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Piscine defense and hydro-actuated deformation strategies: Paths to Bioinspired Design

Abstract

Mother nature is an ingenious master on developing efficient structural and functional materials, which manifest various fascinating properties that are superior to synthetic materials. Here, we systematically investigate two topics: the materials design for piscine defense and hydro-actuated reversible deformation of plant organs. In each topic, we selected several types of biological materials to study and unravel the connection between their intelligent hierarchical structure and superb mechanical properties.

We selected three fish and fully investigated the structure and mechanical properties of their scales. The first is the legendary lobe-finned fish coelacanth, which is extant for 400 million years. This defense is provided by primitive elasmoid scales having a double-twisted Bouligand structure of collagenous lamellae. The collagen fibrils in coelacanth scale form bundles which are embedded in a matrix composed of fibers arranged perpendicular to the layered structure, providing added rigidity and resistance to deformation. The second one we studied is a more evolved scale from common carp. Carp has typical modern elasmoid fish scales which are commonly found on most current teleosts. Like coelacanth scale, the outer surface of carp scale is composed of mineralized layers and the inner core is comprised of collagenous lamellae. The lamella orientations in carp scale follows a single twisted Bouligand pattern, with a rotation angle of 36°. Moreover, perpendicular to the lamellae, thinner collagen fibrils, which are called threading fibrils here, form a “sheet-like” structure oriented from the basal part to the external layer. Using in situ synchrotron small-angle x-ray scattering during uniaxial tensile testing, the deformation mechanisms of the collagen in these two scales are identified in terms of fibril stretching, reorientation, sliding, bending and delamination. The third scale we studied is from one of the largest freshwater fish, Arapaima, which has successfully survived in piranha-infested seasonal lakes of the Amazon. To quantitatively investigate the scale’s fracture toughness, we developed a new fixture and measured the J-integral based fracture toughness of the scale and find that the crack-growth toughness as high as ~200 kJm-2, which is one of the toughest flexible biological materials. This toughness is primarily the result of multiple mechanisms which are identified by in situ SEM observation. Our results may bring some critical thinking for developing novel armor materials.

Instead of evolving body armor to protect themselves passively, some fish develop powerful weapons to defend actively. We fully investigated the thorny catfish (Doradidae; order Siluriforme), which has barbed pectoral fin spines and mid-lateral scutes that work in concert to provide an active mechanical defense capability. The structural design of these two weapons is very impressive, including a hollow structure, porous components, and gradient transitions, leading to an outstanding performance by maintaining strength, toughness and light weight synergistically. These designs can provide inspiration for developing new structural materials.

The second topic we studied is the hydro-actuated reversible deformation in plant organs. Plants have developed many intelligent strategies to respond to external stimuli, significantly benefiting their survival. Here we studied a classic: pine cone, which opens to release the pods upon drying and can reclose upon rehydrating. We unraveled a novel mechanism of reversible deformation actuated by hydration. Our findings provide an interdisciplinary perspective combining materials science, structural engineering and biology, as well as offering some design models for development of novel smart responsive materials which have improved mechanical properties and biocompatibility yet simpler strategy.

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