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Structural Design Elements in Biological Materials: REVIEW Application to Bioinspiration

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Structural Design Elements in Biological Materials: REVIEW Application to Bioinspiration www.advmat.de www.MaterialsViews.com Structural Design Elements in Biological Materials: REVIEW Application to Bioinspiration Steven E. Naleway , * Michael M. Porter , Joanna McKittrick , and Marc A. Meyers * biological materials often presents similar Eight structural elements in biological materials are identifi ed as the most solutions, since the number of materials common amongst a variety of animal taxa. These are proposed as a new available in nature is fairly limited and paradigm in the fi eld of biological materials science as they can serve as therefore resourceful combinations of a toolbox for rationalizing the complex mechanical behavior of structural them have to be developed to address spe- biological materials and for systematizing the development of bioinspired cifi c environmental constraints. We have identifi ed these common designs and designs for structural applications. They are employed to improve the named them “structural design elements.” mechanical properties, namely strength, wear resistance, stiffness, fl exibility, In the emerging fi eld of biological fracture toughness, and energy absorption of different biological materials materials science, there is a great need for for a variety of functions (e.g., body support, joint movement, impact protec- systematizing these observations and to tion, weight reduction). The structural elements identifi ed are: fi brous, helical, describe the underlying mechanics prin- ciples in a unifi ed manner. This is neces- gradient, layered, tubular, cellular, suture, and overlapping. For each of the sary as similar designs are often reported structural design elements, critical design parameters are presented along under various names. As an example, the with constitutive equations with a focus on mechanical properties. Addition- presence of numerous interfaces within ally, example organisms from varying biological classes are presented for a composite that introduce a signifi cant each case to display the wide variety of environments where each of these property mismatch, which we suggest be elements is present. Examples of current bioinspired materials are also intro- named a “layered” structure, has been pre- viously referred to as “lamella” in bone [ 2 ] duced for each element. and fi sh scales,[ 3 ] “brick and mortar” in abalone, [ 4–6 ] and a “laminated structure” in sea sponges[ 7 ] despite providing most 1. Introduction if not all of the same structural advantages. We propose herein a new system of eight structural design elements that are most In spite of an estimated 7 million animal species living on common amongst a wide variety of animal taxa. These structural earth, [ 1 ] there is remarkable repetition in the structures observed elements have each evolved to improve the mechanical proper- among the diversity of biological materials. This is due to the ties, namely strength, stiffness, fl exibility, fracture toughness, fact that many different organisms have developed similar solu- wear resistance, and energy absorption of different biological tions to natural challenges (e.g., ambient environmental con- materials for specifi c multi-functions (e.g., body support, joint ditions, predation). As a result, the vast body of research on movement, impact protection, mobility, weight reduction). These structural design elements are visually displayed in Figure 1 : S. E. Naleway, Prof. J. McKittrick, Prof. M. A. Meyers • Fibrous structures; offering high tensile strength when Materials Science and Engineering Program aligned in a single direction, with limited to nil compressive University of California San Diego, La Jolla , CA 92093–0411 , USA strength. E-mail: [email protected]; • Helical structures; common to fi brous or composite materi- [email protected] als, offering toughness in multiple directions and in-plane Prof. M. M. Porter isotropy. Department of Mechanical Engineering • Gradient structures; materials and interfaces that accom- Clemson University modate property mismatch (e.g., elastic modulus) through Clemson , SC 29634 , USA a gradual transition in order to avoid interfacial mismatch Prof. J. McKittrick, Prof. M. A. Meyers Department of Mechanical and Aerospace Engineering stress buildup, resulting in an increased toughness. University of California • Layered structures; complex composites that increase the San Diego, La Jolla , CA 92093–0411 , USA toughness of (most commonly) brittle materials through the Prof. M. A. Meyers introduction of interfaces. Department of Nanoengineering • Tubular structures; organized porosity that allows for energy University of California San Diego, La Jolla , CA 92093–0411 , USA absorption and crack defl ection. • Cellular structures; lightweight porous or foam architectures DOI: 10.1002/adma.201502403 that provide directed stress distribution and energy absorption. Adv. Mater. 2015, 27, 5455–5476 © 2015 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim wileyonlinelibrary.com 5455 www.advmat.de www.MaterialsViews.com These are often surrounded by dense layers to form sandwich structures. Steven E. Naleway is a Ph.D. • Suture structures; interfaces comprising wavy and interdigi- candidate in the Materials tating patterns that control strength and fl exibility. Science and Engineering REVIEW • Overlapping structures; featuring multiple plates or scutes Program at the University that overlap to form fl exible and often armored surfaces. of California, San Diego. He received his B.S. degree in As with all biological materials, these structural design ele- Mechanical Engineering and ments are composed of biopolymers (e.g., collagen, chitin, M.S. degree in Materials keratin) and biominerals (e.g., calcium carbonate, calcium Science both from Oregon phosphates, silica) that are hierarchically assembled from the State University. His research nano- to mesoscales. [ 8–10 ] However, the extraordinary mechan- focuses upon the intercon- ical properties observed in these natural materials are often nected fi elds of biological a product of the intricate structural organization at different materials science and bioinspired design both with a focus spatial scales (nano, micro, meso, and macro) where these upon structural applications. structural design elements are observed ( Table 1 ). As a result, in many cases organisms with different base materials will Joanna McKittrick has a B.S. employ the same structure for the same purpose (e.g., tubules in Mechanical Engineering found in human dentin composed of hydroxyapatite/collagen from the University of and also in ram horns composed of keratin [ 11 ] can both absorb Colorado, a M.S. in Materials energy). Science and Engineering from Examples of the structure–function relationships of the Northwestern University and common structural design elements in biological materials a Ph.D. in Materials Science can be found in a number of different organisms from varying and Engineering from MIT. biological classes (shown herein), illustrating the wide range of She works in the area of environments where these design elements are observed. In the structure-mechanical addition, bioinspired materials that incorporate these common properties (strength, stiffness, structures are becoming more prevalent as modern manufac- toughness, impact resist- turing allows for more control at the important spatial scales ance) of biological composites and developing bioinspired where these design elements are most often present. This designs. She also works in the area of luminescent mate- paper organizes these eight elements by their relative size and rials, most recently on phosphor development for solid- complexity (e.g., from smaller, less-complex fi brous structures state lighting. to larger, more-complex overlapping structures) and provides constitutive equations that describe their basic mechanical and/ Marc André Meyers is a or structural advantages. distinguished professor at the University of California, San Diego. He focuses his 2. Fibrous Structures research on the mechanical behavior of materials. He Biological materials that require high tensile strength or stiff- is a Fellow of TMS, APS, ness in a single direction are organized as fi brous structures, and ASM and a member of designed with numerous aligned fi bers (and fi brils or fi la- the Brazilian Academy of ments at smaller spatial scales) that often exhibit hierarchy Sciences. across multiple length scales ( Figure 2 a). They are commonly found within non-mineralized, soft biological materials, such as muscle, tendon, and silks. However, there are a number of notable exceptions such as the chitin fi bers in arthropod exoskeletons and collagen fi bers in bones where these fi bers are mineralized. These structures occur within the nano- to in two regimes of elastic-plastic behavior. In the fi rst of these microstructures of biological materials. Specifi c examples regimes the aligned fi bers unfurl, slide past each other, and given here are spider silk (Figure 2 b),[ 14,33 ] hagfi sh slime straighten without signifi cant resistance, following the power (Figure 2 c), [ 12,34,35 ] silkworm silk (Figure 2 d)[ 8 ] and rat tendon law (Figure 2 f(i) to 2f(ii)). [ 41 ] (Figure 2 e). [ 13,36 ] dσ ∝ ε n (>1)n (1) Mechanically, fi brous structures present a dichotomy of dε strength, high in tension and low to effectively nil in compres- sion. This results in dramatic tension–compression asymmetric where σ is the stress, ε is the strain, and n varies with the mate- behavior. Thus, they are typically applied in a tensile mode rial, with n = 1 associating with the mechanical
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