The natural world, of which we are a significant part,
has many examples of survival with minimum use of
energy. These examples range from the production
and use of materials to the organization of entire
populations. But not all organisms exist in a half-lit,
miserly half-life. Their (that is to say, our) driving
purpose in life is to reproduce, and no organism (that
is, me or you) would be here unless our parents had a
strong urge to reproduce, something which we,
mostly, inherit. So any way that we can have the
largest number of surviving offspring will be favored.
In doing this we are in competition with nearly all the
other organisms in the vicinity. The ones with which
we are overtly friendly are our immediate genetic (or
to a lesser extent, social) relatives, and much has
been made of the concept that it is our genes, rather
than ourselves, that crave dominance.
The science of ecology recognizes two basic types of
community, whose differentiation depends on how readily
available the resources are. With abundant resources,
commonly found in developing communities invading new
habitats, the resources will be used wastefully in the race for
reproduction and life will be short, but (presumably) sweet
(r-selection). As the community develops towards maturity
and resources become scarce, nutrients are recycled, the
reproduction rate falls, and organisms tend to be larger and
more long-lived (K-selection1).
Man, by using technology, has managed to tap resources
that are unavailable to most organisms and so has followed
by Julian F. V. Vincent
Survivalof the cheapest
Department of Mechanical Engineering,University of Bath,Bath BA2 7AY, UKEmail: [email protected]
ISSN:1369 7021 © Elsevier Science Ltd 2002December 200228
Most of our resources, especially materials, are
treated by economics as if the supply were infinite,
when demonstrably it is not for those that are non-
renewable. In his engineering, use of materials and
energy, man lets design takes second place, whereas
nature treats materials as expensive and designs with
apparent care and attention to detail. This results in
durable materials and cheap structures that are easy
to recycle under ambient conditions. Examples
illustrating this principle, which are given here, are
drawn from both animals and plants with comments
on the underlying mechanisms such as self-assembly
of liquid crystal systems, use of composite structures,
and control of fracture properties.
REVIEW FEATURE
the pattern of invasion and colonization. This is inherently
wasteful, but is the quickest way to dominance. But a time
will come when resources become limiting, both because of
their depletion and the overabundance of organisms
competing for them, as Malthus pointed out. Most industrial
communities represent r-selection, but it is necessary for our
survival to move to K-selection. The easiest way to drive this
would be to make resources artificially more scarce before
they disappear, which of course flies in the face of all we
‘know’ about how the economy works. ‘Cheap’ resources are
‘better’.
Jim Gordon, an engineer of much insight, highlighted a
number of examples of the saving graces of proper pricing2.
He took his cue from economists who say that there is
always an optimum price for land and labor, which results in
efficient social development. If materials are cheap, there will
be little incentive to use them carefully and economically,
resulting in bad, heavy, ugly, and thoughtless design. Even so,
since the cost of a finished product depends on costs of
processing, as well as the cost of the raw material, it may
well turn out cheaper to pay more for a more malleable
starting material. This is partly why plastics and composite
materials are gaining acceptance. Since money and energy
can be directly equated, it makes sense to see how natural
systems apportion their energy between various functions
and how they design materials, mechanisms, and structures.
EnergyA good working hypothesis is that organisms exist on the
minimum amount of energy, which commonly they gain as
‘food’ or sunlight. They have evolved such that the available
energy is optimally partitioned between the various life
functions in some proportion representing their relative
importance for the survival and reproduction of the organism
in the particular context (physical and biotic) within which it
finds itself.
For any particular function studied, therefore, it is
important to know the context within which it is functioning.
For any particular function there will also be an organism or
group of organisms that will best repay study since they
perform the particular function best. It is important to realize
that ‘optimization’ does not imply the function of any one
organ or material is the best possible; it means that the
energy available has been used in the best possible way
between the functions necessary for the survival of the
organism. This is an assumption, but it seems to work fairly
well. Thus, the function of the organ or material will be good
enough for survival, including a suitable safety margin. The
minimum energy criterion means that chemical reactions will
occur at ambient or only slightly elevated temperatures. The
existence of the H-bond (necessary for easily reversible
interactions such as when enzymes – organic catalysts –
control chemical processes) and conformational control limits
most proteins to temperatures of no more than about 45°C.
This may slow down some chemical reactions and make
others impossible. Speed is not necessarily important to an
organism; if it can live long enough it might be better to
reproduce tomorrow than today.
Since the production of all polymers and structures is
controlled by the genetic system at the molecular level,
materials of very high quality can be produced, with almost
no flaws in them. Molecular control also allows interactions
of relatively high energy to occur, which would necessitate
high temperatures in our technology. Those high
temperatures, of course, introduce their own problems of
thermal motion that will reduce the perfection of the
product, especially if the product is non-crystalline.
The starting materials that organisms use are readily
available in their environment or are chosen for compatibility
with the existing chemistry. Ceramics are made mostly from
CaCO3, SiO2, and occasionally of oxides of Fe or other
transition elements. Nearly all non-ceramics are made from
protein or polysaccharide, which can be fibrous (silk, collagen,
cellulose, chitin, or elastin) or space-filling (matrix of insect
shells, cartilage at joints). Water is very important as a
medium for interaction and as a plasticizer. Partitioning and
separation of components is achieved with lipids, mostly as
bilayer membranes. Hydrophobicity is used to achieve
orientations (e.g. liquid crystal structures). Liquid crystallinity
is an example of the mechanisms available for processing and
post-processing of materials.
For instance, silk is partially aligned before being spun by
forming liquid crystal structures. Thus, the energy required
for spinning the silk is reduced, since part of the molecular
orientation associated with spinning has been produced
already. This is also an example of nanofabrication and
emphasizes the general principle that because biological
materials are made ‘from the molecule up’ they are
necessarily designed from this level and have to be assembled
into a number of hierarchies (Fig. 1). This in itself is probably
December 2002 29
an advantage, partly because hierarchical structures tend to
be more efficient3, and partly because it is then possible to
produce a greater variety of properties by varying the degree
of interaction at the interfaces between the various levels of
the hierarchy. However, although a hierarchical structure is
adaptable, it necessarily introduces more scope for
uncontrolled variability. So although the underlying genetic
system is extremely conservative, yielding very uniform
materials at the molecular level, biological materials in bulk
can be rather variable in their properties.
If we can ask the correct and appropriate questions of
nature – if we can divine what natural structures and
materials are doing – then perhaps we can learn from them.
An example of how we can be misled by preconceptions, and
how a new understanding can suggest new concepts, is given
by a comparison of hedgehogs and porcupines.
Hedgehog spine and porcupine quillHedgehogs and porcupines are covered in modified hairs that
are enlarged, stiffened, and strengthened to form spikes of
different sizes and shapes. They have in common their basic
structure (a tube), their material (keratin, a fibrous protein),
and their sharply-pointed outer ends. They differ in that
porcupine quills are very obviously of different lengths over
different parts of the body, can be pulled out relatively easily,
and tend to be rather long for their diameter, whereas
hedgehog spines are well embedded into the skin (you can
pick up a hedgehog by a single spine), the same length all
over the body, and slightly curved4.
In functional terms, it appears that the porcupine quill is
primarily for defense whereas the hedgehog spine is a shock-
absorber. The hedgehog bounces when it falls, as it must do
quite often since it climbs walls and trees with amazing
abandon. The foam-like structure down the center of spines
and quills supports the thin outer walls against local buckling,
allowing the structure to bend further without failing. Other
REVIEW FEATURE
December 200230
Global bending stiffness
Resistance to Brazier ovalisation
Resistance to local buckling
Improve resistance to local buckling
Remove central unstressed material
Fig. 2 Characteristics of ‘foam’ filling of hedgehog spines – a tentative evolution6. Eachpair of cross-sections of the spine represents the next stage in optimization of thestructure.
Fig. 1 Hierarchies: hair is made up of six hierarchies of structure with a factor of about 10 size difference between each level32. Diagram shows the diameters of a typical 'fiber' at each level.
REVIEW FEATURE
animals have similar spines or quills that show several
different internal structures to the basic tubes (Fig. 2):
• An isotropic three-dimensional core (porcupines such as
Coendou and Erithizon);
• The same, but with added solid ribs running longitudinally
down the tube (the porcupine Hystrix);
• Orthogonal longitudinal and circumferential stiffeners in a
‘square honeycomb’ (the European hedgehog Erinaceus
and spiny rat Hemiechinus);
• Thin septa very closely spaced (as in the tenrec Setifer).
These four structures were analyzed as cylindrical shells
with a compliant (soft) core. The theory of cellular materials5
shows that the ratio of the stiffness of the cellular structure
to that of the material from which it is constructed (Ec/E) is
the ratio of the densities (ρc/ρ) raised to a power dependent
upon the geometry of the cellular structure.
In the spines of hedgehogs and porcupines, this ratio6 is
between 0.05 and 0.1. Porcupine quills perform more or less
the same as hollow cylinders in buckling as struts with an
axial load; in bending they are 40% or so better. But the
spines of the hedgehog, with their square honeycomb core
and longitudinal stiffening, are three times better than they
would be without the core. For a given bending stiffness, the
mass of the tube can be reduced by increasing the relative
radius. This basically gives the tube a greater second moment
of area, I, and therefore a greater flexural rigidity, EI. But it
then runs into the problem of the tube going flat at the point
of highest force (Brazier ovalization, as shown in Fig. 3) and
of local buckling.
The foam core alone can resist the ovalization, but local
buckling demands radially oriented material for its resistance.
This reinforcement is thus best provided as longitudinal,
circumferential, or orthogonal stiffeners. If these stiffeners
are sufficiently massive they can also do the job of the foam
core, which can be removed with no reduction in mechanical
performance. Additionally, material in the central part of the
core will have a low second moment of area and provide
much less support in proportion to its mass. It can, therefore,
safely be omitted from the structure.
The recent development of a process which allows the
production of cylindrical metal shells with an integral foam-
like or honeycomb-like core means that the excellence of this
design, previously confined to nature, can be extended to
lightweight tubular struts such as are found in the suspension
of racing cars.
Advantages of biological materialssynthesisMuch has been written about the advantages of the ways
organisms synthesize materials, in particular the low
(ambient) temperatures at which materials with excellent
mechanical properties can be made, whereas man needs
much higher temperatures. I think the message is slowly
trickling through that you can do most things at low
temperature if you are prepared to wait long enough!
The fastest bone can grow is about 1 µm a day7 and egg
shells are doing pretty well to put on 5 g in 24 hours8. There
are probably two main considerations – the energy required
to join the components of the material together (bond
energy) and that required to define the shape of the
structure. The bond energy is dictated by the chemistry and
would appear not to be open to manipulation. But for a given
set of material properties, biological materials can be made
of less ‘good’ components because they are assembled
(structured) so well that they perform to the best theoretical
predictions. For instance, the shell and spines of the sea
urchin, made of brittle CaCO3, are full of holes yet very
strong. This may be because any small flaws on the surface,
which could start a crack9, can be dissolved away by the cells
that make the skeleton. It may also be that the lower density
December 2002 31
Tensileforce
Local
buckling
Fig. 3 Brazier ovalization of a hedgehog spine that has been end-loaded as a strut showingthe general change in shape4.
outer surface provides a sacrificial layer, protecting the more
robust layers beneath from direct damage.
RecyclingAnimals and plants are continually repairing and recycling
their constituent materials. There is some evidence from
work by Robert Ker on the creep rupture of wallaby tail
tendon10 that the collagen is not capable of sustaining
maximum loads for any length of time and is continually
being renewed. This raises an interesting point: is it
energetically cheaper to make enough material that will be
able to support 99% of loads put on it, with the attendant
problems of producing the material and carrying it around,
risking that it contains unrepaired damage (a dangerous
strategy, since such damage can initiate failure)? Or is it
better to repair the material as a matter of course, putting up
with the continual expenditure of energy, but having less
material to carry and being certain that what is there is up to
specification? The tendency is for man to choose the former,
except in lightweight structures such as aircraft, which
require continual maintenance. The implication is, yet again,
that while in nature material is expensive, technologically
speaking, material is cheap.
Materials have to be designed so that they can not only be
repaired, but also recycled within the organism. The outer
covering or cuticle (which is also the skeleton) of an insect or
crab has to be renewed as a larger structure as the animal
grows. It is largely dissolved before it is shed, partly to aid its
removal (it is thinner and more flexible) and partly so that
the new cuticle can grow more quickly and cheaply using
resources from the previous cuticle. But the stiffness of the
cuticle is a function of the number of bonds within it and
their energy. More covalent bonds will make the cuticle
stiffer, so that the animal needs less material to provide the
same amount of support, but the cuticle will then require
more energy to dissolve it at the molt, or may even be totally
insoluble. The optimization problem then is: how much to
stiffen, how much to resorb? The balance involves not
putting in bonds that are more stable than are required for
the function. This may be important in the evolution of types
of cuticle. In the higher insects, the proteins tend to be more
polar so that it is (presumably) more difficult to expel the
water of plasticization during sclerotization (the process of
cuticular hardening). But this may make cuticle more easily
dissolvable at the molt, since water will be able to penetrate
the matrix more easily and enzymatic degradation can be
more complete. It may also mean that the proteins are more
able to form extended regular structures before the water is
removed, so that the resulting structure is more fibrous with
more intermolecular interactions.
This general argument probably applies to all structural
biological materials. It may be more efficient, especially if
weight is an important consideration, to keep all materials
under metabolic control and allow as small an amount as
possible to be ‘dead’. With plants such as trees, which do not
move and for which bulk can be an important stabilizing
influence, it may be advantageous for material (wood) to be
outside the metabolic pool, since it can provide mass at no
extra cost. As far as I know this concept has not been
addressed.
Ashby diagramsBiological materials, like any used in technological
applications, have to perform to a minimum specification.
True, they are adaptable and can change their properties to
some extent, but the minimum energy approach demands
that the minimum amount of material should be used for a
particular function. Certainly, the materials found in living
organisms tend to be very ‘efficient’ (e.g. measured as
stiffness per unit weight, or specific stiffness). For animals
this is even more important, since all their materials have to
be transported, which demands metabolic energy.
It is not only possible to measure these properties and
compare them with artificial materials, but also to decide
what ratio of properties will best perform the functions
required. Thus a tie (a member taking pure tension, such as a
tendon) performs best per unit weight when the ratio of
stiffness to density (E/ρ or specific stiffness) is at its highest.
But for a beam or column (such as the branch or trunk of a
tree), the greatest efficiency is achieved when E½/ρ is
maximized. This information has been around for some time2
and has been very effectively presented by Ashby11, who
plots stiffness or strength versus density, specific stiffness
versus specific strength, etc. (Fig. 4). These diagrams can also
be used to show what design properties biological materials
may be maximizing. For instance, wood parallel to the grain
seems to be designed to resist tension best, but across the
grain seems to be better at being a column or beam.
Obviously, these characteristics have to be some sort of
compromise or optimization. When biological materials are
REVIEW FEATURE
December 200232
REVIEW FEATURE
thus analyzed, they are found to be very high performance
and some, such as wood, cannot be bettered by anything that
we currently make. This has made biological materials of
great importance in a wide variety of technologies12.
Nacre as a tough materialBill Clegg developed a platey ceramic based on nacre (Fig. 5).
Nacre has a tenuous protein matrix between the platelets of
aragonite. Clegg’s idea was to use the platelets, but with
different matrix materials in the sandwich.
By adapting the technology used to make multilayer
capacitors for electrical circuits, he made the production
cheap and simple. Ceramic powder is mixed with a polymer
and formed into sheets about a fifth of a millimeter thick.
This is formed into sheets like pastry, coated to give the right
interfacial properties, pressed together to give the desired
shape, and cooked at 1000°C without pressure. When the
ceramic is SiC and the sheets are coated with graphite (which
stops them sticking together), the material has a work of
fracture (measured in three-point-bending) of the order of
6 kJ/m2, two to three times greater than nacre. However, this
material still has problems, being weak in tension and tough
in only one direction when a crack is made to progress across
the layers. The graphite does no more than separate the
plates, so the material is also weak in shear or fatigue tests.
Nevertheless, the material was used to make a prototype
combustor liner for a gas turbine. The current metal version
has fine holes through which cooling air is blown, but this air
can combine with unburned fuel to give local hot spots. A
combustor made from a single thick layer of SiC broke the
December 2002 33
Drycoconuttimber
Wood (II)
Plywood
Elastin
ResilinParenchyma
Muscle
Cartilage
Skin
Leather
Viscidsilk
Cork
Cocoonsilk
Molluscshell
Coral(T)
Coral(C)
KeratinDentine
Compactbone
Wood ( )
Cancellousbone
WoolCuticle
Collagen
Rattan Antler
Calcite
Aragonite
Dragline silk
Cotton
Wood cell wall
Bamboo
FlaxHemp
Engineeringceramics
Chitin &cellulose
Greencoconuttimber
Engineeringalloys
Enamel
Hydroxyapatite
100
10
1
0.1
0.01
0.0010.10.1 10 100 1000 10 000
1000
Specific strength [(MPa)/(Mg/m3)]
Spe
cific
mod
ulus
[(G
Pa)
/(M
g/m
3 )]
T
Fig. 4 Comparison of specific stiffness versus specific strength of biological materials and‘engineering’ materials. The latter have a better performance only at the higher end of thedistribution12.
Fig. 5 Types of structure found in mollusc shell34. Lines and numbers give scales inmicrons.
first time it was used, but the toughness of the laminated
version showed a dramatic improvement in resistance to
thermal shock. The graphite is still a problem, though, since it
tends to burn away at the high temperatures. It is important
to allow the plates to move against each other as the
platelets heat and cool, so the interlaminar layer has to be
significantly softer than the platelets. Therefore, the graphite
was replaced with a layer of the same material as the
platelets, but with holes in it. The holes are made by mixing
starch granules in with the ceramic paste, which burn away
when the material is heated. Starch comes in a variety of
shapes and sizes, depending on its origin, is cheap, and
disperses readily in water. The separated plates can store a
charge between them in the same way as a capacitor in an
electrical circuit. The ability to store charge depends, among
other things, on the distance between the plates and the
state and nature of the material between them. If these
change, as might happen when the material is deformed, then
the capacitance will change, which can be measured and used
to monitor loads and damage in service in a non-invasive
manner.
Nacre is not the only tough ceramic found in mollusc shell
– it just happens to be the one that has been studied most.
Liquid crystalsThe similarities between liquid crystals and insect cuticle
(Fig. 6) were first noticed by Charles Neville and Conmar
Robinson (a polypeptide chemist) and reported at a meeting
at the Shell Building in London in 196713. The optical
properties were very similar; in insect cuticle the parallel and
helicoidal fibrous structures rotate the plane of polarized
light in the same way as nematic and cholesteric liquid
crystals.
The difficulty in this comparison is that the conformation
of liquid crystals is controlled from the molecular level,
whereas the orientations in insect cuticle are at the sub-
micron level – a difference of at least two orders of
magnitude. But the attractiveness of liquid crystals is that
they self-assemble from a disordered state, and so represent
a way in which order, and therefore morphology, can be
generated in a purely chemical system. Since living tissues
are made of chemicals, and ‘life’ is achieved as a result of the
ordering of these chemicals, there is much interest in any
mechanism for achieving that order. Liquid crystals can also
generate a variety of types of order from relatively simple
molecules and can transform from one type of order to
another in response to changes in external conditions
(e.g. changes in salt concentration). There are times when
this ease of transformation is an advantage, such as in the
development of the dogfish egg-case14 and the production of
silk15. But there are, equally, other times when the resulting
structure has to be stable so that it can carry or generate
forces. Under those circumstances, the order has to be locked
into the structure by processes that lead to cross-linking of
the components16.
Liquid crystals also conform to one of the criteria of
biological systems – that what they do is achieved with the
minimum expenditure of energy. For instance, the energy
required to convert a nematic liquid crystal into helicoidal
conformation with a pitch of 1 µm is 10-5 times the amount
of energy needed to induce nematic order in an initially
random system. The generation of the nematic system can be
rendered even more energy-efficient by orienting the
molecules against a flat surface. Self-assembly systems for
the generation of biological materials are more energy
efficient than those that do not self-assemble (note the
production of order is not solely dependent on self-assembly
or ATP; it can be supplied externally in directed assembly, e.g.
by the application of strain or extensional flow) and therefore
need enzymatic control and the hydrolysis of energy-rich
phosphate bonds in ATP.
REVIEW FEATURE
December 200234
Fig. 6 Some liquid crystalline structures found in nature illustrating the transformationsavailable to them13. Most are found in insects, plant cell walls, etc.: (a) cylindricalhelicoidal; (b) planar random; (c) 45° helicoid; (d) twisted orthogonal; (e) monodomainhelicoidal; (f) orthogonal; (g) polydomain helicoid; (h) parallel; (i) pseudo-orthogonal.
REVIEW FEATURE
On the face of it, liquid crystalline structures should be
ubiquitous. They offer advantages at the morphological and
energetic levels. The problem remains that the mechanisms
by which the structures are generated in biological systems
are not clear. It may be that we have to think of liquid
crystalline structures as low-energy in terms of structural
maintenance rather than generation, so that the cell drives a
structure towards a liquid crystalline morphology but
stability comes from the intrinsic properties of that
morphology.
Insect cuticleInsect cuticle is an archetypal fibrous composite. The fibrous
component is chitin, a polysaccharide closely related to
cellulose, which is embedded in a matrix of protein. The
chitin is present as nanofibers about 3 nm in diameter and up
to 1000 nm long.
The various mechanical properties of cuticle arise from a
combination of the properties of the matrix (whose hydration
can be controlled to give a wide variation in stiffness) and
the orientation and amount of chitin present. The chitin is
laid down in layers in which all the nanofibers are oriented in
the same direction. In some cuticles this orientation is held
constant for many layers, in others it changes rapidly, giving
a variety of structures (Fig. 6). These layers are also known as
lamellae.
The morphology of lamellae has been described in general
terms many times, but rarely quantified. The larva of a
skipper butterfly, Calpodes ethlius, has been closely studied
over the years by Michael Locke of the University of Western
Ontario, and its development timed almost to the minute. It
is possible to measure the rate of reorientation of the liquid
crystal morphology from layer to layer. During the first
66 hours of the last larval stage of this butterfly, the lamellae
in the cuticle are 500 nm deep and take 3 hours for each
180° rotation in the direction of orientation of the protein-
chitin fibrils (Fig. 7). Later on in the development process, the
lamellae are 100 nm deep and deposited in only 10 minutes.
Since the diameter of the chitin nanofiber is 3 nm and its
volume fraction about 0.5, the two categories of lamella
could have up to 85 laminae changing in orientation by about
2°, and 16 laminae with an 11° shift. Since the rate of
deposition is close to one lamina every 4 minutes and one
every 40 seconds respectively, that represents a rotational
change17 in orientation from 0.5° to 18° per minute.
Ultimately nobody yet knows what controls the liquid
crystal-like structures in insect cuticle, but it seems certain
that it has to be the protein component, since the chitin
nanofibers are totally obscured by the protein layer, although
the protein binds to the chitin in a very regular manner and
so may be producing a composite liquid crystalline
structure18,19.
Plant cell wallsCellulose is a polysaccharide that, because of the β-1,4 links
between the sugar units, produces a strongly linear ribbon
structure, which is very stiff and forms stable fibers. The
theoretical modulus of the cellulose molecule is 250 GPa, but
the best experimental estimate for the stiffness of cellulose
(and, for that matter, other linear polysaccharides in the cell
walls) is about 130 GPa. The specific gravity of cellulose is
about 1.5, so it is possible to compare its mechanical
(strength and stiffness) performance with other engineering
materials (Fig. 4). One concludes that cellulose is a high-
performance material, comparable to the best fibers
technology can produce.
Cellulose is produced from rosette-shaped enzymes that
float around in the fluid cell membrane. The primary
microfibril is about 5 nm in diameter, but 100 or so of these
combine to form larger microfibrils (Fig. 8). The cellulose is
December 2002 35
Fig. 7 Calpodes ethlius larva – rate of change of orientation of chitin in the developingcuticle17.
REVIEW FEATURE
December 200236
assembled into a shell around the cell, thus forming the
skeleton both of the cell and the plant. The orientation of the
cellulose microfibrils in this cell wall is influenced by several
factors. Structures reminiscent of liquid crystals have been
found in the cell walls of a wide variety of plants13. The
orientation of the cellulose microfibrils can be parallel or
helicoidal, corresponding to nematic and cholesteric liquid
crystals (Fig. 6). The liquid crystalline structures are
assembled most probably in the periplasm, a narrow region
confined between the most recently deposited cell wall layers
(outer side) and the cell plasma membrane (inner side). This
is such a thin layer that its existence is disputed, though it
has been observed in the epidermis of quince seeds20. Within
this assembly layer, the molecules are oriented into liquid
crystalline forms. The intrinsic stiffness of the cellulose
molecule aids its self-assembly, as do the bulky side chains
often found on hemicelluloses. However, cellulose itself
cannot control this process since it does not form liquid
crystals, except in unphysiological conditions or when mixed
with hemicelluloses. These, therefore, are the most likely
candidates for controlling the system and can contribute up
to 40% of the cell wall. The asymmetry required for liquid
crystal self-assembly is provided by the C-5 of the
hemicellulose sugar ring. A credible model is then that the
cellulose microfibrils are surrounded by a sheath (however
thick that needs to be) of hemicellulose, which can then
direct the self-assembly process13.
There is another influence in the orientation of cellulose
in the cell wall: the orientation of microtubules arranged on
the inner face of the cell cortex (Fig. 9). The orientation of
the cortical microtubules can be changed by external stimuli
such as light (amount, color), auxin, and mechanical strains
such as those caused by bending21. These stimuli are
additive, so a small amount of auxin makes the cells more
sensitive to other stimuli. At the same time the growth rate
5 nm nanofibrils
Enzyme rosette
Raft of rosettes
Cellulosefibrils
Lipidbilayer
Lipidbilayer
Plasmamembrane(exterior)
Fig. 8 Production of cellulose according to Preston’s original model35.
Cellulosemicrofibril
Enzymerosette
Microtubule
Fig. 9 Orientation of microtubules controlling the orientation of cellulose in the cell wall.The microtubules act like tracks to guide the cellulose enzymes floating in the cellmembrane13.
REVIEW FEATURE
changes, so it is the reorientation of cellulose microfibrils,
mediated by changes in the cortical microtubules, that
governs growth, both qualitatively and quantitatively. Blue
light causes the microtubules to orient longitudinally, red
light makes them orient transversely allowing the plant to
elongate22. How is the orientation of the microtubules
controlled at the cellular level? Somehow, these two
mechanisms must coexist.
Clues are provided by the work of Overall on wound
healing in pea roots23. The wound was created by removing a
wedge of tissue across the axis of the root of three to four
day old seedlings 3 mm from the tip. Sections were stained
with fluorescent markers for the microtubules and examined
in the confocal microscope. Cells from an intact root are long
and thin, extending parallel to the main axis of the root
because the cellulose fibers of the cell wall are oriented
circumferentially. However, in cells taken from the vicinity of
the wound about 24 hours after wounding, the microtubules
have rotated their orientation so that they are parallel to the
wound surface, which is more or less orthogonal to the long
axis of the root (Fig. 10). This is accompanied by elongation
of the cells towards the wound, suggesting that the cellulose
is being laid down in the new direction. The final step in the
initiation and maintenance of this new cell polarity around a
wound is the establishment of new planes of cell division,
which are again parallel to the contours of the wound. All
these responses ensure that the plant tissue grows in towards
the wound area and fills it with new cellular material.
The one thing Overall does not mention is how the
reorientation of the cellulose fibers is achieved. The
implication is that it is simply due to changed orientation of
the microtubules causing the newly laid down cellulose to
have a different orientation. But this would be insufficient to
account for the shape changes. The necessary change in the
anisotropy of stiffening could occur only if the cellulose
through the entire thickness of the cell wall changed its
orientation, and this would be possible only if the cell wall is
adaptively labile – or in a liquid crystalline state. The same
has been postulated for the lability of orientations in insect
cuticle but never, as far as I know, shown experimentally. This
might be easier in a cellular system, where the external state
of strain can be changed more easily. The mechanism of
change has been speculated upon (‘acid loosening’, etc.) but,
as far as I know, never quantified. By analogy with other
water-miscible composites such as paper and insect cuticle,
the change in water content (driven, perhaps, by changes in
pH) need be only a few percent. The more directed the
structural bonds in the system, the fewer the bonds that
need to be solvated, since these can be identified by the
biochemistry of the system. Once again a liquid crystal
system has distinct advantages.
The stiffness of the cell wall varies according to the
amount and orientation of the various components, including
water. Cowdrey and Preston24 used two models to describe
the mechanical properties of lignified cell wall. Their first – a
composite model of cellulose fibers in a lignin matrix –
December 2002 37
Fig. 10 Repair of a cut in a pea root: the cells at the end of the cut have reorientated their cellulose and are expanding into the cut area23.
proved to fit their measured data best. However, their second
model, in which the cellulose microfibrils spiral helically
around the cell, has proved more useful in predicting the
properties of unlignified cells, even though this model has a
significant flaw: the matrix that binds cellulose microfibrils
together is ignored. It is possible to take a middle route,
allowing for limited connectivity between the components,
expressed in a variable shear modulus. In addition, molecular
chemistry very often imposes much more regular and precise
structures than engineering theory demands. There is a
much more hierarchical progression of molecular types,
rather than just crystalline fibers and rubbery matrix. The
progression is from crystalline microfibrils to linear
polysaccharides with side chains, which are well oriented but
not crystalline, down to random polymer networks like
lignin25.
In a new molecular model for the cell wall26, developed
using the partially lignified cell wall of the ‘woody’ tissue of
tobacco, Nicotiana tabacum, the cellulose microfibrils are
continuous along the length of the cell and arranged at an
angle of about 10° to the long axis (Fig. 11). The matrix
molecules are organized at two levels. The hemicelluloses and
pectins are oriented orthogonal to the longitudinal axis of the
cell with little or no interconnectivity; the lignins are
randomly oriented and fill in some of the gaps in the
structure, depending on how much lignin is present (Fig. 12).
When the cell wall is stretched, the helix will open out and
the wall surface area will be reduced. This reduction will
result in the microfibrils being forced closer together, because
the surface area of the cell is reduced. Thus, the matrix
material between the microfibrils will be compressed. The
reduction in wall area will lead to an increase in wall
thickness as the lignin is squashed out radially. If the
hemicelluloses and pectins are not oriented at 90° to the
long axis of the cell, they will experience some direct tensile
loading transmitted from the microfibrils, and the angle of
the microfibril helix will not change as much. The tensile
modulus is now dependent on the mechanical properties of
the matrix chains in tension and compression, as well as the
compressive properties of the lignin. There is no direct tensile
stress transfer through the matrix from one microfibril to
another as in a normal composite. Even with a large helical
angle to the vertical, the microfibrils could still display their
full tensile modulus if the gaps in the matrix were filled with
a stiff incompressible material. The hemicelluloses and
REVIEW FEATURE
December 200238
Hemicellulose
Cellulosemicrofibril
Stretch
Lignin
Waterfilled
space
Fig. 12 The presence of small amounts lignin restricts the freedom of the cellulose in thestretched cell, but does not glue the microfibrils together26.
Microfibrilsjoined byhemicelluloseswith lignin inthe spaces
Hemicellulosejoining twomicrofibrils
As it is stretched, the cell volume reducesand the cellulose microfibrils pack closer
Fig. 11 Cellulose microfibrils in cell wall – a simplified view of the orientation26.
REVIEW FEATURE
pectins compartmentalize the lignin and store elastic strain
energy produced by the compression of lignin. This model
accounts very well for experimental mechanical data from
cells that are only partly lignified.
The key to this model is specific internal matrix
connectivity and molecular orientation. Where the
hemicellulose and pectin chains are oriented at a large angle
to the long axis, the covalent connectivity of the lignin
becomes crucial in determining the properties26. If lignin
were strongly covalently linked to the matrix polysaccharides,
as well as to other lignin chains, then the matrix would
become connected along the length of the cell and the
mechanical behavior would be described by ordinary
composite theory27.
The idea that plant cell walls are basically liquid crystalline
is not new – the first pertinent observations were made over
20 years ago. But ideas of how the cell organizes the world
on the outer side of its membrane are still rather vague.
Although much is known about the chemistry, very little is
known about the control of morphology. Yet the morphology
of the cell wall – the orientations of fibers and their
interactions with other components – is crucial to the
mechanical properties of the plant. Molecular biology has
shown how intracellular shapes are derived from self-
assembly driven by chemistry – the same must be true
outside the cell.
Responsive materialsThe morphology of liquid crystals can be modified by changes
in concentration, temperature, pH, and salinity. Since the
regular packing of a liquid crystal represents a higher density
and lower energy state, higher pressure and lower
temperature will favor a more liquid crystalline structure. The
protein of the mantis egg-case is arranged as a helicoidal
liquid crystal above pH 5 and isotropic below. Collagen is a
liquid crystal28, as is amply shown in the dogfish egg-case,
and changes its form of packing and hydration with changes
in concentration and type of external salt. So there are many
ways of affecting the packing patterns, which in turn can be
used to indicate the surrounding conditions when the
morphology was formed. These changes can, therefore, be
used to transduce information about the surroundings, and
become the initial stage in a sensor. The interrogation of the
sensor is easily made with polarized light, which is non-
contact and can be remote.
Liquid crystals are susceptible to flow elongation effects,
accounting for much of the structure of natural extrusions
such as arthropod silks and dogfish egg-cases15,29. Such
molecular orientation also gives very high stiffness and great
perfection of structure, leading to high strength.
Dogfish egg-caseThere is a beautiful example of a large complex collagenous
structure produced and molded extracellularly – the egg-case
(‘mermaid's purse’) of the dogfish (and related fish, the
selachians). It is a complex, hierarchical, fibrous composite
whose morphology and properties have been unraveled by
David Knight and his associates30.
The function of the egg-case is to protect the developing
dogfish from the mechanical and microbiological stresses of
life in the sea until it is ready to hatch. To do this, it has to
be strong and tough yet sufficiently permeable to allow
diffusion of oxygen and waste nitrogenous products. This
remarkable capsule allows selachians to lay very few, large
eggs with a development time of at least five months and a
very high probability that the developing animal is well
enough protected to survive and emerge from the egg-case
larger and better able to fend for itself.
The capsule (Fig. 13) would be immediately recognized by
the builder of an F1 racing car or a fighter aircraft, since they
use materials that look very similar. It is made of a series of
sheets of uniaxially oriented fibers laid one over the other
with a precisely controlled change in fiber orientation from
one sheet to the next. Relative to the longitudinal axis of the
egg-case, the fibers are laid parallel, perpendicular, or at 45°.
The fibers are made of collagen, the fibrous part of which
accounts for rather less than half the dry weight. Other
protein fractions probably represent globular regions of
collagen molecules or serve to bond the collagen molecules
together, and non-collagenous layers act as varnishes or
glues. The orientations are achieved by a combination of
December 2002 39
Fig. 13 Dogfish egg case – a general view. The oval shows where the egg is placed withinthe capsule.
directed extrusion through a complex spinneret system
(Fig. 14) and the liquid crystallinity of the collagen.
Phase changeThere is another aspect of liquid crystals – they can change
from one form to another (e.g. nematic to cholesteric),
equivalent to a phase change.
The organic matrix of nacre, comprising just a few percent
of the composite by weight, is normally present as an
apparently amorphous glue, but can be spun into strands
(Fig. 15) that bridge the gaps between the separating plates
when the material is broken31. The matrix protein has a silk-
like complement of amino acids, so the implication is that
these fibers are stiff and strong like silk and are capable of
carrying a significant load32. Simple experiments in which the
nacre was dried, thus stopping the matrix protein from being
spun into fibers, showed that at least half the toughness was
due to this process31. Therefore, nacre’s fracture resistance
resides in the polymer adhesive. The properties of this
adhesive have been revealed with the atomic force
microscope, stretching the matrix proteins exposed on the
surface of freshly cleaved nacre. The adhesive fibers elongate
in a stepwise manner, suggesting that folded domains or
loops are pulled open, requiring forces of a few hundred
picoNewtons. Over a nanoNewton is required to break the
polymer backbone in the threads33, suggesting a strength of
no more than 0.1 MPa, which is actually not very impressive.
This ‘modular’ elongation mechanism might be general for
toughening natural fibers and adhesives, and so might also be
found in spider dragline silk.
Summary and conclusionsThis review is really all about biomimetics, viewed with an
energetics slant. It is therefore relevant that at a recent
REVIEW FEATURE
December 200240
Fig. 15 Craze-like fibers spun from the matrix protein in nacre as it breaks31.
Egg capsule wall
Secretion of outer layer
Direction of production
Spinneretelements
Fig. 14 Section of the wall of the egg case spinneret coextruding the outer layers of theegg case; the inner layers are produced in a similar manner further upstream18.
REVIEW FEATURE
meeting in Japan on biomimetics, a set of three headings was
provided for a panel discussion in which some important
topics were identified.
Under Science there were the following:
• Biology for general inspiration for other sciences;
• Low-energy systems;
• Novel analysis required by new ideas;
• Fusion of scientific concepts.
Under Industry came:
• Multifunctional materials;
• Novel processing routes;
• Low energy usage;
• Adaptability due to multifunctionality;
• ‘Green’ solutions.
And under Society:
• Easy understanding of the basic concepts;
• Better materials and structures available;
• Greater convenience resulting from better quality;
• Easier recycling;
• Low energy usage.
Remarkably, low usage of energy appears under all three
headings. The concept is that on the coat-tails of novelty and
fresh thinking there is the possibility of energy saving at all
levels – development, manufacture, and use. Although the
reasons for grouping and choice of ideas under these three
headings were not demanded, the fact that a group
consisting of physicists, chemists, engineers, and biologists
reached this conclusion is significant. On the other hand it
may simply be that energy conservation is such a big issue
these days that no aspect of science, industry, or society can
be allowed to ignore it. Unfortunately, our supply of
materials is still considered to be inexhaustible. This can only
be so if we recycle them properly (which we don’t, though
nature does) and if we use readily available materials (which
we mostly do, but could do better).
Even so, energy and materials are currently far too cheap
for our effective survival. Proper pricing will allow us to
adjust to reducing resources before the world has reached the
stage of K-selection. For that, we cannot afford to ignore that
biomimetics represents a set of solutions to our energy
problems. MT
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