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...

Full description

Bibliographic Details
Main Authors: Yann Delaunois, Alexandra Tits, Quentin Grossman, Sarah Smeets, Cédric Malherbe, Gauthier Eppe, G. Harry vanLenthe, Davide Ruffoni, Philippe Compère
Format: Article
Language:English
Published: Wiley-VCH 2023-07-01
Series:Natural Sciences
Subjects:
Online Access:https://doi.org/10.1002/ntls.20220060
_version_ 1797786753477640192
author Yann Delaunois
Alexandra Tits
Quentin Grossman
Sarah Smeets
Cédric Malherbe
Gauthier Eppe
G. Harry vanLenthe
Davide Ruffoni
Philippe Compère
author_facet Yann Delaunois
Alexandra Tits
Quentin Grossman
Sarah Smeets
Cédric Malherbe
Gauthier Eppe
G. Harry vanLenthe
Davide Ruffoni
Philippe Compère
author_sort Yann Delaunois
collection DOAJ
description 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.
first_indexed 2024-03-13T01:12:21Z
format Article
id doaj.art-1770541bafc04e7cbc87c2d8788819c1
institution Directory Open Access Journal
issn 2698-6248
language English
last_indexed 2024-03-13T01:12:21Z
publishDate 2023-07-01
publisher Wiley-VCH
record_format Article
series Natural Sciences
spelling doaj.art-1770541bafc04e7cbc87c2d8788819c12023-07-05T16:05:48ZengWiley-VCHNatural Sciences2698-62482023-07-0133n/an/a10.1002/ntls.20220060Design strategies of the mantis shrimp spike: How the crustacean cuticle became a remarkable biological harpoonYann Delaunois0Alexandra Tits1Quentin Grossman2Sarah Smeets3Cédric Malherbe4Gauthier Eppe5G. Harry vanLenthe6Davide Ruffoni7Philippe Compère8Laboratory of Functional and Evolutionary Morphology FOCUS Research Unit, Department of Biology, Ecology and Evolution, University of Liège Liège BelgiumMechanics of Biological and Bioinspired Materials Laboratory Department of Aerospace and Mechanical Engineering, University of Liège Liège BelgiumMechanics of Biological and Bioinspired Materials Laboratory Department of Aerospace and Mechanical Engineering, University of Liège Liège BelgiumLaboratory of Functional and Evolutionary Morphology FOCUS Research Unit, Department of Biology, Ecology and Evolution, University of Liège Liège BelgiumMass Spectrometry Laboratory MolSys Research Unit, Department of Chemistry, University of Liège Liège BelgiumMass Spectrometry Laboratory MolSys Research Unit, Department of Chemistry, University of Liège Liège BelgiumDepartment of Mechanical Engineering KU Leuven Leuven BelgiumMechanics of Biological and Bioinspired Materials Laboratory Department of Aerospace and Mechanical Engineering, University of Liège Liège BelgiumLaboratory of Functional and Evolutionary Morphology FOCUS Research Unit, Department of Biology, Ecology and Evolution, University of Liège Liège BelgiumAbstract 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.https://doi.org/10.1002/ntls.20220060biocompositecrustaceanharpoonhigh stiffness and toughnessstomatopodspike
spellingShingle Yann Delaunois
Alexandra Tits
Quentin Grossman
Sarah Smeets
Cédric Malherbe
Gauthier Eppe
G. Harry vanLenthe
Davide Ruffoni
Philippe Compère
Design strategies of the mantis shrimp spike: How the crustacean cuticle became a remarkable biological harpoon
Natural Sciences
biocomposite
crustacean
harpoon
high stiffness and toughness
stomatopod
spike
title Design strategies of the mantis shrimp spike: How the crustacean cuticle became a remarkable biological harpoon
title_full Design strategies of the mantis shrimp spike: How the crustacean cuticle became a remarkable biological harpoon
title_fullStr Design strategies of the mantis shrimp spike: How the crustacean cuticle became a remarkable biological harpoon
title_full_unstemmed Design strategies of the mantis shrimp spike: How the crustacean cuticle became a remarkable biological harpoon
title_short Design strategies of the mantis shrimp spike: How the crustacean cuticle became a remarkable biological harpoon
title_sort design strategies of the mantis shrimp spike how the crustacean cuticle became a remarkable biological harpoon
topic biocomposite
crustacean
harpoon
high stiffness and toughness
stomatopod
spike
url https://doi.org/10.1002/ntls.20220060
work_keys_str_mv AT yanndelaunois designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon
AT alexandratits designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon
AT quentingrossman designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon
AT sarahsmeets designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon
AT cedricmalherbe designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon
AT gauthiereppe designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon
AT gharryvanlenthe designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon
AT davideruffoni designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon
AT philippecompere designstrategiesofthemantisshrimpspikehowthecrustaceancuticlebecamearemarkablebiologicalharpoon