Biomimetics--a review (PDF Download Available)

REVIEW PAPER 919

Biomimetics – a review J F V Vincent Department of Mechanical Engineering, Centre for Biomimetic and Natural Technologies, University of Bath, Claverton Down, Bath BA2 7AY, UK. email: [email protected]; [email protected] The manuscript was received on 12 December 2008 and was accepted after revision for publication on 28 July 2009. DOI: 10.1243/09544119JEIM561

Abstract: Biology can inform technology at all levels (materials, structures, mechanisms, machines, and control) but there is still a gap between biology and technology. This review itemizes examples of biomimetic products and concludes that the Russian system for inventive problem solving (teoriya resheniya izobreatatelskikh zadatch (TRIZ)) is the best system to underpin the technology transfer. Biomimetics also challenges the current paradigm of technology and suggests more sustainable ways to manipulate the world. Keywords: bionic, biomimetic, biomimicry, bio-inspiration, TRIZ, lexicography, technology transfer, sustainability

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INTRODUCTION

It is possible to find references to the wonders of nature’s engineering in the earliest of recorded writings, and the parallel wish of importing the ideas and mechanisms into the present technology. The earliest success was probably flight, presaged by da Vinci’s sketches [1]; the next was polymeric fibres in the form of nylon [2]. In 1957, Otto Schmitt, who coined the word ‘biomimetics’ said: ‘Biophysics is not so much a subject matter as it is a point of view. It is an approach to problems of biological science utilizing the theory and technology of the physical sciences. Conversely, biophysics is also a biologist’s approach to problems of physical science and engineering, although this aspect has largely been neglected.’ Expanding the first of these sentences in the light of the second leads to the following [3]: ‘Biomimetics is not so much a subject matter as it is a point of view. It is an approach to problems of technology utilizing the theory and technology of the biological sciences.’ The word bionics was coined by Jack Steele of the US Air Force in 1960 at a meeting at Wright–Patterson Air Force Base in Dayton, Ohio, USA. He defined it as ‘the science of systems which have some function copied from nature’, or which represent characteristics of natural systems or their analogues. At another meeting at Dayton in 1963, Schmitt said: ‘Let us consider what bionics has come to mean operationally and what it or some word like JEIM561

it (I prefer biomimetics) ought to mean in order to make good use of the technical skills of scientists specializing, or rather, I should say, despecializing into this area of research. Presumably our common interest is in examining biological phenomenology in the hope of gaining insight and inspiration for developing physical or composite bio-physical systems in the image of life.’ The word biomimetics made its first public appearance in Webster’s dictionary in 1974, accompanied by the following definition: ‘The study of the formation, structure, or function of biologically produced substances and materials (as enzymes or silk) and biological mechanisms and processes (as protein synthesis or photosynthesis) especially for the purpose of synthesizing similar products by artificial mechanisms which mimic natural ones.’ Biomimetics then went through a quiet period during which biologists consolidated the engineering approach to biology [4, 5] and emerged fully fledged at a meeting in Seattle in the late 1980s, became ‘green’ as ‘biomimicry’ [6] in the late 1990s and now has become a mainstream area of study, since the number of studies and patents which are newly labelled as ‘biomimetics’ is increasing [7] and people are inventing an increasing number of other words to label the area, thus giving them some sort of exclusivity. Under this heading is found biognosis (a little-used word whose main function is to pacify the classicists who do not like mixing Latin and Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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Greek roots), bioinspiration [8], biological design [9], bio-inspired design [10], and others. Hollywood invented ‘bionic man’ and so rendered the word ‘bionic’ unfit for serious use in the English-speaking world, but elsewhere bionics (e.g. bionique in France and bionik in Germany) has been retained. Even so, the word ‘biomimetics’ is becoming more popular in non-anglophone countries. A search of the internet requires the use of all the above terms. In medicine the word ‘biomimetics’ has become more widespread, apparently replacing the word ‘biomechanics’ so that a prosthesis is now considered to be biomimetic. The number of products or materials which have emerged as a result of biomimetics is limited, which is not unreasonable for a new area of study since it can take 20 years or more to get a new product or idea to market. Probably the fastest innovation was carbon fibre which took 12 years from the first fibre to the usable product, with a large amount of industrial and governmental support. Even then it was extremely expensive until the Japanese started to use it in the handles of golf clubs. This review will cover mainly those materials and products that have emerged, or are ready to emerge, from the research and development environment as fledged engineering, otherwise the task is too great since there are many reports of the mechanical or engineering properties of biological constructs that end with the pious hope that there is yet another candidate for a world-beating product. Even so the topic should have to cover quite a wide field, ranging from materials and robotics [11] to mathematical modelling [12] and techniques for organizing and searching for information, together with innovation and creativity. Also, taking Go¨del’s theorem into account, it is now possible to challenge our current paradigm of engineering as the best way to organize the world, since biomimetics are solving similar problems to technology but are outside technological systems! The UK Technology Strategy Board web site states: ‘Advanced materials encompasses technologies over the entire technology readiness level spectrum, from the conceptual development stage of biomimetics to the everyday use of metal, plastic, ceramic and natural material-based products.’ Biomimetics is moving to centre-stage.

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MATERIALS

Biological materials are made from one or both of two polymers: proteins (poly(amino acids)) and polysaccharides (polymers mostly of six-carbon Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

sugars or hexoses). As a general observation, the mechanical properties of biological materials are closely similar to those of man-made materials, if their density is taken into account (Fig. 1). To the biomimeticist this presents a challenge, since technology resorts to over 300 polymers, plus metals, to produce the same range of properties. If such a wide range of properties could be produced with only two base polymers, problems of recycling would be greatly eased [14]. Indeed ease of recycling may well be a prime reason for biology having only two polymers and thus only two types of bond to be broken. Although there is no direct evidence for this assertion, the bond energy of biological materials is typically low enough that the materials are only just stable under the ambient conditions, suggesting that not only is the energy of synthesis kept low but also the energy for breakdown is also low, benefiting the organisms which perform this process. In most instances this means a temperature of no more than 40 uC, but animals living around the black ‘smokers’ that form at the divide between continental plates have to resist temperatures of several hundreds of degrees Celsius, showing that more stable higherenergy bonds are possible with biological polymers [15]. Other indirect evidence comes from the lush abundance of tropical forests, which is almost entirely due to the rapid turnover of material [16]. Such forests could not exist if the materials were not easily recycled Many biological materials are less dense than man-made materials of the same properties, probably because their structure is more tightly controlled and therefore the bonds are better oriented. The outstanding example is silk, which can be stiffer, stronger, and tougher in tension than high tensile steel. Otherwise the density is low because proteins and polysaccharides are low-density materials, because there is a large amount of water in many biological materials, and because any metals present are not significantly structural.

2.1

Single-polymer materials

There are several materials made from cellulose and, in that they are fibres, they could be considered biomimetic since the earliest fibres used by man were silk, sinew, and various plant fibres. The first biomimetic fibre was probably nylon, in that it is not a reconstituted natural material, and the recognition of its utility comes from its similarity to natural fibres, especially silk. However, its discovery was essentially accidental [2]. The first objectively proJEIM561

Biomimetics – a review

Fig. 1

A log–log plot of specific density versus specific stiffness, showing all technical and all biological materials. (Data derived mainly from reference [13])

duced biomimetic material must be the elastin analogues designed and produced using chemical synthetic methods by Dan Urry, who showed that it can transfer energy in a number of ways (Fig. 2), giving rise to a wide range of controllable mechanical properties presenting numerous opportunities for biomimetic materials and molecular machines. The elasticity of elastin has its origin in a chain of five hydrophobic amino acids: valine–proline– glycine–valine–glycine. This short chain is repeated many times to make an open helix which, in its normal working state, has water surrounding and within it and so is mobile like a rubber molecule [17, 18]. If the temperature is raised, the water is suddenly expelled and the protein shrinks, turning JEIM561

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the chemical energy of the water–protein interaction into mechanical energy. This change is reversible. Substitutions in, and additions to, this sequence can produce a wide range of useful materials. For instance, changing glycine to alanine at the end of the chain produces a durable elastic material that can be melted and moulded. Similarly, adding two glutamic acids per 100 amino acids produces a polymer that is soluble at physiological pH but turns into an elastic solid at pH 3. Urry has also developed polymers that absorb vibrational energy produced by submarine machinery. Elastin analogues are now being produced in fibre form using in-vitro genetic methods [19]. These are used to make tissue scaffolds for arterial grafts or skin growth. Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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Fig. 2 Energy transformations by elastin. (Adapted from data in reference [17])

In another success story, spider silk proteins have been produced from mammalian cells and successfully spun into fibres [20]. The aim is to develop a commercial spinning process and produce enough of the synthetic silk for clinical development of synthetic ligaments and sutures [21]. In addition, the US Army is trying to develop the synthetic silk for soft body armour.

2.2

Water-based systems

All biological materials contain water at some level or another, and water is crucial for the organization and functioning of biological systems, although it is becoming more obvious that the role of water and how it works are not understood. There is much evidence to show that it is structured [22]. Although research on biological lubricants is well established, there is increasing interest in biomimetic systems based on tethered brush-like polymers which can entrain large amounts of water against applied loads [23]. This interest is driven by the threatened introduction of EU-wide regulations forbidding the use of heavy metals such as lead in automotive and other lubricants. While these may not be available, the obvious relevance to medical uses of lubricants in prosthetic joints may speed up development in Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

this area [24, 25]. Note that technology as a whole regards water as a nuisance, whereas in biology it is one of the main assets and organizing influences, since the hydrophobic zones of biological molecules act as adhesive sites when in water. Technology spends large amounts of time and money trying to solve the problems of waterproofing, but one of the most useful projects would be to reinvent technology in a wholly aqueous environment. This not only would remove water as a potentially destructive element but also would add one of the most useful materials to technology. The biological end of nanotechnology is embracing this approach simply because many of the synthetic processes are performed in water. However, it seems that the concept of using water in a positive way has been missed. The extreme properties of biological materials such as silk, produced in an aqueous environment, show that this can be a productive route. As a specific example, the tough and stiff external covering (cuticle) of insects is composed largely of chitin fibres in a protein matrix. When the protein is being laid down, it contains a significant amount of water that acts as a plasticizer, giving the constituent molecules room to adjust their position relative to each other in an otherwise strain-free environment. A major event when the cuticle is stiffened into a load-bearing skeleton is the removal of this water, at JEIM561


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least in part due to the addition of reactive phenolic residues, allowing the formation of bonds between the protein chains which can then show crystallinity and silk-like structures [26–29]. Despite its watery origins, cuticle can be very waterproof and resist degradation in the wet soil for thousands of years. Plastics (the technical equivalent) are not designed to be processed in this way and so do not produce materials with the high performance of insect cuticle. There is no mechanism to encourage orientation in the molecular structure of the polymeric matrix of a man-made composite material.

2.3

Ceramic composites

From the energy point of view, the cheapest way of reinforcing biological tissues is crystalline or semicrystalline calcium carbonate (e.g. aragonite, calcite, or dahlite), silica (as opal), hydroxyapatite, dolomite, and a few other salts. These are commonly grouped as ‘ceramics’. The simplest biological ceramic is nacre (also known as mother-of-pearl (Fig. 3)). It is stiff (60–70 GPa) with high work to fracture (maximum about 1.3 kJ/m2) and fracture toughness Kc of 3–5 MN/m3/2 made of thin (0.5 mm) plates of aragonite (volume fraction, 0.95) with small amounts of protein polymer between the plates [31]. The polymer contributes greatly to resistance to fracture maximally expressed when the material is tested under high-shear conditions; it is important that the matrix is wet, and therefore soft and deformable [32, 33]. The first (and probably only) practical biomimetic nacre was made of laminae 200 mm thick of silicon carbide, sintered, with graphite as the separator between the laminae. It has a work to fracture of 4.5 kJ/m2 and is about six times stiffer than nacre [34]. The absence of a matrix allows the plates to move relative to each other so that the material is very resistant to thermal fatigue; it was developed for use in the ignition systems of jet engines. Even so, the properties of the interface are important since a soft matrix material not only can stop and deflect cracks [35] but also can allow the material to heal [36, 37]. Overall the properties are much better with an interface 100 nm or less thick [37]. In an unpublished study on the reinforcement of the glass protecting the forward-pointing radar of fighter aircraft, which may be shattered if the plane flies through a rainstorm, water droplets were fired at a material at supersonic speed. Abalone shell (a form of nacre) survived the best, losing only one or two layers of aragonite. Other translucent materials were shattered. The technical solution finally used JEIM561

Fig. 3

Mollusc shell ceramics, including nacre, also known as mother-of-pearl. (From reference [30], with permission)

was glass with a 10 mm layer of titanium on the outside, but nacre still performed better mechanically. There are other, more or less practical, analogues of nacre. One, made of alternating layers of polyelectrolyte and clay, has a respectable modulus (13 GPa) and reasonable work to fracture [38]. Another, made with laminae of alumina about 1 mm thick stuck together with very-high-bonding adhesive transfer tape 9473-PC about 2.5 mm thick showed the advantages of the soft matrix, giving a structure with good energy absorption and selfhealing properties [39]. This analogue demonstrates that nacre models are scaleable, since the matrix can yield at a stress lower than the breaking stress of the ceramic phase. However, ultimately there are no products available that use nacreous structures Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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to achieve the toughness as well as the hardness expected of a ceramic material. There are several other ceramic composite materials that are informing biomimetics, either because they are of immediate importance (e.g. bone) or because they are particularly intriguing (e.g. sponge spicules). The most studied sponge is Euplectella, the Venus basket. Its particular interest lies in the orthogonal complexity of its structure (Fig. 4) and

Fig. 4

Euplectella, the Venus basket. The scale bar is 1 cm. (From reference [40], with permission)

Fig. 5

the extreme toughness of the rods (spicules) of which it is made. Their fracture-resisting principle is the same as nacre, namely many thin layers separated by a soft protein [41]. These two factors (complexity and layering) combine to contribute seven layers of hierarchy to the structure (Fig. 5) [40]. This greatly increases the durability of the structure, allowing it to be very damage tolerant and to bend much further before breaking (Fig. 6). Two classic treatments of resistance to cracking are Griffith’s [44] criterion an energy-based method, and a method based on the stress-intensity factor [45]; these present a paradox. For a linear elastic structural element containing a crack of infinitesimal length, both these methods of continuum-based linear elastic fracture mechanics, shown to be equivalent [46], incorrectly predict an infinite load at failure. Conversely from elasticity, a singularity in the stress field at the crack tip [45] is derived also for infinitesimal crack length; combined with the classical assumption that failure occurs when the maximum stress equals or exceeds the material strength, failure must occur at the physically unreasonable zero load. Since on this size scale the nature of fracture mechanics changes, it is necessary to consider the discontinuous nature of matter on the scale of individual crystallites, such as are observed in biogenic (opaline) silica [40]. Quantized fracture mechanics allows these paradoxes to be overcome and produces a much more flexible theory without assumptions [47]. However, this approach has not been applied to bioceramics. Reverting to the current cruder approach, since the size of a typical Griffith flaw in a ceramic or crystalline material is of the order of 10–30 nm, it follows that, if the reinforcing particles in a biologi-

Levels of hierarchy in the structure of Euplectella. (Redrawn with modification from reference [42])

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Fig. 6

Comparison of the bending of a monolithic rod of glass with the bonding of a layered rod from a sponge such as Euplectella. (From reference [43], with permission)

cal ceramic composite are smaller than that dimension, they will be free of flaws. In bone the crystallites of hydroxyapatite are less than 5 nm thick and about 25 nm wide, and so they will not be able to accommodate a stress-concentrating flaw at normal operating stresses. However, it is these crystallites that provide the stiffness of bone. In ox leg bone, three levels of hierarchy have been distinguished by the level of strain which they support [48], which vary in the ratio 12:5:2 (a differential of about 2.5 between the levels) and is interpreted as a form of load shielding by load sharing. In bovine bone the

Fig. 7 JEIM561

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microcracks which control fracture are 2–20 mm long, orders of magnitude larger than the hydroxyapatite crystallites [49]. This means that fracture will, essentially, occur at a higher size level within the hierarchical structure, thus enabling the stiffening element to function with no danger of failure. Thus the particles which are large enough to accommodate a flaw are themselves composite, and the strain energy which the crack might cause to be released can be dissipated by plastic deformation between the subparticles, so that the interatomic interactions providing stiffness do not themselves have to show ductility as might happen in a metal, which has no hierarchy. Essentially, therefore, hierarchy allows the origins of stiffness and toughness in a material to be separated in terms of size and therefore separately controlled [50]. This argument varies with different types of bone, since bovine bone has, for example, a much higher volume fraction of calcium salts than does antler and fractures differently [51]. Hence a single material, ‘bone’, which shows a number of levels of hierarchy (Fig. 7) displays a remarkable range of properties depending on the volume fractions of the components and the control of the interfaces between the levels of hierarchy. Thus the nature and type of damage in bone are also constrained to be hierarchical. The concept that nanoparticles can provide highperformance materials is well established, but the practice seems not. For a start there are very few

Levels of hierarchy in bone. (From reference [52], with permission) Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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materials produced which actually use nanoparticles; mostly the inclusions are measured in hundreds of nanometres. Second the particles are not oriented. Third the volume fraction is very low, commonly only 0.05. There are often problems with mixing, leading to clumping. This is probably a chemical problem. Finally the advantages of hierarchy, namely greater versatility in production and properties and, in particular, the separate manipulation of fracture toughness and stiffness (and possibly other properties), are not realized. Much of nanotechnology relies on self-assembly, and yet techniques are available for supplementing self-assembly. Selfassembly is really available only at the very lowest size level. After that there are other assembly techniques available that are well established within our technology (Fig. 8). For instance, in order to orient the nanoparticles and bring them to a size which can be handled, it seems that electrospinning is a prime technique [53], after which these oriented microfibres (with a diameter of a few micrometres) can be brought together into a composite fibre and hence into a composite structure. It may be that all that is necessary is to introduce heterogeneity over a range of size scales. One of the aims of materials processing in technology is to produce a uniform material, presumably under the impression that this will make its properties predictable. However, iron is a versatile material precisely because it can be heterogeneous

Fig. 8

(steel) with heteroatoms between the crystals causing important differences and improvements in mechanical performance. The study of biological materials suggests that the introduction of heterogeneity, at the right size levels, can improve durability without unduly affecting stiffness. An unresolved question remains: why can nacre and sponge spicules support a much larger basic ceramic unit than bone? The answer is probably that, although they have a less good performance per unit weight, sponges and bivalve molluscs are sedentary, and so they can accumulate strength by accumulating mass, which serves also to anchor the animal. Bone has to be transported by the animal and so must be efficient.

2.4

Fibrous composites

There are many biological fibrous composites: plant cell walls (the fibre is cellulose), arthropod cuticle (the fibre is chitin), connective tissues (the fibre is collagen), skin (the fibres are collagen and keratin) and, arguably, bone (the fibre is collagen). There are some in which the fibre types are mixed: mussel byssus thread protein contains domains which are like silk, collagen, and elastin, the three types of domain contributing to the stiffness or compliance of the distal and proximal portions respectively of the thread, which thus is a sort of block copolymer.

Assembly techniques arranged according to size (vertical) and incorporation of smart technologies (horizontal)


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Fig. 9

A tube made of glass-fibre-reinforced plastic with the fibres wound at 15u to the longitudinal axis. The tube has been stretched and the matrix between the fibres has failed, leaving the fibres intact. (From reference [56], with permission)

In its simplest form and in medicine, the necessity of collagen for good establishment of invading cells, and the control of porosity, has led to the production of tissue scaffolds using a moulding technique [54]. Many other techniques, such as three-dimensional (3D) weaving using a yarn made of poly(glycolic acid) (which produces a more substantial matrix which can support a load even before cellular invasion, and thus be an effective cartilage replacement) is more prosthetic than biomimetic [55] and is not considered further. One of the few, and possibly the only, fibrous composite which can properly be called biomimetic is the wood analogue invented and developed by Gordon and Jeronimidis [56]. The starting question in 1975 was how to account for the high work of fracture of wood. The current model was simple fibre pull-out, which was shown not to account for the high energy absorption. The thickest wall of a wood cell in a softwood such as spruce, about 80 per cent of the thickness, is called the S2 layer. In it the cellulose is oriented in a single direction, spiralling along the cell at an angle of about 15u to the longitudinal axis. In a model system made of a tube with (glass) fibres wound around it at this angle, broken in tension, it does so partly by buckling inwards and partly by the development of a spiral fracture running some distance along it (Fig. 9). This not only provides toughness due to the length of the crack but also gives a force–deflection behaviour like that of a metal with a distinct yield point and a postyield region where the material, although having failed, is still capable of supporting a load (Fig. 10). This type of failure has been observed in wood, where the individual cells additionally pull apart laterally as they buckle inwards, absorbing even more energy (Fig. 11). The spiral organization of the cellulose fibres increases toughness but the axial stiffness is reduced. When the two halves of the piece of wood finally part company, the spiral fractures have left sharp-ended splinters. JEIM561

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Fig. 10

Tensile force–deflection curve of the tube in Fig. 9. Because failure is between rather than across the fibres, the first major failure does not compromise the specimen. (From reference [56], with permission)

Fig. 11

Spruce wood failed in tension. Note the spiral fractures (between the cellulose nanofibres) and the cells pulling away laterally from their neighbours. (From reference [56], with permission)

Early forms of the models were assemblages of straws of spirally wound glass fibres stuck together with resin [56], but these are not very easy to wind and glue together, although weight for weight they Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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are 50 times tougher than any other man-made material (Table 1). There is a cheaper and easier way, although the energy absorption is not so good. Sheets of uniaxial glass fibre prepreg are folded to produce a corrugated structure looking like corrugated cardboard [57]. The fibres are arranged at an angle (about 15u) to the long gaps between the corrugations, so producing a structure like the spiral windings in the wood cell wall (Fig. 12). This material was developed for protection against explosives and against knives and bullets. It is particularly well suited to use in clothing since it is so light, being a cellular material. In a series of tests in which bullet-like projectiles were fired into this wood analogue, its in-plane compressive strength was hardly compromised, whereas a solid carbonfibre-reinforced plastic sheet retained less than 40 per cent of its strength and was therefore severely compromised. In a design study using the wood analogue as a riot shield, the increased cost was about 25 per cent, but the weight of the shield was halved. The current design of riot shield is heavy and the tests are not analytical. There are two types: a rectangular shape with a series of bends that can be linked with adjacent shields. It has a mass of 6.5– 7.0 kg. The second is a three-dimensionally shaped circular shield which has a mass of 2.3–2.4 kg. Both designs are tested to resist penetration from a test ‘javelin’ at a given energy. Both are tested also after contamination with a selection of solvents, acids, alkali, and fire. The main design difference is that, whereas the current shield is designed to resist penetration and thus will be compromised if anything penetrates it, the wood analogue is designed to accept penetration and to absorb the energy. Like many biological materials it is designed to be damaged (damage is, ultimately, inevitable) but to retain its strength even in the damaged state. Armour is not designed with this philosophy in mind. 3

SURFACE STRUCTURES

Anti-reflective surfaces on the eyes and wings of insects are generated by cylindrical protrusions with

Fig. 12 Another way of making the glass-fibre-reinforced plastic wood analogue, using techniques from the corrugated cardboard industry. (From reference [57], with permission)

rounded tips arrayed hexagonally with a periodicity of about 240 nm [58]. They produce a gradient in refractive index between the cuticle of the eye and the air, reducing reflectivity by an order of magnitude. Such structures have been used to reduce reflectivity of windows and lenses. A sinusoidal antireflective grating with 250 nm periodicity, discovered on the eye of a fossil fly, is useful where light shines on to the surface at a range of angles. It has been used on the surface of solar panels, giving a 10 per cent increase in energy capture [59]. There are several types of physical coloration, loosely classified as scattering (coherent and incoherent), diffraction, and interference. They can be produced by close-packed arrays of spheres or platelets, by surface lines, by layered materials with varying refractive index and responses to polarized light, and by 3D structures. Biology has managed to produce physical colours which can be seen over a much wider range of viewing angles than technical colours [60]. The details of this form of colour production are still unknown, but some of the mechanisms are used in textiles [60, 61]. There are several effects employing a mix of superhydrophobicity and hydrophilicity which are giving rise to applications ranging from self-cleaning

Table 1 Characteristics of various materials Material

Specific gravity

Stiffness (GPa)

Specific stiffness

Toughness (kJ/m2)

Specific toughness

Carbon-fibre-reinforced polymer Oak Analogue, corrugated Tough aluminium Tough steel Analogue, tubes

1.6 0.68 0.61 2.7 7.8 0.65

140 10 11 70 206 11

87.5 15 18 26 26 17

1 7 10 400 1220 500

0.6 10 33 150 156 820


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facades of buildings [62, 63] to surface ‘channels’ on microanalytical plates [64] and dew-point water collection [65]. Self-cleaning surfaces are found not only on leaves (archetypically the lotus), but on insect wings and, no doubt, will be found on many other surfaces. The concept is a product of two effects in a hierarchy: a hydrophobic surface created by a layer of hydrocarbons, usually crystalline, arranged on a rugose landscape of bumps at a spacing of about 10 mm (Fig. 13). There is no indication how many times such surfaces have been evolved. Research on these surfaces is not new [67]. At one end of the scale are lumpy surfaces that Chinese researchers have dubbed ‘non-smooth’ and are covered in small bumps or domes. The low-drag surface presented by the denticles on shark skin are in this category [68–70]. At the other end of the scale is the insect plastron (Fig. 14), an arrangement of ‘hairs’ (actually outgrowths of the cuticle, and so very different from mammalian hairs) a few micrometres long arranged at a density of 107 cm22 or more [71]. This is not only a common adaptation of insects living on and around water but also a means for keeping the skin of the animal dry and insulated [73]. Thus a plastron in the shape of a thick pile or pelage of hairs gives a waterproof surface, since water cannot penetrate between the hairs. A successful textile similar to velvet has been developed by a sportswear company, Finisterre, in the UK as a breathable and warm waterproof material for surfers to wear. The inventor did not realize that he was reinventing the plastron, although he based his initial concepts on the waterproof pelage of seals and otters. Another technical version of the same concept is provided by the surface of an extremely water-repellent foam which mimics this mechanism and allows direct extraction of oxygen from aerated

Fig. 14

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The hydrophobic surface of a lotus leaf. (From reference [66], with permission)

A section through the plastron of Aphelocheirus, showing the closely packed ‘hairs’. (From reference [72], with permission)

water [74] and so, presumably, the evaporation of water from the skin surface providing the equivalent of Goretex as a 3D material rather than a single sheet. Water-repellent surfaces are also being developed to make devices which can walk on water [75]. This is clearly a rich area for development. The ‘nonsmooth’ surfaces found on the elytra of many soilburrowing beetles have also been shown to be selfcleaning, but in a totally different way from the lotus effect. The mechanism appears to be due to the high local shear stresses developed at the top of the domes. Experiments showed that the main characteristic is simply the unevenness of the surface, which reduces friction against the soil by up to 40 per cent. The morphology has been used in the design and development of new mould boards on ploughs and new bulldozing plates in the People’s Republic of China [76, 77] and has shown significant fuel savings.

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Fig. 13

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MECHANISMS

High-speed actuators in engineering are based on rotating mechanisms or deflecting plates; in biology they are mostly linear (muscles), oscillating (cilia) or rotating. In plants the actuation is low speed, driven by high internal pressures (typically 10 bar), or high speed using elastic mechanisms for power amplification. Biomimetic muscle systems fall into two classes, which can overlap: the McKibben (USA) or Festo (Germany) pneumatic actuator [78–80], and Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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hydrogel systems [81]. Neither is much like muscle, although the pneumatic actuators rely on a crosshelical bag that looks rather like the perimysium of muscle. However, it has been derived by a totally non-biomimetic route. A current EU project led by Philips of Eindhoven is developing an artificial cilium that will be used to move and mix liquid in microchannels, leading to improved ‘lab-on-a-chip’ devices [82].

4.1

Sensors

It is difficult to include sensors here, since many of those in use (e.g. audio and olfactory devices, and visual systems) may be prosthetic but are mostly not biomimetic. Exceptions occur. The auditory system of the fly Ormia, although of millimetre dimensions, is as good as human hearing for locating the origin of a noise [83]. This directional information is derived from the relative timing of receptor responses in the two ears, dependent on a newly discovered set of specific coding strategies employed by the nervous system. This technology is being built into microelectromechanical systems (MEMSs) [84] where the directional information can be used in hearing aids, cell phones, transceivers, and so forth. By using the directional microphone systems derived from Ormia, background noise is muted, making it easier to track a sound source. Another sonic development, the Ultracane, was derived from work by Dean Waters, a scientist working on bat echolocation at the University of Leeds. It is a walking stick which emits ultrasonic signals and listens to the echoes [85]. A small computer calculates the direction and relative range of an object and sends information to four vibrating buttons on the handle. The stick has received excellent reviews from visually impaired users.

4.2

Robots

Robots have been developed for exploration of all types of terrestrial space and aerospace. Biomimetic robots have been the subject of many reviews [86] and is really too large a topic to be considered properly here. Biomimetic robots have been produced which fly, jump, walk, and swim. Mostly they do not perform as well as the biological prototype, but the comparison has rarely been quantified. Jumping robots are probably easier than most to compare with animals since a single jump is a welldefined activity which does not rely on the nature of the substrate and is easy to measure. Thus it is Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

possible not only to compare the performance of robots and animals (Fig. 15) but also to plot the improvements in design as the study progresses [87].

5

HIERARCHY

Hierarchy has been a topic in materials for many years [52], but the number of levels of hierarchy in biological materials [89, 90] is far greater than that observed in (for instance) a sword made using the Damascus process, in which layers of high- and lowcarbon steel are interwoven either by crystallization or by forging to form a tough lamellate structure on to which a hard cutting edge is hammer welded [91]. Recent work on the design of materials (especially metals and ceramics) is more concerned with the hierarchy of the computational approach than with the hierarchy of the materials themselves [92]. Olson [92] reported the development of a ‘Terminator 3’ ‘self-healing biomimetic, smart steel composite’ in which he claimed that ‘a number of biomimetic concepts have been combined … [to give] … the reinforcement of a brittle ceramic by a rubbery polymeric component to provide ‘crack bridge’ toughening in which rubbery ligaments stretch across cracks’. Such ligaments were first reported in nacre [32] and the inclusion of rubber in ceramics has a distinguished history [93]. Hierarchy in engineering materials and structures is therefore little explored, but a proper implementation could increase the efficiency (e.g. weight supported per unit weight of the support) and strength of a structure by several orders of magnitude (Fig. 16) with associated improvements in durability [52]. The hierarchical structure of biological materials arises from the generation of systems (e.g. wood) resulting from the accretion of subsystems (e.g. cellulose and lignin) during self-assembly and growth. In turn, the systems combine to form supersystems (e.g. tree and forest). Depending on the extent to which each level of the hierarchy is dependent on its lower levels, adaptation or optimization of the material is independently possible at each level of hierarchy. Size differences between hierarchy levels tend to be a factor of about 10. A major advantage of hierarchical structuring is that the material can be made multi-functional and that a specific material property, such as the fracture toughness, can be improved by optimization at different size levels (see above). A direct consequence is increased adaptability of natural materials. Indeed, functions can be modified or enriched by structuring on an additional level of hierarchy. JEIM561


Fig. 15

Comparison of the performances (i.e. vertical jump heights) of animals and robots which jump, showing the design improvements of Jollbot, a jumping-and-rolling robot. (Adapted from reference [88], with permission)

Fig. 16

The improvement in compression strength of honeycomb material with hierarchy of cell size, keeping the density constant. (Modified from reference [52])

Adaptability increases, therefore, as a function of the number of levels of hierarchy. This is probably why such a wide range of material and structural properJEIM561

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ties can be provided by such a small range of base materials. This hypothesis seems to be novel, and so there is no confirmation from the literature. It Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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therefore requires testing experimentally. There are probably several ways of doing this, but it seems likely that the initial stage will be to make a material sufficiently finely divided that the particle size is less than its critical Griffith dimension under reasonable loads. It would probably be necessary to have a fairly high volume fraction of the main load-bearing phase at this scale, say 0.5 at least. This is then used as the filler or fibre particles of a material whose critical crack length is even larger, by using a more compliant matrix, and the process is repeated such that a material with at least three levels of hierarchy is produced. The question then might be whether the net orientation of the primary particles can be varied independently of the fracture characteristics at the third level of hierarchy. There is no doubt that this experimental design is primitive (experiments can be refined only by experiment!) and so it remains only a suggestion of how this concept might be investigated. Bottom-up synthesis remains a challenge if selfassembly is the only technique used. Materials with three levels of hierarchy have been obtained by chemical synthesis and self-assembly, up to a size range of hundreds of nanometres. However, assembly is possible at greater sizes using appropriate engineering techniques (Fig. 8), retaining the hierarchical arrangements. Further work in this direction is strongly needed and is likely to yield a range of new materials with wide-ranging properties. Some of these approaches are being developed with the production of prosthetic materials such as cellular scaffolds, but the degree of detail and hierarchy are severely limited. Once hierarchical structuring is controlled in technological processes, it can be used to create new functional materials based on cheap and/or widely accessible base substances. Such materials could be more widely accessible and based on renewable resources. Indeed, it is conceivable to generate materials with various thermal, optical, and mechanical properties, derived from the same base substances. Natural materials, designed from the nanomaterial level upwards, provide the prototypes.

6

CROSSING THE DIVIDE

The living world is taken to be a vast collection of tried and tested ‘patents’ for solving problems of existence. There is a need to provide a way both of describing and cataloguing the ‘technology’ of life and of prescribing relevant biomimetic solutions to engineering problems. This general approach could Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

be encapsulated in the idea that engineering presents problems and it is necessary to find a solution, whereas biology presents a solution and it is necessary to find out what the problem was. In biology this has led to internal comparisons of physiology and morphology and the recognition that functions in different organisms are similar but solved in different ways. For instance, there are several types of organ for maintaining the ionic milieu of animals, but there has been little or no objective recognition that these organs are meeting apparently conflicting requirements, such as retaining liquid within a permeable tube. The answers to these problems are well known within biology, but their applicability often remains to be illustrated. Hence biomimetics cannot be effective without the knowledge and skills of a biologist, at least at present. Currently there are three main ways of trying to cross the divide between biology and engineering.

6.1

The adventitious approach

Most examples of biomimetic projects and products have stemmed from the desire of a biologist or other observer of nature to find out how a biological system works, whereupon a technologist of some sort sees a technical advantage and attempts to derive an artificial version of the function. This is how Velcro [94] and Lotusan [95] were invented and developed, how George’s wood was born [58], and how the version of nacre made by Clegg et al. [34] was conceived. The advantage of this approach is that a model system is clearly identified having useful properties which can be copied or developed. This approach requires skills to take the essentials of a system out of its immediate context in biology and to make it into an engineered product. A partial solution has been proposed by The Biomimicry Institute which has recently made available Ask Nature, a commented database of relevant publications [96], although it is not as complete as a standard search on Google. While this takes some of the labour out of searching the literature, and the excellent presentation and graphics make up for the routine approach of Google, it adds little to the basic requirement of a general set of tools, since it still relies on the vagaries of biological research topics, which are commonly chosen for very different reasons from engineering, are rarely analysed in a manner accessible to engineering in thinking or context, and may well analyse the concept incorrectly. Indeed, many times a technologist will wish to JEIM561


solve a specific problem and either be unaware of a biological model or may not even realize that the required function exists outside engineering. Under these circumstances it is necessary to implement a more systematic approach, which has the advantage that the answer being sought can be expressed on a more abstract level. On the positive side, Ask Nature gives a few hints on how to formulate a question so that its context is neutralized and it can therefore be made more general. These techniques are expanded and elaborated in section 6.3.

6.2

Lexical analysis

Chiu and Shu [97] have developed a word-based method for deciding on appropriate biological paradigms on which to base engineering solutions. Their analogies are mapped by analysis of natural language and so are a focused subsystem of semantic data mining, or the semantic internet [98, 99]. Chiu and Shu have developed a method to identify biological keywords suggested from the problem to be solved in engineering, and can organize and rank them. As an example, they [97] have done this for the engineering functions of cleaning, encapsulation, and microassembly. The search starts with a digital version of biology conveniently gleaned from textbooks and research papers. Keywords are specifically verbs since they imply functionality; the starting point in engineering is derived by listing the functions which are to be delivered. The problems arise when the engineering words are compared with those in biology. Chiu and Shu used the example of cleaning in engineering, which has hardly any equivalent in biology. However, the question ‘What is the function of cleaning?’ yields the answer ‘To combat contamination’, which in turn elicits the biological equivalent of defence against pathogens. This becomes a fruitful path: defend R invade R evacuate R eliminate R remove R clean. The next stage is to see how organisms defend themselves against invading pathogens, using antibodies, leucocytes, encapsulation, and isolation. In order to make this process computable, the linguistic environment of the word is also analysed, so that its position in a semantic hierarchy becomes a part of its description and defines the context. This context then provides extra keywords that help to define the bridging concept being sought. The relative importance of the various bridging words is then reflected by their frequency of occurrence, which can be used to guide the engineer to more relevant or more useful biological JEIM561

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examples of the phenomenon being sought for production of analogy. Thus these techniques suggest more useful analogies for technology. Obviously this bridging process, being linguistic, is not limited to biology and can be used for any other domain given the availability of appropriate domainspecific knowledge sources and references.

6.3

TRIZ

The adventitious approach provides a necessarily incomplete and therefore flawed catalogue of the biological domain. In the guise of ‘Ask Nature’ it covers only those areas which have already been examined and so is not always of use to the nonbiologist who is looking for a novel solution whose answer has not yet been delivered from biomimetics. Lexical analysis narrowly surpasses this, since it can show the non-biologist which areas of biology are likely to yield information on functions relevant to the problem to be solved. Neither chance nor lexical analysis can properly underpin biomimetics. Neither technique recognizes that the number of manipulations available for changing a system (e.g. so that it will deliver the function required) is likely to be limited, although there is the assumption basic to biomimetics that the manipulations developed within biology can be translated to engineering. It seems rather obvious that, rather than trying to develop a technique de novo, a technique that has already been developed should be adapted. This very concept of adaptation is basic to the Russian approach, namely the teoriya resheniya izobreatatelskikh zadatch (the theory of solving problems inventively (TRIZ)). TRIZ was conceived as a system of interlocking techniques which, used properly, could solve any technical problem. The basic tenet was that all the major functions which contribute to the survival and success of mankind have been discovered and recorded, since they rely on physical principles, and the advancement of engineering could be summarized as the development of more advanced ways of delivering those functions. A simple example might be in transport, where humans have ‘advanced’ from walking or running, to riding an animal, to harnessing one or more animals to a chariot or a stage coach, to using fuel in an external combustion engine such as a steam engine, to using oil-based fuel in an internal combustion engine, to electrical engines. TRIZ was formulated essentially by one man, Genrich Altshuller [100], whose insight was that the manipulations required to deliver these functions could be summarized and Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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reduced to a manageable number (about 40), and that these manipulations were relevant across a wide field of applications. Most people when faced with a problem will proceed to ‘solve’ it with the most obvious object to hand, but a real problem requires a much more innovative approach. Altshuller developed a rigorous set of methods (eventually captured as an algorithm in the TRIZ route map ARIZ), which concentrates on defining the function to be delivered (and hence is independent of the hardware and capable of much more basic generalization), the working environment in which it is to be delivered, and the resources available within that environment. Frequently he found that the solution is best delivered by altering the environment rather than by altering the immediate mechanism of delivery. This enabled him to draw on the experience (through patents) of a vast number of inventive minds, since by this technique he showed that any branch of technology could provide a solution to a specific problem. The specific application depended only on the means of delivery of a generalized manipulation. The starting premise was that, if TRIZ can work as a problem solver, requiring only a careful definition of the problem, then biomimetics can be deskilled and the biological knowledge can be captured by TRIZ, in the same way that TRIZ has captured engineering and design. However, Altshuller pointed out that TRIZ can assist the imagination but not provide a substitute. Since biology is one of the most complex of sciences, biologists will always be needed for effective information transfer, although the lexical analysis by Chiu and Shu [97] would provide a useful ‘front end’ to the biological part of the process. Despite the fact that TRIZ is the most

Fig. 17

promising system for biomimetics, there is still a mismatch, since one of the basic features of living systems is the appearance of autonomy or independence of action, with a degree of unexpectedness directly related to the complexity and intentional (goal-seeking) behaviour of living systems. This gives living systems great adaptability and versatility, but at the expense of the predictability of the system’s behaviour by an external observer. In general, unpredictability is not acceptable in technical systems; indeed, it is avoided. It is possible to develop a version of TRIZ based on biomimetic principles which can solve technical problems using biomimetics without the technologist needing to know biology. This is ‘BioTRIZ’ [101]. This technique eliminates the concept of ‘bioinspiration’ because all the links between biology and engineering have been made and codified using TRIZ [101, 102]. Direct inspiration from a biological prototype has therefore been removed from the pathway leading from the problem to its solution. BioTRIZ has not been available for long but has already had success. The problem to be addressed was that buildings in hot areas accumulate heat during the day. In order to reduce heat gain they are insulated, but this stops the building losing heat to the night sky, the best way of cooling it. It turned out, using BioTRIZ, to be possible to make the insulation keep heat out during the day, but to provide a route for radiation during the night [103]. This was achieved by structuring the insulation to provide an exit pathway (Fig. 17). This solution to the problem does not (as far as the present author knows) actually exist in the natural world; it has no natural prototype. Thus a novel solution has been achieved using the general design strategies that

Insulation on a roof that insulates against short-wave radiation by day but allows longwave radiation to escape at night. (From reference [103], with permission)


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exist in nature, but in the absence of a specific model. It is no longer necessary to know biology in order to benefit from biomimetics!

7

BIOMIMETIC FUTURES

TRIZ as currently formulated is more than a problem-solving system for engineers. It is a means of analysing and diagnosing problems and has been adapted for use in food science, quality control, sustainability, management, medicine, etc. It is also a compendium of the techniques available for solution of problems and so can be viewed as an abstraction of how those technologies are performed. Since the techniques are gleaned from the strongest patents and from interviewing successful practitioners, it is also a compendium of best practice within those particular areas. TRIZ can also subsume biology and thus produces an abstraction of the mechanisms that drive life on this planet. These mechanisms are obviously sustainable within the constraints of planet Earth, and so biomimetics in this form can provide a paradigm for the survival of the technical culture. Since natural selection has provided the quality control, this abstraction is also a compendium of best practice. A comparison of biology and technology should therefore provide formulations for truly sustainable technologies. Such a comparison should require a large amount of information, but a short cut is possible. The manipulations required to solve a problem can broadly be divided among six operational fields: substance, structure, energy, space, time, and information [101]. A sample of solutions to problems (about 2500 from biology, and 5000 from technology) along these lines, taken from sizes ranging from molecular through to a community of organisms (Fig. 18), shows that, whereas technology solves 70 per cent of problems in the general area of materials processing (taken to be in the micrometre size range) using energy as a control parameter, in biology energy is the least significant control parameter over the entire size range. Mostly biology depends on information (derived from the order of bases along the deoxyribonucleic acid molecule, and presumably from external influences when on a scale of millimetres and greater) which also dictates structure. Hence the pleiotropic abilities of two polymers in Fig. 1 can be accounted for [104]. Although most engineers would not readily admit it, biomimetics presented in this fashion, far from being a miscellaneous collection of techniques and JEIM561

Fig. 18

The number of times that one of the six operations (substance, structure, energy, space, time, and information) is manipulated to control a problem versus the size at which the problem has occurred, comparing (a) technology and (b) biology

ideas for incorporation into the current engineering paradigm, is the first challenge to the way in which engineering is carried out. In many respects it finds engineering wanting, not least in its extreme reliance upon energy. This was already known in a vague sort of way, but the TRIZ-based analysis puts numbers to the differences. This challenge has some urgency about it since worldwide the consumption of energy far exceeds the instantaneous supply. Therefore, at present, it is not possible to be ‘sustainable’, but could biomimetics help? It is disputable that the biological system inherited on this planet is the paradigm for sustainability, but there is no evidence that any other system would provide the resources needed for survival, at least on planet Earth. There are several approaches alluded to above (Fig. 8). The first is to combine net forming and assembly techniques; net forming is being developed with moulding (a technique with roots in the past) and rapid manufacture. Unfortunately rapid manufacture does not make use of the possibilities of hierarchical construction, although it is possible immediately to think of ways in which an extruded fibre could be made composite as produced and have orientations in both fibre and matrix. Rapid manufacturing can produce cellular structures rather like biological structures [105] but these have little or Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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no hierarchy. This area is also being explored within medicine, where the other main advance, namely water-based manufacturing, should be much easier to introduce. TRIZ would suggest that any process has to drive itself internally; therefore assembly becomes self-assembly, which is the basis of the genesis of biological structures. Where the forces available for self-assembly become too weak because of increasing size, then TRIZ suggests that resources are sought, and that the most convenient resources, and the most easily controlled, are fields (gravity, air pressure, and electromagnetic fields). This suggests that self-assembled components should be organized by precipitation or aggregation within a controlled field. This, too, happens in biology, where environmentally induced strains are a main driver for shape, size, and microstructure [106–109]. The next phase of biomimetics should be looking more closely at the processes which biology uses to produce morphology. While this is studied in embryology and cellular morphogenesis [110–112], there has been very little work taking these observations into a non-living technical environment [113, 114]. Biomimetics can point the way towards a more sustainable future, but it is not sufficient to translate its lessons into the present technology. It is necessary to translate that technology into a biological format. Medicine may well be best placed to lead such innovation. F Author 2009 REFERENCES 1 Richter, I. A. The notebooks of Leonardo da Vinci, 1952 (Oxford University Press, Oxford). 2 Mossman, S. T. I. Parkesine and celluloid. In The development of plastics (Eds S. T. I. Mossman and P. J. T. Morris), 1994, pp. 10–25 (Royal Society of Chemistry, London). 3 Harkness, J. M. An ideas man. IEEE Engng Med. Biol., 2004, 23, 20–41. 4 Bowie, M. A., Layes, J. D., and DeMont, M. E. Damping in the hinge of the scallop Placopecten magellanicus. J. Expl Biol., 1993, 175, 311–315. 5 Gordon, J. E. The new science of strong materials, or why you don’t fall through the floor, 1976 (Penguin, Harmondsworth, Middlesex). 6 Benyus, J. M. Biomimicry: innovation inspired by nature, 1997 (William Morrow, New York). 7 Bonser, R. H. C. and Vincent, J. F. V. Technology trajectories, innovation, and the growth of biomimetics. Proc. IMechE, Part C: J. Mechanical Engineering Science, 2007, 221(10), 1177–1180. DOI: 10.1243/09544062JMES522. Proc. IMechE Vol. 223 Part H: J. Engineering in Medicine

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