The natural armor of fish: an exploration of a biological composite

Abstract

In the search for advanced structural materials, scientists are finding inspiration from materials in nature and biological composites. The need for lighter protective materials has directed attention to armored skins, which possess a combination of flexibility, puncture resistance and capacity for energy dissipation. This rare combination of properties is found in the armored skin of modern fish, and achieved by overlapping scales with exceptional specific strength and toughness. Research on these materials has focused on their mechanical properties, with limited regard for the microstructure and potential spatial variations over the fish body. If fish scales will serve to inspire future generations of flexible wearable armor, a better understanding of the relationships between structure and properties is essential. Therefore, the main objectives of this research were to develop new understanding on the constituent layers and lamination patterns of elasmoid scales from teleost fish, and understand their importance to the mechanical properties relevant to armor performance. The investigation consists of five aims that address properties of the scales as a structural material, the spatial variations over the body of fish, the microstructure and properties of the individual layers, and the design and performance of the interface between these layers. This investigation enrolled a combination of experimental, analytical and numerical efforts to achieve the aims. An exploration of scales from Cyprinus carpio showed that the fracture resistance of elasmoid fish scales is largely dependent on the anatomical position and the corresponding microstructure. Elasmoid scales were found to consist of three principle layers, including the external highly mineralized limiting layer (LL), as well as the external (EE) and internal (IE) elasmodine, which consist of a number of lamina (or plies) of unidirectional type I collagen fibrils. While the fracture resistance increased with scale thickness, it was highly correlated with the number of plies in the elasmodine and ratio of mineralized plies in the EE. Furthermore, the hierarchical structure of the scales and the molecular level bonds were found to be of importance. Removal of the intra molecular water enabled inter-peptide bonding of the collagen fibrils, which increased the strength and elastic modulus. Furthermore, mineral crystals at the intra-fibrilar spaces impeded the formation of new inter-peptide bonds and reduced the degree of toughening achieved. Through an evaluation of the laminate structural characteristics, it was found that the ply stacking sequence and the distribution of mineralized plies play a key role on the mechanical response of fish scales. In light of that importance, this study was the first to fully characterize the lamination patterns of fish scales from different species, to distinguish differences in the LL thickness and the EE ratio between species and across anatomical locations, and connect those qualities to their unique needs for locomotion and protection. Results from this phase of the investigation detailed the differences in microstructure between selected fish species, the need to characterize the microstructure of the scales in characterizing the structural behavior and how spatial variations in structural behavior are achieved through modulation of the LL and EE. An analytical model was developed for the elastic properties of scales that describes the elastic behavior in terms of the relative contributions of the LL and the EE and IE. The mechanical properties of scales from the Megalops atlanticus (i.e. tarpon) were characterized in tension and compared with predictions from the model. The average error between the predictions and experimental properties was 7%. It was found that the mineralization gradient and aspect ratio of the apatite crystals in the LL played the most important roles on the elastic modulus of the scales. Furthermore, misalignment of the EE plies was shown to reduce the elastic modulus significantly and is one approach that appears to be employed by fish to modulate the scale flexibility for a specific mineral content that is required for protection. The detailed exploration of the limiting layer revealed a suture-like transition area between the LL and the EE in both carp and tarpon scales. This region was found to exhibit a geometry akin to the distribution of circuli that are formed by mineral protrusions on the surface of the scale. The effect of the LL profile and suture line geometry on the structural behavior of the scales and bioinspired analogues was studied using complementary experimental and numerical efforts. Results showed that the bending stiffness and work to fracture of the scales in flexure decrease with increasing amplitude and decreasing wavelength of the LL profile. Furthermore, the gradient in elastic modulus of the suture region was instrumental in the scale flexibility. The structural behavior of the scales can be effectively tuned by the suture line shape, its relative position in the LL and the LL profile. The results establish the potential for tailoring the mechanical response of flexible composite laminates by carefully adjusting the layer architectures and their interfaces. The suture line geometry appears to play a key role on the scale protecto-flexibility, and can help extend the possibilities for bioinspiration derived from scales well beyond applications for body protection.