Inherent Role of Water in Damage Tolerance of the Prismatic Mineral–Organic Biocomposite in the Shell of Pinna Nobilis

Abstract

The combination of high stiffness, strength, and toughness of many biological tissues is achieved through complex 3D arrangement of hard and soft components. While the hard building blocks are associated with the general stiffness of these biocomposite structures, the soft organic constituents provide the necessary flexibility and toughness and are susceptible to moisture uptake. Because many biological materials reside in humid environments, water is an inherent component of their microstructure. Hence, many studies have emphasized the effect of moisture content on mechanical performance of these materials. High toughness is indeed reported in materials, such as bone, teeth, mollusk shells, and glass sponges, when measured in high relative humidities, nevertheless, not much is known about the exact mechanisms that are responsible for this phenomenon. In the present work, newly developed environmentally controlled nanomechanical characterization techniques are employed to probe the prismatic layer in the shell of Pinna nobilis consisting of hard calcitic blocks surrounded by 1 μm thick organic matrix. Using spatially resolved mechanical data, it is demonstrated that water not only strongly affects the mechanical properties of the biocomposite tissue and its constituents but also is an integral part of explicit intrinsic and extrinsic toughening mechanisms revealed in this study.

Thermodynamic Aspects of Molluscan Shell Ultrastructural Morphogenesis

“…These biogenic mineral units have the morphology and crystallographic properties that are significantly different from the inorganically formed counterparts . Moreover, despite the inherently poor mechanical properties of the constituents, these assemblies exhibit extraordinary mechanical efficiency by combining high stiffness with high fracture toughness and thus, provide the animals with structural support and protection against predators . Hence, besides serving as a model system for understanding the process of mineral formation by living organisms, the molluscan shells are a source of inspiration for novel composite materials design, attracting scientist from many scientific disciplines, such as biology, chemistry, physics and materials science.…”

On the relationship between indenation hardness and modulus, and the damage resistance of biological materials

“…There is ample evidence that the mechanical properties of biological materials are sensitive to hydration, which tends to decrease hardness and modulus, but increase toughness (e. g. 3,22,35,60,71,[106][107][108][109]. It is convenient to define the sensitivity to hydration, S H , as the relative change in indentation hardness/modulus upon dehydration, S H,H I = (H I, d − H I, w )/H I, w and S H,E I = (E I, d − E I, w )/E I, w , where the indices w and d indicate data from hydrated ('wet') and dehydrated ('dry') materials, respectively.…”

Structural Orientation and Anisotropy in Biological Materials: Functional Designs and Mechanics

“…The architectures of biological materials are distinguished by a series of characteristics, including the hierarchical organization of constituents over multiple length scales, the fine modulation of their interfaces, and the incorporation of spatial gradients and heterogeneities . Additionally, the basic building elements of materials in nature, such as fibers, tubules, columns, and lamellae, generally have anisometric geometries and display anisotropic properties; also, they are often aligned preferentially along specific directions to form well‐defined arrangements. These lead to the anisotropic nature of materials and endow them with properties that are dependent on the structural orientations.…”

“…These lead to the anisotropic nature of materials and endow them with properties that are dependent on the structural orientations. Typical examples of such biological materials include those having fibrous, tubular, columnar, and lamellar architectures, as shown in Figure a–d. The anisotropy is widespread at differing levels of structural hierarchy.…”

“…Typical a–d) anisotropic structures in biological materials and e) the composite model illustrating structural orientations. The fibrous, tubular, columnar, and lamellar structures are, respectively, from a) the skin of rabbit, b) the baleen of bowhead whale, c) the prismatic layer of the shell of bivalve Pinna nobilis , and d) the pangolin scale . The main constituents of these structures are, corresponding to their specific length scales, collagen fibrils of ≈50 nm in diameter, tubules with tens to hundreds of micrometers in diameter consisting of keratinized cells, elongated calcitic prisms with an average diameter of roughly 30 µm, and keratin lamellae, ≈3 µm in thickness, respectively.…”