PROGRESS REPORT Natural Defense www.advmat.de On the Materials Science of Nature’s Arms Race Zengqian Liu, Zhefeng Zhang,* and Robert O. Ritchie* materials created by Nature, as opposed to Biological material systems have evolved unique combinations of mechanical “traditional” man-made solids. Extensive properties to fulfill their specific function through a series of ingenious research efforts have been directed to such designs. Seeking lessons from Nature by replicating the underlying principles materials, with emphasis on bamboo,[4,5] [6–8] [9–15] [16–21] of such biological materials offers new promise for creating unique combi- trees, mollusks, arthropods, birds,[22–27] fish,[28–34] mammals,[35–43] and nations of properties in man-made systems. One case in point is Nature’s human beings,[44–53] motivated not only means of attack and defense. During the long-term evolutionary “arms race,” by their unique structures and properties/ naturally evolved weapons have achieved exceptional mechanical efficiency functionalities, but also by the salient with a synergy of effective offense and persistence—two characteristics that mechanisms and underlying design prin- often tend to be mutually exclusive in many synthetic systems—which may ciples that account for their long-term perfection. present a notable source of new materials science knowledge and inspiration. Biological systems represent how a This review categorizes Nature’s weapons into ten distinct groups, and dis- wide diversity of generally composite cusses the unique structural and mechanical designs of each group by taking materials can be developed to best fulfill representative systems as examples. The approach described is to extract their specific demands using a fairly small the common principles underlying such designs that could be translated palette of chemical constituents, often into man-made materials. Further, recent advances in replicating the design with relatively meager intrinsic properties but which are environmentally friendly principles of natural weapons at differing lengthscales in artificial materials, and readily available. The combination devices and tools to tackle practical problems are revisited, and the chal- and arrangement of these constituents lenges associated with biological and bioinspired materials research in terms in biological materials are ingeniously of both processing and properties are discussed. modulated from molecular- to macrolevels to create complex, multiple lengthscale, hierarchical architectures with abundant internal gradients and interfaces.[8,38,54–61] 1. Introduction Such designs enable marked enhancements in the properties of these materials, sometimes by orders of magnitude com- The progressive synthesis of differing fields of scientific and pared to those of their constituents (Figure 2a,b).[1–3,38,62–64] In engineering endeavor has led to the emergence of a multitude light of the intricacies of Nature’s design of materials, scien- of interdisciplinary topics that are so vibrant and promising to tific endeavor in the form of biomimetics and bioinspiration attract increasing research interest yet are still far from being has begun to offer significant potential in providing creative fully exploited. Biological materials science stands out among solutions to developing unprecedented combinations of prop- these topics at the interface of the biological and physical sci- erties and functionalities in synthetic materials.[2,3,65–74] In this ences, representing the union of mechanics, physics, chem- respect, aside from the inherent difficulties in processing syn- istry, and engineering (Figure 1).[1–3] The materials-science thetic materials in the image of Nature, any success in bioin- approaches of processing, properties, characterization, and spired materials’ design rests on a sufficient knowledge about theoretical modeling have been applied to probe biological the structure and properties of biological systems and, in par- ticular, the underlying rationales and design motifs. Accord- Dr. Z. Q. Liu, Prof. Z. F. Zhang ingly, to bridge the gulf between biological materials science to Shenyang National Laboratory for Materials Science bioinspiration, biomimetics, and the actual processing of bioin- Institute of Metal Research spired materials, three sequential stages of endeavor are neces- Chinese Academy of Sciences Shenyang 110016, China sary (Figure 1): E-mail: [email protected] Dr. Z. Q. Liu, Prof. R. O. Ritchie 1) Characterizing the structure and properties/functionalities of Department of Materials Science and Engineering biological materials, especially under their specific physiological University of California Berkeley conditions, and clarifying the structure–property relationships Berkeley, CA 94720, USA which serve as the basis for any attempt to mimic them. E-mail: [email protected] 2) Understanding the mechanisms responsible for their unique The ORCID identification number(s) for the author(s) of this article can be found under https://doi.org/10.1002/adma.201705220. properties/functionalities and extracting the key design prin- ciples conferring such mechanisms—it is these principles DOI: 10.1002/adma.201705220 that need to be translated into bioinspired design as opposed Adv. Mater. 2018, 30, 1705220 1705220 (1 of 16) © 2018 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.advancedsciencenews.com www.advmat.de to a rigid replication of the naturally occurring structures per se.[65,67] Zengqian Liu is an Associate 3) Learning from Nature by implementing the biological prin- Professor in the Institute ciples in synthetic materials and components to improve of Metal Research, Chinese their performance so as to better meet the requirement for Academy of Sciences (IMR, practical application, and (perhaps the most difficult part) CAS). He received his developing processing pathways to create multiscale hierar- Ph.D. degree from Beihang chical architectures, coupled with gradients, that allow for a University in 2013. From 2013 more effective control of materials characteristics to accom- to 2015, he worked with Prof. plish it. Zhefeng Zhang at IMR, CAS as a T. S. Ke postdoctoral research fellow. He joined Among the large diversity of biomaterial systems, one critical the IMR, CAS in 2015. From feature for most organisms is the means of attack and defense. 2015 to 2017, he worked with Prof. Robert O. Ritchie at Indeed, natural weapons play a role principally for these mul- the University of California, Berkeley as a postdoctoral tiplex mechanically stringent applications, e.g., capturing and research associate. He works in the field of biological and killing prey, feeding, fighting, self-defense against predators, bioinspired structures and materials with a special focus which are vital for survival and consequently have been opti- on their mechanical properties. mized within their environmental constraints for mechanical [30,31,75–79] efficiency. Unique combinations of mechanical prop- Zhefeng Zhang is a Professor erties have been developed in these materials so that they can in the Institute of Metal maximize the offence exerted to opponents, while at the same Research, Chinese Academy time maintaining sufficient persistence by minimizing damage of Sciences (IMR, CAS). After to themselves. Both these functional features are crucial for any receiving his Ph.D. degree weapon yet tend to be mutually exclusive in a single material, from IMR, CAS in 1998, he i.e., an efficient attack in biological systems frequently results joined the IMR as a research from the use of considerable force and velocity which invariably associate. From 2000 to 2001, increases the risk of self-injury. he worked at the National In this scenario, the natural weapons represent a vast treasure Institute of Advanced trove of discoveries for fascinating structures, properties/ Industrial Science and functionalities, and design motifs created by Nature, which Technology, Japan as a JSPS may present abundant new knowledge in materials science. fellow. From 2001 to 2003, he worked with Prof. L. Schultz Of still further significance is their promising role as a rich and Prof. J. Eckert at the Institute for Metallic Materials, source of inspiration for man-made systems, specifically those IFW-Dresden, Germany. He assumed his present position for structural applications where significant impact and wear in 2004. His research focuses on the mechanical proper- resistance are desired. Unfortunately, such materials remain ties, specifically associated with the fatigue and fracture largely to be explored, especially when compared to the wealth behavior, of materials. of information on their opponents, i.e., the protective armors that provide passive defense to organisms, such as the mol- lusk shells,[9–12,14,15,61] fish and pangolin scales,[28–34,41,80,81] and Robert O. Ritchie is the Chua the turtle carapace.[82–84] In particular, to develop a high attack Distinguished Professor of efficiency in addition to a protective role, the natural weapons Engineering in the Materials have evolved a series of unique designs that distinguish Science and Engineering them from Nature’s armors and other structural materials. Department at the University Numerous hidden mechanisms and design principles associ- of California Berkeley, and ated with such weapons still need to be identified, validated, Faculty Senior Scientist at the and possibly implemented in the bioinspired materials of the Lawrence Berkeley National future. Laboratory. He holds M.A., Here, we revisit