Energetics of median and paired fin swimming, body and caudal fin swimming, and gait transition in parrotfish (Scarus schlegeli) and triggerfish (Rhinecanthus aculeatus).

To determine the energetic costs of rigid-body, median or paired-fin (MPF) swimming versus undulatory, body-caudal fin (BCF) swimming, we measured oxygen consumption as a function of swimming speed in two MPF swimming specialists, Schlegel's parrotfish and Picasso triggerfish. The parrotfish swam exclusively with the pectoral fins at prolonged swimming speeds up to 3.2 total lengths per second (L s(-1); 30 min critical swimming speed, U(crit)). At higher speeds, gait transferred to a burst-and-coast BCF swimming mode that resulted in rapid fatigue. The triggerfish swam using undulations of the soft dorsal and anal fins up to 1.5 L s(-1), beyond which BCF undulations were recruited intermittently. BCF swimming was used continuously above 3.5 L s(-1), and was accompanied by synchronous undulations of the dorsal and anal fins. The triggerfish were capable of high, prolonged swimming speeds of up to 4.1 L s(-1) (30 min U(crit)). In both species, the rates of increase in oxygen consumption with swimming speed were higher during BCF swimming than during rigid-body MPF swimming. Our results indicate that, for these species, undulatory swimming is energetically more costly than rigid-body swimming, and therefore support the hypothesis that MPF swimming is more efficient. In addition, use of the BCF gait at higher swimming speed increased the cost of transport in both species beyond that predicted for MPF swimming at the same speeds. This suggests that, unlike for terrestrial locomotion, gait transition in fishes does not occur to reduce energetic costs, but to increase recruitable muscle mass and propulsive surfaces. The appropriate use of the power and exponential functions to model swimming energetics is also discussed.

[1]  Robert J. Wootton,et al.  The swimming endurance of threespine sticklebacks, Gasterosteus aculeatus L., from the Afon Rheidol, Wales , 1987 .

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

[3]  P. W. Webb,et al.  Kinematics of Pectoral Fin Propulsion in Cymatogaster Aggregata , 1973 .

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

[5]  Theodore Y Wu,et al.  Introduction to the Scaling of Aquatic Animal Locomotion , 1977 .

[6]  P. Bushnell,et al.  An automated swimming respirometer , 1984 .

[7]  C. Gerstner,et al.  Maneuverability of four species of coral-reef fish that differ in body and pectoral-fin morphology , 1999 .

[8]  Mark W. Westneat,et al.  FUNCTIONAL MORPHOLOGY OF AQUATIC FLIGHT IN FISHES : KINEMATICS, ELECTROMYOGRAPHY, AND MECHANICAL MODELING OF LABRIFORM LOCOMOTION , 1996 .

[9]  James Lighthill,et al.  Biofluiddynamics of balistiform and gymnotiform locomotion. Part 3. Momentum enhancement in the presence of a body of elliptic cross-section , 1990, Journal of Fluid Mechanics.

[10]  Paul W. Webb,et al.  Efficiency of Pectoral-Fin Propulsion of Cymatogaster Aggregata , 1975 .

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

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

[13]  L. Rome.  The mechanical design of the muscular system. , 1994, Advances in veterinary science and comparative medicine.

[14]  J. Murray,et al.  Scale Effects in Animal Locomotion. , 1978 .

[15]  P. Webb.  Exercise performance of fish. , 1994, Advances in veterinary science and comparative medicine.

[16]  R. Blake.  Efficiency and economy in animal physiology: On the efficiency of energy transformations in cells and animals , 1992 .

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

[18]  Robert W. Blake,et al.  Biofluiddynamics of balistiform and gymnotiform locomotion. Part 1. Biological background, and analysis by elongated-body theory , 1990, Journal of Fluid Mechanics.

[19]  G. Kronnie,et al.  Muscle fibre types in the myotome of stickleback, Gasterosteus aculeatus L.; a histochemical, immunohistochemical and ultrastructural study , 1983 .

[20]  L C Rome,et al.  The influence of temperature on muscle velocity and sustained performance in swimming carp. , 1990, The Journal of experimental biology.

[21]  R. M. Alexander,et al.  Optimization and gaits in the locomotion of vertebrates. , 1989, Physiological reviews.

[22]  E. G. Drucker,et al.  Kinematic and electromyographic analysis of steady pectoral fin swimming in the surfperches , 1997, The Journal of experimental biology.

[23]  C. Breder.  The locomotion of fishes , 1926 .

[24]  L. Bernatchez,et al.  Influence of temperature and current speed on the swimming capacity of Lake Whitefish (Coregonus clupeaformis) and Cisco (C. artedii) , 1985 .

[25]  George V. Lauder,et al.  Pectoral Fin Locomotion in Fishes: Testing Drag-based Models Using Three-dimensional Kinematics , 1996 .

[26]  J A Walker,et al.  Does a rigid body limit maneuverability? , 2000, The Journal of experimental biology.

[27]  Paul W. Webb,et al.  Locomotor Patterns in the Evolution of Actinopterygian Fishes , 1982 .

[28]  Lawrence C. Rome,et al.  Why animals have different muscle fibre types , 1988, Nature.

[29]  Sheila N. Patek,et al.  Vertebral Column Morphology, C-Start Curvature, and the Evolution of Mechanical Defenses in Tetraodontiform Fishes , 1998 .

[30]  Kjell Johansen,et al.  OXYGEN CONSUMPTION AND SWIMMING PERFORMANCE IN HYPOXIA-ACCLIMATED RAINBOW TROUT SALMO GAIRDNERI , 1984 .

[31]  Mark W. Westneat,et al.  Mechanics of propulsion by multiple fins: kinematics of aquatic locomotion in the burrfish (Chilomycterus schoepfi) , 1996, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[32]  Paul W. Webb,et al.  Mechanics and Physiology of Animal Swimming: The biology of fish swimming , 1994 .

[33]  J A Walker,et al.  Mechanical performance of aquatic rowing and flying , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[34]  Measurements of aerobic metabolism of a school of horse mackerel at different swimming speeds , 1996 .

[35]  J. Videler.  Fish Swimming , 1993, Springer Netherlands.

[36]  R. Full.  Efficiency and economy in animal physiology: The concepts of efficiency and economy in land locomotion , 1992 .

[37]  G. R. Parsons,et al.  Swimming Efficiency of the White Crappie, Pomoxis annularis , 1992 .

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

[39]  P. Bushnell,et al.  Oxygen consumption in four species of teleosts from Greenland: no evidence of metabolic cold adaptation , 2004, Polar Biology.

[40]  M. Lighthill.  Large-amplitude elongated-body theory of fish locomotion , 1971, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[41]  P W Webb,et al.  Boxfishes (Teleostei: Ostraciidae) as a model system for fishes swimming with many fins: kinematics. , 2001, The Journal of experimental biology.

[42]  J. Videler,et al.  Energetic advantages of burst-and-coast swimming of fish at high speeds. , 1982, The Journal of experimental biology.

[43]  George V. Lauder,et al.  Function of the Caudal Fin During Locomotion in Fishes: Kinematics, Flow Visualization, and Evolutionary Patterns1 , 2000 .

[44]  P W Webb,et al.  Boxfishes as Unusually Well‐Controlled Autonomous Underwater Vehicles* , 2000, Physiological and Biochemical Zoology.

[45]  Lauder,et al.  KINEMATICS OF PECTORAL FIN LOCOMOTION IN THE BLUEGILL SUNFISH LEPOMIS MACROCHIRUS , 1994, The Journal of experimental biology.

[46]  E. G. Drucker,et al.  A hydrodynamic analysis of fish swimming speed: wake structure and locomotor force in slow and fast labriform swimmers. , 2000, The Journal of experimental biology.

[47]  P. Webb.  THE EFFECT OF SOLID AND POROUS CHANNEL WALLS ON STEADY SWIMMING OF STEELHEAD TROUT ONCORHYNCHUS MYKISS , 1993 .

[48]  D. Bellwood,et al.  The relationship between swimming ability and habitat use in wrasses (Labridae) , 2001 .

[49]  George V. Lauder,et al.  The evolution and interrelationships of the actinopterygian fishes , 1983 .

[50]  Westneat,et al.  Motor patterns of labriform locomotion: kinematic and electromyographic analysis of pectoral fin swimming in the labrid fish Gomphosus varius , 1997, The Journal of experimental biology.

[51]  R. W. Blake,et al.  Short Communications: The Mechanics of Labriform Locomotion: II. An Analysis of the Recovery Stroke and the Overall Fin-Beat Cycle Propulsive Efficiency in the Angelfish , 1980 .

[52]  Jeffrey A. Walker,et al.  Performance limits of labriform propulsion and correlates with fin shape and motion. , 2002, The Journal of experimental biology.

[53]  Rome Lc.  The mechanical design of the muscular system. , 1994 .

[54]  J. R. Brett.  The Respiratory Metabolism and Swimming Performance of Young Sockeye Salmon , 1964 .

[55]  Malcolm S. Gordon,et al.  How puffers (Teleostei: Tetraodontidae) swim , 1996 .

[56]  Paul W. Webb,et al.  Is the high cost of body/caudal fin undulatory swimming due to increased friction drag or inertial recoil? , 1992 .

[57]  R. W. Blake,et al.  On Balistiform Locomotion , 1978, Journal of the Marine Biological Association of the United Kingdom.

[58]  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.

[59]  Jeffrey A. Walker,et al.  Labriform propulsion in fishes: kinematics of flapping aquatic flight in the bird wrasse Gomphosus varius (Labridae) , 1997, The Journal of experimental biology.

[60]  D. Bellwood,et al.  Locomotion in labrid fishes: implications for habitat use and cross-shelf biogeography on the Great Barrier Reef , 2001, Coral Reefs.

[61]  W. McGillis,et al.  The boundary layer of swimming fish. , 2001, The Journal of experimental biology.