Biaxial mechanical characterization of bat wing skin

The highly flexible and stretchable wing skin of bats, together with the skeletal structure and musculature, enables large changes in wing shape during flight. Such compliance distinguishes bat wings from those of all other flying animals. Although several studies have investigated the aerodynamics and kinematics of bats, few have examined the complex histology and mechanical response of the wing skin. This work presents the first biaxial characterization of the local deformation, mechanical properties, and fiber kinematics of bat wing skin. Analysis of these data has provided insight into the relationships among the structural morphology, mechanical properties, and functionality of wing skin. Large spatial variations in tissue deformation and non-negligible fiber strains in the cross-fiber direction for both chordwise and spanwise fibers indicate fibers should be modeled as two-dimensional elements. The macroscopic constitutive behavior was anisotropic and nonlinear, with very low spanwise and chordwise stiffness (hundreds of kilopascals) in the toe region of the stress-strain curve. The structural arrangement of the fibers and matrix facilitates a low energy mechanism for wing deployment and extension, and we fabricate examples of skins capturing this mechanism. We propose a comprehensive deformation map for the entire loading regime. The results of this work underscore the importance of biaxial field approaches for soft heterogeneous tissue, and provide a foundation for development of bio-inspired skins to probe the effects of the wing skin properties on aerodynamic performance.

[1]  S. Swartz,et al.  Polarized Image Correlation for Large Deformation Fiber Kinematics , 2013 .

[2]  Y Lanir,et al.  Two-dimensional mechanical properties of rabbit skin. I. Experimental system. , 1974, Journal of biomechanics.

[3]  John M. Gosline,et al.  Elastin as a random‐network elastomer: A mechanical and optical analysis of single elastin fibers , 1981 .

[4]  Stefan M Duma,et al.  Freezing affects the mechanical properties of bovine liver - biomed 2009. , 2009, Biomedical sciences instrumentation.

[5]  William R. Walsh,et al.  Mechanical properties of bat wing membrane skin , 1996 .

[6]  D. Vorp,et al.  The effects of aneurysm on the biaxial mechanical behavior of human abdominal aorta. , 2006, Journal of biomechanics.

[7]  Some mechanical properties of collagenous frameworks and their functional significance , 1965 .

[8]  John Lambros,et al.  Fluorescent image correlation for nanoscale deformation measurements. , 2006, Small.

[9]  V. Barocas,et al.  Effects of Freezing and Cryopreservation on the Mechanical Properties of Arteries , 2006, Annals of Biomedical Engineering.

[10]  W. Oates,et al.  Aerodynamic control of micro air vehicle wings using electroactive membranes , 2013 .

[11]  Yasuaki Seki,et al.  Biological materials: Structure and mechanical properties , 2008 .

[12]  Jorn A. Cheney,et al.  Membrane muscle function in the compliant wings of bats , 2014, Bioinspiration & biomimetics.

[13]  K Zanger,et al.  Mechanical properties of the skin of Xenopus laevis (Anura, Amphibia) , 1995, Journal of morphology.

[14]  R. Wootton,et al.  The hind wing of the desert locust (Schistocerca gregaria Forskål). II. Mechanical properties and functioning of the membrane. , 2000, The Journal of experimental biology.

[15]  Morton B. Brown,et al.  Robust Tests for the Equality of Variances , 1974 .

[16]  N. C. Goulbourne,et al.  A Structurally Motivated Constitutive Model for Bat Wing Skin , 2014 .

[17]  R. Bonser,et al.  Young's modulus varies with differential orientation of keratin in feathers. , 2003, Journal of structural biology.

[18]  E. Heikkinen,et al.  Mechanical properties of fast and slow skeletal muscle with special reference to collagen and endurance training. , 1984, Journal of biomechanics.

[19]  M. Coret,et al.  Mechanical characterization of liver capsule through uniaxial quasi-static tensile tests until failure. , 2010, Journal of biomechanics.

[20]  B Calvo,et al.  Passive nonlinear elastic behaviour of skeletal muscle: experimental results and model formulation. , 2010, Journal of biomechanics.

[21]  Gregory W. Reich,et al.  Bat-Inspired Flapping Flight , 2014 .

[22]  D Hawkins,et al.  Muscle and tendon force-length properties and their interactions in vivo. , 1997, Journal of biomechanics.

[23]  Gerhard A. Holzapfel,et al.  On planar biaxial tests for anisotropic nonlinearly elastic solids. A continuum mechanical framework , 2009 .

[24]  David J. Willis,et al.  Wing structure and the aerodynamic basis of flight in bats , 2007 .

[25]  Sounok Sen,et al.  Human annulus fibrosus material properties from biaxial testing and constitutive modeling are altered with degeneration , 2011, Biomechanics and Modeling in Mechanobiology.

[26]  W. F. Ranson,et al.  Applications of digital-image-correlation techniques to experimental mechanics , 1985 .

[27]  J. Clark,et al.  Elastic properties of single elastic fibers. , 1962, Journal of applied physiology.

[28]  Chris A. Van Ee,et al.  The effect of postmortem time and freezer storage on the mechanical properties of skeletal muscle , 1998 .

[29]  Patrick Zdunich,et al.  Development and Testing of the Mentor Flapping-wing Micro Air Vehicle , 2007 .

[30]  R. Shadwick,et al.  The structure and mechanical design of rhinoceros dermal armour. , 1992, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[31]  Bret Stanford,et al.  Aerodynamic Coefficients and Deformation Measurements on Flexible Micro Air Vehicle Wings , 2007 .

[32]  Yanping Cao,et al.  Wrinkling Phenomena in Neo-Hookean Film/Substrate Bilayers , 2012 .

[33]  Satyandra K. Gupta,et al.  Characterization of the Mechanics of Compliant Wing Designs for Flapping-Wing Miniature Air Vehicles , 2013 .

[34]  B. Gupta THE HISTOLOGY AND MUSCULATURE OF PLAGIOPATAGIUM IN BATS , 1967 .

[35]  Wei Sun,et al.  Multiaxial mechanical behavior of biological materials. , 2003, Annual review of biomedical engineering.

[36]  John G Flanagan,et al.  Biaxial mechanical testing of human sclera. , 2010, Journal of biomechanics.

[37]  R. Ogden,et al.  Hyperelastic modelling of arterial layers with distributed collagen fibre orientations , 2006, Journal of The Royal Society Interface.

[38]  Ulla M. Norberg,et al.  Bat wing structures important for aerodynamics and rigidity (Mammalia, chiroptera) , 1972, Zeitschrift für Morphologie der Tiere.

[39]  T. Vaughan Morphology and Flight Characteristics of Molossid Bats , 1966 .

[40]  Michael S. Sacks,et al.  Orthotropic Mechanical Properties of Chemically Treated Bovine Pericardium , 1998, Annals of Biomedical Engineering.

[41]  R. Bullen,et al.  Bat wing airfoil and planform structures relating to aerodynamic cleanliness , 2007 .

[42]  F H Silver,et al.  Viscoelastic behavior of human connective tissues: relative contribution of viscous and elastic components. , 1983, Connective tissue research.

[43]  M. Sacks,et al.  Biaxial mechanical properties of passive right ventricular free wall myocardium. , 1992, Journal of biomechanical engineering.

[44]  Roberto Albertani,et al.  In-Flight Wing-Membrane Strain Measurements on Bats , 2011 .

[45]  Kenneth Breuer,et al.  Aeromechanics of Membrane Wings with Implications for Animal Flight ArnoldSong, ∗ XiaodongTian, † EmilyIsraeli, ‡ RicardoGalvao, § KristinBishop, ¶ SharonSwartz, ∗∗ , 2008 .

[46]  Jian Chen,et al.  Quantifying the complexity of bat wing kinematics. , 2008, Journal of theoretical biology.

[47]  Sharon M. Swartz,et al.  A mixed Von Mises distribution for modeling soft biological tissues with two distributed fiber properties , 2012 .

[48]  Ulla M. Norberg,et al.  Moments of Inertia of Bat Wings and Body , 1991 .

[49]  Wei Sun,et al.  Effects of boundary conditions on the estimation of the planar biaxial mechanical properties of soft tissues. , 2005, Journal of biomechanical engineering.

[50]  B. Jayne,et al.  Mechanical behaviour of snake skin , 1988 .

[51]  F. Yin,et al.  Biaxial mechanical behavior of excised porcine mitral valve leaflets. , 1995, The American journal of physiology.

[52]  Wei Shyy,et al.  Flexible-wing-based Micro Air Vehicles , 2002 .

[53]  W. F. Ranson,et al.  Determination of displacements using an improved digital correlation method , 1983, Image Vis. Comput..

[54]  W. Peters,et al.  Digital Imaging Techniques In Experimental Stress Analysis , 1982 .

[55]  Kenton R Kaufman,et al.  Correlation between isometric force and intramuscular pressure in rabbit tibialis anterior muscle with an intact anterior compartment , 2009, Muscle & nerve.

[56]  S. Woo,et al.  Effects of postmortem storage by freezing on ligament tensile behavior. , 1986, Journal of biomechanics.

[57]  Holbrook Ka,et al.  A Collagen and Elastic Network in the Wing of the Bat , 1978 .

[58]  Y. Fung,et al.  Biomechanics: Mechanical Properties of Living Tissues , 1981 .

[59]  T. Best,et al.  The effect of stretch rate and activation state on skeletal muscle force in the anatomical range. , 2007, Clinical biomechanics.

[60]  Joseph W Bahlman,et al.  Design and characterization of a multi-articulated robotic bat wing , 2013, Bioinspiration & biomimetics.

[61]  King H. Yang,et al.  Mechanical characterization of porcine abdominal organs. , 2002, Stapp car crash journal.