Design strategies of the mantis shrimp spike: How the crustacean cuticle became a remarkable biological harpoon

Abstract

Spearing mantis shrimps are aggressive crustaceans using specialized appendages with sharp spikes to capture fishes with fast movement. Each spike is a biological tool that has to combine high toughness, as required by the initial impact with the victim, with high stiffness and strength, to ensure sufficient penetration while avoid breaking. We performed a multimodal analysis to uncover the design strategies of this harpoon based on chitin. We found that the spike is a slightly hooked hollow beam with the outer surface decorated by serrations and grooves to enhance cutting and interlocking. The cuticle of the spike resembles a multilayer composite: An outer heavily mineralized, stiff, and hard region (with average indentation modulus and hardness of 68 and 3 GPa), providing high resistance to contact stresses, is combined with a less mineralized region, which occupies a large fraction of the cuticle (up to 50%) and features parallel fibers oriented longitudinally, enhancing stiffness and strength. A central finding of our work is the presence of a tiny interphase (less than 10 μm in width) based on helical fibers and showing a spatial modulation in mechanical properties, which has the critical task to integrate the stiff but brittle outer layer with the more compliant highly anisotropic parallel‐fiber region. We highlighted the remarkable ability of this helicoidal region to stop nanoindentation‐induced cracks. Using three‐dimensional multimaterial printing to prototype spike‐inspired composites, we showed how the observed construction principles can not only hamper damage propagation between highly dissimilar layers (resulting in composites with the helical interphase absorbing 50% more energy than without it) but can also enhance resistance to puncture (25% increase in the force required to penetrate the composites with a blunt tool). Such findings may provide guidelines to design lightweight harpoons relying on environmentally friendly and recyclable building blocks. Key Points –The heavily mineralized biological appendages of the mantis shrimp are a constant source of inspiration for developing new engineering materials. –We use characterization methods of material science to investigate a biological harpoon based on chitin. –Several morphological, compositional, microstructural, and biomechanical features are highlighted, allowing the spikes of the mantis shrimp to be remarkable lightweight, tough, and stiff harpoons.

Structural diversity of crustacean exoskeletons and its implications for biomimetics

“…The preferential orientation of the organic fibres in the longitudinal direction of elongated skeletal elements results in a mechanical anisotropy of the cuticle that contrasts the isotropic mechanical properties of the Bouligand structure. This has been demonstrated in isopods [ 39 , 40 ] as well as in mantis shrimps [ 14 ].…”

“…This fibre organization, universally present among arthropods, has been referred to as the twisted plywood structure or the Bouligand structure [ 13 ]. It provides the cuticle with isotropic mechanical properties in the plane of the cuticle [ 14 ]. The number and thickness of lamellae in the cuticle differ between layers of the cuticle [ 15 ], between regions of the body [ 6 ] and between species [ 16 , 17 ].…”

“…This is a characteristic of isopod incisor processes and claws, amphipod mouthparts, and tips of claws in some crabs. Both approaches can result in less wear under certain conditions [ 14 , 53 ] and it is possible that different uses of a structure favour a different strategy. Mantis shrimp raptorial appendages penetrate prey, necessitating a hard surface, whereas the claws of terrestrial isopods do not and may instead reduce wear by being covered in flexible cuticle.…”

“…The presence of amorphous minerals in the inner layers of the cuticle and crystalline phases in the external layers has often been interpreted mechanically as an adaptive feature that increases fracture resistance. The strengthening of a material by this arrangement of stiffer and more pliant layers has been demonstrated experimentally [ 14 ]. An alternative interpretation has also been proposed, however: amorphous minerals in the inner layers of the cuticle are much more soluble than crystalline ones, and it has been shown that the mineral in these layers is resorbed before the moult [ 12 , 24 , 46 ].…”

“…The effect of fibre organization on crack propagation in the exoskeleton has been examined by nanoindentation followed by scanning electron microscopy and by in situ experiments using transmission electron microscopy [ 33 ]. By examining the failure of the mantis shrimp's spike cuticle and synthetic approximations of the spike cuticle, it has been demonstrated that a layer of Bouligand structure between the hard exterior and the flexible interior effectively limits crack propagation and failure of the spine [ 14 ].…”