Mechanical design of the highly porous cuttlebone: A bioceramic hard buoyancy tank for cuttlefish

Abstract

Cuttlefish, a unique group of marine mollusks, produces an internal biomineralized shell, known as cuttlebone, which is an ultra-lightweight cellular structure (porosity, ∼93 vol%) used as the animal’s hard buoyancy tank. Although cuttlebone is primarily composed of a brittle mineral, aragonite, the structure is highly damage tolerant and can withstand water pressure of about 20 atmospheres (atm) for the species Sepia officinalis. Currently, our knowledge on the structural origins for cuttlebone’s remarkable mechanical performance is limited. Combining quantitative three-dimensional (3D) structural characterization, four-dimensional (4D) mechanical analysis, digital image correlation, and parametric simulations, here we reveal that the characteristic chambered “wall–septa” microstructure of cuttlebone, drastically distinct from other natural or engineering cellular solids, allows for simultaneous high specific stiffness (8.4 MN⋅m/kg) and energy absorption (4.4 kJ/kg) upon loading. We demonstrate that the vertical walls in the chambered cuttlebone microstructure have evolved an optimal waviness gradient, which leads to compression-dominant deformation and asymmetric wall fracture, accomplishing both high stiffness and high energy absorption. Moreover, the distribution of walls is found to reduce stress concentrations within the horizontal septa, facilitating a larger chamber crushing stress and a more significant densification. The design strategies revealed here can provide important lessons for the development of low-density, stiff, and damage-tolerant cellular ceramics.

Thermomechanical Analysis of a Bio‐Inspired Lightweight Multifunctional Structure

“…The material's plastic property is given by the relationship between the plastic stress (MPa) and corresponding plastic strains: 350, 0; 368.71, 0.001; 376. 5 12. All four models are meshed using wedge and tetrahedral elements, with about 180 000 elements for each case.…”

“…[ 3,4 ] Previous studies have suggested that cuttlebone's remarkable damage tolerance and high stiffness can be attributed to its characteristic “wall‐septa” internal morphology. [ 5 ] Several previous studies on cuttlebone have explored its potential applications by exploiting its chemical, structural, and mechanical characteristics as a natural cellular material. For example, cuttlebone itself can be used as a filler in natural rubber [ 6 ] and acrylic bone cement, [ 7 ] the mechanical properties of which are comparable to commercial products.…”

Mechanically Efficient Cellular Materials Inspired by Cuttlebone

“…[ 25,32,33 ] The role of the aragonite crystallites has been demonstrated to enhance strength, damage tolerance, and toughness, and the organic content also plays an important role in the improved damage resistance. [ 34 ] Based on these observations, we hypothesize that the rationally manipulated lamellae structure plays an important role in the fracture mechanism of cuttlebone.…”

“…These phenomena can be understood by the different deformation mechanisms: compression/stretching-dominated deformation mechanism and the bending-dominated deformation mechanism. [10,16,34] Kelvin foam is a typical bending dominated structure, which usually experiences uniform deformation under compression. Although such a deformation behavior is beneficial to avoid catastrophic failure, it sacrifices the strength and modulus of the structure.…”

Microstructural design for mechanical–optical multifunctionality in the exoskeleton of the flower beetle Torynorrhina flammea

“…These evolutionary processes frequently act both independently and synergistically, resulting in characters that exhibit multifunctionality (3)(4)(5)(6). While classical characters, particularly those that have been employed for trait-based taxonomic purposes, typically represent macroscale features such as the size and shapes of bird beaks (7), species-specific characters (or phenotypes) also exist at the "material level" as nano-and microstructures (8)(9)(10)(11)(12). These micro-and nanoscale architectures have evolved to enable specific and diverse biological functions including, for example, mechanical protection and optical appearance (10,(13)(14)(15).…”