Mechanical properties of crossed-lamellar structures in biological shells: A review.

The self-fabrication of materials in nature offers an alternate and powerful solution towards the grand challenge of designing advanced structural materials, where strength and toughness are always mutually exclusive. Crossed-lamellar structures are the most common microstructures in mollusks that are composed of aragonites and a small amount of organic materials. Such a distinctive composite structure has a fracture toughness being much higher than that of pure carbonate mineral. These structures exhibiting complex hierarchical microarchitectures that span several sub-level lamellae from microscale down to nanoscale, can be grouped into two types, i.e., platelet-like and fiber-like crossed-lamellar structures based on the shapes of basic building blocks. It has been demonstrated that these structures have a great potential to strengthen themselves during deformation. The observed underlying toughening mechanisms include microcracking, channel cracking, interlocking, uncracked-ligament bridging, aragonite fiber bridging, crack deflection and zig-zag, etc., which play vital roles in enhancing the fracture resistance of shells with the crossed-lamellar structures. The exploration and utilization of these important toughening mechanisms have attracted keen interests of materials scientists since they pave the way for the development of bio-inspired advanced composite materials for load-bearing structural applications. This article is aimed to review the characteristics of hierarchical structures and the mechanical properties of two kinds of crossed-lamellar structures, and further summarize the latest advances and biomimetic applications based on the unique crossed-lamellar structures.

[1]  S. Keten,et al.  Stiffness Enhancement in Nacre-Inspired Nanocomposites due to Nanoconfinement , 2015, Scientific Reports.

[2]  E. G. Boulding.  Crab-resistant features of shells of burrowing bivalves: decreasing vulnerability by increasing handling time , 1984 .

[3]  M. Labarbera,et al.  FATIGUE DAMAGE: REPEATED LOADING ENABLES CRABS TO OPEN LARGER BIVALVES. , 1986, The Biological bulletin.

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

[5]  I Corni,et al.  A review of experimental techniques to produce a nacre-like structure , 2012, Bioinspiration & biomimetics.

[6]  Sridhar Santhanam,et al.  Analysis of toughening mechanisms in the Strombus gigas shell. , 2015, Journal of the mechanical behavior of biomedical materials.

[7]  Toshihiro Nakamura,et al.  Crystalline arrangement and nanostructure of aragonitic crossed lamellar layers of the Meretrix lusoria shell. , 2010, Zoology.

[8]  Luc Ortlieb,et al.  Microstructure, nanostructure and composition of the shell of Concholepas concholepas (Gastropoda, Muricidae) , 2003 .

[9]  Jian-Guo Wang,et al.  Laminated microstructure of Bivalva shell and research of biomimetic ceramic/polymer composite , 2004 .

[10]  Bharat Bhushan,et al.  Biomimetics: Bioinspired Hierarchical-Structured Surfaces for Green Science and Technology , 2012 .

[11]  M. Meyers,et al.  Structural characterization and mechanical behavior of a bivalve shell (Saxidomus purpuratus) , 2011 .

[12]  J. Bonarski,et al.  Irregularities of crystallographic orientation and residual stresses in the crossed-lamellar shell as a natural functionally graded material , 2015, Journal of The Royal Society Interface.

[13]  H. Nagasawa,et al.  Crystallographic characterization of the crossed lamellar structure in the bivalve Meretrix lamarckii using electron beam techniques. , 2011, Journal of structural biology.

[14]  Geerat J. Vermeij,et al.  A Natural History of Shells , 2021 .

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

[16]  S. Weiner,et al.  Control and Design Principles in Biological Mineralization , 1992 .

[17]  John D. Currey,et al.  Further studies on the mechanical properties of mollusc shell material , 2009 .

[18]  E. Zolotoyabko,et al.  Microstructure of natural plywood-like ceramics: a study by high-resolution electron microscopy and energy-variable X-ray diffraction , 2003 .

[19]  R. Mullen,et al.  A biomimetic example of brittle toughening: (I) steady state multiple cracking , 1996 .

[20]  Daolun L. Chen,et al.  Cymbiola nobilis shell: Toughening mechanisms in a crossed-lamellar structure , 2017, Scientific Reports.

[21]  Huajian Gao,et al.  Materials become insensitive to flaws at nanoscale: Lessons from nature , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  John D. Currey,et al.  The mechanical behaviour of some molluscan hard tissues , 2009 .

[23]  Jie Zhao,et al.  The relationship between mechanical properties and crossed-lamellar structure of mollusk shells , 2008 .

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

[25]  S. Spearing,et al.  Fracture mechanisms of the Strombus gigas conch shell: implications for the design of brittle laminates , 1996, Journal of Materials Science.

[26]  Xiaodong Li,et al.  Origin of flaw-tolerance in nacre , 2013, Scientific Reports.

[27]  D. J. Barber,et al.  Electron microscopy of molluscan crossed-lamellar microstructure , 1992 .

[28]  Markus J Buehler,et al.  Three-Dimensional-Printing of Bio-Inspired Composites. , 2016, Journal of biomechanical engineering.

[29]  Y. Kauffmann,et al.  Atomic structure and ultrastructure of the Murex troscheli shell. , 2012, Journal of structural biology.

[30]  Bharat Bhushan,et al.  Hierarchical structure and mechanical properties of nacre: a review , 2012 .

[31]  X. Li,et al.  Biological Self‐Arrangement of Fiber Like Aragonite and Its Effect on Mechanical Behavior of Veined rapa whelk Shell , 2015 .

[32]  Yuri Estrin,et al.  Enhanced Mechanical Performance of Bio-Inspired Hybrid Structures Utilising Topological Interlocking Geometry , 2016, Scientific Reports.

[33]  Zhihui Zhang,et al.  Study of the microstructure and mechanical properties of white clam shell. , 2016, Micron.

[34]  Benjamin Marie,et al.  Molluscan shell proteins: primary structure, origin, and evolution. , 2008, Current topics in developmental biology.

[35]  Francois Barthelat,et al.  Structure and mechanics of interfaces in biological materials , 2016 .

[36]  Rui Li,et al.  Structural and Mechanical Characterization of Thermally Treated Conch Shells , 2015, JOM.

[37]  K. Faber,et al.  Synthetic crossed-lamellar microstructures in oxide ceramics , 2005 .

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

[39]  John D. Taylor,et al.  The mechanical properties of bivalve (Mollusca) shell structures , 1972 .

[40]  F. Barthelat,et al.  A laser-engraved glass duplicating the structure, mechanics and performance of natural nacre , 2015, Bioinspiration & biomimetics.

[41]  Qiang Chen,et al.  Bio-mimetic mechanisms of natural hierarchical materials: a review. , 2013, Journal of the mechanical behavior of biomedical materials.

[42]  J. Currey,et al.  Fatigue fracture of mother‐of‐pearl and its significance for predatory techniques , 2009 .

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

[44]  J. G. Carter.  Skeletal biomineralization : patterns, processes, and evolutionary trends , 1991 .

[45]  J. Currey,et al.  Fracture in the crossed-lamellar structure ofConus shells , 1976 .

[46]  S. Santhanam,et al.  Strombus gigas inspired biomimetic ceramic composites via SHELL—Sequential Hierarchical Engineered Layer Lamination , 2013 .

[47]  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.

[48]  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.

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

[50]  M. Kunz,et al.  Structure and mechanical properties of a pteropod shell consisting of interlocked helical aragonite nanofibers. , 2011, Angewandte Chemie.

[51]  J. Mansot,et al.  Use of nanoindentation technique for a better understanding of the fracture toughness of Strombus gigas conch shell , 2013 .

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

[53]  Z. Zhang,et al.  Mechanical behavior of mother-of-pearl and pearl with flat and spherical laminations. , 2016, Materials science & engineering. C, Materials for biological applications.

[54]  A. Lin.  Structural and functional biological materials : abalone nacre, sharp materials, and abalone foot adhesion , 2008 .

[55]  Xiaodong Li.  Nanoscale structural and mechanical characterization of natural nanocomposites: Seashells , 2007 .

[56]  O. Bøggild.  The shell structure of the Mollusks , 1930 .

[57]  Zengqian Liu,et al.  Intrinsic hierarchical structural imperfections in a natural ceramic of bivalve shell with distinctly graded properties , 2015, Scientific Reports.

[58]  A. Heuer,et al.  Tissue Regeneration in the Shell of the Giant Queen Conch, Strombus gigas , 2004 .

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

[60]  X W Li,et al.  Structure and mechanical properties of Saxidomus purpuratus biological shells. , 2011, Journal of the mechanical behavior of biomedical materials.

[61]  Xiaodong Li,et al.  Multiscale hierarchical assembly strategy and mechanical prowess in conch shells (Busycon carica). , 2013, Journal of structural biology.

[62]  R. Ritchie.  The conflicts between strength and toughness. , 2011, Nature materials.

[63]  D. Hou,et al.  Conch shell structure and its effect on mechanical behaviors. , 2004, Biomaterials.

[64]  H. Kahn,et al.  Bioinspired micro-composite structure , 2005 .

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

[66]  Richard Weinkamer,et al.  Nature’s hierarchical materials , 2007 .

[67]  Q. Yuan,et al.  Hierarchical and intersectional microstructure of Graceful Fig shell , 2010 .

[68]  Wei Zhang,et al.  Fractal analysis of microstructure-related indentation toughness of Clinocardium californiense shell , 2014 .

[69]  Huajian Gao,et al.  Nanotwin-governed toughening mechanism in hierarchically structured biological materials , 2016, Nature Communications.

[70]  J. Currey.  The design of mineralised hard tissues for their mechanical functions. , 1999, The Journal of experimental biology.

[71]  Adam J. Stevenson,et al.  Strong, tough and stiff bioinspired ceramics from brittle constituents. , 2014, Nature materials.

[72]  H. Ji,et al.  Microstructural Characteristic and its Relation to Mechanical Properties of Clinocardium californiense Shell , 2014 .

[73]  D. Kisailus,et al.  Fracture Mitigation Strategies in Gastropod Shells , 2013 .

[74]  E. Harper.  Are calcitic layers an effective adaptation against shell dissolution in the Bivalvia , 2000 .

[75]  Huajian Gao,et al.  A study of fracture mechanisms in biological nano-composites via the virtual internal bond model , 2004 .

[76]  X. Wang,et al.  Three-Point Bending Fracture Behavior of Single Oriented Crossed-Lamellar Structure in Scapharca broughtonii Shell , 2015, Materials.

[77]  Z. Zhang,et al.  Anisotropic mechanical behaviors and their structural dependences of crossed-lamellar structure in a bivalve shell. , 2016, Materials science & engineering. C, Materials for biological applications.

[78]  F. Nudelman.  Nacre biomineralisation: A review on the mechanisms of crystal nucleation. , 2015, Seminars in cell & developmental biology.

[79]  Bela Imre Sandor,et al.  Fundamentals of cyclic stress and strain , 1972 .

[80]  A. P. Jackson,et al.  Comparison of nacre with other ceramic composites , 1990 .

[81]  Jie Zhao,et al.  Mechanical properties and structure of Haliotis discus hannai Ino and Hemifusus tuba conch shells: a comparative study , 2010 .

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

[83]  M. Meyers,et al.  Structural Design Elements in Biological Materials: Application to Bioinspiration , 2015, Advanced materials.

[84]  F Barthelat,et al.  Overcoming the brittleness of glass through bio-inspiration and micro-architecture , 2014, Nature Communications.

[85]  R. Ritchie,et al.  Developing strength and toughness in bio-inspired silicon carbide hybrid materials containing a compliant phase , 2015 .

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

[87]  Guang-Ping Zhang,et al.  Microstructural Characterization and Hardness Behavior of a Biological Saxidomus purpuratus Shell , 2011 .

[88]  Xiaodong Li,et al.  Micro/nanomechanical characterization of a natural nanocomposite material—the shell of Pectinidae , 2003 .

[89]  A. Heuer,et al.  Fracture mechanisms of the Strombus gigas conch shell: II-micromechanics analyses of multiple cracking and large-scale crack bridging , 2004 .

[90]  Christine Ortiz,et al.  Pervasive nanoscale deformation twinning as a catalyst for efficient energy dissipation in a bioceramic armour. , 2014, Nature materials.

[91]  Baohua Ji,et al.  Mechanical properties of nanostructure of biological materials , 2004 .

[92]  E. Macías-Sánchez,et al.  Biological strategy for the fabrication of highly ordered aragonite helices: the microstructure of the cavolinioidean gastropods , 2016, Scientific Reports.

[93]  R. Ballarini,et al.  Structural basis for the fracture toughness of the shell of the conch Strombus gigas , 2000, Nature.

[94]  M. Willinger,et al.  Crystallographic relationships in the crossed lamellar microstructure of the shell of the gastropod Conus marmoreus. , 2012, Acta biomaterialia.

[95]  Xiaoxiang Wang,et al.  Structure and roles of the various layers in the shells of conch Conus litteratus , 2016 .

[96]  M. Willinger,et al.  New Crystallographic Relationships in Biogenic Aragonite: The Crossed-Lamellar Microstructures of Mollusks , 2016 .

[97]  H. Schuh,et al.  Probing the solar corona with very long baseline interferometry , 2014, Nature Communications.

[98]  Xiaodong Li,et al.  Plastic deformation enabled energy dissipation in a bionanowire structured armor. , 2014, Nano letters.

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

[100]  Markus J. Buehler,et al.  Structural hierarchies define toughness and defect-tolerance despite simple and mechanically inferior brittle building blocks , 2011, Scientific reports.

[101]  M. Buehler,et al.  Tough Composites Inspired by Mineralized Natural Materials: Computation, 3D printing, and Testing , 2013 .

[102]  A. Hall,et al.  ENVIRONMENTAL AND BIOLOGICAL CONTROLS ON BIVALVE SHELL MINERALOGY , 1969, Biological reviews of the Cambridge Philosophical Society.

[103]  F. Barthelat,et al.  Architectured materials in engineering and biology: fabrication, structure, mechanics and performance , 2015 .

[104]  Pengchao Zhang,et al.  Recent progress of abrasion-resistant materials: learning from nature. , 2016, Chemical Society reviews.

[105]  A. Heuer,et al.  Novel composite microstructure and mechanical behavior of mollusk shell , 1989 .

[106]  Michael F. Ashby,et al.  The mechanical efficiency of natural materials , 2004 .

[107]  B. Ji.  A study of the interface strength between protein and mineral in biological materials. , 2008, Journal of biomechanics.