www.advmat.de www.MaterialsViews.com REVIEW Natural Flexible Dermal Armor Wen Yang , Irene H. Chen , Bernd Gludovatz , Elizabeth A. Zimmermann , Robert O. Ritchie , * and Marc A. Meyers * alligators, crocodiles, lizards, turtles) and Fish, reptiles, and mammals can possess fl exible dermal armor for protec- numerous fi sh. Four representative spe- tion. Here we seek to fi nd the means by which Nature derives its protection cies (of both extinct and current-day spe- [1–3] by examining the scales from several fi sh ( Atractosteus spatula , Arapaima cies) are shown in Figure 1 : a dinosaur ( Edmontonia ), a mammal ( Dasypus novenc- gigas , Polypterus senegalus, Morone saxatilis, Cyprinius carpio) , and osteo- inctus , armadillo), a reptile ( Dermochelys derms from armadillos, alligators, and leatherback turtles. Dermal armor has coriacea , leatherback turtle), and a fi sh clearly been developed by convergent evolution in these different species. In ( Arapaima gigas , arapaima). Despite the general, it has a hierarchical structure with collagen fi bers joining more rigid wide variation in the structure and compo- units (scales or osteoderms), thereby increasing fl exibility without signifi - sition of their armor, there is distinct com- monality: the armor is composed of rigid cantly sacrifi cing strength, in contrast to rigid monolithic mineral composites. plates connected to the body and to them- These dermal structures are also multifunctional, with hydrodynamic drag (in selves by collagen fi bers/muscles. In the fi sh), coloration for camoufl age or intraspecies recognition, temperature and case of the dinosaurs, these plates could fl uid regulation being other important functions. The understanding of such be as thick as 100 mm. In other cases, fl exible dermal armor is important as it may provide a basis for new synthetic, such as the bichir that will be discussed yet bioinspired, armor materials. in Section 3, the thickness is a few mil- limeters. In small fi sh, the scales can be fractions of a millimeter. The ratio of plate size to animal size can govern how fl exible 1. Introduction the armor is; generally, the lower the ratio, the greater the fl ex- ibility. In some cases, such as in adult sauropod dinosaurs from Protective armor can be traced to Placoderm fossils found as Madagascar, the osteoderms found isolated under the dermis many as 380 million years ago. Many dinosaurs possessed served as an internal source of calcium.[ 4 ] defensive armor, prime examples being the Stegosaurus. The Fish have, for the most part, a dermal protection arrange- clade of Thyreophora includes the Ankylosauria, huge herbiv- ment where the overlap of scales is prominent; this is some- ores that existed in the Late Cretaceous (99.6–65.5 Ma) as well what different to osteoderms. This is a necessity of the fl uid as the Stegosauria. Prior to that, fi sh with bony scales, Ostraco- mechanics requirements to minimize drag in water. The sur- derms, evolved in the Ordovican ( ∼ 500 Ma). face topography of the dermal protection layer in terrestrial ani- Many current-day animals also possess armor. These include mals is not governed by the same limitations because of the mammals (e.g., armadillos and pangolin), reptiles (e.g., much lower dynamic viscosity of air. Turtles, [ 5–7 ] armadillos, [ 8,9 ] alligators, [ 10,11 ] lizards [ 12–14 ] and other terrestrial animals tend to W. Yang, I. H. Chen, Prof. M. A. Meyers have juxtaposed plates that have different degrees of fl exibility Materials Science and Engineering Program and are connected by collagen fi bers. An exception is the pan- University of California golin, [ 15,16 ] which has overlapping keratin scales. San Diego, La Jolla, CA 92093, USA The scales of fi sh are classifi ed into four groups: pla- E-mail: [email protected] [17,18] [18,19] [17,20–22] coid, ganoid, cosmoid, and elasmoid (cycloid B. Gludovatz, E. A. Zimmermann, Prof. R. O. Ritchie [23–25] Department of Materials Science and Engineering and ctenoid). These are shown in Figure 2 together with University of California illustrations indicating their arrangement and overlap. Placoid Berkeley, CA 94720 (Figures 2 a [ 26 ] ,b) are typical scales of sharks or rays. They have E-mail: [email protected] a surface structure that generates small-scale vorticity in water, Prof. R. O. Ritchie thereby decreasing drag. [ 27 ] The ganoid scales (Figures 2 c,d) Materials Sciences Division Lawrence Berkeley National Laboratory are composed of a thin surface layer of ganoine, akin in Berkeley, CA 94720 hardness to tooth enamel, riding on a softer but tougher Prof. M. A. Meyers bony foundation. These are the hardest scales in fi sh, and are Department of Mechanical and Aerospace Engineering characteristic of the Alligator gar (Figures 2 c,d) and Senegal and Nanoengineering bichir. The elasmoid class consists of two kinds of scales, University of California cycloid and ctenoid. They have similar shapes, but there are San Diego, La Jolla, CA 92093, USA signifi cant differences. For example, the outer surface of the DOI: 10.1002/adma.201202713 cycloid is smooth while the ctenoid has a comb-like outer Adv. Mater. 2013, 25, 31–48 © 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim wileyonlinelibrary.com 31 www.advmat.de www.MaterialsViews.com surface. Some fi sh can have both cycloid and ctenoid scales as armor. Wen Yang is a postdoctoral Table 1 [ 9,10 , 19, 28–36 ] shows representative animals and their researcher in the Materials different types and sizes of scales and osteoderms as well as Science and Engineering REVIEW their primary functions. The primary function of scales and Program at the University of osteoderm is to provide protection. However, these dermal California, San Diego. She structures are also multifunctional, with hydrodynamic drag received the B.S. degree (in fi sh), [ 37–38 ] coloration for camoufl age or intraspecies rec- in Physics from Shenyang ognition, [ 39 ] luminescence, [ 27 , 40 ] temperature [ 10 , 41 ] and fl uid University of Technology, regulation [ 37 ] being other important functions. For example, and M.S. and Ph.D. degrees the U-shaped valleys in a shark scale (Figure 2 a) can reduce in Materials Science from frictional drag by up to 8% [ 27 , 38 ] and are inspiring synthetic Northeastern University in designs. Seidel [ 10 ] proposed that the bony plates of the stego- China. Her research focuses saurus could have served as heat absorbers like alligator osteo- on bioinspired materials and specifi cally on the relation- derms. In the Rapetosaurus , a dinosaur, calcium storage was an ship between structural characterization and mechanical important additional function. [ 33 ] behavior of biological materials. Robert O. Ritchie is the H.T. 2. Hierarchical Structure of Selected Animals & Jessie Chua Distinguished Professor of Engineering in One of the main reasons that these small and lightweight scales the Departments of Materials are strong is their hierarchical structure. Figure 3 shows sche- Science & Engineering and matic illustrations of the hierarchical structures of the dermal Mechanical Engineering at the armors from three selected animals. Arapaima gigas , shown University of California Berke- in Figure 3 a, is one of the largest freshwater fi sh in the world ley; he is also Senior Fac- and is native to the Amazon basin in South America. [ 42–44 ] In ulty Scientist at the Lawrence adults, the scales have dimensions of 50–100 mm in length and Berkeley National Laboratory. ∼ 40 mm in width, and are composed of two layers: an external He received B.A., M.A., Ph.D. layer about 600 μ m thick and an internal layer ∼ 1000 μ m thick. and Sc.D. degrees in physics/ The external layer is highly mineralized with ridges, while the materials science from Cambridge University, and is known internal layer contains collagen fi bers in orientations making for his research into the mechanics and mechanisms of an angle with each other that is in the range 60–75 ° . This con- fracture and fatigue of structural and biological materials. fi guration can produce the Bouligand [ 45 ] arrangement with the He is a member of the National Academy of Engineering, orientations describing a helicoid. This stacking of lamellae the U.K. Royal Academy of Engineering, and the Russian of parallel fi bers is characteristic of ctenoid scale of teleost Academy of Sciences. fi sh. [ 46–50 ] The diameter of the collagen fi bers is around 1 μ m, and they are comprised of collagen fi brils of roughly 100 nm in diameter. The arapaima scales overlap by more than 60% on Marc André Meyers , Dis- the surface, which is far more than in the alligator gar where tinguished Professor in the the scales only overlap by ∼ 30% (Figure 3 b). Departments of Nanoen- The alligator gar scale (Figure 3 b), a ganoid scale, also gineering, and Mechanical contains two layers. The outer layer, termed “ganoine”, is and Aerospace Engineering, ∼ 600 μ m thick (in adult specimens) and hard, being comprised University of California San of hydroxyapatite crystals; the inner layer is thicker ( ∼ 3500 μ m) Diego, focuses his research and consists of a bone basal layer (these dimensions naturally in the mechanical behavior scale with the size of the fi sh). Similar to the arapaima scale, of materials.He is a gradu- the external ganoine layer is highly mineralized, providing a ate of the Federal Univeristy hard-protection barrier to external attack, whereas the inner of Minas Gerais, a member bone layer with its collagen fi bers provides a “soft/buffer” layer of the Brazilian Academy of to promote toughness. However, as discussed below in Section Sciences, and writes fi ction. 3, the mechanical properties are quite different from those of the cycloid and ctenoid scales. Figure 3 c shows the hierarchical structure of osteoderm[ 9 ] in the nine-banded armadillo ( Dasypus novemcinctus ).