Journal of Structural Biology 194 (2016) 199–204

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Journal of Structural Biology

journal homepage: www.elsevier.com/locate/yjsbi

Damage-tolerance strategies for nacre tablets

Shengnan Wang a,1, Xinqiao Zhu a,1, Qiyang Li b, Rizhi Wang c, Xiaoxiang Wang a,⇑
a
School of Materials Science and Engineering, Zhejiang University, Hangzhou 310027, China
b
School of Aeronautics and Astronautics, Zhejiang University, Hangzhou 310027, China
c
Department of Materials Engineering, University of British Columbia, Vancouver, BC V6T 1Z4, Canada

a r t i c l e i n f o a b s t r a c t

Article history: Nacre, a natural armor, exhibits prominent penetration resistance against predatory attacks. Unraveling
Received 22 October 2015 its hierarchical toughening mechanisms and damage-tolerance design strategies may provide significant
Received in revised form 11 February 2016 inspiration for the pursuit of high-performance artificial armors. In this work, relationships between the
Accepted 15 February 2016
structure and mechanical performance of nacre were investigated. The results show that other than their
Available online 15 February 2016
brick-and-mortar structure, individual nacre tablets significantly contribute to the damage localization of
nacre. Affected by intracrystalline organics, the tablets exhibit a unique fracture behavior. The synergistic
Keywords:
action of the nanoscale deformation mechanisms increases the energy dissipation efficiency of the tablets
Nacre
Nanostructure
and contributes to the preservation of the structural and functional integrity of the shell.
Intracrystalline organics Ó 2016 Elsevier Inc. All rights reserved.
Deformation
Energy dissipation

1. Introduction ning transmission electron microscopy (HAADF-STEM) images

Organisms have developed diverse strategies to synthesize bio-
logical composites that exhibit excellent mechanical properties
(Bruet et al., 2008; Kamat et al., 2000; Killian et al., 2011; Li and
Ortiz, 2014; Meyers et al., 2013, 2008, 2012; Tai et al., 2007;
Weaver et al., 2012). One particularly intriguing material is nacre,
which is found in mollusk shells. Nacre possesses a unique combi-
nation of remarkable strength and toughness and therefore offers
outstanding protection against mechanical attacks (Barthelat and
Espinosa, 2007; Barthelat et al., 2007; Currey, 1977; Gao et al.,
2003; Jackson et al., 1988). Until recently, individual nacre tablets
were not thought to contribute to the high toughness of nacre;
instead, the toughness was attributed to the brick-and-mortar
architecture and precisely designed organic-inorganic interfaces
(Evans et al., 2001; Wang et al., 2012, 2001; Wang and Gupta,
2011) (Fig. 1a). However, recently, elaborate nanostructures within
individual nacre tablets have been reported (Gries et al., 2009;
Suzuki et al., 2011; Wang et al., 2015; Younis et al., 2012)
(Fig. 1b), indicating that the nanoscale architecture may indeed
contribute to the toughening mechanisms of nacre. In contrast to
conventional single crystals, the nacre tablets contain randomly
distributed defects that are visible in the bright-field transmission
electron microscopy (TEM) and high-angle annular dark-field scan-
⇑ Corresponding author.
E-mail address: msewangxx@zju.edu.cn (X. Wang).
1
These authors contributed equally.
shown in Fig. 1c and d. An increased C/Ca ratio, as measured by
energy dispersive X-ray spectroscopy (EDX) (Fig. 1e) and electron
energy loss spectroscopy (ELLS), confirmed that these defects were
intracrystalline organics (Gries et al., 2009; Suzuki et al., 2011;
Wang et al., 2015; Younis et al., 2012). In addition, detailed high
resolution transmission electron microscopy (HRTEM) investiga-
tions demonstrated that the crystal structure of the aragonite scaf-
fold is homogeneous and continuous throughout the whole tablet
and that the trapped intracrystalline organics do not affect the
integrity of the scaffold (Wang et al., 2015).
Meanwhile as the structural study, the mechanical performance
of individual nacre tablet was revealed (Bruet et al., 2005; Huang
and Li, 2013; Huang et al., 2011; Katti et al., 2006; Li et al., 2006,
2004; Sumitomo et al., 2008). The impressions from nanoindenta-
tion tests showed characteristics of plastic deformation (Bruet
et al., 2005; Li et al., 2004). Further investigations demonstrated
that the toughness of the tablet originates from its sophisticated
nanostructure (Huang and Li, 2013; Li et al., 2006). A recent study
reported theoretical calculations that suggest the intracrystalline
organics enhance the fracture resistance of nacre because they
have lower elastic moduli than the aragonite scaffold; however,
no experimental support was provided (Younis et al., 2012). These
studies and calculations indicate that conventional toughing mech-
anisms at the brick-and-mortar level are insufficient to compre-
hensively explain nacre’s damage tolerance. Thus, the nanoscale
deformation mechanisms of the individual nacre tablets must be
investigated.

http://dx.doi.org/10.1016/j.jsb.2016.02.017
1047-8477/Ó 2016 Elsevier Inc. All rights reserved.
200 S. Wang et al. / Journal of Structural Biology 194 (2016) 199–204
Fig. 1. Hierarchical architecture in nacre. (a) Schematic diagram of the brick-and-mortar architecture of nacre. (b) Schematic diagram of the nanostructure in an individual
nacre tablet. (c) Bright-field TEM image and (d) HAADF-STEM image of a nacre tablet. The randomly distributed defects are indicated with arrow heads. (e) EDX spectra from
the areas labeled in (a), showing the increased C/Ca ratio for the defect.
In this work, the origin of the damage localization in nacre
(Pinctada maxima) at multiple scales is determined. Our results
demonstrate that in addition to the brick-and-mortar architecture,
the nanostructure of the individual tablets greatly affects the frac-
ture behavior of nacre. These nanoscale deformation mechanisms
lead to additional energy dissipation and promote the mechanical
optimization of the shell.
2. Experimental section
2.1. Materials
Mature nacre materials from fresh P. maxima shells found in the
South China Sea were chosen for the investigation. To minimize the
detrimental effects from dehydration on the nanostructure and
fracture behavior of the samples, the shells were cleaned and deliv-
ered in ice by airplane to the laboratory. The block nacre samples
were cut from the nacreous layer of the shells with a water-
cooled, low speed diamond saw.
2.2. Nanoindentation and FIB
The (0 0 2) plane of the block nacre samples and the geologic
aragonite samples were successively ground with wet abrasive
paper (up to 800 grit) and polished with a suspension of 20 nm alu-
minum oxide particles. Then, nanoindentation tests were per-
formed on a Nano Indenter G200 (Agilent Technologies) using a
spherical tip with a radius of 1 lm. The maximum load varied from
10 to 100 mN. A Dual Beam System (FEI Quanta 3D FEG) was used
to cut samples from the indentations for TEM (Fig. S1 in the Sup-
porting Information).
2.3. Microindentation and PIPS
Microindentations were performed using an HRD-150 Rockwell
hardness tester at a load of 60 kg. The indented surfaces from two
different samples were then bound together and 0.5 mm thick
slices from the cross-sections of the indentations were cut. After
mechanically grinding the sections to a thickness of 40 lm and
polishing both sides, the sections were glued onto single-hole Cu
microscopy grids. Ion milling was performed using a Precision
Ion Polishing System (Gatan 695). Fig. S2 shows this sample prepa-
ration process.
2.4. SEM and TEM
Prior to SEM and TEM observations, all of the samples were
sputter-coated with a thin film of Pt. SEM micrographs were
acquired using a HITACHI S-4800 field emission scanning electron
microscopy at an accelerating voltage of 5 kV. TEM micrographs
were acquired using a Tecnai G2 F20 field emission transmission
electron microscope at an accelerating voltage of 200 kV.
3. Results
The fracture behavior of nacre in comparison to geologic arago-
nite was investigated via instrumented nanoindentation. A spher-
ical diamond tip with a radius of 1 lm was used to avoid
extrinsic anisotropic mechanical responses. Fig. 2 shows the resid-
ual nanoindentations from five different loads (10, 30, 50, 80, and
100 mN). The geologic aragonite exhibits good fracture resistance
at 10 mN (Fig. 2a). However, as the load increases, radial cracks
appear (50 mN) and cause catastrophic fracture (100 mN). In con-
trast, nacre has a more uniform and localized fracture behavior
(Fig. 2b). To quantitatively analyze the indentations, two parame-
ters were employed: R0, the radius of the residual indentation cra-
ter that was directly in contact with the tip during the test and R1,
the radius of the entire fracture pattern determined by fitting it
with the smallest possible circle (Li and Ortiz, 2014). Ten indenta-
tions were measured for each load and the R1/R0 values are pre-
sented in the histogram in Fig. 3. It is interesting to note that R1/
R0 and the standard deviation increase as the indentation load
increases for geologic aragonite, but these values are relatively
constant for nacre. The results indicate that the damaged area of
the geologic aragonite increases with the load, whereas nacre is
able to confine the fracture within an optimal range at different
loading conditions.
How does nacre achieve damage localization? To determine the
underlying deformation mechanisms of the nacre, cross-sectional
TEM samples of the indentations were prepared using a focused
ion beam (FIB). Fig. 4a shows the damaged region around the
indentation site. The tablets located more than 1 lm away from
 S. Wang et al. / Journal of Structural Biology 194 (2016) 199–204
Fig. 2. SEM images of the nanoindentations in geologic aragonite (a) and nacre (b), at loads of 10, 30, 50, 80, and 100 mN. R0 is the radius of the residual indentation crater
that was directly in contact with the tip during the test and R1 is the radius of the entire fracture pattern determined by fitting it with the smallest possible circle.
Fig. 3. Statistical histogram of R1/R0 in nacre and geologic aragonite.
the indentation impression maintain their original morphology.
Randomly distributed intracrystalline organics in Tablet 3 are
clearly visible (indicated with black arrow heads) in the magnified
bright field TEM image shown in Fig. 4b. The corresponding
selected area electron diffraction (SAED) pattern for Tablet 3 exhi-
bits single crystal diffraction spots (Fig. 4c), indicating that the
structural integrity of the tablet was not destroyed. However, the
severely deformed region just below the indentation contains
crushed tablets (Tablets 1 and 2 in Fig. 4b) and disrupted inter-
lamellar organic interfaces (indicated with black arrows in
Fig. 4b). In contrast to Tablet 3, it is difficult to identify intracrys-
talline organics in Tablets 1 and 2. The SAED pattern obtained from
Tablet 1 has characteristics of a polycrystal (Fig. 4d), indicating for-
mation and reorientation of nanoparticles has occurred. In the dark
field image shown in Fig. 4e, numerous dispersed nanoparticles are
present. The HRTEM image shows the details of the misoriented
nanoparticles (Fig. 4f). The lattice parameters are estimated to be
0.188 nm, 0.287 nm and 0.219 nm for particles 1, 2 and 3, respec-
tively and correspond to the {2 0 2}, {0 0 2} and {2 1 1} crystal planes
of aragonite, respectively (lattice parameters a = 4.9623 Å,
b = 7.968 Å, c = 5.7439 Å, space group Pmcn (62), JCPDS file 41-
1475). The stress-affected tablets on the lateral sides of the impres-
sion are shown in Fig. 4g and h. One can see that the applied load
201
induces fracture of the tablet accompanied by deformation of the
interlamellar organic layers (indicated by white arrows).
The question we must now concern ourselves with is: how does
the crack interact with individual nacre tablets and lead to the for-
mation of nanoparticles? To address this question, TEM samples
with larger deformation regions were prepared by using microin-
dentation combined with Precision Ion Polishing System (PIPS)
milling. As observed in Fig. 5a, the bright field TEM image of the
deformed region shows significant distortion and delamination of
the tablets and elongation and deformation of the interlamellar
organics. In the magnified HAADF-STEM and bright field TEM
images, the interactions between the cracks and the intracrys-
talline organics are identified. Fig. 5b–d shows the crack propaga-
tion pathways inside the individual nacre tablet. Rather than
propagating vertically across the tablet, the crack propagates in a
winding pattern (indicated with the dashed red lines). In Fig. 5b,
we note that the crack encounters some intracrystalline organics
(indicated with arrow heads) during its propagation. In
Fig. 5c and d, densely clustered intracrystalline organics along
the crack propagation pathway are identified. Fig. 5e–g show the
interactions of multiple cracks inside the individual nacre tablet.
The interlaced cracks divide the aragonite scaffold into several par-
ticles (dyed different colors). Compared with the interiors of the
particles, the intracrystalline organics are more concentrated at
the boundaries (indicated with arrow heads). Relative slip of the
fractured tablet was also detected (Fig. 5h).
4. Discussion
The fracture behavior of nacre has been extensively investi-
gated in previous studies that emphasized the effect of its brick-
and-mortar structure. Based on this unique architecture, toughen-
ing mechanisms, such as crack deflection, plate pull-out and the
deformation of organic layers, were established (Kakisawa and
Sumitomo, 2011). In the present study, elongation of interlamellar
organics and delamination of adjacent tablets were observed, thus
confirming the mechanical contributions of the brick-and-mortar
structure. Additionally, the elaborate nanostructure within the
individual tablets greatly influences the fracture behavior of nacre.
Previous investigations have confirmed the existence of
intracrystalline organics inside biogenic minerals (Addadi and
Weiner, 1992; Albeck et al., 1993; Li et al., 2011). For decades, their
effects on the mechanical properties of the crystals have been
202 S. Wang et al. / Journal of Structural Biology 194 (2016) 199–204

Fig. 4. TEM images of the region deformed by nanoindentation. (a) Bright field TEM image of the indentation in cross-section (spherical diamond tip; radius = 1 lm;
maximum load = 30 mN). (b) Magnified bright field TEM image of the area outlined in (a). The intracrystalline organics are indicated with arrow heads and the disrupted
interlamellar organic interfaces are indicated with black arrows. (c) and (d) SAED patterns obtained from the corresponding areas labeled in (b), showing characteristics of
single crystals (c) and polycrystals (d). (e) Dark field TEM image obtained using the diffraction spot indicated by the white circle in (d). (f) HRTEM image taken from the area
labeled in (b), showing the misoriented aragonite nanoparticles. (g) and (h) Magnified bright field TEM images of the areas outlined in (a). The white arrows indicate stretched
interlamellar organics.

addressed (Aizenberg, 2006; Berman et al., 1990; Herman et al.,
1988). Robach et al. (2005) surmised that the occluded organic
macromolecules in biogenic CaCO3 may deflect cracks and thus
increase the total crack length and energy absorbed. Moreover,
Younis et al. (2012) proposed that when the crack propagates
within an inhomogeneous medium, it tends to deflect toward the
regions with lower elastic moduli. As a result, the presence of
organic inclusions in nacre tablets may induce the perturbations
in the crack propagation pathway. Our experiment results support
these speculations. As observed in Fig. 5b–d, the cracks propagate
through the tablets in winding trajectories. More significantly, the
intracrystalline organics are clustered along the crack propagation
paths. In this case, we conclude that compared with the mineral
phase, the cracks may be more likely to propagate along the loca-
tions of the intracrystalline organics – that is, these occluded
organics within the individual tablets may provide a preferred
crack propagation pathway.
In addition to crack propagation, fragmentation of the tablets
was observed. When multiple cracks interlace and interact with
each other, they divide the tablet into several particles (Fig. 5e–
g). The intracrystalline organics around the particles are still
clearly visible. In some situations, the increased stress may lead
to the further fragmentation of these particles, accompanied by
the formation and rotation of the nanocrystals (Tablets 1 and 2
in Fig. 4b). We note that, at this stage, the intracrystalline organics
lost their original morphology and were difficult to identify.
Previous research proposed that the highly ductile biopolymers
found in nacre deform and reform when subjected to the applied
stress (Sumitomo et al., 2011). In this context, the variation in
the morphology of the intracrystalline organics may indicate the
deformation of these bio-macromolecules.
Then, the key question becomes: what is the role of intracrys-
talline organics in crack energy dissipation? One possible role is
the increase of crack propagation path (Fig. 6a). Similar to the pre-
ferred crack deflection along interlamellar organic layers at the
micron scale, a preferential crack propagation pathway within
individual nacre tablets at the nanoscale also exists. In contrast
to propagating vertically across the tablet, the crack follows a ser-
pentine trajectory through the intracrystalline organics, increasing
the crack length and more efficiently dissipating energy. The
intracrystalline organics may also blunt the crack tip (Fig. 6b).
When a crack encounters an organic inclusion, the stress field
around the crack tip is locally released. In this case, an increased
load is required to advance the crack, dissipating additional energy.
In addition to these mechanisms, the fragmentation of the tablet
may also play a critical role in energy dissipation (Fig. 6c). The for-
mation and reorientation of the nanoparticles may induce the
deformation of the intracrystalline organics. Previous investiga-
tions proposed that the biopolymer molecules in nacre have a
modular structure. When loaded in tension, the modular domains
in the molecules repeatedly unfold, resulting in energy dissipation
(Smith et al., 1999; Xu and Li, 2011) (Fig. 6d). In this context,
 S. Wang et al. / Journal of Structural Biology 194 (2016) 199–204 203

Fig. 5. TEM images of the region deformed by microindentation. (a) Bright field TEM image of the distorted tablets showing the delamination and fracture of the tablets. The
white boxes indicate the corresponding areas magnified in (b) (e) and (h). (b) Magnified HAADF-STEM image and (c, d) bright field TEM images of the cracked nacre tablets.
The dashed red lines indicate the crack propagation pathway and the arrow heads indicate the locations of the intracrystalline organics. (e) Magnified HAADF-STEM image
and (f, g) bright field TEM images of the fractured nacre tablets. The particles in the tablet are dyed different colors and the intracrystalline organics are indicated with arrow
heads. (h) Bright-field TEM image of the area outlined in (a). The deformed intracrystalline organics are indicated with arrow heads.

deformation of the intracrystalline organics may lead to additional reorientation and deformation of intracrystalline organics. The
energy absorption. Based on the synergistic effect of these mecha- findings in this work may reveal the origin of nacre’s multi-hit
nisms, catastrophic deformation can be localized to minimum capability and provide design principles for high-performance arti-
tablets, sparing the remaining tablets. ficial composites.

5. Conclusion
In this work, the fracture behavior of nacre from P. maxima was
investigated. The results show that in addition to their brick-and-
mortar structure, the individual tablets also contribute signifi-
cantly to the damage localization in nacre. Individual nacre tablets
have several possible energy dissipation mechanisms, including
crack deflection, crack tip blunting, nanoparticle formation and
Acknowledgements
We acknowledge Dahui Yu from the South China Sea Fisheries
Research Institute for providing the Pinctada maxima shells. We
appreciate the TEM technical support provided by Chuanhong Jin,
Yuewu Zeng and Ya Wang from the Center of Electron Microscope
at Zhejiang University. We also express gratitude to Xiaohui Yan
204 S. Wang et al. / Journal of Structural Biology 194 (2016) 199–204
Fig. 6. Schematic diagrams of nanoscale deformation mechanisms in an individual
nacre tablet. (a) Crack deflection along intracrystalline organics. (b) Crack tip
blunting at the locations of intracrystalline organics. (c) The formation and
reorientation of aragonite nanoparticles. (d) The deformation of intracrystalline
organics induced by nanoparticle rotation.
from The Chinese University of Hong Kong for providing specific
guidance and suggestions for this article.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at http://dx.doi.org/10.1016/j.jsb.2016.02.017.
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