Enamel-like stiffness achieved by poorly oriented nanocrystals in the capping tissue of Mexican beaded lizard osteoderms

Osteoderms, skeletal structures in the skin, are found in many animals and serve diverse roles. In some lizards, the bony osteoderm has a capping tissue (CT) whose composition and structure remain unknown. Here, the composition and nanostructure of osteoderms from the Mexican beaded lizard (Heloderma horridum) are investigated. The CT is highly mineralized with an extraordinarily high elastic modulus. Within the osteoderm, a transition zone between capping and bone tissue forms a graded increase in mineralization towards the superficial CT. Unlike other examples of mineralized tissues, the CT demonstrates a new combination of physical properties and nanostructural organization. It displays stiffness and hardness similar to enamel, and hydroxyapatite crystals that are an order of magnitude larger than those within the bone tissue and are, thus, reminiscent of enamel crystals. However, in stark contrast to enamel, the CT displays only minimal preferred orientation of the crystallites. Thus, it achieves very high mechanical properties with enamel-like crystal sizes but with near-isotropic microstructural orientation. The Mexican beaded lizard CT presents a highly unusual structural design resulting in high-performance mechanics. Statement of Significance: The stiffest tissue in vertebrates is enamel, which is characterized by large, highly oriented nanocrystals. The less stiff bone has smaller nanocrystals and a lower, but still high degree of texture. The osteoderms of the Mexican beaded lizard are herein investigated by a combination of mechanical testing, spatially resolved X-ray diffraction and fluorescence, and 3D X-ray imaging. Surprisingly, the osteoderms have a capping tissue with enamel-like stiffness, significantly larger crystals than the underlying bone but are much less textured. This provides a new type of design for hard biological tissues.