Hierarchical structure and mechanical properties of nacre: a review

Nacre (known as mother of pearl) is the iridescent inner shell layer of some mollusks. Nacre is composed of 95 wt% aragonite (a crystallographic form of CaCO3) and 5 wt% organic materials (proteins and polysaccharides). It is well known that it exhibits high fracture toughness, much greater than that of monolithic aragonite, because of its ingenious structure. It also exhibits energy absorption properties. It has a complex hierarchical microarchitecture that spans multiple length scales from the nanoscale to the macroscale. It includes columnar architectures and sheet tiles, mineral bridges, polygonal nanograins, nanoasperities, plastic microbuckling, crack deflection, and interlocking bricks, which exhibit a remarkable combination of stiffness, low weight and strength. Nacre's special self-assembly characteristics have attracted interest from materials scientists for the development of laminated composite materials, molecular scale self-assembly and biomineralization. This paper reviews the characteristics of hierarchical structure and the mechanical properties of nacre that provide the desired properties, and the latest developments and biomimetic applications.

[1]  A. Colaço,et al.  The Influence of Hydrostatic Pressure on Shell Mineralization of Anodonta cygnea: A Comparative Study with a Hydrothermal Vent Bivalve Bathymodiolus azoricus , 2009 .

[2]  Bharat Bhushan,et al.  Biomimetics: lessons from nature–an overview , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[3]  S. Sinha,et al.  Scratch and indentation tests on seashells , 2009 .

[4]  Qunfeng Cheng,et al.  Layered nanocomposites inspired by the structure and mechanical properties of nacre. , 2012, Chemical Society reviews.

[5]  Yong Huang,et al.  Biomimetic structure design — a possible approach to change the brittleness of ceramics in nature☆ , 2000 .

[6]  Francois Barthelat,et al.  Biomimetics for next generation materials , 2007, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[7]  S. Weiner,et al.  Design strategies in mineralized biological materials , 1997 .

[8]  K. Katti,et al.  Experimental investigation of nanomechanics of the mineral-protein interface in nacre , 2008 .

[9]  Zhigang Suo,et al.  Deformation mechanisms in nacre , 2001 .

[10]  Doron Shilo,et al.  Nanometer‐Scale Mapping of Elastic Modules in Biogenic Composites: The Nacre of Mollusk Shells , 2010 .

[11]  Jingwei Zhang,et al.  Preparation and characterization of self-assembled organic–inorganic nacre-like nanocomposite thin films , 2004 .

[12]  Xiaodong Li,et al.  In situ observation of nanograin rotation and deformation in nacre. , 2006, Nano letters.

[13]  M. Fritz,et al.  The nacre protein perlucin nucleates growth of calcium carbonate crystals , 2003, Journal of microscopy.

[14]  J. Cartwright,et al.  The dynamics of nacre self-assembly , 2007, Journal of The Royal Society Interface.

[15]  Marc A. Meyers,et al.  Growth and structure in abalone shell , 2005 .

[16]  Zhangli Peng,et al.  Macromolecular structure and viscoelastic response of the organic framework of nacre in Haliotis rufescens: A perspective and overview , 2011 .

[17]  Yasuaki Seki,et al.  Biological materials: a materials science approach. , 2011, Journal of the mechanical behavior of biomedical materials.

[18]  K. Katti,et al.  Photoacoustic FTIR spectroscopic study of undisturbed nacre from red abalone. , 2006, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[19]  C. Brinker,et al.  Continuous self-assembly of organic–inorganic nanocomposite coatings that mimic nacre , 1998, Nature.

[20]  Horacio Dante Espinosa,et al.  An Experimental Investigation of Deformation and Fracture of Nacre–Mother of Pearl , 2007 .

[21]  Lei Jiang,et al.  Bio-inspired design of multiscale structures for function integration , 2011 .

[22]  M. Fritz,et al.  Gastropod nacre: structure, properties and growth--biological, chemical and physical basics. , 2011, Biophysical chemistry.

[23]  H. Wenk,et al.  Microstructure and texture patterns of mollusc shells , 1998 .

[24]  X. Bourrat,et al.  Thermal-Induced Wear Mechanisms of Sheet Nacre in Dry Friction , 2009 .

[25]  N. Yao,et al.  Crystal growth via spiral motion in abalone shell nacre , 2006 .

[26]  L. Zhang,et al.  High toughness silicon carbide/graphite laminar composite by slip casting , 1995 .

[27]  Michael Kube,et al.  Parallel evolution of nacre building gene sets in molluscs. , 2010, Molecular biology and evolution.

[28]  F. Barthelat,et al.  On the mechanics of mother-of-pearl: a key feature in the material hierarchical structure , 2007 .

[29]  J. Machado,et al.  Microstructural Characterization of Inner Shell Layers in the Freshwater Bivalve Anodonta cygnea , 2010 .

[30]  Peter Zioupos,et al.  Mechanical properties of nacre and highly mineralized bone , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[31]  G. Mayer,et al.  New toughening concepts for ceramic composites from rigid natural materials. , 2011, Journal of the mechanical behavior of biomedical materials.

[32]  I. Aksay,et al.  Biomimetic Processing of Ceramics and Ceramic-Metal Composites , 1990 .

[33]  M. Brendlé,et al.  Tribological behaviour of nacre—Influence of the environment on the elementary wear processes , 2006 .

[34]  C. Hedegaard.  SHELL STRUCTURES OF THE RECENT VETIGASTROPODA , 1997 .

[35]  Christine Ortiz,et al.  Bioinspired Structural Materials , 2008, Science.

[36]  Wenjian Wu,et al.  Evaporation-induced self-assembly of organic–inorganic ordered nanocomposite thin films that mimic nacre , 2006 .

[37]  Paul K. Hansma,et al.  Does Abalone Nacre Form by Heteroepitaxial Nucleation or by Growth through Mineral Bridges , 1997 .

[38]  Horacio Dante Espinosa,et al.  Mechanical properties of nacre constituents and their impact on mechanical performance , 2006 .

[39]  E. Zolotoyabko,et al.  Nacre in Mollusk Shells as a Multilayered Structure with Strain Gradient , 2009 .

[40]  Mario Viani,et al.  Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites , 1999, Nature.

[41]  Y. Bai,et al.  Microstructure and Characteristics in the Organic Matrix Layers of Nacre , 2002 .

[42]  Himadri S. Gupta,et al.  Deformation and Fracture Mechanisms of Bone and Nacre , 2011 .

[43]  Yuh J. Chao,et al.  Nanoscale Structural and Mechanical Characterization of a Natural Nanocomposite Material: The Shell of Red Abalone , 2004 .

[44]  Steve Weiner,et al.  Mollusk shell formation: mapping the distribution of organic matrix components underlying a single aragonitic tablet in nacre. , 2006, Journal of structural biology.

[45]  John D. Currey,et al.  Mechanical properties of mother of pearl in tension , 1977, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[46]  T. Sumitomo,et al.  The toughening mechanism of nacre and structural materials inspired by nacre , 2011, Science and technology of advanced materials.

[47]  João F Mano,et al.  Biomimetic design of materials and biomaterials inspired by the structure of nacre , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[48]  G. Mayer,et al.  Rigid Biological Systems as Models for Synthetic Composites , 2005, Science.

[49]  Zhiyong Tang,et al.  Nanostructured artificial nacre , 2003, Nature materials.

[50]  Marc André Meyers,et al.  Mechanical strength of abalone nacre: role of the soft organic layer. , 2008, Journal of the mechanical behavior of biomedical materials.

[51]  G. Mayer,et al.  New classes of tough composite materials—Lessons from natural rigid biological systems , 2006 .

[52]  白以龙,et al.  Mineral bridges of nacre and its effects , 2001 .

[54]  F. Ren,et al.  Study on microstructure and thermodynamics of nacre in mussel shell , 2009 .

[55]  João F. Mano,et al.  Mineralized structures in nature: Examples and inspirations for the design of new composite materials and biomaterials , 2010 .

[56]  Michael Rubner.  Materials science: Synthetic sea shell , 2003, Nature.

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

[58]  Horacio Dante Espinosa,et al.  An elasto-viscoplastic interface model for investigating the constitutive behavior of nacre , 2007 .

[59]  Jean-Marie Rouillard,et al.  Layer-by-layer assembly of nacre-like nanostructured composites with antimicrobial properties. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[60]  F. Shi,et al.  Artificial Nacre by Alternating Preparation of Layer-by-Layer Polymer Films and CaCO3 Strata , 2007 .

[61]  Stephen Mann,et al.  Critical Transitions in the Biofabrication of Abalone Shells and Flat Pearls , 1996 .

[62]  K. Katti,et al.  Nanomechanical properties of nacre , 2006 .

[63]  M. Meyers,et al.  Interfacial shear strength in abalone nacre. , 2009, Journal of the mechanical behavior of biomedical materials.

[64]  M. Meyers,et al.  The growth of nacre in the abalone shell. , 2008, Acta biomaterialia.

[65]  Yong Huang,et al.  An efficient biomimetic process for fabrication of artificial nacre with ordered-nanostructure , 2008 .

[66]  A. Waas,et al.  Ultrastrong and Stiff Layered Polymer Nanocomposites , 2007, Science.

[67]  V. Tomar,et al.  Role of Molecular Level Interfacial Forces in Hard Biomaterial Mechanics: A Review , 2010, Annals of Biomedical Engineering.

[68]  A K Soh,et al.  Structural and mechanical properties of the organic matrix layers of nacre. , 2003, Biomaterials.

[69]  K. Vecchio,et al.  Quasi-static and dynamic mechanical response of Strombus gigas (conch) shells , 2001 .

[70]  Mehmet Sarikaya,et al.  Mechanical Property-Microstructural Relationships in Abalone Shell , 1989 .

[71]  Huajian Gao,et al.  Application of Fracture Mechanics Concepts to Hierarchical Biomechanics of Bone and Bone-like Materials , 2006 .

[72]  Yasuaki Seki,et al.  The role of organic intertile layer in abalone nacre , 2009 .

[73]  R. Ritchie,et al.  Tough, Bio-Inspired Hybrid Materials , 2008, Science.

[74]  Eduardo Saiz,et al.  A novel biomimetic approach to the design of high-performance ceramic–metal composites , 2010, Journal of The Royal Society Interface.

[75]  Ludwig J. Gauckler,et al.  Bioinspired Design and Assembly of Platelet Reinforced Polymer Films , 2008, Science.

[76]  D. Pasini,et al.  Multiscale mechanics and optimization of gastropod shells , 2011 .

[77]  B. Lawn,et al.  In Situ Processing of Silicon Carbide Layer Structures , 1995 .

[78]  Zhiyong Tang,et al.  Can nature's design be improved upon? High strength, transparent nacre-like nanocomposites with double network of sacrificial cross links. , 2008, The journal of physical chemistry. B.

[79]  X. Bourrat,et al.  Sheet nacre growth mechanism: a Voronoi model. , 2005, Journal of structural biology.

[80]  X. Bourrat,et al.  Mechanical properties of the elemental nanocomponents of nacre structure , 2010 .

[81]  F. Cui,et al.  Observations of damage morphologies in nacre during deformation and fracture , 1995 .

[82]  K. Katti,et al.  Platelet interlocks are the key to toughness and strength in nacre , 2005 .

[83]  K. Katti,et al.  Nature of water in nacre: a 2D Fourier transform infrared spectroscopic study. , 2007, Spectrochimica acta. Part A, Molecular and biomolecular spectroscopy.

[84]  L. Xie,et al.  Molecular approaches to understand biomineralization of shell nacreous layer. , 2011, Progress in molecular and subcellular biology.

[85]  Julyan H E Cartwright,et al.  Mineral bridges in nacre. , 2011, Journal of structural biology.

[86]  Georg Grathwohl,et al.  On the nature of the stiffness of nacre , 2008 .

[87]  A. P. Jackson,et al.  The mechanical design of nacre , 1988, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[88]  Buddy D Ratner,et al.  Biomaterials: where we have been and where we are going. , 2004, Annual review of biomedical engineering.

[89]  Robert M. Panas,et al.  Nanoscale Morphology and Indentation of Individual Nacre Tablets from the Gastropod Mollusc Trochus Niloticus , 2005 .

[90]  K. Katti,et al.  Modeling microarchitecture and mechanical behavior of nacre using 3D finite element techniques Part I Elastic properties , 2001 .

[91]  Jiyu Sun,et al.  Fracture toughness properties of three different biomaterials measured by nanoindentation , 2007 .

[92]  Marc A. Meyers,et al.  Quasi-static and dynamic mechanical response of Haliotis rufescens (abalone) shells , 2000 .

[93]  Wei-Han Huang,et al.  Bioinspired Assembly of Colloidal Nanoplatelets by Electric Field , 2009 .

[94]  P. de Gennes,et al.  Why is nacre strong? Elastic theory and fracture mechanics for biocomposites with stratified structures , 2001 .

[95]  Eduardo Saiz,et al.  Freezing as a Path to Build Complex Composites , 2006, Science.

[96]  Daniel Chateigner,et al.  Mollusc shell microstructures and crystallographic textures , 2000 .

[97]  Zhigang Suo,et al.  Model for the robust mechanical behavior of nacre , 2001 .

[98]  I. Aksay,et al.  Structure-Mechanical Property Relationships In A Biological Ceramic-Polymer Composite: Nacre , 1991 .

[99]  Francois Barthelat,et al.  Nacre from mollusk shells: a model for high-performance structural materials , 2010, Bioinspiration & biomimetics.

[100]  R. Spolenak,et al.  The influence of internal length scales on mechanical properties in natural nanocomposites: a comparative study on inner layers of seashells. , 2008, Acta biomaterialia.

[101]  M. Sarikaya,et al.  An introduction to biomimetics: A structural viewpoint , 1994, Microscopy research and technique.

[102]  R. Asaro,et al.  Macromolecular structure of the organic framework of nacre in Haliotis rufescens: implications for growth and mechanical behavior. , 2008, Journal of structural biology.

[103]  M. Willinger,et al.  The key role of the surface membrane in why gastropod nacre grows in towers , 2009, Proceedings of the National Academy of Sciences.

[104]  Andreas Walther,et al.  Supramolecular control of stiffness and strength in lightweight high-performance nacre-mimetic paper with fire-shielding properties. , 2010, Angewandte Chemie.

[105]  K. Katti,et al.  3D finite element modeling of mechanical response in nacre-based hybrid nanocomposites , 2001 .

[106]  Fan Song,et al.  Effect of a negative Poisson ratio in the tension of ceramics. , 2008, Physical review letters.

[107]  K. Katti,et al.  Dynamic nanomechanical response of nacre , 2006 .

[108]  G. Schneider,et al.  On the mechanical properties of hierarchically structured biological materials. , 2010, Biomaterials.

[109]  Fu Song,et al.  Numerical investigation of the adverse effect of wind on the heat transfer performance of two natural draft cooling towers in tandem arrangement , 2001 .

[110]  J. Cartwright,et al.  Spiral and target patterns in bivalve nacre manifest a natural excitable medium from layer growth of a biological liquid crystal , 2009, Proceedings of the National Academy of Sciences.

[111]  C. Baudín,et al.  Design and processing of a ceramic laminate with high toughness and strong interfaces , 2009 .

[112]  Stephen Mann,et al.  Flat pearls from biofabrication of organized composites on inorganic substrates , 1994, Nature.

[113]  K. Katti,et al.  Modeling mechanical responses in a laminated biocomposite , 2005 .