J. Am. Ceram. Soc., 97 [12] 3991–3998 (2014) DOI: 10.1111/jace.13246 © 2014 The American Ceramic Society
Journal
Microstructural Characteristic and its Relation to Mechanical Properties of Clinocardium californiense Shell Hong-Mei Ji,‡ and Xiao-Wu Li‡,§,† ‡
Institute of Materials Physics and Chemistry, College of Sciences, Northeastern University, Shenyang 110819, China
§
Key Laboratory for Anisotropy and Texture Engineering of Materials, Ministry of Education, Northeastern University, Shenyang 110819, China mechanical properties. For instance, to compare the mechanical properties of nacre and a highly mineralized rostral bone of whale, Currey et al.15 performed three-point bending fatigue tests and their results showed that the rostral bone was weaker and more brittle than nacre with extremely wellordered microstructures. Jackson et al.16 also found that the work of fracture for the abalone nacre was 3000 times greater than that of the mineral constituent. The hardness of antler bone and dentin determined via indentation is 0.16–0.21 GPa and 0.49–0.52 GPa, respectively.17,18 In contrast, the hardness of the cross-lamellar structure of Saxidomus purpuratus is as high as 2.7 GPa,5 and it can even reach 3.0–6.0 GPa for conch shell.19 Therefore, the ability of biologic shells to outperform other biomaterials results from their hierarchical structures. Fleischli et al.20 investigated five seashell species with techniques of microindentation, nanoindentation, and single-edge-notched three-point bending, and they reported that the mechanical properties of shells were also affected by the building block (i.e., aragonite platelet) dimensions and matrix weight fraction. So far, most of studies on the mechanical properties of shells have focused on the comparison of different species or the local positions of single species. The important fact, which has been frequently ignored, is that the distribution of microstructures is not unalterable on one shell. The changes in microstructures on different positions should exert specific influences on the mechanical properties of shells. In this work, the systematic examinations of microstructures and relevant mechanical properties of Clinocardium californiense shell were experimentally carried out, in order for further understanding the relationship between the microstructures and mechanical properties for the same shell.
The microstructures and mechanical properties of Clinocardium californiense shell were investigated in relation to the different parts of shell. It is found that the shell can be divided into three parts, that is, the dorsal side, body part, and marginal side based on the variation of microstructures along the longitudinal cross section. Specifically, all areas exhibit a cross-lamellar structure on the dorsal side, and a hierarchical structure comprising three layers including inner (with a crosslamellar structure), middle (with a complex cross-lamellar structure), and outer (with a prismatic structure) layers was observed on the body part, whereas on the marginal side, the orientation of aragonite sheets shows an obvious deflection. The structural architecture, the dimensions of different-order lamellae in the same kind of structure and the orientation between the indenting direction and aragonite sheet all contribute to the unique mechanical properties of this shell. It is also found that a low value of the ratio of hardness-to-Young’s modulus (H/E) corresponds to an improved indentation toughness. The middle layer with the densest and most complicated structure on the body part shows the lowest H/E ratio and the highest hardness and Young’s modulus.
I.
M
Introduction
investigations have been carried out on the microstructures and mechanical properties of mollusk shells, especially in the last few years.1–6 It is now known that mollusk shells are a kind of two-phased composite materials comprising calcium carbonate (~95 wt.%) and protein matrix (~5 wt.%), and their distinctive properties are mainly derived from the well-defined arrangement of microstructures over several length scales, although they present multifarious shapes. Ever since the 1930s, the microstructures of shells have been studied successively in some detail by investigators.7–11 Prismatic, homogeneous, nacreous (columnar and sheet), foliated, crossed-lamellar, and complex crossed-lamellar structures are seven generally accepted kinds of structures for shells,9 among which the cross-lamellar structure built up by aragonite needles (third-order lamellae) is the most widespread in the class Bivalvia.12,13 The aragonite sheets are arranged in bundles to form second-order lamellae, which are rotated 60°–90° against each other to form a first-order lamellae.14 Due to these diverse and exquisite structures coming from natural selection, shells exhibit some noticeably extraordinary UCH
II.
Experimental Procedures
The target material, C. californiense shell, which is a member of the cardiidae family of the class Bivalvia, was taken from the Huang/Bo sea area of China, and all shell specimens were cleaned carefully and dried in air at room temperature. For easily determining the microstructural and mechanical characteristics at different positions, the shell was broken down into three parts, that is, dorsal side, body part, and marginal side, as shown in Fig. 1(a). The straight length from dorsal to marginal side is about 5.5 mm. Dozens of ridges, commonly called growth lines, are arranged in order on the surface of the shell, as marked by dotted lines in Fig. 1(a). In this work, the longitudinal (parallel to the growth lines) cross section was selected as the observation planes [Fig. 1(b)]. Polished specimens at different positions were etched by Ethylene Diamine Tetraacetic Acid (EDTA) for 8 min and then observed by optical microscopy (OM) for structural characterizations. To further reveal the structures in microscale, the directly broken shell samples along the growth line were observed by scanning electron microscopy
R. Ballarini—contributing editor
Manuscript No. 35080. Received May 31, 2014; approved August 19, 2014. † Author to whom correspondence should be addressed. e-mail:
[email protected]
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(SEM). Samples of three parts grinded to fine powders were prepared for X-ray diffraction (XRD) examinations. The mechanical properties examined here are the microhardness H, the Young’s modulus E, and the hardnessto-modulus ratio H/E on those three different parts. Microindentation experiments were performed in an attempt to measure the microhardness on the cross section of this shell, for which the samples were grounded with emery papers from 600 # to 2000 # carefully, and further polished with 0.5 # diamond abrasion paste. On each part three rows of Vicker’s and Knoop’s indents under a load of 200 g were measured from internal to external portions on the longitudinal cross section, as clearly indicated in Fig. 1(c). The values of H/E ratios were evaluated from measurements of Knoop’s indentation dimensions according to the following empirical equation:21 c=d ¼ 1=7:11 0:45 ðH=EÞ where c and d are short and long characteristic diagonal dimensions of Knoop’s indentations, respectively, as shown in Fig. 1(d). In addition, the H value was measured from Vicker’s indentation, and the value of E can be correspondingly determined.
III.
Results and Discussion
(1) Phase Composition and Microstructures Figure 2 shows the XRD patterns obtained from the body part, dorsal, and marginal sides of the shell. The phase compositions of all parts of this shell consist mainly of crystalline CaCO3 (arragonite), for which the main three diffraction peaks are (111), (012), and (221), showing a similar peak intensity distribution in three parts. However, the full width at half maximum (FWHM) of peaks for the marginal side is slightly lower than those for the dorsal side and body part, which means that the grain size of arragonite on the marginal side is smaller than those on the dorsal side and body part. Such a difference in the grain size implies that the deposition velocity of CaCO3 might be varied on different parts during the growth of the shell. The overall view of the longitudinal cross section of C. californiense shell is shown in Fig. 1(b), from which it can be clearly seen that the shell structure exhibits layered features
(a)
Fig. 2. XRD patterns of the dorsal side, body part, and marginal side of C. californiense shell.
in the thickness direction, albeit not evenly distributed in those three parts of the shell. On the dorsal side of the shell, all areas appear to exhibit a cross-lamellar structure, and this structure can be divided into a three-level hierarchy, as presented in Fig. 3. The firstorder lamellae highlighted by red dashed lines in Fig. 3(a) are constructed of the second-order lamellae, which are further comprised of the third-order lamellae (arragonite sheets). Clear observations demonstrate that the morphologies and characteristic dimensions of microstructures are actually different depending on the location from internal to external portions. For example, the coarsest crossed-lamellar feature of the second-order lamellae in the internal portion gradually develops into finely organized and mountain range-like morphologies in the external portion. Specifically, the thickness of the second-order lamellae in the internal portion is ~40 lm, which is larger than those in the middle (~25 lm) and external portions (~20 lm); meanwhile, the thickness of the third-order lamellae also decreases correspondingly from the internal (250–380 nm) to the external (120–250 nm) portion, as presented in Table I.
(b)
(c) (d)
Fig. 1. (a) Overall view of C. californiense shell, (b) OM images of longitudinal cross section of the shell, (c) arrangement of indentations on the cross section, and (d) the illustration of Knoop’s indentation.
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(c)
(d)
(e)
(f)
(g)
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(a)
OM (a) and SEM (b)–(g) images of the microstructures on the cross section of C. californiense shell on the dorsal side.
Fig. 3.
Table I. Dimension of the Different-Order Lamellae in Cross-Lamellar Structure on the Dorsal Side of the C. californiense Shell Portion
2nd-order (lm)
3rd-order (nm)
Degree (bproj)
~40 ~25 ~20
240–380 150–280 120–250
95°–105° 85°–95° 60°–70°
Internal Middle External
The apparent angles between the lamellae on different locations were measured, as seen in Fig. 3. Yang et al.6 have confirmed that the projection angle bproj is higher than the real angle b. Thus, bproj can also reflect angular relation between lamellae as the specimens are examined under the same viewing condition. Obviously, the structure in the external portion shows the smallest angle (~60°–70°), and in the
Table II. Class
Gastropods
Polyplacophora Bivalve
internal portion it exhibits the largest one (~95°–105°). As stated above, the arragonite sheets in the external portions are more finely and densely arranged in the dorsal side. For comparisons, Table II representatively lists the thickness of third-order lamellae in cross-lamellar structure of shells belonging to different classes. For instance, Yang et al.22 reported that the thickness of aragonite sheets in Saxidomus purpuratus belonging to class Bivalve was 200–500 nm. For Pectinidae,14 the thickness is approximately 200 nm. Kamat et al.13 measured the dimensions of the structure of Strombus gigas, which is covered in gastropods, and found that the aragonite sheets are comparably 100–380 nm thick. All those results are close to the measurements of the present C. californiense (100–400 nm). Therefore, such comparisons indicate that there is little difference in the thickness of aragonite sheets (the building block) in various shells. Nonetheless, the dimension of the secondorder lamellae seems to depend upon the species of shell. For
Thickness of the Different-Order Lamellae in Cross-Lamellar Structure of Various Shells Name
First-order lamella (lm)
Strombus gigas Patella vulgata Oliva sayana Littorina littorea Conus litteratus Conus magus Pomatias elegans Acanthopleura revispinosa Pectinidae Saxidomus purpuratus Arca tetragona Clinocardium californiense
5–60 2–8 10–30 2–8.5 13 10–25 7.5–12.5 1.7–5 10–20
Second-order lamella (lm)
5–60 0.25 0.1
2–20
7.5–28 20–40
Third-order lamella (nm)
References
60–380 100–400 50–280 200–400 40–250 100–200 80–280
13 23
200 200–600 80–600 120–380
23 14 22 23 Present work
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(a) (e)
(b)
(d)
(c)
(f)
Fig. 4. OM (a) and SEM (b–f) images of the microstructures on the cross section of C. californiense shell on the body part. (a) OM images of the body part, (b) inner layer, (c) middle layer, (d) outer layer, (e) transition area 1 between inner and middle layers, and (f) transition area 2 between middle layer and outer layers.
(c)
(b)
(a)
(d)
(e)
Fig. 5. OM (a) and SEM (b–e) images of the microstructures on the cross section of C. californiense shell on marginal side. (a) OM images of the marginal side, (b) internal portion, (c)–(d) middle portions, and (e) external portion.
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Fig. 6. Schematic illustration of the overall structure of the C. californiense shell. Note that the “Numbers” standing for the microstructures are marked on the schematic of the cross section.
example, the thickness of the second-order lamellae for the bivalve shells, like Pectinidae14 and the present C. californiense, are very close; however, for gastropods shells, for example, Strombus gigas13 and Conus litteratus,23 the thickness of the second-order lamellae differs greatly from 5–60 lm to 0.1 lm. On the body part of the shell, the layered structure was found to consist clearly of three layers, that is, the inner, middle, and outer layers [Fig. 4(a)]. The microstructures change greatly among these three layers. For example, the inner layer is also featured by a cross-lamellar structure with the aragonite sheets perpendicular to the cross section [Fig. 4(b)], whereas the middle layer exhibits a complex cross-lamellar structure, where the arrangement of the aragonite sheets is much denser and more irregular than that in inner layer [Fig. 4(c)]. In contrast, the outer layer is significantly different from the other two layers as it apparently presents a simple structure called prismatic structure consisting of parallel prisms of ~5 lm in width, as shown in Fig. 4(d). Furthermore, the transition areas between the middle layer with the inner and outer layers were characterized by SEM, respectively, as seen in Figs. 4(e) and (f). Through the detailed detections on the structures of the transition areas, it can be speculated that the arrangement of shell structures experiences a successive change in the process of its growth, that is, the structure becomes densified from inner to middle layers, but loosened from middle to outer layers. On the marginal side of the shell, the most obvious change in microstructures is that the orientation of aragonite sheets
has a deflection from internal to external portions, as shown in Fig. 5. In the internal portion, most of the sheets are perpendicular to the growth lines. On moving to the middle portion, the angle between the arragonite sheets and growth lines turns into ~45°, and eventually the arragonite lamellae become almost parallel to the growth lines in the external portion. Meanwhile, it can be seen that the arrangement of structure becomes gradually looser from internal to external portions in addition to the changes in angular relation. The schematic diagram of the overall structure for the cross section is shown in Fig. 6. The external portions indicated by “7” and “8” of the shell are almost covered by loose structures except for that of “2” on the dorsal side, whereas the dense structures occupy the external portion on the dorsal side, middle layer on the body part, and the internal portion on the marginal side, respectively, as indicated by “2”, “3”, and “4” in Fig. 6. It has been known that the growth lines on seashell reflect the intermittent deposition process of CaCO3, which is deposited from the external to the internal portion in each growth period.24 Thus, such structural distributions observed in this shell might partially indicate that the mineral deposit process roughly follows the numeric order from “1” to “9”, as marked in Fig. 6.
(2) Mechanical Properties The distributions of the average values of microhardness and Young’s modulus along the thickness direction are shown in Fig. 7, from which it can be seen that the mechanical
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(a)
Fig. 8. Distributions of the H/E ratio on three parts of C. californiense shell. Here, note that the unit of H has been transformed into GPa on calculation of the H/E ratios.
(b)
(c)
Fig. 7. Distributions of the hardness and Young’s modulus on dorsal side (a), body part (b), and marginal side (c) of C. californiense shell, along with the schematics of microstructural features at different portions of shell. Note that the Knoop’s indentations in different portions can visually indicate that the diameter of the indented zone is clearly different in the internal, middle and external portions on three parts.
properties exhibit considerable variations, depending upon the microstructures, which are characteristic of the different portions of the shell. The complex crossed-lamellar structure in the body part shows both the highest microhardness (~3.04 GPa) and Young’s modulus (~170 GPa), as seen in Fig. 7(b). Apparently, the irregular and dense arrangement of the sheets in such a unique microarchitecture is crucial for the superior mechanical performances. In 1972, Taylor and layman9 measured microhardness on 70 specimens, and they found that the hardness of the complex crossed-lamellar structure was ~2.84 GPa, which is similar to that measured in the present work. Yang et al.6 have summarized the Young’s moduli of many species of shells measured by bending tests, and found that the Young’s modulus of the complex crossed-lamellar structure also yielded the highest value (~82 GPa). Thus, the complex crossed-lamellar structure shows a great capability to resist the localized deformation. In stark contrast to the complex crossed-lamellar structure, the prismatic structure is the softest structure (H < 1.96 GPa, E < 50 GPa), as seen in Figs. 7(b) and (c). The representative SEM images of the prismatic structure in Figs. 4(d) and 5(e) show that the simple and loose stack of thick prisms cannot efficiently resist the damage localization. Simultaneously, there are many noticeable interfaces between prisms, which might lower the microhardness value to some extent provided the interfaces happen to be indented. In addition to the influence of structural architectures, the dimension and arrangement in the same kind of structure are also important factors contributing to the mechanical properties. For example, on the dorsal side with the crossedlamellar structure, the Young’s modulus increases monotonically from internal to external portions and gradually to an average value of ~80 GPa at the external site. The microhardness first decreases and then increases up to a roughly constant value of 2.70 GPa from internal to external portions. The internal portion exhibits the widest second-order lamellae, the thickest third-order lamellae, and the largest angle included between aragonite sheets, thus resulting in low values of hardness and Young’s modulus. However, the structural dimensions are quite comparable in the middle and external portions; as a result, the hardness reaches a roughly constant value. In short, the values of the Young’s modulus of the crossed-lamellar structure range from 30 to 85 GPa in this shell; such measurements are basically consistent with the values of 87 5 GPa of the crossed-lamellar structure in Pectinidae14 and ~37 GPa in conch shell.25 It should be further pointed out that, on the marginal side of this shell, there exists another factor, that is, the
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orientation between the indenting direction and aragonite sheet, which may also take effect on the mechanical properties to some extent, in addition to the above-mentioned effects of arrangement of the structural architectures and dimensions. For example, as shown in Fig. 7(c), when indentation loading is applied parallel to the aragonite sheets, as the case at the internal portion, the shell exhibits the highest hardness (~2.84 GPa) and Young’s modulus (~65 GPa), whereas the external portion shows very low values of hardness (~1.20 GPa) and Young’s modulus (~23 GPa), as the loading direction is almost perpendicular to the aragonite sheets in this case. In light of the above experimental results, it has been strongly confirmed that such a shell with complex and hierarchical structures exhibits a remarkable mechanical anisotropy, primarily depending on microarchitecture features, the dimension of different-order lamellae, the angle between arragonite sheets, and the orientation between the indenting direction and aragonite sheet. Furthermore, the H/E ratio as an important indicator for the mechanical properties, especially for toughness, was calculated and discussed in term of microstructures. To the best of our knowledge, only Fleischli et al.20 adopted the H/E ratio to characterize the mechanical properties of seashells, and they reported that a low H/E ratio led to an improved fracture toughness by comparing the fracture toughness and H/E ratios of Haliotis rufescens with those of Pteria penguin. Figure 8 shows the distribution of the H/E ratios on three parts of the present C. californiense shell for comparisons. It is found that the H/E ratio has a strong relationship with microstructure, for example, the loose structures located on the internal portion of the dorsal side, the outer layer of the body part and the external portion of the marginal side all show a higher H/E ratio. On the contrary, the middle layer on the body part with the most complicated structure exhibits the lowest one. Our previous work26 have measured the indentation toughness on the body part of the shell, and it was found that the indentation toughness was the highest for the middle layer and the lowest for the outer layer on the body part of C. californiense shell. That is to say, the present results have also confirmed that a lower H/E ratio corresponds indeed to an improved toughness in this shell. By comparison, the H/E ratios of the inner and middle layers on the body part are much lower than those on the dorsal and marginal sides, implying that the body part of the shell actually plays a major role in providing strength to resist the crushing force. In particular, the middle layer on the body part with the most densified and complicated crossed-lamellar structure in this shell is a unique constituent of high hardness (~3.04 GPa), high Young’s modulus (~170 GPa), and high toughness (~0.7 MPam1/2). Therefore, such a complicated crossed-lamellar structure can be considered as a potential biomimetic structure in practical design for fabricating tough engineering ceramic materials.
IV.
Conclusions
The microstructure-dependent mechanical properties on different parts of C. californiense shell were investigated and discussed with the following conclusions: 1. The C. californiense shell consists of three parts, that is, the dorsal side, body part, and marginal side, on which the microstructures are quite different. The dorsal side exhibits cross-lamellar characteristics with portion-dependent structural dimensions. The body part shows an ordered structure comprising three layers, that is, the inner layer with a cross-lamellar structure, the middle layer with a complex cross-lamellar structure, and the outer layer with a prismatic structure. On the marginal side, there exists an obvious deflection of arragonite sheets in addition to the
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difference in the structural densification from internal to external portions. 2. The mechanical properties (hardness H and Young’s modulus E) of the shell are closely dependent upon microarchitecture features, the structural dimension of lamellae, the angle between arragonite sheets, and the orientation between the indenting direction and aragonite sheet. A low value of H/E ratio does reflect an improved indentation toughness. 3. The middle layer with the most densified and complicated crossed-lamellar structure in the body part of the shell exhibits superior mechanical properties, such as the highest hardness, the highest Young’s modulus, and the lowest H/E ratio. Such experimental results may provide beneficial principles for well-designing engineering structural materials with both the high strength and toughness.
Acknowledgments This work was financially supported by the Fundamental Research Funds for the Central University of China under grant nos. N110105001 and N120505001, and partially by the National Natural Science Foundation of China (NSFC) under grant nos. 51231002 and 51271054. Prof. X.W. Li is grateful for the support.
References 1
L. Addadi, D. Joester, F. Nudelman, and S. Weiner, “Mollusk Shell Formation: A Source of new Conception for Understanding Biomineralization Processes,” Chem. Eur. J., 12 [4] 980–7 (2006). 2 A. Y. M. Lin, M. A. Meyers, and K. S. Vecchio, “Mechanical Properties and Structure of Strombus Gigas, Tridacna Gigas, and Haliotis Rufescens sea Shells: A Comparative Study,” Mater. Sci. Eng., C, 26 [8] 1380–9 (2006). 3 M. A. Meyers, P. Y. Chen, A. Y. M. Lin, and Y. Seki, “Biological Materials: Structure and Mechanical Properties,” Prog. Mater Sci., 53 [1] 1–206 (2008). 4 P. Y. Chen, A. Y. M. Lin, Y. S. Lin, Y. Seki, A. G. Stokes, J. Peyras, E. A. Olevsky, M. A. Meyers, and J. McKittrick, “Structure and Mechanical Properties of Selected Biological Materials,” J. Mech. Behav. Biomed. Mater., 1 [3] 208–26 (2008). 5 W. Yang, N. Kashani, X. W. Li, G. P. Zhang, and M. A. Meyers, “Structure Characterization and Mechanical Behavior of a Bivalve Shell (Saxidomus Purpuratus),” Mater. Sci. Eng., C, 31 [4] 724–9 (2011). 6 W. Yang, G. P. Zhang, X. F. Zhu, X. W. Li, and M. A. Meyers, “Structure and Mechanical Properties of Saxidomus Purpuratus Biological Shells,” J. Mech. Behav. Biomed. Mater., 4 [7] 1514–30 (2011). 7 O. B. B/ggild, “The Shell Structure of the Mollusks,” K. Danske Vidensk. Selsk. Skr. Copenhagen, 2, 232–325 (1930). 8 I. Kobayashi, “Internal Microstructure of the Shell of Bivalve Mollusks,” Am. Zool., 9 [3] 663–72 (1969). 9 J. D. Taylor and M. Layman, “The Mechanical Properties of Bivalve (Mollusca) Shell Structures,” Palacontology, 15 [1] 73–87 (1972). 10 J. D. Currey and J. D. Taylor, “The Mechanical Behavior of Some Molluscan Hard Tissues,” J. Zool. Lond, 173 [3] 395–406 (1974). 11 D. Chateigner, C. Hedegaard, and H. R. Wenk, “Mollusc Shell Microstructures and Crystallographic Textures,” J. Struct. Geol., 22 [11–12] 1723–35 (2000). 12 Y. Dauphin, and A. Denis, “Structure and Composition of the Aragonitic Crossed Lamellar Layers in six Species of Bivalvia and Gastropoda,” Comp. Biochem. Phys. A, 126 [3] 367–77 (2000). 13 S. Kamat, X. Su, R. Ballarini, and A. G. Heuer, “Structural Basis for the Fracture Toughness of the Shell of the Conch Strombus Gigas,” Nature, 405, 1036–40 (2000). 14 X. D. Li and P. Nardi, “Micro/Nanomechanical Characterization of a Natural Nanocomposite Material – The Shell of Pectinidae,” Nanotechnology, 15 [1] 211–7 (2004). 15 J. D. Currey, P. Zioupos, P. Davies, and A. Casinos, “Mechanical Properties of Nacre and Highly Mineralized Bone,” Proc. R. Soc. Lond. B, 268 [1462] 107–11 (2001). 16 A. P. Jackson, J. F. V. Vincent, and R. M. Turner, “The Mechanical Design of Nacre,” Proc. R. Soc. Lond. B, 234 [1277] 415–40 (1988). 17 A. G. Evans and E. A. Charles, “Fracture Toughness Determinations by Indentation,” J. Am. Ceram. Soc., 59 [7–8] 371–2 (1976). 18 J. H. Kinney, M. Balooch, S. J. Marshall, G. W. Marshall, and T. P. Weihs, “Hardness and Young’s Modulus of Human Peritubular and Intertubular Dentin,” Arch. Oral Biol., 41 [1] 9–13 (1996). 19 L. Yan, Z. Jie, and W. Lai, “The Structure and Micromechanical Properties of Mollusc Shells,” Chin. J. Mater. Res, 21, 556–60 (2007). 20 F. D. Fleischli, M. Dietiker, C. Borgia, and R. Spolenak, “The Influence of Internal Length Scales on Mechanical Properties in Natural Nanocomposites: A Comparative Study on Inner Layers of Seashells,” Acta Biomater., 4 [6] 1694–706 (2008).
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21 B. R. Marshall, T. Noma, and A. G. Evans, “A Simple Method for Determining Elastic-Modulus-to-Hardness Ratios Using Knoop Indentation Measurements,” J. Am. Ceram. Soc., 65 [10] 175–6 (1982). 22 W. Yang, G. P. Zhang, H. S. Liu, and X. W. Li, “Microstructural Characterization and Hardness Behavior of a Biological Saxidomus Purpuratus Shell,” J. Mater. Sci. Technol., 27 [2] 139–46 (2011). 23 N. V. Wilmot, D. J. Barber, J. D. Taylor, and A. L. Graham, “Electron Microscopy of Molluscan Cross-Lamellar Microstructure,” Phil. Trans. R. Soc. Lond. B, 337 [1279] 21–35 (1992).
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24 G. J. Vermeij, A Natural History of Shells. Princeton University Press, Princeton, 1993. 25 S. Kamat, Toughening Mechanisms in Laminated Composites: A Biomimetic Study in Mollusk Shells. PhD thesis, Department of Materials Science and Engineering, Case Western Reserve University, August 2000. 26 H. M. Ji, W. Q. Zhang, and X. W. Li, “Fractal Analysis of Microstructure-Related Indentation Toughness of Clinocardium Californiense Shell,” Ceram. Int., 40 [5] 7627–31 (2014). h
