Bio-mimetic mechanisms of natural hierarchical materials: A review

Abstract

Natural selection and evolution develop a huge amount of biological materials in different environments (e.g. lotus in water and opuntia in desert). These biological materials possess many inspiring properties, which hint scientists and engineers to find some useful clues to create new materials or update the existing ones. In this review, we highlight some well-studied (e.g. nacre shell) and newly-studied (e.g. turtle shell) natural materials, and summarize their hierarchical structures and mechanisms behind their mechanical properties, from animals to plants. These fascinating mechanisms suggest to researchers to investigate natural materials deeply and broadly, and to design or fabricate new bio-inspired materials to serve our life.

Introduction

Nature, acting as a stealth hand, cultivates and shapes all lives in the planet (Thompson, 1945). It provides a huge amount of biological materials with different functions, such as, abalone nacre (Curry, 1977), crab exoskeleton (Chen et al., 2008a, Chen et al., 2008b, Chen et al., 2008c), turtle shell (Rhee et al., 2009), armadillo shell (Chen et al., 2011), and gecko feet (Autumn et al., 2000). Several decades ago, most of these biological materials were explored only by biologists. However, since Material Science and Engineering (MSE), a vibrant discipline, emerged in the 1950s, biological materials have been being added to its interest from the 1990s and drawn much attention due to their fascinating multi-functionality (self-organization, self-assembling, self-healing, self-cleaning, etc., Meyers et al., 2008a, Meyers et al., 2008b). For instance, on the one hand, from the point of view of mechanics, natural materials usually exhibit many interesting properties, e.g. light-weight, high-toughness (Ritchie et al., 2009), mechanical-efficiency (Wegst and Ashby, 2004), flexible-switch attaching and detaching (Tian et al., 2006), and self-cleaning properties (Cheng et al., 2006, Lepore and Pugno, 2011), etc. In particular, nacre shell, with brittle bio-mineralized tablets and a small percent of organic matrix, has excellent mechanical properties (Jackson et al., 1988, Schäffer et al., 1997, Kamat et al., 2000, Lin et al., 2006, Espinosa et al., 2011), and its toughness is approximately 3000 times greater than that of a single crystal (Song et al., 2003). On the other hand, from the point of view of other physical properties, Bejan (2000) proposed a law for the occurrence of shape and structure configurations; after that, employing the law in minimizing the body heat loss and blood pumping power, he predicted the proportionality between metabolic rate and body mass to the power 3/4 (West et al., 1997, Bejan, 2001, Bejan, 2005; Guiot et al., 2006, 2007; Brianza et al., 2007, Pugno et al., 2008a, Delsanto et al., 2008, Delsanto et al., 2009).

Inspired by these interesting phenomena, researchers start to reveal their components and find that even though natural materials, e.g. bone, show various abilities due to their different ambient environments (Srinivasan et al., 1991), they often possess two major constituents: biopolymer and bio-mineral, which are made of several fundamental elements, primarily C, N, Ca, H, O, Si (Chen et al., 2008a, Chen et al., 2008b, Chen et al., 2008c, Meyers et al., 2008a, Meyers et al., 2008b); the two constituents are often quite weak compared with their final smart “products” (Fratzl and Weinkamer, 2007). Then, questions rise: How nature can build so strong/tough materials or structures with such weak constituents? Why natural materials have a variety of structures and functions, e.g. difference between bones and tendons, though they have same constituents? What is the structure–function relationship behind these properties? Although Wegst and Ashby (2004) have established elevation indices and presented them as materials property charts/Ashby map for natural materials, how nature develops the mechanical efficiency of natural materials is still unknown. With these doubts, material scientists and engineers are devoting themselves to dig the principles and mechanisms out (Smith et al., 1999, Autumn and Peattie, 2002, Qin et al., 2009, Nova et al., 2010) and try to pave a way to fabricate bio-mimetic materials. In this regard, Fratzl (2007) provided a guideline to realize the process, which is divided into three steps: (1) Elucidating structure–function relationships of biological materials; (2) extracting the physical/chemical principles of the relationships; (3) developing manufacturing technologies to synthesize bio-inspired materials. The first step starts with experimental observations of natural materials, which give us an intuitive correlation between structure and function; then, basing on these experimental images and data, the quantitative relationships or principles between structures and functions are extracted; finally, the new bio-inspired materials are designed. In line with these steps, to date, an abundant of experimental observations and developed theories on different natural materials are obtained, such as recent developments on gecko foot (Autumn et al., 2006a, Autumn et al., 2006b, Pugno and Lepore, 2008a, Pugno and Lepore, 2008b, Varenberg et al., 2010), nacre shell (Espinosa et al., 2011), Armadillo armor (Chen et al., 2011). These studies show that hierarchical structures at several length scales, from nano- to macro-scale, determine the functions of natural materials, and the structure at each hierarchical level is optimized by Nature. Many biomimetic materials have already been synthesized, such as, gecko tape inspired by Gecko (Geim et al., 2003) and self-repairing slippery surfaces by Nepenthes (Wong et al., 2012). Several works summarized the contributions from the stand of the structure–function relationship. The earlier work can be traced to the review by Srinivasan et al. (1991); in this work, they characterized the natural materials from the features of the multi-functionality, hierarchical structures, adaptability, and reviewed the structural and mechanical properties of natural materials—wood, insect cuticle, bone and mollusk. Later, Lakes (1993) reviewed mechanical properties of several typical materials with structural hierarchy, which included man-made structures, e.g. the Eiffel tower, natural materials, e.g. tendon and hierarchical cellular solids. Recently, considering the functional adaptation (in particular, mechanics) of structures at all levels of hierarchy, Fratzl and Weinkamer (2007) summarized work on revealing basic principles, which are employed by Nature to design natural cellular materials (bone, wood, and glass sponge skeletons) and an elastomer (tendon); Buehler et al. (2008) focused on protein materials (e.g. spider silk) and employed multi-scale approaches (especially, large-scale atomistic simulations) to study and understand dynamic and fracture mechanisms that happen at nano- or meso-scale; furthermore, starting with the basic building blocks, i.e. bio-minerals, proteins and polysaccharide, Meyers et al., 2008a, Meyers et al., 2008b illustrated systematically the growth mechanism and hierarchical structures of the four types of natural materials, which are categorized according to Wegst and Ashby (2004); Espinosa et al. (2009) described the microstructure and mechanics of nacre and bone, and reviewed the fabrication of nacre-inspired artificial and related materials; Curry (2010) reviewed some less familiar bony tissues, e.g. deer's antler; Bhushan and Jung (2011), addressing the properties of natural and bio-mimetic surfaces, reviewed the latest achievements and developments; Jagota and Hui (2011) systematically reviewed recently developed bio-inspired materials and discussed the surface mechanical properties—adhesion, friction, and compliance and discussed the relationship between structural parameters and mechanical behaviors.

In this review, we focus ourselves on several selected natural materials and summarize their bio-mimetic mechanisms, which are extracted from a huge amount of literature. Nacre shell, gecko foot, mussel and spider silk are well-known natural materials and have been studied for a very long time; here, we overview some classical and recent literature to discuss respectively the toughening mechanisms for nacre shell and spider silk, and adhesion mechanism for gecko foot and mussel. As for the exoskeleton of lobster or crab, armadillo shell, turtle carapace, diatoms and plant stem, new developments on these fields are reviewed; the light-weight but mechanical-efficiency cellular structures are unveiled and the biomechanical properties are illustrated. This paper does not have the aim to present a complete review but to discuss some new and important results.