Protection mechanisms of the iron-plated armor of a deep-sea hydrothermal vent gastropod

Abstract

Biological exoskeletons, in particular those with unusually robust and multifunctional properties, hold enormous potential for the development of improved load-bearing and protective engineering materials. Here, we report new materials and mechanical design principles of the iron-plated multilayered structure of the natural armor of Crysomallon squamiferum, a recently discovered gastropod mollusc from the Kairei Indian hydrothermal vent field, which is unlike any other known natural or synthetic engineered armor. We have determined through nanoscale experiments and computational simulations of a predatory attack that the specific combination of different materials, microstructures, interfacial geometries, gradation, and layering are advantageous for penetration resistance, energy dissipation, mitigation of fracture and crack arrest, reduction of back deflections, and resistance to bending and tensile loads. The structure-property-performance relationships described are expected to be of technological interest for a variety of civilian and defense applications.exoskeleton | mollusc | biomechanics | nanomechanics | nanoindentation M any organisms have evolved robust protective exterior structures over millions of years to maximize survivability in their specific environments. Biological exoskeletons or "natural armor" must fulfill various performance requirements such as wear resistance, dissolution prevention, thermal and hydration regulation, and accommodations for feeding, locomotion, and reproduction. Another critical function of these systems is mechanical protection from predators that can induce damage from, for example, penetration, fatigue, drilling, peeling, chipping, hammering, crushing, and kinetic attacks (1). Hence, a diverse array of macroscopic geometries, sizes, and hierarchical, multilayered composite structures exist (2). The shells of gastropod molluscs have long provided key insights into the mechanical performance of biological armor materials. Early on, Wainwright carried out macroscopic mechanical experiments on bivalve shells and formulated important questions on the contributions of different crystal textures to their strength and other functional properties (3). Soon after, Currey and Taylor characterized the properties of numerous mollusc shell microstructures and determined that the inner nacreous layer had superior mechanical properties (4). Subsequently, three decades of investigations ensued on nacre (5-9), leading to the generalized concept of "mechanical property amplification;" i.e., order of magnitude increases in strength and toughness exhibited by biological composites compared to their individual constituent materials beyond simple rule of mixture formulations (10-12). These discoveries engendered numerous efforts to produce nacre-mimetic composite materials that also exhibit mechanical property amplification (12-15). Design, inspired by nature, of engineering materials with robust and multifunctional mechanical properties [i.e., those which sustain a variety of loading condi...

Structure and mechanical properties of selected protective systems in marine organisms

“…An example is the deep sea scaly-foot gastropod Crysomallon squamiferum (Fig. 11), which employs an outer layer of FeS and a calcified inner layer that are separated by a relatively thick organic layer [92,109,110]. FeS is deposited on the surface of the mollusk by the deep sea vents in its natural habitat and incorporated into its structure [92,110].…”

Textured fluorapatite bonded to calcium sulphate strengthen stomatopod raptorial appendages

“…Ultra-high mineralization 3,4 is an obvious choice to optimize the hardness and stiffness near free surfaces, and most species indeed fine-tune the biomineralization process such that the mineral phase at the free surface exhibits a combination of mechanical properties that is optimized for impact or abrasion tolerance 5,6 . Illustrative examples of this strategy include, among others, protective scales of fish 7 , the chiton radular teeth 8 or the external protective armour of deep-sea gastropods 9 . Microstructural adjustments are also commonly employed by species as a way to provide an extra level of control over the properties of their extracellular tissues and tools, with specific examples including porosity gradients in bones 10 or the preferred crystalline orientation in both vertebrate and invertebrate teeth 11 .…”

Stretchable heterogeneous composites with extreme mechanical gradients

“…Constructing heterogeneous composite materials with locally tuned mechanical properties in all three dimensions is a recurring strategy in nature to achieve unusual mechanical properties and to couple surfaces with very different elastic moduli [7][8][9][10][11][12][13][14] . For instance, the biological tissue that connects tendons to bone exhibits locally tuned elastic moduli that can vary by as much as two orders of magnitude to match the stiff surface of bone with the soft tendon [15][16][17] .…”