There is such a long and colourful historyof engineers, scientists and artificersgaining inspiration from nature that onecould be forgiven for thinking that all the bestideas have been spoken for. In the nineteenthcentury, biomimesis was at least as much anaesthetic as a practical pursuit. Artists andarchitects delighted in Ernst Haeckels drawings of radiolarians for their beautyalone. When the French designer Ren Binetconceived of the elaborate entrance gate to theWorld Exposition in Paris in 1900, he toldHaeckel: everything about it, from the gener-al composition to the smallest details, hasbeen inspired by your studies1 (Fig. 1).

But others recognized the inventiveness,economy and sound engineering of naturesstructures. The Wright brothers took flightafter watching vultures swoop, giving a nodto Leonardo da Vincis explicitly aviamor-phic flying machines. Joseph Paxton is said tohave paid tribute to the ribbed stem of a lilyleaf in his Crystal Palace, which housed theGreat Exhibition of 1851. Gustave Eiffelstower supports its own immense weightalong elegant curves inspired by bone structure. DArcy Thompson2 tells how in1866 the engineer C. Culmann in Zrich,pondering on the design of a new construc-tion crane, wandered into the laboratory ofthe anatomist Hermann Meyer who wasstudying cross-sections of bone. Observinghow the trabeculae of the porous materialtraced out lines of tension and compression,he cried out: Thats my crane!

This rich heritage means that the diversearray of scientists and technologists whotoday take their lead from nature may feelthey are immersed in the paradigm of an earlier age, with its traditional-soundingconsiderations of morphology, stress distri-bution and hydrodynamic forces. And yetthe materials and devices emerging frombiomimetics are unmistakably forward-looking: new solar cells, smart sensors,advanced robotics and aerospace materials.

But today, biomimetics has somethingmuch more dramatic to offer than an aircraftwing or an anti-drag surface coating modelled after some natural example. One ofthe biggest obstacles to taking full advantageof what nature has to offer is that the living

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Lifes lessons in designPhilip Ball

world has an awesomely elaborate means ofconstruction. There is no assembly plant sodelicate, versatile and adaptive as the cell. But as modern methods of investigation and analysis decode and elucidate the cells molecular machinery piece by piece, this disparity between the natural and syntheticart of manufacture begins to diminish. Whenbiomimicry proceeds at the molecular scale,as it is now beginning to do, its entire basis istransformed.

And the inevitable corollary of molecularbiomimetics is a new conceit, which onemight call biosynergic engineering: mergingnatures machinery with synthetic constructsto develop a new kind of synthetic methodol-ogy at the molecular scale. The scattered,primitive beginnings of such a movementalready reveal that nature may have evenmore potential than it displays in the wild.

Small is beautifulBiomimetics has encompassed some grandengineering, but it is undoubtedly small science indeed, often budget science. Thereasons are clear: nature does not employexotic materials, nor extreme energies or highpressures. The living world comes almost with

a guarantee of economy, for that is evolutionsexigency. Maximum return for minimal(metabolic) outlay: this is the stipulation thatkeeps nature lean and, in some sense, optimal.

Yet in what sense, exactly? The engineermust consider that carefully. It would be foolish to assume that natural selectionstands proxy for the testing laboratory or themarket, refining a design in just those waysthat a new product demands. The complex ofcompromises that shape the fitness landscapeof evolution is likely to bear only incidentalcorrespondences with that which determinesthe contours of technological and economicviability. This, after all, is why we seek tomimic and not to duplicate. One of theattractions, as well as one of the main challenges, of biomimetics is that it demandscreative solutions. Natures pool of ideas isvaluable only if it can be translated into termsthat the technologist can work with, particu-larly in terms of materials and processingmethods.

Take wood, for example. There has beenrelatively little serious attempt to produce anartificial analogue, for the simple reason thatwood itself is already an almost peerlessstructural material for certain applications:

So long as it avoids a Panglossian view of nature, the science ofbiomimetics has the potential to enrich many areas of technology. Butaccurate mimicry will require greater understanding of natural mechanismsat the molecular scale. As this continues to unfold, emulation mayincreasingly give way to assimilation of biological machinery.

Figure 1 Ren Binets entrance to the World Exposition in Paris, 1900, inspired by Haeckelsdrawings of radiolarians.

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cheap, lightweight, tough, mouldable andeasily shaped. But it is not perfect, especiallyin terms of durability in the face of damp and pests. Yet which features of woods enormously complex structure are the mostsalient for mimicry in a synthetic version?

The material developed 20 years ago byGordon and Jeronimidis3 latches onto thefibrous structure to capture fracture-resistance, and so uses glass fibre in a resinmatrix. The low-density cellular structure isonly crudely imitated in this material, by cor-rugating some of the laminated layers thissuffices to keep the material light withoutsacrificing too much robustness.

But there is more to be learned from thenatural engineering of wood. Many engineering materials must be punctured forjoining purposes. But it is one of the oldestprinciples in the engineers handbook, notorious ever since Inglis worried nearly ahundred years ago why British ships werebreaking in half, that holes produce stressconcentration and so allow cracks to nucleate. The fibres that reinforce woodsglassy lignin matrix are severed and renderedstructurally ineffective where a hole is drilled in timber.

The tree, however, drills no holes, eventhough it must disrupt the trunks wood wherea new branch pushes through. The solution isobvious to see in planking: the fibres deformaround a knothole, remaining continuous.This simple solution avoids a significantreduction in fracture strength, yet has been little exploited in fibrous composite materials.Jeronimidis is now proposing to do so4.

High fracture strength is also the alluringaspect of the abalone shell nacre, in many ways the type specimen for biomimetic mate-rials science. Nacre combines several of thefeatures recognized as characteristic of howthe properties of superior materials are engi-neered in natural substances. It is a composite material, and incorporates both inorganic(here calcium carbonate) and organic compounds. The microscopic structure isfinely wrought: plates of the hard mineralinterleave with sheets of proteins and othermacromolecules. The mineralization processis highly controlled, promoting the less thermodynamically stable crystal polymorph(aragonite rather than calcite) with crystallo-graphic planes aligned in different plateletsand the crystal morphology constrained toflat sheets. Some of these features recur inbone, eggshell, tooth enamel and theexoskeletons of diatoms and radiolarians.

The macromolecules are presumedresponsible for guiding nucleation andgrowth of the mineral, but beyond that muchis mysterious. The idea that acidic groups inthe protein sheets provide a template for thearagonite crystal planes now looks overlysimplistic; soluble acidic proteins insteadseem to be a major determinant of crystal-lization5. But the growth process is not just a

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matter of engineering growth in the placesand shapes it is required; it also demands thatnucleation is suppressed elsewhere in a fluidthat is supersaturated with the salt.

It seems quite possible that the solubleproteins act in a manner comparable to thatof the antifreeze proteins in cold-water fish,which can both inhibit and promote icenucleation according to taste. These proteinsare thought to have repetitive hydrogen-bonding groups commensurate with the lattice spacings in ice.

Understanding the molecular-scale mechanisms of the nucleation and growth(two distinct phenomena, dont forget) ofcrystals promises dividends in the industrialpreparation of metastable polymorphs, or thesuppression of degradative mineralization onengineering structures. De novo design ofcrystallization regulators is still at an early,exploratory and largely empirical stage6,although combinatorial methods includingimmunization techniques for raising crystal-binding antibodies7 look encouraging.

The toughening mechanism of nacre crack deflection and energy absorption atweak interfaces is now well established,and has been demonstrated in synthetic laminated materials. But close inspectionshows that there is more to it than that,reminding us that nature is cautious and gen-erally seeks several simultaneous solutions toa challenge. As the mineral plates are pulled

apart during deformation and fracture of the shell, tiny strands are pulled out from the intervening organic layers8 (Fig. 2a). Single-molecule measurements of the forceextension curve of these strands with theatomic force microscope show that theylengthen in modular fashion, producing aseries of sawtooth jumps9 (Fig. 2b). By com-bining relative stiffness (before each jump)with large extensibility, this creates a highwork of fracture (equal to the area under theforce curve). The same principle seems to beat work in the titin molecule, the elastic cordthat prevents the interdigitating sarcomeresfrom separating when skeletal muscle is high-ly extended. Here the sawtooth pattern hasbeen shown to have a clever structural origin:the protein consists of a series of identicalglobular domains that unravel one by one10.

Ant strategiesTo appreciate that nature does not necessarilyhave all the best ideas, we need only point tothe wheel. Nevertheless, most of the problemsof controlled motion and manoeuvrabilityhave been explored and elegantly resolved inthe living world. The Wrights and Otto Lilien-thal drew comfort from the evident fact thatthey were not attempting the impossible.

Yet nature shows too how all flight is notthe same. The smaller an airborne creaturegets, the more manoeuvrable it typically is,which tells the engineer at once about theimportance of Reynolds number: in a medi-um of fixed viscosity, aerodynamic phenom-ena have a particular size scale. It is becominggradually clear that this allows insects accessto different tricks, and thus different flightpatterns, than buzzards and gulls.

Specifically, insects are conjurors of thevortex. With deft flappings and rotations oftheir wings, they are able to manipulate thevortices shed from the edges to control theirmotion in ways that flight engineers can onlydream of: taking off backwards, for example,or landing upside down. By such means,insects subvert the conventional aerofoilprinciples of flight, giving rise to the canardthat the bee is aerodynamically impossible.In essence, the flight of the bumble-bee is aflight beyond the dynamical steady state: liftis generated at particular, exquisitely timedmoments during the flap cycle. By rotatingthe wing so that it is parallel to the ground onthe downstroke but perpendicular on therecovery stroke, an insect is able to recaptureenergy from the vortices shed from the wingedge11. This reveals a new mechanism forflight that one could hardly have deducedfrom first principles, and which might beadopted for the development of miniatur-ized robotic flyers for remote sensing, surveying and planetary exploration.

The actuators and sensors needed to driveand direct robot motion can benefit fromstudies of nature. Here an important part ofthe motivation may be simplicity. There has

Figure 2 Molecular-scale toughening of nacrea, Strands of proteinaceous material betweenthe mineral layers. (Photo: J. Vincent, Univ.Bath.) b, The force curve for individualprotein molecules, measured with the atomicforce microscope. (From ref. 9.)

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been a tendency to overdesign robots, imbu-ing them with actuators that permit everyconceivable mechanical rearrangement oflimbs and with sensors that provide exhaus-tive information about the surroundings.Nature, always seeking economy, makes dowith far less. An understanding of how animals navigate by landmarks, trail laying, geomagnetism or mental integrationof the path already covered should indicatethe minimal requirements in different landscapes. And the articulation of movingparts often provides a lesson in creative simplification. Instead of having active control mechanisms for movement in eachdirection, limbs are often moved by the passive properties of the hinge materials. Ininsects, for example, the wing hinge is notattached to the flight muscles at all. Rather,these muscles deform the elastic, resilientcuticle of the thorax, which translates itschange of shape to a wing oscillation12. Thismechanism, which permits small strains togive rise to large-amplitude motion, is surely instructive to engineers wonderinghow to extract large displacement from thegenerally small strains available from piezoelectric smart actuator materials. Infact, a similar principle is already used in thecrescent-shaped moonie actuators devisedby Newnham and co-workers13, and in thepiezoelectric heads in some dot-matrixprinters.

One of the most striking messages forrobotics coming from the study of animalmotion is that some tasks are more efficientlyconducted by many small, simple entitiesthan by a single large and complex one.Approaches to robot design that attempt tosearch design space in a pseudo-evolution-ary way rather than to impose a preconceivedstrategy14 may now include the option offragmentation: of allowing for a distributedsolution15. This is, of course, how an antcolony operates as a kind of super-organismwhen foraging.

A recent study of ant-mimicking divisionof labour in a swarm of cooperative robotslacking decentralized control showed thatthis does indeed provide an efficient foragingstrategy16. The robotic swarms exhibit anoptimal size, reminiscent of the size selectionseen in animal colonies: for larger groups,the (programmed) tendency to avoid otherrobots begins to inhibit a thorough search ofthe territory. Social insects often operate taskrecruitment, whereby one communicateswith another to draw it towards a resource-rich area. The inclusion of such a capabilityin the robot swarm boosts its ability toexploit clustered resources.

Search algorithms derived from those ofant colonies confer benefits not only in real-space tasks, but also in computation. Ofcourse, the original biomimetic computerapplication is the genetic algorithm. Butsome search tasks, such as trawling a large

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database (as in a web search engine), lendthemselves to schemes that implement akind of trail-laying, like the pheromonesdeposited by foraging ants17. Evaporationof the trail is essential to prevent chasing offalse leads or movement towards depletedsources, and the efficiency of the search canbe highly dependent on identifying the optimal evaporation rate.

Search for systemsEngineers interested in flight, or in toughmaterials, do not find it hard to know where tolook in nature (even if the answers they findare subtle and hard to tease out). But theroutes of technology transfer from biology toengineering sciences are not always so obvi-ous. There might be a myriad of good ideasburied in the living world for an engineersearching for innovation in a particular area but how to find them? In nature there arelots of hidden patents, is the rather merce-nary but nevertheless apt way that the Russianengineer Genrich Altshuller expresses it.

Altshuller has attempted the apparentlyoxymoronic task of systematizing creativityin technical innovation. By analysing over amillion engineering patents, he has identified39 principles on which particular engineer-ing problems hinge. The problems then arisefrom situations in which one of these princi-ples or parameters has to satisfy conflictingrequirements. The contradiction matrixthus contains 1,482 (39238) standard technical conflicts, which Altshuller suggestscan be addressed by a series of standard solutions. He calls this the Theory of Inventive Problem Solving, denoted by itsRussian acronym TRIZ18.

Altshuller claims that almost all innova-tion requires knowledge already available, ifsometimes from disciplines far removedfrom the immediate one. TRIZ claims to easethat process of information retrieval. Julian

Vincent has considered how TRIZ fares ifapplied to the engineering problems faced byliving organisms19. The assessment, whileanecdotal, is revealing.

First, it is possible to identify natural analogues of all 40 of the standard solutions,which include such things as segmentation ofparts, asymmetrical design, nesting of objects,multiple functionality and porosity. This initself implies some kind of mapping betweenbiology and technology. Yet nature does notseem to use the same contradiction matrix tosolve problems20. For example, the drag-reducing properties of shark skin make it one ofthe archetypal examples of natural engineer-ing. But identifying on the TRIZ matrix thecontradictions that arise in this hydrodynamicproblem suggests that appropriate solutionsshould involve weight compensation, movingparts or changes in some ambient parametersuch as compliance. In contrast, shark skin usesa solution not included in Altshullers list: surface conformation. The microscopic ribs ofthe sharks scales suppress turbulence in theboundary-layer flow.

This does not imply that TRIZ is a uselessconcept. Rather, it suggests that human ingenuity is a restricted resource: severalthousand good engineering heads cannotcompete with the billions of years that evolu-tion has had to experiment, select and refine.In other words, says Vincent, nature may be atreasure trove for that small but vital fractionof engineering problems that, in Altshullersreckoning, require genuine innovation andeven fresh discovery.

BiosynergyYet the question remains: are natures solutions practically accessible to us? It mightnot be fruitful, or even possible, to isolate andimitate one aspect of a functioning organismwhile neglecting the dynamic system in whichit is embedded, and which is responsible for itsfabrication, maintenance and adaptation. Silkis a sobering example.

No one expected that simply mimickingthe amide linkages in the polymer chains, asin nylon, would generate a material quite asappealing. But Kevlar, the aramid fibre inwhich intermolecular hydrogen bondingcreates a degree of liquid crystallinity similarto that in concentrated silk solution, deepensthe mimesis and greatly improves thestrength. Shear-induced alignment of polyethylene during the extrusion process,copying that which occurs in the silk spidersspinneret, produces the high-strength fibreknown as rocket wire.

Best of all, one might think, is to takemimicry to the point of plagiarism, and copythe silk protein exactly. But although silkshave been sequenced and silk genes splicedinto the bacterium Escherichia coli and goats(which express the protein in their milk),synthetic silk is still not a mass-produced,high-strength technological material. The

Figure 3 Artificial photosynthesis driving ATP formation in liposomal membranes. Alight-harvesting molecular triad transfers an electron to a shuttle molecule in themembrane, which ferries protons into the liposomes interior. The resulting proton-motive force then powers ATP synthesis byATP synthase.

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crucial aspect of mimicry is not, it seems, inthe protein composition but in the process-ing. It is the weaving of strands in the spinneret that gives them their strength. Thedetails of this process are not understood;but it may be that not until we can build anartificial, miniaturized spinning mechanismwill silk be an industrial material.

This is why biomimetics must reachdown to the microscopic and ultimately themolecular scale. Some of natures best tricksare conceptually simple and easy to rational-ize in physical or engineering terms; but realizing them requires machinery of exquis-ite delicacy. The smaller the scale [at whichmimicry is conducted], the better theprospects for emulation, says Steven Vogel,who points out that natures artefacts aremade in factories smaller than their products21. It is precisely this bottom-upapproach to fabrication that is being soughtwithin the field of nanotechnology which,ever since its beginnings in Richard Feyn-mans famous talk22, has acknowledged theinspiration and guidance that biology offers.

Photosynthesis, for instance, is a trickworth mastering. This is not a matter of effi-ciency: commercial silicon solar cells alreadydo several per cent better at converting light toelectrical energy than the chloroplast does inmaking the conversion to chemical energy.But the nanocrystal solar cells developed byGrtzel and co-workers23 show the benefit ofthe chloroplasts design principles. Allocatingcharge generation and charge separation todifferent entities in the leaf, to chlorophylland to pheophytin, plastoquinone and otherelements of the electron relay reduces thechances of recombination of the light-excitedhole and electron. In silicon solar cells, thesemiconductor serves both ends, and recom-bination can limit the quantum efficiency ofthe process. Grtzels concept was to capturethe photon energy using dye moleculesadsorbed to the surface of nanocrystals of titania. These semiconducting particles thenferry the charge to the collecting electrode.This helps to secure a respectable efficiencythat, although by no means outstanding initself, promises a competitive device whencoupled to the very low manufacturing andmaterials costs.

But more transparently biomimetic is theliposome-based system developed by Moore,Gust, and their co-workers24,25. This is specu-lative mimicry emulation without a current application for the sunlight is hereused to make ATP, as it is in the chloroplast,rather than to generate a flow of current. Themotivation might therefore be construed asmore akin to biocatalysis than photovoltaics:storing up photonic energy in a form accessi-ble to biological systems. The liposomesmimic the thylakoid membrane of the chloroplast, anchoring and organizing thelight-harvesting and energy-transfer molec-ules while also providing a barrier across

explores all options and finds the best is stillsurprisingly pervasive. Nature has good reasons to avoid metallic components, forexample, but this does not mean that humanengineers should strive to do so.

Yet fundamental research on the characterof natures mechanisms, from the elephant tothe protein, is sure to enrich the pool fromwhich designers and engineers can drawideas. The scope for deepening this pool isstill tremendous. It is at the molecular scale,however, that we will surely see the greatestexpansion of horizons, as structural studiesand single-molecule experiments reveal themechanics of biomolecules. If any reminderwere still needed that nanotechnology shouldnot seek to shrink mechanical engineering,cogs and all, to the molecular scale, it is foundhere. Natures wheel the rotary motor ofthe bacterial flagellum never got any largerthan this, nor is it fashioned from hard, wear-resistant materials, nor is it driven electro-magnetically or by displacement of a piston.But it is efficient, fast, linear and reversible32.Somewhere there is a lesson in that.Philip Ball is a consultant editor for Nature.1. Krausse, E. in Die Rezeption von Evolutionstheorien im 19.

Jahrhundert (ed. Engels, E.-M.) (Frankfurt, 1995).

2. Thompson, D. W. On Growth and Form (Cambridge Univ.

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3. Gordon, J. E. & Jeronimidis, G. Phil. Trans. R. Soc. Lond. A 294,

545550 (1980).

4. Jeronimidis, G. Proc. Workshop on Bionics and Biomimetics

(Wissenschaftskolleg, Berlin, 1998).

5. Belcher, A. M. et al. Nature 381, 5658 (1996).

6. Coveney, P. V. et al. J. Am. Chem. Soc. 122, 1155711558 (2000).

7. Bromberg, R., Kessler, N. & Addadi, L. J. Cryst. Growth 193,

656664 (1998).

8. Jackson, A. P., Vincent, J. F. V. & Turner, R. M. Proc. R. Soc.

Lond. B 234, 415440 (1988).

9. Smith, B. L. et al. Nature 399, 761763 (1999).

10.Fisher, T. E., Marszalek, P. E. & Fernandez, J. M. Nature Struct.

Biol. 7, 719 (2000).

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2733 (1993).

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15.Kube, C. R. & Zhang, H. Adapt. Behav. 2, 189218 (1994).

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992995 (2000).

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Theory of Inventive Problem Solving (Technical Innovation

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which an electrochemical gradient can beestablished. The role of the photosyntheticreaction centre and antenna array is adoptedby a synthetic molecular triad in which a photoexcited porphyrin passes energy to anelectron donor, which releases an electron toan acceptor group. From here it is transferredto a mobile shuttle molecule within themembrane, the surrogate for the electron carrier NADPH in photosynthesis. The elec-tron-charged shuttle picks up a hydrogen iontoo and carries them both to the inner face ofthe membrane. There it returns the electron tothe triad, and releases the hydrogen ion intothe liposomes hollow interior. This light-driven hydrogen-ion pump thus creates a pro-ton-motive force, which is harnessed by ATPsynthase embedded in the membrane (Fig. 3).

As a demonstration that a complex natural molecular process can be imitated ina self-assembling synthetic system, this workcarries an encouraging message to deter anyvitalistic suggestion that lifes mechanics areincomparably intricate. But perhaps itstretches the definition too far to regard asgenuinely biomimetic a system that uses molecules such as ATP synthase ready-made?

Of course, it is eminently sensible to doso, rather than trying to devise a proton-driven catalyst de novo. There is thus goodreason to imagine that any molecular-scaleengineering that seeks to achieve things atwhich the cell is already adept such asenergy conversion, construction or replica-tion will be wise to incorporate, ratherthan to imitate, biological machinery.

This sort of biosynergy has been elegantlyexplored with motor proteins. Work on wholly synthetic molecular motors is still in itsinfancy, and so far takes few cues fromnature26,27. But the possibility of modifyingmotor proteins to do non-natural tasks isalready apparent28,29. For example, Dennis etal.29 have used immobilized kinesins orientedalong corrugations in shear-aligned polytetrafluoroethylene films to transportmicrotubules across a surface with directionalpreferences. The development of peptides byin vitro selection that can recognize differentmetal30 and semiconductor31 surfaces suggests the possibility of using geneticrecombination methods to append theseselective hooks to motor proteins to transportand organize semiconductor nanoparticles(quantum dots) into arrays for informationtechnology. In any event, molecular nan-otechnologists would surely be short-sightedif they did not merely take inspiration but alsoworking machines and devices from the cell.

Choices and challengesVogel21 presents elegant and persuasive arguments for why it would be foolish toassume that nature has all the best ideas,which the engineer must then determinehow to translate into workable solutions.The caricature of evolution in which nature

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