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11 Biomimetic Artifi cial Nanostructured Surfaces Emmanuel I. Stratakis and Vassilia Zorba

11.1 Introduction

The study and simulation of biological systems with desired properties is popularly known as biomimetics (from the Greek bios , meaning life, and mimesis , meaning to imitate). This approach involves the transformation of the ideas, concepts and underlying principles that have been developed by Nature into man - made technol- ogy. Biological systems have, through almost four billion years, discovered unique solutions for complex problems which are smart, energy - effi cient, agile, adaptable, fault -tolerant, eco- friendly, and multifunctional. Such solutions emerged as a direct consequence of evolutionary pressure which, typically, forces natural species to become highly optimized and effi cient. The adaptation of methods and systems found in Nature into synthetic constructs is therefore desirable, and Nature pro- vides a unique source of working solutions that can serve as models of inspiration for synthetic paradigms. The superior functions found in natural systems are often achieved through a sophisticated control of structural features at all length scales, starting from the macroscopic world down to the fi nest detail, right down to the level of the atom. Although the building blocks of bone, cartilage, cuticle, mucus, and silk can be relatively simple, they are organized in a rather complex, often hierarchical, manner. Such structural complexity is possible because the manufacture, deposi- tion, and secretion of biological entities are regulated at the cellular and subcellular (gene) level; thus, natural materials are not designed in their fi nal form, but rather are self - assembled. Although the concept of biomimetics emerged during the 1960s, it has been developing rapidly during the past decade due to advancements in nano - and biotechnologies. Currently, a large area of biomimetic research deals with func- tional micro - and nanostructures for nanoscale devices, water repellence, self- cleaning, drag reduction in fl uid fl ow, energy conversion and conservation, high adhesion, reversible adhesion, aerodynamic lift, materials and fi bers with high mechanical strength, antirefl ection, structural coloration, thermal insulation, self - healing and sensory aid mechanisms. All of these exceptional functionalities are

Nanomaterials for the Life Sciences Vol.7: Biomimetic and Bioinspired Nanomaterials. Edited by Challa S. S. R. Kumar Copyright © 2010 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim ISBN: 978-3-527-32167-4 380 11 Biomimetic Artifi cial Nanostructured Surfaces

excellently demonstrated by natural systems, and are based on a variety of ingen- ious designs of biological surfaces. Similar to all natural materials, biological surfaces exhibit hierarchical structuring at both the micro - and nano - scales although, due to their structural and chemical complexity, the exact working mechanisms involved have been clarifi ed only for a few systems. In this respect, biological surfaces hide a virtually endless potential of technological ideas for the development of novel artifi cial materials and systems. Since all biological surfaces serve different functions simultaneously – that is, they are multifunctional – they become even more interesting from the point of view of biomimetics. It is also important to mention here their rather special properties as living structures, such as growth without any interruption of function, an ability to adjust to changing environments, and the capability of self -repair. Whilst these smart and responsive properties are still unavailable to scientists, they clearly represent a challenge for future developments. In this chapter, attention is focused on artifi cial nanostructured surfaces that have resulted from both mimicking, and being inspired by, Nature. (Note: in the following sections, the term “ nanostructures ” includes submicron - sized or smaller structures.) Representative examples among the huge variety of biological nanos- tructured surfaces which have been used – or which can potentially be used – for the development of artifi cial functional materials will be presented. In addition, a comprehensive review of the different approaches used to date for the fabrication of bioinspired artifi cial nanostructured surfaces is provided. Finally, an overview of technical applications that are either under development or available in the current marketplace, is followed by an outlook of future methods for the fabrica- tion of novel artifi cial functional nanosurfaces. It is postulated that, the success of biologically inspired artifi cial surfaces is an indication that knowledge from Nature is an interminable source of inspiration to scientists and engineers in their quest for novel nanotechnological applications. It is also concluded that new, interdisci- plinary, strategies and routes should be required in the future in order to fully understand and accurately mimic the complex adaptive functionalities of biologi- cal nanostructures. Besides presenting recent advances achieved by these tech- niques, the chapter will also delineate existing limitations and discuss emerging possibilities and future prospects.

11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces

Nature offers a diverse wealth of functional surfaces, the properties of which are unmatched in today ’ s artifi cial materials. This is a consequence of the fact that biological surfaces provide multifunctional interfaces to their environment. There is a growing body of information describing natural surfaces with sophisticated design strategies, which lend the organisms and plants superior mechanical, self - cleaning, optical, adhesive, actuation, sensing and responsive capabilities. Nature develops biological objects by means of growth or biologically controlled self - 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 381

assembly adapting to the environmental condition. Such adaptive and responsive self - assembly is provided by means of a hierarchical self - organization and optimi- zation of the biological material at each level of hierarchy, so as to yield outstanding performance [1] . Indeed, well - ordered, multiscale structures with dimensions of features ranging from the macroscale to the nanoscale are extremely common in natural materials. Additionally, the common feature of the largely unrelated natural surface designs is the use of high - aspect - ratio microstructures and nanos- tructures, with the desired functionality being achieved through a tailored synergy of surface morphology and chemistry. In the following subsections, the most prominent properties and different func- tionalities of natural nanostructured surfaces will be reviewed. The few case studies from fl ora and fauna presented here provide examples of the role that surface nanotexture plays in the functionality of biological materials. The impor- tant role of hierarchical multi - length scale roughness when tailoring the superior functional properties of surfaces, and which provides inspiration to scientists in their quest to design novel artifi cial materials, is also described.

11.2.1 Wetting Properties

The special functionalities of certain organisms are usually not governed by the intrinsic property of materials, but are more likely related to the unique surface microstructures and nanostructures. This is especially the case for the special wetting characteristics that have been frequently observed in nature. Biological surfaces are quite diverse in their wettability 1) characteristics, some interesting examples of which are shown in Figure 11.1 a,b. In particular, plants with leaves that emerge from the water surface or grow on land are found to exhibit hydro- phobic and water - repellent properties. In contrast, plants with fl oating leaves, submerged water - growing plants and some tropical and subtropical plants, dem- onstrate an opposite behavior as these are constructed for effi cient water absorp- tion through their surfaces [2] . Alternatively, the rough and sometimes piliferous surface epidermis of animals plays a similar role in maintaining remarkable wetting properties [3] . The outermost layer of the primary biological surface is known as the cuticle (in plants) or integument (in animals). Among the most important attributes of this layer is its wettability, that enables organisms to overcome the physical and

1) The wettability of a surface can be quantifi ed exhibits at least two remarkable wetting by measuring the macroscopic contact angle characteristics originating from a very high ( CA ) of a sessile water droplet deposited on CA (> 150 ° ) and a very small water roll - off it. A surface is termed hydrophilic or (sliding) angle ( < 5 ° ). The sliding angle hydrophobic when the CA is lower or higher denotes the lowest angle to which a surface than 90 ° , respectively, super - hydrophilic if the must be tilted for the roll- off of water droplets CA is less than 10 ° , and super - hydrophobic if it to occur. is above 150 ° . A water - repellent surface 382 11 Biomimetic Artifi cial Nanostructured Surfaces

Figure 11.1 Multiscale structured surfaces in shells; (d) Optical properties: cicada wings, biology. Four types of superior properties can moth compound eyes, and sponge spur. In be found in hierarchical natural surfaces. each case the fi rst row shows a photograph of (a) Wetting and self- cleaning properties: lotus the biological surface, while the second and leaf, duck feather, and mosquito eye (from left third rows show scanning electron microscopy to right); (b) Mechanical and adhesive (SEM) images of corresponding micro- and properties: gecko feet, octopus suckers, and nanometer - scale structures. Reproduced with water strider; (c) Structural coloration: permission from Ref. [1] ; © 2008, Wiley - VCH. peacock feather, butterfl y wings, and beetle

physiological problems connected to an ambient environment, such as desiccation [2] . Depending on the desired functionality, a wide spectrum of hierarchical struc- tures exist and are combined with various chemistries, which modify surface wettability and also have a signifi cant infl uence on particle adhesion. 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 383

11.2.1.1 Water Repellency and Self - Cleaning Properties In the leaves of water - repellent plants, the cuticle is a composite material mainly built up by a hydrophobic polymeric matrix, called cutin, and hydrophobic inte- grated and superimposed lipids called waxes . Water repellence has been qualita- tively (and sometimes also quantitatively) attributed to not only the chemical constituency of the cuticle covering their surface but, even more importantly, to the specially textured topography of the surface [4] . It is understood that the micro - and nano -structured rough surface enhances the effect of surface chemistry into super - hydrophobicity, and water repellency [5] . The super - hydrophobic property of such leaves is also related to reduced particle adhesion, namely the ability of the hydrophobic leaves to remain clean after being immersed into dirty water; this is known as the “ self - cleaning property. ” This ability is excellently demonstrated by the Lotus plant ( Nelumbo nucifera ) which, although growing in muddy waters, has leaves that are untouched by the pollution or contaminants. It is for this reason that in several oriental cultures the Lotus plant is considered as “ sacred ” and a symbol of purity. Scanning electron microscopy ( SEM ) images of the Lotus leaf surface (see Figure 11.2 d – f) reveal a dual scale roughness created by papillose epidermal cells and an additional layer of epicuticular waxes. The roughness of the papillae leads to a reduced contact area between the surface and a liquid drop (or a particle) with droplets residing only on the tips of the epicuticular wax crystals on the top of the papillose epidermal cells. Thus, droplets cannot penetrate into the structure grooves, as air pockets exist between the water and the surface (Figure 11.3 c), such that the contaminating particles can be picked up by the liquid and carried away as the droplet rolls off the leaf. This process, which was coined the “ Lotus - effect ” [4] , is shown schematically in Figure 11.4 . As far as biological implications of the Lotus effect, it is suggested that self- cleaning plays an important role in the defense against pathogens that bind to the leaf surface. Many fungal spores and bacteria require water for germination, and can infect leaves in the presence of water; therefore, the removal of water will minimize the chances of infection. In addition, dust particle removal from leaf surfaces minimizes the changes of, for example, the plant overheating or salt injury. Although the Lotus leaf has been used as a model surface for water repel- lence and self - cleaning, many other biological surfaces have been found to exhibit similar properties belonging both in fl ora and fauna families [6] . A common feature among these surfaces is that the special wetting characteristics derive as a direct consequence of the synergy of microstructured and nanostructured mor- phologies and hydrophobic surface chemistry.

11.2.1.1.1 Surface Roughness and Wettability The effect of macroscopic rough- ness on the wettability of surfaces has been approached on a theoretical basis by two different models. In the Wenzel model [7] , the liquid is assumed to wet the entire rough surface, without leaving any air pockets underneath it (Figure 11.3 d).

The apparent contact angle, θ w , is given by the following equation:

cosθθwo= r cos (11.1) 384 11 Biomimetic Artifi cial Nanostructured Surfaces

(a) (b) (c)

μ μ 2 μm 20 m (d) 10 m (e) (f)

(g) (h) (i)

Figure 11.2 Water repellence and self - cleaning wax tubules on the cells; (g) A spherical water property of the Lotus surface. (a) A fl owering droplet on a super - hydrophobic leaf; plant of Lotus (Nelumbo nucifera ); (b) A Lotus (h) Lipophilic particles (Sudan red - stained) leaf contaminated with clay; (c) Re - movement adhere onto the surface of a water droplet, of the adhering particles by water; (d – f) SEM rolling over the Lotus leaf; (i) SEM image of a images showing the lotus leaf surface at droplet, illustrates the super- hydrophobic different magnifi cations; (d) Randomly property of the leaf surface. Reproduced with distributed microsized cell papilla; (e) Detail permission from Ref. [2] ; © 2008, Elsevier. of the cell papilla; (f) Epicuticular nanosized

where r is the ratio of the unfolded surface to the apparent area of contact under

the droplet, and θo is the contact angle on a fl at surface of the same nature as the rough surface. Since r is always greater than unity, this model predicts that the contact angle will decrease/increase with surface roughness for an initially

hydrophilic ( θo < 90 ° )/hydrophobic ( θo > 90 ° ) surface. In contrast, Cassie and Baxter ( CB ) assumed [8] that the liquid does not completely permeate the rough surface because air becomes trapped beneath it and, as a result, a droplet will form a composite solid– liquid/air – liquid interface with the sample in contact (Figure 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 385

Figure 11.3 Different wetting states of smooth surfaces and is minimized in hierarchical and rough surfaces. (a) Smooth surface; structured surfaces; (d) The Wenzel ’ s or (b) Enhancement of surface hydrophobicity impregnating wetting state; (e) The Cassie – due to microscale roughness; (c) Super - Baxter state; (f) The hysteresis of a water hydrophobicity exhibited by a hierarchically droplet on a tilted surface represents the structured surface due to the additional adhesion of the liquid on the surface, and can nanoscale roughness; the white areas be determined by measuring the lowest angle represent sealed air pockets. The largest to which the surface must be tilted for roll - off contact area between the droplet and the of a water droplet (tilt angle) or the advancing, surface is given in fl at and microstructured θadv , and receding, θrec , angles measured just surfaces, but is reduced in nanostructured before the droplet starts to roll off.

11.3 b,c,e). In order to calculate the contact angle for the heterogeneous interface, Wenzel ’s equation can be modifi ed by combining the contribution of the fractional area of wet surfaces and the fractional area with air pockets ( θ = 180 ° ). In this case, the apparent contact angle, θCB , is an average of the fl at surface, θo , and the value for perfect hydrophobicity (i.e., 180 ° ) and is given by the equation:

θθ=−+() θ cosCBrfr cos ola 1 cos o , (11.2)

where f la is the fractional fl at geometric area of the liquid – air interfaces under the droplet. As f la is always lower than unity ( f la + f ls = 1), this model always predicts an enhancement of the hydrophobicity, independently of the value of the initial contact angle θo . Thus, even for a hydrophilic surface, the contact angle increases with an increase of fla . The contact angle hysteresis is another important characteristic of a solid– liquid interface. When a droplet sits on a tilted surface (Figure 11.3 f), the contact angles at the front and back of the droplet correspond to the advancing, θadv , and receding,

θ rec, contact angle, respectively. When the advancing angle is greater than the reced- ing angle, this results in contact angle hysteresis (defi ned as θadv – θ rec ) occurring 386 11 Biomimetic Artifi cial Nanostructured Surfaces

Figure 11.4 Self - cleaning property of a As the droplet rolls off the surface it picks up super - hydrophobic surface and the two modes the particles and hence cleans it (the Lotus of droplet motion. (a) Schematic effect); (b) In contrast, in the case of a representation of the motion of a droplet on smooth surface the particles are only an inclined nanostructured super- hydrophobic redistributed by the moving droplet. surface covered with contaminating particles.

due to surface roughness and heterogeneity. Contact angle hysteresis is a measure of energy dissipation during the fl ow of a droplet along a solid surface. Surfaces with low contact angle hysteresis have a very low water roll - off angle, which is the angle to which a surface must be tilted for a droplet to roll off it. A relationship for contact angle hysteresis as a function of roughness has been derived [9] , given as: θθ− ()cosadv,, o cos rec o θθadv−= recfr la −1 . (11.3) 21r cosϑo +

For a homogeneous interface f la = 0, whereas for a composite interface f la is a non -zero number. It is observed from Equation 11.3 that, for a homogeneous interface, an increasing roughness (high r ) leads to increasing contact angle

hysteresis (high values of θadv − θrec ), while for a composite interface, an approach

of f la to unity provides both a high contact angle and a low contact angle hysteresis. Therefore, a heterogeneous interface is desirable for super - hydrophobicity and self -cleaning as it dramatically reduces not only the area of solid– liquid contact, but also the adhesion of a liquid droplet to the solid surface and contact angle hysteresis. The formation of a composite interface is a multiscale phenomenon that depends on the relative sizes of the liquid droplet and roughness details. Such an interface is metastable and can be transformed irreversibly into a homogeneous form, thus damaging the super -hydrophobicity. Even though it may be geometri- 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 387 cally possible for the system to become heterogeneous, it may be energetically profi table for the liquid to penetrate into the valleys between asperities and to form a homogeneous interface. Destabilizing factors, such as capillary waves, nanodroplet condensation, surface inhomogeneities and liquid pressure, may be responsible for this transition [10] . It has been shown that the mechanisms involved in super - hydrophobicity are scale - dependent, with effects at various scale ranges acting simultaneously. Thus, a multiscale, hierarchical, roughness can help to resist the destabilization. A high value of r can be achieved by both micro- patterns and nanopatterns. For high fla , nanopatterns are desirable, because whether the liquid –air interface is generated depends on the ratio of the distance between two adjacent asperities and droplet radius. Furthermore, nanoscale asperities can pin the liquid – air interface and thus prevent liquid from fi lling the valleys between the micro -asperities, even in the case of a hydrophilic material. Yet, despite numerous experimental and theoretical studies, the effect of the hier- archical roughness on wettability remains a nonclarifi ed issue and a subject of intense scientifi c discussion.

11.2.1.2 Super - Hydrophilicity In contrast, it has been observed that some natural surfaces are hydrophilic or super - hydrophilic [11] ; such surfaces can either absorb water or allow it to spread over the surface. It has also been shown that almost all species which grow in their natural habitat completely under water, or which partially fl oat on the water surface, are completely wettable [3] . The analysis of super- hydrophilic plants, using SEM, has shown that fl oating and submerged leaves have relatively smooth cuticle surfaces (tabular and slightly convex cells), with no three - dimensional ( 3 - D ) nanos- tructured waxes [2] .

11.2.1.3 Increased Water - Supporting Force Water striders (see Figure 11.1 b) have the ability to fl oat effortlessly and walk quickly on a water surface, without getting wet; this is the result of the striking super - hydrophobic force provided by the insect ’ s legs. Even the impact of rain droplets larger than the strider ’s own size cannot force it to be immersed into the water. The force –displacement curves of the striders’ legs pressing on the water surface [12] indicate that the leg does not pierce the water surface until a dimple of 4.38 ± 0.02 mm depth is formed. The maximal supporting force of a single leg was found to be 1.52 mN, which is about 15- fold the insect’ s total body weight, while the corresponding volume of water ejected is approximately 300 -fold that of the leg itself. This striking repellent force is attributed to the super- hydrophobicity of the legs, which has been verifi ed by a static contact angle of about 167 ° . The SEM images shown in Figure 11.1 b reveal the unique hierarchical structure of the strider ’ s legs, which are covered by a large number of oriented micrometer- scale needle- shaped hairs (microsetae), with many fi ne nanogrooves being found, in turn, on each microseta. These microstructures and nanostruc- tures on the leg surface seem to be responsible for its water resistance and the strong supporting force. 388 11 Biomimetic Artifi cial Nanostructured Surfaces

11.2.1.4 Antifogging Mosquito eyes exhibit antifogging properties so as to provide excellent vision [13] . The single eye (see Figure 11.1 a) is composed of hundreds of microscale micro- spheres termed ommatidia , that are organized into a hexagonal closed - packed arrangement that act as individual sensory units. The surface of each microsphere is covered with nanoscale nipples of average diameter 101 nm and pitch 47 nm, organized in a non- close - packed array. This hierarchical structure is responsible for the antifogging properties of the eye.

11.2.1.5 Under - Water Air - Retaining Surfaces A variety of aquatic and semi - aquatic animals possess hierarchically micro- structured and nanostructured surfaces that enable them to retain air fi lms very effectively while submerged under water, which in turn prevents them from being completely wetted. When under water, the silvery shine of the surface of these species is due to the difference in the refractive indices of the trapped air and water. Trapped- air fi lms serve for different purposes: they enable the organisms to breathe under water, to move at high speeds with low energy input by exhibiting a remarkable reduction of the hydrodynamic drag, to prevent biofouling, or to provide thermal isolation [3] . The potential for the surfaces of many fl oating plants and semi -aquatic animals to provide technical solutions for the design of air- trapping surfaces that reduce drag has been investigated recently [14] . The results suggested that fi ve components should be taken into consideration in order for a stable long - lasting underwater air fi lm to be attained: (i) hydrophobicity; (ii) hairs with lengths of a few micrometers to several millimeters; (iii) additional fi ne nanostructures such as ridges, hairs or waxes; (iv) micro - and nanocavities; and (v) elasticity of the structures.

11.2.2 Mechanical and Adhesive Properties

Many biological systems have mechanical properties that are far beyond those that can be achieved using the same synthetic materials [15] . Biological evolution over a long period of time has led to an optimization of their mechanical characteristics. By mostly using components with modest mechanical performances, it is possible to achieve a surprisingly high mechanical strength and enhanced adhesive proper- ties, due to these very well - constructed microstructures being organized over several length scales. Although, in most cases, the superior mechanical properties are attributed to the hierarchical structure of the bulk (i.e., bone, teeth, nacre, shells, antler), several examples have been identifi ed where the nanoscale surface structuring plays the principal role.

11.2.2.1 Dry Adhesion The attachment pads of several creatures, including many insects (e.g., beetles and fl ies), spiders and lizards (e.g., geckos) and mollusks (e.g., octopuses) are capable of attaching to a variety of surfaces, and are used for anchoring and locomotion, 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 389 even on vertical walls or across ceilings [5, 16] (see Figure 11.1 b). Although these species have different foot or sucker morphologies, in most cases they have small hairs, called setae, that cover the surfaces of their attachment pads. By using the setae, animals can develop a close contact with a substrate so as to provide enough attachment force that they can cling to and crawl on different smooth, slippery, and rough surfaces. However, the setae also provide a reversible adhesion, as they retain the ability to detach at will by peeling; this dynamic attachment ability is referred to as reversible adhesion or smart adhesion [17] . Among a diverse range of smart adhesive species, Tokay gecko or Gekko gecko has been the most widely studied, due to the fact that they exhibit the most advanced attachment ability found in Nature. This ability was known even in ancient times; almost 2500 years ago the ability of geckos “ … to run up and down a tree in any way, even with the head downwards ” was observed by Aristotle [18] . However, little was understood about the mechanism of this phenomenon until the microscopic and nanoscopic hairs that covered the surface of the gecko ’ s toe were discovered during the late nineteenth century. Subsequently, a hierarchical morphology of the Tokay gecko toe was revealed following the advent of SEM during the 1950s. Figure 11.5 shows SEM images of a gecko foot, demonstrating the hierarchical structure down to the nanoscale [19] . The gecko foot comprises an intricate hierarchy of structures, beginning with lamellae; these are soft ridges of 1 – 2 mm length that are located on the attachment pads (toes), and which compress easily so that a good contact can be made even on rough, bumpy surfaces. The setae, which typically are 30 – 130 μ m long and 5 – 10 μm in diameter, extend from the lamellae (ca. 14 000 setae per mm2 ). At the end of each seta are located between 100 and 1000 spatulae , of diameter 200 –300 nm, that branch out and form the points of contact with the surface. The tips of the spatulae are approximately 200 – 300 nm wide, 500 nm long, and 10 nm thick. This hierarchical surface construction provides the gecko with the ability to create a large real area of contact with surfaces. In fact, the attachment pads on two feet of the Tokay gecko have an area of about 220 mm2 , which is suffi cient to produce a clinging ability of about 20 N (the vertical force required to pull a lizard down a near- vertical, 85 ° , surface) [20] and allows them to climb vertical surfaces at speeds over 1 m s − 1 , by attaching and detaching their toes in milliseconds. In contrast, in order to “ unstick ” its feet, the gecko is able to mechanically curl its toes, a movement which breaks the van der Waals forces and allows movement across substrates. The critical angle needed to break such forces is 30.6 ± 1.8 ° [16] . When considering these animal hair systems, the density of setae is known to increase strongly in line with the animal ’s body weight, with geckos having the highest hair density among all animal species studied to date [21] . Yet, various mechanical models have been developed to model these specifi c hairy attachment systems, an example being the fi ber array structure [22] . In particular, the John- son –Kendall – Roberts (JKR ) model [23] of contact mechanics has been used to show that the splitting of a single contact into multiple smaller contacts will always result in an enhanced adhesion strength [24] , thus providing a theoretical basis for understanding the hairy attachment system. These authors assumed the 390 11 Biomimetic Artifi cial Nanostructured Surfaces

(a) (b)

Adhesive Lamellae

(c) (d) (e) Arrays of SetaeSeta Spatulae

75 μm 20 μm1 μm

Figure 11.5 Structural hierarchy of the gecko proximal portion of a single lamella, adhesive system. (a) Macrostructure: ventral with individual setae in an array visible; view of a tokay gecko (G. gecko ) climbing (d,e) Nanostructure: single seta with vertical glass; (b) Mesostructure: ventral view branched structure at upper right, terminating of the foot, with adhesive lamellae visible as in hundreds of spatular tips. Reproduced with overlapping pads. Note the clean appearance permission from Ref. [19] ; © 2005, National of the adhesive surface; (c) Microstructure: Academy of Sciences, USA.

spatula to be a hemisphere of radius, R, such that the adhesion force F α predicted by the JKR theory would be: 3 FWRaa= π , (11.4) 2

where Wa is the work of adhesion per unit area. Equation 11.4 shows that the adhesion force of a single contact is proportional to a linear dimension of the contact. For a constant area divided into a large number of contacts or setae, n ,

the radius of a divided contact, Rd , is given by RRn d = (self - similar scaling) [24] . Therefore, the adhesion force defi ned in Equation 11.4 can be modifi ed for mul- tiple contacts such that: 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 391

3 FWRnnnFaa′ = π ()= a, (11.5) 2 where F a′ is the total adhesive force from the divided contacts. Thus, the total adhesive force is simply the adhesive force of a single contact multiplied by the square root of the number of contacts. The above model, however, only considers contact with a fl at surface. On natural rough surfaces, the compliance and adaptability of setae represent the primary sources of high adhesion. Intuitively, the hierarchical structure of gecko setae allows for a greater contact with a natural rough surface than a nonbranched attachment system [25] . Modeling of the contact between gecko setae and rough surfaces is discussed in detail in Ref. [5] . Besides this, material properties also play an important role in the adhesion process. A soft material is able to achieve a greater contact with a mating surface than a rigid material. Although, gecko skin is comprised primarily of β - keratin (a stiff material with a Young ’ s modulus in the range of 1 – 20 GPa), the effective modulus of the seta arrays on gecko feet is about 100 kPa [26] – approximately four orders of magnitude lower than the bulk material. Thus, Nature has selected a relatively stiff material to avoid clinging to adjacent setae, whereas the division of contacts (as discussed above) provides an enhanced adhesion.

11.2.2.2 Wet Adhesion Some amphibians, such as tree and torrent frogs and arboreal salamanders, are able to attach to and move over wet (or even fl ooded) environments, without falling [27] . These species attach to mating surfaces by wet adhesion, and are capable of climbing on wet rocks even when water is fl owing over the surface. The toe attachment pads of the tree frog consist of an hexagonal array of fl at - topped epidermal cells of approximately 10 μ m in size, separated by approximately 1 μ m - wide mucus - fi lled channels; the fl attened surface of each cell consists of a submicrometer array of nanopillars or pegs of approximately 100 – 400 nm diam- eter. The toe pads are composed of an extremely soft, inhomogeneous material, while the epithelium itself has an effective elastic modulus of approximately 15 MPa, equivalent to that of silicone rubber [28] . The pads are permanently wetted by mucus secreted from glands that open into the channels between the epidermal cells. This pad structure is believed to produce high adhesion and friction by conforming to the mating rough surface at different length scales, and by main- taining a very thin fl uid fi lm at the interface, which is responsible for animal locomotion and maneuverability. The adhesion is believed to occur primarily by a meniscus contribution, resulting from menisci formed around the edges of the pads. The presence of static friction suggests that the fl uid fi lm is very thin in order to have some dry contact between the tips of the nanopillars and the mating surface. These dry contacts are created by squeezing out the fl uid fi lm from the interface. The hierarchical structure and material properties facilitate squeezing and avoid the formation of trapped liquid islands during draining, which would favor sliding. During walking, the squeezing is expected to occur rapidly. 392 11 Biomimetic Artifi cial Nanostructured Surfaces

In contrast, torrent frogs can resist sliding, even on fl ooded surfaces. The surface of the torrent frog toe pads is similar to that of tree frogs, but with the structure modifi ed so as to handle the large fl ow of water [29] . Nonetheless, the toe pad structures of both species have been used to develop structures with reversible adhesion under wet or fl ooded conditions. For example, the treads of tires used for cars and trucks were inspired by the patterns on the toe pads of tree frogs. On a wet road, the water/snow is able to fl ow out through channels located between the treads, and this in turn provides an intimate contact between the tire treads and the road. This leads to the high adhesion required to achieve a good grip when driving on a wet road.

11.2.2.3 Friction Reduction Terrestrial animals, such as snakes, must overcome problems related to friction when they are in contact with solid or friable media. This is achieved through friction -modifying nanostructures observed on their scaly surface [30] . Snake scales include an ordered nanostructured array, presumably to achieve adaptable friction characteristics. The signifi cant reduction of adhesive forces observed in the contact areas is caused by the nanoridge microfi brillar geometry providing ideal conditions for sliding in a forward direction, with minimum energy con- sumption. The highly asymmetric profi le of the microfi brillar ending with a radius of curvature of 20 – 40 nm may induce friction anisotropy along the longitudinal body axis, and functions as a type of “ stopper ” for backward motion, while provid- ing a low friction for forward motion. Additionally, the system of micropores that penetrates the snake skin may serve as a delivery system for a lubrication or anti- adhesive lipid mixture that provides a boundary lubrication of the skin. This sophisticated microscopic design is an extraordinary example of a very effective evolutionary solution for locomotion. The combination of a nanoscale ordered array of low - adhesive nanoridge microfi brils with the ultra- micropore system for the delivery of boundary lubricants produces unique tribological properties. Fur- thermore, a low surface adhesion in those local contact points may reduce wear and skin contamination by environmental debris.

11.2.2.4 Mechanical Stiffness and Stretching Mussels are aquatic sessile organisms, the survival of which in exposed habitats depends largely on the byssus, an adaptive holdfast that secures the animal to a solid surface and dissipates the shock of wave impact through repeated large strains. A typical byssus consists of hundreds of collagenous threads or fi bers, with each fi ber being formed in the groove of the mussel foot by injection molding of the self -assembling precursors secreted from specialized cells in the groove lining. In the fi nishing touch of this process, a nascent thread is covered by a thin (2 – 4 μm) cuticle that consists of proteins with highly repetitive sequences and which protects the underlying collagen fi bers from abrasion and microbial attack. Some mussel species are found predominantly on turbulent wave - swept seashores (intertidal), whereas others reside in deeper, stiller waters (subtidal). Clearly, sur- vival in the former environment will require a greater capacity for energy dissipa- tion by the byssal threads. 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 393

Investigations of intertidal mussels have revealed that the threads of one mussel ( Mytilus galloprovincialis; MG ) are coated with a protective cuticle that is hard, but highly extensible – typically, it is sevenfold more “ stretchable ” than the cuticle of subtidal mussels (e.g., Perna canaliculus ; PC ) [31] . It is the surprisingly complex nanostructure of the mussel thread cuticle that confers this unusual combination of mechanical properties. In particular, when viewed in cross - section, the subtidal PC cuticle seems uniformly homogeneous, whereas the surface of the intertidal MG cuticle is nanostructured, consisting of distinct biphasic granules in a homo- geneous matrix. The granules show an intriguing phase - separated morphology, with a domain size of 20– 40 nm and typical diameter of 0.8 μm, and comprise about 50% of the cuticle volume. These nanostructures seem to be the only struc- tural features that distinguish the cuticles of the two mussel species. When the threads of PC were stretched 30% beyond their length, transmission election microscopy ( TEM ) and atomic force microscopy ( AFM ) imaging revealed large cracks propagating through the cuticle, exposing the underlying core material. A strikingly different result was observed in the threads of MG where, although microcracks formed in the cuticle at 30% extension, their progression through the material was interrupted by the numerous biphasic granules embedded within the cuticle matrix, a structural feature not present in the PC cuticle. As a result, the MG cuticle was almost as extensible as the core it protected, stretching an impressive 70% before rupturing. Such nanostructured mussel cuticles might provide new insights into the design and manufacture of thin composite coatings that are both hard and extensible.

11.2.3 Optical Properties

Nature makes use of submicron surfaces in many ways in order to achieve unique optical effects [32] . Light can be a signifi cant selection pressure for the evolution of certain biological species, leading to the astonishing diversity of natural phot- onic structures present in the natural world. Since 2001, when the fi rst photonic crystal in an animal was identifi ed [33], scientifi c effort in this area has accelerated. Currently, variety of two - dimensional ( 2 - D ) and 3 - D photonic structures have been identifi ed in Nature, including some designs not encountered previously in physics (see Figure 11.1 c,d). In particular, one species of Brittlestar uses photonic elements composed of calcite to collect light, Morpho butterfl ies use multiple layers of cuticle and air to produce their striking blue color, and some insects use arrays of ele- ments (known as nipple arrays) to reduce refl ectivity in their compound eyes. Natural photonic structures continue to provide inspiration for technological appli- cations, initiating a novel active fi eld of “ optical biomimetics. ”

11.2.3.1 Structural Coloration Coloration strategies observed in biological systems have long been a topic of interest to naturalists and philosophers, and even featured prominently in Aristo- tle ’ s Historia Animalium , written more than 2000 years ago [34] . Natural species are able to produce their color by using either a structural or pigmentary medium. 394 11 Biomimetic Artifi cial Nanostructured Surfaces

A pigmented material has selective absorbance properties that determine the spectral refl ectance of the incident light, whereas structural coloration involves materials that are themselves colorless, with the colors being created by using highly precise and sophisticated nanometer - scale architectures. Indeed, the inter- action of light with structures of a size comparable to its wavelength gives rise to bright directional effects; this is in contrast to chemical pigments, which scatter light diffusely. Many birds, insects (particularly butterfl ies and beetles), fi shes and lesser -known marine animals exploit photonic nanostructures on their surfaces to create color changes as the viewing angle changes ( iridescence, from the Greek Goddess Iris, associated with the rainbow), and/or they may also appear “ metallic. ” Such visual effects appear more pronounced than those produced by pigments, and are used to attract the attention of potential mates, as camoufl age, or to startle predators [35] . Structural colors are produced by the physical interaction between light and nanometer -scale variation in the integumentary tissues. The mechanisms respon- sible for producing structural color have been summarized in several excellent reviews [32, 36 – 39] , and are described briefl y here. When light encounters bounda- ries between media that differ in refractive index, structural coloration can be produced by interference, diffraction, or scattering. In particular, special coloration can occur with, roughly, four classes of different structures (Figure 11.6 ): • A random arrangement of more- or - less localized scatterers, which results in the wavelength- dependent scattering of light (Figure 11.6 a). Tyndall or Mie scatter- ing, which favors the redirection of short - wavelength radiation, is an example of such fi ltering by extremely small (subwavelength) particles. • A thin, multilayer refl ectors structure, also referred to as a one - dimensional ( 1 - D ) photonic crystal, where near - planar stacks of alternating values of the refractive index modify the color contents of the specularly refl ected light (Figure 11.6 b). • Surface gratings, which include diffraction gratings and Bragg gratings (Figure 11.6 c,d). Diffraction gratings, sometimes referred to as 2 - D photonic crystals, consist of nanometric periodic parallel slits or grooves, the spacing of which is of the order of magnitude of the wavelength of light, and produce white - light decomposition in the nonzero diffraction orders [37] . Bragg gratings will be considered in the category “ surface gratings, ” along with diffraction gratings, because they are surface structures; that is, the plane containing the periodicity is parallel to the surface plane. However, the mechanism of refl ection is most similar to that of a multilayer refl ector. A Bragg grating consists of a series of ridges where the ridge width (or period) is λ /2 n (where λ is the wavelength and n the refractive index), and is almost like the edge of a multilayer refl ector. One period can be subdivided into two regions; one with a mean refractive index that is close to that of the surrounding medium (air or water), and one with a mean refractive index that is close to that of the material of the animal structure (e.g., chitin). Color is observed in retrorefl ection when the illumination and observation directions form a grazing geometry with respect to the surface plane 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 395

Figure 11.6 Diagrammatic examples of the the refl ection due to interference of light major categories of animal structural colors refl ected at the air - coating layer and at the and antirefl ection property. (a) Scattering of coating layer – substrate interfaces. For white light by small particles (represented by simplicity, only one refl ection path is shown, black dots). If the particles are smaller than which stands for the multiple refl ections approximately 575 nm in diameter, more blue occurring at the interfaces. For the graded light will be refl ected ( “scattered ” ) and more index coating, no refl ection occurs, as the red light transmitted. If the particles are refractive index is matched at the top and larger, all wavelengths will, on average, be bottom interfaces; (ii) A simple, step- like refl ected equally, and the resultant refl ection binary pattern of subwavelength period on the will appear white; (b) Multilayer refl ector; substrate surface; (iii) A more - complex (c) Diffraction grating, where the periodicity step - like structure patterned in the same is greater than or equal to the wavelength of substrate is equivalent to a multilayer stack of violet light; (d) Bragg grating on the surface thin fi lms, each of which has a slightly of a fl attened seta; (e) Monocrystalline 3 - D different refractive index based on the area, or inverse opal structure composed of a matrix fi ll factor, of the corresponding step; (iv) The of chitin containing air spaces of moth - eye structure, which a continuously approximately 250 nm in diameter. Light is varying surface profi le, behaves as if it were a refl ected and diffracted from the air – chitin gradient - index fi lm with a refractive index that interfaces more than once; (f) Polycrystalline varies continuously from that of the 3 - D inverse opal, in which the structure is surrounding medium to that of the underlying subdivided into domains or crystallites substrate. Thus, according to (i), it serves as (indicated by circles); (g) (i) Schematic of the an impedance - matching layer that eliminates refl ections of a substrate with a homogeneous Fresnel refl ections at the air – substrate (left) and a graded refractive - index coating interface. (right). The homogeneous coating reduces 396 11 Biomimetic Artifi cial Nanostructured Surfaces

(Figure 11.6 d). Surface gratings, like thin - layer refl ectors, produce “ iridescent ” effects (some changing color with orientation, others appearing only as one color). Some butterfl ies use this type of grating to send signals, and in these cases, even blazing geometries are used to put all of the emerging energy into one of the diffraction orders. • The full 3 - D photonic crystal, a material with an ordered subwavelength nanos- tructure (Figure 11.6 e,f). Photonic crystals are 3- D complex periodic lattices within which the propagation of light is controlled at the level of a single wave [40] . As a result, incident light of a particular wavelength is entirely refl ected, irrespective of its angle of incidence. In contrast, light is only refl ected from an ideal multilayer refl ector at specifi c incidence angles. Photonic crystals are characterized by the presence of light band gaps, in which certain range of wavelengths cannot propagate as a result of the 3- D periodicity of the lattice.

11.2.3.1.1 Structural Coloration due to Nanometric Surface Scatterers When Tyndall- or Mie- scattered light is polarized under obliquely incident light, it is the relative sizes of the particles that determine the shade of color. For instance, in the dragonfl y Orthetrum cledonicum, epidermal cells contain particles in the cyto- plasm that always are smaller than the wavelength of light [41] . However, if the particles responsible for the scattering coalesce to form larger particles with a diameter in excess of 1 μ m, then white light is observed. An example of this is the gradation from blue to white scattering ( “ small ” to “ large ” particles) that occurs on the wings of the extant dragonfl y Libellula pulchella [41] .

11.2.3.1.2 Structural Coloration due to Nanoperiodic Diffraction Gratings Diffrac- tion gratings are remarkably widespread throughout the orders Coleoptera and Hymenoptera [39] . For example, diffraction gratings in beetles occur in a wide variety of forms, from weakly organized arrays of parallel nanoridges to dense strigulae. These structures disperse white light into its constituent wavelengths, creating rainbow - like refl ectance patterns [39] .

11.2.3.1.3 Structural Coloration due to Nanosized Multilayer Refl ectors The blue - lined octopus, Hapalochlaena fasciata, is well known for its potentially deadly bites and fl ashing blue rings. By using SEM [42] , the rings were shown to consist of densely packed refl ective nanothick plates (up to about 30 in one iridophore), grouped together in a parallel arrangement, and suggested that the blue irides- cence was caused by multilayer constructive interference [42] . Indeed, the refl ec- tive plates have thicknesses of approximately 70 nm; this is the thickness required

for the stack to behave as an ideal quarter - wave refl ector for which λmax = 4nd , where n is the refractive index and d is the thickness of the plate. Thus, assuming a refractive index of 1.59 [43] , the wavelength of maximum refl ectance of the blue- ringed iridophores would be at 445 nm. Furthermore, each iridophore was seen to be oriented at a different angle relative to the surface of the skin; this correlates well with the optical appearance of the rings, as the blue iridescence was visible over a wide range of angles. 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 397

11.2.3.1.4 Structural Coloration due to Photonic Crystal Structures To date, butterfl ies have been the taxon most studied for structural color, revealing a wide diversity of photonic crystal structures. In particular, butterfl y scales exhibit complex architectures that can include micro -ribs with nanoridges, concave multilayered pits, blazed gratings, and randomly punctuated nanolayers. As a result, butterfl ies dispose most of the types of photonic structures that have been identifi ed in Nature so far (Figure 11.7 a – l). However, there is today a growing interest in studying the diverse 3 - D photonic crystals found in butterfl y scales, due primarily to their potential for exciting technological applications. Such complex crystals have been mainly reported from the lumen of butterfl ies, particularly the Lycaenidae [37] (Figure 11.7 i – l). These are typically composed of a matrix of chitin (high -refractive - index material) containing regularly arranged spherical air spaces (low - refractive - index material) of approximately 250 nm in diameter. This is often termed “ inverse opal ” (see Figure 11.6 e), since in the mineral opal , a low - refractive - index material forms the matrix in which spheres of the high - refractive - index material, silicon dioxide, are regularly embedded. In butterfl ies, the lattice may be either monocrystalline, in which case it is oriented in a single horizontal plane and is periodic across the entire volume, or polycrystalline , where it is sub- divided into domains or crystallites that differ from one another in their horizontal orientation but display structural periodicity within each crystallite (see Figure 11.6 f). The former arrangement is, to date, unique to butterfl ies [44] . The appear- ance of scales containing photonic crystals may vary from being relatively matt and invariant with viewing angle, as in the case of a polycrystalline lattice in which color averaging ( “ pointillism ” ) occurs, or iridescent and variable in color with angle, as in the case of a monocrystalline structure.

11.2.3.2 Broad - Range Coloration and Strong Flicker Contrast The coloration of the male Ancyluris meliboeus Fabricius butterfl y is attributed to patches of unusual nanostructures present on the ventral wing scales [45] . The iridescent scales of this butterfl y comprise multilayers of cuticle and air within a discrete nanometer -wide ridging that runs the length of each scale. These layers are tilted at about 30 ° to the base of the scale, causing two distinct optical effects: • The abrupt termination of each cuticle layer at the upper ridge surface presents a strong periodicity of about 700 nm, which contributes a diffractive component. This component appears to combine additively with interference from the underlying multilayer to produce a broad range of coloration, as well as a limited reverse color change with angle compared to that associated with conventional fl at multilayering. • A more striking effect arises from the tilted multilayering, and accounts for the strongly bistable nature of the wing refl ectivity in diffuse white light: it is either “ on, ” when an observer sees one of a broad range of colors; or it is “ off ” and produces no refl ected iridescence. The 30 ° layer tilt causes a 60 ° portion of the wing ’s “ observation hemisphere” not to appear iridescent, but over the remain- ing 120 ° of the hemisphere, diffuse light produces iridescent refl ection. 398 11 Biomimetic Artifi cial Nanostructured Surfaces 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 399

Under identical illumination conditions, other structurally colored insects and animals are seen as iridescent at angles over the entire hemisphere above their refl ecting surfaces. This structural arrangement is important in signaling by the butterfl y. For example, on or near the edge of the Ancyluris meliboeus dark zone, wing movements of no more than a few degrees generate ultra- high - contrast color fl icker in refl ectivity. Among species in which the observation hemispheres have no dark zone, wing movements of large amplitude are necessary to achieve color fl icker.

11.2.3.3 Antirefl ection Coatings Although the character of many natural systems is associated with bright color or broad - angle refl ectivity, Nature presents a specifi c form of nanostructure that minimizes refl ectivity while increasing transmission at a surface over broad angles or frequency ranges. For instance, some insects benefi t from antirefl ective sur- faces, either on their eyes so that they can see in low -light conditions, or on their wings so as to reduce surface refl ections from transparent structures, for the purpose of camoufl age. Antirefl ective surfaces are found on the corneas of moth and butterfl y eyes, and on the transparent wings of hawkmoths. In all cases, antirefl ection is achieved by using subwavelength, nanosized surface architec- tures. For instance, the surface of a moth’ s eye comprises conical nodules with rounded tips arranged in a hexagonal array with a height of 200 nm and periodicity of around 220 nm (see Figure 11.1 b). A moth- eye structure creates what is effectively a gradient- index fi lm from a material of uniform refractive index (see Figure 11.6 g(i)). By itself, an optical substrate exhibits a discontinuity in refractive index at the interface between it and a surrounding medium of differing refractive index (such as air). This index

Figure 11.7 (a) Scanning electron microscopy views of the cover scales from the iridescent (SEM) image of the dorsal wing scales of blue regions of Ptychandra lorquini (Satyrinae: Heliophorus saphir (Lycaeninae: Lycaenidae) Nymphalidae); (h) Sithon nedymond chitra showing cover scales (Co) overlaying basal (Theclinae: Lycaenidae). SEM image of a plan scales (Ba). The fi gure is oriented left to right, view of scutes, showing lateral contact towards the wing edge; (b) An unbleached between adjacent scutes (Sc); (i) SEM image Morpho rhetenor; (c,d ) Pieris brassicae showing a transverse view of a green cover (Pierinae: Pieridae); (c) SEM image of a single scale from the ventral wing of V. blackburnii scale, indicating the longitudinal ridges (Lr); (Polyommatinae: Lycaenidae); (j) Turquoise (d) Nanostructure of a cover scale (Cr, dorsal wing surface of Thecla imperialis cross - rib; Fl, fl utes; Lu, lumen; Pig, pigment (Theclinae: Lycaenidae); granules; Sc, scutes; Tr, trabecula); (e) SEM (k) Thecla coronata (Theclinae: Lycaenidae). image of an unpigmented cover scale from a SEM image of the cover scale from the blue male Morpho sp., showing the diffracting region of the dorsal hindwing regions; longitudinal nanoridges (Lr); (l) Thecla imperialis (Theclinae: Lycaenidae). (f) SEM image of a pigmented basal scale SEM image of the cover scale from the blue from the same specimen as in (e), showing region of the dorsal hindwing regions. the multilayered (Ml) and diffractive (Df) Reproduced with permission from Ref. [37] ; scutes; (g) SEM images showing the lateral © 2008, Royal Society Publishing. 400 11 Biomimetic Artifi cial Nanostructured Surfaces

mismatch is responsible for the refl ected wave that is generated when a beam of light is incident on its surface. If a simple, step - like binary pattern of subwave- length period is created on the substrate surface (Figure 11.6 g(ii)), the binary structure behaves as if it were a thin fi lm having the same height as that of the binary step, but with an effective index that is a spatial average of the surrounding medium and substrate refractive indexes. A more- complex, steplike structure pat- terned in the same substrate is equivalent to a multilayer stack of thin fi lms (Figure 11.6 g(iii)), each of which has a slightly different refractive index based on the area, or fi ll factor, of the corresponding step. In the limit of a continuously varying surface profi le (Figure 11.6 g(iv)) the moth- eye structure behaves as if it were a gradient - index fi lm with a refractive index that varies continuously from that of that of the surrounding medium (i.e., air, n = 1.0) to that of the underlying substrate (i.e., chitin, a polysaccharide with a refractive index of 1.54) [35] . This continuous matching of the refraction index at the boundary of the adjacent mate- rials (cornea and air) gives rise to an increased transmission and reduced refl ec- tion [46] (Figure 11.6 g(i)). For a moth - eye surface with the height of the protuberances of h and the spacing of d (Figure 11.6 g(iv)), the refl ectance would be expected to be very low for wavelengths less than about 2.5 h and greater than d at normal incidence, and for wavelengths greater than 2d for oblique incidence. (Note: Light is not refl ected when the periodicity of the surface pattern is smaller than the light wavelength.) For protuberances with 220 nm depth and the same spacing (typical values for the moth eye), a very low refl ectance is expected for the wavelengths between 440 and 550 nm [47] . The moth- eye effect should not be confused with the reduction of the specular refl ectance by roughening of a surface. Roughness merely redistributes the refl ected light as diffuse scattering. In the case of the moth eye, there is no increase in diffuse scattering, the transmitted wavefront is not degraded, and the reduction in refl ection gives rise to a corre- sponding increase in transmission [47] . A different type of antirefl ective device, in the form of a sinusoidal grating of 250 nm periodicity, was discovered on the cornea of a 45 million- year - old fl y pre- served in amber [35] . This type of grating is particularly useful where light is incident at a range of angles.

11.2.4 Intelligent Biological Nanostructured Surfaces

Organisms sense their environments and alter their properties, in an intelligent manner, in order to adapt to them. Indeed, biological systems provide a very high capability of discrimination, sensitivity and adaptability to environmental changes. In many cases, the different response functions take place on biological surfaces, which is the part of the organism that interfaces the immediate environment. Intelligent surfaces in biology may be divided into two basic categories: • Smart surfaces , which tailor their structure and properties towards the realization of different functionalities. In Nature, smart surfaces are achieved by applying variations in the morphology and/or chemistry of multiscale surface structures. 11.2 Learning from Nature: Properties of Natural Nanostructured Surfaces 401

• Responsive surfaces , which respond to external stimuli by a characteristic behavior to the outside world. In this case, surface molecules are required to be functional with the capability to change their conformational structure and/or chemical properties upon being exposed to an external stimulus. Although some distinct examples of intelligent natural surfaces are presented in the following sections, it should be emphasized that this topic is still in its infancy, and further investigations are required to explore the abundance of intelligent materials in nature. Such effort may be potentially useful for the design and per- formance optimization of future bioinspired artifi cial sensors.

11.2.4.1 Anisotropic Wettability The anisotropic surface structure has great infl uence on wettability. For example, the surfaces of rice, bamboo, screwpine and some grass leaves are anisotropic, which means that it is much easier for water droplets to roll off lengthways than transversely [48] . One example is the anisotropic dewetting phenomenon on the rice leaf [49] , which has a hierarchical structure on its surface similar to that of the lotus leaf, as shown in SEM images. Although, accordingly, the surface is super -hydrophobic, the papillae are arranged in 1- D order parallel to the edge of the leaf and randomly in other directions. As a result, the water drop can roll off freely parallel to the leaf edge, but moves with much more diffi culty along the perpendicular direction. The corresponding sliding angles in these two directions are 3 – 5 ° and 9 – 15 ° , respectively. Another good example of directional wettability can be seen in the super- hydro- phobic wings of a butterfl y [1] . In this case, the droplets easily roll off the wing surfaces in a radial outward ( RO ) direction from the central axis of the body, but are pinned tightly against the surface in the opposite direction. Interestingly, these two distinct states are controlled by the position of the wings (downwards or upwards), and the direction of the airfl ow across the surface (in or against the RO direction). This results from the directional arrangement of fl exible nanotips on overlapping ridged nanostrips and microscales at the 1- D level. Two distinct contact modes of water droplets and orientation -tunable microstructure are pos- sible, thus providing two different water - adhesive forces. Consequently, the arrangement and orientation of a micro/nanostructure can control different states of super - hydrophobicity.

11.2.4.2 Smart Friction Reduction The desert sand fi sh skink (Scincus scincus) is a lizard that has adapted to an underground existence. The skink can virtually dive and “ swim ” beneath the surface of loose sand due to special properties of its scales – they have very low friction and abrasion. The skink ’ s scales are covered by “ nanothresholds ” – long ridges of submicron height and an inter - ridge distance of 10 μ m or less [50] . Rechenberg and El Khyari [51] , who brought attention to this lizard and to what they called the “ sandfi sh effect, ” suggested that an electrostatic charge created by such submicron - sized threshold on the scale played a role in friction reduction by creating a repulsive force between the scale and the sand grains. 402 11 Biomimetic Artifi cial Nanostructured Surfaces

11.2.4.3 Responsive Coloration Change As noted above, the key feature of iridescent colors is that their hue, saturation and brightness are directly dependent on the dimensions and refractive indices of the color - producing nanostructures. Nanometer - scale differences in either of these characteristics can cause dramatic variation in color both across species. Such a property has important implications because it might allow an animal to alter its coloration in response to changes in its environment [52] . These changes might be driven by abiotic factors such as in fi shes, where corneal iridescence changes in response to light availability, which may enhance visual sensitivity in low - light conditions. In the reed frog Hyperolius viridifl avus , dry season increases in tem- perature induce changes in iridescence that result in a higher overall refl ectance, which is thought to help the frogs thermoregulate [53] .

11.2.4.4 Thermal Response Several types of viper, python and other snakes identify warm - blooded targets objects by detecting the minute differences in radiated temperature, with excep- tional discrimination levels (a sensitivity of 0.003 ° C) [54] . Physiological studies have shown that the snake pit organs located on the upper and/or lower jaw can function as highly sensitive infrared (IR ) receptors capable of detecting minute and distant temperature variations, and can provide an additional imaging channel independent from ocular vision. High - resolution TEM and AFM studies have revealed a well - developed array of surface nanopits of several tens of nanom- eters in diameter, and with several hundred nanometers spacing. The actual average spacing of the nanopit array, determined as 520 nm, is close to the value of the grating spacing required for the effi cient fi ltration of nonspecifi c radiation of both ultraviolet ( UV ) and visible spectral ranges below the actual IR range. Furthermore, it is very close to the position of the maximum (550 nm) on the bell- shaped distribution of the sunlight radiation and, in fact, blocks the most inten- sive range almost completely without affecting the IR -sensitive range. Therefore, the effi ciency of refl ection of incoming radiation with such surface grating, should be the highest in the range close to the maximum emmitance of natural sunlight. This can effectively reduce overheating of these receptor areas and allow them to function under conditions of a very strong thermal background.

11.2.4.5 Vapor Response By taking advantage of the hierarchical nanostructure that leads to bright irides- cence in butterfl y scales, Nature provides a different design for selective response to diverse vapors. Indeed, the scales of the Morpho sulkowskyi butterfl y were observed to give a different optical response to various individual organic vapors which dramatically outperformed that of existing nanoengineered photonic sensors [55] . In particular, upon interaction with different vapors, such photonic structures produce remarkably diverse differential refl ectance spectra. This remarkable selectivity is provided by the hierarchical and highly ordered photonic structure of the scales. The principle of a highly selective vapor response, based on hierarchical photonic structures, is illustrated in Figure 11.8 . Measurements 11.3 Fabrication of Biomimetic Artifi cial Nanostructures 403

Reflected light to detector Morpho sulkowskyi Vapor butterfly wing (%) R Δ

Hierarchical λ photonic structure (nm) Distinct spectral response of butterfly scale 500 nm to different vapors

Figure 11.8 Principle of highly selective vapor Δ R = 100% × ( R / R 0 − 1), where R is a response based on hierarchical photonic spectrum collected from scales upon vapor structures, and demonstrated using M. exposure, and R0 is a spectrum collected from sulkowskyi iridescent scales. Measurements of scales upon exposure to a carrier gas. differential refl ectance spectra Δ R provide Reproduced with permission from Ref. [55] ; information about the nature and © 2007, npg publishing. concentration of the vapors: of differential refl ectance spectra Δ R provide information regarding the nature and concentration of the vapors. Exposure to solvent vapors caused refl ectance increases, while immersion in a liquid solvent caused a refl ectance decrease due to the drop in the lamellae – external medium refractive index contrast. Strikingly different Δ R response patterns of the scales were found to these closely related vapors, with the most pronounced differences in Δ R occurring at 325 – 500 nm, and in response magnitude at 500 – 600 nm.

11.3 Fabrication of Biomimetic Artifi cial Nanostructures

In the emerging fi eld of biomimetics, the ever - growing knowledge base of biology is brought together with the rapidly developing ability to measure and manipulate properties at very small length scales [56] . As a result, over the past few years several methodologies have been developed to facilitate the formation of biomi- metic patterns on substrates, with lateral dimensions ranging from hundred of nanometers to several microns [57] . There are two main routes for the fabrication nanostructures, based on top - down and bottom- up processing schemes respectively. In the “ top - down ” approach, a material is produced in bulk and then shaped into a fi nished part through a variety of processes (e.g., casting, molding, rolling, forging, extruding, machining, and 404 11 Biomimetic Artifi cial Nanostructured Surfaces

etching of fi ne features). In “ bottom - up ” techniques, the desired features are con- structed from fundamental building blocks (e.g., self - assembly, sol – gel methods, layer - by - layer deposition), without the need for patterning. However, a combina- tion of top -down and bottom- up approaches is often required for the fabrication of complex hierarchical structures with roughness at different length scales, in order to reproduce the patterns found in natural surfaces. In the following section the basic strategies are reviewed for the fabrication of micro/nanostructured artifi cial surfaces to mimic the wetting, adhesive and optical properties of biological surfaces. The morphology and/or surface chemistry of the natural surfaces are reproduced on different types of material, and the extent to which the resulting surfaces can reproduce the properties of the given biological surfaces is discussed. Finally, details are provided on some currently available (commercial) applications, and of the novel potential applications of biomimetic artifi cial nanostructures.

11.3.1 Wetting Properties of Biomimetic Artifi cial Nanostructures

Surfaces that either strongly attract (super- hydrophilic) or repel (super- hydrophobic) water are key to the two basic routes of self - cleaning, through fi lm or droplet fl ow, respectively [58] . The initial attempts to fabricate super - hydrophobic or super - hydrophobic structures were based on the combination of materials with appropriate surface chemistries (hydrophobic or hydrophilic, respectively), and single -scale roughness surface topology. Several different physi- cal and chemical patterning approaches have been employed to structure the surfaces of a variety of substrates, so as to tailor their wettability in both bottom - up or top - down fabrication schemes [59] . These include photolithography [60] , templated electrochemical deposition [61] , plasma treatments [62] , electron - beam lithography (EBL ) [63] , the deposition of functionalized particles [64 – 66] , solvent treatment of polymer surfaces [67] , the growth of aligned carbon nanotube s (CNT s) [68] or ZnO nanorod fi lms [69] , deep dry etching of silicon (Si) [70] , as well as anisotropic plasma etching [71] . However, the role of surface structures has been revisited recently after studies of a number of biological systems, including the lotus leaf (Nelumbo nucifera [58] , Colocasia esculenta , and Namib desert beetle [72] ) revealed the signifi cance of complex hierarchical micro/nanostructures for the realization of extreme wetting surfaces. Indeed, these studies prompted a new strategy for self- cleaning technolo- gies based on mimicking the morphology of natural surfaces [72] , with emphasis placed on achieving super - hydrophobicity. The lotus leaf surface has been considered as a “ model ” super - hydrophobic, water - repellent surface. As a consequence, the main strategy for fabricating any artifi cial super - hydrophobic and water - repellent surface has been to mimic its surface topology. Simplifi ed schemes of micro - nanomanufacture, enabling the reproducible creation of such complex surface topologies with different length scales, are therefore very desirable. 11.3 Fabrication of Biomimetic Artifi cial Nanostructures 405

11.3.1.1 Hierarchical Super - Hydrophobic Surfaces Attempts to achieve hierarchical structuring in different classes of materials have been reported during the past few years. Particular interest has been directed towards their reproduction on polymer surfaces, because of the wide variety of possible applications that might emerge on a commercial scale. In the studies of Bhushan et al . [73, 74] , the fabrication of artifi cial hierarchical super -hydrophobic surfaces was possible by the replication of natural surfaces or by using micropatterned Si replicas, through a two- step process. In this case, a negative replica of a template was generated using a polyvinylsiloxane dental wax, and a positive replica prepared with a liquid epoxy resin. The subsequent deposi- tion of lotus wax by thermal evaporation led to the formation of double - length scale surface structures. The contact angles achieved were 171 ° and 173 ° for the lotus replica (Figure 11.9 a) and the micropatterned Si replica (Figure 11.9 b), respectively, while the contact angle hysteresis was between 1– 2 ° . The resulting surfaces also exhibited self cleaning properties. Using a similar methodology, the same group [75] also deposited wax from several plants on micropatterned epoxy resins. Tubular waxes of Tropaeolum majus and Leymus arenarius leaves, when assembled on the micropatterned surfaces, resulted in the formation of hierarchi- cal surfaces that exhibited contact angles in the range 160 – 170 ° and a contact angle hysteresis of 2 – 5 ° . Choi et al . [76] used the direct UV replica molding of biomimetic hierarchical structures for selective wetting. The fabricated structures, which were based on photo- crosslinked perfl uoropolyether ( PFPE ), exhibited dual - scale hierarchical structure and super - hydrophobic behavior, with a contact angle in the 160 ° range and contact angle hysteresis as low as 1 ° . Super - hydrophobic polyolefi n surfaces were prepared by simultaneous micro - and nanostructuring by Puukilainen et al . [77] . In this case, the surface patterning was achieved by injection molding, using microstructured aluminum and dual - structured anodized aluminum oxide mold inserts. The structuring had a marked effect on the contact angle between the injection - molded polyolefi ns and water; for example, when the optimized microstructure was covered with the nanostruc- ture, the static contact angle between polypropylene and water reached about 165 ° , with a sliding angle of 2.5 ° . Jiang et al . [78] used an electrohydrodynamic method to fabricate super - hydrophobic polystyrene fi lms with a novel composite structure consisting of porous microspheres and nanofi bers. The resultant morphologies could be controlled by adjusting the concentration of the starting solution. The porous microspheres contributed to the super -hydrophobicity by increasing the surface roughness, while the nanofi bers interweaved to form a 3 - D network that reinforced the composite fi lm. In this way, contact angles of the order of 160 ° were obtained for the resulting porous microsphere/nanofi ber composite fi lms [78] . Zhao et al. [79] developed a simple method for the fabrication of biomimetic super -hydrophobic surfaces (Figure 11.9 c,d) that resembled the natural lotus leaf. This involved a simple plasticization and coagulation procedure using coagulators such as methanol or water on amorphous polycarbonate plates, and resulted 406 11 Biomimetic Artifi cial Nanostructured Surfaces

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10 μm 2 μm 0.8 μm

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Figure 11.9 (a,b) Artifi cial hierarchical panel (c) shows the apparent static water super - hydrophobic surfaces. Side SEM images contact angle on the surface. Reproduced with showing three magnifi cations of hierarchical permission from Ref. [79] ; © 2006, Wiley - VCH; structures created using (a) lotus and (e) SEM image of the top view of the lotus - like (b) micropatterned Si replicas. Reproduced ACNT fi lms; (f) Enlarged view of a single with permission from Ref. [73] ; © 2009, papilla from panel (e); Reproduced with American Chemical Society; (c,d) SEM images permission from Ref. [80] ; © 2002, Wiley - VCH; of a polycarbonate plate (c) after being swelled (g) Transmission electron microscopy (TEM) by acetone fi rst and then precipitated by image of raspberry - like silica particles. methanol. Panel (d) shows an enlarged view of Reproduced with permission from Ref. [82] ; a single particle from panel (c). The inset in © 2005, American Chemical Society.

in contact angles of the order of ∼ 160 ° , with sliding angles below 10 ° for 7 μ l water drops. Hierarchical structures based on the creation of nanostructures on microstruc- tures could also be achieved on CNT surfaces. Feng et al. [80] reported the fabrica- tion of Lotus - like aligned carbon nanotube ( ACNT ) fi lms with both a large contact 11.3 Fabrication of Biomimetic Artifi cial Nanostructures 407 angle and a small contact angle hysteresis (Figure 11.9 e,f). The resultant contact angle on these surfaces was ∼ 166 ° , with a hysteresis of 3 ° . In investigations conducted by Shirtcliffe et al . [81] , hierarchical copper surfaces were prepared by electrodeposition from acidic copper sulfate solution onto fl at copper, and subsequent coating with a fl uorocarbon hydrophobic layers. The resultant apparent contact angles were approximately 160 ° . Assembly from colloidal systems was used by Ming et al . [82] to prepare hierarchical double -length scale surfaces consisting of silica- based, raspberry- like particles (Figure 11.9 g). These structures were created by covalently grafting amine - functionalized silica particles of 70 nm to epoxy - functionalized silica parti- cles of 700 nm, via the reaction between epoxy and amine groups. The surface became super -hydrophobic after being modifi ed with polydimethylsiloxane ( PDMS ), with an advancing contact angle of 165 ° and a contact angle hysteresis of ∼ 2 ° . Subsequently, Zorba et al . [83, 84] employed Ultrafast laser processing of Si in an SF6 atmosphere, followed by the deposition of chloroalkylsilane monolayers; this led to the formation of double -length scale lotus leaf- like structures (Figure 11.10 a). Apart from mimicking the surface morphology of the lotus leaf (Figure 11.10 b), these artifi cial structures exhibited similar wetting behavior to the natural surface. The structured Si surfaces were super -hydrophobic, with a contact angle and contact angle hysteresis comparable to that of the lotus leaf. The water - repelling performance of both surfaces was then examined. By defi nition, a surface is termed “ repellent ” when an incoming drop bounces away from the surface upon impact; the lowest velocity suffi cient for a complete rebound then provides a quantitative measure of repellence. Effi cient waterproof surfaces must also exhibit a strong resistance against penetration by water drops impacting on them, even at large velocity regimes [85] . The water - repellence of the super - hydrophobic struc- tured Si samples were studied and directly compared to the lotus leaf (Figure 11.10 c – e), to identify striking similarities in the overall water - repelling perform- ance – that is, the velocity threshold for repellence, the elasticity of the shocks, and the wetting behavior at high - velocity regimes [83] . This structuring technique led to the production of one of the most water- repellent artifi cial surfaces ever reported, silicon. Self -cleaning ability was also demonstrated on these Si- based artifi cial structures [86] .

11.3.1.2 Hierarchical Super - Hydrophilic Surfaces Hierarchical surfaces provide the appropriate template for the observation of extreme wetting behavior. Hierarchical structuring approaches for the fabrication of super- hydrophilic surfaces are often based on UV light activation of photore- sponsive materials, such as ZnO and TiO 2 [87] . In this case, reversible switching between two wetting states (super - hydrophilic/super - hydrophobic) is possible by alternately exposing the surface to UV irradiation and storing it in the dark. Pho- toresponsive hierarchical surfaces include fl ower - like nanostructured titanium dioxide fi lms prepared by hydrothermal [88] and photoelectrochemical etching methods [89] , and nanostrawberry fi lms from aqueous solution via a seeded 408 11 Biomimetic Artifi cial Nanostructured Surfaces

Figure 11.10 (a) SEM image of a laser - (c – e) Demonstration of water repellency on structured Si surface comprising micrometer - artifi cial and natural super - hydrophobic sized cones. The inset shows a hierarchical surface structures. Selected high - magnifi cation SEM image of a single snapshots of a millimetric water drop impact cone, depicting nanometer -sized protrusions; (c) on a laser - structured Si surface; (d) on a (b) SEM image of the leaf surface comprising lotus leaf surface; and (e) on an unstructured micrometer- sized papillae (scale bar = 10 μ m). Si surface, with the same impact velocities. The inset shows a high - magnifi cation SEM Reproduced with permission from Ref. [83] ; image of a single papilla, depicting © 2008, Wiley - VCH. nanometer - sized branch like protrusions;

growth method [90] . Recent attempts to produce a multilayer assembly of TiO 2 nanoparticles and polyethylene glycol [91, 92] showed a super- hydrophilic surface without the use of UV irradiation, for which the extreme wetting behavior sub- sided after a few wetting– dewetting cycles. Despite this approach showing promis- ing results, chemically stable surfaces are required for certain types of application [76, 93, 94] . Unique hierarchical pore structures were fabricated by electron irradiation of a silicone grease (a mixture of organic PDMS and inorganic silica nanoparticles) by Lee et al . [93] . In this case, the hierarchical pore structures consisted of microm- eter- sized pores and macroporous walls; however, due to the high surface rough- 11.3 Fabrication of Biomimetic Artifi cial Nanostructures 409

(a) (b) (d)

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500 nm Figure 11.11 (a) SEM image of coated exhibiting antifogging properties of raspberry - raspberry - like nanospheres after calcination. like nanosphere coating - coated (upper) and Images of immediate water contact angles on control (lower) slide glasses. Both slides were (b) the raspberry - like nanosphere coating after cooled at ca. − 15 ° C for 3 h in a refrigerator calcination (contact angle ∼ 0 ° ) and and then exposed to humid laboratory air (c) deionized water- cleaned glass substrates (relative humidity ca. 50%). Reproduced with (contact angle ∼ 36 ° ); (d) Digital images permission from Ref. [94] ; © Elsevier.

ness the deposition of high - surface energy layers on the structures led to super - hydrophilicity, with a contact angle of 3 ° . Liu et al . [94] reported the formation of raspberry - like silica nanospheres pre- pared by the electrostatic self - assembly of polyelectrolytes and monodisperse silica nanoparticles. The resulting surfaces were then coated via layer - by - layer assembly with polyelectrolytes, and subsequently calcinated (Figure 11.11 a). The wetting behavior of the resulting hierarchical coatings was examined and compared to that of glass slides (Figure 11.11 c,d). The hierarchical surface exhibited super- hydrophilic behavior with a contact angle close to 0 ° (Figure 11.11 b) and antifog- ging behavior (Figure 11.11 d). The instantaneous spreading and sheet - like wetting by water could be used to provide self - cleaning functions.

11.3.1.3 Anisotropic Wettability of Hierarchical Structures The design of smart, fl uid- controllable interfaces may be applied in novel micro- fl uidic devices. Gradients in surface tension can induce a net motion of a liquid drop on a surface; such fl ow arising from the action of a surface tension gradient can be created by several approaches, including thermal [95] , chemical [96] , electrochemical [97] , and light - driven methods [98] . Zorba et al. [99] used a biomimetic approach for the fabrication of double- length scale hierarchical structures on Si, based on femtosecond laser structuring. By designing and fabricating specifi c textures on the Si surface, anisotropic wetting and spontaneous motion of liquids could be induced. To achieve a surface tension gradient on the Si surface, successive regions were structured at different laser fl uences (Figure 11.12 a). Each one of these regions consisted of different surface morphologies (which formed a different static contact angle with water), thus inducing a wettability gradient on the Si surface. 410 11 Biomimetic Artifi cial Nanostructured Surfaces

(a) 2 mm

(b) (c)

(i) (i) Increasing Hydrophilicity Increasing Hydrophilicity

(ii) (ii)

(iii) (iii)

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(v) (v) Figure 11.12 (a) Optical microscopy image of from the drop deposition: 0 s (i), 2.5 s (ii), 3.9 s the Si surface structured with a wettability (iii), 4.4 s (iv), and 5.7 s (v); (c) Photographs of gradient. Here, four different regions with a water drop ascending the same area tilted at different wettability can be seen, 25 ° . Time from the drop deposition: 0 s corresponding to surfaces processed under (i), 2.4 s (ii), 5.0 s (iii), 5.8 s (iv), and 7.6 s different laser conditions. The arrow indicates (v). The shift of the center of mass from the the direction of increasing hydrophilicity initial to the fi nal position is marked by the (decreasing surface roughness); vertical dashed lines in panels (b) and (c). (b) Photographs of a water drop spreading on Reproduced with permission from Ref. [99] ; the same area, on a nontilted surface. Time © 2006, Institute of Physics Publishing.

During the deposition of a water drop on the most hydrophobic edge of the structured surface regions, the advancing edge of the liquid made contact with the adjacent (more hydrophilic) area, which in turn caused the droplet to start elongat- ing in the direction of motion (Figure 11.12 b). Tilting the same surface by 25 ° led to an upwards shift of the center of mass of the droplet as it ascended the struc- 11.3 Fabrication of Biomimetic Artifi cial Nanostructures 411 tured regions in the direction of the most hydrophobic to the most hydrophilic region (Figure 11.12 c). The possibility of driving drops to ascend a structured Si surface, tilted at any angle (even upwards) by fabricating a proper texture gradient on it, was also demonstrated.

11.3.2 Adhesion Properties of Biomimetic Artifi cial Nanostructures

Having derived inspiration from biological systems such as geckos and mussels, the mechanical and adhesion properties of a number of bioinspired surfaces have undergone intensive investigation during the past few years [100, 101] . Geim et al . [102] microfabricated an adhesive that mimicked the gecko foot - hair - arrays, whereby submicrometer polyamide hairs were obtained using EBL, thermal evaporation and lift - off, and dry - etching in oxygen plasma. The polyamide nanohairs were originally grown on a Si substrate, for which system the adhesive force was small (0.01 N for a 1 cm 2 patch), and revealed that less than 1% of the hairs were in actual contact with the glass surface. The polyamide fi lm was then transferred from the wafer onto a soft bonding substrate, so that the resulting material could be handled as an adhesive tape (Figure 11.13 a). The use of a soft base resulted in a high adhesive capacity of the system, exhibiting a 1000 - fold increase compared to polyamine nanohairs grown on a Si substrate. The average force per hair was 70 nN, and the whole 1 cm 2 patch was able to support 3 N (approximately one -third of the estimated adhesive force for the gecko foot hair). The gecko tape was used to support the weight of a Spider- man toy on a horizontal glass plate (Figure 11.13 c). Although the artifi cial gecko hair was shown capable of passing through several detachment –attachment cycles, bunching of the nano- hairs was seen as one of the main mechanisms responsible for the reduction in their adhesive strength (Figure 11.13 b). In the study of Kim et al . [103] , gecko - inspired polymer microfi bers with fl at spatulate tips were used as repeatable fi brillar adhesives. These structures were fabricated by molding a master template that had been created by using deep reactive - ion etching (RIE ) and the notching effect. The surfaces produced demon- strated macroscale adhesion pressures up to 18 N cm − 2 . Kustandi et al . [104] com- bined colloidal lithography, Si etching and nanomolding technology to fabricate fl exible polymer surfaces with high- aspect ratio nanofi brillar - structured surfaces that mimicked the gecko foot hairs. While a single nanofi bril exhibited a mean adhesive force ranging from ∼ 0.91 to ∼ 1.35 nN, on a macroscopic scale the nanos- tructured surface was capable of adhering fi rmly to a smooth glass substrate. Moreover, it inherited the in -use, self- cleaning properties of the setal nanostruc- tures found in the gecko lamellae. Lee et al. [105] reported the fabrication of a reversible wet/dry adhesive by com- bining the important elements of gecko and mussel adhesion. This new adhesive material – termed “ geckel ” – functioned like a sticky note and exhibited strong yet reversible adhesion in both air and water. The fabrication process was based on the replication of structures created by the EBL of poly(methylmethacrylate) 412 11 Biomimetic Artifi cial Nanostructured Surfaces

(a) (c)

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40 Force (nN) 20 50 μ 0 10 m 0

Individual pillar force (nN) 200 400 600 800 1,000 1,200 Number of adhesion cycles Gecko-air Geckel-air Gecko-water Geckel-water Figure 11.13 Adhesion properties of a carrying capacity of > 100 g. Reproduced with biomimetic artifi cial surfaces. (a) Scanning permission from Ref. [102] ; © 2003, npg electron microscopy (SEM) images of publishing; (d) SEM image of a reversible microfabricated polyimide hairs used to wet/dry adhesive ( “ geckel ” ), which combines evaluate the macroscopic adhesive properties important elements of gecko and mussel of a biomimetic material; (b) Bunching was adhesion. The nanopillar array was fabricated found to be one of the mechanisms using electron- beam lithography; (e) Adhesion responsible for the reduction of adhesive force per pillar for the uncoated (referred to strength of the artifi cial hair; (c) Re - attachable as gecko) and mussel - adhesive - protein - dry adhesives based on the gecko principle; a mimetic polymer coated pillar array in water Spider - man toy clinging with one of its hands and in air; (f) Performance of geckel adhesive to a horizontal glass plate. The toy (15 cm during multiple contact cycles in water (red) high, weight 40 g) has its hand covered with and air (black). Reproduced with permission the microfabricated gecko tape, which from Ref. [105] ; © 2007 npg publishing. provides a ∼ 0.5 cm2 contact with the glass and 11.3 Fabrication of Biomimetic Artifi cial Nanostructures 413

(PMMA ), replication on PDMS, and subsequent coating with a mussel- adhesive - protein - mimetic polymer. The wet adhesion of the nanostructured polymer pillar arrays (Figure 11.13 d) was increased almost 15 - fold when the surface was coated with the mussel - mimetic polymer (Figure 11.13 e). Moreover, the system main- tained its adhesive performance for over one thousand contact cycles, in both dry and wet environments (Figure 11.13 f). The geckel nanoadhesive was shown to be highly effective at adhering reversibly to surfaces under water, and with a func- tional performance resembling that of a sticky note. When the mechanical adhe- sion properties were measured using AFM for individual posts, the extrapolation of adhesion measurements to larger areas revealed that a 1 cm 2 surface area of geckel adhesive would transmit 9 N of force under water (90 kPa) – a value which was similar to estimates of the strength of gecko dry adhesion. The use of hierarchical structures for improved adhesion was also tested using a more sophisticated approach. In this case, gecko - inspired reversible adhesives were fabricated [56] that consisted of a silicon dioxide platform covered with organic- looking polymeric nanorods (“ organorods ” ) that were, in turn, supported by a single- crystal Si pillar. The combination of these structures constituted mul- tiscale compliant structures that could be created across an entire 100 mm wafer. By developing and implementing a technique to measure the adhesion properties (based on a nanoindenter instrumentation to measure the pull- off force between a 5 mm - diameter aluminum fl at punch and test surfaces), it was shown that the integration of multiple scales of compliant structures would lead to a signifi cant increase in the adhesion of the system. More recently, Northen et al. [106] reported a novel approach for a reversible adhesive system. Inspired by the Tokay gecko, a hierarchical system was fabricated which consisted of aligned vertical nanorods that coated fl exible micrometer - scale cantilever paddles made from nickel. The nickel - composed paddles were able to rotate when subjected to a magnetic fi eld, and this rotation resulted in changes in adhesion that could be both controlled and reversed. The fabrication of adhesives based on nonpolymeric materials has also been demonstrated. Zhao et al . [107] were able to fabricate a multiwalled carbon nano- tube (MWCNT ) - based dry adhesive over larger areas on Si substrates, by using chemical vapor deposition (CVD ). This led to the creation of adhesive strengths in the region of 10 N cm − 2 , comparable to the gecko ’ s foot, for macroscale adhesion. Zhao et al . described using a 2 × 3 mm 2 area of their adhesive to attach a toy bear (weighing 40 g) to a glass slide. Notably, the excellent thermally and electrically conducting properties of these adhesives permitted their use as unique interfacial materials with additional functionalities. Yurdumakan et al . [108] reported a fabrication process for constructing polymer surfaces with multiwalled carbon nanotube (MWCNT ) hairs which exhibited strong nanometer - level adhesion forces. Following the use of CVD to grow the MWCNTs on quartz or Si substrates, the structures were transferred into a PMMA matrix and subsequently exposed on the surface, after solvent etching. When the adhesive behavior of the MWCNT brushes was measured using multimode 414 11 Biomimetic Artifi cial Nanostructured Surfaces

scanning probe microscopy ( SPM ), the adhesive forces measured on the surfaces were 200 - times higher than are found in gecko foot - hairs. Mahdavi et al . [109] developed a biocompatible and biodegradable elastomer, for a tissue - compliant synthetic gecko - inspired adhesive that might be useful for a range of medical applications. After using the biocompatible polymer poly(glycerol - co - sebacate acrylate), molding was employed to modify the surface to mimic the nanotopography of gecko feet. Coating the nanomolded pillars of biodegradable elastomers with a thin layer of oxidized dextran led to a signifi cant increase in interfacial adhesion strength on porcine intestine tissue in vitro , and in the rat abdominal subfascial in vivo . The in vivo characterization of implanted gecko tapes demonstrated a minimal tissue response. This strategy might provide an effective method for the development of tissue adhesives that could provide a platform for many practical and useful additions to the surgical armamentarium.

11.3.3 Optical Properties of Biomimetic Artifi cial Nanostructures

11.3.3.1 Structural Coloration The morpho - butterfl y wing refl ects interfered brilliant blue, which originates from nanostructures on its scales, for any incident angle of white light. In a study conducted by Watanabe et al. [110] , brilliant blue was observed from a morpho- butterfl y - scale quasi - structure on diamond - like carbon ( DLC ). The biomimetic structures were fabricated using focused ion beam- chemical vapor deposition ( FIB - CVD ), and the refl ection spectra of the quasi- structures were very similar to those of morpho - butterfl y scales. Both, the natural and artifi cial surfaces had a wavelength with peak intensity near 440 nm, and intensity curves of very similar shape for various incident angles of light. Zhang et al. [111] fabricated biomimetic oxide replicas with structural color using butterfl ies (Ideopsis similis) as templates. The butterfl y wing scale templating procedure provided a simple method for the synthesis of hierarchically periodic ZnO material. The biomorphic 3 - D porous structures maintained the microstruc- tural features of the original butterfl y wing scale and membrane morphology, down to the sub - micrometer level. Gu et al . [112] were able to combine structural color and super - hydrophobicity when they demonstrated a convenient method of fabricating uniform inverse opal fi lms on glass substrates, with a nanostructured surface (Figure 11.14 a). The resulting 3- D - ordered structures contributed to the stop band. Incident light with a wavelength identical to the position of the stop band was refl ected (Figure 11.14 c) and, as a result, the inverse opal fi lms exhibited brilliant colors when their stop

Figure 11.14 (a) SEM image of an inverse structural periods. The center- to - center opal fi lm with a center - to - center distance distances between two neighboring holes between neighboring holes of 275 nm. were 275, 310, and 400 nm, respectively. Pictures (b) and transmission spectra (c) of Reproduced with permission from Ref. [112] ; three types of inverse opal fi lm with different © 2003, Wiley - VCH. 11.3 Fabrication of Biomimetic Artifi cial Nanostructures 415

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80 275 310 400

60 (au) R 40

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0 400 500 600 700 800 l (nm) 416 11 Biomimetic Artifi cial Nanostructured Surfaces

bands fell into the visible region (Figure 11.14 b). Moreover, the color could easily be engineered to range from blue to red by changing the size of the polystyrene spheres during the fabrication process. Super -hydrophobicity was achieved simul- taneously by the deposition of fl uoroalkylsilane on the surfaces.

11.3.3.2 Iridescence and Chiral Refl ectors Many birds, insects (particularly butterfl ies and beetles), fi shes and lesser - known marine animals exploit photonic nanostructures on their surfaces to make their color change with viewing angle (iridescence) and/or appear “ metallic ” [35] . In a study conducted by Vigneron et al . [113] , a multilayer of alternating thick silicon monoxide plates and thin nickel layers was designed with the aim of pro- viding the same visible light fi ltering as the ventral segments of the metallic woodboring beetles (Figure 11.15 a). In the artifi cial multilayer, normal incidence led to a red refl ectance, while higher incident angles led to yellow and green col- orations (Figure 11.15 b,d). This correctly matched the optical behavior of some parts of the exocutile of Chrysochroa vittata (Figure 11.15 b,c). Deriving inspiration from the Manuka beetle, De Silva et al . [114] deposited chiral titanium oxide on textured Si substrates to produce wide - angle refl ectors by using electron - beam deposition. In this case, when the optical properties the natural and nanoengineered chiral coatings were compared they were found to be optically equivalent. De Silva et al. were also able to fabricate Bragg refl ectors for elliptically polarized light, by depositing alternately thin layer components of a chiral titanium oxide medium and a birefringent titanium oxide medium.

11.3.3.3 Antirefl ection Coatings Huang et al . [115] reported the fabrication of antirefl ection nanostructures by replicating fl y eyes. The fi ne structure of the household fl y compound eye was carefully examined, and the entire confi guration was replicated on alumina through a low - temperature atomic layer deposition ( ALD ) process. The same structure was achieved by removing the fl y compound eye template at high temperature, such that the alumina coating crystallized simultaneously. By measuring the refl ective spectra, the alumina replica of a fl y eye was shown to serve as an effi cient antirefl ecting structure of visible light, at an angle of up to 80 ° . Biomimetic antirefl ective Si nanopillar arrays were fabricated by Xu et al . [116] , who combined the self - assembly of polymer spheres into 2 - D arrays with RIE, to generate Si structures that greatly suppressed the refl ectivity of Si. A refl ectance of less than 10% in the 600 – 1300 nm wavelength range was reported in this case. Min et al. [117] developed a technique for producing subwavelength antirefl ection coatings on Si and glass substrates, based on RIE and soft lithography replication. The high -aspect ratio pillar arrays fabricated in this way exhibited excellent broad- band properties, with a refl ectance of less than 2.5% for a wavelength range of 300 to 1700 nm being reported for Si. For glass pillars, refl ectance in the visible spectral range was less than 0.5%. The patterned surfaces were then modifi ed with fl uor- osilane to obtain super - hydrophobic behavior. The antirefl ection properties, com- 11.3 Fabrication of Biomimetic Artifi cial Nanostructures 417

(b) (a)

2 μm

(c) (d) 1200 80 q = 0° 1000 70 q q q = 30° 60 = 30° = 0° 800 50 q = 75° 600 40 400 q = 75° 30 20 200 Reflection factor (%) Reflection factor (%) 10 0 0 450 500 550 600 650 700 400 500 600 700 800 Wavelength (nm) Wavelength (nm) Figure 11.15 (a) SEM image of the surface of specular direction, for three incidence angles. the cuticle of Chrysochoa vittata (inset), The strong refl ection band shifts from red to consisting of a stack of about 20 planar slabs green as the angle of incidence is increased; of chitin, with a refractive index of 1.56; (d) Measured refl ected intensities from the (b) The artifi cial surface and the ventral surface of the artifi cial iridescent plate segments of the carapace of C. vittata , viewed fabricated to match the optical properties of together under two incidences. Under normal the beetle C. vittata . The dominant wavelength incidence (above), the surface refl ects red sweeps a large part of the visible spectrum light, while under a larger incidence angle when the angle of incidence is varied. (below), the coloration turns to green; Reproduced with permission from Ref. [113] ; (c) Spectrum of light refl ected from the © 2006, American Physical Society. ventral side of the body of C. vittata in the

bined with an improved wetting response, highlight the possibility of creating multifunctional surfaces via this processing technique. Moth eye- type structures were fabricated on Si by Huang et al . [118] . For this, aperiodic arrays of Si nanotips (Figure 11.16 a,b) over extended areas were obtained using electron cyclotron resonance (ECR ) plasma etching with various reactive gases [silane (SiH 4 ), methane (CH4 ), hydrogen (H2 ) and argon (Ar)]. The resulting surfaces were capable of suppressing the refl ection of light near zero at a range of wavelengths from the UV, through the visible part of the spectrum, to the tera- hertz region (Figure 11.16 c,d). A reduced refl ection was observed for a wide range of angles of incidence, and for both s- and p- polarized light. The antirefl ective 418 11 Biomimetic Artifi cial Nanostructured Surfaces

(a) (b)

200 nm 100 nm

(c) (d) Wavelength (cm–1) 4,000 3,000 2,000 1,000 500 100 100 80 80 60 40 60 1 40 0.1 Reflectance (%) Reflectance (%) 20 0.01 0.001 0 0.5 1.0 1.5 2.0 2.5 5 101520 Wavelength (μm) Wavelength (μm) Figure 11.16 SEM images showing (a) a Si nanotips (symbols), as a function of cross - sectional view and (b) a tilted top view wavelength for unpolarized light at of Si nanotips; (c) Comparison of the wavelengths between 2.5 and 20 μ m for four specular refl ectance from planar Si wafer different values of angles of incidence: 30 ° (symbols) and Si nanotips (solid lines), as a (black), 60 ° (green), 75 ° (blue) and 80 ° function of wavelength for unpolarized light (red). The direction of the arrows indicates at wavelengths below 2 μ m for four different the variation in refl ectance as the angles of values of angles of incidence: 5 ° (black), incidence were increased. Reproduced with 30 ° (green), 45 ° (blue) and 60 ° (red); permission from Ref. [118] ; © 2007, npg (d) Comparison of the specular refl ectance publishing. from a planar Si wafer (solid lines) and

properties of the surface were attributed to changes in the refractive index caused by variations in the height of the Si nanotips. The bioinspired antirefl ection coatings mentioned above suppress optical trans- mittance along with refl ectance. Lohm ü ller et al . [119] developed biomimetic sur- faces for the fabrication of highly transmissive, antirefl ective optical interfaces, which exhibited high -performance optics in the deep- UV range. For this, the sur- faces were prepared by self -assembly - based nanolithography and RIE on fused silica, and the antirefl ective properties of the structures were demonstrated using both transmission and refl ection measurements for wavelengths ranging from deep - UV to IR, and at oblique angles of incidence. When the applicability of the 11.4 Applications of Biomimetic Artifi cial Nanostructures 419 fabrication method was demonstrated for planoconvex fused silica lenses, it resulted in a substantial increase in the transmittance of light in the deep - UV region, between 185 and 300 nm. Min et al. [120] reported a bioinspired templating technique for fabricating moth - eye antirefl ection gratings on gallium antimonide substrates. In this case, non - close - packed colloidal monolayers were utilized as etching masks to pattern subwavelength- structured nipple arrays on GaSb. The resulting gratings exhib- ited broadband antirefl ective properties and thermal stability that were superior to those of conventional multilayer dielectric coatings. The specular refl ection of the templated nipple arrays was greatly suppressed as compared to the unstruc- tured GaSb wafer. It is most likely that these types of biomimetic coating will be of great technological importance in the development of effi cient thermophoto- voltaic cells.

11.4 Applications of Biomimetic Artifi cial Nanostructures

Since research into bioinspired interfacial materials is mainly driven by functional applications, biomimetic and bionspired approaches for the fabrication of func- tional materials would be expected to rate among the most promising scientifi c strategies in the coming years.

11.4.1 Wetting Applications

When the Lotus - Effect ® was fi rst trademarked, intense interest was drawn towards its commercial exploitation for the fabrication of self - cleaning products for everyday life applications. Clearly, fabricated surfaces that would remain dry and clean, in the same way as the lotus leaf, could be used for products ranging from self - cleaning coatings, paints, roof tiles and water - repellent textiles to applications relevant to anti -bouncing additives for pesticides [121] . Many of these ideas have been already commercialized; examples include facade paints, coatings for the reduction of biodeterioration, coatings for self - cleaning glasses, sprays for generating self - cleaning fi lms and nanoparticle powders for multipurpose applications, including containers that can be emptied without residues [14] . The ability to switch reversibly between hydrophobic and hydrophilic states, or to induce changes in the hydrophobic/hydrophilic properties of a surface under the infl uence of an electric potential, light irradiation or temperature, represents an important area of wettability applications. External stimuli as such, provide the ability to switch between the Cassie and Wenzel states. Both, Krupenkin et al . [122] and Bhushan [123] et al. for example, reported that droplet behavior could be reversibly switched between the super -hydrophobic Cassie state and the hydrophilic Wenzel state, by the application of an electrical voltage and current 420 11 Biomimetic Artifi cial Nanostructured Surfaces

(electrowetting). Changes to the external stimuli in any of these approaches may lead to a change in the surface energy and, thus, to a transition from a hydrophobic to hydrophilic state (and vice versa). At least potentially, these mechanisms could be used to promote energy conversions in applications such as bio - microelectro- mechanical systems ( MEMS ) or lab - on - the - chip devices, where autonomous sources of energy are required. The ability of a super- hydrophobic surface to retain air when immersed in water leads to a number of potential applications. One such area is related to the drag reduction of an underwater vessel (e.g., a submarine). Resistance to fl ow can be reduced signifi cantly by liquid slip, which is a characteristic of super - hydrophobic surfaces. Surface roughness can increase the ability of a surface to retain air and form a composite interface which can in turn reduce water friction with the walls of a channel. In addition to drag reduction, a super - hydrophobic surface may also protect against marine fouling, and thereby play a role in the defense against adhesion and the growth of marine organisms [57] . Super - hydrophilic surfaces have been considered as an alternative route to self- cleaning applications. The concept is based on the self - cleaning of windows through fi lm or fl uid fl ow, with studies focusing primarily on photoresponsive

materials such as TiO 2 . The main advantage of these surfaces is their combined hydrophilicity –photodegradation effect, which aids signifi cantly in the cleaning process [58] . Although the super - hydrophilic effect is reversible in principle, the aging of these surfaces under real conditions may be an issue in this respect. A combination of optical transparency along with an induced super - hydrophilicity on the surfaces might fi nd use in antifogging applications. The controllable manipulation of liquids has also been considered for the devel- opment of droplet - based microfl uidics and lab- on - chip devices. In this case, the process can be used to effi ciently drive drops to specifi c sites, in order to perform discrete functions such as mixing, analysis, reaction, and storage. Driving the liquid along the channels and forcing them to merge at predefi ned locations offers a novel means of mixing reactants or steering biochemical reactions – defi ning exactly the concept of a “ liquid microchip. ”

11.4.2 Adhesion Applications

Engineered adhesive nanostructures inspired by biological systems such as the gecko foot and mussel attachments are today under consideration as the “ next - generation ” adhesives [124] . The ability to achieve dry adhesion could be imple- mented in many applications, ranging from everyday consumer objects such as tapes, fasteners and toys, to microelectronic and space applications, and even wall - climbing robots [5] . Geckel nanoadhesives which can adhere effectively and revers- ibly to surfaces under water may be used in the design of wet, temporary adhesives for industrial consumer, military, and medical surfaces [105] . Within the medical arena there is a signifi cant need for tough, biodegradable polymeric adhesives that can both adapt to and recover from various mechanical 11.5 Conclusions and Future Outlook 421 deformations, while remaining strongly attached to an underlying tissue. The implementation of existing gecko -inspired adhesives for medical applications is complex, however, as multiple parameters must be optimized, including: biocom- patibility, biodegradation and strong adhesive tissue bonding, as well as compli- ance and conformability to the tissues [109] . Gecko- inspired medical adhesives might be used for sealing wounds and as a replacement or augmentation of sutures or staples. Such adhesives might also be used to deliver drugs or as growth factors in order to promote the healing process.

11.4.3 Optical Applications

Bioinspired surfaces with structural color may fi nd application in the fi elds of nanomaterials and optical devices, or they may even serve as a paradigm for the next generation of decorative materials [112] . Iridescent structures might even fi nd a role in the anti - counterfeiting industry [125] , with the recent development of devices having different degrees of sophistication, ranging from effects that are discernable by eye to fi ne - scale optical characteristics (e.g., polarization and angular properties) that can be read only by specialized detectors. Interestingly, the fact that the range of refractive indices available in artifi cial structures is much wider than those found in natural surfaces, has created interest in extending the use of these to more diverse fi elds such as paints, printing, cosmetics, and clothing [35] . Biomimetic antirefl ective structures might also fi nd application in optical and optoelectronic fi elds, to improve the performance of photon- sensitive devices [116] . Moth eye- type structures that provide broadband anti- refl ective properties might have applications in renewable energy and electro - optical devices for the military [118] . Although antirefl ection coatings are commonly used to suppress the refl ec- tion of light from the surfaces of optical components, they also reduce the essential transmission of light which, for some applications, is of major technological importance. For example, the fabrication of highly light - transmissive, antirefl ec- tive optical materials could be used for display panels and for projection optics, as well as for heat - generating microscopic and laser applications [119] .

11.5 Conclusions and Future Outlook

In this chapter, the exciting properties of micro - and nanopatterns found on bio- logical surfaces, the principal approaches used to fabricate biomimetic artifi cial nanostructured surfaces, and their current and potential applications have been reviewed. Emphasis has been placed on the fact that biological tissues and surfaces exhibit an hierarchical organization which is a consequence of evolutionary demands to control processes at several scale levels. In particular, it has been stressed that biological surfaces hide a virtually endless potential of technological ideas for the development of new materials and systems. Due to the diversity of 422 11 Biomimetic Artifi cial Nanostructured Surfaces

functions, inspiration from biological surfaces might prove interesting for a broad range of topics in engineering sciences, including adhesion, friction, wear, lubrica- tion, fi ltering, sensorics, wetting phenomena, self- cleaning, antifouling, ther- moregulation, and optics. Moreover, the fact that all biological surfaces are multifunctional makes them even more interesting from the point of view of biomimetics. Although current fabrication techniques of biomimetic surfaces are valuable within a limited range of functions, future engineering methods must interlace multiple functionalities with exceptional controllability. For example, precision control over different size scales – that is, the tailored fabrication of nanofeatures imprinted on the surface of 3 - D microfeatures – will be required to mimic the complex hierarchical structure and functionality of natural surfaces. Clearly, this represents one of the greatest challenges of these technologies towards engineer- ing truly biomimetic, hierarchically structured artifi cial surfaces, in order to take full advantage of the potential for nanofeature incorporation. In addition to con- ventional engineering approaches, a number of other strategies for biomimicry have recently emerged, and might potentially be exploited to expand the breadth and novelty of applications. Efforts to understand and control biomolecular self - assembly, phase separation, confi nement, chirality in complex systems, as well as the use of genetically engineered proteins for inorganics, should provide additional routes. Furthermore, the ability to harness the nanoengineering effi ciency of living cells so as to create biomimetic materials via cell culture techniques [35] shows much promise. There is no doubt that each of these possibilities requires further development before it can be at all competitive. Nonetheless, the extreme range of technical applications for biomimetic artifi cial surfaces and the number of emerging new interdisciplinary, biomimicking approaches suggest a future where the control of artifi cial biomaterial structures and their subsequent functionality might be accomplished with a sophistication that cannot presently be envisaged. It is most likely that the coming years will belong primarily to the fi eld of bio- inspired multifunctional surfaces, as topics such as understanding intelligent biological functions and the development of responsive biomimetic artifi cial mate- rials are still in their infancy. One major problem to overcome is that intelligent natural structures do not always function in a unique way, but rather adapt to local functional requirements – even the simplest plants and animals “ sense ” their world, integrate the information, and respond accordingly. Feedback - control mechanisms are extremely important features that endow organisms with fl exibil- ity and robustness. For example, despite lacking a nervous system, a plant can grow leaves and branches towards the light, roots towards water, or spatially regu- late growth so as to minimize mechanical stress. In this respect, the functions of biological structures cannot be fully understood, nor accurately mimicked, without taking this complex dynamic feedback into account. Research into intelligent biomimetic surfaces, combined with the principles of evolution for optimization, should give rise to multifunctional materials surfaces that currently remain beyond the grasp of humankind. No doubt this is, and would be, an excellent example of biologically inspired science. References 423

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