4830 date. Duringsuchajump,E.minuta jumping musclerangedfrom28,000to140,200 exerted aforceof12–29 energy expenditureof76–225 experienced 225–375 5.8 ms 402 Received 3July2013; Accepted3October2013 *Author ([email protected]) for correspondence Zoology, Cambridge, CambridgeCB23EJ, of UK. University of Department muscles inthethoraxtopropel rapidmovementofthetwohind characterised bytheuseofsamelarge trochanteraldepressor Cercopoidea (froghoppers)andFulgoroidea().All are jumpers: theMembracoidea(leafhoppersandtreehoppers), the contains threegroupsthateachhavemembersare able sub-order ,whichisunlikelytobemonophyletic, of insectsthatcontainsthemostablejumpersisHemiptera. The specialisations ofthemuscles,skeletonandlimbjoints.One order legs inadifferent way from thoseusedforwalking,and movements requiresparticularmotorpatternsthatcoordinate the or tolaunchintoflight.To generatesuchrapidandpowerful repertoire toenablefastmovementorrapidescapefrompredators, Many speciesofinsectsincludejumpingintheirlocomotory Auchenorrhyncha KEY WORDS:Kinematics,Biomechanics,Resilin, velocity, the tibiae.Inbestjumps,definedasthosewithfastesttake-off by largemusclesinthethorax,andwasaccompaniedextensionof simultaneous depressionofthetrochanterabothhindlegs,powered were ofsimilarlength.Jumpingwaspropelledbyrapidand species inwhichthefrontlegswereparticularlylargesothatall body lengthand30–50%longerthanthefrontlegs,exceptinone length andfrom6to23 streamlined appearance.Thebodysizerangedfrom6to9 characterised byanelongatedandtaperingheadthatgavea were analysedfromhigh-speedimages.Thebodyshapeinallwas the familyDictyopharidae,fromEurope,SouthAfricaandAustralia, The jumpingperformanceoffourspecieshemipteransbelongingto Malcolm Burrows* (, Dicytyopharidae) Jumping mechanismsindictyopharidplanthoppers RESEARCH ARTICLE © 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,402-413doi:10.1242/jeb.093476 substantially affect forwardmomentum. performance byreducingdrag,which,forasmallinsect,can is suggestedthattheirstreamlinedbodyshapeimprovesjumping be usingapoweramplificationmechanismincatapult-likeaction.It muscle. To achievesuchajumpingperformance,theseinsectsmust thus greatlyexceededthemaximumactivecontractilelimitofnormal INTRODUCTION ABSTRACT ms −1 Engela minuta , whichisthefastestachievedbyanyinsectdescribedto −2 or 490 g,whileotherspeciesinthesamefamily g. Thebestjumpsinallspeciesrequiredan accelerated in1.2

mg inmass.Thehindlegswere80–90%of mN. Therequiredpoweroutputpermassof μJ, apoweroutputof12–80 experienced anaccelerationof

ms toatake-off velocityof

W

kg − 1 muscle and

mW and mm in family affects jumpingperformance. Itisshown groupandtoassess whethertheelongatedbodyof discovered foronefamilyextend acrossotherfamiliesofthe of thispaperistodetermine whetherthecharacterssofar so thattherangeofoverallappearance differs markedly. Theaim families showagreatdiversity inthesizeandshapeofbody so farbeenanalysedtodetermine jumpingmechanisms.Theother between thetwohindlegswhenjumping(Burrows,2009). lacking infroghoppers,andthatensuressynchronyofmovement mechanical interactionbetweentheleftandrighttrochanterathat is femur thatbearsnomicrotrichia. is prominentbutitengageswithaflat,slightlyraisedareaon the absent. Intheplanthoppers (Burrows, 2006b).Bycontrast,inleafhopperstheprotrusions are and mustdisengagebeforedepressionofthehindlegscan occur coxal andfemoralprotrusionsthatarebothcoveredinmicrotrichia levated inpreparationforajump.Froghoppershaveprominent engagement betweenthecoxaeandfemurwhenhindlegs are hind legs(Burrows,2010). rapidly toreleasethestoredenergy andpropelthedepressionof energy oftheseprolongedmusclecontractionsandthenunfurl in preparationforajump(Burrowsetal.,2008).Theystorethe archery bowswhenthelarge trochanteraldepressormusclescontract resilin (AndersenandWeis-Fogh, 1964),andwhicharebentlike that areacompositeofhardcuticleandtherubber-like protein internal skeletalstructuresinthemetathorax,calledpleuralarches, leaves, thespecialityofleafhoppers. more compliantsurfacesandthereforeenabletake-off fromflexible Longer legsshouldthereforereduceenergy losswhenjumpingfrom than thoseappliedbyshorterlegs(BurrowsandSutton,2008). take longertoacceleratesothatgroundreactionforcesarelower rate (Alexander, 1995;Bennet-Clark,1990).Longerlegs,however, stored inelasticcuticularstructuresisnearlyindependentofstrain when acatapultmechanismisusedbecausethereleaseofenergy length ofthehindlegsdoesnot,however, affect thetake-off velocity 50–70% ofbodylength(Burrows,2006a;Burrows,2009).The that areonly40–50%longerthantheotherlegsandapproximately 2007b). Bycontrast,froghoppersandplanthoppershavehindlegs than theotherlegsandare90%ofbodylength(Burrows, and intheanatomyofcoxae. include differences inbodyshape,thelengthofhindlegs specialisations ofitsownthatdefinejumpingabilities.These important commonfeatures,eachgrouphasparticular (Burrows, 2006a;Burrows,2007b;2009).Despitethese contract slowly, energy isstoredandthenreleasedsuddenly mechanism isusedinwhichthetrochanteraldepressormuscles legs inthesameplaneunderneathbody. A catapult-like There are20familiesofplanthoppers,butonlyone()has The threegroupsofhopperalsodiffer inthemechanical Planthoppers, likefroghoppersbutunlikeleafhoppers,havelarge Most leafhoppershavehindlegsthataretwotothreetimeslonger coleoptratus,thecoxalprotrusion su coleoptratus Issus also havea

The Journal of Experimental Biology for anyinsect. which themeasurements weretaken.Dataaremeans ±s.e.m.Theratioofleglengthsis givenrelativetothefrontlegs. Body lengthandmass, andlengthsofthehindfemora andtibiaeinthefourspeciesofdictyopharids analysed. Species velocities of4–5.8 mechanism toacceleratein1–2 that fourspeciesfromthreecontinentsalluseacatapult species studied. Fig. RESEARCH ARTICLE europaea Raphiophora vitrea Thanatodictya praeferrata Engela minuta Table vitrea the side(A)andfromdorsal(B).(C)Photographofhead ( ( ( ( C B A N N N N

.Bodystructureindictyopharidsillustrated bytwoofthefour 1. 3 . . . . . 21.7 3.4 2.8 3.3 82 89 1.5 91 82 1.3 1.5 1 1 1 1.1 1 0.8 1 1 1 1.4 4.2±0.2 2.9 4.1±0.1 2.2±0.1 0.8 2±0.1 1.9 8.8±0.3 8.9±0.2 8.3 22.9±0.7 6.6 19.6±1.0 8.1 5.7 =7) =7) =3) =1) to showtheanteriorprotrusionfromhead. 1. Bodyformofdictyopharids Raphiophora vitrea Dictyophara europaea (A,B) Photographsof m s −1 that rankwiththehighestvaluesrecorded m)(m fmr(m tibia(mm femur(mm) (mm) (mg) oyms oylnt Hn e, Hindleg, Hindleg, Bodylength Body mass Dictyophara europaea

ms toremarkabletake-off 0.5 mm 2 mm 2 mm viewed from Raphiophora 3.5 inR.vitrea the cuberootofbodymassrangedfrom1.7in length. Thelengthofthehindlegsexpressedasaratiorelativeto species, thehindlegsrepresentedbetween82and91%ofbody suggesting thattheymightbeusedingraspingorsearching.Inall because boththefemurandtibiawereflattenedwider, front legsalsoappearedtobemoresubstantialthantheother 2).The middle tibiaeandonly13%shorterthanthehind(Fig. femora, andtothefronttibia,whichwere30%longerthan femora, whichwere50%longerthanboththemiddleandhind middle legs,sothattheratiowas1:0.8:1.Thisisduetofront the samelengthasfrontlegsbutbothwerelongerthan 1:1.1:1.5 inthelatter. Bycontrast, in longer thanthefrontlegs,withratiosof1:1:1.5informerand studied. of thehindlegsrelevanttojumpingappliesallfourspecies (Table ratio relativetothefrontlegswas1front:1middle:1.3hind hind legswere30%longerthanthefrontandmiddlesothat pairs oflegsinthreethefourspeciesanalysed.In the undersurfaceofbody. Theywerelongerthantheothertwo and bothmovedinthesameplaneaseachother, almostparallelwith each ofthefourspeciesanalysed.Theywereheldbeneathbody The hindlegsprovidedthemainpropulsiveforceforjumpingin species analysedhere, were setbackfromthefrontofheadby1to2 prominent forwardprojectionofthefronssothatcompoundeyes The bodyshapeofthefourspeciesanalysedwascharacterisedbya mesothorax andtheanterioredgesoftwohindcoxae was The ventralregionofthemetathoraxbetweenboundarywith the the fourthspecies, giving thebodyapointedandseeminglystreamlinedappearance.In minuta Structure of thehindlegs of Structure Body shape RESULTS Coxa 6.6 beyond thetipofabdomen.Thelengthbodyrangedfrom pairs ofwingsweremembranousandinallbutE.minuta were setventraltothecompoundeyesonsideofhead.Both was moreabrupt(Fig. only 100 μmindiameter, sothatthetransitionwithrestofhead higher at22.9±0.7 1). (Table mm inE.minuta )

1). InT. praeferrata and Body masswaslowestat5.7 Ratio ofleglengths rn ideHn length body Hind mass Middle Front The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476 Thanatodictya praeferrata (Table

Raphiophora vitrea mg inD.europaea. to athirdlongerat8.9±0.2

1C). Inallspeciestheantennaewereshortand 1). Thefollowingdescriptionofthestructure Dictyophara europaea N and indicates thenumber ofindividualsfrom D. europaea, thehindlegswere50% , thefronswas1.4 mg inE.minuta fbd Length(mm)/ % ofbody Hind leglength R. vitrea , theheadtaperedgradually,

mm (N , thehindlegswere (Fig.

mm. Inthreeofthe T. praeferrata 1A,B), =7) inR.vitrea E. minuta,the but fourtimes

mm longbut extended Engela 1/3 (mg) 403 to

The Journal of Experimental Biology 404 RESEARCH ARTICLE around eachside ofthebodyandcouldbeseen topivotwiththe The blackcuticleofthehindcoxae extendedlaterallyandwrapped posterior andventralextremesof thepleuralarches(Fig. the ventralmidlineandlaterally theywerefusedtothethoraxat depressed. and posteriorlywithinthethorax asthehindlegswerelevatedand of thetrochanter. Thesetendonscouldbeseentomoveanteriorly structure thatranthroughthecoxatoitsinsertiononanterior rim expansion ofthelarge tendon, whichthentaperedtoastrap-like 3A).Thefibresofthesemusclesinsertedonananteriorcircular (Fig. be seenthelarge trochanteral depressormusclesofthehindlegs covered bytransparentandflexiblemembranethroughwhich could Fig. tibial jointviewedlaterallyandthehindtibio-tarsaljointsventrally. long andthin;themiddlelegisshortest.(B)Photographsofhindfemoro- middle andhindleg.Thefrontleghasawidefemurtibia;thetibia is B A joint Hind femoro-tibial The coxaeofthehindlegswere closelyopposedtoeachotherat Femur Middle leg Hind leg

Front leg .AnatomyofthelegsRaphiophoravitrea. 2. Tibia Coxa Coxa Tarsus Trochanter Trochanter Coxa joint Hind tibio-tarsal 100 µm Femur Femur Femur Tibia Tibia Tarsus (A) Drawingsofafront, Tibia Tarsus Tibia Tarsus 1 mm

,Fg 4A). 3, Fig. in preparationforajump. which thecoxacomesintocontactwhenhindlegislevatedfully and thusfrictionwithaparticularareaofthedorsalfemur becoming morepointed.Thesemicrotrichiaincreasethesurfacearea changed inshapealongtheprotrusionitself,withtheirtips from thesurfaceofcuticleandwas5 base oftheprotrusion,eachmicrotrichiaprotrudedsome6 with microtrichiaarrangedinoverlappingrows(Fig. whole protrusionandtheadjacent,anteriorofcoxawerecovered narrowing alongits170 ventral regionofeachcoxathatmeasured80 their fullylevatedandcockedpositions. depressor musclescontractedwithoutmovingthehindlegsfrom were bentduringpreparationforajumpwhenthetrochanteral fluorescence isindicativeofthepresenceresilin.Thesestructures which didnotshowanyfluorescence(Fig. bright blue,clearlydelineatingthemfromotherthoracicstructures, illuminated withultraviolet(UV)light,thepleuralarchesfluoresced hind wings.Whenthemetathoraxwasclearedofsofttissueandthen anteriorly fromthecoxaetowardtheirdorsalarticulationswith Ugsprungsplatte (HeiligandSander, 1986;Sander, 1957)]curve thorax. both thefrontandmiddlelegspivotedindependentlywith middle coxaebythemouthpartscontainingstylets.Theof each otheratthemidlinebyposteriorpartofhead,and of theothercoxa.Bycontrast,frontcoxaewereseparatedfrom of some20 lateral wallofthethorax,allowingaforwardandbackwardrotation segment wasapair ofhooks. prevent thehindlegsfromslipping. Atthetipofdistaltarsal during ajumpandtheirorientation shouldincreasetractionandthus proximal twojoints.Thesespines werepressedagainsttheground segments witharraysofshort ventrallypointingspinesatthe its articulationwiththetarsus(Fig. spines alongitslengthandan array ofventrallypointingspinesat thin, tubularandlight.Ithadaseriesoffouroutwardlypointing (Burrows, 2006b). with thecoxalprotrusionduringpreparationforjumping location wherefroghoppershaveafemoralprotrusionthatengages a numberoflonghairsatitsperimeter. Thispatchisinthesame femur wasasmall,raisedbutflatandsmoothareaofcuticle with trochantero-femoral joint.Ontheproximaldorsalsurfaceof the (Fig. seven campaniformsensillaonitsproximalventralsurface through some170 joint consistedoftwopivotsthatallowedextensionandflexion angular excursionofthedistalpartleg.Thefemoro-tibial The jointbetweenthetrochanterandfemurallowedasmall and lateral(Fig. achieved attake-off. Thejointconsistedoftwopivots,oneventral readiness forjumping,toitsfullydepressedpositionthatwas from itsfullylevatedpositionwhenthehindlegswerecockedin A hindtrochantercouldrotateabout acoxathroughsome130 Distal segments Trochanter with thecoxa. was formedbyablackcuticularhornofthetrochanterthatengaged A posteriorlydirectedprotrusionemerged fromthelateraland The pleuralarchesoftheinternalthoracicskeleton[alsocalled The hindtibiawasthelongestsegmentofanylegs,but 4A) thatmightgiveinformationaboutstrainsatthenearby The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476 deg. A hindcoxadidnotappeartomoveindependently

3A), andonedorsalmoremedial.Eachpivot

deg (Fig. μm lengthtoapoint(Fig. 2B). Thefemurhadapatchoffiveto 2A,B). Thetarsusitselfhadthree μm widebutprogressively

3, Fig. μm atitsbase,

3B). Theblue

4B,C). Atthe 4A,B). The

μm deg

The Journal of Experimental Biology so thatthefemora werepressedagainsttheventral surfacesofthe hind legs.Theresultwasthatboth hindlegswererotatedforwards launch ofajumpwaslevation thecoxo-trochanteraljointsofboth Jumps byallspeciesanalysedshowed thefollowingfeatures. E. minuta between thetwohindlegs(Figs sequence ofmovementsindividualjointsandtheco-ordination surface oftheglasschambergavedetailedinformationabout the an insectfromunderneathasajumpwaspropelledthe front contact withthegroundandinsectbecameairborne.Views of detectable movementsofthehindlegstotimeatwhichthey lost the accelerationtimeforajumpcouldbemeasuredfrom first jump trajectories,tobedetermined(Fig. different legsandenabledthe bodyangleattake-off, aswellthe provided detailedinformationaboutthetimingofmovementsby the Side viewsasthisdictyopharidjumpedfromthehorizontal floor T. praeferrata from different orientations;side andventralviewsareillustratedfor Jumping movementswereanalysedfromhigh-speedvideostaken RESEARCH ARTICLE Kinematics of thejump Kinematics of Pleural protrusion B A arch A key elementinthepreparatorymovementsthatpreceded protrusion Coxal Coxal Femur and Pleural R. vitrea Fg 5,6;seesupplementarymaterialMovies (Figs arch Coxa Trochanter Coxa r lutae nFg and9,respectively. 8 , areillustratedinFigs Femur Femur

6, 7).Jumpsbytwofurtherspecies, Depressor tendons Middle legs Depressor tendons Femur

,Tbe2).Furthermore, 5, Table Coxa Trochanter Trochanter Coxa Trochanter 100 µm Pleural arch

ih Left Right 1, 2). ih Left Right Posterior 200 µm Posterior Anterior Anterior (Table posterior segmentsoftheabdomen(Figs the tarsiwereplacedongroundclosetolateraledgesof the legs. Thetibiaewerealsopartiallyflexedaboutthefemoraso that small protrusionsfromthedorsalsurfaceoffemorabothhind coxae andthemetathorax.Thecoxalprotrusionsthencontacted legs occurredat thesametimewithinresolution limitof0.2 views fromunderneath(Figs depression ofbothtrochanteraabout thecoxae,mostclearlyseenin propulsive movementofthe hindlegswasasimultaneous forward propulsionofthebody totake-off inajump.The first simultaneous depressionand extension ofbothhindlegsanda 41 over anarrowrangeinthedifferent species:fromameanangleof body relativetotheground.Attake-off, thebodyanglevariedonly of thefrontlegsduringthisperiodsetelevationangle the dorsal articulationofthehindwingwereseentobend.Adjustments pleural archesthatlinkthelateralarticulationofcoxawith the was variableandcouldextendtoseconds.Duringthistime, the held foraminimumoffewhundredmilliseconds,butthisperiod This initial,preparatoryperiod wasfollowedbyarapidand deg inT. praeferrata

2). arches onbothsidesfluorescebrightblueunderUVillumination. ventrally underUVandthenbrightfieldillumination.Thepleural the trochanteraldepressormuscleswereremoved,viewed (B) Superimposedimagesofthedissectedthorax,fromwhich seen throughthetransparentsoftcuticleofmetathorax. large tendonsofthetrochanteraldepressormusclescanbe dorsally arebothvisibleatthelateraledgesofthorax.The lateral andventralpartofacoxatothehingehindwing depressed aboutthecoxae.Thepleuralarcheslinking (A) Ventral viewwiththetrochanteraofbothhindlegsfully show thestructureofproximaljointshindlegs. Fig. The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476

to vitrea PhotographsofthethoraxRaphiophora 3. to ameanangleof53 6, 7).Thismovementofthetwo hind

5, 6).Thesepositionswere

deg inE.minuta 405

ms

The Journal of Experimental Biology praeferrata contact withtheground.In raised itfromthegroundsothatmiddlelegswerefirstto lose (Figs downward movementofthefemurandanextension tibia continuing depressionofahindtrochantercausedfurther closer applicationoftheproximaltarsustosubstrate.The and backwardsmovementofthefemurthatinturnresulted obscured, thisfirstpropulsivemovementwasvisibleasadownward 406 RESEARCH ARTICLE movements ofthehindlegs. Unfurling ofthebentpleuralarchesaccompaniedtheserapid (0.2 than 1%ofthejumps,onetrochanterwasseentomove1frame set bytheframerateof5000 supported byother jumpsinwhichthefrontlegs werestretchedout the laterstagesofacceleration phase.Thisconclusionis with thegrounddidnotprovide substantivethrusttosuchjumpsin coxo-trochanteral orfemoro-tibial jointssuggestedthattheircontact front legsandthelackofobservable changesintheanglesoftheir completed whenthefrontlegs lefttheground.Thepostureof ground. Inthesecircumstances, therefore,take-off was only and extensionmovementsbeforethefrontlegslostcontact with sometimes meantthatthehindlegshadcompletedtheirdepression provide propulsion.In jump onlythehindlegswereincontactwithgroundand could later, sothatduringthelastpartofacceleration phaseofthe before take-off. Thefrontlegs lostcontactbetween0.2and0.4 A BC In sideviews(Figs protrusion ms) beforetheother, butnogreaterasynchronieswereseen. Coxal 5, 8,9).Thesemovementspropelledthebodyforwardsand Trochanter Femur and D. europaea protrusion 100 µm Coxal R. vitrea 5, 8,9),wherethetrochanterwaslargely R. vitrea

s − at , however, thelengthoffrontlegs 1 used tocapturethejumps.Infewer − oaCoxa Coxa 0.8 this happenedat ms andE.minuta − 1.4 at Campaniform ms, inT. − 0.6 sensilla

ms ms ih Left Right 500 µm trochanteral Posterior Anterior 10 µm Coxo pivot during thefirst 4 one jumpby accelerated totake-off bythe movementsofthehindlegs.Inonly closed andwereneitheropenednorflappedasthebody was jumps thencrossed. hind tarsialsocametogetheratthemidlineofbodyandin some the abdomen,ortibiaecouldpartiallyflexagain(Fig. After take-off, thehindlegs eitherremainedinthisstatealongside in all,rangingonlyfrom61to 69 minuta. Intheotherthreespecies, valuewashigherbutsimilar period andinthefirst4 body relativetothegroundduring thelast1 The take-off angle,definedastheanglesubtendedbypath ofthe transition fromjumpingtoflying. after theinsectbecameairborne,sothattherewasasmooth their depressionandextensionmovements,respectively(Figs coxo-trochanteral andfemoro-tibialjointsreachedthefullextentof ground andtheinsectwasairborne(Fig. take-off, onlytodeclineoncealllegshadlostcontactwiththe velocity ofthebodycontinuedtoriseandreachedapeakjustbefore the ground. was nodifferent fromthoseinwhichthefrontlegswereinitiallyon the entireaccelerationphase.Thetake-off velocityofsuchjumps in frontofthebodyandwerenotcontactwithgroundduring Trajectories In all64jumpsanalysedinthefourspecies,wingsremained Throughout thisaccelerationphaseofajump,theforward The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476 (C) A regionofthemicrotrichiaathigherpower. covered inmicrotrichia,whichspreadanteriorlyoverthecoxa. enlarged viewoftherightcoxalprotrusionshowsittobe campaniform sensillaisvisibleoneachproximalfemur. (B)An trochanteral andtrochanteral-femoralarticulations.A groupof Dictyophara europaea structure oftheproximaljointshindlegs Fig. D. europaea

.Scanningelectronmicrographstoshowthe 4.

ms aftertake-off werehighlystablewith no

ms whenairborne,was40±5.4 did thewingsstarttoopensome2 . (A) Ventral viewoftheventralcoxo-

deg (Table

5A). Attake-off, boththe

ms oftheacceleration

2). Thetrajectories deg inE.

7). Both

5–7).

ms

The Journal of Experimental Biology off timesof1.2 species, particular speciesrangedfrom 3.1±0.2 off. Themeanofmeansvelocitiesforalltheindividuals ofa vitrea lightest species;theywereslightlylongerat1.55±0.05 same at1.40±0.03 defined inthefollowingterms.Meanaccelerationtimeswere the These kinematicanalysesallowedthejumpingperformance to be mostly bythehindlegs. trajectory waspurelytheresultofpropulsiveforcesgenerated Movie plane waslimitedtoalowrate(seesupplementarymaterial measurable rotationsinthepitchandyawplanes.Rotationroll RESEARCH ARTICLE 4.8±0.5 individuals ofall specieshadtake-off velocities above4 Jumping performance successive frames,andtherefore at0.2 velocity wasmeasuredasa rollingthree-pointaveragefrom of hindlegs First movement LH LH RH , butsignificantlylongerat2.44±0.08 RH 2). Thewingsdidnotmoveduringthisperiodsothe m D. europaea. Thefirstthreespeciesachievedfastesttake-

s − 1 in

ms, butD.europaea RM RM . . . . E. minuta .

ms inE.minuta LM LM –1.4 ms –0.4 ms –0.8 ms –1.2 ms –0.6 ms RF RF (Table LF LF only achieved2.0

2). Intheirfastestjumps, ms intervals,justbeforetake- and LH RH RH T. praeferrata,thetwo

m LH Take-off

s

− ms intheheaviest 1 in R. vitrea

ms. Take-off RM

m .

ms inR.

s . − 1 , with LM . to RF LF heaviest species minuta respectively. Theforceexertedwasatitslowest28–29 T. praeferrata the heavier these performancesrangedfrom76 the bodymass,asinplanthopper depressor musclesofthehindlegsconstituteapproximately10% of 2009), sothatapowerpermuscle massof48,400–140,200 with species experiencedforcesinexcessof200 (Table would berequiredinthefastest jumpsbythedifferent species E. minuta accelerations inthesejumpsrangedfrom2200 to morethantwicethisat4830 distance jumped ( and heightsachievedinnatural jumping.Therefore,toestimatethe specimens ofsomespeciesmade itdifficult tomeasurethedistances The speedofthesejumpsand smallnumbersofavailable +0.8 ms +0.4 ms –0.2 ms 2 mm E. minuta 0 ms

2). and achieving theremarkablevalueof5.8 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476 D. europaea. Thepoweroutputrangedfrom63 T. praeferrata,andhighestat5864 to 127and129 of 0.05 captured atrateof5000 Fig. reference. corner ofeachimagerepresentsaconstantpoint with take-off designatedas images arearrangedintwocolumnsatthetimesindicated, piercing mouthpartsislabelledwithabluesquare.Selected (LF, RF)byarrowswithyellowheads.Thetipofthe (LM, RM)byarrowswithwhiteheads,andthefrontlegs are indicatedbyarrowswithpinkheads,themiddlelegs conventions areused:theleft(L)andright(R)hind(H)legs praeferrata experiencing 490 D. europaea s

.Sideviewofajumpby 5. ) andthemaximum heightreached( ms. InthisandFigs from ahorizontalsurface. mW inD.europaea

m

and g

. Theenergy requiredtoachieve s μJ inT. praeferrata −

2 images in R. vitrea

6, 8and9,thefollowing t =0 I. coleoptratus E. minuta ms; thebottomleft-hand

Thanatodictya

s g − 1 in theirfastestjumps,

with anexposuretime m . Thetrochanteral

m s −

Images were . Attake-off, all 2 s − in 1 and . Theapplied D. europaea to 254 μJin

mN inthe (Burrows, h

R. vitrea mN inE. ), itwas

W mW in

kg 407 − 1 ,

The Journal of Experimental Biology smallest speciesachievedatake-off velocityof5.8 particular species,andachieved fasttake-off velocities.Indeed, the than 100timesitsbodylength. where 408 RESEARCH ARTICLE a jumpinonly1.2to2 This paperhasshownthatdictyopharids acceleratedtheirbodiesto the equationsbelow: assumed thatthebodyactedlikeasmallprojectileasdescribedby velocities of4 studied thathavemorethan three timesthemasshadtake-off the highestrecordedforanyinsect todate.Eventhelarger species DISCUSSION species suchas more than550timesitsbodylength.Evenalongerandheavier dictyopharids analysed,ispredictedtojumpforwardsfor3 remarkable. Forexample, 3. 1968) werethenmadeandareshowninTable Calculations basedonthemotionofsuchaninertbody(Alexander, of hindlegs First movement The distancesandheightspredictedforthebestjumps are RH LH v is thevelocityattake-off and RM LM

m R. vitrea

s − 1 s h or higher. Thesejumps wereallpropelledby = v = (v RF cosϴ –0.8 ms –1.2 ms –1.0 ms

–1.4 ms ms, dependingonthebodymass ofthe is predictedtojumpalmost1.5 sinϴ (2v E. minuta,thesmallestof LF ) 2 / (2×9.81) sinϴ LH RH /9.81) Take-off RH LH ϴ RM (2) , is thetake-off angle. LM ,

m

s − 1 RF , whichis Tarsus

m, more

Femoro-tibial m or (1) Tibia angle LF Femur hemipterans. Recordings fromthejumpingmuscles ofhemipterans Clark andLucey, 1967),locusts(Bennet-Clark,1975) and mechanism suchasthatprovided byacatapult,asinfleas(Bennet- in dictyopharidsmusttherefore alsoinvolveapoweramplification 1985; Josephson,1993;Weis-Fogh andAlexander, 1977).Jumping from 28,000to140,200 requirements forthebestjumpsofdictyopharidsanalysedranged comprise approximately10%ofbodymass.Onthisbasis,thepower 2009), thelarge trochanteral musclesthatprovidethepower froghoppers (Burrows,2006a)andplanthoppers(Table power outputsfromthemuscles.Inmanyjumpingbugs,such as Calculations fromthekinematicsindicatethatjumpingrequires high performance byreducingdrag. the elongatedbodyshape,whichisalsosuggestedtoimprove body spininanyplane,perhapsreflectingastabilisinginfluenceof accompanied bymovementsofthewingsandnoneshowedmarked trochanteral depressormusclesinthethorax.Nojumpswere shorter thantheoverallbodylength.Allwerepoweredbylarge hind legsthatareonly30–50%longerthantheotherlegs,and outputs from250to500 muscle; directcontractionofthe muscleswouldonlyproducepower are farbeyondthemaximumactivecontractilelimitofnormal Power outputfor jumping Body-femur +1.0 ms –0.2 ms –0.4 ms angle 2 mm 0 ms The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476 5000 underneath. surface oftheglasschamberandviewedfrom by Thanatodictyapraeferrata Fig. black. TheanglesplottedinFig. the tarsiingreen,andlongitudinalaxisofbody legs duringajump,withthefemorainpink,tibiaecyan, stick diagramsshowthepropulsivemovementsofhind

.Selectedimages,atthetimesindicated,ofajump 6.

images

W W

s Images werecapturedatarateof

− kg kg 1 and withanexposuretimeof0.05 − –1 1 in thedifferent species.Such outputs (Askew andMarsh,2002;Ellington, from thevertical,front

7 areindicated. 2) (Burrows,

ms. The

The Journal of Experimental Biology RESEARCH ARTICLE

Table2. Jumping performance of dictyopharids Body mass Time to take-off Take-off Take-off angle Body angle Acceleration Power/muscle (m) (t) velocity (v) (elevation) at take-off (f) g force Energy (E) Power (p) Force (F) mass Formula f=v/t g=f/9.81 E=0.5m v2 p=E/t F=mf p/(0.1m) Units mg ms ms1 deg deg ms2 g μJ mW mN Wkg1 Engela minuta (N=1, n=9) Mean 5.7 1.4±0.1 4.8 ± 0.5 40±5 53±9 3430 350 66 47 20 82,300 Best 5.7 1.2 5.8 35 35 4830 490 96 80 28 140,200 Thanatodictya praeferrata (N=3, n=18) Mean 8.1 1.4±0.1 3.7±0.2 69±3 41±5 2570 260 53 38 21 46,300 Best 7.8 1.2 4.4 68 35 3670 375 76 63 29 80,700 Raphiophora vitrea (N=4, n=20) Mean 19.6 ± 1.0 1.6±0.1 3.1±0.2 65±4 45±2 1930 200 82 55 38 28,000 Best 19.3 1.2 4.0 57 33 3330 340 154 129 64 66,700 Dictyophara europaea (N=4, n=16) Mean 22.9 ± 0.7 2.4±0.1 3.9±0.1 61±3 51±3 1630 170 174 73 37 31,700 Best 26.2 2.0 4.4 75 60 2290 225 254 127 58 48,400 aIssus coleoptratus, male The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476 Mean (N=31) 21.5±0.56 1.49±0.04 3.2±0.21 42.7±1.8 17.1±2.4 2261±176.2 231±17.9 121±14.9 89±11.6 49±3.9 37,600 Best 22 0.78 5.5 56 10 7051 719 303 388 141 160,300 aIssus coleoptratus, female Mean (N=27) 32.2±2.01 1.6±0.03 2.2±0.14 44.7±1.7 26.5±1.5 1403±105.5 143±10.8 85±10.4 55±7.0 44±3.5 15,500 Best 30 1.25 3.8 52 34 3040 310 195 156 82 47,000 The jumping performance of the four species of dictyopharids analysed. Data in the five columns on the left are the means ± s.e.m. (E. minuta), or the mean of means for the performance of each individual of the other three species of dictyopharids; the best performance of a particular individual is also given. A best jump is defined by the highest take-off velocity achieved by an individual of the named species. The calculated values in the five columns on the right for acceleration are derived from these measured data. N indicates the number of , n the total number of jumps analysed for that species. aData from Burrows (Burrows, 2009). 409

The Journal of Experimental Biology 410 RESEARCH ARTICLE bathing solution (Neff etal.,2000).Furthermore, inaspeciesofthe specificity oftheemissionsand bytheirdependenceonthepHofa (Burrows etal.,2008).Two keysignaturesofresilinaremet bythe pleural archesoffroghoppers, which havebeenanalysedindetail properties ofthisfluorescence arethesameasthatemittedby fluoresce brightblueunderspecific wavelengthsofUV light. The al., 2008).Inthedictyopharids analysedhere,thesestructuresalso in theplanthopper extend. Theythereforeactlikethepleuralarchesinfroghoppers and in preparationforajumpandthentounfurlasthehindlegsrapidly the pleuralarchesofhindlegshavebeenobservedhereto bend which isthenreleasedsuddenlytopropelajump.Indictyopharids, (Burrows etal.,2008).Energy isstoredinbendingthesestructures, a compositeofhardcuticleandtherubber-like protein resilin bend internalskeletalstructures(thepleuralarches)thatarebuilt of planthopper Power amplificationrequiresenergy storage.Infroghoppersandthe 2007a) andplanthoppers[ such asfroghoppers(Burrows,2007c),leafhoppers Energy storage Energy Bräunig, 2010). part ofthedepressormusclelocatedincoxa(Burrowsand of thetrochanteraldepressormuscle,perhapsbyaseparatebutsmall enigmatic. Theotherpossibilityliesincontrolofthelineaction engagement couldactasamechanicalrestraint,soitsroleremains position inpreparationforajump.Itseemsunlikelythatthis the coxalprotrusionwhenahindlegislevatedintoitscocked dorsal surface.Thisflatpatchbearsnomicrotrichiabutdoescontact femoral protrusionisrepresentedonlybyaslightraisingofthe coxal protrusionispresentandcoveredinmicrotrichia,butthe (Gorb, 2001).Inplanthoppers,suchastheonesanalysedhere, where bodypartsofinsectsneedtoengageandevenlocktogether of contactandmayinterdigitate.Theyarefoundmoregenerally protrusions arecoveredinmicrotrichiathatincreasethesurfacearea sufficient forcehasbeengenerated(Burrows,2006b).These mechanical restrainttodepressionthatisovercomeonlywhen of theirprominentandcoxalfemoralprotrusionsprovidesa required forajumphasbeenstored?Infroghoppers,theengagement contractions fromextendingthehindlegsuntilallenergy movements ofthehindlegs.Whatthenpreventstheseslow 2010)] showthattheycontractwellinadvanceoftherapidjumping Joint angle (deg) 120 160 200 40 80 3– 10 –1 –2 –3 Tarsus angle Femoro-tibial ,theslowcontractionsofmuscles Tibia Issus coleoptratus Femur –1.4 ms angle Body-femur –1.0 ms –0.8 ms –0.4 ms .coleoptratus I. Time (ms) (Burrows, 2009;Burrowset (Burrows andBräunig, Take-off 1 –0.2 ms Take-off +1.0 ms 2 expected tolose aquarterofitsrangetodragand thelarger species length similartothatof estimated thatthefroghoppers the body(Bennet-ClarkandAlder, 1979; Vogel, 2005).Vogel has calculations considertheconsiderabledragthatwillbeexerted on approximately 100timestheirbodylengths.Noneof the lose 80%(Vogel, 2005). a smallerfleabeetlewouldlose 40%andanevensmallerfleawould 2006a)] wouldlosesome25%of itsjumpingrangebecauseofdrag, mean massof12 and The heightspredictedareequallyimpressive;both with approximately 1 and extraordinary distances: the fourspecies. jump trajectoryrangedmorewidely, withmeansof40to69 53 was similarforthefourspeciesanalysed,withmeansof41to of thelongitudinalaxisbodyrelativetogroundattake-off from 225to490inthebestjumpsbydifferent species.Theangle shape (Burrowsetal.,2008). energy forajumpandthenfinallyreturnthebodytoitsoriginal store therequisiteenergy forajump,unfurltodeliverthestored hard cuticlethatcanwithstandbendingstrainswithoutfracturing, planthoppers. Infroghoppers,theresilinformsacompositewith therefore indicatethatthepleuralarchescontainresilinin resilin inthreeotherinsectorders(Lyons etal.,2011). Threecriteria rubbery hydrogelcalledRec-1resilin.Theantibodyalsostains soluble protein,andwhichwhencross-linkedformedaresilient, gene hasbeenclonedinEscherichiacoli,whichitexpresseda Drosophila melanogaster 2011) thestainingwithanantibodyraisedagainstgeneCG15920in fluorescence inthepleuralarchespreciselymatches(Burrowsetal., and infroghoppers(Hemiptera,familyCercopidae),the planthopper genus jumping muscleresultsintheinsectsexperiencing The rapidaccelerationofthebodyandpowerdevelopedby Jumping performance These valuesarecalculatedtopropeltheseinsects to deg. Bycontrast,theangleofelevationforinitialpart D. europaea R. vitrea during thejumpby Fig. shows thetimeoftake-off (0 left andrighthindlegsatthetimesindicated.Theyellowverticalbar the positionsoffemora(pink),tibiae(cyan)andtarsi(green) femoro-tibial joint(blacksquares)areplotted.Thestickdiagramsshow angles betweenthebodyandfemur(pinktriangles)of E. minuta

.Graphsoftheangularchangesatjointshindlegs 7. The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476 to almost1.5 predicted toreachalmost500timesitsbodylength.

m. Allaremorethan100timestheirbodylengths, are predictedtoreachaheightofalmost1

mg andameanlengthof6.1 Delphacodes Thanatodictya praeferrata Engela minuta E. minuta Philaenus spumarius,mightthereforebe (Elvin etal.,2005).Thefirstexonofthis

m andtheheaviest ms). Philaenus spumarius (Hemiptera, familyDelphacidae) to morethan3 , whichhasabodymassand shown inFig.

m, g D. europaea

mm (Burrows, T. praeferrata forces ranging T. praeferrata [which hasa deg for

6.

m or The to

The Journal of Experimental Biology 0.03 which somespecies canoutperform(Table squat andbluntbodyshapeof 2006a). Thestreamlinedshape ofdictyopharidscontrastswiththe spumarius jumpers suchasPhilaenus forwards elevatetheseinsectsto arankalongsidethebestofinsect velocity andtheexpecteddistances jumpedbothupwardsand effect onjumpingperformance?Therapidacceleration,the take-off head, thatseeminglyequateswithstreamlining,startstohave an somewhat less.Isthiswheretheelongatedandtaperedshapeof the Image wascapturedatrateof5000 Sideviewofajumpby 8. Fig. RESEARCH ARTICLE of hindlegs First movement LH LH ms. Take-off occurredattime0 RH RH RM –1.0 ms –0.6 ms –0.8 ms –1.4 ms –1.6 ms Engela minuta RF

images ms. I. coleoptratus LH LM LH Take-off

s − 1 (Burrows, 2003;Burrows, with anexposuretimeof from ahorizontalsurface.

2). RH RH RM (Burrows, 2009), LF +0.4 ms –0.2 ms –0.4 ms 2 mm 0 ms RF Mountain, SouthAfrica(34°04 Slovenia, time of0.05 the side,andimagewascapturedat5000 150°18′ Blackheath intheBlueMountains, NSW, Australia( and Biosphere Reserve,Mpumalanga,South Africa(23°54 Raphiophora vitrea Adult Raphiophora vitrea Selectedimages,atthetimesindicated,ofajumpby 9. Fig. Auchenorrhyncha, superfamilyFulgoroidea,familyDictyopharidae. MATERIALS ANDMETHODS of hindlegs First movement Thanatodictya praeferrata RH Dictyophara europaea RH 39.9456″ Engela minuta

ms. Take-off occurredattime0 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093476 LH E). Allspeciesbelong totheorderHemiptera,suborder (Schaum 1850)onStrychnos LM LH from ahorizontalsurface. RM Distant 1906atSilvermineNature Reserve, Table –2.0 ms –1.4 ms –0.6 ms –1.8 ms –1.0 ms (Linnaeus 1767)werecaughtaroundLjubljana, RF (Distant 1892)onGovettstrack near LF ′ 30″ S, 18°23′ Take-off RH RH

ms.

images The insectisviewedfrom trees atLapalala,Waterberg 55″ ′

0.70″ s − E, 450 1 LH with anexposure LH − LM S, 28°19′ 33°37′ 5 mm RM m altitude), –0.2 ms +0.6 ms –0.4 ms 28.9632″ RF 23.67″ 0 ms LF 411 E), S,

The Journal of Experimental Biology 412 RESEARCH ARTICLE 4000 512PCI camera(PhotronEurope,West Wycombe, Bucks,UK)atarateof D. europaea, ninejumpsbyone were recordeddirectlytoacomputerforlateranalysis.Sixteenjumpsbyfour an exposuretimeof0.03or0.05 jumps byfour image planeofthecamera(seesupplementarymaterialMovies the middleofthischamber, theshapeofwhichconstrainedmostjumpsto 60 UK) sothatthetarsididnotslipwhenjumping.Thecamera,fittedwitha of high-densityfoam(Plastazote,Watkins andDoncaster, Cranbrook,Kent, 10 chamber madeofopticalqualityglass(width80 or wereelicitedbyfinemechanicalstimulationwithasmallpaintbrush,in take-off time( the groundandinsectthereforebecameairbornewasdesignatedas Imaging, Tucson, AZ,USA).Thetimeatwhichthehindlegslostcontactwith image fileswereanalysedwithMotionscopecamerasoftware(Redlake axis relativetothehorizontalbothwhenstandingandduringajump.Selected image. Thebodyanglewasdefinedasthesubtendedbyitslongitudinal behind thehindlegsandclosetocentreofmasswasfollowedineach balancing aninsectonapinpostmortem.A fixedpointonthebodyjust the finalmillisecondbeforetake-off. Thecentreofmasswasdeterminedby rolling three-pointaverageofsuccessiveimagesandthevaluesgivenarefor joint orbodyangles.Peakvelocitywascalculatedasthedistancemovedina were calculatedtoresultinamaximumerrorof10%themeasurements chamber. Jumpsthatdeviatedfromtheimageplaneofcameraby±30 from underneathasadictyopharidjumpedthefrontglasssurfaceof in jointanglesweremeasuredfromtheseimagesandthosecaptured to theimageplaneofcamera,orasclosepossiblethisplane.Changes Measurements ofdistancesmovedweremadefromjumpsthatparallel jumps viewedfromthesideandventralsurfaceofinsect,respectively). to aLeicaMZ16 microscopeandprojectedontoa 24 an accuracyof0.1 numbers ofindividualsfromeachspecies) weremeasuredagainstarulerto The Netherlands).Lengthsofthe legs offixedspecimens(seeTable examined inaPhilipsXL-30Scanning ElectronMicroscope(Eindhoven, were alsomountedonspecimenholders, sputtercoatedwithgoldandthen DXM1200 digitalcameraattached to thesamemicroscope.Driedspecimens ). Individualcolourphotographs weretakenwithaNikon of adrawingtubeattachedtoLeicaMZ16stereomicroscope(Wetzlar, hydroxide. Drawingsofthelegs,jointsandmusclesweremadewith aid in 70%alcoholor50%glycerol;andclearedbyboiling10%potassium formaldehyde andsubsequentstoragein70%alcohol;fixation andinthosepreservedthefollowingways:fixation5%buffered Temperatures rangedfrom24to30°C. small (seeTables because thenumberofindividualseachspeciesthatcouldbeobtained was the insectbecausedifferences betweenindividualswerenotmarkedand error inmeasuringaccelerationtime.Datawerenotsortedaccordingto sex of the firstmovementofhindlegsandtake-off timewouldresultina10% defined theaccelerationtimeofajump.A one-frameerrorinestimatingboth The periodfromthefirstdetectablemovementofhindlegsuntiltake-off properties of a projectile with no influence of wind resistance. properties ofaprojectilewithnoinfluencewindresistance. Calculated distancesandheightsofthebestjumpsbyindividuals Table Dictyophara europaea Raphiophora vitrea Thanodictya praeferrata Engela minuta Species Sequential imagesofjumpswerecapturedwithasinglePhotronFastcam The anatomyofthehindlegsandmetathoraxwasexaminedinintact mm MicroNikkorlensora100 mm atfloorlevelexpandingto25 s −  3. Jumping distances and heights 3. Jumpingdistancesandheights 1

and anexposuretimeof0.25 t =0 T. praeferrata

ms) sothatdifferent jumpscouldbealignedandcompared. mm fromimages captured withadigitalcameraattached

1, 2).Measurementsaregivenasmeans±s.e.m.

4.4 4 4.4 5.8 (m Take-off velocity were captured.Jumpsoccurredspontaneously,

 s

E. minuta,20jumpsbyfourR.vitrea  ms fortheotherthreespecies.Theimages 1

mm microTokina lens,pointeddirectlyat )

mm attheceiling).Thefloorwasmade ms forD.europaea, andat5000 (deg) Take-off angle 75 57 68 35

mm, height80

inch monitor. Body

1 and2for 8.8 8.9 8.3 6.6 (mm) Body length mm, depth ofthefourspeciesdictyopharidinsectsanalysed.Thecal

s and 16 −

1 for 1

deg and USA). were superimposedinCanvas14(ACDSystemsInternational,Seattle,WA, through adichroicbeamsplitter. ImagescapturedunderUV andwhitelight fluorescence emissionwascollectedatwavelengthsfrom413to483 edged (1%transmissionlimits)bandfrom350to407 Brightline seriesUV filterset(Semrock,Rochester, NY, USA)withasharp- Chandlers Ford,Hants,UK)wasconditionedbyaSemrockDAPI-5060B UV lightfromanX-citeseries120metalhalidesource(EXFO, Olympus BX51WIcompoundmicroscope(OlympusUK,London,UK). NA objectivelenses,underultraviolet(UV)orwhiteepi-illuminationonan viewed throughOlympusMPlan×5/0.1NA andOlympusMPlan×10/0.25 AB104 balance(BeaumontLeys,Leicester, UK). masses weredeterminedtoanaccuracyof0.1 http://jeb.biologists.org/lookup/suppl/doi:10.1242/jeb.093476/-/DC1 Supplementary materialavailableonlineat commercial, ornot-for-profitsectors. This researchreceivednospecificgrantfromanyfundingagencyinthepublic, The authordeclaresnocompetingfinancialinterests. with thedataanalysis. suggestions duringthecourseofthiswork.MarinaDorosenkohelpedenormously help incollectingthesebugsAustralia,andprovidingmanyhelpful collecting someoftheseinsects.IalsothankSteveRogersandSwidiOttfortheir Steve SimpsoninAustraliaforthehospitalityoftheirlaboratoriesandhelp I ammostgratefultoMikePickerinSouthAfrica,MetaVirant inSloveniaand lxne,R.M. Alexander, R.M. Alexander, nesn .O n esFg,T. Weis-Fogh, and S.O. Andersen, entCak H.C. Bennet-Clark, R.L. Marsh, and G.N. Askew, References Supplementary material Funding Competing interests Acknowledgements entCak .C n ue,E.C.A. Lucey, and H.C. Bennet-Clark, G.M. Alder, and H.C. Bennet-Clark, H.C. Bennet-Clark, urw,M. Burrows, urw,M. Burrows, M. Burrows, M. Burrows, urw,M. Burrows, M. Burrows, M. Burrows, 987 1490 1371 3222 distance (mm) Horizontal power output:quailflightmuscle. cuticle. Adv. InsectPhysiol. vertebrates andinsects. gregaria energetics andamodelofthemechanism. jumping performanceofinsects. F. Chapman andA.Joern),pp.173-203.NewYork, NY: JohnWileyandSons. in froghopperinsects. 424 Auchenorrhyncha, Cicadellidae). jumping inleafhopperinsects. 4607-4621. Exp. Biol. J. Neurophysiol. To searchforthepossiblepresenceofresilin,dissecteddictyopharidswere , 509.

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nm

J. ,

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