High strength and damage-tolerance in echinoderm stereom as a natural bicontinuous ceramic cellular solid.

Due to their low damage tolerance, engineering ceramic foams are often limited to non-structural usages. In this work, we report that stereom, a bioceramic cellular solid (relative density, 0.2-0.4) commonly found in the mineralized skeletal elements of echinoderms (e.g., sea urchin spines), achieves simultaneous high relative strength which approaches the Suquet bound and remarkable energy absorption capability (ca. 17.7 kJ kg-1) through its unique bicontinuous open-cell foam-like microstructure. The high strength is due to the ultra-low stress concentrations within the stereom during loading, resulted from their defect-free cellular morphologies with near-constant surface mean curvatures and negative Gaussian curvatures. Furthermore, the combination of bending-induced microfracture of branches and subsequent local jamming of fractured fragments facilitated by small throat openings in stereom leads to the progressive formation and growth of damage bands with significant microscopic densification of fragments, and consequently, contributes to stereom's exceptionally high damage tolerance.

Multiscale mechanical design of the lightweight, stiff, and damage-tolerant cuttlebone: A computational study.

Cuttlebone, the endoskeleton of cuttlefish, offers an intriguing biological structural model for designing low-density cellular ceramics with high stiffness and damage tolerance. Cuttlebone is highly porous (porosity ∼93%) and lightweight (density less than 20% of seawater), constructed mainly by brittle aragonite (95 wt%), but capable of sustaining hydrostatic water pressures over 20 atmospheres and exhibits energy absorption capability under compression comparable to many metallic foams (∼4.4 kJ/kg). In this work, we computationally investigate how such remarkable mechanical efficiency is enabled by the multiscale structure of cuttlebone. Using the common cuttlefish, Sepia Officinalis, as a model system, we first conducted high-resolution synchrotron micro-computed tomography (µ-CT) and quantified the cuttlebone's multiscale geometry, including the 3D asymmetric shape of individual walls, the wall assembly patterns, and the long-range structural gradient of walls across the entire cuttlebone (ca. 38 chambers). The acquired 3D structural information enables systematic finite-element simulations, which further reveal the multiscale mechanical design of cuttlebone: at the wall level, wall asymmetry provides optimized energy absorption while maintaining high structural stiffness; at the chamber level, variation of walls (number, pattern, and waviness amplitude) contributes to progressive damage; at the entire skeletal level, the gradient of chamber heights tailors the local mechanical anisotropy of the cuttlebone for reduced stress concentration. Our results provide integrated insights into understanding the cuttlebone's multiscale mechanical design and provide useful knowledge for the designs of lightweight cellular ceramics. STATEMENT OF SIGNIFICANCE: Cuttlebone has been demonstrated to be a biological ceramic cellular material with remarkable lightweight, high stiffness and energy absorption. However, our knowledge on how such mechanical properties are enabled by cuttlebone's multiscale structure is not complete. Here, we combine systematic tomography-based 3D structural analysis and finite-element simulations to reveal how the hierarchical structure of cuttlebone at multiple length scales synergistically contribute to cuttlebone's impressive mechanical efficiency. These findings have important implications for designing biomimetic low-density cellular ceramic materials.

AFM Manipulation of EGaIn Microdroplets to Generate Controlled, On-Demand Contacts on Molecular Self-Assembled Monolayers.

Liquid metal droplets, such as eutectic gallium-indium (EGaIn), are important in many research areas, such as soft electronics, catalysis, and energy storage. Droplet contact on solid surfaces is typically achieved without control over the applied force and without optimizing the wetting properties in different environments (e.g., in air or liquid), resulting in poorly defined contact areas. In this work, we demonstrate the direct manipulation of EGaIn microdroplets using an atomic force microscope (AFM) to generate repeated, on-demand making and breaking of contact on self-assembled monolayers (SAMs) of alkanethiols. The nanoscale positional control and feedback loop in an AFM allow us to control the contact force at the nanonewton level and, consequently, tune the droplet contact areas at the micrometer length scale in both air and ethanol. When submerged in ethanol, the droplets are highly nonwetting, resulting in hysteresis-free contact forces and minimal adhesion; as a result, we are able to create reproducible geometric contact areas of 0.8-4.5 µm2 with the alkanethiolate SAMs in ethanol. In contrast, there is a larger hysteresis in the contact forces and larger adhesion for the same EGaIn droplet in air, which reduced the control over the contact area (4-12 µm2). We demonstrate the usefulness of the technique and of the gained insights in EGaIn contact mechanics by making well-defined molecular tunneling junctions based on alkanethiolate SAMs with small geometric contact areas of between 4 and 12 µm2 in air, 1 to 2 orders of magnitude smaller than previously achieved.

Lightweight lattice-based skeleton of the sponge Euplectella aspergillum: On the multifunctional design.

The glass sponge, Euplectella aspergillum, possesses a lightweight, silica spicule-based, cylindrical lattice-like skeleton, representing an excellent model system for bioinspired lattices. Previous analysis suggested that the E. aspergillum's skeletal lattice exhibits improved buckling resistance and suppressed vortex shedding. How the sponge's skeletal lattice with diagonally-oriented reinforcing bundle of fused spicules and the ridge system behaves under different loading conditions and achieves dual mechanical and fluidic transport performance requires further investigation. Here, we first quantified the structural descriptors such as length and thickness of the bundles of fused spicules and hole opening diameter of the sponge skeletons with and without the soft tissue covered. Secondly, parametric modeling and simulations of the sponge lattice in comparison with other bioinspired designs under different loading conditions were implemented to obtain the structure-mechanical property relationship. Our results reveal that the double-diagonal reinforcements of the E. aspergillum's lattices show i) tendency to maximize the torsional rigidity in comparison to longitudinal and radial modulus and flexural rigidity, and ii) independency of mechanical properties on the diagonal spacing, leaving freedom to control the hole-opening position for the sponge's fluid transport. Furthermore, our coupled fluid-mechanical simulations suggest that the ridge system spiraling the cylindrical lattice simultaneously improves the radial stiffness and fluid permeability. Finally, we discuss the general mechanical strategies and design flexibility in the sponge's skeletal lattice. Our work provides understanding of the mechanical and functional trade-offs in E. aspergillum's skeletal lattice which may shed light on the design of lightweight tubular lattices.

Biomineralized Materials as Model Systems for Structural Composites: Intracrystalline Structural Features and Their Strengthening and Toughening Mechanisms.

Biomineralized composites, which are usually composed of microscopic mineral building blocks organized in 3D intercrystalline organic matrices, have evolved unique structural designs to fulfill mechanical and other biological functionalities. While it has been well recognized that the intricate architectural designs of biomineralized composites contribute to their remarkable mechanical performance, the structural features within and corresponding mechanical properties of individual mineral building blocks are often less appreciated in the context of bio-inspired structural composites. The mineral building blocks in biomineralized composites exhibit a variety of salient intracrystalline structural features, such as, organic inclusions, inorganic impurities (or trace elements), crystalline features (e.g., amorphous phases, single crystals, splitting crystals, polycrystals, and nanograins), residual stress/strain, and twinning, which significantly modify the mechanical properties of biogenic minerals. In this review, recent progress in elucidating the intracrystalline structural features of three most common biomineral systems (calcite, aragonite, and hydroxyapatite) and their corresponding mechanical significance are discussed. Future research directions and corresponding challenges are proposed and discussed, such as the advanced structural characterizations and formation mechanisms of intracrystalline structures in biominerals, amorphous biominerals, and bio-inspired synthesis.

A damage-tolerant, dual-scale, single-crystalline microlattice in the knobby starfish, Protoreaster nodosus.

Cellular solids (e.g., foams and honeycombs) are widely found in natural and engineering systems because of their high mechanical efficiency and tailorable properties. While these materials are often based on polycrystalline or amorphous constituents, here we report an unusual dual-scale, single-crystalline microlattice found in the biomineralized skeleton of the knobby starfish, Protoreaster nodosus. This structure has a diamond-triply periodic minimal surface geometry (lattice constant, approximately 30 micrometers), the [111] direction of which is aligned with the c-axis of the constituent calcite at the atomic scale. This dual-scale crystallographically coaligned microlattice, which exhibits lattice-level structural gradients and dislocations, combined with the atomic-level conchoidal fracture behavior of biogenic calcite, substantially enhances the damage tolerance of this hierarchical biological microlattice, thus providing important insights for designing synthetic architected cellular solids.

Biomineralized Materials as Model Systems for Structural Composites: 3D Architecture.

Biomineralized materials are sophisticated material systems with hierarchical 3D material architectures, which are broadly used as model systems for fundamental mechanical, materials science, and biomimetic studies. The current knowledge of the structure of biological materials is mainly based on 2D imaging, which often impedes comprehensive and accurate understanding of the materials' intricate 3D microstructure and consequently their mechanics, functions, and bioinspired designs. The development of 3D techniques such as tomography, additive manufacturing, and 4D testing has opened pathways to study biological materials fully in 3D. This review discusses how applying 3D techniques can provide new insights into biomineralized materials that are either well known or possess complex microstructures that are challenging to understand in the 2D framework. The diverse structures of biomineralized materials are characterized based on four universal structural motifs. Nacre is selected as an example to demonstrate how the progression of knowledge from 2D to 3D can bring substantial improvements to understanding the growth mechanism, biomechanics, and bioinspired designs. State-of-the-art multiscale 3D tomographic techniques are discussed with a focus on their integration with 3D geometric quantification, 4D in situ experiments, and multiscale modeling. Outlook is given on the emerging approaches to investigate the synthesis-structure-function-biomimetics relationship.

Black Drum Fish Teeth: Built for Crushing Mollusk Shells.

With an exclusive diet of hard-shelled mollusks, the black drum fish (Pogonias cromis) exhibits one of the highest bite forces among extant animals. Here we present a systematic microstructural, chemical, crystallographic, and mechanical analysis of the black drum teeth to understand the structural basis for achieving the molluscivorous requirements. At the material level, the outermost enameloid shows higher modulus (Er = 126.9 ± 16.3 GPa, H = 5.0 ± 1.4 GPa) than other reported fish teeth, which is attributed to the stiffening effect of Zn and F doping in apatite crystals and the preferential co-alignment of crystallographic c-axes and enameloid rods along the biting direction. The high fracture toughness (Kc = 1.12 MPa⋅m1/2) of the outer enameloid also promotes local yielding instead of fracture during crushing contact with mollusk shells. At the individual-tooth scale, the molar-like teeth, high density of dentin tubules, enlarged pulp chamber, and specialized dentin-bone connection, all contribute to the functional requirements, including confinement of contact compressive stress in the stiff enameloid, enhanced energy absorption in the compliant dentin, and controlled failure of tooth-bone composite under excessive loads. These results show that the multi-scale structures of black drum teeth are adapted to feed on hard-shelled mollusks. STATEMENT OF SIGNIFICANCE: The black drum fish feeds on hard-shelled mollusks, which requires strong, tough, and wear-resistant teeth. This study presents a comprehensive multiscale material and mechanical analysis of the black drum teeth in achieving such remarkable biological function. At microscale, the fluoride- and zinc-doped apatite crystallites in the outer enameloid region are aligned perpendicular to the chewing surface, representing one of the stiffest biomineralized materials found in nature. In the inner enameloid region, the apatite crystals are arranged into intertwisted rods with crystallographic misorientation for increased crack resistance and toughness. At the macroscale, the molariform geometry, the two-layer design based on the outer enameloid and inner dentin, enlarged pulp chamber and the underlying strong bony toothplate work synergistically to contribute to the teeth's crushing resistance.

Microscopic origins of the crystallographically preferred growth in evaporation-induced colloidal crystals.

Unlike crystalline atomic and ionic solids, texture development due to crystallographically preferred growth in colloidal crystals is less studied. Here we investigate the underlying mechanisms of the texture evolution in an evaporation-induced colloidal assembly process through experiments, modeling, and theoretical analysis. In this widely used approach to obtain large-area colloidal crystals, the colloidal particles are driven to the meniscus via the evaporation of a solvent or matrix precursor solution where they close-pack to form a face-centered cubic colloidal assembly. Via two-dimensional large-area crystallographic mapping, we show that the initial crystal orientation is dominated by the interaction of particles with the meniscus, resulting in the expected coalignment of the close-packed direction with the local meniscus geometry. By combining with crystal structure analysis at a single-particle level, we further reveal that, at the later stage of self-assembly, however, the colloidal crystal undergoes a gradual rotation facilitated by geometrically necessary dislocations (GNDs) and achieves a large-area uniform crystallographic orientation with the close-packed direction perpendicular to the meniscus and parallel to the growth direction. Classical slip analysis, finite element-based mechanical simulation, computational colloidal assembly modeling, and continuum theory unequivocally show that these GNDs result from the tensile stress field along the meniscus direction due to the constrained shrinkage of the colloidal crystal during drying. The generation of GNDs with specific slip systems within individual grains leads to crystallographic rotation to accommodate the mechanical stress. The mechanistic understanding reported here can be utilized to control crystallographic features of colloidal assemblies, and may provide further insights into crystallographically preferred growth in synthetic, biological, and geological crystals.

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

Biological systems have a remarkable capability of synthesizing multifunctional materials that are adapted for specific physiological and ecological needs. When exploring structure-function relationships related to multifunctionality in nature, it can be a challenging task to address performance synergies, trade-offs, and the relative importance of different functions in biological materials, which, in turn, can hinder our ability to successfully develop their synthetic bioinspired counterparts. Here, we investigate such relationships between the mechanical and optical properties in a multifunctional biological material found in the highly protective yet conspicuously colored exoskeleton of the flower beetle, Torynorrhina flammea Combining experimental, computational, and theoretical approaches, we demonstrate that a micropillar-reinforced photonic multilayer in the beetle's exoskeleton simultaneously enhances mechanical robustness and optical appearance, giving rise to optical damage tolerance. Compared with plain multilayer structures, stiffer vertical micropillars increase stiffness and elastic recovery, restrain the formation of shear bands, and enhance delamination resistance. The micropillars also scatter the reflected light at larger polar angles, enhancing the first optical diffraction order, which makes the reflected color visible from a wider range of viewing angles. The synergistic effect of the improved angular reflectivity and damage localization capability contributes to the optical damage tolerance. Our systematic structural analysis of T. flammea's different color polymorphs and parametric optical and mechanical modeling further suggest that the beetle's microarchitecture is optimized toward maximizing the first-order optical diffraction rather than its mechanical stiffness. These findings shed light on material-level design strategies utilized in biological systems for achieving multifunctionality and could thus inform bioinspired material innovations.

Strategies for simultaneous strengthening and toughening via nanoscopic intracrystalline defects in a biogenic ceramic.

While many organisms synthesize robust skeletal composites consisting of spatially discrete organic and mineral (ceramic) phases, the intrinsic mechanical properties of the mineral phases are poorly understood. Using the shell of the marine bivalve Atrina rigida as a model system, and through a combination of multiscale structural and mechanical characterization in conjunction with theoretical and computational modeling, we uncover the underlying mechanical roles of a ubiquitous structural motif in biogenic calcite, their nanoscopic intracrystalline defects. These nanoscopic defects not only suppress the soft yielding of pure calcite through the classical precipitation strengthening mechanism, but also enhance energy dissipation through controlled nano- and micro-fracture, where the defects' size, geometry, orientation, and distribution facilitate and guide crack initialization and propagation. These nano- and micro-scale cracks are further confined by larger scale intercrystalline organic interfaces, enabling further improved damage tolerance.

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

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.