Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles

Grunenfelder, Lessa Kay; Milliron, Garrett; Herrera, Steven; Gallana, Isaias; Yaraghi, Nicholas; Hughes, Nigel; Evans-Lutterodt, Kenneth; Zavattieri, Pablo; Kisailus, David

doi:10.1002/adma.201705295

Title: Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles

Abstract

Ecological pressures and varied feeding behaviors in a multitude of organ-isms have necessitated the drive for adaptation. One such change is seen in the feeding appendages of stomatopods, a group of highly predatory marine crustaceans. Stomatopods include “spearers,” who ambush and snare soft bodied prey, and “smashers,” who bludgeon hard-shelled prey with a heavily mineralized club. The regional substructural complexity of the stomatopod dactyl club from the smashing predator Odontodactylus scyllarus represents a model system in the study of impact tolerant biominerals. The club consists of a highly mineralized impact region, a characteristic Bouligand architec-ture (common to arthropods), and a unique section of the club, the striated region, composed of highly aligned sheets of mineralized fibers. Detailed ultrastructural investigations of the striated region within O. scyllarus and a related species of spearing stomatopod, Lysiosquillina maculate show consistent organization of mineral and organic, but distinct differences in macro-scale architecture. Evidence is provided for the function and substructural exaptation of the striated region, which facilitated redeployment of a rapto-rial feeding appendage as a biological hammer. Furthermore, given the need to accelerate underwater and “grab” or “smash” their prey, the spearer and smasher appendages are specifically designed with a significantly reduced drag force.

Authors:

Grunenfelder, Lessa Kay ^[1]; Milliron, Garrett ^[1]; Herrera, Steven ^[1]; Gallana, Isaias ^[2]; Yaraghi, Nicholas ^[1]; Hughes, Nigel ^[1]; Evans-Lutterodt, Kenneth ^[3]; Zavattieri, Pablo ^[4];

^[1]

Univ. of California, Riverside, CA (United States)
Purdue Univ., West Lafayette, IN (United States); Univ. Nacional de La Plata, Buenos Aires (Argentina)
Brookhaven National Lab. (BNL), Upton, NY (United States)
Purdue Univ., West Lafayette, IN (United States)

Publication Date:: Tue Jan 16 00:00:00 EST 2018

Research Org.:: Brookhaven National Lab. (BNL), Upton, NY (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

OSTI Identifier:: 1436264

Report Number(s):: BNL-203618-2018-JAAM
Journal ID: ISSN 0935-9648

Grant/Contract Number:: SC0012704

Resource Type:: Accepted Manuscript

Journal Name:: Advanced Materials

Additional Journal Information:: Journal Volume: 30; Journal Issue: 9; Journal ID: ISSN 0935-9648

Publisher:: Wiley

Country of Publication:: United States

Language:: English

Subject:: 36 MATERIALS SCIENCE; biominerals; composites; impact; toughness; ultrastructure

Citation Formats


                    Grunenfelder, Lessa Kay, Milliron, Garrett, Herrera, Steven, Gallana, Isaias, Yaraghi, Nicholas, Hughes, Nigel, Evans-Lutterodt, Kenneth, Zavattieri, Pablo, and Kisailus, David. Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles.  United States: N. p., 2018. 
Web.  doi:10.1002/adma.201705295.

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                    Grunenfelder, Lessa Kay, Milliron, Garrett, Herrera, Steven, Gallana, Isaias, Yaraghi, Nicholas, Hughes, Nigel, Evans-Lutterodt, Kenneth, Zavattieri, Pablo, & Kisailus, David. Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles.  United States.  https://doi.org/10.1002/adma.201705295

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                    Grunenfelder, Lessa Kay, Milliron, Garrett, Herrera, Steven, Gallana, Isaias, Yaraghi, Nicholas, Hughes, Nigel, Evans-Lutterodt, Kenneth, Zavattieri, Pablo, and Kisailus, David. Tue .  
"Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles".  United States.  https://doi.org/10.1002/adma.201705295.  https://www.osti.gov/servlets/purl/1436264.

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@article{osti_1436264,

  title        = {Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles},

  author       = {Grunenfelder, Lessa Kay and Milliron, Garrett and Herrera, Steven and Gallana, Isaias and Yaraghi, Nicholas and Hughes, Nigel and Evans-Lutterodt, Kenneth and Zavattieri, Pablo and Kisailus, David},

  abstractNote = {Ecological pressures and varied feeding behaviors in a multitude of organ-isms have necessitated the drive for adaptation. One such change is seen in the feeding appendages of stomatopods, a group of highly predatory marine crustaceans. Stomatopods include “spearers,” who ambush and snare soft bodied prey, and “smashers,” who bludgeon hard-shelled prey with a heavily mineralized club. The regional substructural complexity of the stomatopod dactyl club from the smashing predator Odontodactylus scyllarus represents a model system in the study of impact tolerant biominerals. The club consists of a highly mineralized impact region, a characteristic Bouligand architec-ture (common to arthropods), and a unique section of the club, the striated region, composed of highly aligned sheets of mineralized fibers. Detailed ultrastructural investigations of the striated region within O. scyllarus and a related species of spearing stomatopod, Lysiosquillina maculate show consistent organization of mineral and organic, but distinct differences in macro-scale architecture. Evidence is provided for the function and substructural exaptation of the striated region, which facilitated redeployment of a rapto-rial feeding appendage as a biological hammer. Furthermore, given the need to accelerate underwater and “grab” or “smash” their prey, the spearer and smasher appendages are specifically designed with a significantly reduced drag force.},

  doi          = {10.1002/adma.201705295},

  journal      = {Advanced Materials},

  number       = 9,

  volume       = 30,

  place        = {United States},

  year         = {Tue Jan 16 00:00:00 EST 2018},

  month        = {Tue Jan 16 00:00:00 EST 2018}

}

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https://doi.org/10.1002/adma.201705295

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Cited by: 39 works

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Figures / Tables:

Figure 1: Stomatopods are divided into two groups based on the structure of their feeding appendage. The structure of the dactyl from the second maxilliped enables the identification of: A) a bulbous hammer from the smasher O. scyllarus and B) a harpoon-like raptorial appendage from the spearer L. maculate.

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Title: Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles

Abstract

Citation Formats

Figures / Tables:

Twisting cracks in Bouligand structures journal, December 2017

Scanning X-ray microdiffraction of complex materials: Diffraction geometry considerations journal, January 2003

Stomatopod predation on fossil gastropods from the Plio-Pleistocene of Florida journal, May 1991

The phylogeny of the stomatopod Crustacea journal, January 2000

Comparative spring mechanics in mantis shrimp journal, December 2012

Adaptive FEM computation of geometric and material nonlinearities with application to brittle failure journal, August 1998

Enamel inspired nanocomposite fabrication through amelogenin supramolecular assembly journal, July 2007

Pore canal shape related to molecular architecture of arthropod cuticle journal, January 1969

A Sinusoidally Architected Helicoidal Biocomposite journal, May 2016

Linkage mechanics and power amplification of the mantis shrimp's strike journal, October 2007

The Stomatopod Dactyl Club: A Formidable Damage-Tolerant Biological Hammer journal, June 2012

Modularity and Scaling in fast Movements: Power Amplification in Mantis Shrimp: Modularity and Scaling of Power Amplification journal, October 2010

Torsional Strengthening of Spandrel Beams with Fiber-Reinforced Polymer Laminates journal, April 2004

Palaeo- and archaeostomatopods (Hoplocarida, Crustacea) from the Bear Gulch Limestone, Mississippian (Namurian), of central Montana journal, January 1998

On the architecture and function of cuttlefish bone journal, July 1983

Bio-inspired impact-resistant composites journal, September 2014

Revealing the Design Principles of High-Performance Biological Composites Using Ab initio and Multiscale Simulations: The Example of Lobster Cuticle journal, January 2010

Paleozoic Proto-Mantis Shrimp Revisited journal, September 2007

Evolution of mantis shrimps (Stomatopoda, Malacostraca) in the light of new Mesozoic fossils journal, January 2010

Dynamic, multiaxial impact response of confined and unconfined ceramic rods conference, January 1994

Flexural–torsional buckling of fiber-reinforced plastic composite open channel beams journal, April 2005

Strike mechanics of an ambush predator: the spearing mantis shrimp journal, November 2012

Linkage mechanics and power amplification of the mantis shrimp's strike journal, October 2010

Elastic energy storage in the mantis shrimp's fast predatory strike journal, November 2009

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Calcified cuticle in the stomatopod smashing limb journal, July 1982

Phylogenetic Analysis of the Stomatopoda (Malacostraca) journal, November 1997

Failure phenomenology of confined ceramic targets and impacting rods journal, January 1990

Evolution of anatomical and physiological specialization in the compound eyes of stomatopod crustaceans journal, October 2010

Modularity and Rates of Evolutionary Change in a Power-Amplified prey Capture System: Evolution of Power Amplification journal, July 2013

Crustacean-Derived Biomimetic Components and Nanostructured Composites journal, May 2014

Smashing Energetics: Prey Selection and Feeding Efficiency of the Stomatopod, Gonodactylus bredini journal, January 1989

Extreme impact and cavitation forces of a biological hammer: strike forces of the peacock mantis shrimp Odontodactylus scyllarus journal, October 2005

Relationships between the J-integral and the crack opening displacement for stationary and extending cracks journal, August 1981

Twisted fibrous arrangements in biological materials and cholesteric mesophases journal, January 1972

Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology journal, January 2004

The Structure and Mineralization of the Carapace of the Crab (Cancer pagurus L.) 3. The epicuticle journal, June 1978

Robustness and optimal use of design principles of arthropod exoskeletons studied by ab initio-based multiscale simulations journal, February 2011

Deadly strike mechanism of a mantis shrimp journal, April 2004

Preferred crystallographic texture of α-chitin as a microscopic and macroscopic design principle of the exoskeleton of the lobster Homarus americanus journal, November 2007

Average stress in matrix and average elastic energy of materials with misfitting inclusions journal, May 1973

Crab Shell Chitin Whisker Reinforced Natural Rubber Nanocomposites. 1. Processing and Swelling Behavior journal, May 2003

The composition of the exoskeleton of two crustacea: The American lobster Homarus americanus and the edible crab Cancer pagurus journal, October 2007

Supercontinuum Generation in Naturally Occurring Glass Sponges Spicules journal, July 2016

Influence of Structural Principles on the Mechanics of a Biological Fiber-Based Composite Material with Hierarchical Organization: The Exoskeleton of the Lobster Homarus americanus journal, January 2009

A Sinusoidally-Architected Helicoidal Biocomposite text, January 2016

Multiscale Toughening Mechanisms in Biological Materials and Bioinspired Designs journal, July 2019

Smashing mantis shrimp strategically impact shells journal, June 2018

Mantis shrimp are the key to smashing new materials journal, April 2018

The Power of Mantis Shrimp Strikes: Interdisciplinary Impacts of an Extreme Cascade of Energy Release journal, July 2019

Twisting cracks in Bouligand structures
journal, December 2017

Scanning X-ray microdiffraction of complex materials: Diffraction geometry considerations
journal, January 2003

Stomatopod predation on fossil gastropods from the Plio-Pleistocene of Florida
journal, May 1991

The phylogeny of the stomatopod Crustacea
journal, January 2000

Comparative spring mechanics in mantis shrimp
journal, December 2012

Adaptive FEM computation of geometric and material nonlinearities with application to brittle failure
journal, August 1998

Enamel inspired nanocomposite fabrication through amelogenin supramolecular assembly
journal, July 2007

Pore canal shape related to molecular architecture of arthropod cuticle
journal, January 1969

A Sinusoidally Architected Helicoidal Biocomposite
journal, May 2016

Linkage mechanics and power amplification of the mantis shrimp's strike
journal, October 2007

The Stomatopod Dactyl Club: A Formidable Damage-Tolerant Biological Hammer
journal, June 2012

Modularity and Scaling in fast Movements: Power Amplification in Mantis Shrimp: Modularity and Scaling of Power Amplification
journal, October 2010

Torsional Strengthening of Spandrel Beams with Fiber-Reinforced Polymer Laminates
journal, April 2004

Palaeo- and archaeostomatopods (Hoplocarida, Crustacea) from the Bear Gulch Limestone, Mississippian (Namurian), of central Montana
journal, January 1998

On the architecture and function of cuttlefish bone
journal, July 1983

Bio-inspired impact-resistant composites
journal, September 2014

Revealing the Design Principles of High-Performance Biological Composites Using Ab initio and Multiscale Simulations: The Example of Lobster Cuticle
journal, January 2010

Paleozoic Proto-Mantis Shrimp Revisited
journal, September 2007

Evolution of mantis shrimps (Stomatopoda, Malacostraca) in the light of new Mesozoic fossils
journal, January 2010

Dynamic, multiaxial impact response of confined and unconfined ceramic rods
conference, January 1994

Flexural–torsional buckling of fiber-reinforced plastic composite open channel beams
journal, April 2005

Strike mechanics of an ambush predator: the spearing mantis shrimp
journal, November 2012

Linkage mechanics and power amplification of the mantis shrimp's strike
journal, October 2010

Elastic energy storage in the mantis shrimp's fast predatory strike
journal, November 2009

The exoskeleton of the lobster Homarus americanus as an example of a smart anisotropic biological material☆
journal, May 2007

Calcified cuticle in the stomatopod smashing limb
journal, July 1982

Phylogenetic Analysis of the Stomatopoda (Malacostraca)
journal, November 1997

Failure phenomenology of confined ceramic targets and impacting rods
journal, January 1990

Evolution of anatomical and physiological specialization in the compound eyes of stomatopod crustaceans
journal, October 2010

Modularity and Rates of Evolutionary Change in a Power-Amplified prey Capture System: Evolution of Power Amplification
journal, July 2013

Crustacean-Derived Biomimetic Components and Nanostructured Composites
journal, May 2014

Smashing Energetics: Prey Selection and Feeding Efficiency of the Stomatopod, Gonodactylus bredini
journal, January 1989

Extreme impact and cavitation forces of a biological hammer: strike forces of the peacock mantis shrimp Odontodactylus scyllarus
journal, October 2005

Relationships between the J-integral and the crack opening displacement for stationary and extending cracks
journal, August 1981

Twisted fibrous arrangements in biological materials and cholesteric mesophases
journal, January 1972

Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology
journal, January 2004

The Structure and Mineralization of the Carapace of the Crab (Cancer pagurus L.) 3. The epicuticle
journal, June 1978

Robustness and optimal use of design principles of arthropod exoskeletons studied by ab initio-based multiscale simulations
journal, February 2011

Deadly strike mechanism of a mantis shrimp
journal, April 2004

Preferred crystallographic texture of α-chitin as a microscopic and macroscopic design principle of the exoskeleton of the lobster Homarus americanus
journal, November 2007

Average stress in matrix and average elastic energy of materials with misfitting inclusions
journal, May 1973

Crab Shell Chitin Whisker Reinforced Natural Rubber Nanocomposites. 1. Processing and Swelling Behavior
journal, May 2003

The composition of the exoskeleton of two crustacea: The American lobster Homarus americanus and the edible crab Cancer pagurus
journal, October 2007

Supercontinuum Generation in Naturally Occurring Glass Sponges Spicules
journal, July 2016

Influence of Structural Principles on the Mechanics of a Biological Fiber-Based Composite Material with Hierarchical Organization: The Exoskeleton of the Lobster Homarus americanus
journal, January 2009

A Sinusoidally-Architected Helicoidal Biocomposite
text, January 2016

Multiscale Toughening Mechanisms in Biological Materials and Bioinspired Designs
journal, July 2019

Smashing mantis shrimp strategically impact shells
journal, June 2018

Mantis shrimp are the key to smashing new materials
journal, April 2018

The Power of Mantis Shrimp Strikes: Interdisciplinary Impacts of an Extreme Cascade of Energy Release
journal, July 2019