2001, The Journal of experimental biology.

[42]  Lauder,et al.  Tail kinematics of the chub mackerel Scomber japonicus: testing the homocercal tail model of fish propulsion. , 1999, The Journal of experimental biology.

[43]  Paul W. Webb,et al.  3 - Hydrodynamics: Nonscombroid Fish , 1978 .

[44]  K. Kishinouye Contributions to the comparative study of the so-called scombroid fishes , 1923 .

[45]  John J. Magnuson,et al.  Hydrostatic Equilibrium of Euthynnus affinis, a Pelagic Teleost Without a Gas Bladder , 1970 .

[46]  B. Collette II. – ADAPTATIONS AND SYSTEMATICS OF THE MACKERELS AND TUNAS , 1978 .

[47]  K. Dickson Unique adaptations of the metabolic biochemistry of tunas and billfishes for life in the pelagic environment , 2004, Environmental Biology of Fishes.

[48]  J. M. Donley,et al.  Effects of temperature on sustained swimming performance and swimming kinematics of the chub mackerel Scomber japonicus. , 2002, The Journal of experimental biology.

[49]  Lauder Speed effects on midline kinematics during steady undulatory swimming of largemouth bass, Micropterus salmoides , 1995, The Journal of experimental biology.

[50]  L. Rome,et al.  The influence of temperature on power output of scup red muscle during cyclical length changes. , 1992, The Journal of experimental biology.

[51]  J. R. Brett,et al.  Metabolic Rates and Critical Swimming Speeds of Sockeye Salmon (Oncorhynchus nerka) in Relation to Size and Temperature , 1973 .

[52]  J. Graham,et al.  Swimming performance studies on the eastern Pacific bonito Sarda chiliensis, a close relative of the tunas (family Scombridae) I. Energetics , 2003, Journal of Experimental Biology.

[53]  B. Block Endothermy in fish: thermogenesis, ecology and evolution , 1991 .

[54]  Mark W. Westneat,et al.  7. Mechanical design for swimming: muscle, tendon, and bone , 2001 .

[55]  C. S. Wardle,et al.  Tuning in to fish swimming waves: body form, swimming mode and muscle function , 1995, The Journal of experimental biology.

[56]  J. Magnuson Digestion and Food Consumption by Skipjack Tuna (Katsuwonus pelamis) , 1969 .

[57]  R. Laurs,et al.  O2 tension, swimming-velocity, and thermal effects on the metabolic rate of the Pacific albacore Thunnus alalunga. , 1989, Experimental biology.

[58]  A. F. Bennett,et al.  Partitioning the effects of temperature and kinematic viscosity on the C-start performance of adult fishes , 1998, The Journal of experimental biology.

[59]  Richard W. Brill,et al.  Selective advantages conferred by the high performance physiology of tunas, billfishes, and dolphin fish , 1996 .

[60]  J. Graham,et al.  The evolution of thunniform locomotion and heat conservation in scombrid fishes: New insights based on the morphology of Allothunnus fallai , 2000 .

[61]  J. Altringham,et al.  Why do tuna maintain elevated slow muscle temperatures? Power output of muscle isolated from endothermic and ectothermic fish. , 1997, The Journal of experimental biology.

[62]  H. Dewar,et al.  Tuna metabolism and energetics , 2001 .

[63]  K. Dickson,et al.  Maximum sustainable speeds and cost of swimming in juvenile kawakawa tuna (Euthynnus affinis) and chub mackerel (Scomber japonicus). , 2000, The Journal of experimental biology.

[64]  C. A. Pell,et al.  The horizontal septum: Mechanisms of force transfer in locomotion of scombrid fishes (Scombridae, Perciformes) , 1993, Journal of morphology.

[65]  D. Ellerby,et al.  Fish swimming: patterns in muscle function. , 1999, The Journal of experimental biology.

[66]  M. Lighthill Aquatic animal propulsion of high hydromechanical efficiency , 1970, Journal of Fluid Mechanics.

[67]  Richard,et al.  ON THE STANDARD METABOLIC RATES OF TROPICAL TUNAS, ma INCLUDING THE EFFECT OF BODY SIZE AND ACUTE TEMPERATURE CHANGE , 2004 .

[68]  B. Collette,et al.  Systematics and morphology of the bonitos (Sarda) and their relatives (Scombridae, Sardini) , 1975 .

[69]  J. Magnuson,et al.  Courtship, locomotion, feeding, and miscellaneous behaviour of Pacific bonito (Sarda chiliensis). , 1966, Animal behaviour.

[70]  B. Collette,et al.  Unstable and Stable Classifications of Scombroid Fishes , 1995 .

[71]  J. Finnerty,et al.  Evolution of endothermy in fish: mapping physiological traits on a molecular phylogeny. , 1993, Science.

[72]  Pingguo He,et al.  Tilting behaviour of the Atlantic mackerel, Scomber scombrus, at low swimming speeds , 1986 .

[73]  K Kinosita,et al.  Rotation of F(1)-ATPase and the hinge residues of the beta subunit. , 2000, The Journal of experimental biology.

[74]  G. Recovery metabolism of skipjack tuna ( Katsuwonus pelamis ) white muscle : rapid and parallel changes in lactate and phosphocreatine after exercise , 2004 .

[75]  D. Ellerby,et al.  Slow muscle function of Pacific bonito (Sarda chiliensis) during steady swimming. , 2000, The Journal of experimental biology.

[76]  P. W. Hochachka,et al.  Mammalian metabolite flux rates in a teleost: lactate and glucose turnover in tuna. , 1986, The American journal of physiology.

[77]  P. Bushnell,et al.  Metabolic and cardiac scope of high energy demand teleosts, the tunas , 1991 .

[78]  R. Laurs,et al.  Metabolic rate of the albacore tuna Thunnus alalunga , 1982 .

[79]  L. Rome,et al.  The influence of temperature on power production during swimming. II. Mechanics of red muscle fibres in vivo. , 2000, The Journal of experimental biology.

[80]  C. C. Lindsey 1 - Form, Function, and Locomotory Habits in Fish , 1978 .

[81]  I. E. Gray COMPARATIVE STUDY OF THE GILL AREA OF MARINE FISHES , 1954 .

[82]  M R Hebrank,et al.  Mechanical properties of fish backbones in lateral bending and in tension. , 1982, Journal of biomechanics.

[83]  Graham,et al.  STUDIES OF TROPICAL TUNA SWIMMING PERFORMANCE IN A LARGE WATER TUNNEL - ENERGETICS , 1994, The Journal of experimental biology.

[84]  Shadwick,et al.  Muscle dynamics in skipjack tuna: timing of red muscle shortening in relation to activation and body curvature during steady swimming. , 1999, The Journal of experimental biology.