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Structural Integrity Procedia 00 (2016) 000–000
www.elsevier.com/locate/procedia
ScienceDirect
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Procedia Structural
Structural IntegrityIntegrity
Procedia200
(2016) 042–049
(2016) 000–000
www.elsevier.com/locate/procedia
21st European Conference on Fracture, ECF21, 20-24 June 2016, Catania, Italy
1. Introduction
Fracture mechanics is a relatively young science: we are still working to understand concepts such as the nature
of toughness, the role of microstructure in determining toughness, and the interaction of failure modes in structures,
such as cracking, yielding and buckling. In our work we can take inspiration from Nature, where we find many
examples of toughening mechanisms operating at different length scales and the evolution of structures with good –
in some cases optimal – strength to weight ratios, equipped to resist several competing failure mechanisms. In this
paper I describe some of the recent work carried out in my laboratory. Our aim is to study as wide a variety of
natural, biological materials as possible, applying the engineering techniques of failure analysis, fracture mechanics
and structural integrity to help understand how these materials fulfill their functions in many different types of
animals and plants. For illustration purposes I will focus on three examples. The first example is concerned with the
fracture toughness of eggshell, the development of a novel method to measure this property and its value discussed
in the context of other calcium carbonate materials in nature which display different toughness values as a result of
various toughening mechanisms at the microstructural level. The second example is concerned with crack
propagation in the skeletons of animals and the ability of living systems to detect and repair damage. The third
example considers a leg segment – the tibia of an insect - as an example of an optimized structure taking account of
two competing failure modes.
2. Fracture toughness and toughening mechanisms in nature: eggshell and related materials
2.1. Background
It is immediately evident to anyone with understanding of the concept of toughness that the shells of eggs are
made from a very brittle material. But how brittle exactly? Surprisingly, there have been very few previous
publications on the measurement of fracture toughness (Kc or Gc) in eggshell, and all of these previous studies have
resulted in incorrect values. Mabe et al (2003) reported values of Kc for typical hen’s eggs of the order of
11MPa√m. This value was arrived at by compressing whole eggs between parallel metal platens until failure
occurred: a formula was quoted in the paper, expressing Kc in terms of the failure load and egg dimensions. As far
as I can discover, there is no derivation of this formula in any published paper. In principle it should be possible to
deduce toughness from this type of test, because failure occurs by the propagation of cracks which initiate at the
contact points, so the problem is somewhat similar to that of the cracking of a brittle material during an indentation
test. Macleod et al (2006) developed the mechanics of this phenomenon in considerable detail, though they stopped
short of actually estimating toughness by this approach.
Anyone with a knowledge of the fracture toughness of materials will immediately realise that the above value of
11MPa√m is much too high to be correct. Eggshell is a ceramic material consisting of calcium carbonate crystals
plus a small amount of organic material (various natural polymers). There are almost no ceramic materials with Kc
values greater than 10MPa√m. Furthermore, a simple calculation based on knowledge of the tensile strength of
eggshell would deduce that, given this value of Kc, the critical crack length would be larger than the size of an egg,
implying that eggs will never break by cracking. What is even more worrying is that the work of Mabe et al has
been duplicated by other workers: Xiao et al (2014) used the same approach, with the same equation (though
slightly misquoted in the paper) and obtained similar results, with an average of 12.6MPa√m.
The only other paper which I could find on this subject was by Gosler et al (2011) who measured Gc in the eggs
of the Great Tit by measuring the energy to cut samples using a scissors. Their results were very varied (0.5-
17kJ/m2): when converted to Kc these give values of the same order of magnitude as above. So we can conclude
that, up to now, there have been no reliable measurements made of the fracture toughness of eggshell. This is really
remarkable considering the importance of eggs, and the fact that small cracks formed during their handling and
transport are responsible for considerable wastage of the product and also give rise to health risks.
44 David Taylor / Procedia Structural Integrity 2 (2016) 042–049
Author name / Structural Integrity Procedia 00 (2016) 000–000 3
To fill this gap, we devised a novel way to measure fracture toughness (Taylor et al 2016). The test rig is
illustrated in figure 1. It is based on the principle that if a thin walled hollow sphere is compressed along its poles, a
very simple state of stress arises at locations remote from the loading points. Bending is prevented, leaving a biaxial
membrane stress consisting of a compressive stress normal to an equal and opposite tensile stress. It is the tensile
stress, which acts in the circumferential direction around the equator of the sphere, which is of interest here. At the
equator this stress has a magnitude given by (for an applied force F, sphere radius b and thickness t):
F
(1)
2bt
Our method involves placing a notch in this region, as shown in figure 1, such that the above tensile stress causes
brittle fracture from the notch. To prevent failure occurring near the loading points we used hemispherical cups and
layers of foam to distribute the applied force. We tested notches with different root radii and extrapolated the results
to zero root radius to estimate the effect of a sharp crack: root radii less than about 0.1mm gave results very similar
to the sharp crack estimate.
Fig.1. Schematic illustration of the test rig (on the left) and the biaxial stress state near the notch (on the right)
Using this approach we obtained a value for the fracture toughness Kc of 0.3MPa√m. It is interesting to discuss
this value in the context of the values already measured for related natural materials. The mineral which makes up
the great majority of eggshell is CaCO3 in the calcite form. Geological mineral calcite has a toughness of about 0.2
MPa√m. Many organisms, especially shellfish of various kinds, have shells made from calcite, or the related form
aragonite. Examples are mussels, conch shells and nacre, which is the material found in oysters and often called
“mother of pearl”. These materials have fracture toughness values which are an order of magnitude higher, in the
range 3-5 MPa√m. All of these biological forms, including eggshell, have essentially the same composition, with
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just a few percent of organic material, so how does this large variation in toughness come about? Recent research
has shown that several toughening mechanisms operate as a result of structure at a scale of the order of microns and,
in some cases, even smaller (Currey et al 2001, Barthelat et al 2007). Nacre, for example, has a brick-like structure
in which individual ceramic units are separated by very thin layers of organic polymer. This creates a lot of weak
interfaces which delaminate ahead of the main crack, using up energy, and also cause extensive crack deflection, as
shown in figure 2. Other toughening mechanisms which have been identified include crack deflection at twin
boundaries within calcium carbonate crystals in the conch shell. By contrast, our work showed that these
mechanisms are not active in eggshell. As figure 2 shows, cracks in this material are very straight, showing little
deflection or branching, Examination of fracture surfaces showed large facets made up of multiple individual
cleavage planes on the micron scale, mostly having low angle relationships to each other and therefore not inducing
crack deflection.
This explains why the toughness of eggshell is so low, only slightly higher than that of pure mineral calcite. And
for the chicken, this is a very good thing. The egg needs to be relatively stiff to prevent deformation when the
mother bird is sitting on the egg, but then during hatching the young chick needs to be able to break the shell, which
it does with its beak, making a small hole and enlarging it, causing failure by brittle fracture. So the correct
specification for this material is one which has a high Young’s modulus and a low fracture toughness, and indeed it
turns out that eggshell has one of the highest ratios of E/Kc of any material, natural or manmade.
50m
Fig.2. The photograph on the left shows crack propagation in nacre (Currey et al 2001); the crack path is illustrated schematically in the inset.
The photograph on the right shows crack propagation in eggshell, from our work (Taylor et al 2016).
This kind of work has also been done for another material system, and one which is of more immediate concern
to human beings: the hydroxyapatite/collagen system which is present in various mammalian tissues such as bone,
tooth enamel and dentin, as well as the antlers of deer. Previous work by ourselves and others (e.g. Nalla et al 2004)
has shown that, just as in the calcium carbonate based system described above, one can identify a series of
increasing toughness, from pure crystals of the ceramic phase (Kc = 0.5MPa√m) through enamel, dentin, bone and
finally antler, which display increased toughness values up to about 5 MPa√m. Changes in microstructure are
responsible, as well as increasing amounts of the polymeric phase, which leads to decreased hardness in the same
sequence. In bone, fibrous features at the 100-micron scale (osteons, and in particular their boundaries) have a
strong role in causing crack arrest and deflection. These findings are clearly of considerable medical importance. For
example, changes in the microstructure and mineral content of bone are linked to diseases such as osteoporosis, so-
called “brittle bone disease”, which is highly debilitating.
Another very exciting development arising from studies of this kind is the creation of new materials, through the
concept of biomimetics. There is much interest in making new ceramic/polymer composites based on natural
46 David Taylor / Procedia Structural Integrity 2 (2016) 042–049
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structures such as nacre, using advanced manufacturing techniques such as 3D printing. In the last few years there
has been a real explosion in the quantity and quality of this work, whereby some very significant increases in
toughness have been achieved.
The bones of animals are ceramic/polymer composites; they are essentially brittle materials with low Kc values.
The principal failure modes during normal use are fatigue crack propagation and brittle fracture. So the fracture
mechanics concepts which we use in engineering are very much applicable to improve our understanding of the
function of the skeleton. This applies not only to the skeletal material of humans and other mammals, but also to the
exoskeletons of arthropods such as insects. One very exciting aspect of skeletal material is its capacity for self
repair. There has been a lot of work done by ourselves and others to understand how fatigue microcracks develop in
bone and how they are being continuously repaired by systems of living cells (Taylor et al 2007). This work has
been valuable in areas such as sports medicine, where better predictive models can prevent stress fractures in
athletes, and also in the detection and treatment of osteoporosis and other bone diseases in which bone becomes less
capable of self repair.
By contrast, there has been very little research done on cracking and repair in other organisms, including both
animals and plants. Recently, we published the first biomechanical study of damage repair in the exoskeleton of an
arthropod (Parle et al 2016). We introduced sharp notches into the legs of locusts, with a scalpel. By conducting
cantilever bending tests we measured the fracture toughness of the material (which is called cuticle) to be
4.1MPa√m and showed that it decreased to 2.1MPa√m when the cuticle (which normally contains a significant
amount of water) was allowed to dry out.
We then introduced similar notches into the legs of living insects. We found that after a period of three weeks or
more the Kc value had apparently increased to 7.0MPa√m (see figure 3).
Fig.3. Apparent fracture toughness of insect cuticle after injury (a sharp notch) and repair. “Control” indicates tests results from material removed
from the insect: “Injured (no repair)” refers to insects which did not form an endocuticle patch. The photographs show SEM images of fracture
surfaces. The cut surface of the notch is at the top: highlighted in pink colour is the fracture surface of the endocuticle patch.
Further examination showed that this was not due to any change in the material itself, but rather caused by the
formation of a new layer of cuticle, which had been deposited on the inside of the tube. Figure 3 shows a fracture
surface in which the original cut notch can be seen along with this new material, which is called endocuticle. We
were able to prove by further experiments that the deposition of this endocuticle was triggered by the damage which
we had introduced, and was deposited preferentially in the area near the notch.
We used finite element analysis to study this repair process (see figure 4). By modelling the cut and also the new
endocuticle layer we predicted that this layer should reduce the stress intensity K by a factor of 3.3, which was
somewhat larger than the increase in Kc measured experimentally. The reason for this difference is most likely that
David Taylor / Procedia Structural Integrity 2 (2016) 042–049 47
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failure occurs first in the patch of endocuticle, when it reaches its tensile strength, after which it is no longer able to
protect the damaged area. Figure 4 shows the highly stressed material in the patch.
Figure 4: Finite element model of the leg of a locust containing a sharp notch and repaired with an endocuticle patch. Note the high stresses in the
patch immediately below the cut surface.
This work demonstrates the existence of a sophisticated repair process by which an injury that significantly
reduces structural integrity can be detected and repaired. This process is, we presume, orchestrated by living cells in
the epithelial layer on the inside of the skeleton, but as yet little is known about the biology of this system.
Thin walled tubes under stress can fail in a number of different ways. The problem has been analysed by Wegst
and Ashby (2007) for the case of bending in tubes made from orthotropic material, which is a common situation in
plant stems such as bamboo. We extended this approach to consider mixed bending and axial loading as found in the
exoskeletons of arthropods such as insects and crustaceans, and also in the tubular bones of humans and other
vertebrates (Taylor and Dirks 2012). Figure 5 shows theoretical predictions which suggest that the optimal
radius/thickness ratio r/t for the locust tibia in bending is 7.2. Tubes with larger values of r/t were predicted to fail by
local elastic buckling, whilst tubes with smaller r/t were predicted to fail when the bending stress exceeded the
strength of the material. Actual tibiae, tested when the adult insect was 14 days old, failed by buckling as predicted
(Parle et al 2015). More recent results have shown that as the insect ages, r/t decreases as a result of thickening of
the limb, passing through the optimal value, and the failure mode changes from buckling to fracture at the
compressive strength of the cuticle, in accordance with our predictions. This suggests that the exoskeletons of
48 David Taylor / Procedia Structural Integrity 2 (2016) 042–049
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arthropods have evolved to have the best possible strength to weight ratio, given the constraints of their particular
method of making and growing their skeletons.
Fig.5. Theoretical predictions of optimum r/t ratios for insect cuticle in bending and in compression, with experimental results for the locust
tibia at age 14 days.
5. Concluding remarks
Natural materials and structures, in common with their engineering equivalents, need to maintain structural
integrity when subjected to applied forces. Nature works with a limited range of materials; almost all are composites
in which a soft, polymeric phase is reinforced with a harder, stiffer phase in the form of fibres or other high aspect-
ratio structures such as plates in nacre. These materials have, without exception, low toughness values, and are
constantly under threat of failing by cracking, so fracture mechanics is very relevant if we wish to understand and
learn from these materials. We find that they have developed some excellent strategies for maximizing toughness by
introducing structure at the micro and nano scales. Furthermore, natural materials are often able to compensate for
their poor resistance to damage development by using a continuous process of detection and repair, considerably
increasing their effective strength and durability. At the level of the structural component, Nature comes under
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severe constraints to produce high strength/weight ratios in the face of competing failure modes. We find that, at
least in some cases, evolution has worked in such a way as to provide solutions which are close to the optimum,
given the practical constraints which apply.
In conclusion, the study of natural materials and structures is a fascinating topic, and one in which important
discoveries can be made by applying well know concepts of fracture mechanics and structural integrity.
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