Ecologically Driven Ultrastructural and Hydrodynamic Designs in Stomatopod Cuticles

Abstract

Ecological pressures and varied feeding behaviors in a multitude of organisms 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 architecture (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 raptorial feeding appendage as a biological hammer. Moreover, 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.

Multiscale Toughening Mechanisms in Biological Materials and Bioinspired Designs

“…At the macroscale level, the structure, morphology and arrangement of the architecture features could also affect the mechanical behavior under different loading conditions. Examples include curvatures found in horns and turtle carapace,90b,92 different shapes of cross‐sectional designs for hydrodynamic and aerodynamic applications, overlapping scales in fish, pangolin, and chiton,61b,82,94 and the tessellated scale arrangements in boxfish armor and mineralized cartilage in the endoskeleton of Elasmobranchii 90a,95. The characteristic morphology and element arrangement at the macroscale in these organisms can provide specific mechanical solutions to adapt to the loading conditions.…”

Discontinuous fibrous Bouligand architecture enabling formidable fracture resistance with crack orientation insensitivity

“…Varying the arrangements can create materials with vastly different macroscale mechanical properties (1,2,6,7). One prime example is the Bouligand architecture characterized by the stacking of fibrous layers rotated by a pitch angle in chitin nanofibrils-based natural materials (8)(9)(10)(11)(12)(13)(14)(15)(16)(17)(18), such as the exoskeleton of arthropods (e.g., crab, lobster, beetles, and shrimp) and mammal bone, etc. The dactyl club of mantis shrimp composed of mineralized chitin nanofibrils lamellae organized in a twisted plywood (Bouligand) structure exhibits exceptional damage resistance (9,11,16,17).…”

Smashing mantis shrimp strategically impact shells

“…This study lays the groundwork for future studies of impact fracture in biology, provides a functional context for studies of mantis shrimp hammer material design (Grunenfelder et al, 2014(Grunenfelder et al, , 2018Guarín-Zapata et al, 2015;Suksangpanya et al, 2017;Weaver et al, 2012;Yaraghi et al, 2016) and models an approach for integrating animal behavior and physical modeling to elucidate complicated physical processes. Ninjabot enabled controlled testing and interpretation of mantis shrimp behavioral strategies, including those outside the mantis shrimp's repertoire, and thus yielded insight into underlying fracture mechanics.…”

“…The hammers move so quickly that water cavitates during impact, such that by wielding their pair of raptorial appendages (second thoracopods), they generate up to four peaks of force (impact and cavitation of both raptorial appendages) (Patek and Caldwell, 2005;Patek et al, 2004). The materials and mechanics of mantis shrimp hammers have been studied extensively (McHenry et al, 2012(McHenry et al, , 2016Anderson et al, 2014;Grunenfelder et al, 2014Grunenfelder et al, , 2018Guarín-Zapata et al, 2015;Patek and Caldwell, 2005;Patek et al, 2004Patek et al, , 2007Suksangpanya et al, 2017;Weaver et al, 2012;Yaraghi et al, 2016). In addition, a physical model of mantis shrimp hammers (Ninjabot) was developed to replicate mantis shrimp strike rotations, accelerations and impacts in water, complete with associated cavitation (Cox et al, 2014) (Fig.…”