Material properties of the skin of the Kenyan sand boa Gongylophis colubrinus (Squamata, Boidae)

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.

[1]  A. Brush,et al.  The molecular heterogeneity and diversity of reptilian keratins , 1979, Journal of Molecular Evolution.

[2]  E. Fuchs,et al.  Type I and type II keratins have evolved from lower eukaryotes to form the epidermal intermediate filaments in mammalian skin. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[3]  L. Alibardi,et al.  Cytochemical, biochemical and molecular aspects of the process of keratinization in the epidermis of reptilian scales. , 2006, Progress in histochemistry and cytochemistry.

[4]  N. Alexander.  Comparison of α and β keratin in reptiles , 1970, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[5]  W. James,et al.  Keratin and keratinization. , 1994, Journal of the American Academy of Dermatology.

[6]  V. Toffolo,et al.  Isolation of a mRNA encoding a glycine‐proline–rich β‐keratin expressed in the regenerating epidermis of lizard , 2005, Developmental dynamics : an official publication of the American Association of Anatomists.

[7]  Lisa A. Pruitt,et al.  Nanoindentation of biological materials , 2006 .

[8]  S. Weiner,et al.  Strain-structure relations in human teeth using Moiré fringes. , 1997, Journal of biomechanics.

[9]  J. Deuschle.  Mechanics of soft polymer indentation , 2008 .

[10]  S. Gorb,et al.  Local mechanical properties of the head articulation cuticle in the beetle Pachnoda marginata (Coleoptera, Scarabaeidae) , 2006, Journal of Experimental Biology.

[11]  E. Williams,et al.  Scanning electron microscopy of changes in epidermal structure occurring during the shedding cycle in squamate reptiles , 1988, Journal of morphology.

[12]  R. Fraser,et al.  Molecular structure and mechanical properties of keratins. , 1980, Symposia of the Society for Experimental Biology.

[13]  G. Rogers,et al.  Feather Keratin: Composition, Structure and Biogenesis , 1986 .

[14]  Stanislav N. Gorb,et al.  Exploring biological surfaces by nanoindentation , 2004 .

[15]  Stanislav N. Gorb,et al.  Towards a micromechanical understanding of biological surface devices , 2002 .

[16]  Christopher Mattison,et al.  The encyclopedia of snakes , 1995 .

[17]  B. Tandler,et al.  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 , 1998, Journal of morphology.

[18]  G. Pharr,et al.  Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology , 2004 .

[19]  E. Arzt,et al.  Surface detection in nanoindentation of soft polymers , 2007 .

[20]  L. Alibardi,et al.  Immunological characterization and fine localization of a lizard beta-keratin. , 2006, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[21]  R. Bonser,et al.  The Young's modulus of feather keratin , 1995, The Journal of experimental biology.

[22]  L. Alibardi,et al.  Immunocytochemical analysis of beta keratins in the epidermis of chelonians, lepidosaurians, and archosaurians. , 2002, The Journal of experimental zoology.

[23]  A. Lettington.  Applications of diamond-like carbon thin films , 1993, Philosophical Transactions of the Royal Society of London. Series A: Physical and Engineering Sciences.

[24]  A. R. Ennos,et al.  The fracture properties and mechanical design of human fingernails , 2004, Journal of Experimental Biology.

[25]  B. Filshie,et al.  A N E L E C T R O N , 2022 .

[26]  A. Schermer,et al.  Patterns of keratin expression define distinct pathways of epithelial development and differentiation. , 1987, Current topics in developmental biology.

[27]  R. Sawyer,et al.  Development and keratinization of the epidermis in the common lizard, Anolis carolinensis. , 1987, The Journal of experimental zoology.

[28]  J. Bereiter-Hahn,et al.  Biology of the integument. 2. Vertebrates. , 1986 .

[29]  Travis Glenn,et al.  The Expression of Beta (β) Keratins in the Epidermal Appendages of Reptiles and Birds1 , 2000 .

[30]  Mehmet Sarikaya,et al.  Nano-mechanical properties profiles across dentin–enamel junction of human incisor teeth , 1999 .

[31]  T. Fusayama,et al.  Effect of Pulpectomy on Dentin Hardness , 1969, Journal of dental research.

[32]  S. Gorb,et al.  Mechanical properties of a single gecko seta , 2008 .

[33]  Agnes Weth,et al.  The sandfish’s skin: Morphology, chemistry and reconstruction , 2007 .

[34]  L. Landmann.  Keratin formation and barrier mechanisms in the epidermis of Natrix natrix (Reptilia: Serpentes): An ultrastructural study , 1979, Journal of morphology.

[35]  Zhou Zhongrong,et al.  On the friction and wear behaviour of human tooth enamel and dentin , 2003 .

[36]  W. Epstein,et al.  KERATINIZATION , 1976, International journal of dermatology.

[37]  A. F. Bennett,et al.  A Scaleless Snake: Tests of the Role of Reptilian Scales in Water Loss and Heat Transfer , 1972 .

[38]  Goslar Hg.  Skin shedding of snakes. I. Histological and topochemical studies on the skin of Natrix natrix L. during the phases of the normal skin shedding cycle , 1958 .

[39]  R. Bonser.  The elastic properties of wing and contour feather keratin from the Ostrich Struthio camelus , 2008 .

[40]  A. Mittal,et al.  Histochemistry of the epidermis of the Chequered water snake Natrix piscator (Colubridae, Squamata) , 2009 .

[41]  Zhihui Xu,et al.  Nanoindentation on diamond-like carbon and alumina coatings , 2002 .

[42]  L. Alibardi,et al.  Alpha- and beta-keratins of the snake epidermis. , 2007, Zoology.

[43]  M. Ashby,et al.  Cellular solids: Structure & properties , 1988 .

[44]  L. Alibardi,et al.  Immunolocalization and characterization of beta-keratins in growing epidermis of chelonians. , 2006, Tissue & cell.

[45]  Bharat Bhushan,et al.  Nanomechanical characterization of human hair using nanoindentation and SEM. , 2005, Ultramicroscopy.

[46]  E Romberg,et al.  Indentation Damage and Mechanical Properties of Human Enamel and Dentin , 1998, Journal of dental research.

[47]  G. Pharr,et al.  An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments , 1992 .

[48]  D. Lyons,et al.  Preliminary work on the development of a novel detection method for osteoporosis , 2007, Journal of materials science. Materials in medicine.

[49]  J. Bereiter-Hahn,et al.  Biology of the Integument , 1984, Springer Berlin Heidelberg.

[50]  P. Maderson,et al.  Morphological and biophysical identification of fibrous proteins in the amniote epidermis. , 1970, The Journal of experimental zoology.