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: j.f.v.vincent@bath.ac.uk

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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