Abstract
On the basis of structural data, it has been previously assumed that the integument of snakes consists of a hard, robust, inflexible outer surface (Oberhäutchen and β-layer) and soft, flexible inner layers (α-layers). The aim of this study was to compare material properties of the outer and inner scale layers of the exuvium of Gongylophis colubrinus, to relate the structure of the snake integument to its mechanical properties. The nanoindentation experiments have demonstrated that the outer scale layers are harder, and have a higher effective elastic modulus than the inner scale layers. The results obtained provide strong evidence about the presence of a gradient in the material properties of the snake integument. The possible functional significance of this gradient is discussed here as a feature minimizing damage to the integument during sliding locomotion on an abrasive surface, such as sand.
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References
Alexander NJ (1970) Comparison of α and β keratin in reptiles. Z Zellforsch 110:153–165
Alibardi L, Sawyer RH (2002) Immunocytochemical analysis of beta keratins in the epidermis of chelonians, lepidosaurians, and archosaurians. J Exp Zool 293:27–38
Alibardi L, Toni M (2006a) Cytochemical, biochemical and molecular aspects of the process of keratinization in the epidermis of reptilian scales. Prog Histochem Cytochem 40:73–134
Alibardi L, Toni M (2006b) Immunological characterization and fine localization of lizard beta-keratin. J Exp Zool 306B:528–538
Alibardi L, Toni M (2006c) Immunolocalization and characterization of beta-keratins in growing epidermis of chelonians. Tissue Cell 38:53–63
Arzt E, Enders S, Gorb S (2002) Towards a micromechanical understanding of biological surface devices. Z Metallkunde 93:345–351
Astbury WT, Bell FO (1939) X-ray data on the structure of natural fibres and other bodies of high molecular weight. Tabulae Biol 17:90–112
Baden HP, Maderson PFA (1970) Morphological and biophysical identification of fibrous proteins in the amniote epidermis. J Exp Zool 174:225–232
Banerjee TK, Mittal AK (1978) Histochemistry of the epidermis of the checkered water snake Natrix piscator (Colubridae, Squamata). J Zool 185:415–435
Barbakadze N, Enders S, Gorb S, Arzt E (2006) Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). J Exp Biol 209:722–730
Baumgartner W, Saxe F, Weth A, Hajas D, Sigumonrong D, Emmerlich J, Singheiser M, Böhme W, Schneider JM (2007) The sandfish’s skin: morphology, chemistry and reconstruction. J Bionic Eng 4:1–9
Bonser RHC (2001) The elastic properties of wing and contour feather keratin from the Ostrich Struthio camelus. Ibis 143:144–145
Bonser RHC, Purslow PP (1995) The Young’s modulus of feather keratin. J Exp Biol 198:1029–1033
Carver WE, Sawyer RH (1987) Development and keratinization of the epidermis in the common lizard, Anolis carolinensis. J Exp Zool 243:435–443
Dalla Valle L, Toffolo V, Belvedere P, Alibardi L (2005) Isolation of mRNA encoding a glycine-proline-rich β-keratin expressed in the regenerating epidermis of lizard. Dev Dynam 234:934–947
Deuschle J (2008) Mechanics of soft polymer indentation. Dissertation, Max Planck Institute for Metals Research Stuttgart and Institute for Metallography of the University of Stuttgart
Deuschle J, Enders S, Arzt E (2007) Surface detection in nanoindentation of soft polymers. J Mater Res 22:3107–3119
Ebenstein DM, Pruitt LA (2006) Nanoindentation of biological materials. Nano Today 1:26–33
Enders S, Barbakadze N, Gorb SN, Arzt E (2004) Exploring biological surfaces by nanoindentation. J Mater Res 19:880–887
Farren L, Shayler S, Ennos AR (2004) The fracture properties and mechanical design of human fingernails. J Exp Biol 207:735–741
Filshie BK, Rogers GE (1962) An electron microscope study of the fine structure of feather keratin. J Biophys Biochem Cytol 13:1–12
Fong H, Sarikaya M, White SN, Snead ML (2000) Nano-mechanical properties profiles across dentin–enamel junction of human incisor teeth. Mat Sci Eng 7:119–128
Fraser RDB, MacRae TP (1980) Molecular structure and mechanical properties of keratin. In: Vincent JFV, Currey JD (eds) The mechanical properties of biological materials. Symposia of the Society for Experimental Biology
Furch E, Marchuk D (1983) Type I and type II keratins have evolved from lower eukaryotes to from the epidermal intermediate filaments in mammalian skin. Proc Natl Acad Sci USA 80:5857–5861
Fusayama T, Maeda T (1968) Effect of pulpectomy on dentin hardness. J Dent Res 48:452–460
Gibson LJ, Ashby MF (1988) Cellular solids: structures and properties. Pergamon Press, New York
Goslar HG (1958) Beiträge zum Häutungsvorgang der Schlangen. Acta Histochem 5:182–212
Gregg K, Rogers GE (1986) Feather keratins: composition, structure and biogenesis. In: Bereither-Hahn J, Matoltsy GA, Sylvia-Richards K (eds) Biology of the integument: vertebrates, vol 2. Springer, New York, pp 666–694
Huber G, Orso S, Spolenak R, Wegst UGK, Enders S, Gorb SN, Arzt E (2008) Mechanical properties of a single gecko seta. Int J Mater Res 2008:1113–1118
Irish FJ, Williams EE, Seling E (1988) Scanning electron microscopy of changes in the epidermal structure occurring during the shedding cycle in squamate reptiles. J Morphol 197:105–126
Landmann L (1979) Keratin formation and barrier mechanisms in the epidermis of Natrix natrix (Reptilia: Serpentes): an ultrastructural study. J Morphol 162:93–126
Landmann L (1986) Biology of the integument. In: Bereither-Hahn J, Matoltsy GA, Sylvia-Richards K (eds) The skin of reptiles, Chap 9: Epidermis and dermis. Springer, Heidelberg, pp 150–185
Lettington AH (1998) Applications of diamond-like carbon thin films. Carbon 36:555–560
Licht P, Bennett AF (1972) A scaleless snake: tests of the role of reptilian scales in water loss and heat transfer. Copeia 4:702–707
Maderson PFA (1964) The skin of lizards and snakes. B J Herpet 3:151–154
Maderson PFA, Rabinowitz B, Tandler B, Alibardi L (1998) Ultrastructural contributions to an understanding of the cellular mechanisms involved in lizard skin shedding with comments on the function and evolution of a unique lepidosaurian phenomenon. J Morphol 236:1–24
Matoltsy AG (1976) Keratinization. J Invest Dermatol 67:20–25
Mattison C (1995) The encyclopedia of snakes. Cassel & Co, London
Mercer EH (1961) Keratin and keratinization. Pergamon Press, Inc, Oxford
Moran P, Towler MR, Chowdhury S, Saunders J, German MJ, Lawson NS, Pollock HM, Pillay L, Lyons D (2007) Preliminary work on the development of a novel detection method for osteoporosis. J Mater Sci 18:969–974
O’Guin WM, Galvin S, Schermer A, Sun TT (1987) Patterns of keratin expression define distinct pathways of epithelial development and differentiation. Curr Top Dev Biol 22:97–125
Oliver WC, Pharr GM (1992) An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res 7:1564–1583
Oliver WC, Pharr GM (2004) Measurement of hardness and elastic modulus by instrumented indentation: advances in understanding and refinements in methodology. J Mater Res 19:3–20
Rechenberg I, El Khyari AR (2004) Der Sandskink der Sahara—Vorbild für Reibungs- und Verschleißminderung. http://www.bionik.tuberlin.de/institute/festo04.pdf,Berlin
Sawyer RH, Glenn T, French JO, Mays B, Shames RB, Barnes GL, Rhodes W, Ishikawa Y (2000) The expression of beta keratins in the epidermal appendages of reptiles and birds. Am Zool 40:530–539
Toni M, Alibardi L (2007) Alpha- and beta-keratin of the snake epidermis. Zoology 110:41–47
Wang RZ, Weiner S (1998) Strain-structure relations in human teeth using Moire fringes. J Biomech 31:135–141
Wei G, Bhushan B, Torgerson PM (2005) Nanomechanical characterization of human hair using nanoindentation and SEM, vol 105. Elsevier, Amsterdam, pp 248–266
Wyld JA, Brush AH (1979) The molecular heterogeneity and diversity of reptilian keratins. J Mol Evol 12:331–347
Xu Z, Rowcliffe D (2002) Nanoindenation on diamond-like carbon and alumina coatings. Surf Coat Technol 161:44–51
Xu HHK, Smith DT, Jahanmir S, Romber E, Kelly JR, Thompson VP, Rekow ED (1998) Indentation damage and mechanical properties of human enamel and dentin. J Dent Res 77:472–480
Zheng J, Zhou ZR, Zhang J, Li H, Yu HY (2003) On the friction and wear behaviour of human tooth enamel and dentin, vol 255. Elsevier, Amsterdam, pp 967–974
Acknowledgments
Dr. Guido Westhoff (University of Bonn, Germany) provided frozen snakes and valuable comments on snake biology. S.G. was supported in this work by the Federal Ministry of Education, Science and Technology, Germany (BMBF project Biona 01RB0812A). Animal care for the live G. colubrinus was provided by M.-C. Klein. The experiments comply with the “Principles of animal care”, publication no. 86–23, revised 1985 of the National Institute of Health and also with the current laws of Germany. Figure 1a was reproduced/adapted with permission from The Journal of Experimental Biology, Barbakadze N, Enders S, Gorb S, Arzt E (2006) Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae). J Exp Biol 209:722–730. doi:10.1242/jeb.0206.
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Klein, MC.G., Deuschle, J.K. & Gorb, S.N. Material properties of the skin of the Kenyan sand boa Gongylophis colubrinus (Squamata, Boidae). J Comp Physiol A 196, 659–668 (2010). https://doi.org/10.1007/s00359-010-0556-y
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DOI: https://doi.org/10.1007/s00359-010-0556-y