Mammalian enamel: A universal tissue and diverse source of inspiration.

The natural armors and weapons of the animal kingdom are serving as inspiration in the development of next-generation engineering materials. In this pursuit, seldom considered are the variations in properties across taxa that have evolved to meet their unique functional demands. Here, teeth from six different mammalian species were acquired and categorized according to their bite force quotient (BFQ), which accounts for the allometric scaling between bite force and body size. Selected chemical, microstructural, and mechanical properties of the enamel were quantified across the enamel thickness using spectroscopy and indentation techniques. Results showed that the chemical composition of enamel was significantly (P <  0.05) different between the Low and High BFQ groups, whereas the apatite crystallinity was not. The enamel of all animals exhibited a spatial gradient in mechanical properties that was consistent when evaluated using a normalized framework. Although the elastic modulus, hardness and indentation brittleness were significantly lower in the High BFQ group, the fracture resistance of enamel was significantly higher in this group, potentially reflective of bite force requirements related to diet and predation. Enamel rod decussation was present in all teeth, but there were differences in specific microstructural features. Overall, these results highlight that the diversity of tooth enamel across species should be considered in the pursuit of nature-inspired structural materials. STATEMENT OF SIGNIFICANCE: Natural weapons are serving as inspiration in the development of next-generation engineering materials. Tooth enamel is a viable candidate, but variations in the structure and properties of enamel across taxa have not been explored. Here, teeth from six different mammalian species were categorized according to their bite force quotient (BFQ), and the enamel was compared in terms of selected chemical, microstructural, and mechanical properties. We show that specific aspects of the chemical composition and properties of the Low and High BFQ groups are unique, which appears reflective of bite forces associated with diet and predation. Overall, the results highlight that the diversity of tooth enamel across species should be considered in the pursuit of nature-inspired structural materials.

Contributions of intermolecular bonding and lubrication to the mechanical behavior of a natural armor.

Among many dermal armors, fish scales have become a source of inspiration in the pursuit of "next-generation" structural materials. Although fish scales function in a hydrated environment, the role of water and intermolecular hydrogen bonding to their unique structural behavior has not been elucidated. Water molecules reside within and adjacent to the interpeptide locations of the collagen fibrils of the elasmodine and provide lubrication to the protein molecules during deformation. We evaluated the contributions of this lubrication and the intermolecular bonding to the mechanical behavior of elasmodine scales from the Black Carp (Mylopharyngodon piceus). Scales were exposed to polar solvents, followed by axial loading to failure and the deformation mechanisms were characterized via optical mechanics. Displacement of intermolecular water molecules by liquid polar solvents caused significant (p ≤ 0.05) increases in stiffness, strength and toughness of the scales. Removal of this lubrication decreased the capacity for non-linear deformation and toughness, which results from the increased resistance to fibril rotations and sliding caused by molecular friction. The intermolecular lubrication is a key component of the "protecto-flexibility" of scales and these natural armors as a system; it can serve as an important component of biomimetic-driven designs for flexible armor systems. STATEMENT OF SIGNIFICANCE: The natural armor of fish has become a topic of substantial scientific interest. Hydration is important to these materials as water molecules reside within the interpeptide locations of the collagen fibrils of the elasmodine and provide lubrication to the protein molecules during deformation. We explored the opportunity for tuning the mechanical behavior of scales as a model for next-generation engineering materials by adjusting the extent of hydrogen bonding with polar solvents and the corresponding interpeptide molecular lubrication. Removal of this lubrication decreased the capacity for non-linear deformation and toughness due to an increase in resistance to fibril rotations and sliding as imparted by molecular friction. We show that intermolecular lubrication is a key component of the "protecto-flexibility" of natural armors and it is an essential element of biomimetic approaches to develop flexible armor systems.

Interfibril hydrogen bonding improves the strain-rate response of natural armour.

Fish scales are laminated composites that consist of plies of unidirectional collagen fibrils with twisted-plywood stacking arrangement. Owing to their composition, the toughness of scales is dependent on the intermolecular bonding within and between the collagen fibrils. Adjusting the extent of this bonding with an appropriate stimulus has implications for the design of next-generation bioinspired flexible armours. In this investigation, scales were exposed to environments of water or a polar solvent (i.e. ethanol) to influence the extent of intermolecular bonding, and their mechanical behaviour was evaluated in uniaxial tension and transverse puncture. Results showed that the resistance to failure of the scales increased with loading rate in both tension and puncture and that the polar solvent treatment increased both the strength and toughness through interpeptide bonding; the largest increase occurred in the puncture resistance of scales from the tail region (a factor of nearly 7×). The increase in strength and damage tolerance with stronger intermolecular bonding is uncommon for structural materials and is a unique characteristic of the low mineral content. Scales from regions of the body with higher mineral content underwent less strengthening, which is most likely the result of interference posed by the mineral crystals to intermolecular bonding. Overall, the results showed that flexible bioinspired composite materials for puncture resistance should enrol constituents and complementary processing that capitalize on interfibril bonds.

Designed for resistance to puncture: The dynamic response of fish scales.

Natural dermal armors are serving as a source of inspiration in the pursuit of "next-generation" structural materials. Although the dynamic strain response of these materials is arguably the most relevant to their performance as armors, limited work has been performed in this area. Here, uniaxial tension and transverse puncture tests were performed on specimens obtained from the scales of Asian carp over strain rates spanning seven decades, from 10-4 to 103 s-1. The importance of anatomical variations was explored by comparing the performance of scales from the head, middle and tail regions. In both loading orientations, the scales exhibited a significant increase in the resistance to failure with loading rate. The rate sensitivity was substantially higher for transverse loading than for in-plane tension, with average strain rate sensitivity exponents for measures of the toughness of 0.35 and 0.08, respectively. Spatial variations in the properties were largest in the puncture responses, and scales from the head region exhibited the greatest resistance to puncture overall. The results suggest that the layered microstructure of fish scales is most effective at resisting puncture, rather than in-plane tension, and its effectiveness increases with rate of loading. X-ray microCT showed that delamination of plies in the internal elasmodine and stretching of the fibrils were key mechanisms of energy dissipation in response to puncture loading. Understanding contributions from the microstructure to this behavior could guide the development of flexible engineered laminates for penetration resistance and other related applications.

The limiting layer of fish scales: Structure and properties.

Fish scales serve as a flexible natural armor that have received increasing attention across the materials community. Most efforts in this area have focused on the composite structure of the predominately organic elasmodine, and limited work addresses the highly mineralized external portion known as the Limiting Layer (LL). This coating serves as the first barrier to external threats and plays an important role in resisting puncture. In this investigation the structure, composition and mechanical behavior of the LL were explored for three different fish, including the arapaima (Arapaima gigas), the tarpon (Megalops atlanticus) and the carp (Cyprinus carpio). The scales of these three fish have received the most attention within the materials community. Features of the LL were evaluated with respect to anatomical position to distinguish site-specific functional differences. Results show that there are significant differences in the surface morphology of the LL from posterior and anterior regions in the scales, and between the three fish species. The calcium to phosphorus ratio and the mineral to collagen ratios of the LL are not equivalent among the three fish. Results from nanoindentation showed that the LL of tarpon scales is the hardest, followed by the carp and the arapaima and the differences in hardness are related to the apatite structure, possibly induced by the growth rate and environment of each fish. STATEMENT OF SIGNIFICANCE: The natural armor of fish, turtles and other animals, has become a topic of substantial scientific interest. The majority of investigations have focused on the more highly organic layer known as the elasmodine. The present study addresses the highly mineralized external portion known as the Limiting Layer (LL). Specifically, the structure, composition and mechanical behavior of the LL were explored for three different fish, including the arapaima (Arapaima gigas), the tarpon (Megalops atlanticus) and the carp (Cyprinus carpio). Results show that there are significant differences in the surface morphology of the LL from posterior and anterior regions in the scales, and between the three species. In addition, the composition of the LL is also unique among the three fish. Results from nanoindentation showed that the LL of tarpon scales is the hardest, followed by the carp and the arapaima and the differences in hardness are related to the apatite structure, possibly induced by the growth rate and environment of each fish. In addition, a new feature was indentified in the LL, which has not been discussed before. As such, we feel this work is unique and makes a significant contribution to the field.

Time dependent deformation behavior of dentin.

OBJECTIVE: The viscoelastic behavior of dentin and its ability to undergo time dependent deformation are considered to be important to oral functions and its capacity to resist fracture. There are spatial variations in the microstructure of dentin within the crown, which could be important to the viscous behavior. However, a spatially resolved description for the viscoelastic behavior of coronal dentin has not been reported. METHODS: In this investigation spherical indentations were made in three regions of coronal dentin including the outer, middle and inner regions. Power law relations were developed to quantitatively describe the stress-strain responses of the tissue. RESULTS: Results showed that the deformation behavior was strongly dependent on the composition (mineral to collagen ratio) and microstructure (tubule density), which contributed to an increase in the rate of viscous deformation with increasing proximity to the pulp. CONCLUSIONS: A model accounting for spatial variations in composition and microstructure was developed to describe the steady-state time dependent deformation behavior of coronal dentin, and a good agreement was found with the experimental results.

Importance of tubule density to the fracture toughness of dentin.

OBJECTIVE: The fracture toughness of dentin is critical to the prevention of tooth fracture. Within the tooth crown, the mechanical properties of dentin are influenced by spatial variations in the density and diameter of the dentin tubules with distance from the pulp. There are also relevant changes to the microstructure of dentin with age. In this investigation the importance of tubule density to the fracture toughness of dentin was evaluated in "young" and "old" age groups. METHODS: The variations in microstructure (density and diameter of tubules) from young and old donor teeth were studied by means of optical microscopy. RESULTS: A reduction in the density and diameter of tubules was identified to occur with aging. An approach previously proposed to study the mechanical behavior of porous materials was used to model the fracture toughness of coronal dentin in terms of the tubule characteristics. Results were then compared with published results from previous studies. CONCLUSIONS: The model predictions were consistent with experimental results for the fracture toughness of dentin from young donor teeth, but overestimated the values that have been reported for "old" dentin.

Effect of chemical composition and microstructure on the mechanical behavior of fish scales from Megalops Atlanticus.

This paper presents an experimental study of the composition, microstructure and mechanical behavior of scales from the Megalops Atlanticus (Atlantic tarpon). The microstructure and composition were evaluated by Scanning Electron Microscopy (SEM) and RAMAN spectroscopy, respectively. The mechanical properties were evaluated in uniaxial tension as a function of position along the length of the fish (head, mid-length and tail). Results showed that the scales are composed of collagen and hydroxyapatite, and these constituents are distributed within three well-defined layers from the bottom to the top of the scale. The proportion of these layers with respect to the total scale thickness varies radially. The collagen fibers are arranged in plies with different orientations and with preferred orientation in the longitudinal direction of the fish. Results from the tensile tests showed that scales from Megalops Atlanticus exhibit variations in the elastic modulus as a function of body position. Additional testing performed with and without the highly mineralized top layers of the scale revealed that the mechanical behavior is anisotropic and that the highest strength was exhibited along the fish length. Furthermore, removing the top mineralized layers resulted in an increase in the tensile strength of the scale.

Effect of aging on the microstructure, hardness and chemical composition of dentin.

OBJECTIVE: Understanding the effects of biological aging on human tissues has been a topic of extensive research. With the increase in healthy seniors and quality of life that topic is becoming increasingly important. In this investigation the effects of aging on the microstructure, chemical composition and hardness of human coronal dentin was studied from a comparison of teeth within "young" and "old" age groups. METHODS: The microstructure of dentin within three regions (i.e., inner, middle and outer) was analyzed using electron and optical microscopy. The mineral-to-collagen ratio in these three regions was estimated using Raman spectroscopy and the hardness was evaluated using microindentation. RESULTS: Results showed that there were significant differences in tubule density, tubule diameter and peritubular cuff diameter with depth. Although there was no difference in tubule density and diameter of the tubules between the age groups, there was a significant difference in the occlusion ratio. A significant increase in hardness between young and old patients was found for middle and outer dentin. An increase in mineral-to-collagen ratio from inner to outer dentin was also found for both groups. In old patients, an increase in mineral content was found in outer coronal dentin as a consequence of tubule occlusion. CONCLUSIONS: An increase in occlusion ratio, hardness, and mineral content was found in the dentin of adult patients with age. This increase is most evident in the outer coronal dentin.