The structure of the stomatopod dactyl club--an ultrafast, hammer-like device used by the animal to shatter hard seashells--offers inspiration for impact-tolerant ceramics. Here, we present the micromechanical principles and related micromechanisms of deformation that impart the club with high impact tolerance. By using depth-sensing nanoindentation with spherical and sharp contact tips in combination with post-indentation residual stress mapping by Raman microspectroscopy, we show that the impact surface region of the dactyl club exhibits a quasi-plastic contact response associated with the interfacial sliding and rotation of fluorapatite nanorods, endowing the club with localized yielding. We also show that the subsurface layers exhibit strain hardening by microchannel densification, which provides additional dissipation of impact energy. Our findings suggest that the club's macroscopic size is below the critical size above which Hertzian brittle cracks are nucleated.

Stomatopods are aggressive crustacean predators that use a pair of ultrafast raptorial appendages to strike on prey. This swift 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. An essential component of this system is the saddle structure, in which the elastic energy is stored by bending prior to striking. Here, a comprehensive study that sheds light on the microstructural and chemical designs of the stomatopod's saddle is conducted. MicroCT scans combined with electron microscopy imaging, elemental mapping, high‐resolution confocal Raman microscopy, and nanomechanical mapping show that the saddle is a bilayer structure with sharp changes in chemical composition and mechanical properties between the layers. The outer layer is heavily mineralized whereas the inner layer contains a high content of chitin and proteins, leading to a spatial organization of phases which is optimized for load distribution during saddle bending. The mineralized outer layer sustains compressive stresses, whereas the inner biopolymeric layer provides tensile resistance. These findings reveal that the saddle chemical composition and microstructure have been spatially tuned to generate a stiff, yet flexible structure that is optimized for storage of elastic energy.

Biomineralization, the process by which mineralized tissues grow and harden via biogenic mineral deposition, is a relatively lengthy process in many mineral-producing organisms, resulting in challenges to study the growth and biomineralization of complex hard mineralized tissues. Arthropods are ideal model organisms to study biomineralization because they regularly molt their exoskeletons and grow new ones in a relatively fast timescale, providing opportunities to track mineralization of entire tissues. Here, we monitored the biomineralization of the mantis shrimp dactyl club—a model bioapatite-based mineralized structure with exceptional mechanical properties—immediately after ecdysis until the formation of the fully functional club and unveil an unusual development mechanism. A flexible membrane initially folded within the club cavity expands to form the new club’s envelope. Mineralization proceeds inwards by mineral deposition from this membrane, which contains proteins regulating mineralization. Building a transcriptome of the club tissue and probing it with proteomic data, we identified and sequenced Club Mineralization Protein 1 (CMP-1), an abundant mildly phosphorylated protein from the flexible membrane suggested to be involved in calcium phosphate mineralization of the club, as indicated by in vitro studies using recombinant CMP-1. This work provides a comprehensive picture of the development of a complex hard tissue, from the secretion of its organic macromolecular template to the formation of the fully functional club.

In the absence of minerals as stiffening agents, insects and spiders often use metal‐ion cross‐linking of protein matrices in their fully organic load‐bearing “tools.” In this comparative study, the hierarchical fiber architecture, elemental distribution, and the micromechanical properties of the manganese‐ and calcium‐rich cuticle of the claws of the spider Cupiennius salei, and the Zn‐rich cuticle of the cheliceral fangs of the same animal are analyzed. By correlating experimental results to finite element analysis, functional microstructural and compositional adaptations are inferred leading to remarkable damage resilience and abrasion tolerance, respectively. The results further reveal that the incorporation of both zinc and manganese/calcium correlates well with increased biomaterial's stiffness and hardness. However, the abrasion‐resistance of the claw material cross‐linked by incorporation of Mn/Ca‐ions surpasses that of many other non‐mineralized biological counterparts and is comparable to that of the fang with more than triple Zn content. These biomaterial‐adaptation paradigms for enhanced wear‐resistance may serve as novel design principles for advanced, high‐performance, functional surfaces, and graded materials.

SummaryStomatopods deliver one of the fastest strikes in the animal kingdom using their powerful “dactyl clubs.” This kinematic performance is enabled by a power amplification device whereby elastic energy is stored in a saddle-shape mineralized bilayer structure. We combined a set of comprehensive micro-mechanical measurements with finite element modeling (FEM) to quantitatively elucidate the saddle biomechanical design. Dynamic nano-scale testing reveals that viscoelastic dissipation is minimized in the highly mineralized layer, whereas micro-bending experiments on miniature cantilevers highlight the critical role of the bilayer arrangement in optimizing storage of elastic energy. FEM shows that the saddle shape prevents stress concentration and the stresses remain well within the elastic range during loading, while the neutral surface coincides with the bilayer interface to prevent interfacial delamination. The study unveils the multi-scale design behind the intriguing ability of the saddle to store a high density of elastic energy using stiff but intrinsically brittle materials.Video Abstract

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The evolution success of crustaceans is largely due to the diversification of their mineralized exoskeletons and hunting appendages, which exhibit a large palette of morphometric characteristics that have adapted to meet particular functions. We explored the "snapper claw" of the pistol shrimp, which is used to generate cavitation bubbles and strike prey. Our multi-scale structure-property relationship study reveals that the snapper claw is more brittle than other fast raptorial appendages - such as the stomatopod dactyl club - because it is not directly subjected to direct contact forces during action. This study implies that when higher mechanical stresses are needed to meet the function, the internal structure is built of a more complex architecture that allows to mitigate internal structural damage.