Advanced bio-inspired structural materials: Local properties determine overall performance

Abstract Natural materials have always attracted intensive attention from multidisciplinary scientists all over the world. In fact, the ingenious and reasonable synthetic strategies of the limited components can always make natural materials achieve a superior performance that is far beyond their own. Meanwhile, the local properties can determine the overall performance through regulating multiple characteristics, including structure, composition, and interface. Living organisms can inspire the fabrication of artificial materials, which provides a clear vision for advanced materials research. Therefore, inspired by this strategy, biomimetic structural materials are used to meet the strict and even extreme requirements of engineering materials. In this review, we mainly clarify the difference of local properties in natural materials and explain how living organisms utilize very limited elements and compounds to control the local properties and further realize some specific function to adapt to the specific requirement of the environment. In addition, the manufacturing technologies and strategies common to bio-inspired structural materials are summarized. Finally, a summary and prospects on the limitations of current techniques and the direction of future developments for the design of novel bio-inspired materials are given.

[1]  André R. Studart,et al.  Three-dimensional printing of hierarchical liquid-crystal-polymer structures , 2018, Nature.

[2]  Marc A. Meyers,et al.  Biological materials: Functional adaptations and bioinspired designs , 2012 .

[3]  M. Meyers,et al.  Hydration‐Induced Shape and Strength Recovery of the Feather , 2018, Advanced Functional Materials.

[4]  Swee Hin Teoh,et al.  Fatigue of biomaterials: a review , 2000 .

[5]  R O Ritchie,et al.  Crack blunting, crack bridging and resistance-curve fracture mechanics in dentin: effect of hydration. , 2003, Biomaterials.

[6]  F. G. Torres,et al.  Failure of flight feathers under uniaxial compression. , 2017, Materials science & engineering. C, Materials for biological applications.

[7]  Chao Gao,et al.  Superstructured Assembly of Nanocarbons: Fullerenes, Nanotubes, and Graphene. , 2015, Chemical reviews.

[8]  K. Johnson,et al.  Moisture, anisotropy, stress state, and strain rate effects on bighorn sheep horn keratin mechanical properties. , 2017, Acta biomaterialia.

[9]  N. Pugno,et al.  Nanoscale Mechanics of Graphene and Graphene Oxide in Composites: A Scientific and Technological Perspective , 2016, Advanced materials.

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

[11]  L. Ren,et al.  Active Antifogging Property of Monolayer SiO2 Film with Bioinspired Multiscale Hierarchical Pagoda Structures. , 2016, ACS nano.

[12]  R. Ritchie Mechanisms of fatigue crack propagation in metals, ceramics and composites: Role of crack tip shielding☆ , 1988 .

[13]  Mason R. Mackey,et al.  Protective role of Arapaima gigas fish scales: structure and mechanical behavior. , 2014, Acta biomaterialia.

[14]  P. Maini,et al.  Reptile scale paradigm: Evo-Devo, pattern formation and regeneration. , 2009, The International journal of developmental biology.

[15]  Steven A Herrera,et al.  Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles , 2018, Advanced materials.

[16]  Grace X. Gu,et al.  Hierarchically Enhanced Impact Resistance of Bioinspired Composites , 2017, Advanced materials.

[17]  Z. Zhang,et al.  Structure and mechanical behaviors of protective armored pangolin scales and effects of hydration and orientation. , 2016, Journal of the mechanical behavior of biomedical materials.

[18]  Xiaodong Li,et al.  Elastic modulus of biopolymer matrix in nacre measured using coupled atomic force microscopy bending and inverse finite element techniques , 2011 .

[19]  S. Suresh,et al.  Graded Materials for Resistance to Contact Deformation and Damage , 2001, Science.

[20]  Steven A Herrera,et al.  The Stomatopod Dactyl Club: A Formidable Damage-Tolerant Biological Hammer , 2012, Science.

[21]  L. Szewciw,et al.  Morphology and Development of Blue Whale Baleen: An Annotated Translation of Tycho Tullberg's Classic 1883 Paper , 2009 .

[22]  Xiaodong Li,et al.  Deformation Strengthening of Biopolymer in Nacre , 2011 .

[23]  Xiaodong Li,et al.  Atomistic Origin of Deformation Twinning in Biomineral Aragonite. , 2017, Physical review letters.

[24]  André R Studart,et al.  Towards High‐Performance Bioinspired Composites , 2012, Advanced materials.

[25]  M. Meyers,et al.  Keratin: Structure, mechanical properties, occurrence in biological organisms, and efforts at bioinspiration , 2016 .

[26]  Chunyan Wang,et al.  Bioinspired Materials: from Low to High Dimensional Structure , 2014, Advanced materials.

[27]  Richard Weinkamer,et al.  Mechanical adaptation of biological materials — The examples of bone and wood , 2011 .

[28]  Peter Fratzl,et al.  Iron-Clad Fibers: A Metal-Based Biological Strategy for Hard Flexible Coatings , 2010, Science.

[29]  Amanda L. Forster,et al.  Binary Cellulose Nanocrystal Blends for Bioinspired Damage Tolerant Photonic Films , 2018 .

[30]  E. A. Ossa,et al.  The limiting layer of fish scales: Structure and properties. , 2017, Acta biomaterialia.

[31]  M. Meyers,et al.  Structure and mechanical properties of naturally occurring lightweight foam-filled cylinder--the peacock's tail coverts shaft and its components. , 2015, Acta biomaterialia.

[32]  Chuanjin Huang,et al.  Freeze Casting for Assembling Bioinspired Structural Materials , 2017, Advanced materials.

[33]  Marc A. Meyers,et al.  Functional gradients and heterogeneities in biological materials: Design principles, functions, and bioinspired applications , 2017 .

[34]  Hrishikesh V. Pathak,et al.  Unique fatality due to claw injuries in a tiger attack: a case report. , 2014, Legal medicine.

[35]  Shichao Niu,et al.  A High-Transmission, Multiple Antireflective Surface Inspired from Bilayer 3D Ultrafine Hierarchical Structures in Butterfly Wing Scales. , 2016, Small.

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

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

[38]  Liang Wu,et al.  A Bioinspired Interface Design for Improving the Strength and Electrical Conductivity of Graphene‐Based Fibers , 2018, Advanced materials.

[39]  Hugh Alan Bruck,et al.  Processing bulk natural wood into a high-performance structural material , 2018, Nature.

[40]  Xiaodong Li,et al.  Order-disorder transition of aragonite nanoparticles in nacre. , 2012, Physical review letters.

[41]  Lei Liu,et al.  Synthetic nacre by predesigned matrix-directed mineralization , 2016, Science.

[42]  M. Meyers,et al.  Alligator osteoderms: mechanical behavior and hierarchical structure. , 2014, Materials science & engineering. C, Materials for biological applications.

[43]  Chao Gao,et al.  Ultrastrong Fibers Assembled from Giant Graphene Oxide Sheets , 2013, Advanced materials.

[44]  B. Natarajan,et al.  Bioinspired Bouligand cellulose nanocrystal composites: a review of mechanical properties , 2018, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[45]  F. Barth,et al.  Biomaterial systems for mechanosensing and actuation , 2009, Nature.

[46]  A. Giannakopoulos,et al.  Indentation of solids with gradients in elastic properties: Part II. Axisymmetric indentors , 1997 .

[47]  T. Mokari,et al.  Bioinspired Hierarchical Porous Structures for Engineering Advanced Functional Inorganic Materials , 2018, Advanced materials.

[48]  Glaucio H. Paulino,et al.  Modeling bamboo as a functionally graded material: lessons for the analysis of affordable materials , 2006 .

[49]  A R Boccaccini,et al.  Applications of graphene electrophoretic deposition. A review. , 2013, The journal of physical chemistry. B.

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

[51]  Bin Wang,et al.  Lessons from the Ocean: Whale Baleen Fracture Resistance , 2018, Advanced materials.

[52]  James C. Weaver,et al.  Phase Transformations and Structural Developments in the Radular Teeth of Cryptochiton Stelleri , 2013 .

[53]  D. McAdams,et al.  Nano/Micro‐Manufacturing of Bioinspired Materials: a Review of Methods to Mimic Natural Structures , 2016, Advanced materials.

[54]  N. Kröger The Molecular Basis of Nacre Formation , 2009, Science.

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

[56]  P. Zavattieri,et al.  Crack twisting and toughening strategies in Bouligand architectures , 2018, International Journal of Solids and Structures.

[57]  E. A. Ossa,et al.  Designed for resistance to puncture: The dynamic response of fish scales. , 2019, Journal of the mechanical behavior of biomedical materials.

[58]  Frank W. Zok,et al.  The Transition from Stiff to Compliant Materials in Squid Beaks , 2008, Science.

[59]  D. Raabe,et al.  The composition of the exoskeleton of two crustacea: The American lobster Homarus americanus and the edible crab Cancer pagurus , 2007 .

[60]  Lin Guo,et al.  Bioinspired LDH‐Based Hierarchical Structural Hybrid Materials with Adjustable Mechanical Performance , 2018 .

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

[62]  Jun Chen,et al.  Scalable One‐Step Wet‐Spinning of Graphene Fibers and Yarns from Liquid Crystalline Dispersions of Graphene Oxide: Towards Multifunctional Textiles , 2013 .

[63]  A. Waas,et al.  Abiotic tooth enamel , 2017, Nature.

[64]  J. Tiller,et al.  Enzymatic mineralization generates ultrastiff and tough hydrogels with tunable mechanics , 2017, Nature.

[65]  Bor-Kai Hsiung,et al.  Static flexural properties of hedgehog spines conditioned in coupled temperature and relative humidity environments. , 2017, Journal of the mechanical behavior of biomedical materials.

[66]  Xiaodong Li,et al.  The Art of Curved Reinforcing in Biological Armors — Seashells , 2019, Journal of Bionic Engineering.

[67]  R O Ritchie,et al.  Mechanistic aspects of fracture and R-curve behavior in human cortical bone. , 2005, Biomaterials.

[68]  M. Meyers,et al.  Pangolin armor: Overlapping, structure, and mechanical properties of the keratinous scales. , 2016, Acta biomaterialia.

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

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

[71]  Xiaodong Li,et al.  Unveiling the formation mechanism of pseudo-single-crystal aragonite platelets in nacre. , 2009, Physical review letters.

[72]  André R Studart,et al.  Additive manufacturing of biologically-inspired materials. , 2016, Chemical Society reviews.

[73]  M. Meyers,et al.  Structural Biological Materials: Critical Mechanics-Materials Connections , 2013, Science.

[74]  Dirk Schneider,et al.  Nonlinear control of high-frequency phonons in spider silk. , 2016, Nature materials.

[75]  Xiaodong Li,et al.  Hidden energy dissipation mechanism in nacre , 2014 .

[76]  Chao Gao,et al.  Biomimetic Architectured Graphene Aerogel with Exceptional Strength and Resilience. , 2017, ACS nano.

[77]  D. Raabe,et al.  Influence of Structural Principles on the Mechanics of a Biological Fiber‐Based Composite Material with Hierarchical Organization: The Exoskeleton of the Lobster Homarus americanus , 2009 .

[78]  Y. Oaki,et al.  Synthesis and morphogenesis of organic polymer materials with hierarchical structures in biominerals. , 2011, Journal of the American Chemical Society.

[79]  A. Korsunsky,et al.  Multiscale analysis of bamboo deformation mechanisms following NaOH treatment using X-ray and correlative microscopy. , 2018, Acta biomaterialia.

[80]  R. Ritchie,et al.  On the Fracture Toughness of Advanced Materials , 2009 .

[81]  Shahrouz Amini,et al.  The Mantis Shrimp Saddle: A Biological Spring Combining Stiffness and Flexibility , 2015 .

[82]  Quan-hong Yang,et al.  Self‐Assembled Free‐Standing Graphite Oxide Membrane , 2009 .

[83]  R. Ritchie,et al.  Multiscale structure and damage tolerance of coconut shells. , 2017, Journal of the mechanical behavior of biomedical materials.

[84]  Dongxu Ke,et al.  Additive manufacturing of biomaterials. , 2018, Progress in materials science.

[85]  James C. Weaver,et al.  Microstructural and Biochemical Characterization of the Nanoporous Sucker Rings from Dosidicus gigas , 2009 .

[86]  Wen Yang,et al.  Natural Flexible Dermal Armor , 2013, Advanced materials.

[87]  M. Meyers,et al.  Additive Manufacturing as a Method to Design and Optimize Bioinspired Structures , 2018, Advanced materials.

[88]  Carsten Werner,et al.  The springtail cuticle as a blueprint for omniphobic surfaces. , 2016, Chemical Society reviews.

[89]  A. Evans Perspective on the Development of High‐Toughness Ceramics , 1990 .

[90]  Tianxi Liu,et al.  Ultrastrong Bioinspired Graphene‐Based Fibers via Synergistic Toughening , 2016, Advanced materials.

[91]  Xiaodong Han,et al.  Cloning Nacre's 3D Interlocking Skeleton in Engineering Composites to Achieve Exceptional Mechanical Properties , 2016, Advanced materials.

[92]  P. Fratzl,et al.  Bioinspired Design Criteria for Damage‐Resistant Materials with Periodically Varying Microstructure , 2011 .

[93]  Alberto Redaelli,et al.  Molecular and nanostructural mechanisms of deformation, strength and toughness of spider silk fibrils. , 2010, Nano letters.

[94]  P. Fratzl,et al.  Hindered Crack Propagation in Materials with Periodically Varying Young's Modulus—Lessons from Biological Materials , 2007 .

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

[96]  C. Neinhuis,et al.  Biologically Inspired Omniphobic Surfaces by Reverse Imprint Lithography , 2014, Advanced materials.

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

[98]  S. Nikolov,et al.  Revealing the Design Principles of High‐Performance Biological Composites Using Ab initio and Multiscale Simulations: The Example of Lobster Cuticle , 2010, Advanced materials.

[99]  Robert O Ritchie,et al.  On the Materials Science of Nature's Arms Race , 2018, Advanced materials.

[100]  S. Stankovich,et al.  Preparation and characterization of graphene oxide paper , 2007, Nature.

[101]  Peter Fratzl,et al.  Biological composites—complex structures for functional diversity , 2018, Science.

[102]  Liangbing Hu,et al.  Dense, Self‐Formed Char Layer Enables a Fire‐Retardant Wood Structural Material , 2019, Advanced Functional Materials.

[103]  Eduardo Saiz,et al.  Ice-templated porous alumina structures , 2007, 1710.04651.

[104]  P. Withers,et al.  Time-lapse three-dimensional imaging of crack propagation in beetle cuticle. , 2019, Acta biomaterialia.

[105]  R. Ritchie,et al.  Bioinspired structural materials. , 2014, Nature Materials.

[106]  P. Hansma,et al.  Exploring molecular and mechanical gradients in structural bioscaffolds. , 2004, Biochemistry.

[107]  Xiaodong Li,et al.  Dynamic self-strengthening of a bio-nanostructured armor - conch shell. , 2019, Materials science & engineering. C, Materials for biological applications.

[108]  Hongyun Luo,et al.  Water effects on the deformation and fracture behaviors of the multi-scaled cellular fibrous bamboo. , 2018, Acta biomaterialia.

[109]  B. Hall,et al.  Osteoderm morphology and development in the nine‐banded armadillo, Dasypus novemcinctus (Mammalia, Xenarthra, Cingulata) , 2006, Journal of morphology.

[110]  Markus J. Buehler,et al.  Nonlinear material behaviour of spider silk yields robust webs , 2012, Nature.

[111]  Ke Chen,et al.  A General Bioinspired, Metals-Based Synergic Cross-Linking Strategy toward Mechanically Enhanced Materials. , 2017, ACS nano.

[112]  Deepak Vashishth,et al.  Rising crack-growth-resistance behavior in cortical bone: implications for toughness measurements. , 2004, Journal of biomechanics.

[113]  Xuke Tang,et al.  Strong and Tough Layered Nanocomposites with Buried Interfaces. , 2016, ACS nano.

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

[115]  Jian Lu,et al.  Asymmetric flexural behavior from bamboo's functionally graded hierarchical structure: underlying mechanisms. , 2015, Acta biomaterialia.

[116]  Takashi Kato,et al.  An Acidic Matrix Protein, Pif, Is a Key Macromolecule for Nacre Formation , 2009, Science.

[117]  James C. Weaver,et al.  Analysis of an ultra hard magnetic biomineral in chiton radular teeth , 2010 .

[118]  Xiaodong Li,et al.  Bioinspired, Graphene/Al2O3 Doubly Reinforced Aluminum Composites with High Strength and Toughness. , 2017, Nano letters.

[119]  H. Le Ferrand,et al.  Magnetically assisted slip casting of bioinspired heterogeneous composites. , 2015, Nature materials.

[120]  M. Dargusch,et al.  Granular Nanostructure: A Facile Biomimetic Strategy for the Design of Supertough Polymeric Materials with High Ductility and Strength , 2017, Advanced materials.

[121]  J. Vincent,et al.  Design and mechanical properties of insect cuticle. , 2004, Arthropod structure & development.

[122]  Bor-Kai Hsiung,et al.  Dynamic impact testing of hedgehog spines using a dual-arm crash pendulum. , 2016, Journal of the mechanical behavior of biomedical materials.

[123]  L. Gibson Biomechanics of cellular solids. , 2005, Journal of biomechanics.

[124]  C. Lauer,et al.  Strength-size relationships in two porous biological materials. , 2018, Acta biomaterialia.

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

[126]  R. Ritchie,et al.  Hyperelastic phase-field fracture mechanics modeling of the toughening induced by Bouligand structures in natural materials , 2019, Journal of the Mechanics and Physics of Solids.

[127]  Xiaodong Li,et al.  Bioinspired, Multiscale Reinforced Composites with Exceptionally High Strength and Toughness. , 2018, Nano letters.

[128]  J. Lewis,et al.  Microperiodic structures: Direct writing of three-dimensional webs , 2004, Nature.

[129]  R. Ritchie,et al.  On the Mechanistic Origins of Toughness in Bone , 2010 .

[130]  N. Tamura,et al.  Parrotfish Teeth: Stiff Biominerals Whose Microstructure Makes Them Tough and Abrasion-Resistant To Bite Stony Corals. , 2017, ACS nano.

[131]  D. Ghosh,et al.  Effects of porosity and strain rate on the uniaxial compressive response of ice-templated sintered macroporous alumina , 2018 .

[132]  P. Zavattieri,et al.  Twisting cracks in Bouligand structures. , 2017, Journal of the mechanical behavior of biomedical materials.

[133]  K. Johnson,et al.  Contact mechanics and the wear of metals , 1995 .

[134]  Chengwei Wang,et al.  Muscle‐Inspired Highly Anisotropic, Strong, Ion‐Conductive Hydrogels , 2018, Advanced materials.

[135]  H. Espinosa,et al.  AFM Identification of Beetle Exocuticle: Bouligand Structure and Nanofiber Anisotropic Elastic Properties , 2017 .

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

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

[138]  Jürgen Hartmann,et al.  A Spider's Fang: How to Design an Injection Needle Using Chitin‐Based Composite Material , 2012 .

[139]  Shawn Hoon,et al.  Infiltration of chitin by protein coacervates defines the squid beak mechanical gradient. , 2015, Nature chemical biology.

[140]  O. Ikkala,et al.  Large-area, lightweight and thick biomimetic composites with superior material properties via fast, economic, and green pathways. , 2010, Nano letters.

[141]  Jae-Young Jung,et al.  A Sinusoidally Architected Helicoidal Biocomposite. , 2016, Advanced materials.

[142]  Xiaodong Li,et al.  Uncovering Aragonite Nanoparticle Self-assembly in Nacre—A Natural Armor , 2012 .

[143]  R. Tang,et al.  Biomineralization: From Material Tactics to Biological Strategy , 2017, Advanced materials.

[144]  M. Vickaryous,et al.  The integumentary skeleton of tetrapods: origin, evolution, and development , 2009, Journal of anatomy.