Mechanics and properties of fish fin rays in nonlinear regimes of large deformations.

Fins from ray-finned fishes do not contain muscles, yet fish can change the shape of their fins with high precision and speed, while producing large hydrodynamic forces without collapsing. This remarkable performance has been intriguing researchers for decades, but experiments have so far focused on homogenized properties, and models were developed only for small deformations and small rotations. Here we present fully instrumented micromechanical tests on individual rays from Rainbow trout in both morphing and flexural deflection mode and at large deflections. We then present a nonlinear mechanical model of the ray that captures the key structural elements controlling the mechanical behavior of rays under large deformations, which we successfully fit onto the experiments for property identification. We found that the flexural stiffness of the mineralized layers in the rays (hemitrichs) is 5-6 times lower than their axial stiffness, an advantageous combination to produce stiff morphing. In addition, the collagenous core region can be modeled with spring elements which are 3-4 orders of magnitude more compliant than the hemitrichs. This fibrillar structure provides negligible resistance to shearing from the initial position, but it prevents buckling and collapse of the structure at large deformations. These insights from the experiments and nonlinear models can serve as new guidelines for the design of efficient bioinspired stiff morphing materials and structures at large deformations. STATEMENT OF SIGNIFICANCE: Fins from ray-finned fishes do not contain muscles, yet fish can change the shape of their fins with high precision and speed, while producing large hydrodynamic forces without collapsing. Experiments have so far focused on homogenized properties, and models were developed only for small deformations and small rotations providing limited insight into the rich nonlinear mechanics of natural rays. We present micromechanical tests in both morphing and flexural deflection mode on individual rays, a nonlinear model of the ray that captures the mechanical behavior of rays under large deformations and combine microCT measurements to generate new insights into the nonlinear mechanics of rays. These insights can serve as new guidelines for the design of efficient bioinspired stiff morphing materials and structures at large deformations.

Granular crystals as strong and fully dense architectured materials.

Dense topologically interlocked panels are made of well-ordered, stiff building blocks interacting mainly by frictional contact. Under mechanical loads, the deformation of the individual blocks is small, but they can slide and rotate collectively, generating high strength, toughness, impact resistance, and damage tolerance. Here, we expand this construction strategy to fully dense, 3D architectured materials made of space filling building blocks or "grains." We used mechanical vibrations to assemble 3D printed rhombic dodecahedral and truncated octahedral grains into fully dense face-centered cubic and body-centered cubic "granular crystals." Triaxial compression tests revealed that these granular crystals are up to 25 times stronger than randomly packed spheres and that after testing, the grains can be recycled into new samples with no loss of strength. They also displayed a rich set of mechanisms: nonlinear deformations, crystal plasticity reminiscent of atomistic mechanisms, geometrical hardening, cross-slip, shear-induced dilatancy, and microbuckling. A most intriguing mechanism involved a pressure-dependent "granular crystal plasticity" with interlocked slip planes that completely forbid slip along certain loading directions. We captured these phenomena using a three-length scale theoretical model which agreed well with the experiments. Once fully understood and harnessed, we envision that these mechanisms will lead to 3D architectured materials with unusual and attractive combinations of mechanical performances as well as capabilities for repair, reshaping, on-site alterations, and recycling of the building blocks. In addition, these granular crystals could serve as "model materials" to explore unusual atomic scale deformation mechanisms, for example, non-Schmid plasticity.

Modeling, design and tailoring of a tough, strong and stiff multilayered bone graft material.

Damage tolerance, stiffness, and strength are critical mechanical properties that are difficult to achieve concurrently in synthetic monolithic materials. This limits the range of certain applications, including in bone graft materials where bone-like mechanical reliance is desired. For example, calcium sulfate (CS) is a biologically compatible ceramic that possesses several properties of an ideal bone graft material, but its applications in medicine is limited by its brittleness. Brittleness may be alleviated by the addition of stronger and more ductile reinforcements, with the best mechanical improvements obtained when the layered architecture and the interfaces for these reinforcements are tailored. Here we propose a systematic modeling and design approach to tailor the architecture and properties of a multilayered bone graft material composed of a brittle ceramic and a more ductile material such as metals. More specifically, the volume fraction, moduli, number of layers, and the toughness of the interfaces between the different phases are tailored to maximize overall stiffness, strength, and energy absorption capacity. Our model predicts that when the stiffness of the reinforcement is higher (lower) than the ceramic, the beams with lower (higher) number of layers and higher (lower) volume fraction of metal are stronger. However, while the higher number of layers is always desired in terms of energy dissipation, the effects of other variables is more complex to understand and should thus be studied in conjunction with each other.

Layered Assembly of Graphene Oxide Paper for Mechanical Structures.

Graphene oxide (GO) paper is an attractive material because of high stiffness and strength, light weight, and multiple functionalities. While these properties are now widely exploited in nanoinclusions or flat sheets, three-dimensional (3D) structures from GO paper are not widely studied because of a lack of suitable processing methods. In this study, we report a layered assembly method to make stiff and strong 3D GO structures with the aid of a sodium tetraborate (borax) solution. By comparing mechanical properties of assembled GO paper using water or borax solution, we found that the borax-assembled layers had the highest stiffness. To demonstrate the versatility of our assembly protocol, we then fabricated a variety of 3D structures including I-beams, cylindrical tubes, and bridge-like structures from GO paper. These GO structures were stiff and light weight, and the stiffness to mass ratio was around 2-4 times higher than other polymer samples including cellulose, fluorinated ethylene propylene, and poly(vinyl alcohol). The versatile processing method to make stiff and strong GO structures will enable new engineering applications where nonplanar GO structures are required.

Centrifugation and index matching yield a strong and transparent bioinspired nacreous composite.

Glasses have numerous applications because of their exceptional transparency and stiffness; however, poor fracture, impact resistance, and mechanical reliability limit the range of their applications. Recent bioinspired glasses have shown superior mechanical performance, but they still suffer from reduced optical quality. Here, we present a nacreous glass composite that offers a combination of strength, toughness, and transparency. Micrometer-sized glass tablets and poly(methyl methacrylate) (PMMA) were mixed and structured by centrifugation, creating dense PMMA-glass layers. A transparent composite was created by tuning the refractive index of PMMA to that of glass and using chemical functionalization to create continuous interfaces. The fabrication method is robust and scalable, and the composite may prove to be a glass alternative in diverse applications.

Segmentations in fins enable large morphing amplitudes combined with high flexural stiffness for fish-inspired robotic materials.

Fish fins do not contain muscles, yet fish can change their shape with high precision and speed to produce large and complex hydrodynamic forces-a combination of high morphing efficiency and high flexural stiffness that is rare in modern morphing and robotic materials. These "flexo-morphing" capabilities are rare in modern morphing and robotic materials. The thin rays that stiffen the fins and transmit actuation include mineral segments, a prominent feature whose mechanics and function are not fully understood. Here, we use mechanical modeling and mechanical testing on 3D-printed ray models to show that the function of the segmentation is to provide combinations of high flexural stiffness and high morphing amplitude that are critical to the performance of the fins and would not be possible with rays made of a continuous material. Fish fin-inspired designs that combine very soft materials and very stiff segments can provide robotic materials with large morphing amplitudes and strong grasping forces.

Bioinspired buckling of scaled skins.

Natural flexural armors combine hard, discrete scales attached to soft tissues, providing unique combinations of surface hardness (for protection) and flexibility (for unimpeded motion). Scaled skins are now inspiring synthetic protective materials which offer attractive properties, but which still suffer from limited trade-offs between flexibility and protection. In particular, bending a scaled skin with the scales on the intrados side jams the scales and stiffen the system significantly, which is not desirable in systems like gloves where scales must cover the palm side. Nature appears to have solved this problem by creating scaled skins that can form wrinkles and folds, a very effective mechanism to accommodate large bending deformations and to maintain flexural compliance. This study is inspired from these observations: we explored how rigid scales on a soft membrane can buckle and fold in a controlled way. We examined the energetics of buckling and stability of different buckling modes using a combination of discrete element modeling and experiments. In particular, we demonstrate how scales can induce a stable mode II buckling, which is required for the formation of wrinkles and which could increase the overall flexural compliance and agility of bioinspired protective elements.

Stiff, strong and tough laminated glasses with bio-inspired designs.

Glass is an attractive material with outstanding transparency, hardness, durability and chemical stability. However, the inherent brittleness and low toughness of glass limit its applications. Overcoming the brittleness of glass will help satisfy the rapidly increasing demands of glass in building materials, optical devices, electronics and photovoltaic systems, but it has been a challenge to create glass that is stiff, strong and tough while maintaining its transparency. In this study we explore how the basic design of laminated glass can be enriched with bio-inspired architectures generated with laser engraving. We assess the performance of designs based on continuous plies (90° cross plies, Bouligand), finite glass blocks (segmented Bouligand, nacre-like brick-and-mortar) and hybrid designs. It shows that simultaneous improvements of stiffness, strength and energy absorption upon continuous ply designs can be achieved by promoting delocalized shearing of the polymeric interlayer over brittle fracture of the glass building blocks, and by only placing enriched architectures under tensile deformation so that interlayer shearing can be realized. This principle can be realized simply by adjusting size and arrangement of the building blocks, and by combining continuous plain layers with architectured layers.

Structural and mechanical properties of fish scales for the bio-inspired design of flexible body armors: A review.

Natural protection offered to living beings is the result of millions of years of biological revolution. The protections provided in fishes, armadillos, and turtles by unique hierarchal designs help them to survive in surrounding environments. Natural armors offer protections with outstanding mechanical properties, such as high penetration resistance and toughness to weight ratio. The mechanical properties are not the only key features that make scales unique; they are also highly flexible and breathable. In this study, we aim to review the structural and mechanical characteristics of the scales from ray-finned or teleost fishes, which can be used for new bio-inspired armor designs. It is also essential to consider the hierarchical structure of extinct and existing natural armors. The basic characteristics, as mentioned above, are the foundation for developing high-performance, well-structured flexible natural armors. Furthermore, the present review justifies the importance of interaction between toughness, hardness, and deformability in well-engineered bio-inspired body armor. At last, some suggestions are proposed for the design and fabrication of new bio-inspired flexible body armors.

Plastic Forming of Graphene Oxide Membranes into 3D Structures.

Flat, membrane-like materials made of graphene oxide (GO) nanoflakes have extraordinary mechanical properties including high stiffness, high strength, and low weight. However, the forming of complex nonplanar structures from flat GO membranes is difficult because of the intrinsic brittleness of GO. Here we present a simple and low-cost method to plasticize vacuum-filtrated GO membranes using a cellulose additive. Compared with the pure GO membrane, the GO-cellulose membranes had a lower Young's modulus but significantly improved ductility. Using the flat GO-cellulose membrane, we successfully embossed hemispherical caps with high geometrical fidelity, smooth surfaces, and no tearing or other damages to the membrane. The stiffness of the embossed 3D structure was increased further by cross-linking with a borax solution. Hemispherical caps made of 75 wt % GO with 25 wt % cellulose slurry combining borax cross-linking showed the highest stiffness. This study extends the applications of GO membranes and allows the harnessing of their extraordinary properties to nonplanar structures.

Maximizing the strength of calcium sulfate for structural bone grafts.

Calcium sulfate (CS) combines remarkable properties of biodegradability, biocompatibility, and osteoconductivity but its low strength limits the range of its applications in orthopaedic surgery. In this study we have addressed this limitation by optimizing the fabrication process for pure CS, and by using mechanical testing procedures which are relevant for load carrying, or structural bone grafts (flexural tests in hydrated condition). By optimizing the processing parameters (pressure during setting, CS powder to water ratio, saturated solution) we produced CS samples with the highest flexural strength ever reported in hydrated conditions. Once these optimal conditions are used, the addition of "reinforcing" inclusions in the material decreased its strength because these inclusions actually act as defects instead of reinforcements. In addition, the CS can be formed in precise shapes while maintaining optimal processing conditions and provided a strength similar to that of bone with the same dimensions. Dense and porous materials can be combined to duplicate the trabecular and cortical architecture of long bones, with only a small loss of overall strength.

Discrete element models of tooth enamel, a complex three-dimensional biological composite.

Enamel, the hard surface layer of teeth, is a three-dimensional biological composite made of crisscrossing mineral rods bonded by softer proteins. Structure-property relationships in this complex material have been difficult to capture and usually require computationally expensive models. Here we present more efficient discrete element models (DEM) of tooth enamel that can capture the effects of rod decussation and rod-to-interface stiffness contrast on modulus, hardness, and fracture resistance. Enamel-like microstructures were generated using an idealized biological growth model that captures rod decussation. The orthotropic elastic moduli were modeled with a unit cell, and surface hardness was captured with virtual indentation test. Macroscopic crack growth was also modeled directly through rupture of interfaces and rods in a virtual fracture specimen with an initial notch. We show that the resistance curves increase indefinitely when rod fracture is avoided, with the inelastic region, crack branching, and 3D tortuosity being the main sources of toughness. Increasing the decussation angle simultaneously increases the size of the inelastic region and the crack resistance while decreasing the enamel axial modulus, hardness, and rod stress. In addition, larger contrasts of stiffness between the rods and their interfaces promote high overall stiffness, hardness, and crack resistance. These insights provide better guidelines for reconstructive dental materials, and for development of bioinspired hard materials with unique combinations of mechanical properties. STATEMENT OF SIGNIFICANCE: Enamel is the hardest, most mineralized material in the human body with a complex 3D micro-architecture consisting of crisscrossing mineral rods bonded by softer proteins. Like many hard biological composites, enamel displays an attractive combination of toughness, hardness, and stiffness, owing to its unique microstructure. However few numerical models explore the enamel structure-property relations, as modeling large volumes of this complex microstructure presents computational bottlenecks. In this study, we present a computationally efficient Discrete-element method (DEM) based approach that captures the effect of rod crisscrossing and stiffness mismatch on the enamel hardness, stiffness, and toughness. The models offer new insight into the micromechanics of enamel that could improve design guidelines for reconstructive dental materials and bioinspired composites.

Investigation of surgical adhesives for vocal fold wound closure.

OBJECTIVES: Surgical adhesives are increasingly used for vocal fold microsurgery to assist wound closure and reduce the risks of scar formation. Currently used vocal fold adhesives such as fibrin glue, however, have thus far not been found to promote wound closure or reduce scarring. The objectives of this study were to investigate the mechanical strength and the cytotoxicity of three commercially available adhesives (Glubran 2, GEM, Viareggio, Italy; BioGlue, CryoLife, Kennesaw, GA; and Tisseel, Baxter Healthcare, Deerfield, IL) for vocal fold wound closure. METHODS: Shear and tension tests were performed on 150 porcine larynges. The cytotoxicity of the adhesives to immortalized human vocal fold fibroblasts was investigated using neutral red uptake assays. RESULTS: The average shear adhesive strength for Tisseel, BioGlue, and Glubran 2 was 13.86 ± 5.03 kilopascal (kPa), 40.92 ± 17.94 kPa, and 68.79 ± 13.29 kPa, respectively. The tensile adhesive strength for Tisseel, BioGlue, and Glubran 2 was 10.70 ± 6.42 kPa, 34.27 ± 12.59 kPa, and 46.67 ± 12.13 kPa, respectively. The vocal fold cell viabilities in extracts of Tisseel, BioGlue, and Glubran 2 were 99.27%, 43.05%, and 1.79%, respectively. CONCLUSION: There was a clear tradeoff between adhesive strength and toxicity. The maximum failure strength in shear or tension of the three surgical adhesives ranked from strongest to the weakest was: 1) Glubran 2, 2) BioGlue, and 3) Tisseel. Tisseel was found to be the least toxic of the three adhesives, whereas Glubran 2 was the most toxic. LEVEL OF EVIDENCE: NA Laryngoscope, 129:2139-2146, 2019.

Simultaneous improvements of strength and toughness in topologically interlocked ceramics.

Topologically interlocked materials (TIMs) are an emerging class of architectured materials based on stiff building blocks of well-controlled geometries which can slide, rotate, or interlock collectively providing a wealth of tunable mechanisms, precise structural properties, and functionalities. TIMs are typically 10 times more impact resistant than their monolithic form, but this improvement usually comes at the expense of strength. Here we used 3D printing and replica casting to explore 15 designs of architectured ceramic panels based on platonic shapes and their truncated versions. We tested the panels in quasi-static and impact conditions with stereoimaging, image correlation, and 3D reconstruction to monitor the displacements and rotations of individual blocks. We report a design based on octahedral blocks which is not only tougher (50×) but also stronger (1.2×) than monolithic plates of the same material. This result suggests that there is no upper bound for strength and toughness in TIMs, unveiling their tremendous potential as structural and multifunctional materials. Based on our experiments, we propose a nondimensional "interlocking parameter" which could guide the exploration of future architectured systems.

Tough and deformable glasses with bioinspired cross-ply architectures.

Glasses are optically transparent, hard materials that have been in sustained demand and usage in architectural windows, optical devices, electronics and solar panels. Despite their outstanding optical qualities and durability, their brittleness and low resistance to impact still limits wider applications. Here we present new laminated glass designs that contain toughening cross-ply architectures inspired from fish scales and arthropod cuticles. This seemingly minor enrichment completely transforms the way laminated glass deforms and fractures, and it turns a traditionally brittle material into a stretchy and tough material with little impact on surface hardness and optical quality. Large ply rotation propagates over large volumes, and localization is delayed in tension, even if a strain softening interlayer is used, in a remarkable mechanism which is generated by the kinematics of the plies and geometrical hardening. Compared to traditional laminated glass which degrades significantly in performance when damaged, our cross-ply architecture glass is damage-tolerant and 50 times tougher in energy terms. STATEMENT OF SIGNIFICANCE: Despite the outstanding optical qualities and durability of glass, its brittleness and low resistance to impact still limits its wider application. Here we present new laminated glass designs that contain toughening cross-ply architectures inspired from fish scales and arthropod cuticles. Enriching laminated designs with crossplies completely transforms the material deforms and fractures, and turns a traditionally brittle material into a stretchy and tough material - with little impact on surface hardness and optical quality. Large ply rotation propagates over large volumes and localization is delayed in tension because of a remarkable and unexpected geometrical hardening effect. Compared to traditional laminated glass which degrades significantly in performance when damaged, our cross-ply architecture glass is damage-tolerant and it is 50 times tougher in energy terms. Our glass-based, transparent material is highly innovative and it is the first of its kind. We believe it will have impact in broad range of applications in construction, coatings, chemical engineering, electronics, photovoltaics.

The nonlinear flexural response of a whole teleost fish: Contribution of scales and skin.

The scaled skin of fish is an intricate system that provides mechanical protection against hard and sharp puncture, while maintaining the high flexural compliance required for unhindered locomotion. This unusual combination of local hardness and global compliance makes fish skin an interesting model for bioinspired protective systems. In this work we investigate the flexural response of whole teleost fish, and how scales may affect global flexural stiffness. A bending moment is imposed on the entire body of a striped bass (Morone saxatilis). Imaging is used to measure local curvature, to generate moment-curvature curves as function of position along the entire axis of the fish. We find that the flexural stiffness is the highest in the thick middle portion of the fish, and lowest in the caudal and rostral ends. The flexural response is nonlinear, with an initial soft response followed by significant stiffening at larger flexural deformations. Low flexural stiffness at low curvatures promotes efficient swimming, while higher stiffness at high curvatures enables a possible tendon effect, where the mechanical energy at the end of a stroke is stored in the form of strain energy in the fish skin. To assess the contribution of the scales to stiffening we performed flexural tests with and without scales, following a careful protocol to take in account tissue degradation and the effects of temperature. Our findings suggest that scales do not substantially increase the whole body flexural stiffness of teleost fish over ranges of deformations which are typical of swimming and maneuvering. Teleost scales are thin and relatively flexible, so they can accommodate large flexural deformations. This finding is in contrast to the bulkier ganoid scales which were shown in previous reports to have a profound impact of global flexural deformations and swimming in fish like gar or Polypterus.

A comparative study of bio-inspired protective scales using 3D printing and mechanical testing.

Flexible natural armors from fish, alligators or armadillo are attracting an increasing amount of attention for their unique combinations of hardness, flexibility and light weight. The extreme contrast of stiffness between hard scales and surrounding soft tissues gives rise to unusual and attractive mechanisms, which now serve as models for the design of bio-inspired armors. Despite this growing interest, there is little guideline for the choice of materials, optimum thickness, size, shape and arrangement for the protective scales. In this work, we explore how the geometry and arrangement of hard scales can be tailored to promote scale-scale interactions. We use 3D printing to fabricate arrays of scales with increasingly complex geometries and arrangements, from simple squares with no overlap to complex ganoid-scales with overlaps and interlocking features. We performed puncture tests and flexural tests on each of the 3D printed materials, and we report the puncture resistance - compliance characteristics of each design on an Ashby chart. The interactions between the scales can significantly increase the resistance to puncture, and these interactions can be maximized by tuning the geometry and arrangement of the scales. Interestingly, the designs that offer the best combinations of puncture resistance and flexural compliance are similar to the geometry and arrangement of natural teleost and ganoid scales, which suggests that natural evolution has shaped these systems to maximize flexible protection. This study yields new insights into the mechanisms of natural dermal armor, and also suggests new designs for personal protective systems. STATEMENT OF SIGNIFICANCE: Flexible natural armors from fishes, alligators or armadillos are attracting an increasing amount of attention for their unique and attractive combinations of hardness, flexibility and low weight. Despite a growing interest in bio-inspired flexible protection, there is still little guideline for the choice of materials, optimum thickness, size, shape and arrangement of the protective scales. In this work, we explore how the geometry and arrangement of hard scales affect puncture resistance and flexural compliance, using 3D printing and mechanical testing. Our main finding is that the performance of the scaled skin in terms of puncture resistance can be significantly improved by slight changes in their geometry and arrangement. Our results also suggest that natural evolution has shaped scaled skins to maximize flexible protection. This study yields new insights into the mechanics of natural dermal armors, and also suggests new designs for personal protective systems.

3D-printing and mechanics of bio-inspired articulated and multi-material structures.

3D-printing technologies allow researchers to build simplified physical models of complex biological systems to more easily investigate their mechanics. In recent years, a number of 3D-printed structures inspired by the dermal armors of various fishes have been developed to study their multiple mechanical functionalities, including flexible protection, improved hydrodynamics, body support, or tail prehensility. Natural fish armors are generally classified according to their shape, material and structural properties as elasmoid scales, ganoid scales, placoid scales, carapace scutes, or bony plates. Each type of dermal armor forms distinct articulation patterns that facilitate different functional advantages. In this paper, we highlight recent studies that developed 3D-printed structures not only to inform the design and application of some articulated and multi-material structures, but also to explain the mechanics of the natural biological systems they mimic.

Mechanical properties of striped bass fish skin: Evidence of an exotendon function of the stratum compactum.

Teleost fish skin is a multifunctional natural material with high penetration resistance owing to specialized puncture mechanisms of both the individual scale and the intact scaled integument. In this paper, we explore the possible additional role of the skin in fish undulatory locomotion by examining the structural and mechanical properties of the dermal stratum (s.) compactum layer of striped bass (Morone saxatilis) skin. The structure, mechanical response and function of s. compactum was investigated by combining several methods: optical microscopy and histology, tensile tests on descaled skin specimens in different anatomical locations and orientations, puncture tests, and flexural tests on whole fish with disruption of the s. compactum. Local histological features of the s. compactum, such as collagen fiber angle and degree of crimping, were shown to explain corresponding patterns determined for the tensile properties of the skin along the long axis of the fish, including changes in stiffness, strength and locking strain at stiffening. The fish bending tests demonstrated a tendon-like response of the whole fish and a significant contribution of the s. compactum to the flexural stiffness of the fish. Collectively, the findings show that the s. compactum is a strong tissue with a tendon-like nonlinear response, and which provides an appreciable mechanical protection against sharp puncture and lacerations. Our results also support the theory of an exotendon function of the s. compactum in teleost fish skin. These findings may inspire the design of new multifunctional protective and locomotory systems for a variety of engineering applications.