RESEARCH ARTICLE

Feather roughness reduces flow separation during low Reynoldsnumber glides of swiftsEvelien van Bokhorst1,2, Roeland de Kat3, Gerrit E. Elsinga1 and David Lentink2,*

ABSTRACTSwifts are aerodynamically sophisticated birds with a small arm andlarge hand wing that provides them with exquisite control over theirglide performance. However, their hand wings have a seeminglyunsophisticated surface roughness that is poised to disturb flow. Thisroughness of about 2% chord length is formed by the valleys andridges of overlapping primary feathers with thick protruding rachides,which make the wing stiffer. An earlier flow study of laminar–turbulentboundary layer transition over prepared swift wings suggested thatswifts can attain laminar flow at a low angle of attack. In contrast,aerodynamic design theory suggests that airfoils must be extremelysmooth to attain such laminar flow. In hummingbirds, which havesimilarly rough wings, flow measurements on a 3D printed modelsuggest that the flow separates at the leading edge and becomesturbulent well above the rachis bumps in a detached shear layer. Theaerodynamic function of wing roughness in small birds is, therefore,not fully understood. Here, we performed particle image velocimetryand force measurements to compare smooth versus rough 3D-printed models of the swift hand wing. The high-resolution boundarylayer measurements show that the flow over rough wings is indeedlaminar at a low angle of attack and a low Reynolds number, butbecomes turbulent at higher values. In contrast, the boundary layerover the smooth wing forms open laminar separation bubbles thatextend beyond the trailing edge. The boundary layer dynamics of thesmooth surface varies non-linearly as a function of angle of attack andReynolds number, whereas the rough surface boastsmore consistentturbulent boundary layer dynamics. Comparison of the correspondingdrag values, lift values and glide ratios suggests, however, that glideperformance is equivalent. The increased structural performance,boundary layer robustness and equivalent aerodynamic performanceof rough wings might have provided small (proto) birds with anevolutionary window to high glide performance.

KEY WORDS: Aerodynamic design, Boundary layer, Glideperformance, Laminar, Transition

INTRODUCTIONThe surface texture of many animals that swim or fly in fluid is tunedto change the dynamics of the boundary layer flow at the surface toreduce drag (Bechert et al., 2000). The precise drag reductionmechanism used depends on the Reynolds number (Re, the ratio ofinertial and viscous forces). Sharks, for example, operate at a highReynolds number of the order of millions, for which the boundary

layer will transition from laminar to turbulent flow naturally as aresult of flow instability. Turbulent flow increases the velocitygradient near the surface, and thus friction drag (Bechert et al.,2000). Sharks reduce this friction drag by reorganizing the structureof the turbulent boundary layer with arrays of riblets that cover theirsurface (Bechert et al., 1997, 2000; Dean and Bhushan, 2010).

Another way to reduce friction drag is by shaping the body topreserve laminar flow, because laminar boundary layers have muchlower friction (Schlichting, 1979; Holmes et al., 1984; White, 1991;Bechert et al., 2000). Unfortunately, laminar boundary layers are alsosensitive to small disturbances that can amplify to the point that theflow transitions to turbulence (Hefner and Sabo, 1987). The Reynoldsnumber based on the length it takes a boundary layer to travel andtransition naturally is of the order of a million, under minimaldisturbance conditions (Schlichting, 1979; White, 1991). Laminarflow-based drag-reduction strategies are therefore within reach foranimals swimming and flying at Reynolds numbers below a million.Whereas a lowRe is a requisite for lowdragbased on laminar flow, it isnot sufficient, because laminar boundary layers are more sensitive toboundary flow separation than turbulent ones (Lissaman, 1983;Simons, 1994; Lyon et al., 1997; Giguer̀e and Selig, 1999;Gopalarathnam et al., 2003; Spedding et al., 2008). Flow separationmostly occurs on the upper side of a wing at a positive angle of attack,due to the strong adverse pressure gradient in the boundary layer(Schlichting, 1979; White, 1991; Mueller, 2002; Shyy, 2013; Kunduand Cohen, 2007). As a result, the flow close to the wall deceleratesand comes to a gradual standstill. The boundary layer separates fromthe surface when the velocity gradient is zero (du/dy=0) and reversesdirection, which can ultimately result in large-scale flow separationthat extends well beyond the trailing edge, i.e. stall. Whereas flowreversal also reverses the orientation of shear stress, and thus reducesfriction drag, flow separation increases pressure drag more, and thusincreases net drag (Mueller, 2002; Shyy, 2013;Drela, 2014). This dragincrease ismoderate under certain conditionswhen the boundary layerre-energizes, reattaches and forms an enclosed separation zone – a so-called ‘laminar separation bubble’ (Schmidt and Mueller, 1989;Mueller, 2002; Spedding et al., 2008; Shyy, 2013; Drela, 2014).

Re-energization of the boundary layer is facilitated by theboundary layer transition from laminar to turbulent flow, whichmixes low energy flow near the wall with higher energy flow in theupper boundary layer (Schlichting, 1979; White, 1991; Mueller,2002; Shyy, 2013; Drela, 2014). Transition can occur naturally as aresult of the boundary layer’s sensitivity to small disturbances;alternatively, transition can be promoted by surface roughness andother forms of turbulence generators (Schlichting, 1979; White,1991; Shyy, 2013). Turbulent boundary layers are less sensitive toflow separation up to a point, and under strong adverse pressuregradients, bigger measures are needed to re-energize the boundarylayer, such as vortex generators that reach beyond the boundarylayer height (Bechert et al., 2000). They mix high-energy flowoutside of the boundary layer with the flow inside as shown byReceived 5 March 2015; Accepted 6 August 2015

1Department of Mechanical, Maritime and Materials Engineering, Delft Universityof Technology, Delft 2628 CD, The Netherlands. 2Department of MechanicalEngineering, Stanford University, Stanford, CA 94305, USA. 3Engineering and theEnvironment, University of Southampton, Southampton SO17 1BJ, UK.

*Author for correspondence (dlentink@stanford.edu)

3179

© 2015. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

mailto:dlentink@stanford.edu

Taylor (1947). At the high Reynolds numbers of the pectoral fins ofhumpback whales, fin serrations at the leading edge generatechordwise vortices that are much larger than the thickness of theboundary layer and mix them effectively, which reduces flowseparation and delays stall (Fish and Battle, 1995; Miklosovic et al.,2004; Pedro and Kobayashi, 2008; van Nierop et al., 2008). Thereduction of flow separation induced by leading edge serration hasalso been found on the hand wing of gliding barn owls, whichoperate at much lower Reynolds numbers (Winzen et al., 2014). Theserrations reduce the length of the separation bubble, butremarkably, force measurements did not show a correspondingdrag reduction (Winzen et al., 2014), likely an effect due to lowReynolds number.The Reynolds number at which a boundary layer transitions to a

turbulent state depends on the geometry of the surface and its angleof attack with respect to the flow, a process that is still not fullyunderstood in animal flight (Shyy, 2013). Because many insects,bats and birds fly at Re below 100,000, the prevailing thought in theliterature is that the boundary layer is largely laminar over theirwings (Azuma, 2006; Shyy, 2013). Because birds operate at higherReynolds numbers, and because they are relatively streamlined andefficient (Pennycuick, 2008; Muijres et al., 2012), their wings mightcritically depend on a particularly well-tuned surface texture.Elimelech and Ellington (2013) found that the wing surface ofhummingbirds is rough as a result of the protruding rachides of thehand wing feathers. The effect of this roughness on the boundarylayer was studied by measuring the flow field over a 3D printedmodel of the hummingbird wing. The tests were performed in awind tunnel that replicates glide conditions at Re=5000 and 15,000,for two geometric angles of attack, α=0 and 10 deg. At low Re andlow α, they found the flow is mostly laminar, whereas at high Re andhigh α, the boundary layer separates at the leading edge, andsubsequently transitions to turbulence above the surface, whichenables it to reattach. They concluded: ‘The flow mechanism whichtriggers turbulence is a shear layer which evolves above the wing

surface and not the rough texture of the wing surface’. However,neither a control experiment with a smooth model hummingbirdwing nor experiments at intermediate α were performed in thisstudy. Such experiments would be insightful, because similarroughness created by strip turbulators is known to trigger transitionat the surface and reduce flow separation of model airplanes anddrones operating at higher Re up to 100,000 and beyond (Braslowand Knox, 1958; Gibbings, 1959; Lissaman, 1983; Simons, 1994;Giguer̀e and Selig, 1999; Gopalarathnam et al., 2003). Model wingstudies have, therefore, not fully resolved the influence of featherroughness on boundary layer flow separation, transition andreattachment in bird flight.

The first report of laminar–turbulent flow transition over a real birdwing suggests that the flow over prepared common swift wings isremarkably laminar, despite feather roughness heights of up to 2%chord length. The roughness elements, created by a combination offeather rachides and the overlapping feather vanes, effectively result incorrugated surface analogs to the earlier mentioned strip turbulators(Lentink and de Kat, 2014). A remarkable difference is, however, thattheoretical estimates suggest that the roughness height of swift handwings is similar to the boundary layer thickness (Lentink and de Kat,2014), whereas in model wings it is a small fraction (Braslow andKnox, 1958; Gibbings, 1959; Kraemer, 1961; Lissaman, 1983;Simons, 1994; Lyon et al., 1997; Giguer̀e and Selig, 1999;Gopalarathnam et al., 2003). Subsequent model wing studies withcorrugated versus smooth model swift wings suggest that feather-likeroughness reduces drag at Re=15,000, but not at higher Re (Lentinkand de Kat, 2014). Because the flow field was not measured in theswift study, in contrast to the study of the 3D printed hummingbirdwing (Elimelech and Ellington, 2013), it remains unclear how theboundary layer flow over bird wings responds to feather-inducedroughness versus a smooth surface. Ideally, this would be studiedacross a range of angles of attack and Reynolds numbers that cover abird’s behavioral flight envelope. The swift is an ideal bird to study theeffect of surface roughness, and compare with findings forhummingbirds, because swifts operate at similar low Re≈20,000(Re ranges from12,000 to 77,000; Lentinket al., 2007) and are closelyrelated to hummingbirds (Videler, 2006; McGuire et al., 2014).However, in contrast to hummingbirds, which almost always flap theirwings, swifts glide a substantial part of their lifetime (Videler et al.,2004; Lentink et al., 2007;Henningsson andHedenström, 2011). Thismakes flow tunnel studies for swifts both biologically andaerodynamically representative. We used earlier surface roughnessmeasurements of the common swift (Apus apus) handwings (Lentinkand de Kat, 2014) to 3D print model wings, and perform boundarylayer flowmeasurements using very high-resolution snapshot particleimage velocimetry (PIV). The experiments were carried out in awatertunnel at biologically relevant Re and α at which the swift is known tocruise energy efficiently with fully extended wings (Lentink et al.,2007; Henningsson andHedenström, 2011). To determine the preciseeffect of surface roughness on flow separation, transition andreattachment over the airfoil of the swift wing, we compared a 3Dprinted wing with realistic feather roughness versus a smooth surface(Fig. 1).

RESULTSTo determine the effect of feather roughness on the boundary layerflow over a fully extended swift wing during cruise, we measuredthe flow field over model swift wings using PIV to compare theaverage velocity field, the vorticity fluctuations in instantaneousflow fields, detailed near-surface flow fields, and boundary layervelocity profiles. These differences were quantified using three

List of symbols and abbreviationsc chord lengthCD drag coefficientCL lift coefficientd primary feather rachis diameterD dragH shape factorL liftLC load cellPIV particle image velocimetryRe Reynolds numberReθ Reynolds number based on momentum thicknesss spanu chordwise velocityu′ chordwise velocity fluctuationsU tangential velocity at the edge of the boundary layerU∞ free-stream velocityu0v 0 Reynolds shear stressv′ wall normal velocity fluctuationsv wall normal velocityα angle of attackδ* displacement thicknessδ99 boundary layer thicknessθ momentum thicknessρ densityω′z vorticity fluctuationμ dynamic viscosity

3180

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

boundary layer parameters: boundary layer thickness δ99, shapefactor H and peak Reynolds stress along the chord length. Todetermine whether the changes in boundary flow dynamics changedglide performance, we measured lift and drag with load cells andcalculated the lift-to-drag ratio, which indicates how far the swiftcan glide per meter height loss.

Flow separation zones in average flow fieldsAveraged flow fields showed that wings with feather-likeroughness generate attached flow across cruise Reynoldsnumbers (we tested Re≈13,000 to 30,000) for both low andhigh geometric α (4.5, 9.0 and 13.5 deg). In contrast, the smoothsurface promotes laminar separation bubbles that depend on α,and open trailing-edge separation bubbles that depend on Re(Fig. 2). Across all angles of attack, the flow over the corrugatedairfoil recirculates in the valleys between the rachis, formingwell-contained laminar separation bubbles. Aft of the mostpronounced corrugation, the boundary layer remains attached allthe way to the trailing edge for all Reynolds numbers and αtested (Fig. 2). The smooth surface, in contrast, provides nocontrol over boundary layer development. At low α, the flowseparates beyond the point of maximum height and forms a largeopen laminar separation bubble that connects to the wake(Fig. 2A). The open separation bubble grows with α at low Re upto 20,000, i.e. the cruise Re of swifts (Lentink et al., 2007), butmuch reduces at Re 24,000 and beyond, showing that theboundary layer dynamics on a smooth surface is very sensitive toRe. At maximal α, both the corrugated and smooth surfacegenerate a thick boundary layer with isolated laminar separationbubbles near the leading edge. The open bubble on the smoothsurface is relatively thin and similar for all Re tested, while thesmall bubbles on the rough surface remain contained in thesurface roughness valleys.

Vorticity and velocity fluctuations in the boundary layerThe instantaneous vorticity fields for cruise Reynolds numbersshow that patches of vorticity are shed from the roughnesselements for moderate and high angles of attack (Fig. 3). Muchsmaller vorticity fluctuations are found on the smooth surface,and only in the region of the trailing edge where the flowseparates at moderate angles of attack. For high angles of attack,both surfaces generate extensive vorticity fluctuations induced bythe laminar separation bubble at the leading edge. The associatedvelocity fluctuations mix the low- and high-speed regions in theboundary layer (Fig. 4).

Laminar versus turbulent boundary layer developmentTo understand how the rough versus smooth surface influencesboundary layer dynamics, we define standard boundary layerparameters in Fig. 5, and plot the average boundary layer profiledevelopment along the chord in Fig. 6. The unsteadiness inthe boundary layer is quantified by plotting the standard deviationin the velocity profile. Comparison of the different treatments,rough versus smooth surface, low versus high α, and low versushigh Re, show they have a pronounced effect on boundary layerdevelopment. As expected, a smooth surface, low angle of attackand low Reynolds number promote steady laminar flow.Remarkably, the boundary layer remains laminar over the roughsurface for low α and Re despite a roughness height that is similarto the measured local boundary layer thickness (Fig. 6). Theboundary layer thickness is affected by the roughness; it growsfaster along the chord of the rough wing for low and moderateangles of attack (Fig. 7). The shape factor of the boundary layerprofile, H, increases rapidly at the trailing edge of the smoothsurface where large separation bubbles are formed (Fig. 8). This isexpected as shape factors beyond 4 indicate boundary layer flowreversal (Drela, 2014). The enhanced mixing due to unsteady

Fig. 1. Design of the 3D printed swift-like airfoilwith a corrugated versus smooth surface.(A) Measured roughness profiles of a swift wing at10 mm intervals show that the maximal roughnessheight occurs on the hand wing (three scan linesare indicated in red, left and right. The x- (chord),y- (roughness) and z-axis (span) are scale bars ofthe indicated length. (B) Rough versus smooth swift-like airfoil: the smooth airfoil is based on the averageupper surface camber of the rough airfoil. Theleading edge design of both airfoils is based on amicroscopy image of the cross-section of theleading-edge primary feather of the swift hand wing.Airfoil thickness is based on primary feather rachisdiameter (d ). (C) Average upper surface profile of theswift hand wing (measured, red, versus 3D printed,blue) and smoothed profile (designed, red, versus3D printed, black). Measured differences betweenCAD models and printed wings are due to the 3Dprinting process. The tiny protrusions at the leadingand trailing edge are data-averaging artefacts and donot represent the surface. (D) Exploded view of theparticle image velocimetry (PIV) and forcemeasurement setup in a water tunnel with a0.6×0.6×5.0 m test section. A top plate on the watersurface suppresses the influence of surface waves,ellipse-shaped end plates reduce 3D effects, andload cells (LC) 1–4 provide force data. U∞,free-stream velocity.

3181

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

vorticity patches in the boundary layer enhances turbulent shearstress (Fig. 9; see ‘PIV data analysis’ in Materials and methods),also known as Reynolds stress (Drela, 2014). This Reynolds shearstress is mostly zero over the smooth surface up to moderateangles of attack, showing the flow is indeed laminar and separateslaminar at the trailing edge. Similarly, the Reynolds shear stressremains zero over the rough surface for the lowest α and Re, but

not beyond. The roughness elements cause high peaks in Reynoldsshear stress, after which they converge to values of about 0.002and 0.005 for low and moderate angle of attack. For the highestangle of attack tested, the Reynolds shear stress reaches similarpeak values over both the smooth and rough wing, but beyond thepeak, the rough surface sustains higher values in contrast to astronger drop-off over the smooth surface.

Re=16,000

Re=20,300

Re=24,400

Re=29,700

U∞

Re=15,800

Re=20,400

Re=24,300

Re=30,300

Re=15,500

Re=23,900

Re=29,100

Re=20,100

Re=16,300

Re=22,200

Re=26,200

Re=29,900

Re=16,100

Re=22,300

Re=26,000

Re=29,900

Re=13,300

Re=20,400

Re=23,600

Re=27,000

U∞

B

C

A

α=9.0 deg

α=4.5 deg

α=13.5 deg

−0.5 0 0.5 1 1.5u/U∞

0.1c

U∞U∞

U∞ U∞

Fig. 2. Averaged flow fields for a swift-like airfoilwith feather roughness versus a smooth surfaceas a function of Reynolds numberRe and angle ofattack α. (A) At α=4.5 deg, the flow over the roughairfoil (left) separates and recirculates in the valleysbetween the rachis bumps, but beyond the biggestbumps it remains attached till the trailing edge. Theflow over the smooth airfoil (right) remains attacheduntil about 70% chord length (c), after which the flowseparates beyond the trailing edge. (B) At α=9.0 deg,the flow over the rough airfoil (left) also remainsattached until the trailing edge. At low Re, the flowover the smooth airfoil (right) separates beyond about50% chord length, but at high Re the flow separationis much reduced. (C) At α=13.5 deg, the flow overboth the rough (left) and smooth (right) wing remainsattached beyond a region near the leading edgewhere a laminar separation bubble is formed overboth surface types. u, chordwise velocity

Re=20,100Re=22,200

Re=20,400

Re=20,300

Re=22,300

0.1c

ω′zc/ U∞ −20 −10 0 10 20

α=4.5 deg

α=9 deg

α=13.5 deg

Re=20,400

Fig. 3. Instantaneous vorticity plot based on the flow fluctuation field (u′, v′). Flow is laminar over the rough (left) and smooth (right) surface at low α atcruise Re of swifts. Comparison of rough and smooth surface effects for α=9.0 deg suggests that the surface roughness indeed forms a source of vorticityfluctuation in the shear layer. At α=13.5 deg, both the smooth and rough surfaces generate extensive vorticity fluctuations in the boundary layer, but qualitativelythe vorticity fluctuations appear to be more broadly distributed for the rough surface. ω′z, vorticity fluctuation.

3182

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

The influence of boundary layer dynamics on glideperformanceThe flow field measurements behind the airfoils were used toqualitatively evaluate the momentum deficit in the wake due to

boundary layer deceleration over the airfoil (Fig. 10). Momentumdeficit is an indicator of drag when measured far behind the airfoilwhere the wake is fully developed. Our near-wake measurementsshow that the flow separation over the smooth airfoil greatly increases

Re=20,100

Re=20,400

Re=20,300

0.1c

0.1c

0.1c

0.1c

0.25c00

0

0

0.5c 0.25c0 0.5c

Re=22,200

Re=20,400

Re=22,300

u′/U∞=1

u′/U∞=1

α=4.5 deg

α=9 deg

α=13.5 deg

Fig. 4. Velocity vectors of the flow fluctuation field (u′, v′) confirm that surface roughness promotes boundary layer mixing. At α=4.5 deg, the flowover the rough surface (left) is essentially laminar, but at higher angles there is substantial unsteady boundary layer mixing. Boundary layer mixing due tofluctuations is not apparent for the smooth airfoil at α=4.5 and 9.0 deg (right). At 13.5 deg, the laminar separation bubble forms a source of unsteady fluctuations,which are qualitativelyof lower intensity than those generated by the rough surface. Reference vector length, comparedwith the free-stream velocity, is provided inthe gray box.

Attached flow Separated flow

0

y=δ99

y=δ99

δ99=y(u/U=0.99)

δ99

Momentum thickness:

Shearlayerthickness

Shape factor: Hsep>4:

H=δ*/θ

Boundary layer height:

Atta

ched

flow

Sep

arat

ed fl

ow

Displacement thickness:

Distanceto shearlayer

Displacedmass

0

y

y

000 11 0 1

δ*

δ*

δ*

θ

θ

θ

~8θ

u/U=0.99 u/

u/U

U u/U u/U

u/U=0.99 u/U u/U u/U

1-u/U u/U(1-u/U)

u/U(1-u/U)1-u/U

0 1

H=2.7

H=10.74

Hlam≈2.6

Inflectionpoint

(Mean)velocityprofile

airfoil & laser shadow

Viscous

Inviscid

Inflectionpoint

separation point

Hturb≈1.3

δ*

A

B

U∞ α

3.5�magnification

δ*=∫1-u/U dyδ99

0θ=∫u/U(1-u/U) dy

δ99

Fig. 5. Idealized boundary layer flow development over the smooth wing. This figure, intended to help introduce the boundary layer parameters used inFigs 6–8, and its explanations are adapted fromWhite (1991) and Drela (2014). (A) Illustration of boundary layer flow over the smooth wing using average (black)and instantaneous (rainbow) flow profiles measured at α=9.0 deg and Re=20,400 (U∞, free-stream velocity). The development of the boundary layer from theleading to trailing edge is characterized by the boundary layer thickness (δ99, black dashed line), the displacement thickness (δ*, orange dashed line), themomentum thickness (θ, blue dashed line) and the inflection points (red dots connected by a red line). For clarity, we magnified the vertical axis in the boundarylayer by a factor of 3.5. (B) Graphical illustration of the integral boundary layer parameters that characterize boundary layer development, local laminarversus turbulent attached flow, and flow separation (Drela, 2014). Boundary layer height, δ99, is the vertical position at which the flow reaches 99% of tangentialvelocity at the edge of the boundary layer (y, wall-normal location; u, chordwise velocity; U, tangential velocity at the edge of the boundary layer). Displacementthickness, δ*, is ameasure for how far themain flow is pushed away from the surface. Momentum thickness, θ, is ameasure for how far themomentum of themainflow is pushed away from the surface. Shape factor,H, is the ratio of displacement andmomentum thickness, and characterizes the shape of the velocity profile forattached turbulent (Hturb≈1.3) and laminar (Hlam≈2.6) flow. For separated flows, the corresponding shape factor is Hsep>4 and δ* is a measure for how far theshear layer is separated from the wall, while the thickness of the separated shear layer can be estimated as 8θ (Drela, 2014).

3183

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

the momentum deficit behind the airfoil at intermediate α and low Re.Under other conditions, themomentumdeficit generated by the roughversus smooth airfoil is more similar. The effect of these and otherflow differences on performancewas evaluated quantitativelywith liftand drag force measurements using load cells (Fig. 1). Thecomparison of drag coefficients and lift-to-drag ratio (glide ratio;Fig. 11) shows that the glide ratio obtained with a swift-like roughversus engineering-like smooth surface is essentially equivalentwithin the precision of our drag measurements.

DISCUSSIONTo determine the effect of feather roughness on the boundary layerflow over a fully extended swift wing during cruise and glideperformance, we contrasted high-resolution flow fields and forcemeasurements. We found that feather roughness makes theboundary layer flow robust to laminar flow separation acrossReynolds numbers – improving the aerodynamic robustness of theswift hand wing. Remarkably, this significant flow improvementhas only a small effect on glide performance in terms of drag or lift-to-drag ratio.

Feather roughness suppresses Reynolds number and angle-of-attack effectsThe measured flow fields show that wings with feather-likeroughness generate attached flow across cruise Reynolds numbers(we tested Re≈13,000 to 30,000) for both low and high geometric α(4.5, 9.0 and 13.5 deg). In contrast, flow over the smooth surfaceexperiences massive laminar flow separation, which depends on αand Re in a non-linear fashion. The surface roughness thuseffectively controls the dynamics of laminar separation bubbleformation throughout the glide envelope of the swift. The uppersurface corrugation of swift hand wings resembles the corrugationof dragonfly airfoils, but is concentrated towards the leading edgeand has a 5–10 times smaller amplitude (Kesel, 2000; Jongerius andLentink, 2010; Lentink and de Kat, 2014). Corrugated dragonflyairfoils also generate laminar separation bubbles in the valleysformed by the corrugation (Rees, 1975a; Buckholz, 1986; Lentinkand Gerritsma, 2003; Vargas and Mittal, 2004; Kim et al., 2009;Levy and Seifert, 2009, 2010; Murphy and Hu, 2010; Hord andLiang, 2012); such effects of corrugation have not beendemonstrated before in birds (Elimelech and Ellington, 2013).

Re=16,000

0

0.5

1 Re=13,300

0

0.5

1 Re=27,000 Re=29,700

0

0.5

1 Re=16,100 Re=15,800

Re=30,300

0

0.5

1 Re=29,900

0 0.2 0.4 0.6 0.8 10

0.5

1 Re=29,9000

0.5

1 Re=16,300 Re=15,500

0 0.2 0.4 0.6 0.8 1

Re=29,100

A

B

C α=13.5 deg

α=9 deg

α=4.5 deg

y/δ99

y/δ99

y/δ99

x/c

Fig. 6. Boundary layer separation is reduced by roughness,high Reynolds number and high angle of attack.Boundary layerthickness, δ99, is defined based on when the velocity reaches 99%of the tangential velocity at the edge of the boundary layer. Solidlines indicate the average velocity profile for different chordpositions x/c, whereas the colored area indicates boundary layerprofile standard deviation. An inflected boundary layer profileindicates flow separation, which can be reduced by flow fluctuationsthat mix the boundary layer, indicated by large standard deviation.Boundary layer profiles are shown for rough (left) versus smooth(right) surface at three different angles of attack, α=4.5 deg (A),9.0 deg (B) and 13.5 deg (C), at the minimum versus maximumReynolds number tested for the rough and smooth surface. Thenon-zero velocity standard deviation at the surface of thepronounced corrugation is due to PIV limitations.

3184

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

The similarity in laminar separation bubbles found on dragonfly andswift wings is remarkable, considering dragonflies operate at Rebelow 10,000 for which experiments show the boundary layer flowremains laminar (Levy and Seifert, 2009), whereas the flow overhummingbird wings at Re=15,000 and α=10 deg can be turbulent inthe separated shear layer above the surface (Elimelech andEllington, 2013). But it is still not entirely clear to what extentboundary layers are either laminar or turbulent over the surface ofbird wings.

The boundary layer is laminar over rough swift wings at lowbut not high α and ReSnapshots of flow fluctuations in the boundary layer, and the averagedboundary layer profiles, show that the corrugated and smooth surfacesgenerate laminar boundary layers at low α. At intermediate α, thecorrugation generates turbulent vortex structures that greatly enhanceboundary layer mixing and prevent flow separation, whereas thesmooth surface generates a laminar boundary layer that separates atlow Re. Flow separation is prevented at high α, because both thesmooth and corrugated surface generate similar turbulent structuresthat originate from the leading edge region. In this region the flowappears to transition into turbulence as a result of shear layerinstability over the laminar separation bubble (Fig. 3). We furtherstudied this by zooming in on our high-resolution flow data (Fig. 4),which suggested that the function of surface corrugation is to generateclusters of small vortices that greatly enhance boundary layer mixing(Figs 3, 4). The smooth surface does not promote such mixing at lowα; however, it does at high α through the shear layer instability overthe laminar separation bubble near the leading edge of the wing. This

induces strong flow fluctuations that mix the boundary layer to asimilar extent to that found for the corrugated surface (Fig. 4). Tobetter characterize under which conditions the flow remains laminar,we plotted both the boundary layer velocity profile and its standarddeviation (Fig. 6). The insignificant standard deviation of the velocityat low Re demonstrates that the flow is indeed laminar over both thesmooth and corrugated wing at α=4.5 deg. This supports earlierfindings of laminar flow over prepared swift wings in a wind tunnel,despite their roughness height of up to 2% chord length (Lentink andde Kat, 2014). The smooth surface also generates a laminar boundarylayer; however, it features pronounced flow separation beyond 60%chord at allRe tested for α=4.5 deg. In contrast, the corrugated surfacegenerates well-contained laminar separation bubbles above thecorrugated surface near the leading edge, and not beyond. Similarto findings for prepared swift wings, we also found that the extent oflaminar flow over the rough wing depends on both Re and α. Thevelocity fluctuations at α=9 and 13.5 deg (Fig. 4) show that thecorrugated surface induces a standard deviation – due to the vortices itgenerates (Fig. 3) – in the velocity profile (Fig. 6). At high Re, thesmooth surface also generates such vortices (Fig. 3) and standarddeviation, reducing flow separation (Fig. 6). Across α and Re, thecorrugated surface successfully locks the extent of flow separation tothe corrugated region. In contrast, the smooth surface generates largeopen separation bubbles near the trailing edge at low α and smallerseparation bubbles near both the leading and trailing edge at high α.This further suggests that wing corrugation helps to control the extentof flow separation over the surface. The extensive laminar flow overthe corrugated surface for α=4.5 deg and Re=13,300, but not forα=9 deg and Re=16,300 (Fig. 6), suggests that the turbulent flow in a

0

0.05

0.1

0.15

0.2

0.25

0

0.05

0.1

0.15

0.2

0.25

0 0.2 0.4 0.6 0.8 1 0

0.05

0.1

0.15

0.2

0.25

x/c0 0.2 0.4 0.6 0.8 1

Re=13,300Re=20,400Re=23,600Re=27,000

α=4.5 deg

α=9 deg

α=13.5 deg α=13.5 deg

α=9 deg

α=4.5 degRe=16,000Re=20,300Re=24,400Re=29,700

Re=16,100Re=22,300Re=26,000Re=29,900

Re=15,800Re=20,400Re=24,300Re=30,300

Re=16,300Re=22,200Re=26,200Re=29,900

Re=15,500Re=20,100Re=23,900Re=29,100

δ 99/c

Fig. 7. Boundary layer thickness (as a proportion ofchord) over the rough and smooth surface is similar tothe swift wing roughness. Boundary layer thickness,δ99, increases with relative chord position x/c and is notvery sensitive to Reynolds number, instead dependingprimarily on α and roughness. At α=4.5 and 9.0 deg, δ99 isclose to 0.02 (2%) chord length for the rough (left) andsmooth (right) surface. At α=9.0 deg, the boundary layerover the rough surface quickly increases in thicknessbeyond x/c=0.2 as a result of mixing induced by thesurface roughness (Fig. 4). The surface roughness of theswift wing is thus equivalent to boundary layer thicknessover the smooth airfoil (at the location of this roughness)and over the rough airfoil at α=4.5 deg and up to x/c=0.2for α=9.0 deg.

3185

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

separated shear layer above a 3D printed hummingbird wing reportedby Elimelech and Ellington (2013) is likely due to the high angle ofattack. We note, however, that the shear layer over our model swiftwing re-attaches immediately behind the corrugated area for α=4.5–13.5 deg. We think this enhanced performance of the printed swiftversus hummingbird wing can be attributed to the additional care wehave taken in measuring and replicating a nose radius that isrepresentative for the leading primary feather of the swift wing(Fig. 1). Based on recently published aerodynamic measurements onprepared hummingbird wings (Kruyt et al., 2014), we know theleading edge of a hummingbird hand wing (Calypte anna) is thinnerthan the 3D printed hummingbird wing of Elimelech and Ellington(2013). The leading edge shape of the avian hand wing matters foraerodynamic performance, as reported earlier for swift wing models,which need a sharp leading edge to generate a leading edge vortex(Videler et al., 2004; Videler, 2006), and for gliding barn owls, forwhich the serration of their leading-edge primary feather helps reduceflow separation (Winzen et al., 2014).

Feather roughness keeps trailing-edge flow separationunder control by forcing turbulenceBoundary layer height measurements show that the roughnessheight of a swift hand wing is indeed equivalent to boundary layerthickness over a smooth surface under similar conditions (Fig. 7).The boundary layer shape factor, H, confirms that the boundarylayer over the smooth airfoil is fully separated at low andintermediate α, highlighted by shape factors beyond H=4 (Drela,

2014), with the exception of intermediate α at high Re, which showsa dramatic divide due to Re (Fig. 8). In contrast, the corrugatedsurface generates boundary layer profiles that are the same acrossReynolds number. Shape factor H peaks at maximal α for all Re onboth surfaces, indicating separated flow at the leading edge. Tobetter quantify the state of the boundary layer, we computed thedevelopment of the Reynolds number based on momentumthickness, Reθ, over the corrugated surface as a function of α. Forlow α, Reθ reaches values of about 71–175 at the trailing edge of thecorrugated wing for increasing Re. For intermediate α, Reθ rangesfrom 194 to 384, and for the highest α from 566 to 1061. Theminimum Reθ value for a sustained turbulent boundary layer is 320according to Preston (1958); this supports our interpretation that theboundary layer is laminar at low α and Re and reaches a transitionalor turbulent state at higher α and Re.

Reynolds shear stress plots indeed confirm laminar flow at low α,which transitions at high Re for the corrugated wing. Atintermediate α, the Reynolds shear stress distributions becomeapproximately constant starting at values beyond 0.02 andconverging to values close to 0.005. Very similar values andtrends were found in the region behind a zigzag roughness strip(Elsinga and Westerweel, 2012) and the order of magnitudecorresponds with turbulent flow conditions over a flat plate(Klebanoff, 1955; Erm and Joubert, 1991; Ducros et al., 1996; deGraaff and Eaton, 2000). On the smooth surface the Reynolds shearstress values and distribution found are comparable to those foundfor separation bubbles on lowReynolds number airfoils (Yuan et al.,

0

5

10

15

20

0

5

10

15

20

H

0 0.2 0.4 0.6 0.8 1 0

5

10

15

20

0 x/c

0.2 0.4 0.6 0.8 1

Re=13,300

Re=20,400

Re=23,600

Re=27,000

Re=16,000

Re=20,300

Re=24,400

Re=29,700

Re=16,100

Re=22,300

Re=26,000

Re=29,900

Re=15,800Re=20,400Re=24,300Re=30,300

Re=16,300

Re=22,200

Re=26,200

Re=29,900

Re=15,500

Re=20,100

Re=23,900

Re=29,100

α=4.5 deg

α=9 deg

α=13.5 deg α=13.5 deg

α=9 deg

α=4.5 deg

Fig. 8. Shape-factor development over the roughsurface is similar across Re and α, in contrast tothe smooth surface. Boundary layer shape factors,H, beyond 4 highlight areas where the boundary layerseparates. Only the peak values of the shape factorvary substantially withRe over the rough surface (left):they shift backward at higher α. In contrast, the shapefactor development over the smooth surface (right) isstrongly Reynolds number dependent at α=9.0 deg,with high values that confirm the flow is separated.Shape factor development varies with α.

3186

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

2005; Lian and Shyy, 2007). At high α, both surfaces generate highpeak Reynolds stress values that indicate turbulent flow. Turbulenceat low Reynolds numbers, however, more likely represents a state oftransitional turbulence without a pronounced −5/3 spectrum (Ermand Joubert, 1991; Mydlarski and Warhaft, 1996); further studiesare needed to test this hypothesis. Finally, we compared the wakevelocity deficit profile to understand how surface roughness affectsairfoil drag. The profiles confirm that the smooth surface airfoil isReynolds sensitive, whereas the rough surface is not. Otherwise, thewake profiles are relatively similar, which suggests that profile dragis relatively similar beyond the Reynolds effect because of flowseparation on the smooth surface at α=9.0 deg. Thewake profiles aremeasured at 5% chord length behind the trailing edge and are,therefore, not fully developed. Thus, small differences in wakeprofiles cannot be interpreted directly in terms of profile drag(Spedding and Hedenström, 2009).

Influence of wing corrugation on flight performance andstructural functionEarlier studies of the corrugated airfoils of dragonfly wings haveshown they function well at low Reynolds numbers in terms ofaerodynamic and structural performance. The corrugation improvesthe structural stiffness of the wing (Rees, 1975b; Kesel, 2000).Similarly, elevated rachis height will improve the stiffness of birdhand wings (Lentink and de Kat, 2014), a feature that is thought tobe an important prerequisite for the flight of protobirds (Nudds andDyke, 2010). Precise lift and drag measurements on model swift

wings in a wind tunnel showed that surface roughness due to rachisheight results in either equivalent or better aerodynamicperformance than smooth wings, in particular at the cruiseReynolds number of swifts (Lentink and de Kat, 2014). Thepresent force measurements on model swift wings in the watertunnel support this finding: the rough and smooth wings generateequivalent drag, and equivalent lift-to-drag ratio (Fig. 11), to withinour measurement uncertainties due to Reynolds differences and loadcell resolution limits. Further aerodynamic analysis is needed tounderstand why performance differences are small. The fact,however, that such rough wings perform equivalent to smoothwings, similar to findings for barn owls (Winzen et al., 2014), is animportant insight specific for low Reynolds numbers. Our detailedhigh-resolution PIV study supports earlier qualitative measurementsshowing that the boundary layer stays laminar over rough swiftwings at low angles of attack, a remarkable feat for 2% rough wings,but becomes turbulent at high angles of attack. Turbulenceprevents laminar separation development over the rough wing,which gives it more reliable aerodynamic qualities, in contrast to thesmooth surface. The equivalent glide performance of smooth andvery rough airfoils is specific to the extremely low Reynoldsnumbers of about 20,000 at which swifts glide; at the higherReynolds numbers of albatrosses, smooth wings should outperformrough, aerodynamically unsophisticated, wings. The demonstratedinsensitivity of glide performance to surface roughness at lowReynolds numbers might have provided small protobirds with anevolutionary window to high glide performance (Lentink and de

0.9 10

0.005

0.01

−0.02

0

0.02

0.04

0.06

0.08

0.1

−0.02

0

0.02

0.04

0.06

0.08

0.1

0 0.2 0.4 0.6 0.8 1 0 0.2 0.4 0.6 0.8 1 −0.02

0

0.02

0.04

0.06

0.08

0.1

Re=13,300

Re=20,400

Re=23,600

Re=27,000

Re=16,000

Re=20,300

Re=24,400

Re=29,700

Re=16,100

Re=22,300

Re=26,000

Re=29,900

Re=15,800

Re=20,400

Re=24,300

Re=30,300

Re=16,300

Re=22,200

Re=26,200

Re=29,900

Re=15,500

Re=20,100

Re=23,900

Re=29,100

0.8 0.9 10

0.010

0.005

0.8 0.9 10

0.005

0.010

0.8 0.9 10

0.01

0.02

0.03

x/c

Max

(– u

′v′/U

2 ∞)

α=4.5 deg

α=9 deg

α=13.5 deg

α=4.5 deg

α=9 deg

α=13.5 deg

Fig. 9. Swift feather roughness generatessignificant Reynolds shear stresses of theorder of 0.01 and up, a signature oftransitional turbulent flow. At α=9.0 and13.5 deg, the roughness generates vortices(Fig. 4) that strongly enhance mixing and thusgenerate Reynolds shear stress. The smooth(right) and rough (left) surface only generatesimilar Reynolds shear stress at α=13.5 deg,when the shear layer separates on the smoothairfoil and becomes turbulent above a laminarseparation bubble (Figs 2–4 and 7). Thechordwise Reynolds shear stress production isweakly dependent on Reynolds number, exceptfor the rough surface at α=4.5 deg, where itlocally jumps from zero to non-zero when Reincreases from 13,300 to 20,400.

3187

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

Kat, 2014). Simultaneously, the higher allowable wing roughnessenabled the rachis to be thicker, which might have been a criticalstep towards high glide performance in protobirds, which neededthis rachis height to lift their body weight (Nudds and Dyke, 2010).In modern birds, elevated rachis height helps withstand higher wingloading (G-loading) during turning maneuvers. Similarly, thefinding that high wing roughness is allowable at the Reynoldsnumbers of swifts will help set more reasonable manufacturingtolerances on the wings of hand-sized micro air vehicles. Futurestudies might show how optimal wing roughness varies as afunction of ecotype and Reynolds number across birds, rangingfrom hummingbirds to albatrosses.

MATERIALS AND METHODSWater tunnelThe experiments with the wings were carried out in a water tunnel with a testsection that was 60 cm wide, 60 cm high and 500 cm long, and a flow speedthat could be controlled up to 1 m s−1 (Schröder et al., 2011; Harleman,2012). The turbulence level of the free-stream velocity was below 0.5% at afree-stream velocity of 0.53 m s−1; this value contains both the free-streamturbulence and the measurement noise. As we took measurements atsomewhat lower speeds of roughly 0.1 and 0.2 m s−1, we conservativelyestimated the turbulence level to be below 1%. For natural boundary layertransition over a flat plate, the present free-stream turbulence levels (

The resulting wing had a 36 cm wingspan and 15 cm chord length, andwas built up by three sections that spanned 12 cm each. To reduce 3Dflow effects, we attached a 2 mm thin elliptical endplate to each wing tip(Mueller, 1999), and performed PIV measurements at the centerline ofthe wing.

Model swift wing manufactureWe designed and 3D printed (Projet 3500 HD Max) the three wingsegments using a transparent plastic (VISIJET EX 200) with a resolutionof 32 μm (layer thickness). To minimize deformations of individual wingelements due to melt-off of wax that supports the 3D printed structure,the models were heated in water at 60°C and clamped down duringcooling. To improve chordwise stiffness and shape, we added thin ribson the lower side of the wing with a spacing of 4 cm such that there wasno rib on the lower surface at the centerline where we performed the PIVmeasurements. At the location of the model rachis, small holes remainedin the 3D printed structure that we used to connect the three wingsegments with stainless steel rods (1–2 mm diameter), glued in placewith epoxy (Scotch Well DP810). We measured the cross-section of the

assembled rough and smooth wing in the PIV laser sheet to compare itwith the computer-aided design (CAD) model (Fig. 1): the rough modelhad about 1% less camber, and the smooth model had about 1.5% morecamber than designed.

Reynolds number, geometric angle of attack and PIVWe selected combinations of Re (roughly 15,000–30,000; step size 5000)and α (geometric; 4.5, 9.0 and 13.5 deg) that are representative for swiftsgliding at high efficiency (Lentink et al., 2007). Here, the Reynoldsnumber is defined as Re=ρU∞c/μ, where ρ is the density and μ is thedynamic viscosity. The boundary layer flow over the model wings wasmeasured using a PIV system consisting of three 16 megapixel cameras(Imager LX 16 Mpix, LaVision) positioned side by side in streamwisedirection, imaging optics (Nikon AF Micro-Nikkor 105 mm f/2.8D,f=105 mm set at f 5.6), and a pulsed laser (Quanta ray Nd:YAG, SpectraPhysics; 200 mJ pulse−1, 4.2 Hz). The fields of view of the three high-resolution cameras spanned the entire chord length (150 mm) over theupper surface. The tracer particles (hollow microspheres, Sphericel;10 μm in diameter) were illuminated within the laser sheet (about 1–2 mm thick), which spanned the free-stream and cross-stream direction.Within the sheet, light was directed at a shallow angle with the modelsurface, to minimize surface reflections, while avoiding shadows inbetween roughness valleys. Calibration of the setup was carried out witha 3D printed calibration plate positioned in the chordwise direction. Thecalibration error was about 1 pixel or 0.0017 mm. The time delaybetween laser pulses was selected to resolve the velocity gradient of theslower inner boundary layer, resulting in a free-stream particledisplacement of about 10 pixels. The cross-correlation of the particleimages was carried out in DaVis (LaVision 2013) using a multi-gridmethod and three iterative steps with 50% overlap for 300 image pairs tocompute the ensemble average. The final interrogation window size was32×32 pixels (0.56×0.56 mm2). The estimated displacement error wasabout 0.1–0.2 pixels (Adrian and Westerweel, 2010) or 0.0017–0.0034 mm. Finally, we used the results of the load cells toapproximate the angle of attack at which the wings obtain zero lift,which is −6.6 deg (±1.8 deg s.d.) for the rough wing and −3.1 deg(±1.4 deg s.d.) for the smooth wing (averaged over Re and fitted basedon all three α). This facilitates coarse comparison with earliermeasurements on prepared swift wings (Lentink et al., 2007; Lentinkand de Kat, 2014).

PIV data analysisThe flow fields obtained with the PIV setup were processed to determinethe average flow field, vorticity field and Reynolds shear stressdistribution over the model wings. The average velocity field wascomputed using 60, 120, 180 and 240 instantaneous flow fields in orderto determine how many fields should be taken to get a convergedaverage; we found 180 to be sufficient. To assure convergence, weacquired and processed 300 flow fields for each experiment. The averagevelocity field was computed using 60,120,180 and 240 instantaneousflow fields in order to determine how many fields should be taken to geta converged average. We found 180 to be sufficient, but to assureconvergence, we acquired and processed 300 flow fields for eachexperiment. To determine the presence of vortices in the flow, wesubtracted the mean velocity field from an instantaneous velocity field toobtain the velocity fluctuation field (u′,v′) and calculated the associatedfluctuations in the vorticity field as follows: ω′z=(∂v′/∂x)−(∂u′/∂y).

To evaluate the laminar versus turbulent state of the boundary layer, wecalculated the boundary layer thickness, shape factor and Reynolds shearstress. A limitation of the first two measures is that the theoretical valuesassociated with turbulent flow are only known for the boundary layer on aflat plate at higher Reynolds numbers. In comparison, the calculation ofReynolds shear stress, u0v0, provides better contrast, because this stress isstraightforward to calculate and is known to be significant in transitional andturbulent boundary layers. For a laminar boundary layer, the Reynolds shearstress will be very close to zero and, for the canonical fully developedturbulent boundary layer, typically normalized values are around 0.001–0.002 (Klebanoff, 1955; Erm and Joubert, 1991; Ducros et al., 1996; de

Re≈15,000Re≈20,000Re≈25,000Re≈30,000

0

0.2

0.4

0.6

CL/CD

CD

4.5 9.0 4.5 9.0

CL

0 0

4

8

12

0 α (deg)

2.0

1.5

1.0

0.5

0

13.5 13.5

Fig. 11. Drag and lift coefficients (CD and CL) based on load cellmeasurements show surface texture has a small effect on drag and glideratio. The drag measurements show that drag is weakly dependent on surfacetexture. Because the Reynolds number varies between the rough (left) andsmooth (right) surface measurement (e.g. at α=4.5 deg, we compareRe=13,300 for the smooth surface versus Re=16,000 for the rough surface),we cannot interpret the small differences asRe is not strongly controlled for andminimal drag measurement is not very precise. Whereas differences in lift aremore pronounced, the glide ratio calculations based on the lift and drag forcemeasured with the load cells further suggest that surface roughness has alimited effect on glide performance.

3189

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

Graaff and Eaton, 2000). For comparison between experiments, we selectedthe maximum Reynolds shear stress at each chordwise position, within theboundary layer height, to assess the local turbulence level along the wingchord. Next, the boundary layer thickness (δ99) and the shape factor (H )were determined along the entire chord in 0.01c steps (where c is the chord)(Fig. 5).

Load cell analysisLift and drag forces were measured with a configuration of four linearload cells (EP2 Scaime), which have a capacity of 20 N and accuracy of0.02 N (Fig. 1). Drag and lift calibrations were carried out by applyingknown loads in 0.5 kg steps over the full lift and drag range of the cells.A linear fit gave RMSE (root mean square error) values of 0.07 and0.13 N for the lift and drag, respectively. The data showed there wasnegligible cross-talk between the load cells. In order to extract the forcesattributed to the model, forces created by the mounting system andendplates were measured independently for all angles of attack andvelocities and corrected for. Forces for each angle of attack and Reynoldsnumber were sampled at 1000 Hz and averaged over about 2 min ofdata. Based on the lift (L) and drag (D) forces, we calculated thecorresponding dimensionless force coefficients as follows:

CD ¼ Dð1=2ÞrU21sc;

CL ¼ Lð1=2ÞrU21sc;

where s is the span and c is the chord length of the wing in meters, ρ is thedensity of water and U∞ is the free-stream velocity. The uncertaintycalculation combined the standard deviation of the force measurements withand without the model. At low velocities, the magnitude of the drag forceswas about 0.1 N, which led to relatively large uncertainties in the CDcoefficients and CL/CD ratios, much larger than those in an earlier study(Lentink and de Kat, 2014). We therefore consider the earlier publishedwind tunnel force measurements more precise, whereas the present flowanalysis is more detailed and sophisticated. Regardless, both studies aresupportive of the performance conclusions based on the less precise forcedata presented here.

Competing interestsThe authors declare no competing or financial interests.

Author contributionsE.v.B. performed the experiments. E.v.B., R.d.K., G.E. and D.L. conceived anddesigned the experiments, analyzed data and wrote the paper.

FundingThis research received no specific grant from any funding agency in the public,commercial or not-for-profit sectors. R.d.K. is supported by a Leverhulme EarlyCareer Fellowship.

ReferencesAdrian, R. J. and Westerweel, J. (2010). Particle Image Velocimetry. Cambridge:Cambridge University Press.

Azuma, A. (2006). The Biokinetics of Flying and Swimming. Reston, VA: AmericanInstitute of Aeronautics and Astronautics.

Bechert, D. W., Bruse, M., Hage, W. andMeyer, R. (1997). Biological surfaces andtheir technological application – laboratory and flight experiments on dragreduction and separation control. 28th Fluid dynamics conference, SnowmassVillage, CO: AIAA Meeting Papers.

Bechert, D. W., Bruse, M., Hage, W. and Meyer, R. (2000). Fluid mechanics ofbiological surfaces and their technological application. Naturwissenschaften 87,157-171.

Brandt, L., Schlatter, P. and Henningson, D. S. (2004). Transition in boundarylayers subject to free-stream turbulence. J. Fluid Mech. 517, 167-198.

Braslow, A. L. and Knox, E. C. (1958). Simplified Method for Determination ofCritical Height of Distributed Roughness Particles for Boundary Layer Transitionat Mach numbers from 0 to 5 (Technical Note 463). Washington: NACA.

Buckholz, R. H. (1986). The functional role of wing corrugations in living systems.J. Fluid. Eng. 108, 93-97.

de Graaff, D. B. and Eaton, J. K. (2000). Reynolds-number scaling of the flat-plateturbulent boundary layer. J. Fluid Mech. 422, 319-346.

Dean, B. and Bhushan, B. (2010). Shark-skin surfaces for fluid-drag reductionin turbulent flow: a review. Philos. Trans. A Math. Phys. Eng. Sci. 368,4775-4806.

Drela, M. (2014). Flight Vehicle Aerodynamics. Cambridge, MA: MIT Press.Ducros, F., Comte, P. and Lesieur, M. (1996). Large-eddy simulation of transition

to turbulence in a boundary layer developing spatially over a flat plate. J. FluidMech. 326, 1-36.

Elimelech, Y. and Ellington, C. P. (2013). Analysis of the transitional flow field overa fixed hummingbird wing. J. Exp. Biol. 216, 303-318.

Elsinga, G. E. and Westerweel, J. (2012). Tomographic-PIV measurement of theflow around a zigzag boundary layer trip. Exp. Fluids 52, 865-876.

Erm, L. P. and Joubert, P. N. (1991). Low-Reynolds-number turbulent boundarylayers. J. Fluid Mech. 230, 1-44.

Fish, F. E. and Battle, J. M. (1995). Hydrodynamic design of the humpback whaleflipper. J. Morphol. 225, 51-60.

Fransson, J. H. M., Matsubara, M. and Alfredsson, P. H. (2005). Transitioninduced by free-stream turbulence. J. Fluid Mech. 527, 1-25.

Gibbings, J. C. (1959). On Boundary Layer Transition Wires (Technical Report462). London: ARC.

Giguer̀e, P. and Selig, M. S. (1999). Aerodynamic effects of leading-edge tape onaerofoils at low Reynolds numbers. Wind Energy 2, 125-136.

Gopalarathnam, A., Broughton, B. A., McGranhan, B. D. and Selig, M. S. (2003).Design of low reynolds number airfoils with trips. J. Aircraft 40, 768-775.

Harleman, M. (2012). On the effect of turbulence on bubbles. PhD thesis, DelftUniversity of Technology, Delft.

Hefner, J. N. and Sabo, F. E. (1987). Research in natural laminar flow andlaminar-flow control. Proceedings of a symposium sponsored by the NationalAeronautics and Space Administration. Langley Research Center, Hampton,VA: NASA.

Henningsson, P. and Hedenström, A. (2011). Aerodynamics of gliding flight incommon swifts. J. Exp. Biol. 214, 382-393.

Holmes, B. J., Obara, C. J. and Yip, L. P. (1984). Natural Laminar FlowExperiments onModern Airplane Surfaces (Technical Paper 2256). Hampton, VA:NASA.

Hord, K. and Liang, Y. (2012). Numerical investigation of the aerodynamic andstructural characteristics of a corrugated airfoil. J. Aircraft 49, 749-757.

Jongerius, S. R. and Lentink, D. (2010). Structural analysis of a dragonfly wing.Exp. Mech. 50, 1323-1334.

Kesel, A. B. (2000). Aerodynamic characteristics of dragonfly wing sectionscompared with technical aerofoils. J. Exp. Biol. 203, 3125-3135.

Kim, W.-L., Ko, J. H., Park, H. C. and Byun, D. (2009). Effects of corrugation of thedragonfly wing on gliding performance. J. Theor. Biol. 260, 523-530.

Klebanoff, P. S. (1955). Characteristics of Turbulence in A Boundary Layer withZero Pressure Gradient (NACA report 1247). Washington: NACA.

Kraemer, K. (1961). Über die wirkung von stölperdrähten auf dengrenzschichtumschlag. Z. Flugwissensch 9, 20-27.

Kruyt, J. W., Quicazán-Rubio, E. M., van Heijst, G. F., Altshuler, D. L. andLentink, D. (2014). Hummingbird wing efficacy depends on aspect ratio andcompares with helicopter rotors. J. R. Soc. Interface 11, 12.

Kundu, P. and Cohen, L. (2007). Fluid Mechanics. Waltham, MA: Academic Press.Lentink, D. and de Kat, R. (2014). Gliding swifts attain laminar flow over rough

wings. PLoS ONE 9, e99901.Lentink, D. and Gerritsma, M. (2003). Influence of airfoil shape on performance in

insect flight. Proceedings of 33rd AIAA fluid dynamics conference and exhibit.Orlando, FL: AIAA.

Lentink, D., Müller, U. K., Stamhuis, E. J., De Kat, R., Van Gestel, W., Veldhuis,L. L. M., Henningsson, P., Hedenström, A., Videler, J. and van Leeuwen, J. L.(2007). How swifts control their glide performance with morphing wings. Nature446, 1082-1085.

Levy, D.-E. and Seifert, A. (2009). Simplified dragonfly airfoil aerodynamics atReynolds numbers below 8000. Phys. Fluids 21, 071901.

Levy, D.-E. and Seifert, A. (2010). Parameter study of simplified dragonfly airfoilgeometry at Reynolds number of 6000. J. Theor. Biol. 266, 691-702.

Lian, Y. and Shyy, W. (2007). Laminar-turbulent transition of a low Reynoldsnumber rigid or flexible airfoil. AIAA J. 45, 1501-1513.

Lissaman, P. B. S. (1983). Low-Reynolds-number airfoils. Annu. Rev. Fluid Mech.15, 223-239.

Lyon, C. A., Selig, M. S. and Broeren, A. P. (1997). Boundary layer trips on airfoilsat low Reynolds numbers. 35th Aerospace sciences meeting & exhibit, Reno, NV:AIAA.

McGuire, J. A., Witt, C. C., Remsen, J. V., Jr, Corl, A., Rabosky, D. L., Altshuler,D. L. and Dudley, R. (2014). Molecular phylogenetics and the diversification ofhummingbirds. Curr. Biol. 24, 910-916.

Miklosovic, D. S., Murray, M. M., Howle, L. E. and Fish, F. E. (2004). Leading-edge tubercles delay stall on humpback whale (Megaptera novaeangliae) flippers.Phys. Fluid. 16, L39-L42.

3190

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

http://dx.doi.org/10.2514/4.862502http://dx.doi.org/10.2514/4.862502http://dx.doi.org/10.1007/s001140050696http://dx.doi.org/10.1007/s001140050696http://dx.doi.org/10.1007/s001140050696http://dx.doi.org/10.1017/S0022112004000941http://dx.doi.org/10.1017/S0022112004000941http://dx.doi.org/10.1115/1.3242550http://dx.doi.org/10.1115/1.3242550http://dx.doi.org/10.1017/S0022112000001713http://dx.doi.org/10.1017/S0022112000001713http://dx.doi.org/10.1098/rsta.2010.0201http://dx.doi.org/10.1098/rsta.2010.0201http://dx.doi.org/10.1098/rsta.2010.0201http://dx.doi.org/10.1017/S0022112096008221http://dx.doi.org/10.1017/S0022112096008221http://dx.doi.org/10.1017/S0022112096008221http://dx.doi.org/10.1242/jeb.075341http://dx.doi.org/10.1242/jeb.075341ttp://dx.doi.org/10.1007/s00348-011-1153-8ttp://dx.doi.org/10.1007/s00348-011-1153-8http://dx.doi.org/10.1017/S0022112091000691http://dx.doi.org/10.1017/S0022112091000691http://dx.doi.org/10.1002/jmor.1052250105http://dx.doi.org/10.1002/jmor.1052250105http://dx.doi.org/10.1017/S0022112004002770http://dx.doi.org/10.1017/S0022112004002770http://dx.doi.org/10.1002/(sici)1099-1824(199907/09)2:33.0.co;2-5http://dx.doi.org/10.1002/(sici)1099-1824(199907/09)2:33.0.co;2-5http://dx.doi.org/10.2514/2.3157http://dx.doi.org/10.2514/2.3157http://dx.doi.org/10.1242/jeb.050609http://dx.doi.org/10.1242/jeb.050609http://dx.doi.org/10.2514/1.C031135http://dx.doi.org/10.2514/1.C031135http://dx.doi.org/10.1007/s11340-010-9411-xhttp://dx.doi.org/10.1007/s11340-010-9411-xhttp://dx.doi.org/10.1016/j.jtbi.2009.07.015http://dx.doi.org/10.1016/j.jtbi.2009.07.015http://dx.doi.org/10.1098/rsif.2014.0585http://dx.doi.org/10.1098/rsif.2014.0585http://dx.doi.org/10.1098/rsif.2014.0585http://dx.doi.org/10.1371/journal.pone.0099901http://dx.doi.org/10.1371/journal.pone.0099901http://dx.doi.org/10.1038/nature05733http://dx.doi.org/10.1038/nature05733http://dx.doi.org/10.1038/nature05733http://dx.doi.org/10.1038/nature05733http://dx.doi.org/10.1063/1.3166867http://dx.doi.org/10.1063/1.3166867http://dx.doi.org/10.1016/j.jtbi.2010.07.016http://dx.doi.org/10.1016/j.jtbi.2010.07.016http://dx.doi.org/10.2514/1.25812http://dx.doi.org/10.2514/1.25812http://dx.doi.org/10.1146/annurev.fl.15.010183.001255http://dx.doi.org/10.1146/annurev.fl.15.010183.001255http://dx.doi.org/10.1016/j.cub.2014.03.016http://dx.doi.org/10.1016/j.cub.2014.03.016http://dx.doi.org/10.1016/j.cub.2014.03.016http://dx.doi.org/10.1063/1.1688341http://dx.doi.org/10.1063/1.1688341http://dx.doi.org/10.1063/1.1688341

Mueller, T. J. (1999). Aerodynamic Measurements at Low Reynolds Number forFixedWingMicro-Air Vehicles. RTOAVT/VKI Special course on development andoperation of UAVs for military and civil applications. Belgium: VKI.

Mueller, T. J. (2002). Fixed and Flapping Wing Aerodynamics for Micro Air VehicleApplications. Reston, VA: AIAA.

Muijres, F. T., Johansson, L. C., Bowlin, M. S., Winter, Y. and Hedenström, A.(2012). Comparing aerodynamic efficiency in birds and bats suggests better flightperformance in birds. PLoS ONE 7, e37335.

Murphy, J. T. and Hu, H. (2010). An experimental study of a bio-inspired corrugatedairfoil for micro air vehicle applications. Exp. Fluids 49, 531-546.

Mydlarski, L. and Warhaft, Z. (1996). On the onset of high-Reynolds-number grid-generated wind tunnel turbulence. J. Fluid Mech. 320, 331-368.

Nudds, R. L. and Dyke, G. J. (2010). Narrow primary feather rachises inConfuciusornis and Archaeopteryx suggest poor flight ability. Science 328,887-889.

Pedro, H. andKobayashi, M. H. (2008). Numerical study of stall delay on humpbackwhale flippers. 46th AIAA Aerospace Sciences Meeting and Exhibit, Reno, NV:AIAA.

Pennycuick, C. J. (2008). Modelling the Flying Bird. Burlington, MA: Elsevier.Preston, J. H. (1958). TheminimumReynolds number for a turbulent boundary layerand the selection of a transition device. J. Fluid Mech. 3, 373-384.

Rees, C. J. C. (1975a). Aerodynamic properties of an insect wing section and asmooth aerofoil compared. Nature 258, 141-142.

Rees, C. J. C. (1975b). Form and function in corrugated insect wings. Nature 256,200-203.

Schlichting, H. (1979). Boundary Layer Theory. New York, USA: McGraw-Hill.Schmidt, G. S. and Mueller, T. J. (1989). Analysis of low Reynolds numberseparation bubbles using semi-emperical methods. AIAA J. 27, 993-1001.

Schröder, A., Geisler, R., Staack, K., Elsinga, G. E., Scarano, F., Wieneke, B.,Henning, A., Poelma, C. and Westerweel, J. (2011). Eulerian and Lagrangianviews of a turbulent boundary layer flow using time-resolved tomographic PIV.Exp. Fluids 50, 1071-1091.

Shyy, W. (2013). An Introduction to Flapping Wing Aerodynamics. Cambridge:Cambridge University Press.

Simons, M. (1994). Model Aircraft Aerodynamics. Argus Books.Spedding, G. R. and Hedenström, A. (2009). PIV-based investigations of animal

flight. Exp. Fluids 46, 749-763.Spedding, G. R., Hedenström, A. H., McArthur, J. and Rosen, M. (2008). The

implications of low-speed fixed-wing aerofoil measurements on the analysis andperformance of flapping bird wings. J. Exp. Biol. 211, 215-223.

Taylor, H. D. (1947). The Elimination of Diffuser Separation by Vortex Generators(R-4012-3). United Aircraft Corporation Report R-4012-3.

van Nierop, E. A., Alben, S. and Brenner, M. P. (2008). How bumps on whaleflippers delay stall: an aerodynamic model. Phys. Rev. Lett. 100, 054502.

Vargas, A. and Mittal, R. (2004). Aerodynamic performance of biological airfoils.2nd AIAA Flow Control conference, Portland, OR: AIAA.

Videler, J. J. (2006). Avian Flight. Oxford: Oxford University Press.Videler, J. J., Stamhuis, E. J. and Povel, G. D. E. (2004). Leading-edge vortex lifts

swifts. Science 306, 1960-1962.White, F. M. (1991). Viscous Fluid Flow. New York, USA: McGraw-Hill.Winzen, A., Roidl, B., Klän, S., Klaas, M. and Schröder, W. (2014). Particle-image

velocimetry and force measurements of leading-edge serrations on owl-basedwing models. J. Bionic Eng. 11, 423-438.

Yuan, W., Mahmood, K., Windte, J., Scholz, U. and Radespiel, R. (2005). Aninvestigation of low-Reynolds-number flows past airfoils. 23rd AIAA Aplliedaerodynamics conference, Toronto, Canada: AIAA.

3191

RESEARCH ARTICLE Journal of Experimental Biology (2015) 218, 3179-3191 doi:10.1242/jeb.121426

Journal

ofEx

perim

entalB

iology

http://dx.doi.org/10.1371/journal.pone.0037335http://dx.doi.org/10.1371/journal.pone.0037335http://dx.doi.org/10.1371/journal.pone.0037335http://dx.doi.org/10.1007/s00348-010-0826-zhttp://dx.doi.org/10.1007/s00348-010-0826-zhttp://dx.doi.org/10.1017/S0022112096007562http://dx.doi.org/10.1017/S0022112096007562http://dx.doi.org/10.1126/science.1188895http://dx.doi.org/10.1126/science.1188895http://dx.doi.org/10.1126/science.1188895http://dx.doi.org/10.1017/S0022112058000057http://dx.doi.org/10.1017/S0022112058000057http://dx.doi.org/10.1038/258141a0http://dx.doi.org/10.1038/258141a0http://dx.doi.org/10.1038/256200a0http://dx.doi.org/10.1038/256200a0http://dx.doi.org/10.2514/3.10210http://dx.doi.org/10.2514/3.10210http://dx.doi.org/10.1007/s00348-010-1014-xhttp://dx.doi.org/10.1007/s00348-010-1014-xhttp://dx.doi.org/10.1007/s00348-010-1014-xhttp://dx.doi.org/10.1007/s00348-010-1014-xhttp://dx.doi.org/10.1017/CBO9781139583916http://dx.doi.org/10.1017/CBO9781139583916http://dx.doi.org/10.1007/s00348-008-0597-yhttp://dx.doi.org/10.1007/s00348-008-0597-yhttp://dx.doi.org/10.1242/jeb.007823http://dx.doi.org/10.1242/jeb.007823http://dx.doi.org/10.1242/jeb.007823http://dx.doi.org/10.1103/PhysRevLett.100.054502http://dx.doi.org/10.1103/PhysRevLett.100.054502http://dx.doi.org/10.1093/acprof:oso/9780199299928.001.0001http://dx.doi.org/10.1126/science.1104682http://dx.doi.org/10.1126/science.1104682http://dx.doi.org/10.1016/S1672-6529(14)60055-Xhttp://dx.doi.org/10.1016/S1672-6529(14)60055-Xhttp://dx.doi.org/10.1016/S1672-6529(14)60055-X

/ColorImageDict > /JPEG2000ColorACSImageDict > /JPEG2000ColorImageDict > /AntiAliasGrayImages false /CropGrayImages true /GrayImageMinResolution 150 /GrayImageMinResolutionPolicy /OK /DownsampleGrayImages true /GrayImageDownsampleType /Bicubic /GrayImageResolution 200 /GrayImageDepth -1 /GrayImageMinDownsampleDepth 2 /GrayImageDownsampleThreshold 1.32000 /EncodeGrayImages true /GrayImageFilter /DCTEncode /AutoFilterGrayImages true /GrayImageAutoFilterStrategy /JPEG /GrayACSImageDict > /GrayImageDict > /JPEG2000GrayACSImageDict > /JPEG2000GrayImageDict > /AntiAliasMonoImages false /CropMonoImages true /MonoImageMinResolution 400 /MonoImageMinResolutionPolicy /OK /DownsampleMonoImages true /MonoImageDownsampleType /Bicubic /MonoImageResolution 600 /MonoImageDepth -1 /MonoImageDownsampleThreshold 1.00000 /EncodeMonoImages true /MonoImageFilter /CCITTFaxEncode /MonoImageDict > /AllowPSXObjects false /CheckCompliance [ /None ] /PDFX1aCheck false /PDFX3Check false /PDFXCompliantPDFOnly false /PDFXNoTrimBoxError false /PDFXTrimBoxToMediaBoxOffset [ 34.69606 34.27087 34.69606 34.27087 ] /PDFXSetBleedBoxToMediaBox false /PDFXBleedBoxToTrimBoxOffset [ 8.50394 8.50394 8.50394 8.50394 ] /PDFXOutputIntentProfile (None) /PDFXOutputConditionIdentifier () /PDFXOutputCondition () /PDFXRegistryName () /PDFXTrapped /False

/CreateJDFFile false /Description > /Namespace [ (Adobe) (Common) (1.0) ] /OtherNamespaces [ > /FormElements false /GenerateStructure false /IncludeBookmarks false /IncludeHyperlinks false /IncludeInteractive false /IncludeLayers false /IncludeProfiles false /MultimediaHandling /UseObjectSettings /Namespace [ (Adobe) (CreativeSuite) (2.0) ] /PDFXOutputIntentProfileSelector /DocumentCMYK /PreserveEditing true /UntaggedCMYKHandling /LeaveUntagged /UntaggedRGBHandling /UseDocumentProfile /UseDocumentBleed false >> ]>> setdistillerparams> setpagedevice