Elasmoid fish scales as a natural fibre composite: microscopic heterogeneities in structure, mineral distribution, and mechanical properties.

Abstract

The elasmoid scales in teleost fish serve as exemplary models for natural fibre composites with integrated flexibility and protection. Yet, limited research has been focused on the potential structural, chemical, and mechanical heterogeneity within individual scales. This study presents systematic characterizations of the elasmoid scales from black drum fish (Pogonias cromis) at different zones within individual scales as a natural fibre composite, focusing on the microscopic structural heterogeneities and corresponding mechanical effects. The focus field at the centre of the scales exhibits a classical tri-layered collagen-based composite design, consisting of the mineralized outermost limiting layer, external elasmodine layer in the middle, and the unmineralized internal elasmodine layer. In comparison, the rostral field at the anterior end of the scales exhibits a two-layered design: the mineralized outermost limiting layer exhibits radii sections on the outer surface, and the inner elasmodine layer consists of collagen fibre-based sublayers with alternating mineralization levels. Chemical and nanoindentation analysis suggests a close correlation between the mineralization levels and the local nanomechanical properties. Comparative finite element modelling shows that the rostral-field scales achieve increased flexibility under both concave and convex bending. Moreover, the evolving geometries of isolated Mandle's corpuscles in the internal elasmodine layer, transitioning from irregular shapes to faceted octahedrons, suggest the mechanisms of mineral growth and space-filling to thicken the mineralized layers in scales during growth, which enhances the bonding strength between the adjacent collagen fibre layers. This work offers new insights into the structural variations in individual elasmoid scales, providing strategies for bioinspired fibre composite designs with local-adapted functional requirements.