Spring-like biomineralized hard structures : lessons from stomatopods

Abstract

Stomatopods (mantis shrimps) are aggressive predators that use a pair of ultra-fast raptorial appendages to either strike or catch prey. This remarkable fast movement is driven by a power amplification system comprising components that must be able to repetitively store and release a high amount of elastic energy, a requirement that is best accomplished if some of their structural elements combine high stiffness with flexibility. An essential component of this system is the saddle, which is used to store a significant amount of elastic energy by bending prior to striking. During repetitive bending used for the storage of a considerable amount of elastic energy prior to their fatal strikes, the saddle requires to be robust enough to sustain mechanical stresses without failure. This work comprises a comprehensive structure–chemical composition–property relationship study that sheds light on the microstructural and chemical designs of the saddle structure. Furthermore, to elucidate the role of the compositional variations in the saddle structure, quasi-static and dynamic mechanical properties of the saddle were investigated. To correlate the micro-scale chemo-structural and micro-mechanical properties with the functionality of the whole structure, finite element analysis was conducted. MicroCT scans combined with electron microscopy imaging, Energy Dispersive Spectroscopy (EDS) mapping, as well as confocal Raman microscopy show that the saddle is a bi-material layer structure, with sharp changes in chemical composition and microstructure between the layers. The outer layer of the saddle is largely made of amorphous mineral phases, whereas the inner layer is predominantly an organic chitin/protein complex with a lower relative mineral content. The inorganic/organic phase distribution correlates with nano-mechanical mapping, with the outer (inorganic) layers being stiffer than the inner layers. With this design, regions of the saddle loaded in compression are primarily made of stiffer inorganic phases that can sustain higher compressive stresses, whereas regions loaded in tension contain a higher relative amount of biopolymeric components. Nanoscale Dynamic Mechanical Analysis (NanoDMA) studies show that the outer layer plays the key role of storing the elastic energy, with a significantly higher storage modulus than the inner layer, while the inner layers mainly acts as a structural support that sustains tensile stresses. 3D finite element analysis (FEA) quantifies the stress level and provides visualization of the stress distribution in the saddle under compressive bending. Comparing the FEA results with the elastic-plastic properties of the saddle extracted from nanoindentation demonstrates that no plastic deformation occurs in the saddle during bending. The thesis reveals that the saddle’s chemical composition and microstructure have been spatially tuned to generate a stiff, yet flexible structure that is optimized for storage of elastic energy. This structure takes advantage of this spatial distribution and geometry to impose a neutral surface right at the interface of the two layers, and to generate a uniform stress distribution that likely enhances the resistance to mechanical fatigue. This comprehensive compositional, geometrical and mechanical study provides bio-inspired insights that could find wide usage in composite materials science.