Rice and Butterfly Wing Effect Inspired Low Drag and Antifouling Surfaces

Critical Reviews in Solid State and Materials Sciences, 40:1–37, 2015 Copyright Ó Taylor & Francis Group, LLC ISSN: 1040-8436 print / 1547-6561 online DOI: 10.1080/10408436.2014.917368

Rice and Butterﬂy Wing Effect Inspired Low Drag and Antifouling Surfaces: A Review

Gregory D. Bixler and Bharat Bhushan* Nanoprobe Laboratory for Bio & Nanotechnology and Biomimetics (NLB2), The Ohio State University, 201 W. 19th Avenue, Columbus, Ohio 43210, USA

In this article, a comprehensive overview of the reported rice and butterfly wing effect discovered by the authors is presented with the hope to attract and inspire others in the field. Living nature has inspired researchers for centuries to solve complex engineering challenges with much attention given to unique structures, materials, and surfaces. Such challenges include drag reducing and antifouling surfaces to save energy, lives, and money. Many flora and fauna exhibit low drag and antifouling characteristics, such as shark skin and lotus leaves, due to their hierarchical microstructured morphologies. The authors have reported that rice leaves and butterfly wings combine the shark skin (anisotropic flow leading to low drag) and lotus leaf (superhydrophobic and self-cleaning) effects, producing the so-called rice and butterfly wing effect. Such surfaces have been fabricated with photolithography, soft lithography, hot embossing, and coating techniques. Fluid drag, anti-biofouling, anti- inorganic fouling, contact angle, and contact angle hysteresis results are presented to understand the role of sample morphology. Conceptual modeling provides design guidance when developing novel low drag and antifouling surfaces for medical, marine, and industrial applications.

Keywords shark skin, rice leaf, lotus effect, butterﬂy wing, low drag, antifouling

Table of Contents

1. INTRODUCTION...... 2 1.1. Examples in Living Nature...... 4 1.2. Commercial Approaches...... 5 1.3. Overview...... 5

2. DRAG AND ANTIFOULING MECHANISMS...... 6 2.1. Drag Mechanisms ...... 6 2.2. Fouling Formation ...... 6 2.2.1. Biofouling...... 6 Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 2.2.2. Inorganic Fouling ...... 7 2.3. Self-cleaning Mechanisms...... 7

3. INSPIRATION FROM LIVING NATURE ...... 8 3.1. Ambient Species...... 8 3.2. Aquatic Species...... 8 3.3. Rice and Butterﬂy Wing Effect ...... 9

4. SAMPLE FABRICATION...... 10 4.1. Fabrication of Replicas ...... 10 4.1.1. Urethane Soft Lithography and Coating Procedure ...... 10 4.2. Rice Leaf Inspired Surfaces ...... 10

*E-mail: [email protected] Color versions of one or more ﬁgures in the article can be found online at www.tandfonline.com/bsms.

1 2 G. D. BIXLER AND B. BHUSHAN

4.2.1. Silicon Master Patterns...... 11 4.2.2. PDMS Soft Lithography procedure ...... 12 4.2.3. Hot Embossing Procedure...... 12

5. EXPERIMENTAL PROCEDURES...... 12 5.1. Pressure Drop Measurements...... 12 5.1.1. Predicting Closed Channel Pressure Drop...... 13 5.2. Antifouling Experiments...... 14 5.2.1. Anti-biofouling ...... 14 5.2.2. Anti-inorganic Fouling...... 14 5.3. Wettability...... 15 6. RESULTS AND DISCUSSION...... 15 6.1. Sample Characterization ...... 15 6.1.1. Actual, Replica, and Rice Leaf Inspired ...... 15 6.2. Pressure Drop Measurements...... 16 6.2.1. Water Flow ...... 17 6.2.2. Oil Flow ...... 18 6.2.3. Air Flow ...... 19 6.2.4. Non Dimensional Pressure Drop Model ...... 19 6.3. Antifouling Experiments...... 21 6.3.1. Anti-biofouling ...... 22 6.3.2. Anti-inorganic Fouling...... 25 6.4. Wettability...... 27 6.4.1. Actual, Replica, and Rice Leaf Inspired Samples...... 27 6.4.2. Wettability, Drag, and Antifouling ...... 29 6.5. Models for Low Drag and Antifouling...... 29 6.5.1. Low Drag Models...... 29 6.6. Antifouling Models ...... 32

7. CONCLUSIONS...... 33 FUNDING...... 34

REFERENCES...... 34

1. INTRODUCTION height and width are non dimensional lengths of a rectangle. A Optimized designs to conserve precious resources using rectangle produced using the Golden Ratio is called the routine materials and fabrication processes are key attributes Golden Rectangle, and for example describes the shape of the found throughout living nature. Therefore, researchers are Milky Way galaxy. Even famous artists have included the Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 constantly seeking living nature for inspiration. Various flora Golden Ratio in their own works, such as Leonardo da Vinci’s and fauna have been studied with much attention given to “Mona Lisa”, as shown in Figure 2. Furthermore, Fibonacci nature’s structures, materials, and surfaces. Shown in Figure 1 numbers and the Fibonacci spiral describe geometries of various are various examples including wall-climbing robots inspired structures found in nature. For example, this includes the number by Gecko feet, low drag, and antifouling surfaces inspired by and sequence of patterns on pineapples and sunflower heads as shark skin, high strength rope inspired by spider webs, flying well as the number of petals on flowers. The Fibonacci numbers machines inspired by birds, anti-reflective surfaces inspired by are described with the mathematical expression Fn D Fn-1 C Fn-2 moth eyes, and “self-cleaning” windows inspired by the super- starting with F0 D 0andF1 D 1 that provides the sequence of hydrophobic lotus leaf (Nelumbo nucifera).1–9 values 0, 1, 1, 2, 3, 5, 8, 13, 21, 34, ...and so on.10,12 Unlocking the secrets of nature has led researchers to study Two properties of commercial interest are fluid drag reduc- the Golden Ratio and Fibonacci numbers – which describe tion13-17 and antifouling.5,6,18–25 Drag is the resistant force unique patterns found throughout the universe.10–12 The against an object moving through the fluid, and is generally Golden Ratio is considered ideal from functionality/aesthetics higher in turbulent vs. laminar fluid flow.26 Biofouling is the height : accumulation of undesired biological matter on hard surfaces, standpoint and is defined as width 1 618 where the values LIVING NATURE INSPIRING BIOMIMETICS 3

FIG. 1. Montage of examples from living nature that have inspired researchers seeking new bioinspired products (adapted from Bhushan3). Shown are (a) water droplet on a self-cleaning lotus leaf and its micropapillae, (b) glands of carnivore plant that traps insects, (c) water strider walking on water and its leg structures, (d) Gecko feet spatula with reversible adhesion, (e) riblet covered low drag and antifouling shark skin, (f) bird wing structure and orientation during landing approach, (g) spider webs made of silk stands, and (h) anti-reﬂective moth eyes. Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

with biofilms created by microorganisms and macroscale bio- includes biofilms often leading to macrofouling19–23 and inor- fouling (macrofouling) created by organisms (for instance, ganic fouling.18,32–35 Shown in Figure 3 is a biofilm on a pace- barnacles). Inorganic fouling includes deposits of dirt, corro- maker wire removed from a patient and barnacles on a flat plate sion, crystals, suspended particles, oil, and ice. The type and representing macrofouling on underwater structures. Inorganic extent of fouling depends on the environment, inorganic fouling examples are shown with dirt deposits on stucco and crys- deposits, and organisms present.25 The term fouling describes tallization fouling on a heat exchanger. Antifouling may also be both biofouling and inorganic fouling, where antifouling is the accomplished through self-cleaning, where undesired liquids or prevention of any biological or inorganic fouling. Conversely, contaminants are removed from a surface in a fluid flow. self-cleaning is the removal of fouling already deposited on a Numerous engineering applications can benefit from low surface. drag and antifouling surfaces. Examples include airplanes,36 Medical, marine, and industrial fouling often exhibits different wind turbines,37 ship hulls,38 implanted medical devices,30 characteristics. For instance, medical fouling includes bio- heat exchangers,39 and pipelines.20 Low drag surfaces often films,27–31 whereas marine and industrial biofouling typically equate to less fouling by washing away any contaminants 4 G. D. BIXLER AND B. BHUSHAN

present, which often leads to energy conservation.6,24,25,40 Fur- thermore, anti-ice fouling may be accomplished with water repellent surfaces, which is beneﬁcial for airplane wings, heli- copter blades, oil platforms, power lines, locks and dams, and wind turbines.41,42

1.1. Examples in Living Nature Many flora and fauna flourish due to their low drag and antifouling properties, with commonly studied examples including shark skin and lotus leaves. The skin of fast swimming sharks is both low drag and antifouling; and lotus leaves are antifouling via self-cleaning.5,43–45 Sharks remain clean due to their microstructured riblets, flexion of dermal denticles, and a mucous layer.1,46–50 Lower drag is necessary for shark survival, since it allows sharks to swim faster in order to catch prey.47,48,50,51 Increased fluid flow velocity at the skin reduces microorganism settlement time and promotes antifouling,44,45,49 along with riblet spacing smaller than microorganisms.5,52–55 Conversely, lotus leaves repel water droplets and provide self-cleaning by removing unwanted contaminants.22,43 Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

FIG. 2. Montage of images showing examples of the Golden Ratio, Golden Rectangle, and Fibonacci numbers found in nature and art (adapted from Bixler and FIG. 3. Biological and inorganic fouling examples. Biofoul- Bhushan57). Examples include galaxies, sunflower heads, ing examples are shown with a biofilm covered pacemaker flower petals, sea shells, Mona Lisa painting, and pineapple wire (adapted from Marrie and Costerton84) and barnacles on fruit (from top left to bottom right). The Golden Rectangle a flat underwater plate (adapted from Edgar133). Inorganic and Fibonacci or Golden spiral are superimposed on select fouling examples are shown with dirt deposits on a stucco images. Such proportions and patterns are considered aes- building exterior (photo courtesy of www.stocorp.com) and thetically pleasing and are believed to enhance performance crystallization on the outside of heat exchanger tubing (photo of systems found throughout nature. courtesy of H&C Heat Transfer Solutions, Inc). LIVING NATURE INSPIRING BIOMIMETICS 5

Inspired by shark skin and lotus leaves, Bixler and Both shark skin50,52,53,62,70 and rice leaf inspired40,56–59 Bhushan40,56–58 found rice leaves and butterfly wings combine antifouling topographical features include micro-sized pillars, the shark skin and lotus effects. It is reported that sinusoidal ribs, and a combination thereof using various dimensions. Sur- grooves in rice leaves and aligned shingle-like scales in butter- faces with appropriately sized topographies prevent coloniza- fly wings provide the anisotropic flow. Hierarchical structures tion by various microorganisms including Ulva spores, consisting of micropapillae superimposed by waxy nanobumps Balanus Amphitrite cyprids,52,53,62 and E. coli (Escherichia in rice leaves and microgrooves on top of shingle like scales in coli).59 Up to 85% spore settlement reduction is reported with butterfly wings provide the superhydrophobicity and low adhe- micro-sized ribs when compared to flat control samples53,62 sion. Various studies suggest that this combination of aniso- (E. coli antifouling is reported in detail in Section 6.3.1). tropic flow, superhydrophobicity, and low adhesion leads to Antifouling is attributed to the micro-sized feature spacing improved drag reduction and antifouling.40,57–59 The concept that is slightly smaller than the microorganisms under investi- of superhydrophobic parallel grooved surfaces with aniso- gation52,53,62 as well as presence of sharp edged dis- tropic wetting behavior have been reported, but not to the continuities.59 The so-called engineered antifouling micro- same degree as described in this article and previous articles topographies are designed to target specific microorganisms by the same authors. based on their shape and size.53 Fabricating inexpensive, drag reducing, and antifouling rice leaf inspired surfaces was demonstrated by embossing patterns 1.2. Commercial Approaches onto flexible polymer films.58,59 Such films could be applied to Living nature has inspired the development of shark skin and flatorcurvedsubstratessuchaspipelineinteriors,airplane lotus leaf inspired low drag and antifouling products. Drag wings, and ship hulls. Hot embossing was conducted with a mas- reducing products include shark skin inspired 3M Corp. experi- ter mold heated and pressed into the polymer film. Fabricating mental vinyl sawtooth riblets60 and Speedo FastSkinÒ fabric embossed surfaces has been the subject of several studies58,71,72 racing swimsuits. Reportedly, 3M riblets reduce water drag by and techniques depend on the type of master mold and molding 13%50 and Speedo swimsuits by 4%.61 Antifouling product materials. Commonly, the master mold is silicon71,73 and the examples include the shark skin inspired SharkletTM microtex- molding material is polymethylmethacrylate (PMMA).58,71,74–77 tured pattern.52,54,55,62 Furthermore, self-cleaning products Embossing can be used to fabricate various structures including, include hydrophobic paints, roof tiles, and fabrics as well as for example, microfluidic flow channels,77–79 plastic micro- hydrophilic windows and membranes. Examples include chips,74 and moveable microstructures.76 Such components are LotusanÒ paints by Sto (www.stocorp.com), Erlus LotusÒ roof reported to yield sub-micron scale features.75,80 tiles (www.erlus.com), NanoSphereÒ fabrics by Schoeller Technologies (www.schoeller-textiles.com), and SunCleanÒ glass by PPG Industries (www.ppg.com). Self-cleaning hydro- 1.3. Overview philic SunCleanÒ glass with titanium dioxide uses the sheeting A comprehensive overview of the reported rice and butter- action of water to efficiently gather and remove contaminants fly wing effect discovered by the authors is presented with the (www.ppg.com).40 hope to attract and inspire others in the field. Included are Multiple coatings and antifouling techniques have been many related works in the field of drag reduction and antifoul- reported for engineering applications. In the medical industry ing by the authors and others to compile all of the learnings these often include hydrophobic polymers with antimicrobial into one document. This creates a comprehensive overview of properties.25,63 Example applications include catheters, endo- the rice and butterfly wing effect by combining previously 64 30

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 tracheal tubes, and orthopedic hip implants. In the marine published papers along with new related discoveries. Results environment, common tributyltin coatings were banned by the from experiments are reported investigating actual and replica International Maritime Organization, adding urgency to the rice leaves, butterfly wings, fish scales, and shark skin as well development of more environmentally friendly antifouling as rice leaf inspired samplescombined with various coatings and foul-release coatings. As a result, researchers have been that provide superhydrophobicity, superoleophilicity, and exploring environmentally friendly methods such as new non- superoleophobicity. Samples were fabricated via photolithog- toxic antifouling paints and foul-release coatings.19,21,23,65 As raphy, soft lithography, and hot embossing techniques. A for industrial antifouling, applications such as food processing series of investigations highlighting the rice leaf inspired sam- require different approaches. For example, antifouling success ples is presented describing drag reduction and antifouling is reported with titanium dioxide nanoparticles on reverse effectiveness. The rice leaf inspired embossed sheets are eval- osmosis membranes66 and antimicrobial silver nanoparticles uated and their characteristics compared to samples fabricated on ultrafiltration membranes.67 Even though fouling preven- by soft-lithography methods, in order to demonstrate the tion is the goal, often fouling must be cleaned using various potential scaled up production. Drag results are presented methods such as scrubbing, chemical disinfection, high-pres- from experiments using closed channel water, oil, and air lam- sure water spray, and membrane back washing.20,23,25,31,68,69 inar through turbulent flowwhich simulates conditions in 6 G. D. BIXLER AND B. BHUSHAN

medical, marine, and industrial applications. Antifouling is transition occurs around Re D 2300 for closed channel and reported from anti-biofouling and anti-inorganic fouling Re D 500,000 for open channel ﬂow.16,81 experiments using bioassay and self-cleaning techniques, respectively. Results are discussed and conceptual models are 2.2. Fouling Formation provided suggesting the effectiveness of rice and butterﬂy In this section, we explain fouling types and the formation wing effect surfaces on drag reduction and antifouling. process of both biofouling and inorganic fouling.

2. DRAG AND ANTIFOULING MECHANISMS 2.2.1. Biofouling In this section, we first present fluid drag mechanisms, which include pressure and skin friction drag in laminar and turbulent The general principles of biofouling formation and factors leading to the settlement on surfaces are similar in medical, flows.We alsopresent biologicalandinorganic foulingtypesand 18,20,21,25,27,31,82,83 formationaswellasself-cleaningmechanisms. marine, and industrial applications. Biofoul- ing morphology is characterized by the thickness, density, structure, composition, bioadhesive strength, and weight of 2.1. Drag Mechanisms 23,31,84–88 Fluid drag on any object is a combination of pressure and skin fouling organisms. During the biofouling process, 13–16,49,81 microorganisms colonize a surface and then attract macrofou- friction drag. Describing such drag is possible by imag- 21,83 ining wading through a pool of water. In this scenario, the lers. In biofilms, microorganisms adhere to one another and required energy to move water from the front to the back of one’s the substrate with an adhesive called the extracellular poly- legs leads to pressure drag. This drag may be reduced with meric substance (EPS). The biofilm continues to grow and streamlined shapes, such as airfoil designs common to aircrafts become more diverse by attracting microorganisms. Shown in and ships. Conversely, skin friction or viscous drag occurs due to Figure 4 is the five-stage colonization process, which includes the interaction of the closest fluid layer to one’s legs in water. initial attachment, irreversible attachment, initial growth, This drag is due to the attraction of fluid molecules to the surface, final growth, and dispersion. Initial attachment starts the coloni- which creates friction and thus resistance. Away from the surface zation process, which begins within days to a few weeks. the velocity of the molecules increases until the fluid achieves Initial attachment of microorganisms is reversible, but once the average fluid flow velocity. Higher viscosity fluids exhibit they secrete the EPS, the bond becomes irreversible. This per- manent attachment allows initial growth, final growth, and higher drag due to the greater attraction between fluid layers, 21,27,82,83 which then leads to increased skin friction.13–16,81 dispersion. Bioadhesion is important to consider for antifouling as it Laminar and turbulent boundary layers help describe fluid 21,27,82,83 flow, where turbulent boundary layers lead to higher skin fric- describes the adhesion strength to a surface. This tion drag. The boundary layer is the fluid layer adjacent to the strength depends on the organism type, substrate, and separat- ing fluid,89 due to influences of electrostatic forces and surface surface, with the innermost layer called the viscous sublayer. 54,90–92 In this layer, laminar flow appears smooth and orderly whilst wettability. The two-stage process starts with the initial turbulent flow appears random and chaotic. Additionally, lam- attachment and then the irreversible attachment. Initial attach- inar flow is controlled by viscous forces between the fluid mol- ment is controlled by a physical adhesion between the micro- ecules whereas turbulent flow is controlled by inertial organism and the substrate. Also known as adsorption, the forces.13,15,16 Turbulent vortices in the viscous sublayer natu- initial colonists attach to a surface through weak, reversible rally translate in the cross flow and streamwise directions, van der Waals bonds, which are slightly stronger than electro- which leads to vortices intermingling and ejecting from the static repulsive force. Irreversible attachment is accomplished with secretion of the EPS, which exhibits a sponge-like matrix. Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 viscous sublayer. This movement increases momentum trans- 26 This adhesive permanently bonds the microorganisms to one fer and shear stress, which results in higher drag. Therefore, 21,27,86 laminar flow is preferred for low drag; however, in many real- another and to the surface. world fluid flow applications, the boundary layers naturally transition from laminar to turbulent. The transition from laminar to turbulent flow may be described with the dimensionless Reynolds number (Re), which includes the fluid average flow velocity, fluid kinematic viscosity, and characteristic length which is the hydraulic diameter (for closed channel) or a distance downstream from the leading edge (for open channel). Transition from laminar to turbulent flow depends on the aforementioned parameters as well as surface roughness and freestream disturbances, where such features may FIG. 4. Biofilm development process. Schematic illustrates “trip” the boundary layer to become turbulent. Such the five stage colonization process (adapted from Monroe82). LIVING NATURE INSPIRING BIOMIMETICS 7

2.2.2. Inorganic Fouling unable to contact and gather contaminant particles that rest 57,58 Inorganic fouling is composed of non biological particles within the Cassie-Baxter regime air pockets. that may form in addition to or independently from biofoul- To further understand mechanisms behind liquid repellent ing.20,25,31,32 Types of inorganic fouling include particulate, surfaces, Young’s equations are useful to examine the roles of 56 freeze, and gas stream particulate. Particulate fouling occurs solid-air, solid-liquid, and liquid-air surface tensions. start, a when suspended solid particles deposit onto a surface, such as water droplet placed on a surface in air forms the solid-air- heat transfer tubing.93 Deposition of crystals from freeze foul- water interface and the droplet contact angle can be measured. ing occurs in locations such as cold region oil pipelines when The equation for the contact angle of a water droplet uW in air 98 waxy hydrocarbons contact cold pipe interior walls. Gas is predicted by Young’s equation: stream particulate fouling occurs in gas pipes, reactors, com- ¡ D gSA gSW ; bustion chambers, and heat exchangers. This includes mineral, cosuW (1) gWA organic, and inorganic particles, which are common in oil or 33 gas combustion systems. where gSA, gSW ,andgWA are the surface tensions of the solid- Biofouling may initiate inorganic fouling, where biocorro- air, solid-water, and water-air interfaces, respectively. Equation > : sion causes the formation of corrosion particles. Such fouling (1) predicts that hydrophilicity is possible when gSA gSW is prevalent in boilers, cooling condensers, desalination plants, However, the equation for the contact angle of an oil drop- food processing equipment, geothermal plants, and oil produc- let uO in air is predicted by Young’s equation: tion equipment.35 Heat exchangers can develop hard deposits ¡ D gSA gSO ; called “scale” or more porous deposits such as “sludge”.34 cosuO (2) gOA Inorganic fouling particles may also originate from corrosion, crystallization, suspended particles, oil, and ice. For instance, where gSA, gSO, and gOA are the surface tensions of the solid- salts from aqueous solutions crystallize and deposit on surfa- air, solid-oil, and oil-air interfaces, respectively. Equation (2) ces. Other deposits may result from minerals found in water predicts that oleophilicity in air is possible when 20,31,32 > such as magnesium, calcium, and barium. gSA gSOwhere the surface energy of a solid surface must be higher than the surface tension of the oil.99,100 Furthermore, the equation for contact angle of an oil droplet 2.3. Self-cleaning Mechanisms uOW in water is predicted by Young’s equation: Wettability plays an important role in antifouling via self- ¡ gSW gSO cleaning, for instance as found in nature with the water repel- cosuOW D ; (3) lent lotus leaf or water attracting pitcher plant surfa- gOW ces.3,5,91,94–96 In general, for liquid repelling surfaces, it is where gSW , gSO, and gOW are the surface tensions of the solid- necessary for the surface tension of the repelling surface to be water, solid-oil, and oil-water interfaces, respectively. Equa- lower than the liquid being repelled. Contact angle (CA) is the tion (30 predicts that oleophobicity underwater (at the solid- angle between the liquid and surface whilst contact angle hys- > : water-oil interface) is possible when gSO gSW teresis (CAH) is the difference between the advancing (down- As previously mentioned, Wenzel regime does not contain hill side) and receding (uphill side) contact angles. an air pocket at the liquid-solid interface unlike the Cassie- Furthermore, common wetting regimes include Cassie-Baxter Baxter regime. This difference inﬂuences the surface wettabil- (droplet sitting on top of asperities with air pocket) and Wen- ity since the air pockets encourage a larger contact angle u and zel (droplet penetrating gaps between asperities). High CAH smaller CAH. Equation (4) describes the Wenzel regime

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 and adhesion strength explains the deformed shape of a water u D u D 97 where contact angle, 0 contact angle of the droplet on droplet adhered to a vertical window. D D the flat surface, Rf roughness factor, AF flat projected With lotus effect, a high CA (>150 ) coupled with low D area, and ASL solid-liquid surface area, whereas Equation CAH (<10 ) repels many liquids and may remove contami- D 3,5,91 (5) describes the Cassie-Baxter regime with fLA fractional nant particles. With pitcher plant effect, a thin surface flat liquid-air contact area:5,97, water film encourages the sheeting or shearing effect which 96 may also remove contaminant particles. This effect occurs Wenzel : cosu D Rf cosuO (4) when water uniformly spreads and traverses the surface where R D A =A removing any contaminants, as compared to droplets beading f SL F up and rolling off with contaminants (i.e., lotus effect). Similar ¡ D ¡ . C :/ self-cleaning mechanisms are possible with a variety of Cassie Baxter : cosu Rf cosuO fLA Rf cosuO 1 (5) liquids, depending on the surface’s ability to repel or attract the liquids. In either case, self-cleaning is most effective when The contact angle of replica rice leaf, butterfly wing, fish the contaminant particles are sufficiently larger than the sur- scales, and shark skin samples is possible by using roughness face microstructures. For instance, the droplets would be factor and fractional liquid-air contact area values.40 8 G. D. BIXLER AND B. BHUSHAN

3. INSPIRATION FROM LIVING NATURE In this section, we explain characteristics and mechanisms of rice leaf, butterﬂy wing, ﬁsh scale, shark skin, and lotus leaf surfaces.

3.1. Ambient Species In the ambient environment, many surfaces including lotus leaves,3–5,43,97 rice leaves, and butterﬂy wings40 exhibit self- cleaning superhydrophobic and low adhesion characteristics. Shown in Figure 5 is a water droplet cleaning inorganic fouling from a lotus leaf surface. The lotus leaf relies on hierarchical micropapillae, which are described as microbumps superimposed with low surface energy waxy nanostruc- tures,22,43 which provide antifouling via self-cleaning properties. It should be noted that several other plant species also exhibit antifouling properties due to superhydrophobic and low adhesion characteristics, with the air pocket at the solid- liquid interface.3–5,43,97 In nature, rain droplets impact the lotus leaf surface and effectively roll off due to the water repellency. This leads to self-cleaning, where droplets collect and remove any contaminant particles, as illustrated in Figure 6 with the mercury droplet on a Taro leaf (which exhibits lotus effect characteristics). The lotus effect relies on roughness induced superhydrophobicity and low adhesion, where air pockets are present at the solid-liquid interface.3–5,43,97 Experiments with lotus effect surfaces show drag reduction in laminar,57,99,102 and turbulent ﬂows.57,102–105 Additionally, self-cleaning experiments show maximum contaminant removal of 99% for the lotus leaf replica.6

3.2. Aquatic Species In the aquatic environment, surfaces including shark skin46–50,70,106–109 and ﬁsh scales40,70 exhibit low drag and antifouling characteristics. Shown in Figure 5 is a comparison between barnacle covered whale skin and clean shark skin, even though both live in the same environment.50 Shark skin is designed with microstructured features (dermal denticles

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 covered by riblets) that effectively control naturally occurring turbulent vortices. Anisotropic flow characteristics of shark skin are due to riblet microstructures aligned in the swimming direction. The riblets reportedly lift and pin any vortices gen- erated in the viscous sublayerwhere lifting reduces the total shear stress and pinning reduces the cross-stream motion of FIG. 5. Biofouling in the marine environment (adapted from fluid and ejection of vortices from the viscous sublayer.46– Bixler and Bhushan40). Images highlight differences between 50,70,106–111 Shark skin effect flow visualization is shown in Humpback whales (adapted from www.southbank.qm.qld.gov. Figure 6, where smoke from atomized oil visually demon- au) and sharks. Even though whales and sharks live in the same strates the lifting and presumably pinning of the turbulent vor- environment, barnacle biofouling growth is evident on the tices,108 which leads to lower drag and antifouling. whale but not shark skin. Reportedly such antifouling shark In addition to shark skin in the aquatic environment, skin properties are due to its riblet microtexture, flexion of certain fish (for example rainbow trout) exhibit low drag in scales, and a mucous layer. Bottom image illustrates the lotus- order to presumably better navigate fast moving streams.40 effect with a water droplet removing contaminant particles Fish are covered with oriented scales that promote from the lotus leaf (adapted from http:jncc.defra.gov.uk). LIVING NATURE INSPIRING BIOMIMETICS 9

3.3. Rice and Butterfly Wing Effect Bixler and Bhushan40,56–58 reported that rice leaves and butterfly wings combine the shark skin (anisotropic flow leading to low drag) and lotus (superhydrophobic and self-cleaning) effects. The combination of anisotropic flow, superhydrophobicity, and low adhesion is reported to reduce drag and facilitate antifouling.40,57 It is believed that since rice plants thrive in humid, marshy environments, self-cleaning prevents unwanted fouling, which may inhibit photosynthe- sis.40 Since butterflies are fragile and unable to clean their wings, these properties are critical to maintain structural color- ation and flight control.113 Shown in Figure 7 are actual rice leaves and butterfly wings that exhibit unique water repellency and anisotropic flow characteristics, where droplets roll down the blade of the rice leaf and axially away from the butterfly body.40 Reportedly, hierarchical structures are found on rice leaves and butterfly wings that provide the anisotropic flow, superhydrophobicity, and low adhesion properties.40 The “shark skin effect” anisotropic flow is facilitated by the longitudinal grooves with a transverse sinusoidal pattern in rice leaves and

FIG. 6. Shark skin and lotus effect mechanisms. Flow visualization images using smoke from atomized oil burned in air to study the turbulent vortices behavior with and without riblets at two velocities (adapted from Lee and Lee108). Top left image shows the vortices on a flat plate with a relatively large amount of surface contact area, which leads to higher drag. Top right image show the vortices are lifted above the riblet Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 tips, with a relatively small amount of surface contact area, which leads to lower drag. Bottom left image shows the lotus effect with a water droplet on a lotus leaf and bottom right FIG. 7. Rice and butterfly wing effect that combines the shark image shows a mercury droplet collecting contaminants on a skin and lotus leaf effects (adapted from Bixler and Taro leaf (adapted from Barthlott and Neinhuis43). Bhushan57). Shown are water droplets resting atop their superhydrophobic and low adhesion surfaces. Rice leaves contain longitudinal grooves with a transverse sinusoidal pattern and anisotropic flow from head to tail. Furthermore, scales are butterfly wings contain aligned shingle-like scales that provide hinged preventing motion in the opposite direction further anisotropic flow. Hierarchical structures consisting of micro- facilitating movement.40 Experiments with shark skin papillae superimposed by waxy nanobumps in rice leaves and inspired riblet and fish scale samples suggest reduced drag microgrooves on shingle-like scales in butterfly wings provide in laminar and turbulent flows.40,50,102,106 Shark skin superhydrophobicity and low adhesion. This combination of and fish scales are also reportedly oil-repellent at the solid- anisotropic flow, superhydrophobicity, and low adhesion leads water-oil interface.56,100,112 to improved drag reduction and antifouling. 10 G. D. BIXLER AND B. BHUSHAN

aligned shingle-like scales in butterfly wings. The “lotus Superhydrophobic (superoleophilic) and superoleophobic effect” superhydrophobicity and low adhesion is facilitated by coatings were selected for various drag and antifouling experi- micropapillae superimposed by self-assembled epicuticular ments. For the nanostructured superhydrophobic (superoleo- waxy nanobumps in rice leaves112,114–117 and hierarchical philic) coating, a solution consisting of 50 nm (§15 nm) scales with microgrooves on butterfly wings (for example hydrophobized silica nanoparticles combined with methylphenyl Blue Morpho didius).40,112,113,118–120 silicone resin dissolved in tetrahydrofuran and isopropyl alcohol was utilized.122,123 For the nanostructured superoleophobic coat- Ò 4. SAMPLE FABRICATION ing, a two-step coating system was selected (Ultra-Ever Dry SE 7.6.110, Glenwood Springs, Colorado). The base and top In this section, we explain sample fabrication processes of 40,56,57 rice leaf, butterfly wing, fish scale, and shark skin replicas as coats were individually applied with an airbrush. These well as rice leaf inspired samples for fluid drag and antifouling two reported wear-resistant coatings were chosen to withstand experimentation by Bixler and Bhushan.40,56–58 Detailed the rigors of fluid drag and antifouling experiments. As for nam- descriptions are included as sample fabrication is vital in con- ing conventions, the uncoated urethane rice leaf sample that ducting the various experiments, and the processes are unique received the superhydrophobic nanostructured coating is called to achieve the desired bio-inspired properties. the rice leaf replica, since it replicates actual rice leaves. Con- versely, the superhydrophobic shark skin sample is the uncoated urethane shark skin sample that received the superhydrophobic 4.1. Fabrication of Replicas nanostructured coating. Furthermore, the samples that received Actual samples of the rice leaf (Oryza sativa), butterfly the superoleophobic coating are described as superoleophobic wing (Blue Morpho didius), rainbow trout fish scale (Onco- (flat), superoleophobic rice leaf, or superoleophobic shark skin. rhynchus mykiss), and Mako shark skin (Isurus oxyrinchus) were collected to fabricate various samples.40 4.2. Rice Leaf Inspired Surfaces 4.1.1. Urethane Soft Lithography and Coating Procedure Rice and butterfly wing effect samples were created using Urethane replicas from actual samples were created using a rice leaves as inspiration due to desirable low drag, antifoul- two-step soft-lithography molding procedure.40 Using liquid ing, and relatively simple morphology.40,56,57 The so-called silicone, negative molds were taken after cleaning the actual rice leaf inspired surfaces were designed and fabricated from samples. With the silicone molds complete, liquid urethane silicon master patterns.57 Sample geometrical dimensions are polymer was applied and cured, yielding precise positive repli- based on actual rice leaf morphology shown in Table 1. Actual cas. To combine shark skin and lotus effects, the rice leaf and rice leaf surfaces are covered by a sinusoidal pattern of micro- shark skin replicas received nanostructured coatings. Such papillae with height 2–4 mm, diameter 2–4 mm, pitch lotus effect coatings are known to exhibit both low drag and 5–10 mm, and peak radius 0.5–1 mm.40 Rice leaf inspired self-cleaning properties.5,6,22,24,99,101,103–105,121 topographies shown in Figure 8 were designed to include

TABLE 1 Physical characterization of surface structures from actual samples (adapted from Bixler and Bhushan40) Actual z-dim x-dim/ y-dim x-spacing Peak radius Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 Sample Description (mm) diameter (mm) (mm) (mm) (mm)

Rice leaf (Oryza Sinusoidal grooves array Grooves 125–150 150–175 Full length 150–175 5–10 sativa) covered with micropapilla Micropapillae 2–4 2–4 dia n/a 5–10 0.5–1 and nanobumps Butterﬂy wing Shingle-like scales with Scales 30–50 50–75 100–125 50–75 n/a (Blue Morpho aligned microgrooves Microgrooves 1–2 1–2 100–125 1–2 0.5–1 didius) Fish scales Overlapping hinged scales Scales 175–200 2–2.5 mm dia n/a 1–1.25 mm n/a (Oncorhynchus with concentric rings Rings 5–8 0.1–2.5 mm dia n/a 20–25 1–2 mykiss) Shark skin Overlapping dermal denticles Dermal denticles 75–100 150–175 135–150 150–175 n/a (Isurus with triangular cross Riblets 10–15 15–25 100–150 30–50 1–2 oxyrinchus) sectional riblets LIVING NATURE INSPIRING BIOMIMETICS 11

anisotropic flow and superhydrophobicity. The arrow indicates flow direction for maximum drag reduction and antifouling benefit. Geometrical dimensions are shown in Table 2 with pillar height, pillar diameter or rib width, and pitch. Samples 1 and 2 represent pillars found in actual rice leaf patterns whereas dual height features are present in Sample 3 (only pillars) and Sample 4 (pillars and ribs). Such dual height features create a hierarchical structure designed to facilitate the anisotropic flow similar to the sinusoidal grooves in actual rice leaves.57 Pitch length of the microstructured features found in Sam- ples 1–4 resembles that of actual rice leaves, in order to promote the so-called thin film effect.56,57 The thin film effect is believed to occur when a thin layer of oil is held stationary at the solid-liquid interface, which is believed to lower drag during oil flow.40,57 Pillars just tall and close enough to develop the thin film are necessary; however, pillars too tall or far apart will impede fluid flow and thus increase the drag. Averaging the actual rice leaf micropapillae pitch length yields the pitch length of 7 mm for Samples 1–4. It is believed that antifouling is most effective when the gap between features is less than the approximate diameter of fouling microorganisms.52,54,55,62 For Samples 1–4, the pitch is 7 mm and thus the gap is 2 mm, which is expected to provide antifouling of microorganisms that measure approximately 2–5 mm in diameter.58

4.2.1. Silicon Master Patterns Creating rice leaf inspired samples with micro-sized features required microfabrication techniques to achieve the FIG. 8. Rice leaf inspired geometries for low drag, self-clean- desired dimensions and tolerances. As such, Samples 1–4 ing, and antifouling (adapted from Bixler and Bhushan58). were fabricated using silicon master patterns and soft-lithogra- 57 These surfaces reportedly combine anisotropic ﬂow, liquid phy techniques. To create the silicon master patterns, a sin- repellency, and low adhesion characteristics. Pillars in samples gle square photomask (130 mm £ 130 mm £ 2.3 mm thick 1-3 are arranged in a hexagonal array in order to maintain con- with the critical dimensional tolerance of C/¡ 0.025 microns) sistent gaps to promote antifouling. Anisotropic ﬂow leading was produced containing each pattern for Samples 1–4. Silicon 00 to lower drag is provided by the dual height pillar design of master patterns for Samples 1–4 were created on separate 4 sample 3 and the dual height pillar and rib combination of (10.16 cm) round silicon wafers with sample areas measuring sample 4. Samples 1 and 2 serve as the baseline samples for 6mm£ 100 mm. The etching procedure included standard

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 comparison. wafer dehydration, wafer prime, resist coating, wafer exposure, post exposure bake, wafer development, and hard bake. Silicon master patterns with pits (negative vs. positive

TABLE 2 Geometric dimensions of rice leaf inspired samples58 Height Pillar diameter (D) Pitch (P) Description (H1 or H2)(mm) or rib width (W) (mm) (mm) Sample 1 257 Hexagonal array of single height pillars Sample 2 4 Sample 3 Alternating rows of dual height pillars 2 & 4 Sample 4 Alternating rows of single height pillars & ribs 2 (pillars) 4 (ribs) 12 G. D. BIXLER AND B. BHUSHAN

features) were fabricated in order to emboss polymer ﬁlms and to accurately produce master patterns. Embossing protrusions onto polymer ﬁlms using master patterns is possible when the master pattern contains pits. In addition, pits are less challeng- ing to fabricate as compared to protrusions for the dual height features.57

4.2.2. PDMS Soft Lithography Procedure Rice leaf inspired Samples 1–4 were fabricated in polydi- methylsiloxane (PDMS) with a three-step soft lithography technique using silicon master patterns.57 PDMS was chosen due to its low surface energy which leads to high contact angle, which is believed to lower drag and increase antifouling efﬁciency. However, PDMS bonds well to bare silicon wafers and to itself, so therefore it was necessary to consider de-molding options for the soft lithography procedure. A hydrophilic vinyl polysiloxane dental impression material was selected to create positive master molds from the negative silicon master patterns. The positive master molds in the dental impression material were used to create negative molds in urethane material. Liquid urethane polymer was chosen due to its dimensional stability, ease of casting, ability to de-mold easily from the dental impression material, and ability to de-mold from PDMS. The negative urethane molds were used to create ﬁnal positive samples in PDMS by pouring liquid PDMS and cur- ing. Final samples were easily de-molded from the urethane negative master molds.

4.2.3. Hot Embossing Procedure FIG. 9. Hot embossing procedure using silicon master pat- To demonstrate the feasibility of scaled-up manufacturing terns and PMMA sheets (adapted from Bixler and Bhushan58). using rice leaf inspired topographies, Bixler and Bhushan57 The sandwich assembly consists of the negative silicon master fabricated samples using a hot embossing procedure. Emboss- pattern on the bottom, PMMA sheet in the middle, and flat sili- ing polymer films was conducted using a commercial hot con wafer on the top. The PMMA sheet requires a low surface embossing machine in a clean room environment. Sample 3 energy coating for proper de-molding. was selected to be embossed due to its superior drag and antifouling properties in PDMS. The hot embosser produces single-sided embossed polymer films (optically clear PMMA 2,000–10,000 N with a minimum hold time at each step. Upon 175 mm thick) from silicon master patterns using a combina- completion, the sandwich assembly was cooled, clamping

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 tion of heat and pressure. The sandwich assembly shown in force was released, and the chamber was vented. De-molding Figure 9 consists of a 400(10.16 cm) round silicon master pat- was possible using a razor blade around the edges without tern on the bottom, 400(10.16 cm) round PMMA sheet in the damaging the silicon.57 middle, and 400 (10.16 cm) round flat silicon wafer on the top. The PMMA film required a low surface energy coating on 5. EXPERIMENTAL PROCEDURES both sides for proper de-molding from the silicon wafers. The In this section, we explain apparatuses which provided aqueous fluorochemical CapstoneTM ST-100 was selected and drag, antifouling, contact angle, and contact angle hysteresis diluted with deionized water. measurements for experiments by Bixler and Bhushan.40,56–58 The hot embossing protocol was developed from previous studies71 as well as trial and error (investigating pressures, temperatures, hold times, release coatings, PMMA thickness) 5.1. Pressure Drop Measurements to ensure desired outcomes. Once assembled, the hot embosser For the various drag experiments by Bixler and chamber was vacuumed and the top and bottom chucks heated Bhushan40,56–58 using replica and rice leaf inspired samples, to ensure proper polymer softening. Once heated, an axial the channel dimensions were based on hospital catheter tubes clamping force was applied and increased in increments of (3–5 mm diameter). A rectangular channel sandwich design LIVING NATURE INSPIRING BIOMIMETICS 13

was selected due to its low surface tension, chemical compati- bility with samples, and low health hazard.124

5.1.1. Predicting Closed Channel Pressure Drop Comparing the predicted pressure drop to experimental data allows one to detect anomalies such as leaks and misalign- ments. Predicting pressure drop of a flat rectangular duct requires use of the incompressible flow equations for straight uniform pipes. Since the Mach number is less than 0.3 for all experiments, incompressible flow equations may be used.14 The predicted pressure drop was calculated using the total channel cross-sectional area. Pressure drop .Dp/ between two points in a flat hydrophilic straight uniform closed channel with incompressible and fully developed flow is found with the Darcy-Weisbach formula:14

rV 2fL Dp D ; (6) 2D

where r is the fluid density, V is the flow velocity, f is the friction factor, L is the length between two points on a channel, and D is the hydraulic diameter. Flow velocity (V) is determined by dividing the volumetric flow rate by the channel cross sectional area. In air experiments, the rotameter values were used with manufacturer provided charts to determine the flow velocity. The friction factor for rectangular duct flow is:

k f D ; (7) Re

where for laminar ﬂow:

k D 64 (8a)

FIG. 10. Apparatuses to measure drag via pressure drop in and for turbulent flow: closed channel flow using water, oil, and air (adapted from Bix- ler and Bhushan50). The split rectangular channel design allows 64 k D for samples to be fabricated inside the channel. Interface views 2 11 b b Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 C 2 ¡ : are shown highlighting the top and bottom halves that are sand- 3 24 a a (8b) wiched together. Flow is regulated with the elevated container b with 1 (water), pumps (water or oil), and laboratory air connected to a a rotameter (air). The pressure drop is measured with a manome- ter connected to both ends of the flow channel. The rectangular closed channel hydraulic diameter is:

2ab D D ; (9) was selected so that samples could be applied to one side and a C b then sandwiched together. In order to measure fluid drag via pressure drop, an experimental apparatus was fabricated where a is the width and b is the height. according to the schematic in Figure 10.50 Experimental Equations (6)–(9) are used to predict the pressure drop for results are reported for water, oil, and air40,56–58using the the rectangular closed channels, as presented later for experi- elevated bottle, gear pump, syringe pump, and rotameter for ments with water, oil, and air (where b/a D 1.5 mm/3.3 mm D controlled flow rates. For oil experiments, white paraffin oil 0.45).40,56–58 Equation (8b) shows the friction factor is 14 G. D. BIXLER AND B. BHUSHAN

FIG. 11. (a) Antifouling bioassay experimental procedure with E. coli cells in the laboratory (adapted from Bixler et al.59). (b) Apparatus to uniformly contaminate samples and conduct self-cleaning wash experimentation (adapted from Bixler and Bhushan40). Water droplets at known velocities and ﬂow rates impact the contaminated sample and particle analysis is conducted to quantify efﬁciency.

dependent on channel geometry and independent of the sur- Samples 1–4 and Embossed sample 3 were placed in the bot- face roughness. In order to account for roughness, friction fac- tom of a sterile polystyrene culture dish and sterilized via tor values for pipes can be estimated with the Moody chart.81 ultraviolet exposure. E. coli broth was added to the culture dish until all samples were covered before final incubation. 5.2. Antifouling Experiments The aforementioned concentrations and incubation times were E. coli In this section, we explain antifouling experimental proce- determined from trial and error to achieve appropriate growth (i.e., to visually determine a difference at 1000x mag- dures and measurement techniques using biological and inor- nification between flat control and rice leaf inspired samples ganic fouling contaminants. under investigation).59 After incubation, samples were removed from E. coli broth 5.2.1. Anti-biofouling and rinsed. Rinsing removed any unattached E. coli from the Several anti-biofouling bioassay experiments have been surface prior to imaging. An auto-pipette with sterile PBS was

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 conducted with various microorganisms such as zoospores clamped and held stationary to rinse samples, and then sam- (Enteromorpha),125 (Ulva linza),126 proteins,127 E. coli,59,128 ples were immediately placed onto a glass microscope slide and MRSA (Methicillin-resistant Staphylococcus aureus),129 with cover slip. Using a light microscope and CCD camera, Bixler et al.59 selected the microorganism E. coli to study the each sample was imaged and processed. Images were collected antifouling effect of rice leaf inspired samples due to its preva- with a 100x oil immersion objective lens for a total magnifica- lence, availability, and access to facilities. Reported are proce- tion of 1000x. Image analysis software recognizes contaminat- dures for the antifouling experiments using rice leaf inspired ing E. coli as dark areas and counts the total number. E. coli samples with E. coli. 59 was manually counted five times in circular areas 35 mmin The bioassay procedure in Figure 11a shows E. coli diameter using two samples within the same bioassay.59 streaked onto tryptone and yeast extract dehydrated agar plates and then incubated overnight.59 To prepare E. coli broth, a single colony was picked from streak plates, inoculated into ster- 5.2.2. Anti-inorganic Fouling ile lysogeny broth in a beveled flask, and grown while Anti-inorganic effectiveness of replica and rice leaf inspired shaking. After incubation, E. coli solution was diluted to samples via self-cleaning experiments was conducted by 1/100 and 1/10 into sterile lysogeny broth and stored on ice. Bixler and Bhushan.57,58 Experiments entailed contaminating LIVING NATURE INSPIRING BIOMIMETICS 15

samples, employing a wash technique, and determining the per- 6.1. Sample Characterization centage of inorganic particles removed. Shown in Figure 11b To characterize the actual and replica samples, Bixler and are the apparatuses to deposit contaminate particles on the sam- Bhushan40,58 examined actual, replica, and rice leaf inspired ples and facilitate self-cleaning. A tray containing hydrophilic samples. Reported are scanning electron microscope (SEM) silicon carbide (SiC) contaminants (400 mesh size ranging and optical profiler images for a qualitative and quantitative from 10–15 mm) was placed in the top chamber with an air comparison and understanding of the relevant mechanisms. hose directed in the center. These particles were chosen The SEM provides high resolution in the x/y direction whereas because of their similar properties to natural dirt (shape, size, optical profiler provides high resolution height map informa- and hydrophilicity). Contaminants were blown with laboratory tion in the z direction. A summary of the various features of air and then allowed to settle before the separator panel was interest from each sample are reported in Table 1. removed. After a wait period, samples were removed and subjected to a pre-wash experiment particle analysis. Using a light micro- 6.1.1. Actual, Replica, and Rice Leaf Inspired scope and CCD camera each sample was imaged and analyzed SEM images in Figure 12a by Bixler and Bhushan40 show with image processing software. This process was performed surface structures of actual rice leaf, butterfly wing, fish scale, before and after each wash experiment. Wash experiments and shark skin. Highlighted are cylindrically tapered micropa- consisted of exposing the tilted replicas to water droplets fall- pillae on rice leaves and microgrooves on butterfly wing ing from a specified heights and drip rates. Droplet velocities scales.40 Fish skin is covered by oriented scales with concen- were approximately 1 and 5.6 m/s at heights of 0.02 and tric rings overlapping and hinged such that water flow is from 0.4 m, respectively. This translates into pressures of 200 and head to tail. Shark skin is covered by diamond-shaped dermal 4000 Pa, respectively.57,58 denticles overlapping and hinged such that the riblets are aligned in the water flow direction from head to tail.40 Optical profiler images in Figure 12b provide three-dimensional ren- 5.3. Wettability derings and height maps of each actual sample showing fea- To understand the role of wettability on drag reduction and tures not clearly observed in the SEM images.40 antifouling, CA and CAH measurements were collected for Replica samples by Bixler and Bhushan57 include both the actual, replica, and rice leaf inspired samples.57–59 Water in uncoated and coated samples. Shown in Figure 13a are SEM air, oil in air, and oil underwater are reportedto understand images of the replica samples and in Figure 13b the flat, rice the self-cleaning efficiency of ambient as well as underwater leaf, and shark skin samples that received the superhydrophobic surfaces. Since fish scales and shark skin are naturally covered and superoleophobic nanostructured coatings. As expected the by mucous, the actual samples were cleaned and dehydrated rice leaf micropapillae hierarchical structure detail was not prior to contact angle measurements. Purified water droplets reproduced in the replica. Furthermore, the coatings increases approximately 1 mm in diameter (5 mL) were deposited and surface nano roughness as compared to the uncoated replicas.40 measured with an automated goniometer. White paraffin oil Using optical profiler height map images, the values of Rf 40 droplets of similar dimensions were deposited using a microli- and fLA were reported by Bixler and Bhushan to calculate ter syringe. For oil CA measurements underwater, the oil CA of samples. Data suggests that the measured and predicted droplet was deposited with the sample inverted since the den- values correlate with the Cassie-Baxter regime for rice leaf sity of white paraffin oil (880 kg m¡3) is lower than water and butterfly wing replicas; and Wenzel regime for fish scales (1000 kg m¡3).130 CAH was determined by tilting the sample and shark skin. This coincides with living nature, since rice

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 until the droplet began to move (up to 90 ), and subtract- leaves and butterfly wings are found in the ambient environ- ing the advancing and receding contact angles. Measure- ment (with air pockets), whereas fish scales and shark skin are ments were taken and images captured with an automated found in the aquatic environment (no air pockets).40 A sum- goniometer. mary of Rf and fLA values along with predicted and measured CA values are shown in Table 3. SEM images in Figure 14 by Bixler and Bhushan58 show 6. RESULTS AND DISCUSSION the surface structures of rice leaf inspired samples. Dual- In this section, we present images and measurements char- height pillars are evident in images of Sample 3 along with the acterizing actual, replica, and rice leaf inspired samples. dual height pillars/ribs of sample 4. Each of the sample fea- Reported are measurements of various features from actual tures appears smooth and with minimal defects from the soft- and replica samples describing surface morphology and repli- lithographic process. Images of Embossed sample 3 show fea- cation success. Also included are results from drag, wettabil- tures have similar characteristics as with the PDMS molded ity, and antifouling experiments. Finally, conceptual models sample 3. There appears to be fine strands of presumably are provided to further understand nature’s mechanisms for PMMA material on select pillars, which are believed to be drag reduction and antifouling. remnants of the hot embossing procedure created during the 16 G. D. BIXLER AND B. BHUSHAN

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 FIG. 12. Montage of SEM and optical profiler images depicting actual rice leaf, butterfly wing, fish scale, and shark skin morphologies (adapted from Bixler and Bhushan40). Shown are (a) SEM images at two magnifications and (b) optical profiler images. Arrows indicate the tendencies of fluid flow in transverse and longitudinal directions.

de-molding step.58 As shown, the features are accurately pro- As appropriate for each fluid, shown are flat channel predicted duced for each sample with geometric dimensions as indicated (using Equation (6)) and measured flat channel (milled or in Table 2. PDMS) lines. In order to account for milled channel surface roughness, friction factor values estimated from the Moody 6.2. Pressure Drop Measurements chart were selected based on the roughness value of e D Pressure drop measurements are reported for replicas40,56,57 0.0025 mm. Trend lines are connected through the origin in and rice leaf inspired samples58 using water, oil, and air flow. each plot. LIVING NATURE INSPIRING BIOMIMETICS 17 Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

FIG. 13. Montage of images depicting ambient and aquatic replicas (adapted from Bixler and Bhushan40,57). Arrows indicate direction of anisotropic water droplet movement. Shown are (a) SEM images of rice leaf, butterfly wing, fish scale, and shark skin surfaces as well as (b) flat, rice leaf, and shark skin replicas coated in superhydrophobic and superoleophobic solutions.

6.2.1. Water Flow superhydrophobic and low adhesion nanostructured coating Water flow results by Bixler and Bhushan57,58 are presented were selected based on their initial drag performance. In gen- comparing the replicas, coated samples, and rice leaf inspired eral, a higher pressure drop reduction is reported for the higher samples. Results are shown from experiments with low veloc- flow velocity conditions, where turbulent vortices are believed ity laminar flow (0 < Re < 200) and high velocity turbulent to be present. flow (0 < Re < 12,500). Calculations use the values for mass Provided in Figure 15 are pressure drop measurements for density (r) equaling 1000 kg m¡3 and kinematic viscosity (n) replica, control, and coated samples.57 When considering error equaling 1.034 £ 10¡6 m2 s¡1.130 Samples that received the bars, the rice leaf and butterfly wing sample pressure drops 18 G. D. BIXLER AND B. BHUSHAN

TABLE 3 Replica sample CA predictions40 Actual Replica Fractional CA calculated CA calculated Roughness liquid-air Measured using using Measured CA Measured CA Sample factor (Rf) contact area (fLA) CA Wenzel Eq. 4 Cassie-Baxter Eq. 5 (uncoated) (coated) Rice leaf (Oryza 3.33 0.85 164** 59 141** 118 155* sativa) Butterﬂy wing (Blue 4.41 0.93 161** 48 152** 84 n/a Morpho didius) Fish scales 1.61 0.33 58* 76* 99 94* n/a (Oncorhynchus mykiss) Shark skin (Isurus 2.14 0.44 n/a 71* 105 98* 158 oxyrinchus) *indicates Wenzel regime **indicates Cassie-Baxter regime

appear similar in both laminar and turbulent flow. The fish < Re < 500). To investigate the role of superoleophobicity on scale and shark skin sample pressure drops appear similar in rice leaf and shark skin replicas in oil flow, a superoleophobic laminar flow but differ in turbulent flow, with shark skin supe- coating was applied in addition to a superhydrophobic (super- rior. In laminar water flow, the maximum pressure drop reduc- oleophilic) coating. Calculations use the values for mass den- tion of 26% is shown with the superhydrophobic flat sample.40 sity (r) equaling 880 kg m¡3 and kinematic viscosity (n) In turbulent water flow, maximum pressure drop reduction is estimated at 2.2 £ 10¡5 m2 s¡1.130 shown with rice leaf replica and superhydrophobic shark skin Shown in Figure 17 are pressure drop measurements for at 26% and 29%; and uncoated at 17% and 19%, respec- replica, control, and coated samples.57 The superoleophilic tively.40 It is reported that the rice leaf replica benefits from and superoleophobic flat samples at high velocity show drag anisotropic flow and low adhesion, which leads to lower increases, which is presumably due to the lack of anisotropic drag.58 In addition, the superhydrophobic shark skin replica flow control and increased surface roughness. Pressure drop benefits from the shark skin effect combined with low adhe- reduction is detected at the high velocities for the rice leaf and sion, which also leads to lower drag. butterfly wing samples. At the low and high velocities, the Shown in Figure 16 are pressure drop measurements superoleophobic rice leaf and shark skin samples reduce drag, reported for rice leaf inspired samples.58 Results from the tur- due to anisotropic flow and low adhesion. In addition, the bulent conditions indicate that samples 1 and 2 increase the superhydrophobic (superoleophilic) rice leaf replica also pro- drag, and samples 3 and 4 reduce the drag, which is believed vides drag reduction due to the so-called thin film effect.56 In due to anisotropic flow characteristics. In laminar flow, sample high velocity, maximum pressure drop reduction is shown 58

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 3 provides the greatest pressure drop reduction at 15% while with superhydrophobic (superoleophilic) and superoleophobic in turbulent flow embossed sample 3 provides the greatest coated rice leaf and the uncoated butterfly wing replicas at pressure drop reduction at 23%.40 Sample 2 shows the greatest 10% and 6%.56 pressure drop increase at 13%, presumably due to the taller pil- Shown in Figure 18 are pressure drop measurements lars impeding the fluid flow and vortices translating on the pil- reported for rice leaf inspired samples.58 A pressure drop differ- lars. Furthermore, in turbulent flow, Embossed sample 3 ence is observed at high velocities when examining the effect of yields more pressure drop reduction than sample 3, with values ribs and embossing for samples 3 and 4. Furthermore, samples of 23% and 12%, respectively.58 1,3,4, and Embossed sample 3 show drag reduction reportedly due to anisotropic flow (all but sample 1) and the thin film effect. Embossed sample 3 provides the greatest drag reduction 6.2.2. Oil Flow in low and high velocity laminar flow, at 5% and 6% pressure Oil flow results by Bixler and Bhushan57,58 are presented drop reduction, respectively.56 Sample 2 shows the greatest comparing the replicas, coated samples, and rice leaf inspired pressure drop increase at 11%, presumably due to the taller pil- samples. Results are shown from experiments with low veloc- lars impeding the fluid flow. The so-called thin film effect is ity laminar flow (0 < Re < 10) high velocity laminar flow (0 believed to be present in all samples expect sample 2.58 LIVING NATURE INSPIRING BIOMIMETICS 19

6.2.3. Air Flow Air flow results are presented comparing the replicas, coated samples, and rice leaf inspired samples,57,58 as shown in Figure 19. With air, the achievable velocity range was higher as compared to the water or oil, and the higher Rey- nolds numbers show continued pressure drop reduction (until expected plateauing). Results are shown from experiments with laminar through high velocity turbulent air flow (0 < Re < 5,500). Calculations use the values for mass density (r) equaling 1.2 kg m¡3 and kinematic viscosity (n) equaling 1.51 £ 10¡5 m2 s¡1.130 When comparing fish scales and shark skin replicas, a smaller difference is observed in air vs. water. The superhydrophobic coated rice and shark skin replicas show an improved pressure drop reduction compared to the uncoated, but this is independent of the superhydrophobicity. When comparing the best performing samples in turbulent flow, in water the superhydrophobic shark skin sample reduces pressure by 29% (Re D 10,000) and in air reduces pressure by 27% (Re D 4200).40 It is believed that the coated shark skin benefits from the shark skin effect combined with reduced surface roughness between riblets, which leads to lower drag.50,57 Furthermore, samples 3 and 4, and Embossed sample 3 show pressure drop reduction, which is believed due to anisotropic flow and vortices pinned.58 Embossed sample 3 provides the greatest drag reduction in laminar and turbulent flow, at 10% and 12% pressure drop reduction, respectively.56 Sample 2 shows the greatest pressure drop increase at 7%, presumably due to the taller pillars impeding the fluid flow and vortices translating on the pillars.58

6.2.4. Non Dimensional Pressure Drop Model A non dimensional pressure drop expression was developed to estimate pressure drop for various ﬂuids and conditions.57 This was accomplished by combining Equations (6)–(9) and the Reynolds number for a ﬂat sample. Solving for the non dimensional pressure drop as a function of Reynolds number yields:57 Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

Dp p D D Re G (11) rLkv2 with G D ; 2D3

FIG. 14. Montage of SEM images for samples 1–4 and where G is the fluid property and channel dimension parame- Embossed sample 3 (adapted from Bixler and Bhushan58). ter. Equation (6) shows that pressure drop is directly propor- Arrows indicate direction of fluid movement for drag and self- tional to velocity and Equation (11) shows that non cleaning experiments. Shown are images of samples 1 and 2 dimensional pressure drop is proportional to the Reynolds with uniform height pillars arranged in the hexagonal array as number. well as sample 3 with dual height pillars and sample 4 with pil- The non dimensional pressure drop vs. Reynolds numbers lars and ribs. for a flat milled channel57 and laser etched shark skin inspired 20 G. D. BIXLER AND B. BHUSHAN Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

FIG. 15. Water pressure drop with replica samples in laminar and turbulent ﬂows (adapted from Bixler and Bhushan40). Shown are the milled channel and ﬂat channel predicted lines as well as results for replicas of ambient and aquatic species, both with and without nanostructured coatings. Higher pressure drop translates into higher drag; therefore lower pressure drop is desirable. Error bars show§1 standard deviation, which is hardly visible in the plots.

riblets50 in water, oil, and air experiments are shown in trend lines based on water flow, with a slope change between Figures 20a and 20b, respectively. These fluids represent a laminar and turbulent flow. In order to account for milled wide range of densities and viscosities found in medical, channel surface roughness, friction factor values estimated marine, and industrial applications. As shown, the non dimen- from the Moody chart were selected based on the relative sional pressure drop values follow similar calculated linear roughness value of e D 0.0025 mm. The Moody chart plots LIVING NATURE INSPIRING BIOMIMETICS 21 Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

FIG. 16. Water pressure drop with rice leaf inspired samples in laminar and turbulent flows (adapted from Bixler and Bhushan58). Shown are the flat PDMS and flat channel predicted lines as well as results for samples 1-4 and Embossed sample 3. Higher pressure drop translates into higher drag; therefore lower pressure drop is desirable. Error bars show§1 standard deviation, which is hardly visible in the plots.

the Darcy-Weisbach friction factor, Reynolds number, and the 6.3. Antifouling Experiments relative roughness value for fully developed pipe ﬂow. The In this section, we present images and measurements char- relative roughness factor is calculated by dividing the pipe acterizing replica and rice leaf inspired samples from anti-bio- roughness by its internal diameter.81 fouling and anti-inorganic fouling experiments. 22 G. D. BIXLER AND B. BHUSHAN Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

FIG, 17. Oil pressure drop with replica samples in laminar flow (adapted from Bixler and Bhushan, 2013d). Shown are the milled channel and flat channel predicted lines. Samples include the flat control and replicas of ambient and aquatic species, both with and without the nanostructured superhydrophobic (superoleophilic) and superoleophobic coatings. Higher pressure drop translates into higher drag; therefore lower pressure drop is desirable. Error bars show§1 standard deviation, which is hardly visible in the plots.

6.3.1. Anti-biofouling are microscopic images the E. coli colonized on a ﬂat sample. To understand the antifouling effectiveness of the rice leaf As shown, the E. coli are long cylindrically shaped microor- inspired samples, Bixler et al.59 conducted a series of bioassay ganisms that tend to cluster in groups and align themselves experiments with E. coli microorganisms. Shown in Figure 21 from head to tail. E. coli cells are approximately 1 mmin LIVING NATURE INSPIRING BIOMIMETICS 23 Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

FIG. 18. Oil pressure drop with rice leaf inspired samples in laminar flow (adapted from Bixler and Bhushan58). Shown are the flat PDMS and flat channel predicted lines as well as results for samples 1-4 and Embossed sample 3. Higher pressure drop translates into higher drag; therefore lower pressure drop is desirable. Error bars show§1 standard deviation, which is hardly visible in the plots.

diameter and 2–4 mm long. When actively growing and divid- shown in Figure 22a (with E. coli highlighted by the soft- ing, the cells stretch to »4 mm before dividing into two ware). As indicated, a higher E. coli cell count is present cells.59 as concentration and incubation time increases. Shown in Presented for ﬂat PDMS samples at the two concentra- Figure 22b are the tabulated results of percentage coverage area tions and incubation times are light microscope images of E. coli on the surfaces for 1/100 and 1/10 concentrations 24 G. D. BIXLER AND B. BHUSHAN Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

FIG. 19. Air pressure drop with replica and rice leaf inspired samples in laminar and turbulent flow (adapted from Bixler and Bhushan57,58). Shown are the milled channel, flat PDMS, and flat channel predicted lines. Results are presented for replicas of ambient and aquatic species, both with and without the nanostructured coating, samples 1-4, and Embossed sample 3. Higher pressure drop translates into higher drag; therefore, lower pressure drop is desirable. Error bars show§1 standard deviation.

at 2 and 4 h incubation times. Furthermore, as expected, the ﬂat PDMS control sample, samples 1–4, and the Embossed lower concentration does not provide as much coverage area, sample 3. Tabulated data of percentage reduced coverage com- however the differences are within 10% for both incubation pared to the ﬂat control samples are shown in Figure 24 with times.59 Shown in Figure 23 are light microscopic images of the error bars. LIVING NATURE INSPIRING BIOMIMETICS 25

FIG. 20. Non dimensional pressure drop parameter related to Reynolds number. Presented are results from water, oil, and air experiments for (a) flat samples (adapted from Bixler and Bhushan57) and (b) riblet samples (adapted from Bixler and Bhushan50) using reported data and the mathematical relationship in Equation (11). This provides channel pressure drop estima- tions based on fluid properties, flow conditions, and channel dimensions.

Bixler et al.59 determined antifouling effectiveness by comparing various samples to the total number of E. coli cells on flat control samples. Results reported in percentage E. coli reduced coverage, where a high percent reduced coverage is desired. Reportedly due to the discontinuities, Sam- ples 1–4 and the Embossed sample 3 provided antifouling benefit.59 The greatest antifouling benefit is demonstrated with sample 4 at 1/100 and 1/10 concentrations at 33% and 29% reduced coverage, respectively. Interestingly, all samples are shown to provide antifouling benefit and are within about 10% of each other’s value. It is reported that E. coli are less likely to settle on and colonize the pillar or rib tops, 59

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 and most often settled in between the features. It should be noted that sample 3 and Embossed sample 3 performed simi- larly, indicating minimal differences between samples fabricated from PDMS or PMMA with the fluorchemical release coating. It is possible that the Embossed sample 3 without the fluorchemical coating would not provide as much antifouling benefit.59 Furthermore, it is believed that high CA and low CAH will amplify the antifouling abilities of the samples, as it is believed that microorganisms will have more difficulty adhering to the surface.59

FIG. 21. Images of E. coli on flat surfaces after the bioassay 6.3.2. Anti-inorganic Fouling procedure (adapted from Bixler et al.59) and at a higher magni- To understand the anti-inorganic fouling effectiveness of fication (adapted from www.universityofcalifornia.edu). the various samples, Bixler and Bhushan57,59 conducted a 26 G. D. BIXLER AND B. BHUSHAN Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 FIG. 23. Light microscope images of rice leaf inspired samples after bioassay experiments using E. coli (adapted from Bixler et al.59). Presented are images of flat PDMS, samples 1–4, and Embossed sample 3 with two E. coli concentrations and two incubation times. Long and narrow cylindrically shaped objects are the E. coli. FIG. 22. Light microscope images of (a) flat PDMS control samples and (b) tabulated results after E. coli bioassay experiments (adapted from Bixler et al.59). As indicated, E. coli cov- series of self-cleaning wash experiments. Contaminant par- ers the majority of the surface after 4 h in ideal growing ticles on rice leaf and shark skin replica surfaces are shown in conditions. This baseline serves to compare the various sam- Figure 25, highlighting the shape of the particles as well as ples 1–4 and Embossed sample 3 when calculating percentage their relative size to replica surface features. Tabulated data reduced coverage. are shown in Figure 26a for replica samples and Figure 26b LIVING NATURE INSPIRING BIOMIMETICS 27

FIG. 25. Scanning electron microscope (SEM) images of silicon carbide (SiC) contamination particles on rice leaf and shark skin replicas before anti-inorganic fouling self-cleaning wash experimentation (adapted from Bixler and Bhushan40).

Interestingly, the Embossed sample 3 provides nearly the same self-cleaning ability as the rice leaf replica, even though Embossed sample 3 is not superhydrophobic. Nevertheless, high CA and low CAH is believed to amplify the self-cleaning abilities of the samples, as it is believed that the droplets are able to roll and collect the particles after impact. Further- more, the nanostructure-coated samples exhibit lower adhesion forces, suggesting that the particles are easier to remove versus uncoated.40 FIG. 24. Anti-biofouling results from with rice leaf inspired samples after E. coli bioassay experiments (adapted from Bix- 6.4. Wettability 59 Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 ler et al. ). Results are presented for flat PDMS, samples 1–4, To understand the role of CA and CAH on drag and anti- and Embossed sample 3. The percentage reduced coverage is fouling, Bixler and Bhushan57,59 conducted a series of experi- calculated from the flat PDMS control samples. It is believed ments with actual, replica, flat control, and rice leaf inspired that antifouling efficiency improves with high CA and low samples. Measurements are reported for both the stream-wise § CAH. Error bars show 1 standard deviation. and transverse flow directions, with the maximum values reported. For instance, rice leaf samples show a lower water contact angle when viewed in the stream-wise compared to the for rice leaf inspired samples from both low and high velocity cross-stream direction, since the droplets are pinned between droplet wash experiments. the longitudinal grooves. Measurements are reported for solid- As expected, the superhydrophobic rice leaf replica out- air-water, solid-air-oil, and solid-water-oil interfaces. performed the other samples, and more particles were removed at higher versus lower velocities. Self-cleaning is demonstrated with rice leaf replica and Embossed sample 3 at 6.4.1. Actual, Replica, and Rice Leaf Inspired Samples 95% and 86% contaminant removal, respectively; as com- In air, Bixler and Bhushan40 report that actual rice pared to uncoated samples at 85% and 70%, respectively.57,59 leaf and butterfly wing samples exhibit superhydrophobic 28 G. D. BIXLER AND B. BHUSHAN

FIG. 26. Anti-inorganic self-cleaning results from particle wash experiments (adapted from Bixler and Bhushan57,59). (a) Results are presented for flat urethane and replica samples as well as select samples coated in superhydrophobic and superoleophobic coatings. (b) Results are presented for replica rice leaf, flat PDMS, and rice leaf inspired samples. Self-cleaning efficiency improves with high CA and low CAH. Error bars show§1 standard deviation.s

characteristics due to Cassie-Baxter wetting. Conversely, the leaves is 164.131 Also as expected, the coated rice leaf and fish scales and shark skin show lower contact angles, presum- shark skin replica samples exhibit a higher contact angle than ably due to the Wenzel wetting, see images in Figure 27.40 the uncoated samples, showing the effectiveness of the super- With oil droplets in air, each of the actual samples exhibits hydrophobic coating.40 The superhydrophobic coating is also superoleophilicity.56 Furthermore, with oil droplets underwa- reported oleophilic at the solid-water-oil interface, and the ter, actual rice leaf and butterfly wing samples exhibit supero- superoleophobic coating is superoleophobic at the solid-air- leophilicity, however fish scale and shark skin samples exhibit oil interface.57 For the rice leaf inspired samples, samples superoleophobicity. It is reported that the rice leaf hierarchical 1–4 exhibit hydrophobic contact angles with sample 3 the 58

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 morphology leads to the low contact angle, and that oil pene- highest at 146 and Embossed sample 3 at 101 . It should trates into the butterfly wing open lattice microstructure. With be noted that the oil CAH cannot be determined due to the fish scales, it is reported that a thin water layer forms between low oil contact angle in air.57,58 the oil droplet and the impenetrable scale surface to encourage When comparing measurements from various samples, there superoleophobicity. With shark skin, water soaks into the skin is a noticeable difference between actual and replica samples. and combined with the impenetrable dermal denticle micro- Using Equations (5) and (6) with experimental data provides structures produces superoleophobicity.40,56 results shown in Table 3. A comparison shows that rice leaf Experimental results from CA and CAH experiments by and butterfly wing measurements align well with the Cassie- Bixler and Bhushan57,58 are tabulated. For actual, replica, Baxter equation, whereas fish scales and shark skin measure- and coated samples, Figures 28a and 28b show CA and ments align well with the Wenzel equation.40 This is reportedly CAH, respectively; for rice leaf inspired samples, due to the different mechanisms at work and how the sample Figures 28c and 28d show CA and CAH, respectively. For materials and structures differ.57 For instance, a low surface actual samples at the solid-air-water interface, the rice leaf energy nanostructured coating was applied to rice leaf urethane shows the highest CA D 164 and lowest CAH D 3.For replicas in order to mimic actual rice leaves; however the nano- comparison, maximum water contact angle of actual lotus structured morphology differs from actual rice leaves.40,56 LIVING NATURE INSPIRING BIOMIMETICS 29

smooth for such benefit. For instance, sample 2 shows a relatively high water contact angle of 137 but also shows a drag increase in water, oil, and air. The tall pillars of sample 2 are believed to impede fluid flow and the benefit from high contact angle is negated.58 For drag reduction, it is important to achieve high CA and low CAH with a relatively smooth surface such as the one employed with the rice leaf replica.57 The greatest self-cleaning is shown with the lotus effect samples; where the maximum contaminant removal is reported with Embossed sample 3 and rice leaf replica at 86% and 95%, respectively.58 It is believed that anti-biofouling may also improve with lotus effect surfaces.59 Understanding drag reducing and antifouling mechanisms is possible with water control models for rice leaf, butterfly wing, fish scale, and shark skin.40,58 As shown with simplified conceptual models in Figure 29, self-cleaning rice leaves and butterfly wings easily repel water, whereas the fish scale and shark skin attract water. Furthermore, the longitudinal grooves, scales, or riblets efficiently direct fluid, which is reported to lower drag. The water droplets sit above the hierarchical surface structures of the rice leaf and butterfly wing, whereas they penetrate the surface structures of fish scales and shark skin. By staying above, the droplet can more easily roll and collect contaminants to improve antifouling efficiency. FIG. 27. Water droplet images indicating that actual rice Mucous found on fish scale and shark skin is believed to act as leaves and butterfly wings are superhydrophobic, whereas fish a lubricant, and further reduce drag with the lower skin fric- scales and shark skin are hydrophilic (adapted from Bixler and tion. This also provides antifouling benefits since the water Bhushan40). next to the fish scales and shark skin moves quickly and prevents microorganisms from attaching.40

6.4.2. Wettability, Drag, and Antifouling 6.5. Models for Low Drag and Antifouling In this section, we explain mechanisms behind rice leaf A comparison of drag results with wettability shows no inspired low drag and antifouling surfaces from experimental direct correlation, however high CA coupled with low CAH results involving actual, replica, and rice leaf inspired samples. leads to efficient antifouling. Drag reduction mechanisms differ for various fluids under investigation with considerations given to liquid repellency, adhesion, and anisotropic flow 6.5.1. Low Drag Models characteristics. Reportedly drag reduction occurs with super- It is believed that the combination of anisotropic flow, liq- hydrophobic/ oleophobic and superoleophilic surfaces; and uid repellency, and low adhesion are major contributors to 25,40 57,58

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 antifouling with superhydrophobic/ oleophobic surfaces. drag reduction. The anisotropic flow present with rice In the case of water flow, superhydrophobicity and low adhe- leaves and butterfly wings helps to facilitate efficient fluid sion provides the greatest drag reduction.40 However, in oil movement over the surface. This control minimizes movement flow, the superoleophilic surfaces provide drag reduction via of fluid molecules in the viscous sublayer and thus reduces the the thin film effect but superoleophobic surfaces perform sim- energy losses, which leads to lower drag. A similar effect is ilarly due to liquid repellency and low adhesion.56 Therefore, also believed to be present with oil flow and superoleophobic lower drag is achieved when appropriate wettability is cou- surfaces.56 pled with the appropriate surface morphology, which can Lowering drag using the rice leaf inspired sample 3 is dem- lead to anisotropic flow, liquid repellency, low adhesion, con- onstrated in Figure 30 with closed channel flowwhere trol of turbulent vortices, and/or production of the thin oil hydrophobicity and oleophilicity (thin film effect) are believed film. to increase slip length (b) and reduce drag.58 Reportedly, with Bixler and Bhushan57,58 report that high CA and low CAH rice leaf surfaces in oil flow, oil becomes trapped and holds alone does not always lead to drag reduction or antifouling. It stationary between the micropapillae, and lubricates the solid- has been shown that superhydrophobic surfaces provide drag liquid interface.56 The lubricating effect is believed to increase reduction,57,102,103 however the surface must be relatively slip length (b), so therefore the flow velocity increases at the 30 G. D. BIXLER AND B. BHUSHAN Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

FIG. 28. Wettability results with water and oil droplets (both in air and underwater) using actual, replica, and rice leaf inspired samples (adapted from Bixler and Bhushan40,56–58). Shown are values for apparent CA for (a) actual, replica, and coated samples and (b) rice leaf inspired samples. Also shown are values for CAH (c) actual, replica, and coated samples and (d) rice leaf inspired samples. Self-cleaning efﬁciency improves with high CA and low CAH. Error bars show§1 standard deviation. LIVING NATURE INSPIRING BIOMIMETICS 31

FIG. 29. Water droplet control conceptual models of rice leaves, butterfly wings, fish scales, and shark skin (adapted from Bix- ler and Bhushan40,57,58). Each example contains mechanisms that are believed to promote low drag, self-cleaning, and antifouling. Arrows indicate the tendencies of fluid flow in transverse and longitudinal directions. Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015

channel wall. A similar effect is expected with the Pitcher regimes) when: plant (Nepenthes genus) peristome,3,91 which was later demonstrated with the so-called biomimetic slippery liquid infused pffiffiffi . ¡ /2= ; porous surfaces.95 2P D R H (12) Using the experimental and modeling information, design- ing new bioinspired low drag and surfaces is possible with rice where the known parameters are pitch (P), diameter (D), drop- leaf inspired models.40,56–58 The rice leaf surface is attractive let radius (R), and uniform cylindrical pillar height (H). Equa- due to its low drag properties, as well as relatively simple two- tion (12) provides guidance in developing surfaces to mimic dimensional cylindrical pillar geometry. As developed by Bix- rice leaf geometry with Cassie-Baxter regime. Bixler and ler and Bhushan,58 the basic morphology is shown in Bhushan58 utilized Equation (12) to design the new rice leaf Figure 31. Jung and Bhushan (2009) reported that with similar inspired surfaces with hexagonal arrays of hierarchical mor- patterns water droplets fully penetrate the area between the pil- phologies.40,56,57 Shown is the dual height pillar geometry lars when d D H (transitioning from Cassie-Baxter to Wenzel of sample 3 which is believed to encourage drag reduction, 32 G. D. BIXLER AND B. BHUSHAN

FIG. 30. Drag reducing mechanisms with rice leaf inspired samples (adapted from Bixler and Bhushan57,58). Velocity pro- files show that slip length (b) is believed to increase with the rice leaf inspired surfaces. This leads to lower drag, increased flow rate, and improved antifouling. Sample 3 is shown based on the rice and butterfly wing effect with dual height pillars to promote anisotropic flow. It is believed that drag reduction leading to self-cleaning may be achieved by either superhydro- FIG. 31. Anti-inorganic fouling mechanisms with rice leaf 40,57,58 phobic/oleophobic or superoleophilic (thin film effect) inspired samples (adapted from Bixler and Bhushan ). surfaces. Model shown utilizes uniformly spaced micro-sized single height pillars in a hexagonal array. Inorganic fouling may be washed away in fluid flow via self-cleaning when coupled

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 with high CA and low CAH. self-cleaning, and antifouling by ensuring liquid repellency, low adhesion, and anisotropic ﬂuid control.

reported in this article, the dual-height design of Sample 3 pro- 6.6. Antifouling Models vides superior antifouling properties.59 It is believed that rice leaf inspired surfaces are antifouling As indicated in Figure 32, E. coli shaped and sized micro- against biological and inorganic foulers via self-cleaning and organisms are unable to effectively colonize sample 3 as well microstructured sharp edged discontinuities, respectively.59 as the ﬂat control sample.59 In many cases, E. coli prefer to Furthermore, superoleophobic surfaces effectively repel oil settle in clusters and around the bases of the pillars, which pro- contaminants and provide superior anti-smudge properties. vide multiple attachment points of contact. It is believed that Self-cleaning may also be possible with superhydrophilic sur- microorganisms slightly larger than the gap spacing between faces, as evident with pitcher plant.3,5,91,95,96 Self-cleaning features are less likely to effectively colonize the surface. occurs with the pitcher plant when water uniformly spreads Furthermore, it is reported that the sharp edges of the pillars and slides off carrying contaminants.5,132 As far as the samples discourage the settling and eventual colonization of LIVING NATURE INSPIRING BIOMIMETICS 33

found with the sharp edged micro sized pillars are demonstrated to provide antifouling beneﬁt by delaying colonization.59 The height of the pillars also seems to play a role in antifouling, as shorter pillars found with samples 1 and 3 were covered with E. coli sooner than the taller features with samples 2 and 4. Nevertheless, such mechanisms are believed to be effective against microorganisms of various shapes and sizes. It is believed that postponing microorganism colonization time could aid in the preventing and spread of infectious diseases. This is true since often surfaces are cleaned periodi- cally and therefore will be less likely to harbor a hazardous bioﬁlm.59

7. CONCLUSIONS Living nature provides many examples of flora and fauna that inspire innovative engineering solutions. Rice leaves and butterfly wings have been reported by authors to exhibit a combination of shark skin (anisotropic flow leading to low drag) and lotus leaf (superhydrophobic and self-cleaning) effectsproducing the so-called rice and butterfly wing effect. A detailed comprehensive overview from previous papers by the authors along with new discoveries on the rice and butterfly wing effect is presented with the hope to attract and inspire others in the field. To understand this effect, rice leaf, butterfly wing, fish scale, and shark skin surfaces were investigated and experiments were conducted with actual, replica, and rice leaf inspired samples. Such samples were fabricated with hierarchical structures using photolithography, soft-lithography, hot-embossing, and coating techniques. Fluid drag, anti-bio- FIG. 32. Anti-biofouling mechanisms with rice leaf inspired fouling, anti-inorganic fouling, contact angle, and contact 59 samples (adapted from Bixler et al. ). Shown are conceptual angle hysteresis experiments are reported to understand the models based on anti-biofouling experiments using E. coli role of sample geometrical dimensions. Measurements and with low and high concentrations and short and long incuba- images are included from optical microscope, SEM, and opti- tion times. Microorganisms prefer to cluster in groups and cal profiler to provide qualitative and quantitative information around the base of pillars. Microstructured discontinuities and on surface features related to fluid drag and antifouling. Fluid sharp edges are believed to discourage E. coli colonization. drag is reported with pressure drop measurements from sample Similar anti-biofouling mechanisms are expected with micro- lined closed channels (using water, oil and air in laminar and

Downloaded by [Ohio State University Libraries] at 05:35 29 January 2015 organisms of various shapes and sizes. turbulent regimes). Antifouling is reported from anti-biofouling and anti-inorganic fouling experimentsusing E. coli microorganisms on the surface. E. coli are shaped and sized microorganisms and SiC contaminant particles. such that the edges provide an inconvenient landing zone for When examining the replica and rice leaf inspired samples, settlement, and thus they continue searching for an ideal loca- the greatest drag reduction occurs in turbulent water flow. tion to colonize. It is believed during this process that many E. Reportedly, the maximum pressure drop reduction is shown coli that do not attach remain metabolically active throughout with Embossed sample 3 and rice leaf replica at 23% and the experiment.59 26%, respectively. In laminar oil flow, a 6% pressure drop Incubation times are short, only a few E. coli are able to reduction is reported using the PMMA Embossed sample 3 colonize the sample surface. However, when the concentra- (dual height micro-sized pillar design) as compared to 10% tions are high and the incubation times are long, the E. coli with the rice leaf replica. In turbulent air flow, a 12% pressure eventually cover the surface creating a biofilm. Such surfaces drop reduction is reported using the Embossed sample 3 as may be useful in applications where fluid flow is present (i.e., compared to 20% with the rice leaf replica. Additionally, the continue to wash away fouling) as well as where cleaning is Embossed sample 3 shows similar anti-biofouling perfor- routine (i.e., in hospitals). Nevertheless, the discontinuities mance as the PDMS sample 3, at 28% and 29% coverage area 34 G. D. BIXLER AND B. BHUSHAN

reduction, respectively. The greatest anti-inorganic fouling is 7. R. Allen, Ed., Bulletproof Feathers How Science Uses Nature’s shown with the lotus effect samples, where the maximum con- Secrets to Design Cutting Edge Technology, Ivy Press, London, taminant removal is reported with Embossed sample 3 and U.K. (2010). rice leaf replica at 86% and 95%, respectively. 8. R. E. Armstrong, M. D. Drapeau, C. A. Loeb, and J. J. Valdes, Rice leaf inspired samples are believed to provide aniso- Eds., Bio-Inspired Innovation and National Security, National tropic flow, liquid repellency, and low adhesion characteristics Defense University Press, Washington, D.C. (2010). 9. Y. Bar-Cohen, Biomimetics: Nature Based Innovation, CRC which reportedly leads to drag reduction and antifouling. Press, Boca Raton, Florida (2011). Mechanisms are discussed and models provided to help under- 10. S. 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