In contrast to the majority of inorganic or artificial materials, there is no ideal long-range ordering of structures on the surface in biological systems. Local symmetry of the ordering on biological surfaces is also often broken. In the present paper, the particular symmetry violation was analyzed for dimple-like nano-pattern on the belly scales of the skin of the pythonid snake Morelia viridis using correlation analysis and statistics of the distances between individual nanostructures. The results of the analysis performed on M. viridis were compared with a well-studied nano-nipple pattern on the eye of the sphingid moth Manduca sexta, used as a reference. The analysis revealed non-random, but very specific symmetry violation. In the case of the moth eye, the nano-nipple arrangement forms a set of domains, while in the case of the snake skin, the nano-dimples arrangement resembles an ordering of particles (molecules) in amorphous (glass) state. The function of the nano-dimples arrangement may be to provide both friction and strength isotropy of the skin. A simple model is suggested, which provides the results almost perfectly coinciding with the experimental ones. Possible mechanisms of the appearance of the above nano-formations are discussed.
Power Spectrum Hexagonal Arrangement Symmetry Violation Distance Histogram Snake Skin
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Snake skin material was kindly provided by Dr. Guido Westhoff (Tierpark Hagenbeck, Hamburg, Germany). This study was supported by the SPP 1420 priority program of the German Science Foundation (DFG) “Biomimetic Materials Research: Functionality by Hierarchical Structuring of Materials” (Project GO 995/9-2) to S.N.G. and COST STSM ECOST-STSM-MP1303-010216-071056.
Correlation analysis of the structure distribution on ommatidium surface in the moth Manduca sexta within a moving circular area. For detailed information see Fig. 1. Supplementary material 1 (AVI 1974 kb)
“Frozen dynamics” simulation of nano-dimple distribution on the skin scales in Morelia viridis. Corresponding correlation analysis is provided. For detailed information see Figs. 4 and 5. Supplementary material 2 (AVI 610 kb)
M. Baum, L. Heepe, S.N. Gorb, Friction behavior of a microstructured polymer surface inspired by snake skin. Beilstein J. Nanotechnol. 5, 83–97 (2014)CrossRefGoogle Scholar
R.A. Berthé, G. Westhoff, H. Bleckmann, S.N. Gorb, Surface structure and frictional properties of the skin of the Amazon tree boa Corallus hortulanus (Squamata, Boidae). J. Comp. Physiol. A 195, 311–318 (2009)CrossRefGoogle Scholar
M.-C.G. Klein, J.K. Deuschle, S.N. Gorb, Material properties of the skin of the Kenyan sand boa Gangylophis colubrinus (Squamata, Boidae). J. Comp. Physiol. A 196, 659–668 (2010)CrossRefGoogle Scholar
M.-C.G. Klein, S.N. Gorb, Epidermis architecture and material properties of the skin of four snake species. J. R. Soc. Interface 9, 3140–3155 (2012)CrossRefGoogle Scholar
M.-C.G. Klein, S.N. Gorb, Ultrastructure and wear patterns of the ventral epidermis of four snake species (Squamata, Serpentes). Zoology 117(5), 295–314 (2014)CrossRefGoogle Scholar
M. Varenberg, G. Halperin, I. Etsion, Different aspects of the role of wear debris in fretting wear. Wear 252, 902–910 (2002)CrossRefGoogle Scholar
H. Peisker, S.N. Gorb, Always on the bright side of life: anti-adhesive properties of insect ommatidia grating. J. Exp. Biol. 213, 3457–3462 (2010)CrossRefGoogle Scholar
D.G. Stavenga, S. Foletti, G. Palasantzas, K. Arikawa, Light on the moth-eye corneal nipple array of butterflies. Proc. R. Soc. Lond. B Biol. Sci. 273, 661–667 (2006)CrossRefGoogle Scholar
A. Blagodatski, A. Sergeevb, M. Kryuchkova, Y. Lopatinad, V.L. Katanaev, Diverse set of Turing nanopatterns coat corneae across insect lineages. PNAS 112(34), 10750–10755 (2015)ADSCrossRefGoogle Scholar
R. Li, B. Bowerman, Symmetry breaking in biology. Cold Spring Harb. Perspect. Biol. 2(3), a003475 (2010)CrossRefGoogle Scholar
R.O. Prum, R.H. Torres, Structural colouration of avian skin: convergent evolution of coherently scattering dermal collagen arrays. J. Exp. Biol. 206, 2409–2429 (2003)CrossRefGoogle Scholar
C.G. Bernhard, W.H. Miller, A corneal nipple pattern in insect compound eyes. Acta Physiol. Scand. 56, 385–386 (1962)CrossRefGoogle Scholar
G.W. Miskimen, N.L. Rodriguez, Structure and functional aspects of the Scotopic compound eye of the sugarcane borer moth. J. Morphol. 168, 73–84 (1981)CrossRefGoogle Scholar
J. Stalleicken, T. Labhart, H. Mouritsen, Physiological characterization of the compound eye in monarch butterflies with focus on the dorsal rim area. J. Comp. Physiol. A 192, 321–331 (2006)CrossRefGoogle Scholar
K.C. Lee, U. Erb, Remarkable crystal and defect structures in butterfly eye nano-nipple arrays. Arthropod Struct. Dev. 44, 587–594 (2015)CrossRefGoogle Scholar
A. Sergeev, A.A. Timchenko, M. Kryuchkov, A. Blagodatski, G.A. Enin, V.L. Katanaev, Origin of order in bionanostructures. RSC Adv. 5, 63521–63527 (2015)CrossRefGoogle Scholar
C.V. Thompson, Structure evolution during processing of polycrystalline films. Ann Rev. Mater. Sci. 30, 159–190 (2000)ADSCrossRefGoogle Scholar