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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.
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Exoesqueleto/anatomia & histologia , Exoesqueleto/fisiologia , Besouros/anatomia & histologia , Besouros/fisiologia , Flores/parasitologia , Fenômenos Ópticos , Animais , Fenômenos Biomecânicos , Modelos Biológicos , Fótons , Pigmentação , Espalhamento de RadiaçãoRESUMO
Cuttlefish, a unique group of marine mollusks, produces an internal biomineralized shell, known as cuttlebone, which is an ultra-lightweight cellular structure (porosity, â¼93 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 MNâ 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.
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Materiais Biomiméticos/química , Osso e Ossos/química , Sepia/química , Animais , Fenômenos Biomecânicos , Cerâmica/química , Desenho de Equipamento , Dureza , PorosidadeRESUMO
The elasmoid scales in teleost fish serve as exemplary models for natural fibre composites with integrated flexibility and protection. Yet, limited research has been focused on the potential structural, chemical, and mechanical heterogeneity within individual scales. This study presents systematic characterizations of the elasmoid scales from black drum fish (Pogonias cromis) at different zones within individual scales as a natural fibre composite, focusing on the microscopic structural heterogeneities and corresponding mechanical effects. The focus field at the centre of the scales exhibits a classical tri-layered collagen-based composite design, consisting of the mineralized outermost limiting layer, external elasmodine layer in the middle, and the unmineralized internal elasmodine layer. In comparison, the rostral field at the anterior end of the scales exhibits a two-layered design: the mineralized outermost limiting layer exhibits radii sections on the outer surface, and the inner elasmodine layer consists of collagen fibre-based sublayers with alternating mineralization levels. Chemical and nanoindentation analysis suggests a close correlation between the mineralization levels and the local nanomechanical properties. Comparative finite element modelling shows that the rostral-field scales achieve increased flexibility under both concave and convex bending. Moreover, the evolving geometries of isolated Mandle's corpuscles in the internal elasmodine layer, transitioning from irregular shapes to faceted octahedrons, suggest the mechanisms of mineral growth and space-filling to thicken the mineralized layers in scales during growth, which enhances the bonding strength between the adjacent collagen fibre layers. This work offers new insights into the structural variations in individual elasmoid scales, providing strategies for bioinspired fibre composite designs with local-adapted functional requirements.
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A bioinspired study on replicating the superior damage tolerance of bioceramic composites requires a detailed understanding of the intrinsic properties of biogenic mineral units. Here, we investigate and compare the intrinsic properties of biogenic calcite (Atrina rigida) and aragonite (Sinanodonta woodiana) by conducting microbending experiments on the separated prismatic building blocks. Analyzed bending results indicate that the biogenic calcite has a higher modulus (36.24 ± 14.4 GPa for A. rigida vs. 29.9 ± 10.5 GPa for S. woodiana) and strength (446.5 ± 141.5 MPa for A. rigida vs. 338.6 ± 63.2 MPa for S. woodiana) than the biogenic aragonite, while the nanoindentation results indicate the opposite trend. Further systematic fractographic analysis suggests that the biogenic calcite fractures like amorphous glass, while the biogenic aragonite resembles polycrystalline ceramics. These contradictory behaviors of biogenic calcite and aragonite under tension-dominated (microbending) and indentation loading conditions are attributed to their different intrinsic structures, i.e., intracrystalline organic inclusions in single-crystal calcite vs. interlocked nanograins in polycrystalline aragonite.
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Carbonato de Cálcio , Minerais , Carbonato de Cálcio/química , CerâmicaRESUMO
Biogenic minerals are often reported to be harder and tougher than their geological counterparts. However, quantitative comparison of their mechanical properties, particularly fracture toughness, is still limited. Here we provide a systematic comparison of geological and biogenic calcite (mollusk shell Atrina rigida prisms and Placuna placenta laths) through nanoindentation under both dry and 90% relative humidity conditions. Berkovich nanoindentation is used to reveal the mechanical anisotropy of geological calcite when loaded on different crystallographic planes, i.e., reduced modulus Er{104} ≥ Er{108} > Er{001} and hardness H{001} ≥ H{104} ≥ H{108}, and biogenic calcite has comparable modulus but increased hardness than geological calcite. Based on conical nanoindentation, we elucidate that plastic deformation is activated in geological calcite at the low-load regime (<20 mN), involving r{104} and f{012} dislocation slips as well as e{018} twinning, while cleavage fracture dominates under higher loads by cracking along {104} planes. In comparison, biogenic calcite tends to undergo fracture, while the intercrystalline organic interfaces contribute to damage confinement. In addition, increased humidity does not show a significant influence on the properties of geological calcite and the single-crystal A. rigida prisms, however, the laminate composite of P. placenta laths (layer thickness, â¼250-300 nm) exhibits increased toughness and decreased hardness and modulus. We believe the results of this study can provide a benchmark for future investigations on biominerals and bio-inspired materials.
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Carbonato de Cálcio , Moluscos , Animais , Cristalografia , MineraisRESUMO
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.
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Materiais Biomiméticos , Nácar , Materiais Biomiméticos/química , Biomimética/métodos , Modelos Biológicos , Tomografia Computadorizada por Raios XRESUMO
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.
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Carbonato de Cálcio , Durapatita , Carbonato de Cálcio/química , Durapatita/química , Modelos BiológicosRESUMO
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.
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Equinodermos , Ouriços-do-Mar , Animais , CerâmicaRESUMO
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.
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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 MPaâ 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.
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Dente , Animais , Apatitas , Força de Mordida , Peixes , MoluscosRESUMO
It has been a consistent challenge to develop eco-friendly packaging in its entire life cycle with multiple barriers. Herein, a lignocellulose-derived strategy was developed for enhancing barrier properties of cellulose-based packaging. Porosity and hydrophilicity of paper packaging were remedied by the sequential deposition of oxalic acid modified microfibrillated cellulose (OMFC) and infiltration of nanosized alkaili lignin (NAL). OMFC deposition and NAL infiltration could fill the void among fibers and create hydrophobic micro/nano-roughness on paper surface, which showed synergetic effect on enhancing barrier and mechanical properties by self-bonding and crosslinking between cellulose and lignin. Water vapor transmission rate was reduced by 93 % with initial water contact angle at 113°. Besides, more than four-fold increase in tensile strength along with persisted water and grease resistance were achieved. The result suggests the barrier-enhanced packaging by multilayer surface construction has great potential in bio-based applications considering the biodegradability, biocompatibility, and recyclability.
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Biological cellular materials have been a valuable source of inspiration for the design of lightweight engineering structures. In this process, a quantitative understanding of the biological cellular materials from the individual branch and node level to the global network level in 3D is required. Here we adopt a multiscale cellular network analysis workflow demonstrated in the first paper of this work series to analyze the biomineralized porous structure of sea urchin spines from the species Heterocentrotus mamillatus over a large volume (ca. 0.32mm3). A comprehensive set of structural descriptors is utilized to quantitatively delineate the long-range microstructural variation from the spine center to the edge region. Our analysis shows that the branches gradually elongate (~50% increase) and thicken (~100% increase) from the spine center to edge, which dictates the spatial variation of relative density (from ~12% to ~40%). The branch morphology and network organization patterns also vary gradually with their positions and orientations. Additionally, the analysis of the cellular network of individual septa provides the interconnection characteristics between adjacent septa, which are the primary structural motifs used for the construction of the cellular structure in the edge region. Lastly, combining the extracted long-range cellular network and finite element simulations allows us to efficiently examine the spatial and orientational dependence of local effective Young's modulus across the spine's radius. The structural-mechanical analysis here sheds light on the structural designs of H. mamillatus' porous spines, which could provide important insights for the design and modeling of lightweight yet strong and damage-tolerant cellular materials. STATEMENT OF SIGNIFICANCE: Previous investigations on the cellular structures of sea urchin spines have been mainly based on 2D measurements or 3D quantification of small volumes with limited structural parameters. This limits our understanding of the interplay between the 3D microstructural variations and the mechanical properties in sea urchin spines, which hence constrains the derivation of the underlying principles for bio-inspired designs. This work utilizes our multiscale 3D network analysis, for the first time, to quantify the 3D cellular network and its variation across large volumes in sea urchin spines from individual branch and node level to the cellular network level. The network analysis demonstrated here is expected to be of great interest to the fields of biomineralization, functional biological materials, and bio-inspired material design.
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Estruturas Animais/ultraestrutura , Ouriços-do-Mar/anatomia & histologia , Animais , Carbonato de Cálcio/química , Módulo de Elasticidade , Magnésio/química , Porosidade , TomografiaRESUMO
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.
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Biomineralização , Bivalves/metabolismo , Carbonato de Cálcio/metabolismo , Cerâmica/química , Animais , Simulação por Computador , Modelos BiológicosRESUMO
Man-made armors often rely on rigid structures for mechanical protection, which typically results in a trade-off with flexibility and maneuverability. Chitons, a group of marine mollusks, evolved scaled armors that address similar challenges. Many chiton species possess hundreds of small, mineralized scales arrayed on the soft girdle that surrounds their overlapping shell plates. Ensuring both flexibility for locomotion and protection of the underlying soft body, the scaled girdle is an excellent model for multifunctional armor design. Here we conduct a systematic study of the material composition, nanomechanical properties, three-dimensional geometry, and interspecific structural diversity of chiton girdle scales. Moreover, inspired by the tessellated organization of chiton scales, we fabricate a synthetic flexible scaled armor analogue using parametric computational modeling and multi-material 3D printing. This approach allows us to conduct a quantitative evaluation of our chiton-inspired armor to assess its orientation-dependent flexibility and protection capabilities.
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OBJECTIVE: By means of investigating how the benefit and the influence factors are for the pre-lingual deaf adolescents who received cochlear implantation (CI) METHODS: A questionnaire survey was conducted among 30 prelingually deaf adolescents-cochlear implant recipients, aged 9 approximately 20, 15 of which began to use hearing aid before the age of 6, and 19 of which had received speech testing after the CI, and their families to understand the degree of satisfaction, anticipation of the outcome. Nine of the 15 patients who began to use hearing aid before the age of 6 communicated by the oral communication/labial reading model (oral group), and 10 of the other 15 patients who had not used hearing aid after the age of 6 mainly communicated by sign language (sign group). RESULTS: The satisfaction score of the group with a hearing aid fitting history was 3.93 +/- 0.88, significantly higher than that of the group without a hearing aid fitting history (3.00 +/- 1.13, P < 0.05). The scores of speech production ability in vowel, consonant, single syllable, disyllable, trisyllable, and short sentence in the groups with and without a hearing aid fitting history were 76%/52%, 64%/45%, 71%/26%, 82%/96%, 68%/12%, and 49%/13% respectively (all P < 0.05), and there was no significant difference in the speech production ability in tone (P > 0.05) between these 2 groups. There were no significant differences in the total satisfaction degree, satisfaction degree in speech sound, and satisfaction degree in environmental sound between the oral group and sign group (all P > 0.05). The scores in vowel, consonant, single syllable, disyllable, trisyllable, short sentence, and tone of the oral and sign group were 74%, 60%, 64%, 61%, 57%, 43%, 27% and 43%, 39%, 26%, 26%, 20%, 6%, 5% respectively (all P > 0.01). The anticipation of the patient and the parents about outcome before implantation was negatively correlated with the satisfaction degree after implantation, (gamma = -0.479, P < 0.05). CONCLUSION: Cochlear implantation benefits greatly the deaf adolescent; however, it is necessary to establish a specific evaluation system according to recipients' needs.