sea urchin spines as a model-system for permeable, light-weight ceramics with graceful failure...

Corresponding author: V. Presser E-mail: [email protected]

Journal of Bionic Engineering 6 (2009) 203–213

Sea Urchin Spines as a Model-System for Permeable, Light-Weight Ceramics with Graceful Failure Behavior. Part I. Mechanical

Behavior of Sea Urchin Spines under Compression

V. Presser, S. Schultheiß, C. Berthold, K. G. Nickel Institute for Geosciences, Eberhard-Karls-Universität Tübingen, D-72074 Tübingen, Germany

Abstract The spines of pencil and lance urchins Heterocentrotus mammillatus and Phyllacanthus imperialis were studied as a model

of light-weight material with high impact resistance. The complex and variable skeleton construction (“stereom”) of body and spines of sea urchins consists of highly porous Mg-bearing calcium carbonate. This basically brittle material with pronounced single-crystal cleavage does not fracture by spontaneous catastrophic device failure but by graceful failure over the range of tens of millimeter of bulk compression instead. This was observed in bulk compression tests and blunt indentation experiments on regular, infiltrated and latex coated sea urchin spine segments. Microstructural characterization was carried out using X-ray computer tomography, optical and scanning electron microscopy. The behavior is interpreted to result from the hierarchic structure of sea urchin spines from the macroscale down to the nanoscale. Guidelines derived from this study see ceramics with layered porosity as a possible biomimetic construction for appropriate applications.

Keywords: sea urchin spines, biomimetic, mechanical behavior, compression, calcite Copyright © 2009, Jilin University. Published by Elsevier Limited and Science Press. All rights reserved. doi: 10.1016/S1672-6529(08)60125-0

1 Introduction

Sea urchins (Echinoidea) are a highly diverse and evolutionally very successful group of marine inverte-brates which populated every ocean for over 450 million years. In fact, sea urchins can be found in almost every marine environment from pole to pole and from tidal areas down to depths of more than 5000 meters[1]. The immense diversity in species is also reflected in the

spines of sea urchins which range from very small to very large (30 cm or longer), from very thin to very thick (1 cm or more) and very sharp to completely blunt[1–3]. In this study, we examined sea urchins with blunt, large and thick spines (Fig. 1): Heterocentrotus mammillatus (pencil sea urchin) and Phyllacanthus imperialis (lance sea urchin) which both use their spines (Ø = 1 cm; length up to 12 cm) to wedge themselves into the reef for pro-tection from predators and high tidal energies.

Fig. 1 Photographs of the studied sea urchin species: a) Heterocentrotus mammillatus, b) Phyllacanthus imperialis.

Journal of Bionic Engineering (2009) Vol.6 No.3 204

Spines from these sea urchin species show highly

desirable combination of light-weight construction (up to 60 vol% pore volume; Ref. [4]) with beneficial frac-ture behavior (graceful failure). Both properties can be explained in terms of function and habitat. The open pore volume of sea urchin spines is partially filled with organic material and needs to remain permeable for fluids to enable spine growth and regeneration[1,5]. Fur-thermore, large, fully dense spines would require high expenditure of energy to move and a light-weight con-struction is, therefore, an important way to ensure high mobility with limited musculature[6]. Nonetheless, the spines need to be able to withstand mechanical stress due to high tidal energy environments and predators, which try to pull out the sea urchins from the reef they have wedged themselves into[1,2].

Like all echinoids, sea urchins use magnesium calcite ([CaxMg1-x]CO3) as a basic building material for the highly porous spines[7]. Chemical analysis showed that the magnesium content of sea urchin spines varies between 2 mol% and 15 mol%[2,8,9]. Although earlier described as single-crystals[10–13], newer studies show that sea urchin spines are in fact highly ordered poly-crystalline mesocrystals[5,14–17] consisting of sub-mi-crometer domains (30 nm ~ 50 nm[18], sometimes up to 210 nm[19]) with a very slight misalignment angle be-tween domains (ca. 130 m [19]). In consequence, sea urchin spines do not suffer from the disadvantageous catastrophic crack formation along the {104} cleavage plane but show conchoidal fracture behavior.

Sea urchin spines show great diversity in their mi-crostructure. Pore size, form and distribution vary not only from species to species but also within one sea urchin spine. To aid the description of the local varia-tions of the microstructural architecture of spines and body plates Smith[7] distinguished some basic types of this fenestral Mg-calcite network, called stereom.

Over the last decades, the sea urchin spine micro-structure was used as a template for prosthetic applica-tion[20,21] and photonic crystals[22]. Already in 1969 Weber et al.[6] pointed out that understanding the func-tional elements of sea urchin spine architecture could be the key in developing “new high strength, low density materials”. Our research, therefore, was motivated by the idea to improve the fracture behavior of ceramic bodies by designing a sea urchin spine inspired layered porosity to obtain a macroscopically tough component

from a basically brittle material. This present part of our study describes the basic

beneficial fracture behavior of sea urchin spines and how they reflect the hierarchical structure of the porous carbonate network (stereom). Bulk compression and local pin indentation tests are applied to characterize the mechanical properties while scanning electron micros-copy (SEM), light microscopy and X-ray computer to-mography (X-ray CT) are used to describe microstruc-tural aspects. A later part will provide first results on bioinspired ceramics.

2 Materials and methods

2.1 Sample preparation Spines of Heterocentrotus mammillatus and Phyl-

lacanthus imperialis were used as samples (dried sam-ples without any further treatment from the Philippines). Typical dimensions of these spines range from 60 mm ~ 100 mm in length and 7 mm ~ 13 mm in diameter. For compression tests, 20 mm long axial segments (i.e., along the c-axis) with coplanar ends were cut from the spines. This way, a 2:1 aspect ratio was realized to avoid bending and buckling[6,23].

Spines of living sea urchins are filled with water and minor organic content. In order to investigate the bearing of an infiltration media on the fracture behavior we infiltrated selected spines with gelatine (RUF Le-bensmittelwerk KG, Quakenbrück, Germany), agartine (RUF Lebensmittelwerk KG, Quakenbrück, Germany) and water. Water and gelatine (2 g gelatine in 250 ml water) infiltration were performed at ambient pressure and temperature. For agartine infiltration, the spines were deposited in agartine solution (10 g agartine in 200 ml water) and boiled for two minutes.

In order to elucidate the influence of the original organic material we conducted compression experiments on spine segments of Phyllacanthus imperialis that were removed by disarticulation from living sea urchins only a few minutes before the actual experiment. Other spine segments were heat-treated at 125 C for one week to remove the adsorbed water and most of the interstereom organic material. We chose this temperature to avoid recrystallization of the calcite stereom, which has been observed to become pronounced at temperatures above 150 C[24].

In their natural state, spines of Heterocentrotus mammillatus are covered by a thin epidermal layer[1,25].

Presser et al.: Sea Urchin Spines as a Model-System for Permeable, Light-Weight Ceramics with Graceful Failure Behavior. Part I. Mechanical Behavior of Sea Urchin Spines under Compression 205

The potential bearing of such an external layer on the overall fracture behavior was studied by coating the sea urchin spine segments with latex.

2.2 Mechanical testing procedure

Static compression tests were carried out using a universal testing machine (Instron 4502, Instron Deutschland GmbH, Pfungstadt, Germany) with a con-stant crosshead movement speed of 0.5 mm·min 1. The samples were placed on a plate on the crosshead, pressed against a parallel steel plate above and the resulting force was measured by a force transducer. The total number of tested samples ranged from 5 to 12 (cf. Table 1). During the test the samples were monitored with a video system using two video cameras positioned at different angles relative to the sample to establish a basis for a qualitative in-situ characterization of the fracture behavior.

The testing machine described above was used to drive a blunt tipped hardened stainless-steel pin (Ø = 2 mm) into the sample for indentations tests (carried out on three samples).

Table 1 Compressive strength values (mean value ± standard deviation [number of experiments]) of the tested sea urchin spine samples

Mean compressive strength (MPa)

Heterocentrotus mammillatus

Phyllacanthus imperialis

Dry 47 ± 17 [12] 61 ± 14 [10] Water infiltrated 46 ± 8 [6]

Gelatine infiltrated 42 ± 14 [10] 61 ± 16 [5] Agartine infiltrated 49 ± 13 [6] 66 ± 11 [6]

Latex coated 61 ± 14 [8]

2.3 Sample characterization

The spine microstructure was characterized using

optical light and electron microscopy (LEO® 1450 VP, Carl Zeiss AG, Oberkochen, Germany) before and after compression and indentation tests. SE mode SEM op-erations were carried out using 15 kV as acceleration voltage and the samples were sputter coated with a thin platinum layer.

X-ray computer tomography (X-ray CT) measure-ments before compression tests were done by HeMa-CT (Layher+Waschitschek GbR, Schönaich, Germany) using a Tomoscope® (Werth Messtechnik GmbH, Gies-sen, Germany). For a complete scan, the samples were axially rotated stepwise by 360 with 250 ms duration of exposure (200 mA), resulting in a voxel resolution be-tween 23 μm and 38 μm.

3 Results and discussion

3.1 Microstructure The calcite stereom of sea urchin spines is, apart

from a dense part on the base, highly porous and shows a complex and diverse structure. The macrostructure of the spines of the studied sea urchins differs significantly (Fig. 2). Spines of Heterocentrotus mammillatus show an internal structure with stereom layers separated by more compact layers, which may be interpreted as for-mer shell surfaces or growth marks (Fig. 2a). These compact layers, however, are not completely dense but just porous enough to ensure permeability.

The individual sequences of porous and compact stereom structures are often not uniform and the axial center of the spines has an increased porosity, both in the stereom and the separating layers. The top layer of the spine is a thin epidermal bare skin.

Fig. 2 Microphotographs of a) Heterocentrotus mammillatus and b) Phyllacanthus imperialis spine cross sections.


Medulla (highly porous)

Cortex (thickened edge)

ShaftTip Base

Collar

1 cm

c-axis

(b) Phyllacanthus imperialis

Fig. 2 Continued.

Phyllacanthus imperialisH

eter

ocen

trot

us m

amm

illat

us

Fig. 3 SE-mode SEM images of Heterocentrotus mammillatus and Phyllacanthus imperialis stereom structures. While the typical stereom microstructure is highly porous (a, b), there are thickened areas (c: growth rings and d: cortex).

Spines of Phyllacanthus imperialis have a simpler setup comprising a highly porous inner area (medulla), a somewhat less porous stereom further out and a highly dense outer edge (cortex) (Fig. 2b). The cortex is typically overgrown with small mollusks and calcifying bacteria.

The main microstructure type of the stereom (Fig. 3) can be best described as labyrinthic (Heterocentrotus

mammillatus) or galleried (Phyllacanthus imperialis), using the nomenclature introduced by Smith[7]. The open pore volume varies from almost fully dense (spine base) to approximately 10 vol% (growth marker layer / cortex) and reaches up to 60 vol% in the rest of the stereom. Typical pore size diameters range between 10 μm and 30 μm.


3.2 Fracture behavior under bulk compression 3.2.1 Basic fracture behavior and compressive strength

Under bulk compression, all studied sea urchin spines showed the same qualitative fracture behavior, characterized by graceful failure. Images from the video monitoring system showing characteristic fracture phases are given in Fig. 4 (a: Heterocentrotus mammil-latus, b: Phyllacanthus imperialis).

Time / crosshead travel

Stage 1:

Initial lateral crack

formation

Stage 2:

Axial crack formation and first segment

spallation

Stage 3:

Spallation and

compression of damaged

parts

Stage 4:

Crack formation in remaining

undamaged segment

Fig. 4 Microphotographs showing characteristic stages of the fracture behavior of sea urchin spines under bulk compression.

In the first phase, spines of both studied sea urchin species show initial formation of horizontal cracks which are limited to the very surface of the samples and which usually run around the whole spine. These initial cracks act either as points of origin for cracks running axially upwards or as a stopper for cracks running from the top down which appears at higher loads. This sepa-rates the top part of the specimen into lath-like segments, which eventually spall in the course of further crosshead movement.

It is important to note that while cracks are induced in the upper segments of the spines, the lower part re-mains in an almost completely undamaged state. Only after complete crushing of the upper section between top and ring crack by continued spallation, the next lower section begins to exhibit the same features. Again axial crack formation and spallation of damaged segments happens and this continues until the spine is completely destroyed.

Spines of Phyllacanthus imperialis, as stated before, show the same qualitative fracture behavior. However, the massive outer shell (cortex, cf. Fig. 2) tends to break away in large scales from the inner spine structure.

Fig. 5a gives an example for the force-compression diagram of a sea urchin spine of Heterocentrotus mam-millatus, where the compression of the sample is taken directly from the measured crosshead motion of the machine. Spines of Phyllacanthus imperialis yielded the same qualitative results. Initially the increase in the load yields an elastic response until the measured force de-creases suddenly and significantly due to crack forma-tion accompanied by spallation. As pointed out above, this process is limited to the top section and does not extend into the lower sections. The internal damage of the top section continues until all its parts are spalled or crushed. Then the lower parts of the segment become stressed, carrying similar loads as the initial maximum load. This is reflected by the increase in loading re-corded by the system after the first decrease. Subse-quently we find again and again a slow increase in loading and sudden drops in loading after some time. In fact, the whole spine absorbs energy by crushing and segmentation under bulk compression over almost the whole spine length, that is, tens of millimeters without suffering complete catastrophic failure.

Forc

e (N

)

0.0 0.1 0.2 0.3 0.4 0.5 0.60

2000

4000

6000

8000

Forc

e (N

)

Compression (mm)(b) Porous Al2O3 ceramic (AL25)

Fig. 5 Force-compression diagrams for a) Heterocentrotus mammillatus sea urchin spine and b) conventional porous alumina ceramic. Note the different scaling of the axis in a and b.


This segmental spallation and localized destruction is the key feature of sea urchin spines and the most im-portant difference from traditional porous ceramics, as evidenced by the force-deflection diagram for a con-ventional porous alumina ceramic (Fig. 5b: “AL25” of Friatec AG, Mannheim, Germany; ca. 20 vol% porosity) of comparable sample dimension and geometry (Ø = 9 mm, 20 mm length). Here, after a short distance of (elastic) compression the whole sample suffers catas-trophic failure once a critical load is reached.

From the geometry of the sample we calculated the maximum compressive strength c of the spines from the peak load to the first crack formation (Table 1). The high spread in c between 22 MPa and 84 MPa is in part due to the pronounced heterogeneity of natural materials. Nonetheless there may also be significant differences, because for Heterocentrotus mammillatus we obtained a mean c of 47 ± 17 MPa and for spines of Phyllacanthus imperialis c = 61 ± 14 MPa. These results agree well with the reported values for c of sea urchin spines in the literature. In particular, for spines of Heterocentrotus mammillatus, compressive strength values of 42 MPa ~ 48 MPa were reported[6,20] and Weber et al. [6] reported for Stylocidaris affinis, which belongs to the same family as Phyllacanthus imperialis (Cidarinae), a value for c of 72 MPa.

However, the differences in critical stresses have to be discussed with some caution. The tested samples were segments from natural spines and, therefore, each had a different volume. From the Weibull theory (dis-cussion see below) it is clear that the statistics of reli-ability from samples with distributed critical failure sizes will dictate to find higher strength values in smaller samples. Indeed the spines of Phyllacanthus imperialis with a smaller diameter (Ø = 6 mm ~ 7 mm) showed a higher mean compressive strength ( c = 66 ± 11 MPa) than spines with a larger diameter (Ø = 8 mm ~ 9 mm: c = 54 ± 16 MPa). This size-effect is also in agreement with the study by Currey[26]. The mean values of c below 50 MPa of the especially large spines of Heterocentrotus mammillatus (Ø up to 13 mm) could, thus, be attributed to the statistical volume effect. A later section will dis-cuss the correlation between microstructure and me-chanical fracture behavior in more detail.

Within the experimental error and the scatter due to sample heterogeneity (± 10 MPa ~ 15 MPa), we did not find a difference between freshly disarticulated spines

and spine segments that were dried at 130 C. Schinner et al.[27] reported of differences in elastic modulus and bending strength found for fresh, humid vs. dry, non-macerated spines of spatangoid sea urchins. It is, how-ever, difficult to compare the results from Schinner et al. with our data for three reasons. (1) Compression and bending tests cannot be compared directly. Also, it is important to note that due to the irregular, heterogeneous shape of natural samples, bending tests are more sus-ceptible to systematic errors than compression tests which are carried out on rather cylindrical samples. (2) Spatangoid spines are completely different in their size (Ø 0.3 mm ~ 0.4 mm; several millimeters in length), habitat / spine function (endobenthic organisms: spines are used for burrowing through sediment) and micro-structure (hollow lumen) from the studied spines in this study. (3) Finally, the postulated differences between fresh, humid and dry, nonmacerated spines presented data by Schinner et al.[27] cannot be established based on the high standard deviation of the presented data. Therefore, a clear differentiation or trend cannot be found what, in fact, is in agreement with the data re-ported in this study.

When we look at the force-compression diagrams (Fig. 5a) we see how the measured force decreases sig-nificantly after the initial axial crack formation. The later increase usually will not reach a load as high as the ini-tial maximum load. This, however, does not necessarily correlate with a decrease in compressive strength as the spine diameter decreases due to segment spallation. When we divide the applied force by the real contact area (as determined via the in-situ monitoring camera) and plot the “current” compressive strength against the compression, we see that the compressive strength in fact maintains values between circa 30 MPa ~ 50 MPa for the entire experiment (Fig. 6). This is not unexpected, because a material with identical microstructure should have the compressive stress as a material constant, rela-tivized only by the statistical effects of flaw size distri-butions. We found this to be true for spines of both Heterocentrotus mammillatus and Phyllacanthus impe-rialis.

Another key parameter for materials under com-pressive stress is energy absorption. The integral of the force-compression curve (cp. Fig. 5) yields the absorbed energy and this is plotted against the progressive com-pression in Fig. 7. Here we see that although alumina has


a significantly higher compressive strength, its energy absorption is limited, because after 500 μm of bulk compression catastrophic failure prevents further energy consumption. Although crack formation already starts at loads as low as 2500 N, sea urchin spines can absorb much higher total energies upon compression as illus-trated in Fig. 7, where only the first 10 millimeters of compression are shown.

0 1 2 3 4 5 6 7 8 9 100

10

20

30

40

50

60

Com

pres

sive

stre

ngth

(MPa

)

Compression (mm)

28M

Pa–5

3 M

Pa

Fig. 6 Calculated compressive strength of a typical sea urchin spine segment (Heterocentrotus mammillatus) vs. compression: a high level of compressive strength is maintained.

0 1 2 3 4 5 6 7 8 9 10Compression (mm)

Porous alumina ceramicHeterocentrotus mammillatusPhyllacanthus imperialis Lower sample

segments still undamaged!Catastrophic

failure

02468

101214

Gracefulfailure

Fig. 7 Cumulative energy absorption of sea urchin spines in comparison with a conventional porous ceramic (AL25).

3.2.2 Correlation between microstructure and fracture

behavior Although natural sea urchin spines have a similar

qualitative behavior in compression, they nonetheless show significant scatter in their actual compressive strength and energy consumption. This motivated us to characterize the actual microstructure of spines by non-destructive means (X-ray CT) in advance to com-pression tests.

An example for the influence of the microstructural diversity of the studied samples on the properties is shown in Fig. 8 for the case of a Heterocentrotus mam-millatus spine. The lower spine segment is characterized by a highly porous inner part and dense growth marks running parallel to the spine axis. The upper segment shows several distinct dome-shaped growth marks. These features may explain the differences in the

force-compression curve: the more homogeneous lower part has a higher initial strength but lower energy con-sumption later, when the stabilizing dense marks have spallen. The dome-shaped marks in the upper segment provide crack deflecting horizons, which help to stabi-lize the progress on a higher energy level.

Forc

e (N

)

Fig. 8 X-ray CT-scan of a spine of Heterocentrotus mammillatus in comparison to the resulting force-compression diagrams. Areas with higher density appear as brighter regions.

3.2.3 Influence of infiltration and latex coating

We studied the influence of different infiltration media (in order of increasing viscosity): water, agartine, and gelatine. As shown in Table 1, the compressive strength of samples infiltrated with water, agartine or gelatine was not significantly affected by infiltration. Also, the observed fracture behavior is the same as that of uninfiltrated samples. The same applies for la-tex-coated samples. Here, the coating prevents the fracture debris to be separated from the spine but this loose compound does not positively contribute to the compressive strength after initial crack formation.

3.3 Fracture statistics using the Weibull distribution

For brittle materials, the Weibull theory describes the statistical distribution of observed strength values in a given population. In the plot of failure strength ln( c) against a logarithmic expression of the failure probabil-ity Fi (ln(ln(1/(1 Fi)))) the so called Weibull modulus is obtained as the slope of the linear regression function and is a measure of the reliability of the material. The characteristic fracture strength 0 is taken from this plot as the critical stress, at which 63.2% of the samples have broken.

A Weibull plot of spine segments of Heterocen-trotus mammillatus and Phyllacanthus imperialis is shown in Fig. 9. For this plot the values of all samples (fresh, dried, infiltrated) are included in one plotted set.


The regression yields a fairly well constrained line. This is taken as evidence for the assumption that, to a first approximation, the spread of strength values can be interpreted as due to statistical reasons only and that there are no significant differences between treatments of this type of spine. No significant influence of coating or infiltration was found. A more detailed interpretation of the data in the plot with differences may be possible, but is likely to be an overinterpretation in the light of varying sample sizes and structures.

3.0 3.2 3.4 3.6 3.8 4.0 4.2 4.4 4.6 4.8

3

2

1

0

1

2 Heterocentrotus mammillatus

Phyllacanthus imperialis

ln( c)

m = 3.4

0 = 58 MPan = 38

m = 6.00 = 75 MPa

n = 334

5

Fig. 9 Weibull plot of spine segment samples of Heterocentrotus mammillatus and Phyllacanthus imperialis (n = number of sam-ples analyzed).

A clear difference seems to exist in the comparison between different species. The spines of Phyllacanthus imperialis show a much larger Weibull modulus (6.0) and at the same time higher characteristic fracture toughness (75 MPa) compared with Heterocentrotus mammillatus (3.4 / 58 MPa). In both cases, the data from more than 30 experiments was used (Heterocentrotus mammillatus: 38; Phyllacanthus imperialis: 33). The

spines of Phyllacanthus imperialis have thus a lower variance of failure stresses and this higher reliability of the material may well reflect the greater homogeneity from the more regular type of stereom microstructure.

The differences of the Weibull moduli of Hetero-centrotus mammillatus and Phyllacanthus imperialis may also reflect the different ontogenic history of the two sea urchin species. Heterocentrotus mammillatus is able to regenerate partially damaged or broken spines from any point which creates further discontinuities in the microstructure[28]. However, when a spine of Phyl-lacanthus imperialis is damaged, the spine shaft is first shed before a new shaft is regenerated from the level of the milled ring, preserving a rather uniform and more homogenous microstructure[29]. Consequently, Phylla-canthus imperialis sea urchin spines are expected to show a higher reliability (Weibull modulus).

3.4 Blunt indentation experiments

The graceful failure behavior of sea urchin spines is also well documented by blunt indentation experiments. Fig. 10 is a combination of a force-path diagram and visible macroscopic microstructure of the spine section. The indenter path has straight walls and, thus, the de-struction of the spine microstructure is strictly limited to the indenter pin pathway. Crushed stereom parts are accumulated in front of the more dense growth markers. Each time such a layer is approached the load curve shows a stronger increase with depths. After penetration of the marker layer the force drops again.

Undamagedspine

0 1 2 3 4 5 6 7 80

50

100

150

200

250

300

350

Forc

e (N

)

Pin travel (mm)

Indenter pin path

Fig. 10 Force-path diagram for an indentation test showing that structural deterioration is restricted to the indenter pin pathway.


The interpretation of this behavior is twofold. (1)

The growth marker layers are denser and hence they have higher compression strength. (2) The accumulated debris in front of the travelling pin is pressed into the stereom above the marker layer, which consumes also energy. The accumulation process may also help to cre-ate a thicker dense layer in front of the indenter tip, which might explain the slower increase in force with depth between the markers: only after the build-up of enough stress to press debris into the structure at the side we have a decrease of the curve again.

As a consequence, one should be able to drive a nail easily through this basically brittle material without leading to catastrophic failure. Concepts based on the sea urchin spine architecture, therefore, may well posi-tively contribute for easy handling and machining of derived biomimetic materials.

4 Conclusion

4.1 Hierarchic structuring The special fracture behavior of sea urchin spines is

explained in terms of the hierarchic microstructural setup (Fig. 11).

a) On the nanometer scale, the single-crystal cleavage is compensated with the formation of a highly-ordered polycrystalline mesocrystal causing conchoidal fracture behavior. The slight misalignment of the individual domains and the partially organic inter-phase (referred to as biopolymer mortar by Oaki and Imai[17,30]) cause nanoscale crack deflection and hence an increased toughness, which pushes the strength of the individual dense basic building material. The role of intracrystalline proteins was already pointed out by Berman et al.[31].

b) On the micrometer scale the high porosity of the stereom makes it light but weak. The thinner crosspieces become predetermined breaking points. As described in another part of this paper series, which will deal with FEM simulations, we found that the stress distribution in the stereom is the highest in the crosspieces linking the pores horizontally. Thus, first cracking occurs perpen-dicular to the compression direction, which avoids self-sustaining vertical cracks. This is also directly evi-denced by the appearance of the ring cracks before spallation begins. After a crosspiece is broken the po-rosity avoids crack extension by crack blunting, because

no crack tip is present any more. Further crack initiation then requires introducing a rupture into a juvenile crosspiece segment. This way, the full energy consump-tion potential of the system is conserved. A brittle ma-terial is turned into a crumple zone material.

20 μm

(b) Microscale: predetermined breaking points

2 μm

(a) Nanoscale: compensation of calcite cleavage

150 μm

(c) Macroscale: crack deflection along denser shells

Fig. 11 SEM pictures of fractures of Heterocentrotus mammil-latus. Cracks propagate in the more massive growth rings and lead to separation of small fragments.


c) Nonetheless the presence of larger flaws would induce brittle cracking after a substantial build-up of stress. Here the macroscopic structuring provides an-other helping mechanism: In particular the dome-shaped stacks of denser material in Heterocentrotus mammil-latus make crack deflection possible. Cracks, which would be detrimental to the structure are lead to the outside and support the ordered spallation.

The combination of all these three hierarchic levels explains the beneficial fracture behavior of sea urchin spines and most certainly plays also an important role in examining other mechanical exposure modes like bending which are essential for living sea urchins, too. 4.2 A concept for bioinspired ceramics

As pointed out above, the function of energy ab-sorption may not require a high value of characteristic strength. A constructional concept for sea urchin spine inspired ceramics encompasses predominantly the last two hierarchic levels: on the macro scale we may realize the layered porous architecture with scales of higher and lower porosity to form a laminate structure. This way, segmental delamination improves the impact resistance without catastrophic device failure. Also, the denser shells ensure mechanical stability while the highly po-rous areas enable extreme light-weight construction.

Therefore, our biomimetic ceramics must show at least two different levels of open porosity. This can be realized via different technologies like starch consoli-dation or freeze casting. It is important to ensure that the denser shells are not fully dense so that the other key feature of sea urchin spines, namely permeability, is not lost. The open-pore volume can also be used to introduce further functional elements: Polycaprolactone, or other polymers, as a coating of the pore surface are expected to significantly increase the apparent fracture energy[32]. Infiltration with other media is also a suitable way to tune the electrical conductivity or chemical resistivity of the biomimetic ceramic.

The first hierarchical ordering level, the nanoscale structuring to overcome single-crystal cleavage, may not be important for polycrystalline ceramic bodies. How-ever, by choosing a submicrometer grain size and in-troducing a grain boundary phase, further improvement of the mechanical behavior of biomimetic ceramics can be obtained.

Acknowledgements

The authors gratefully acknowledge the funding of this study by the Landesstiftung Baden-Württemberg foundation as a part of the interdisciplinary project “new materials from bionics”. The workshop of the Institute for Geoscience (N. Walker, B. Maier) is thanked for realizing various modifications on the universal testing machine and constant support throughout the project.

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sea urchin spines as a model-system for permeable, light-weight ceramics with graceful failure...

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