The Stomatopod Telson: Convergent Evolution in the Development of a Biological Shield

Abstract

Mantis shrimp are aggressive marine crustaceans well known for their rapid and powerful hunting strategies. Less well known, however, is the ability of some species of mantis shrimp to defend themselves from the repeated blows of conspecifics during ritualized fighting using a shield-like segment of abdominal armor called the telson. Multiscale structure-mechanical property relationships of this damage-tolerant biological composite is examined in order to reveal strategies that nature uses for resisting failure from repeated high-energy impacts. The telson structures of the smashingtype species, Odontodactylus scyllarus, and the less aggressive spearing-type species, Lysiosquillina maculata, are compared in order to better understand the ecological pressures driving the formation and use of the telson as a biological shield. A higher bulk compressive stiffness is identified within the smasher telson, which is attributed to its concave macromorphology, thicker cuticle, and higher degree of mineralization within its exocuticle. The presence of ridges at the dorsal surface suggests a role in imparting compliance for energy absorption. Fracture analysis identifies an enhanced toughening mechanism of crack twisting within the smasher telson, attributed to its well-defined pitch-graded helicoidal fibrous micro-architecture. Such findings may prove useful for the design of lightweight composite materials with potential flexibility and improved damage tolerance.

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

“…Error bars represent 1 SD measured over at least three samples. fibrils lamellae are arranged in the twisted plywood pattern (9,17,25,44) (Fig. 1A), although not only the structure but also the mechanical properties of the materials, size, and geometry play important roles in the competition between mantis shrimp and abalone shells in nature, we hypothesize that the structure that exhibits the combination of the toughening mechanisms of crack twisting and crack bridging endows the mantis shrimps with remarkable fracture resistance as well as crack orientation insensitivity.…”

“…Both bioinspired toughening mechanisms have been successfully applied in engineering composites (22,(36)(37)(38)(39), respectively, e.g., the impact-resistant nacreous glass and the tough Bouligand composites. Remarkably, experiments and theoretical analyses demonstrated that crack twisting and fibril bridging may coexist during the fracturing process in the natural materials with Bouligand structures, e.g., the stomatopod dactyl club and arapaima fish scale (16,17,(40)(41)(42)(43). In the meanwhile, experimental investigations showed that there exist critical pitch angles (the angle difference in orientation of adjacent fiber layers) corresponding to maximum fracture toughness in synthetic twisted plywood materials (37).…”

“…In the meanwhile, experimental investigations showed that there exist critical pitch angles (the angle difference in orientation of adjacent fiber layers) corresponding to maximum fracture toughness in synthetic twisted plywood materials (37). In natural structural materials, the beetle exocuticle with Bouligand structure has a specific pitch angle about 12°to 18°and a linear twist angles distribution in a pitch (a distance for a 180°rotation) (44), and the pitch angles are about 6.2°and 22.5°in the stomatopod dactyl club (36) and the spearer telson of Lysiosquillina maculata (17), respectively. However, most previous models of twisted plywood with continuous fibers did not predict the experimentally observed hybrid toughening mechanisms of crack bridging and crack twisting.…”

“…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).…”

Multiscale Toughening Mechanisms in Biological Materials and Bioinspired Designs

“…In our traditional view of making a desired material that is tough and damage tolerant, it is crucial to reach a compromise of the strength and ductility. However, Nature has developed several remarkable ways to build lightweight and strong, yet tough materials over millions of years of evolution . Figure a depicts toughness as a function of elastic modulus, highlighting that naturally existing biological materials retain toughness with an increase in stiffness (green banana curve); while the current synthetic engineering materials show an inverted curve (yellow), indicating toughness drops dramatically as stiffness increases.…”