RESEARCHARTICLE

Smokevisualizationoffreeflyingbumblebeesindicates
independentleadingedgevorticesoneachwingpair
RichardJamesBomphreyGrahamK.Taylor
AdrianL.R.Thomas
Received:2June2008/Revised:16January2009/Accepted:5February2009
SpringerVerlag2009
AbstractIthasbeenknownforacenturythatquasi
steadyattachedflowsareinsufficienttoexplainaerody
namicforceproductioninbumblebeesandmanyother
insects.Mostrecentstudiesoftheunsteady,separatedflow
aerodynamicsofinsectflighthaveusedphysical,analytical
ornumericalmodelingbaseduponsimplifiedkinematic
datatreatingthewingasaflatplate.However,despitethe
importanceofvalidatingsuchmodelsagainstlivingsub
jects,fewgooddataareavailableonwhatrealinsects
actuallydoaerodynamicallyinfreeflight.Hereweapply
classicalsmokelinevisualizationtechniquestoanalyzethe
aerodynamicmechanismsoffreeflyingbumblebeeshov
ering,maneuveringandflyingslowlyalongawindtunnel
(advanceratio:0.2to0.2).Wefindthatbumblebees,in
commonwithmostotherinsects,exploitaleadingedge
vortex.However,incontrasttomostotherinsectsstudied
todate,bumblebeesshedbothtipandrootvortices,withno
evidenceforanyflowstructureslinkingleftandright
wingsortheirnearwakes.Theseflowtopologieswillbe
lessefficientthanthoseinwhichleftandrightwingsare
aerodynamicallylinkedandshedonlytipvortices.While
thesetopologiesmightsimplyresultfrombiologicalcon
straint,itisalsopossiblethattheymighthavebeen
specificallyevolvedtoenhancecontrolbyallowingleftand
rightwingstooperatesubstantiallyindependently.
1Introduction
Theurbanmyththataerodynamicistshaveproventhat
bumblebeescannotflycanbetracedbacktoatleast1919,
whenanengineer,Hoff(1919),useddatafromanento
mologist,Demoll(1918),tosuggestthatanimalsflewusing
thesameattachedflowaerodynamicsasfixedwingair
craft.Demoll(1919)responded,usingHoffsequations
(Hoff1919),toshowthatthiscouldnotbetruebecausea
beewouldrequirealiftcoefficientovertwicethatofany
aircraft,oncethespeedofthebeatingwingswastakeninto
account.Studieswithrealandmodelinsectshavesince
shownthattheyuseunsteadyseparatedflowstoenhance
aerodynamicforceproduction,soinitsmostgeneralsense,
thebumblebeeparadoxmaynowbesaidtobesolved
(Bomphreyetal.2005;Dickinsonetal.1999;Ellington
etal.1996;Maxworthy1979;SrygleyandThomas2002;
Thomasetal.2004)(forreviews,seeBomphrey2006;
Lehmann2004;Sane2003).Nevertheless,fundamental
detailsoftheseaerodynamicmechanismsremainunre
solved,anditisthosewhichweaddresshere.
Theseparatedflowsusedbyinsectsusuallyinvolvethe
formationofacoherentvorticalstructureoverthesuction
surfaceofthewing.Thisvortexistypicallygenerated
throughseparationattheleadingedge,andforthisreason
iscommonlyknownasaleadingedgevortex(LEV).One
fundamentalquestionforaerodynamicistsiswhetherand
howLEVtopologyvarieswithwingmorphology,advance
ratio,andstageofstroke.Thisissignificant,becausethe
topologyoftheLEVpotentiallygovernssuchkeyissuesas

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DOI10.1007/s0034800906318

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aerodynamicefficiency,vortexstabilityandcontrol
authority(Bomphrey2006;Thomasetal.2004).Consid
eringonlytheprimaryvortex,thethreemostbasictypesof
flowtopologyareasfollows,eachdifferingfundamentally
intheflowatthewingrootandmidlineoftheanimal:(1)a
singlecontinuousLEVspanningfromleftwingtiptoright
wingtip,withafreeslipfocusoverthethoraxandatip
vortextrailingfromeachwing(Fig.1a);(2)separateLEVs
ontheleftandrightwings,eacharisingfromafocusatthe
wingrootwithatipvortextrailingfromeachwing
(Fig.1b);(3)separateLEVsontheleftandrightwings,
eachleadingintotheirownrootandtipvortexsystem
(Fig.1c).Whereasthefirstcategoryislikelytocome
closesttodevelopinganevendownwashdistribution,
therebymaximizingaerodynamicefficiency,thesecond
andthirdcategoriesmayoffergreaterpotentialforinde
pendentoperationoftheleftandrightwings,andhence
greatercontrolauthority.StabilityoftheLEVineachcase
willdependupontherateoftransportofvorticityalongthe
vortexcore,whichmightbepromotedbythesecondcat
egoryofLEVflowtopology,resemblingasitdoesthe
stableLEVofasweptwingaircraft.Muchattentionhas
beenpaidtothistransportofvorticityinrealinsects(e.g.
Bomphreyetal.2005;Bomphreyetal.2006a,b;Ellington
etal.1996),scalemodels(e.g.BirchandDickinson2001;
Ellingtonetal.1996)andcomputationalsimulations(Shyy
andLiu2007),althoughwithvaryingconclusionsastoits
importance.
ThefirstcategoryofLEVflowtopology(Fig.1a)has
beenobservedinanumberofrealinsects,includingfree
flyingbutterflies(SrygleyandThomas2002)anddragon
flies(Thomasetal.2004).ThesecondcategoryofLEV
flowtopology(Fig.1b)hasbeenobservedinstudieswith
mechanicalmodels(BirchandDickinson2001;Ellington
etal.1996),andislikelyalsotooccurinrealinsects
especiallyintheearlystagesofLEVformation(Bomphrey
etal.2005).ThethirdcategoryofLEVflowtopology
(Fig.1c)issuggestedbyflowvisualizationsonmechanical
models(RamasamyandLeishman2006).Itisimportantto
emphasizethatwhilethesetopologiesarestrictalternatives
atanygiveninstant,thereisnoreasonwhyinsectsshould
nottransitionbetweenthesetopologieswhenmoving
betweenhoveringandforwardflight,orevenatdifferent
stagesofthewingstroke.Indeed,wehaveobservedthe
LEVtopologyoffreeflyinginsectstochangefromoneto
stroketothenext(butterflies:SrygleyandThomas2002)
andevenwithinastroke(dragonflies:Thomasetal.2004).
Thisabilitytorapidlychangekinematics,andtherebyto
controlflowtopology,maywellbeimportantinflight
control.Inthispaper,wedescribetheflowtopologies
observedaroundbumblebeesatdifferentstagesofthe
strokeandinarangeofdifferentfreeflightconditions.No
singleimageshowstheentirewaketopologyatanystage
ofthestroke.Rather,multipleexamplesarepresentedfor
eachoftheflowelementswedescribeandeachare
groupedaccordingtothestageofthewingstrokecyclein
whichtheyareobserved.Withthistechnique,wecan
concludefordifferenttimesthroughoutthecyclewhichis
themostlikelygrosstopologicalstructurefromanumber
ofsimplehypothesesusingwhatareinfactquitecoarse
featuresoftheflow.
Wechoosetoworkwithrealbumblebees,ratherthan
models,becauseweareinterestedinunderstandingthe
aerodynamicsofrealinsects,andexistingmodelsarenot
yetabletoapproachthecomplexityrevealedinstudiesof
insectwingbeatkinematics(Walkeretal.2008,2009).
Althoughmodellingapproacheshavemanyadvantages,the
paucityofhighresolutiondataoninsectwingkinematics
hasmeantthatmodellingstudiestodatehavenecessarily
usedhighlysimplifiedwingkinematics.Inmostcases,the
C
A
B
Fig.1Threehypothesesforseparatedflowsoverinsectwings.a
ContinuousboundLEVspanningfromwingtiptowingtipwithfree
slipfocusoverthebody.Wingtipvorticespresentbutnoroot
vortices.bAconicalspiralLEVstructureoneachwingwithafocus
oneachwingsurfaceclosetotheroot.Wingtipvorticespresentbut
norootvortices,andattachedflowoverthebody.cAseparateLEV
oneachwingwithnofocionthesurfacesofthewings:instead,the
LEVstructuresinflectintothewingtipandwingrootvortices
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wingistreatedasarigidflatplate,whichnecessarily
neglectstheeffectsofvaryingcamberandtwist.Incon
trast,ourhighspeeddigitalvideoofrealbumblebees
showsthattheirwingsnotonlytwistbutalsofoldthrough
upto90alongthehingelikerowofhooksjoiningthe
leadingedgeofthehindwingstothetrailingedgeofthe
forewings.Inconsequence,rigidflatplatemodelscannot
necessarilybeassumedtoreplicatetheflowsgeneratedby
realinsects.
Simplifiedmodelsofinsectaerodynamicsoughtideally
tobetestedagainstdatafromrealinsects.Inrecentyears,
wehavesuccessfullyappliedthequantitativeflowvisual
izationtechniqueofDigitalParticleImageVelocimetry
(DPIV)torealinsects(Bomphrey2006;Bomphreyetal.
2005,2006a,b).Nevertheless,wechoosetousethequal
itativetechniqueofsmokevisualizationforthisstudy,
becauseitisbettersuitedtodescribingtheflowtopologies
ofreal,freeflyinginsectsthanDPIVoranyavailable
quantitativevisualizationtechnique.Inparticular,smoke
visualizationovercomesthepracticaldifficultyofencour
aginganinsecttoflyfreelyundertheconditionsofdim
ambientlighting,brightlaserilluminationandvolume
seedingoftheflowwhichDPIVrequires.Moreover,
althoughDPIVcanyieldprecisemeasurementsoftheflow
field,thedifficultyofderivingforcesfromtimevarying
velocityvectorfieldshasmeantthatthetechniquehas
rarelybeenusedtoitsfullquantitativepotentialinstudying
animallocomotion(Dabiri2005;Nocaetal.1999).In
consequence,wefindthattheclassicaltechniqueofsmoke
visualizationiswellsuitedtoourpurposeofdescribingthe
flowtopologiesofinsects.Itisalsoworthnotinginthis
contextthatallofthefundamentalfluiddynamicsworkon
thetopologyof3Dunsteadyseparatedflowsisbasedupon
qualitativevisualizationtechniques(Dlery2001;Perry
andChong1987).
2Experimentaldetails
Acolonyofapproximately100bumblebeesBombuster
restriswastrainedtoforagefromanestinthelaboratoryto
apollenandnectarsourceintheworkingsectionofalow
speedwindtunneloperatingat1.2ms1.Thispollenand
nectarsourcewasremovedduringexperimentstoavoid
interferingwiththeflow.Weusedahighresolution
smokewiretechnique(Thomasetal.2004)togeneratea
verticalplaneofsmokelineswithapproximately1mm
spacing(onetenthofthewinglength).Theprimaryevi
denceprovidedinthispaperissmokevisualizations,and
whilewebaseourconclusionsonthemostcomprehensive
setofflowvisualizationsofanyanimaltodate,itmustbe
borneinmindthatsmokevisualizationisaninherently
qualitativetechnique,withrestrictedspatialresolution.
Quantitativeconfirmationoftheresultspresentedhereare
required,forexamplethrough3DPIVwithfreeflying
insects.Alimitationwithsmokeinairvisualizationisthat
theresidencetimeofthesmokeparticlescanbelonger
thanthepersistenceofvorticityinthewake.Thiseffectis
knowntobeproblematicinthefarwake,wheresmoke
streaksappeartobedelineatingvorticeslongafterthe
vorticityhasdiffused(Cimbalaetal.1988).Here,however,
wereferonlytowakestructuresyoungerthanonewing
beatperiod(1/180s)ataReynoldsnumberofRe=2,500
(basedonmeanwingtipspeed).
Imagesequenceswererecordedusinghighspeeddigital
videocamerasalignednormaltothesmokeplaneacquiring
dataateither1,000fps(HiDCamII:NACImageTech
nology,CA,USA;1,2809512px;fieldofview
width=85mm;1px=0.066mm;exposuretime=
1/1,000s)or2,100fps(Phantomv7:VisionResearchInc,
NJ,USA;1,0249512px;fieldofviewwidth=90mm;
1px=0.088mm;exposuretime=1/2,100s).
Intotal,wewereabletovisualize511aerodynamically
informativewingbeatsfrom32separateflightsequences,in
whichthebeesperformedavarietyofmaneuvers.In413of
thesewingbeats,thebeesweretravellingapproximately
paralleltothelongaxisofthetunnel,facingeitherintoor
awayfromtheflow.Oftheremaining98wingbeatswe
observed,78involvedquarteringflightinwhichthebee
moveddiagonaltothefreestream,andafurther20in
whichthebeetranslatedsidewayswithrespecttothe
freestream,atairspeedsashighas1.4ms1.
Wewereabletodeterminethebeesairspeed(V)while
theywereflyingintheplaneofthesmokebyreferenceto
theconvectionofsmokestructuresinthefreestreamof
1.2ms1.Thebeesflewatarangeofairspeedsfrom
1.5ms1(slowbackwardsflight)to1.8ms1(slow
forwardsflight).Althoughwedidnotmeasurestroke
amplitude(U)directly,bumblebeestypicallyoperatewith
astrokeamplitudeofapproximately2rad(Dudleyand
Ellington1990).Themeanwingbeatfrequency(f)across
flightsequenceswas180Hz(s.d.=13.6Hz,n=32flight
sequences),sotherangeofairspeedsweobservedcorre
spondsapproximatelytoadvanceratiosintherange
0.2\J\0.2,whereJ=V/2UfR(Ellington1984)and
winglength(R)isapproximately10mm.Flightwithan
advanceratio|J|\0.1isconventionallyclassedashov
ering,sotherangeofflightconditionsweobserved
bracketshoveringflight(Ellington1984).Theseadvance
ratiosareeasilyinterpretableforforwardsandbackwards
flight,butareoflittleuseforthemanyotherorientations
ourfreeflyingbumblebeesadopted.Forexample,how
shouldJbecalculatedwhenthebumblebeeisholding
stationinthewindtunnel,butorientedroughlyperpen
diculartotheincidentflow?Inthiscase,forwards
backwardsvelocityinthebeesframeofreferenceis
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0ms1,buttheoncomingflow(fromtheside)is1.2ms1
soavalueofJ=0wouldbemisleadingsinceitdoesnot
tellthefullstoryabouttheflowphysics.
3Results
Theflowtopologyweobservedchangedthroughthe
wingbeat,butdidsoinaratherstereotypedmanner,
despitetherangeofflightconditions.Figure2
presentsa
typicalwingbeat.Wefoundnoevidenceofflowsepa
rationduringthefirstpartofthedownstroke(Fig.2a)in
anyofourrecordedsequences(furtherevidencein
Fig.3).However,bythetimeofsupinationattheendof
thedownstroke,theflowoverthewingshadseparatedto
formaLEV,andthatLEVpersistedwellintothe
upstroke.Duringsupination(Fig.2c),apointalongthe
forwardlineofattachmentcanclearlybeseenon
theundersideofthewing,whereasmokelineimpacts
thewingapproximatelyhalfwayalongitslength(yellow
arrow).Thesmokelinedirectlyabovethisonebifurcates:
onebranchflowsintothewakebehindthebumblebee;
theotherbranchflowsupstreamandreattachesonthe
winguppersurface(redarrow),delineatingaLEVover
halfachordindiameter.Atthebeginningofthe
upstroke(Fig.2d),thelinesofattachment(yellowarrow)
andreattachment(redarrow)remainontheunderside
anduppersideofthewings,respectively,indicatingthat
thecirculationcontinuestobeofthesamesensefol
lowingstrokereversal.However,bymidupstroke
(Fig.2e),theLEVhasbeenshed.ThetimingofLEV
formationispresentedforafurther10wingbeatsin
Fig.3.Thefirstframecapturingsupinationishighlighted
inyellowandthisisalwaysconcurrentwiththefirst
unambiguousappearanceoftheLEV(whitearrows),
whichindicatesthattheLEVisformedinthelatterpart
ofthedownstroke.Aswenowshow,thetopologyofthe
LEVmatchesthathypothesizedinFig.1catthisstagein
thestrokecycle.
Duringatypicaldownstroke,trailingvorticesareshed
fromboththewingtipsandthewingroots.Thisdemon
stratesthattheLEVisnotoftheformhypothesizedin
Fig.1aorb.Figure4
presentsanexampleofquartering
flight,inwhichtheattitudeofthebeemakesitpossibleto
Fig.2Bumblebeestrokesequenceinforwardsflight,witharrowed
smokelinesvisualizingpointsofattachment(yellow)andreattach
ment(red).Thesmokelinewhichreattachesdelineatestheextentofa
LEVformedatsupination.Webeginthecyclewithpronation
occurringimmediatelypriorto(a):pronationoccursagainin(f).
Overallimagebrightnessandcontrasthavebeenincreasedtobest
visualizethesmokelinesthisinevitablyincursalossofdetailonthe
wingsurfacewhenitisangledsuchthattheilluminationreflectsback
intothecameralens.Framesseparatedby1ms
c
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Fig.3Threebumblebeesin
quartering(greenbackground),
sideways(redbackground)and
slowforwards(blue
background)flight,each
orientedsotheformationofthe
LEV(whitearrow)isvisualized
bysmokelines.Consecutive
framesreaddownthecolumns.
Individualwingbeats(different
columns)havebeenarrangedso
thattheframesshowingthefirst
evidenceforsupinationare
alignedhorizontally(yellow
background).TheLEVfirst
appearsintheseframes(i.e.at
strokereversal)ineach
wingbeatwhereitwas
visualized.Thethirdcolumnis
thesamewingbeatasshown
magnifiedinFig.2
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visualizethestructureofthevortexsystemalongthelength
ofthewing.Ahelicalwingtipvortexcanbeseenin
Fig.4awheretherightwingtiphasimpingedonthe
smokelines(redarrow);thewhitediagonalarrowspointto
vortexloopelementsshedbypreviouswingbeats.By
Fig.4bthewinghaspassedfurtherintothevertical
smokelineplaneandarootvortexisnowvisible(yellow
arrow).Wingtipvortices(redarrows)androotvortices
(yellowarrows)continuetotrailthewingonethirdofthe
wayintotheupstroke(Fig.4c),confirmingagainthatthe
circulationisofthesamesenseasonthedownstroke.
However,1mslater(Fig.4d),therootandtipvorticesare
shedasavortexloopinthewakebehindthebumblebee,
indicatingachangeinthecirculationaroundthewing.The
shedvortexloopdistortsandrotatesasitconvectsback
wardsanddownwardsintothewake(Fig.4df).Figure5
isanotherexampleshowingabeegeneratingacounter
rotatingpairoftip(redarrow)androot(yellowarrow)
vorticeswhileorientedsidewaystothefreestream.
AlthoughtheorientationofthebeesinFigs.4and5
make
itespeciallyeasytoseethe3Dstructureofthevortex
system,rootvorticeswereobservedinthefullrangeof
flightmodeswerecorded(MovieS1).Thestereotyped
Fig.4Bumblebeeinupwindquarteringflight,showingwingtip
vortices(redarrows,af)androotvortices(yellowarrows,bf),
whichareshedintothewakeasavortexloopbythestageofthe
upstrokeshowninpanel(e).Wakeelementsshedonpreceding
wingbeatsarearrowedinwhite(a).Seemaintextfordetailed
description.Framesseparatedby1ms.Overallimagebrightnessand
contrasthavebeenincreasedlinearly
Fig.5Bumblebeeinsidewaysflight,showingsmokelinesbecoming
entrainedincounterrotatingwingtipvortices(redarrow)andwing
rootvortices(yellowarrow).Framesseparatedby1ms
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sequenceofflowtopologieswehavedescribedistherefore
robusttolargescalechangesinthedirectionofflowrel
ativetotheinsectsbody.
FurtherconfirmationthattheLEVisnotoftheform
hypothesizedinFig.1aisprovidedbytheobservationthat
smokelinesrunningalongthemidlineofthebodypass
Fig.6Bumblebeeinforward
flightwithsmokeincidentnear
themidline,showingthe
aerodynamicindependenceof
contralateralwingpairs.See
textforcommentaryonarrowed
structure.Framesseparatedby
1ms.Overallimagebrightness
andcontrasthavebeen
increasedlinearly.Advance
ratio,J\0.2
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smoothlyintothewake,risingintheupwashbetweenthe
rootvorticeswithoutbecomingentrainedbyanycoherent
transversevortexstructure.ThisisthecaseinFig.6,
whichshowsabeeflyingupwindwiththesmokeincident
nearthemidline.InFig.6athewingsareparallelwithone
anotheratthetopoftheupstroke.Thegreenarrow
highlightsapairofsmokelinespassingtothefarsideof
therightwingpair,whichisthebrighterofthevisible
wings;thebluearrowshowsasecondpairofsmokelines
passingnearsideofthebody.Thisdistortioninthevertical
alignmentofthesmokeplaneisduetoflowinducedby
thepreviouswingbeat.InFig.6btherightwingpaircuts
theupperpairofsmokelines(whitearrow),whichquickly
rollupintoawelldefinedrootvortex(Fig.6cd,yellow
arrow).Crucially,thelowersmokelinepair(Fig.6d,blue
arrows)passingnearsideclosetothetipoftheabdo
menremainsrelativelyunaffectedasitpassestheroot
vortex.InFig.6ethesamepairofsmokelinesrisesinthe
upwash(redarrow)betweenthepairofcontralateral
vortexloops.Onlywhentheyareseveralchordlengths
behindthewingsdothesesamesmokelines(redarrows)
becomevisiblydisruptedbytherootvortices(Fig.6g).
Smokelinespassingalongthemidlineofthebodyare
thereforeacceleratedupwardsslightlyattheendofthe
downstrokeundertheinfluenceofthepairofvortexloops
shedbytheleftandrightwings,butinallotherrespects
theypassunperturbedintothewake.
4Conclusions
TheuseofaLEVhasbeenobservedinfreeflyingdrag
onflies(Thomasetal.2004)andbutterflies(Srygleyand
Thomas2002),andalsointetheredhawkmoths(Bomphrey
etal.2005;Ellingtonetal.1996).Ithasbeeninferredin
freeflyingswifts(Videleretal.2004)andhummingbirds
(Warricketal.2005),andhasbeensuggestedbyanalogy
withmechanicalflappersofChalcidwasps(Maxworthy
1979)andfruitflies(BirchandDickinson2001).Acata
logueofthevariationinLEVtopologiesobservedbetween
andwithindifferentspeciesofinsectisgiveninFig.7
(adaptedfromBomphreyetal.2005).Bumblebeessmall
wingsareatthelimitofwhatcanberesolvedwithsmoke
visualizations.Asaresult,whilethenearwakeflowswere
Fig.7Cartoontoshowthequalitativelydifferentflowtopologies
hypothesizedforinsectsonthebasisofmechanicalmodels(a),
observedinliveinsects(b,c2,d1,d2),andorboth(c1).(a)Shows
thetopologydescribedbyMaxworthy(1979)forhismechanical
flapperbasedontheclapandflingmechanismoftheChalcidwasp.
(b)Showsthetopologyfoundovertheforeandhindwingsofa
dragonflyfor75%ofthewingbeatsanalysedinThomasetal.
(2004)theyfoundseveralvariations,butthiswasconsideredtobe
thenormalcounterstrokingtopologyandwasnotsignificantly
differentfromtheinphasewingbeattopology.(c1)and(c2)shows
twotopologiesdescribedforhawkmothsbyEllingtonetal.(1996)
andBomphreyetal.(2005),thelattersuggestingthat(c1)wasa
transientstateand(c2)wasthetopologytowardtheendofthe
downstrokeoncetheflowoverthethoraxhadseparatedtoo.The
bumblebeeflowpatternpresentedin(d1earlydownstroke)and
(d2latedownstroke)representsanoveltopologywithleftandright
wingsactingindependentlyandaLEVformingatsupination(d2).
TheLEVstructuresarethereforeclearlyvariableandcanchange
throughoutthecourseofasinglewingstrokeinhawkmoths,
dragonflies,andbumblebees.AdaptedfromBomphreyetal.2005
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clear,theresolutionoftheLEVinourflowvisualizations
islowerthanhasbeenachieved,forexample,withdrag
onflies(Thomasetal.2004).Nevertheless,thedensityof
smokestreamswassufficienttoidentifythecriticalfea
turesoftheflowtopologysuchasbifurcationsand
attachmentpoints.Thebumblebeetopologieswehave
describedareshowninFig.7d1,d2,whered1represents
themajorityofthedownstrokeandd2isthetopologyatthe
endofthedownstrokeandbeginningoftheupstroke.Itis
apparentthatbumblebeesareunusualincomparisonwith
otherinsectswhichutilizeLEVstogeneratelift,inthatthe
flowappearstoremainattachedforthemajorityofthe
downstroke,firstseparatingaroundthetimeofstroke
reversal.Thismightsuggestaroleforwingrotationinthe
formationoftheLEV,althoughwehavenoinformationas
towhetherthisseparationistheresultoftheangular
velocityofthewingatsupinationortheconcomitant
increaseinangleofattack(Walker2002).
TheultimatestructureofthebumblebeeLEV(Fig.7d2)
bearssomeresemblancetothatofMaxworthys(1979)
flappingmachine(Fig.7a)inthataLEVispresentwhich
doesnotterminateonthewingsurface.Nevertheless,the
twoaredistinctinthattherootvorticesarenotlinkedinthe
bumblebeeastheyareinMaxworthys(1979)flapping
machine.Althoughourdatahaveinsufficienttemporal
resolutiontoobservetransientstagesinLEVdevelopment,
itisquitepossiblethattheLEVtopologywehaveobserved
inbumblebees(Fig.7d2)developsfromanattachedflow
topology(Fig.7d1)viaatransientstatelikethatproposed
byEllingtonetal.(1996)forhawkmoths(Fig.7c1,and
hypothesizedinFig.1b).
Inmostotherflowvisualizationsonbirds,batsandinsects
todate,theleftandrightwingpairsareaerodynamically
linkedbytransversevorticalstructures(birds:(Kokshaysky
1979;Spedding1986;Spedding1987;Speddingetal.2003;
Videleretal.2004;Warrick,TobalskeandPowers2005);
bats:(Hedenstrometal.2007;Norberg1976;Swartzetal.
2005);insects:(Bomphrey2006;Bomphreyetal.2005,
2006b;DickinsonandGtz1996;GrodnitskyandMorozov
1993;Lehmannetal.2005;Maxworthy1979;Srygleyand
Thomas2002;Thomasetal.2004;VandenBergand
Ellington1997;Willmottetal.1997)).Incontrast,our
bumblebeeflowvisualizationsprovidenoevidencefor
suchstructureslinkingtheleftandrightwings.Thesame
maybetrueofotherinsectspecies,includingcrane
flies,whichhavealsobeenshowntogeneratewingroot
vorticesinadditiontotheusualwingtipvortices(Brodsky
1994).Thismustresultinalossofefficiency,because
unlikemanyotherinsects,bumblebeesandcranefliesarenot
usingthefullspanbetweentheirwingtipstogeneratelift,
andindeedwastefullyaccelerateairupwardsinthevicinity
ofthebody.
Figure8depictstheconsequencesofrootvorticesfor
thedownwashdistribution.Figure8aisacartoondepicting
instantaneousstreamlinesinaverticalplanebehindthe
trailingedgesofabumblebeeandalocust.Figure8bisa
cartoonofthecorrespondingdownwashdistributions.In
thecaseofthelocust,wehavemadeuseofquantitative
DPIVmeasurementsofthewaketoinformthefigure
(Bomphreyetal.2006b);inthecaseofthebumblebee,we
havebasedtheexpecteddownwashdistributiononatyp
icalvelocityprofilethroughtwovortexrings.Whilethe
diagramsareidealizedrepresentationsofthetrueflows,the
rootvorticeswhicharepresentinthebumblebeemust
necessarilymakethedownwashdistributionlesseventhan
thatbehindthelocust.Anydeviationfromtheidealeven
A
B
Fig.8Cartoonoftheflowexpectedmiddownstrokebehinda
bumblebee(left)andmeasuredbehindadesertlocust(right).Atthe
toptheinsectsaredepictedflyingintothepage.Redboxes(a)
representaplanealignedverticallybehindthetrailingedgesofthe
insectswingsandshowa2Dslicethroughtheflowwith
instantaneousstreamlines.Yellowboxes(b)showthepredicted
downwashdistributioninthesameplanebehindthetwoinsectsthe
locustdistributionbeinganidealizedprofilebasedonDPIV
measurement(Bomphreyetal.2006b).Greydashedlinesrepresent
theedgeofthetrailingvortexcores
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downwashdistributionisasourceofaerodynamicineffi
ciency,reinforcingourconclusionthattheflowtopologyof
bumblebeesisaerodynamicallyinefficientatallstagesof
thestroke.Thegeneralconclusionoverthebumblebees
inefficiencyisconsistentwiththeconclusionsAltshuler
etal.(2005)drewforhoneybees(Apismellifera).While
theydidnotobservetheaerodynamicsdirectlyandattrib
utedenhancedlifttowakecaptureandrapidrotationofthe
wings,honeybeesfillasimilarecologicalnicheandalso
underperformintermsofefficiencyduringnormalflight
byoperatingwithashallowstrokeamplitude.
Whyhasnaturalselectiontoleratedsuchinefficiency?
Theaerodynamicindependenceofleftandrightwingpairs
inbumblebeesmightsimplyresultfromthebiological
constraintofhavingawidethoraxtohousethemassive
flightmotorrequiredfortheirloadcarryingforagingstyle.
Asaresultthewingrootsarewidelyseparatedinrelation
tothewinglength,andasthisratioincreases,thisisbound
atsomepointtoleadtotheirindependentoperation.
Alternatively,theaerodynamicindependenceofthewing
pairsmightreflectthelowandnegativeadvanceratiosat
whichthebeesflewinthesequenceswehavevisualized.
Atsuchlowairspeeds,theremaysimplybeaninsufficient
flowvelocitynearthewingbasetogenerateasignificant
circulationincomparisonwiththatgeneratedfurtherout
alongthewing.Finally,itisalsopossiblethattheinde
pendenceofleftandrightwingpairsmightenhancecontrol
authorityandcouldthereforerepresentanadaptationfor
manoeuvringbetweenflowers.
AcknowledgmentsResearchsponsoredbyBBSRCStudentship
00A1S06405.RJBisaPDResearchFellowatStAnnesCollege,
Oxford.GKTisaRoyalSocietyUniversityResearchFellowand
RCUKAcademicFellow.TheauthorsaregratefultotheBBCfor
loaningthePhantomhighspeeddigitalvideocamera.
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