Bioinspired structural materials

Journal name:
Nature Materials
Volume:
14,
Pages:
23–36
Year published:
DOI:
doi:10.1038/nmat4089
Received
Accepted
Published online

Abstract

Natural structural materials are built at ambient temperature from a fairly limited selection of components. They usually comprise hard and soft phases arranged in complex hierarchical architectures, with characteristic dimensions spanning from the nanoscale to the macroscale. The resulting materials are lightweight and often display unique combinations of strength and toughness, but have proven difficult to mimic synthetically. Here, we review the common design motifs of a range of natural structural materials, and discuss the difficulties associated with the design and fabrication of synthetic structures that mimic the structural and mechanical characteristics of their natural counterparts.

At a glance

Figures

  1. Material-property chart, and projections for natural and synthetic materials.
    Figure 1: Material-property chart, and projections for natural and synthetic materials.

    a, Ashby plot4 of the specific values (that is, normalized by density) of strength and stiffness (or Young's modulus) for both natural and synthetic materials. Many engineering materials, particularly high-performance ceramics and metallic alloys, have values of strength and toughness that are much higher than those of the best natural materials. Silk stands out as an exception, sometimes reaching the extraordinary toughness of 1,000 MJ m−3 with a modulus of 10 GPa (ref. 122) — approaching that of Kevlar. One might therefore conclude that there is nothing spectacular about the properties of natural materials, as in general they seem similar to what can be made synthetically. However, quite unlike most synthetic materials, all natural structural materials use a limited chemical palette of inexpensive ingredients — typically, proteins, polysaccharides, calcites and aragonites, and rarely metals — whose properties are often meagre, and are formed at ambient temperatures with little energy requirements. Moreover, the constituents of natural materials are typically arranged in a hierarchical architecture of interwoven or interlocking structures that is difficult to reproduce synthetically. Many natural materials also repair themselves when damaged; in contrast, self-healing synthetic structures are still highly limited. b, Many natural composite materials, as exemplified by bone and nacre, have toughness values that far exceed those of their constituents and their homogeneous mixtures (as indicated by the dashed lines), and are able to sustain incipient cracking by utilizing extensive extrinsic toughening mechanisms (Figs 3 and 4b). This results in much higher toughness for crack growth (closed symbols above the solid arrows) than for crack initiation (open symbols), and thus higher fracture toughness (solid arrows). By mimicking the architecture of nacre in a synthetic ceramic material (alumina/PMMA)85, similar behaviour and exceptional toughness can be attained.

  2. Hierarchical structure of bone and bamboo.
    Figure 2: Hierarchical structure of bone and bamboo.

    a, In bone, macroscale arrangements involve both compact/cortical bone at the surface and spongy/trabecular bone (foam-like material with ~100-μm-thick struts) in the interior. Compact bone is composed of osteons and Haversian canals, which surround blood vessels. Osteons have a lamellar structure, with individual lamella consisting of fibres arranged in geometrical patterns. The fibres comprise several mineralized collagen fibrils, composed of collagen protein molecules (tropocollagen) formed from three chains of amino acids and nanocrystals of hydroxyapatite (HA), and linked by an organic phase to form fibril arrays. b, Bamboo is composed of cellulose fibres imbedded in a lignin–hemicellulose matrix shaped into hollow prismatic cells of varying wall thickness. In bamboo and palm, which have a more complex structure than wood, a radial density gradient of parallel fibres in a matrix of honeycomb-like cells increases each material's flexural rigidity. Bamboo increases its flexural rigidity even further by combining a radial density gradient with a hollow-tube cross-sectional shape. Panel a adapted with permission from: right-most bone image, ref. 123, © 1995 by The Journal of Bone and Joint Surgery, Inc.; rest of panel, ref. 124, Nature Publishing Group.

  3. Healthy human cortical bone resists fracture through complementary intrinsic and extrinsic contributions throughout its hierarchical structure.
    Figure 3: Healthy human cortical bone resists fracture through complementary intrinsic and extrinsic contributions throughout its hierarchical structure.

    a, Intrinsic toughening mechanisms that promote plasticity occur ahead of the crack tip and act primarily at the nanoscale, whereas extrinsic toughening mechanisms, specifically those that shield local stresses or strains from promoting fracture, act at larger length scales and mostly behind the crack tip. b, Intrinsically, collagen fibrillar sliding is the prime plasticity mechanism in bone, and as such has the largest impact on the inherent resistance of the hydroxyapatite/collagen composite. Other mechanisms include molecular uncoiling, microcracking and sacrificial bonding, all of which operate at submicrometre length scales. Conversely, extrinsic mechanisms, such as uncracked-ligament bridging and crack deflection, occur at micrometre length scales once the crack begins to grow so as to shield the crack tip. Figure reproduced from ref. 12, 2010 Annual Reviews.

  4. The hierarchical structure and properties of nacre.
    Figure 4: The hierarchical structure and properties of nacre.

    a-d, Nacre is a brick-and-mortar structure (c) of CaCO3 mineral platelets (aragonite), which provide strength, and proteins, which allow for ductility and toughness. The mineral bricks, which until recently were thought to be brittle single crystals, are ~500 nm thick and ~5–10 μm wide, and are comprised of millions of nanograins (~30 nm) glued together by a biopolymer125 (a). If the platelets were rigidly interlocked, the resulting structure would be hard, yet hopelessly brittle. Instead, the biopolymeric mortar between the bricks generates limited deformation between the mineral layers (as shown by the mechanisms depicted in b), thereby allowing for the relief of locally high stresses while also providing ductility without too much loss in strength. Too much 'give' in the mortar, however, would result in lower strength; conversely, a mortar that is too hard would result in brick failure. Optimum properties come about when the strength of the mortar is fractionally less than the strength of the bricks, such that toughening through crack bridging can occur when the bricks pull out without breaking (d; orange arrows indicate the direction of tension). e,f, Comparison of the strength (e) and toughness (f) of natural nacre and nacre-like alumina/PMMA ceramics made using freeze casting84, 85. Toughening is associated with brick pull-out and frictional sliding in the compliant polymeric layer. The nacre-like alumina/PMMA ceramic has exceptional fracture toughness, exceeding Kc = 30 MPa m½, which is an order of magnitude higher than the toughness of its constituent phases and of homogeneous alumina/PMMA nanocomposites. Panels e,f reproduced with permission from ref. 85, © 2008 The American Association for the Advancement of Science.

  5. Processing of nacre-like structures by freeze casting.
    Figure 5: Processing of nacre-like structures by freeze casting.

    a, Freeze casting uses both the directional freezing of, generally, ceramic suspensions and the microstructure of ice to template the architecture of scaffolds, and thus can be used to create porous, layered materials84, 126, 127. b,c, Controlled freezing results in the formation of lamellar ice crystals that expel the particles and/or dissolved molecules as they grow. The particles accumulate in the space between the crystals, leading to the formation of a lamellar material (exemplified by the freeze-cast lamellar alumina (top) and porous chitosan (bottom) micrographs in c) after the ice has been sublimated by freeze drying and the material has been sintered. Particles trapped by the ice crystals form bridges between lamellae, and these bridges make a critical contribution to the mechanical properties of the layered material. The relevant microstructural dimensions — pore and lamellae widths and wavelengths from one to hundreds of micrometres — can be controlled by adjusting the composition of the suspension (solid content and solvent formulation) and the speed at which the ice grows. Figures adapted with permission from: a, ref. 126, 2010 The Royal Society; b, ref. 127, © 2006 Acta Materialia Inc.

  6. Additive-manufacturing techniques.
    Figure 6: Additive-manufacturing techniques.

    a,b, Custom-designed solid materials with complex architectures can be precisely and reproducibly fabricated through free-form additive-manufacturing processes (3D printing). These include direct inkjet writing and robotic-assisted deposition (robocasting), which can generate, for example, glass 3D-printed scaffolds (a), as well as droplet-deposition (jetting), to form, for instance, printed droplet networks (b). Jetting represents a promising platform for the manufacturing of complex functional devices102. These techniques usually involve the layer-by-layer printing of structures generated by computer-aided design or obtained from image sources, such as magnetic resonance imaging. Simultaneously with droplet deposition, a laser pulse can be used to induce the vapourization of organic solvents, the fast sintering of metal and ceramic droplets, or the polymerization of a composite structure.

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Affiliations

  1. Thayer School of Engineering, Dartmouth College, Hanover, New Hampshire 03755, USA

    • Ulrike G. K. Wegst
  2. Materials Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA

    • Hao Bai,
    • Antoni P. Tomsia &
    • Robert O. Ritchie
  3. Centre for Advanced Structural Ceramics, Department of Materials, Imperial College London, London SW7 2AZ, UK

    • Eduardo Saiz
  4. Department of Materials Science & Engineering, University of California, Berkeley, California 94720, USA

    • Robert O. Ritchie

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All authors contributed equally to this work.

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