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ARTICLE IN PRESS

Biomaterials 25 (2004) 751–756

Conch shell structure and its effect on mechanical behaviors


D.F. Houa,b, G.S. Zhoua, M. Zhenga,*
a
School of Materials Science and Engineering, Xi’an Jiaotong University, Xi’an 710049, People’s Republic of China
b
School of Mechanical & Material Engineering, China Three Gorges University, Yichang 443002, People’s Republic of China
Received 2 April 2003; accepted 19 June 2003

Abstract

The shell of pink conch is a kind of natural well-designed composite with excellent mechanical properties, which provides us
information for material design. In this paper the microstructures of pink conch shell are characterized by using SEM and TEM.
The microscopic analysis indicates that the pink conch shell is with crossed-lamellar microstructure and the angle between two
second-order lamellae is 70–90 . The cracking and fracture morphologies indicate that the crack deflection, bridge and fiber pullout
are the main toughening mechanisms. Bamboo lamellae are employed to make the simple bio-mimetic model materials. In the model
material the rotated angle between the fibers of each glued lamella varies from 0 to 90 . Three-point-bending is employed to test the
properties of models material, such as the elastic modulus, the flexural strength and the fracture strain energy density. It is found
that the fracture strain energy density of the specimens with the rotated angle between the fibers of the layers about 60 exhibits the
maximum value, which is close to the angle of the two second-order lamellae of the conch shell.
r 2003 Elsevier Ltd. All rights reserved.

Keywords: Conch shell; Microstructure; Self-strengthening; Fracture strain energy density

1. Introduction The idea that structures determine properties pro-


motes scientists to study the microstructures of natural
The Nature of the growth and the self-strengthening materials. Analysis indicates that the natural materials
of the natural materials is very attractive. According to are usually inhomogeneous and multi-phases, multi-
Darwin [1], the reason for the existence of living things is scale structures, or even porous. Most mollusk shells are
that they could evolve and improve themselves in such a composites containing 95 vol% interlocking aragonite
way that their bodies are always compatible with the (CaCO3) platelets staggered in successive lamina and
environment of the surroundings. Therefore, in such a separated by a 5 vol% protein-polysaccharide matrix [5].
sense, it is no doubt that the natural materials are the These shells are with excellent mechanical properties.
most optimized and compatible materials in the world. For example, the hardness and the toughness of nacre
Their structures are highly integrated in natural organ- are 10 and 1000 times as its principal constituent phases
isms, such as biological hard tissues—bone, tooth, and (monolithic CaCO3), respectively [6]. The nacre has
mollusk shell, bark, skin of our body, etc. The laminated laminated structures, which may be the source of its
organization of these structures is inherent at different highly optimized toughness, etc. It might be possible to
spatial scales (nano, micro, meso, macro). They all mimic this natural structure to fabricate load bearing,
exhibit special properties and functions. In the view- heat-resistant, and corrosion-resistant composite mate-
point of material designer, it is beneficial to learn from rial.
all these natural materials. Actually, learning from Recently, much attention has been paid to study
nature has become now one of the hottest subjects in pearl-mother shell, so that excellent material can be
material research [2–4]. designed. In particular, pink conch shell has different
lamellar staggering form from that of pearl-mother
*Corresponding author. Tel.: +86-29-266-5221; fax: +86-29-266- shell. The specific role of cross-laminated structures, the
3453. response of the structure to the load and the effect of the
E-mail address: mszheng@mail.xjtu.edu.cn (M. Zheng). organic-inorganic interfaces on mechanical behavior of

0142-9612/$ - see front matter r 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/S0142-9612(03)00555-6
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752 D.F. Hou et al. / Biomaterials 25 (2004) 751–756

pink conch shell are lacking, though the previous


investigations have indicated the structural character-
istics and the excellent properties of pink conch. In the
present paper, the results of the microstructures and
their effect on the mechanical behaviors of pink conch
shell are reported.

2. Cross-laminated structures of pink conch shell

Pink conch (Strombus gigas, a large predatory


gastropod) is a member of the conus family of shells.
20 µm
The shell has a logarithmic spiral shape. Conus shells
have a cross-lamellar structure that consists of lath-like
Fig. 2. Fracture surface of crossed-lamellar.
aragonite crystals (99.9 wt%) and a tenuous organic
layer (0.1 wt%) [3]. The macroscopic and microscopic composites, it is quite rare to see this kind of structure.
images of the conch shell in different visions are given in Currey showed that the members of the genus Conus
Figs. 1 and 2. Fig. 1 indicates that the microstructures of have characteristically shaped shells [7]. These shells are
conch shell are in three macro-layers. Each macro-layer with crossed-lamellar structures. This tessellated struc-
consists of many crossed sub-lamellas named first-order ture might be the resource of its excellent properties.
lamellas, which can be subdivided into second-order
lamellae. Furthermore, the second-order lamellae are
made up of third-order lamellae, which are considered 3. Brittleness of the shell
single-crystals and multicrystals (see Fig. 3 for details).
Further analysis indicates that each lamella is connected Curry and Kohn [7] performed three-point bending
to its neighbor lamella with proteinaceous adhesive. The experiments to test the mechanical properties of shells of
first-order lamella is with the thickness of 5–30 mm and Conus striatus in different loading faces. They found
several micrometers wide, while the second one is with that the flexural strength of shells is varying in range of
about 5 mm thickness and 5–30 mm wide. The thickness 70–200 MPa with the orientation. Menig et al. [3]
of the lamellae varies to some extents. In some area designed three-point bend and compression experiments
lamellae becomes rather thinner or eventually disap- to test the mechanical properties of shells. Their samples
pears. From Fig. 2, it is clear that each lamella consists were machined with two different directions, i.e., the
of lath-like crystals. The neighbored first-order lamellas parallel and the perpendicular ones with respect to the
have different orientation. Moreover, one lamella shell axis, which corresponds to parallel and perpendi-
rotates its ‘‘lamellar plane’’ an angle about 70–90 with cular directions of the structure of the outer macro-layer
respect to that of its neighborhood layer. The micro- as well. The results reflect that the shells exhibit
scopic plywood sketch map of conch shell is shown in anisotropic properties. However, it needs to declare
Fig. 4, which is similar to that given by Menig [3]. that the shells used by Menig are in dry state. In fact, the
Conclusively, the characteristic of the microstructure property of biomaterial is living dependent due to the
of conch shell is lamellae type, which consists of sub- thin organic layer being vital to its properties. We have
lamellae and lamellae crossing lamellas. In man-made studied the variation of the shell properties with respect
to the time duration after death; it indicates that the
hardness, the brittleness and the flexural strength
increase with the time duration after death, while the
toughness decreases.
Actually, the brittleness reflects the mechanical
responses of micro-mechanisms in material in a sense.
Therefore brittleness can be used as a factor to
characterize the variation of the property in different
orientation with respect to the shell axis.

3.1. Materials and experiments

All samples are cut out from the same shell in order to
Fig. 1. Fracture surface of conch shell. minimize scatter in the tests, care is taken to prepare
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D.F. Hou et al. / Biomaterials 25 (2004) 751–756 753

(a) (b)

(c) (d)

Fig. 3. TEM micrographs of pink shell and diffraction patterns, (a) and (c) TEM micrographs of single-crystal and multicrystal; (b) and (d)
diffraction patterns of single-crystal and multicrystal.

first order Table 1


lamella Comparison of the brittleness of pink conch shell and some kinds of
ceramics
outer
macrolayer Material Comments H=Kc ðmm1=2 Þ
second order
lamella S1 Parallel 0.20
middle
S2 Perpendicular 0.19
macrolayer
third order
NaCl [8] Monocrystal 0.6
lamella SiC [8] Hot-pressed 5
inner
macrolayer Si3N4 [8] Hot-pressed 3
B4C [8] Hot-pressed 13
Fig. 4. Schematic diagram of crossed-lamellar structure of conch shell.

samples. Two types of specimens (S1, S2) are prepared materials are from [8]. The comparison of the brittleness
from the middle macro-layer, i.e., the parallel and the for pink conch shell and ceramic materials is listed in
perpendicular ones with respect to the shell axis, Table 1.
respectively. Micro-hardness tester (MH-5) is employed In general the sole CaCO3 is brittle, which is the main
to perform the tests. component of conch shell, but the conch shell exhibits
rather tough (see Table 1). The resource of the high
3.2. Results and discussions toughness of conch shell might be its special micro-
structure. Therefore it is necessary to study the response
Using indentation mechanics, a simple index of of the microstructure of conch shell to its mechanical
brittleness, the ratio H=Kc ; has been derived in terms properties of the shell in details.
of basic hardness and toughness parameters [8]. Here H In order to understand the excellent toughness
is hardness (resistance to deformation) and Kc is property of the conch shell, the trace of the indentation
toughness (resistance to fracture). test is studied in detail. Fig. 5 is a typical SEM image of
Sarikaya performed four-point bend fracture tough- the indentation feature, which shows many cracks in the
ness tests for pink conch tested [9], the averaged value of middle macro-layer. The damage zones around the
the toughness is 10 MPa/m1/2. Here we employ this indentation reflect the lamellar character of the micro-
value for Kc to conduct H=Kc ; for the pink conch shell. structure. The extension of cracks is not along the
The values of brittleness H=Kc for other ceramic direction of the two diagonals, which is quite different
ARTICLE IN PRESS
754 D.F. Hou et al. / Biomaterials 25 (2004) 751–756

protruding from the fracture surface. These features


are very similar to those of the advanced ceramic
composite, which utilities fiber pullout as a toughening
mechanism. Additionally, the viscoplastic deformation
of the organic layers can enhance the toughness of the
conch shell as well [3]. Conclusively, the complex
architecture of the conch shell plays a key role in
retarding the failure by delocalizing, bridging and
branching cracks. Up to now, the remained problem is
the significance of the specified angle of 70–90 between
the second-order lamellas.

50 µm

Fig. 5. Feature of the indentation on surface perpendicular to the


conch shell axis in the middle macrolayer. 4. Fabrications of structure mimicking materials and its
properties

from those in most monolith materials. It seems that the 4.1. Materials and methods
cracks are trying to find easy ways to extend. In fact
those weak interface (i.e. organic layer) provides the In order to study the nature of the specified angle 70–
easy way. Therefore, the binding forces between the 90 between second-order lamellas structure in the
organic phase and the aragonite layer will hinder the conch shell, mimicking materials are fabricated and
further propagation of the crack. Crack A initials from a tested.
corner of the indentation but extends in the interfaces Bamboo lamella is employed to manufacture multi-
between the first-order lamellas and then bifurcates and lamella materials. Only the middle part of the bamboo is
deflects. Many cracks stretch from crack A and extend taken to conduct the model materials so as to reduce the
through the second and the third-order lamellae. scatters of the properties of the fabricated materials. The
Apparent parallel second-order interfaces in the region bamboo lamella has fibred structures with the elastic
of cracks become visible optically, whereas they are modulus of 17.7 GPa [11]. The bamboo lamella is
invisible in the intact regions (see Fig. 5). Those main machined as a strip with the size about 60  5 
cracks are clearly segmented with the segments follow- 0.4 mm3.
ing inter-lamellar boundaries. Numerous micro-cracks Gluing the bamboo lamellas with polymeric adhesive
are present parallel to these segments. These observa- whose module is about 2 GPa [11] makes the specimen.
tions identify the idea that inter-lamellar boundary is the Each specimen is composed of five lamellas glued
weak interface, and impedes the direct propagation of together. The thickness of adhesive layer is kept about
cracks. The angle between two groups of parallel cracks 0.1 mm, which indicates that the volume fraction of the
is about 70–90 . In some cases, lamella is very thin or adhesive layer is about 0.15. The lamellas in each
even disappears gradually, as shown in Fig. 5. The specimen are numbered as 1, 2, 3, 4 and 5 from upper
delocalization of damage, the abundant crack bridging layer to the lower one. The orientations of the fibers in
and the cracking branching are also very clear. It is well lamellas with the numbers 1, 3 and 5 are identical. While
known that branching crack dissipates more energy and the fibers in the lamellas with the numbers 2 and 4 rotate
enhances the toughness of materials even for the certain angle with respect to their neighbor lamellas, say
structures composing of relatively brittle constituents. lamellas 1, 3 and 5. The rotated angles between glued
On the other hand, the deflecting crack can prolong the fibers of the neighbor lamellas are selected as 0 , 20 ,
propagation path, which could absorb more energy as 45 , 60 , 75 and 90 for each group of specimens,
well, especially the propagation resistance increases respectively. Air bubbles were carefully excluded by
significantly if the crack deflects to a direction with an applying pressure regularly to the platelets. Pockets of
unfavorable stress state [10]. So such a kind of crack adhesive prevented from accumulating by allowing only
deflection results in toughening the conch shell. In the straightest edges to lie side by side. The adhesive was
addition, the multiple cracking is another effective way allowed to cure at 20 C for 48 h.
to enhance the toughness, which can even decrease the Three-point bending test is conducted to study the
orientation dependence of the toughness, since the shell mechanical response of the model materials at a span of
is a composite structure that composes many layers with 40 mm. The mechanical properties, such as the elastic
varying orientations. Fiber pullout often occurs with modulus, the flexural strength and the fracture energy
crack deflection (see Fig. 2a). Laths can be seen density, etc., are evaluated.
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D.F. Hou et al. / Biomaterials 25 (2004) 751–756 755

4.2. Results and discussions 20

18

4.2.1. Elastic modulus and fracture strength 16

Apparent elastic modulus /GPa


Various theoretical models can be used to predict the 14 Test date
elastic modulus of a composite (see Fig. 6). The Voigt 12 Trend curve

model or ‘‘rule-of-mixtures’’ model reflecting a parallel 10


arrangement of fillers and matrix gives [12] 8

Ec ¼ Vf þ ð1  Vf ÞEm ; ð1Þ 6

4
where V ; E; f; m and c reflect the volume fraction, the 2
elastic modulus, the filler, the matrix and the composite,
0
respectively. In the Reuss model the elements are in 0 20 40 60 80 100
series [12] Rotated angle / o
1 Vf ð1  Vf Þ Fig. 7. Variations of elastic modulus vs. rotated angle of bamboo
¼ þ : ð2Þ
Ec Ef Em lamellas.

The predictions of the two models are in dependence


on the volume fraction and the Young’s moduli of the
200
components only.
180
As to our model material, the volume fraction of Test date
160 Trend curve
adhesive is well fixed. Only the elastic modulus of the
specimens with the angle of 0 between neighbor Flexural strength /MPa 140

lamellas can be estimated by Eq. (1) directly, the 120

predicted value is approximately 15.3 GPa. 100


Fig. 7 shows the variations of the elastic modulus for 80
the model materials with respect to the rotated angle
60
between layers. From this figure it is clear that the elastic
40
modulus decreases with the rotated angle, which is also
in agreement with the fact that the static longitudinal 0 20 40 60 80 100

flexure modulus of bamboo is large than the transverse Rotated angle / o



ones. From Fig. 7, the value of the module with 0 Fig. 8. Variation of flexuous strength vs. rotated angle of bamboo
between neighbor lamellas is about 15.7 GPa, which is lamella.
close to the prediction by using Eq. (1) at Vf ¼ 1 
0:15 ¼ 0:85; says 15.3 GPa.
The trend of the variations of the flexural strength samples with 0 rotated angle is about 152 MPa. The
with respect to the rotated angle between the neighbor flexural strengths decrease with the rotated angle till the
lamellas is shown in Fig. 8. Fracture usually occurs in a angle of 90 . The lamellas with rotated angle of 90
series of steps corresponding to the breakage of failures in traverse rupture. It indicates that these
individual lamellar. Flexural failure mostly concentrates specimens can only suffer lower loads.
on the loading regions. The region under neutral surface
along the load ruptures with fiber pullout under tensile 4.2.2. Fracture strain energy density
stressing, the middle region delaminates and the upper Fig. 9 shows the variations of the fracture strain
failures with compression. The mean flexure strength of energy density with respect to the rotated angle between
the neighbor lamellas. The model material with the
rotated angle about 60 exhibits the maximum value of
the fracture strain energy density in Fig. 9, which differs
parallel from those of the elastic modulus and the flexural
Ef Ec
series strength (see Figs. 7 and 8). This special rotated angle,
60 , is quite close to the orientated angle of the lamellas
in conch shell, the latter is around 70 . So the rotated
GPa
GPa

Ec
angle 70–90 of conch shell might result from the
requirement of fracture strain energy density maximum.
The higher fracture strain energy density, the higher
Em the ductility of the material. Material ductile failure is in
filler matrix fact a proper outcome of excessive internal dissipation in
Vm /(Vf +Vm)*100% the viewpoint of physicist. According to modern non-
Fig. 6. Comparative of elastic moduli of parallel and series models. equilibrium thermodynamics—dissipative structure and
ARTICLE IN PRESS
756 D.F. Hou et al. / Biomaterials 25 (2004) 751–756

0.22 Conch shell with crossed-lamellar microstructure


0.20
takes on excellent properties, which gives material
0.18
design a highlight future. One should take into account
fracture energy density /MPa

0.16 Test date the fact that bio-mineralization has evolved over
0.14 Trend curve
0.12
millions of years, while materials science has only
0.10
developed over a century. In any sense, it is sure that
0.08
there is still more to be learned from our world.
0.06
0.04
0.02 Acknowledgements
0 20 40 60 80 100
Rotated angle / o The authors would like to show their thanks to
Fig. 9. Variation of strain energy density vs. rotated angle of bamboo Chinese doctoral project foundation (98069813) and the
lamellas. excellent young teacher program (20022090) for their
kind financial supports.
synergetic theories [13–15], each stable animate body has
to absorb and dissipate energy in some manners so that
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