An Experimental Investigation of Deformation and Fracture of Nacre–Mother of Pearl
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- Barthelat, F. & Espinosa, H.D. Exp Mech (2007) 47: 311. doi:10.1007/s11340-007-9040-1
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Nacre, also known as mother-of-pearl, is a hard biological composite found in the inside layer of many shells such as oyster or abalone. It is composed of microscopic ceramic tablets arranged in layers and tightly stacked to form a three-dimensional brick wall structure, where the mortar is a thin layer of biopolymers (20–30 nm). Although mostly made of a brittle ceramic, the structure of nacre is so well designed that its toughness is several order of magnitudes larger that the ceramic it is made of. How the microstructure of nacre controls its mechanical performance has been the focus of numerous studies over the past two decades, because such understanding may inspire novel composite designs though biomimetics. This paper presents in detail uniaxial tension experiment performed on miniature nacre specimens. Large inelastic deformations were observed in hydrated condition, which were explained by sliding of the tablets on one another and progressive locking generated by their microscopic waviness. Fracture experiments were also performed, and for the first time the full crack resistance curve was established for nacre. A rising resistance curve is an indication of the robustness and damage tolerance of that material. These measurements are then discussed and correlated with toughening extrinsic mechanisms operating at the microscale. Moreover, specific features of the microstructure and their relevance to associated toughening mechanisms were identified. These features and mechanisms, critical to the robustness of the shell, were finely tuned over millions of years of evolution. Hence, they are expected to serve as a basis to establish guidelines for the design of novel man-made composites.
KeywordsBiological materialBiocompositeTensile strengthFractureToughening mechanisms
Many biological organisms utilize hard tissues for structural support (i.e. human skeleton) or armor against external mechanical aggressions (i.e., sea urchin, seashells). Stiffness, which is a critical quality for these tissues, is achieved by incorporating mineral crystals into soft organic matrices . However, incorporating hard and brittle inclusions into soft, resilient matrices also means that the material becomes more brittle and that its toughness drops significantly. Many examples of soft organic matrices saturated with mineral are indeed relatively brittle (tooth enamel, eggshell, prismatic seashell). Some hard mineralized biomaterials, however, seem not to follow this trend. The case of nacre from seashell is a typical example. Nacre is the material that composes the inner layer of many species of gastropods and bivalves. Made of 95% of aragonite (a form of CaCO3, close to calcite), nacre is stiff (E = 60–80 GPa) while maintaining a relatively high toughness (JIC = 1.5 kJ/m2, this is about 1,000 times the toughness of aragonite). Compared with man-made ceramics, nacre is also less sensitive to internal defects and flaws [2, 3], and is relatively strong in tension (the highest tensile strength amongst all the materials used by seashells ). For these reasons nacre has been the focus of intense research for the past twenty years in the materials science community. Elucidating the exact microstructural features and mechanisms responsible for this high toughness and strength is quite relevant, because it may open the way to new generations of composite designed through biomimetics .
2 The Tensile Behavior of Nacre
Nacre in shells is always found as the inner layer of a two-layer armor system. The outer layer is made of hard, but more brittle calcite. There are several situations where the robustness of the shell relies on the tensile strength of nacre. For example a localized pressure, applied by a predator’s bite or the impact of a rock displaced by currents or tidal waves, can be idealized as a point load normal to the shell. The outer layer is hard and prevents penetration, but as a result of the loading the overall shell experiences bending stress. In this case the outer layer is in compression, which is not a concern for the prismatic ceramic it is made of. On the other hand, the inside nacreous layer is in tension, which is often the loading mode leading to failure for ceramics. It is therefore critical for nacre to be strong in tension in the direction tangential to the shell, which is also the direction of the tablets. In the event of a more severe aggression the outside brittle layer may even completely fail, with cracks emanating from the point of impact (much like indentation on brittle materials, where cracks may emanate from the indenter’s corners when a critical load is reached ). When the outside calcite layer is cracked, only the inner nacreous layer can maintain the integrity of the shell, which again involves nacre being strong in tension to resist forces that may pull the shell apart. For these reasons the strength and behavior of nacre in tension is critical to the robustness of the shell, and the behavior of nacre in tension has been central to numerous studies on nacre [3, 5–7, 24].
2.1 Specimen Preparation
2.2 Testing Procedure
2.3 Tensile Experimental Results
3 The Fracture of Nacre
The work of fracture of nacre was determined in the past for nacre from Pinctada margaritifera  along different directions, with the direction across the tablet being the toughest  (which is consistent with resisting cracks generated by tension along the tablets). So far, only single values of toughness were reported for nacre. While single toughness values properly characterize brittle materials with no toughening mechanisms, they might not be sufficient for nacre, because its impressive crack arrest capabilities  suggest more sophisticated, nonlinear failure mechanisms. In the present work stable crack growth and large inelastic regions were observed, and the full crack resistance curve was determined.
3.1 Preliminary Fracture Experiments
As the load was increased, a white region formed ahead of the notch tip. Whitening for nacre has been identified as an indication of tablets sliding and inelastic deformation [3, 6]. The tablets, in the process of sliding apart, generate sub-micron size voids at their periphery that scatter white light and give a whiter appearance to the material (This optical phenomenon is similar to stress-whitening associated with crazing in polymers). As expected, tablet sliding and inelastic deformations initiate at the root of the notch, where tensile stresses are the highest. More strikingly, the inelastic region significantly increased in size before any crack growth was observed [Fig. 10(b, c) and Wang et al. ]. When the crack finally propagated, the inelastic zone had reached about 1 mm in width. The crack propagated in a very stable fashion, the process resembling stable tearing rather than brittle fracture. As the crack advanced it left a wake of inelastically deformed material on either sides of the crack faces [Fig. 10(d)]. Finally, after about 1 mm of crack extension the configuration became unstable and the specimen completely failed. The inelastic zone that appears ahead of the crack tip and in the wake is commonly called process zone, and its associated mechanisms are central to some of the toughest of the engineering ceramics, such as zirconia [33, 34]. For the case of nacre the size of the process zone is remarkably large, which has two consequences. (1) Small scale yielding (s.s.y.) and linear elastic fracture mechanics (LEFM) approximations, as typically used in ceramics, are not valid for nacre (2) The high fracture toughness of nacre is probably associated with the formation of this process zone (which is detailed in the subsequent results section).
3.2 Fracture Specimens
3.3 Experimental Procedure
3.4 Fracture Experimental Results
Single values for nacre toughness were reported in the past, ranging from 4 to 10 MPa.m1/2 for red abalone . Using equation (4) with E′ = 58 GPa, these values translate into a range of 0.3–1.7 kJ/m2, which is consistent with the present results. The toughness measured here is also in the same range as the work of fracture measured in the past for nacre [6, 7]. For comparison, partially stabilized zirconia has a toughness of about JIC = 0.4 kJ/m2 . As discussed in previous work, testing conditions in laboratory and real life loading conditions can be quite different. It has been noted that the stiff testing machines in the laboratories do not store as much energy as predator jaws or crab pincers, which act as “soft machines” [1, 7]. In terms of fracture mechanics this means that an extending crack in nacre tends to be more stable in displacement-controlled conditions (stiff machine) than in load-controlled condition (soft, muscle actuated machine). However, this statement is true for any material. The crack resistance curve determined in this work for nacre is a material property, i.e., it does not depend on the specimen size, geometry or the loading conditions. It was also argued that although nacre had a high toughness, it was not suitable for crack arrest , as opposed to cross lamellar structures with lower toughness but better crack arrest capability . It is true that very often a high toughness is not sufficient for reliability. A rising JR curve means that existing flaws and cracks within the microstructure are stabilized. This is the case because the defects require more and more energy to propagate. The present work shows that nacre actually does have a pronounced rising crack resistance curve, which imparts damage tolerance and also explains the crack arrest performance observed by Currey . In the following section, fracture mechanics models will be used to connect the measured JR curve with the inelastic area around the crack, and with the microstructural features observed in nacre.
3.5 Extrinsic Toughening Mechanisms
Lastly, note that in the fracture experiment the propagation of the crack did not seem to have reached the steady state; which may require several millimeters of crack growth to be attained. For the case of zirconia, models predict that the steady state regime is reached for crack growths equal to about five times the half width of the process zone . For nacre, the same guideline predicts that a crack would reach steady state after a 2.5 mm extension, which seems to be consistent with the trend of Fig. 16. Once the steady state is reached, no additional toughening occurs. This leads to unstable configurations for the crack, and potentially catastrophic failure. The nacreous layer, however, is only about 1–3 mm thick for red abalone, and even thinner for other species. This means that a crack within the nacreous layer of the shell might actually never reach the steady state regime and will always tend to be stabilized.
Nacre is amongst the strongest of the materials found in seashells, and it has a remarkable toughness despite being mostly made of a brittle ceramic. In order to characterize its mechanical performance, tensile and fracture tests were performed on nacre from the shell red abalone (Haliotis rufescens). Millimeter size specimens, miniature loading stage and non-contact optical methods were used in the experiments. The tensile tests highlighted the relatively large inelastic tensile deformations in nacre (at the condition that it is hydrated). These deformations are generated by the microscopic mechanism of tablet sliding, and by the progressive “dovetail-type” locking made possible by their waviness. The same type of inelastic deformations was found in large regions ahead and behind advancing cracks in nacre. Instead, experimental approaches based on nonlinear fracture mechanics revealed a rising crack resistance curve, which is the characteristic of a material that can stabilize and even arrest cracks. The prominent fracture toughening mechanism in nacre was found to be viscoplastic energy dissipation at the biopolymer between tablets, associated with the sliding of the tablets on one another. Advancing a crack though nacre means that virgin material ahead of the tip must deform inelastically, which consumes a significant amount of energy. For this process to have an impact, the inelastic region must spread over large volumes around the crack, which is made possible by the local hardening and progressive locking generated by tablet waviness. While this result yields a new understanding on the source of toughness for nacre, the synergy of mechanisms operating at nano, micro and mesoscales has yet to be captured with combinations of small-scales experiments and multiscale modeling. Such sophisticated microstructures and mechanisms have been finely tuned over millions of year of evolution, in animals that rely on the robustness of their shell for survival. These findings are likely to inspire new composite materials, through biomimetics.
This work was supported by the National Science Foundation through award No. CMS-0301416. We would like to thank Dr. Ken Chong for his encouragement and support during this investigation.