Reinforcement and adaptation of the mantis shrimp spike: how crustacean cuticle became a perfect harpoon?

Introduction: In the field of bioinspired material, the crustacean cuticle is seen as an example of organo-mineral biomaterial able to endure strong stress thanks to the combination of fibrilar organisation and mineral deposition. Stomatopoda is a crustacean order represented by two groups of species; smashing mantis shrimps and spearing mantis shrimps. Hence, the first group is already well studied for the mechanical abilities of their smashing limbs, this study will focus on the spearing mantis shrimps and their spearing appendage. These appendage present spikes able to impale fish in a fraction of second and are therefore designed to penetrate at high speed, to avoid escape of the prey but also to resist bending during the capture.
Objective: The aim of this study is to determine how the mantis shrimp cuticle adapts its shape, internal organization and composition to endure the intense stress occurring during attacks.
Materials and methods: Specimens of Lysiosquillina maculata were dissected and their spikes were conserved in ethanol or fixed with glutaraldehyde. The samples in ethanol were then embedded in resin and polished to be observed in µCTscan and SEM and analyzed by EDS and nanoindentation. Sample fixed in glutaraldehyde were contrast with OsO4 and embedded in resin to be observed in TEM.
Results: Firstly, the µCTscan highlighted particular features in the external structure, the spike presenting serrations at its edges linked by grooves at its sides. It also show a curvature linked to the angle of attack of the mantis shrimp. But its internal organization also shows important rearrangements in comparison to the classic crustacean cuticle. These rearrangements affect even the arrangement of chitino-proteic fibers as the composition of the mineral. SEM-BSE and TEM observation highlight that the spike cuticle does not show a clear subdivision in the three classical layer found in arthropod cuticle i.e. endo-, exo, and epicuticle but consist in four layer with different organization. These layers are respectively called from the surface to the epidermis: the highly mineralized layer (HML), the outer helicoidal layer (OHL), the striated layer (STL) and the inner helicoidal layer (IHL). EDS analysis also shows that theses layers also present different composition and mineralization rate; the HML has the higher mineralization rate and is composed of flurapatite, the HML has the lower mineralization rate and is, as the OHL and STL, composed of a mix between calcium phosphate and calcium carbonate. The three innermost layers are also characterized by variation in the substitution rates of minor element as Na, K, Mg and F. Analysis of the spike cuticle with nanoindentation tests highlight variation in the reduced modulus between the layers.
Conclusion: During its evolution, the spearing mantis shrimp has strongly modified its exoskeleton either in structure and mineral composition in order to perfectly suit its mechanical constraint. Variation of its internal organization seems to be adapted to endure with anisotropic stresses. On its side, modification of the composition in the mineral part raised its surface reduced modulus and hardness at value comparable with vertebrate teeth. Finally, by both structural and mineral variation, the cuticle spike is also thought to cope with cracks propagations.