Toughening, micromechnics, and multi-scale structural analyses of high-performance biotools

Abstract

Through millions of years of evolution, living organisms have refined a wide range of biomineralized tissues to meet the key functional requirements that are central to their survival. This includes load-bearing elements and protective armor that must display adequate stiffness and strength or sharp and cutting "biotools" that are key in predation and feeding. These mineralized tissues exhibit multi-scale hierarchical structures to meet their functional requirements, with a precise organization of their building blocks to optimize the combination of their mechanical properties including stiffness, strength, and fracture resistance. A distinctive model system that has gathered recent interest is the dactyl club from stomatopods (mantis shrimps). In comparison to many biomineralized composites that play a passive (defensive) mechanical role, dactyl clubs are dynamically active, hammerlike devices which are used by stomatopods to shatter the hard shells of their prey through repetitive impact loading. The mantis shrimp appendage is one of the most fascinating multifunctional biological material "biotools" in the animal kingdom, which the animal uses for its aggressive predatory strategies. Its hierarchical structure helps to strike and catch its prey 50 times faster than the blink of an eye, while exhibiting exceptional damage tolerance properties. In this research project, the multi-scale hierarchical structure and chemical composition of mantis shrimp appendages was comprehensively probed by various analytical techniques. It is demonstrated that dactyl impact surface consists of a finelytuned mineral gradient, with fluorapatite substituting amorphous apatite towards the outer surface. Raman spectroscopy measurements show that calcium sulphate, previously not reported in mechanically active biotools, is co-localized with fluorapatite. Ab initio computations suggest that fluorapatite/calcium sulphate interfaces provide binding stability and promote the disordered-to-ordered transition of fluorapatite. Hertzian contact partial loading-unloading indentation measurements revealed that the different layers of the club possess distinctive deformation and energy dissipation mechanisms. High-resolution electron microscopic studies show that sliding and rotation of fluorapatite crystallites leads to a quasi-plastic response in the outer, impact layer of Abstract ii the club. On the other hand, the presence of micro-channels along mineralized chitin fibrils in the inner layer of the club results in a distinct contact mechanics response. Under hydrated conditions, densification of these micro-channels under compressive load leads to a strain hardening behavior in the inner layer of the club. The work demonstrates that the macroscopic size of the club is below the critical size above which Hertizan cone fracture could be formed. Instead, the club's response remains in the quasi-plastic regime.