Design Strategies of the Mantis Shrimp Spike: How the Crustacean
Cuticle Became a Remarkable Biological Harpoon?
Yann Delaunois1, Alexandra Tits2,
Quentin Grossman2, Sarah Smeets1,
Cédric Malherbe3, Gauthier Eppe3, G.
Harry van Lenthe4, Davide Ruffoni2*and Philippe Compère1,5*
1Laboratory of Functional and Evolutionary Morphology,
FOCUS Research Unit, Department of Biology, Ecology and Evolution,
University of Liège, Liège, Belgium.
2Mechanics of Biological and Bioinspired Materials
Laboratory, Department of Aerospace and Mechanical Engineering,
University of Liège, Liège, Belgium.
3Mass Spectrometry Laboratory, MolSys Research Unit,
Department of Chemistry, University of Liège, Liège, Belgium.
4Department of Mechanical Engineering, KU Leuven,
Leuven, Belgium.
5Center for Applied Research and Education in
Microscopy (CAREM) and Biomaterials Interfaculty Center (CEIB),
University of Liège, Liège, Belgium.
*Equal supervision of the work and corresponding authors.
Corresponding authors:
Davide Ruffoni, druffoni@uliege.be
Department of Aerospace and Mechanical Engineering
University of Liege
Quartier Polytech 1, Allée de la Découverte 9
B-4000 Liège, Belgium
Philippe Compère, pcompere@uliege.be
Department of Biology, Ecology and Evolution,
University of Liège
Quartier Agora, Allée du six Août 15
B-4000 Liège, Belgium
ABSTRACT
Spearing mantis shrimps are aggressive crustaceans using specialized
appendages with sharp spikes to capture fishes with a fast movement.
Each spike is a biological tool that have 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.