The spiky exoskeleton of the spearing mantis shrimp; comparative study of 3 puncturing bio-tools.

From the defensives cacti spines to the offensive felid claws and harpooning honeybee stinger, puncturing tools are found in a wide diversity of living organisms. They fulfil various roles and are based on different biological materials. Among those materials, the arthropod cuticle is often pointed out as the most versatile one. It is made of a complex helicoidal arrangement of chitin-protein fibres embedded into an organo-mineral matrix giving rise to an excellent multifunctional material serving for the organism protection and support and for all other secondary tasks as walking, sensing, or hunting. Among arthropods, impressive examples of puncturing tools can be found in the spearing mantis shrimp, an aggressive hunting crustacean known for its fast spiky appendage designed to impale prey within a fraction of second. This animal has the peculiarity to possess three puncturing tools with different roles but derived from the same basic material. Indeed, in addition to the spearing spikes used for hunting, mantis shrimps also possess defensive back spikes (the uropod spikes) to protect against predators, and maxilliped spikes for food treatment. Each of these tools must cope with specific mechanical challenges and therefore shows distinct structural and compositional adaptations. Following a multiscale structural and compositional analysis, we highlight three key adaptive strategies. All three spikes have the endocuticle subdivided into 3 functional regions. Nevertheless, the ultrastructure and the composition of the superior cuticular layers show divergent features, ranging from highly mineralized exocuticle and reduced epicuticle in the raptorial spike, to an organic and prismatic exocuticle surrounded by a bromine enriched epicuticle in the maxilliped spike and an intermediate structure in the uropod spike. This study gave a unique comparison of three different puncturing tools derived from the same structure, highlighting the incredible versatility of the arthropod cuticle.