Mechanisms of anguilliform locomotion in fishes studied using simple three-dimensional physical models

Physical models enable researchers to systematically examine complex and dynamic mechanisms of underwater locomotion in ways that would be challenging with freely swimming animals. Previous research on undulatory locomotion, for example, has used rectangular flexible panels that are effectively two-dimensional as proxies for the propulsive surfaces of swimming fishes, but these bear little resemblance to the bodies of elongate eel-like swimming animals. In this paper we use a polyurethane rod (round cross-section) and bar (square cross-section) to represent the body of a swimming Pacific hagfish (Eptatretus stoutii). We actuated the rod and bar in both heave and pitch using a mechanical controller to generate a propulsive wave at frequencies between 0.5 and 2.5 Hz. We present data on (1) how kinematic swimming patterns change with driving frequency in these elongate fish-like models, (2) the thrust-generating capability of these simple models, (3) how forces and work done during propulsion compare between cross-sectional shapes, (4) the wake flow patterns in these swimming models using particle image velocimetry. We also contrast kinematic and hydrodynamic patterns produced by bar and rod models to comparable new experimental data on kinematics and wake flow patterns from freely swimming hagfish. Increasing the driving frequency of bar and rod models reduced trailing edge amplitude and wavelength, and above 2 Hz a nodal point appeared in the kinematic wave. Above 1 Hz, both the rod and bar generated net thrust, with the work per cycle reaching a minimum at 1.5 Hz, and the bar always requiring more work per cycle than the rod. Wake flow patterns generated by the swimming rod and bar included clearly visible lateral jets, but not the caudolaterally directed flows seen in the wakes from freely swimming hagfish.

[1]  George V Lauder,et al.  Undulatory locomotion of flexible foils as biomimetic models for understanding fish propulsion , 2014, Journal of Experimental Biology.

[2]  S. Kuratani,et al.  Identification of vertebra-like elements and their possible differentiation from sclerotomes in the hagfish , 2011, Nature communications.

[3]  R. Åke Norberg,et al.  Delta-wing function of webbed feet gives hydrodynamic lift for swimming propulsion in birds , 2003, Nature.

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

[5]  George V Lauder,et al.  Hydrodynamics of C-Start Escape Responses of Fish as Studied with Simple Physical Models. , 2015, Integrative and comparative biology.

[6]  George V. Lauder,et al.  Robotic Models for Studying Undulatory Locomotion in Fishes , 2011 .

[7]  Rajat Mittal,et al.  The effect of fin ray flexural rigidity on the propulsive forces generated by a biorobotic fish pectoral fin , 2010, Journal of Experimental Biology.

[8]  John O Dabiri,et al.  Suction-based propulsion as a basis for efficient animal swimming , 2015, Nature Communications.

[9]  John O. Dabiri,et al.  On the estimation of swimming and flying forces from wake measurements , 2005, Journal of Experimental Biology.

[10]  Lauder,et al.  Locomotor forces on a swimming fish: three-dimensional vortex wake dynamics quantified using digital particle image velocimetry. , 1999, The Journal of experimental biology.

[11]  Melina E. Hale,et al.  Functions of fish skin: flexural stiffness and steady swimming of longnose gar, Lepisosteus osseus , 1996, The Journal of experimental biology.

[12]  M. Koehl,et al.  Using physical models to study the gliding performance of extinct animals. , 2011, Integrative and comparative biology.

[13]  A. Cohen,et al.  Wake structures behind a swimming robotic lamprey with a passively flexible tail , 2012, Journal of Experimental Biology.

[14]  Chun Wai Liew,et al.  Go reconfigure: how fish change shape as they swim and evolve. , 2010, Integrative and comparative biology.

[15]  Sandra Nauwelaerts,et al.  Propulsive force calculations in swimming frogs II. Application of a vortex ring model to DPIV data , 2005, Journal of Experimental Biology.

[16]  Silas Alben Optimal flexibility in flapping appendages , 2008 .

[17]  B. Jayne Swimming in constricting (Elaphe g. guttata) and nonconstricting (Nerodia fasciata pictiventris) colubrid snakes , 1985 .

[18]  J. Dabiri Note on the induced Lagrangian drift and added-mass of a vortex , 2006, Journal of Fluid Mechanics.

[19]  Gillis,et al.  Anguilliform locomotion in an elongate salamander (Siren intermedia): effects of speed on axial undulatory movements , 1997, The Journal of experimental biology.

[20]  Thelma L. Williams,et al.  Strategies for swimming: explorations of the behaviour of a neuro-musculo-mechanical model of the lamprey , 2015, Biology Open.

[21]  T. Winegard,et al.  Diverse anguilliform swimming kinematics in Pacific hagfish (Eptatretus stoutii) and Atlantic hagfish (Myxine glutinosa) , 2015 .

[22]  J. H. Long Muscles, Elastic Energy, and the Dynamics of Body Stiffness in Swimming Eels' , 1998 .

[23]  J. Videler,et al.  How the body contributes to the wake in undulatory fish swimming: flow fields of a swimming eel (Anguilla anguilla). , 2001, The Journal of experimental biology.

[24]  M. Triantafyllou,et al.  Oscillating foils of high propulsive efficiency , 1998, Journal of Fluid Mechanics.

[25]  G. Lauder,et al.  The hydrodynamics of eel swimming , 2004, Journal of Experimental Biology.

[26]  SWIMMING FISH AND FISH-LIKE MODELS: THE HARMONIC STRUCTURE OF UNDULATORY WAVES SUGGESTS THAT FISH ACTIVELY TUNE THEIR BODIES , 1999 .

[27]  C. Richards,et al.  A bio-robotic platform for integrating internal and external mechanics during muscle-powered swimming , 2012, Bioinspiration & biomimetics.

[28]  C. A. Pell,et al.  Mechanical control of swimming speed: stiffness and axial wave form in undulating fish models , 1995, The Journal of experimental biology.

[29]  George V Lauder,et al.  Swimming near the substrate: a simple robotic model of stingray locomotion , 2013, Bioinspiration & biomimetics.

[30]  Eric D Tytell,et al.  The hydrodynamics of eel swimming II. Effect of swimming speed , 2004, Journal of Experimental Biology.

[31]  John H. Long,et al.  The Importance of Body Stiffness in Undulatory Propulsion , 1996 .

[32]  John O Dabiri,et al.  An algorithm to estimate unsteady and quasi-steady pressure fields from velocity field measurements , 2013, Journal of Experimental Biology.

[33]  Silas Alben,et al.  Optimal flexibility of a flapping appendage in an inviscid fluid , 2008, Journal of Fluid Mechanics.

[34]  T. Bohr,et al.  Vortex wakes of a flapping foil , 2009, Journal of Fluid Mechanics.

[35]  Yonatan Munk Kinematics of swimming garter snakes (Thamnophis sirtalis). , 2008, Comparative biochemistry and physiology. Part A, Molecular & integrative physiology.

[36]  R. Shine,et al.  Morphological adaptations to marine life in snakes , 2011, Journal of morphology.

[37]  Marcus Hultmark,et al.  Flowfield measurements in the wake of a robotic lamprey , 2007, Experiments in fluids.

[38]  George V. Lauder,et al.  Passive mechanical models of fish caudal fins: effects of shape and stiffness on self-propulsion , 2015, Bioinspiration & biomimetics.

[39]  Alexander J. Smits,et al.  Maximizing the efficiency of a flexible propulsor using experimental optimization , 2014, Journal of Fluid Mechanics.

[40]  G. Gillis,et al.  Environmental effects on undulatory locomotion in the American eel Anguilla rostrata: kinematics in water and on land , 1998 .

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

[42]  Peter A. Dewey,et al.  Hydrodynamic wake resonance as an underlying principle of efficient unsteady propulsion , 2011, Journal of Fluid Mechanics.

[43]  A. Cohen,et al.  Interactions between internal forces, body stiffness, and fluid environment in a neuromechanical model of lamprey swimming , 2010, Proceedings of the National Academy of Sciences.

[44]  G. Gillis Patterns of white muscle activity during terrestrial locomotion in the American eel (Anguilla rostrata). , 2000, The Journal of experimental biology.

[45]  L Wen,et al.  Hydrodynamic investigation of a self-propelled robotic fish based on a force-feedback control method , 2012, Bioinspiration & biomimetics.

[46]  George V Lauder,et al.  Flexible propulsors in ground effect , 2014, Bioinspiration & biomimetics.

[47]  G. Lauder,et al.  Escaping the flow: boundary layer use by the darter Etheostoma tetrazonum (Percidae) during benthic station holding , 2011, Journal of Experimental Biology.

[48]  S. Vogel Life in Moving Fluids: The Physical Biology of Flow , 1981 .

[49]  Kelsey N. Lucas,et al.  Effects of non-uniform stiffness on the swimming performance of a passively-flexing, fish-like foil model , 2015, Bioinspiration & biomimetics.

[50]  Peter A. Dewey,et al.  Scaling laws for the thrust production of flexible pitching panels , 2013, Journal of Fluid Mechanics.

[51]  P Holmes,et al.  An elastic rod model for anguilliform swimming , 2006, Journal of mathematical biology.

[52]  M. Koehl,et al.  Physical modelling in biomechanics. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[53]  M. A. MacIver,et al.  Mechanical properties of a bio-inspired robotic knifefish with an undulatory propulsor , 2011, Bioinspiration & biomimetics.

[54]  John H Long,et al.  The notochord of hagfish Myxine glutinosa: visco-elastic properties and mechanical functions during steady swimming. , 2002, The Journal of experimental biology.