was orientedalmostparalleltotheground( diameter. Jumpswereoftwotypes.First,thoseinwhichthebody legs buttheirfemoraandtibiaewerenarrowtubesofsimilar protein resilin.Themiddleandhindlegswerelongerthanthefront illuminated withultravioletlight,suggestingthepresenceofelastic sides ofthemeso-andmetathoraxfluorescedbrightbluewhen from aparticularpresetpositionoftheselegs.Ridgesonthelateral largely bythoracictrochanteraldepressormusclesbutdidnotstart *Author ([email protected]) for correspondence 4252 Received 9July2014; Accepted14October2014 1 hind andthemiddle,aremoved together. Synchronizingfourlegs and snowfleas(Mecoptera)(Burrows,2011) twopairsoflegs,the Dickinson, 2008;Zumsteinetal.,2004).Insomeotherdipteran flies flies suchasDrosophila, itisthemiddlepairoflegs(Cardand the singlepairofhindlegsthatpropelsjumping,althoughin small (Evans, 1972;Evans,1973;Kaschek,1984).Mostcommonly itis the rapidmovementofjointbetweenpro-andmesothorax 1993; Christian,1978;1979)andclickbeetleswhich use extension ofanabdominalappendage(BrackenburyandHunt, however, suchasthespringtails(Collembola), whichusethefast move togetherrapidlyandpowerfully. Thereareexceptions, Most insectsthatjumparepropelledbyasinglepairoflegs that movements KEY WORDS:Biomechanics,Kinematics,Flying,Escape captured atarateof1000 movements ofthemiddleandhindlegsasrevealedinvideoimages Lacewings launchthemselvesintotheairbysimultaneouspropulsive Malcolm Burrows and Hemerobiidae) Jumping mechanismsinlacewings(Neuroptera,Chrysopidae RESEARCH ARTICLE © 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,4252-4261doi:10.1242/jeb.110841 of 5.5or6.3 fastest jumpsgreenandbrownlacewingsexperiencedaccelerations mechanism oranenergystore. produced bydirectmusclecontractionswithoutapoweramplification active contractilelimitofnormalmuscle,sothatjumpingcouldbe 0.6 or0.2 5.6 or0.7 μJ,apoweroutputof0.30.1 INTRODUCTION ABSTRACT 5 stable onceanimalswereairborne.Thewingsdidnotmoveuntil lacewings, 13.7±7 − in whichtheheadpointeddownwardsattake-off (greenlacewings, green lacewings(mass9 pitch planeonceairbornewithoutthewingsopening.Thelarger the bodytomeantake-off velocitiesof0.6and0.5 the smallerbrownlacewings(3.6 Department of Zoology, Cambridge, CambridgeCB23EJ, of UK. University of Department
37±3 ms aftertake-off whenflappingflightensued.Second,werejumps deg; brownlacewings, mN. Therequiredpowerwaswellwithinthemaximum g , respectively. Theyrequiredanenergyexpenditureof
deg inbrownlacewings)attake-off andremained 1, * andMarinaDorosenko
mg, bodylength10.3 s − − 1 35±4 . Thesemovementswerepowered
mg and5.3 deg) andthebodyrotatedin mW andexertedaforceof mm) 9
mm) took15 −
7±8 m ms toaccelerate
s − deg ingreen 1 1 . Duringtheir ms and significantly different bothforthemasses( 5.3±0.3 and themottled wingsofthetwobrown species ( wings increasedtheoveralllength ofgreenlacewingsby30±2.4% and thebodylengths( analysed byhigh-speedimaging. examined anatomicallyandtheirmovementsduringtake-off were mechanism. To answerthese questions,thelegsweretherefore are poweredbydirectmusclecontractionsorusedinacatapult combinations oflegsmightbeusedandwhethertheirmovements enabling rapidtake-off. Italsoseekstodeterminewhat jumping playsaroleinthesefastmovementsandparticularly and frequentlylaunchintoflight.Thispaperanalyseswhether move rapidlyaroundwoodyshrubsandtrees,particularlyafterdusk, wings andlegsthatareshorterthantheirbody. Theynevertheless long hindlegsasinbushcrickets(BurrowsandMorris,2003). slower take-off velocitiesevenifleverageisincreasedbytheuseof the legs.Thiswillgenerateslowermovementsoflegsand contractions ofthemusclestopowerpropulsivemovements 2006b; Burrows,2007b).Analternativemechanismistousedirect 1975; Bennet-ClarkandLucey, 1967;Burrows,2006a; sucking bugs(Hemiptera)andfleas(Siphonaptera)(Bennet-Clark, used byavarietyofinsects,includinglocusts(Orthoptera),plant- then bereleasedsuddenlytopowerthejump.Suchamechanismis slowly andstoreenergy indistortionsoftheskeleton,whichcan mechanism thatallowsthepower-producing musclestocontract conflicting demandscanbemetonlybytheuseofacatapult is therequiredoutcome.Ifpropulsivelegsareshortthenthese off velocitiesandshortaccelerationtimes,particularlywhenescape (Burrows, 2013a). of waterbyensuringthatthelegsdonotpenetratesurface Hydrophorus alboflorens off becomespossiblefrommorecompliantsurfaces.Forthefly distributing groundreactionforcesoveralarger surfacearea,take- in itscatapultjumpingaction(Burrows,2011). Furthermore,by fleas italsoallowsfourenergy stores–oneforeachlegtobeused avoiding thespecialisationinshapeandsizeoflegs.Insnow increasing themusclemassthatcanbedevotedtojumpingwhile increases thecomplexityofmusclecontrolbuthasadvantage variegatus were thusheavierandlarger thanthebrownspecies 9.0±1.1 green lacewings( 1A–C).The normally heldpointingupwardsandforwards(Fig. and bytheirlongantennaethatwere75%ofbodylength were The appearanceoflacewingswasdominatedbytheirlarge wings Body shape RESULTS Lacewings (Neuroptera)areagileinsectswithlarge diaphanous In alljumpingmovements,thesamedemandsexistforhightake- mg (mean±s.e.m.)andabodylengthof10.3±0.4 mm (N which hadamassof3.6±0.4 7frec pce)(al 1).The valuesare =7 foreachspecies)(Table Chrysoperla carnea t -test: this evenenablesjumpingfromthesurface t 10 =11.17, P <0.0001). Thetranslucent
mg andabodylengthof group) hadamassof t -test: t 10 =4.49, Micromus Micromus P
mm and =0.001)
The Journal of Experimental Biology increased length ofthehindlegsindifferent speciescanbe were 110% longerthanthefrontlegs givingaratioof1:1.5:2.1.The brown lacewings,themiddlelegs were50%longerandthehindlegs lengths was1:1.2:1.7(front:middle: hind)(Fig. legs were70%longerthanthe frontlegssothattheratioofleg extended aboveandbelowthe body whenfolded. variegatus of anadultthesmallerbrownlacewing Chrysoperla carnea analysed. Fig. RESEARCH ARTICLE levated. The hindtrochanteraarepartiallydepressedandthemiddle are lacewing. (E)Photographofaventralviewthethoraxbrown to showtherelativeproportionsoffront,middleandhindlegsagreen The middlelegsofgreenlacewings were20%longerandthehind E B
C A Trochanter Femur Femur Femur .Shapeofthebodyandlegstwospecieslacewings 1. Coxa Coxa Coxa Trochanter Trochanter Hind legs Front legs Middle legs Side Chrysoperla carnea Micromus variegatus Side Ventral (A) Sideviewofanadultgreenlacewingthatbelongstothe and Hemerobius humulinus)by55±4.5%.Thewingsalso group. (B)Ventral viewofthesameinsect. (C)Sideview 2 mm 2 mm group Micromus variegatus
Right 1D; Table 0.5 mm Posterior 0.5 mm Anterior . (D)Drawings depressor trochanteral Tendon depressor trochanteral Tendon D Left
1). In surfaces (Fig. been removed,thebluefluorescencewasalsovisiblefrominner the presenceofresilin(Fig. blue fluorescencewhenviewedfromtheoutersurface,suggesting methods fordetailsofwavelengths),theseridgesshowedabright the thoraxwasilluminatedwithUV light(seetheMaterialsand 2A).When wings, respectively, tothearticulationofcoxae(Fig. posterior edgesthatextendedfromthehingesoffrontorhind and metathoracicsegmentseachhadaprominentridgetowardtheir absent. Thefivesegmentedtarsiendedincurvedclaws. capable ofgeneratingpowerfulextensionsthetibiaewere shape ofthefemorainparticularindicatesthatlarge muscles thin tubeswithaconsistentdiameteralongtheirwholelength.This Fig. more elongatedthanthoseofthemiddleorhindlegs(Fig. widely separatedfromeachotherattheventralmidlineandwere forwards andclosetotheprothorax.Thefrontcoxaeweremore three pairsoflegsandwereheldwiththefemorapointing of atrochanter(Fig. flexible jointmembraneatitsinsertiononthemedial,ventralrim tendon wasparticularlylarge andwasclearlyvisiblethroughthe depressed orlevatedbymuscleswithinthethorax.Thedepressor rotate through~100 midline (Fig. middle andhindlegswerelarge andcloselyapposedattheventral horizontally andforwards(Fig. away fromtheedgesofbodywithfemorapointingalmost front legsextendedmorelaterallysothatthetarsiwereplaced dorsal surfaceoftheabdomen(Fig. backwards andwhenflexedthefemoro-tibialjointwasabove to thelateralsurfacesofabdomenwithafemurpointing brown lacewingshadratiosof2.7and2.5,respectively. the brownones.Relativetocuberootofbodymass,greenand of greenlacewingswere55%bodylengthcomparedwith70%in attributed totheirlongerfemoraandtibiae(Table to flapuntilthelacewinghadbeenairborneforatleast5 propulsive actions.Furthermore,thewingsdidnotopenorbegin joint anglesofthefrontlegscouldberelatedtoanydirect combined actionsofthemiddleandhindlegs.Nochangesin Jumps bybothgreenandbrownlacewingswerepropelledthe of thebodyremained stable.Propulsivemovements inbothgreen jumps butwillbedescribedfirst forthoseinwhichtheorientation and theinsectcrashed. and flaponceairborne,butthe bodyorientationremainedunstable lacewing andonejumpbyabrown lacewingdidthewingsopen were inthiscategory. Injustoneofthesejumpsbya green 3). Ingreenlacewings41%(35%inbrownlacewings)ofjumps rotating onceairborne(Figs which thebodypitchedforwardsduringtake-off andcontinued lacewings) ofjumpswereinthiscategory. Second,werejumpsin flight thenfollowed.Ingreenlacewings59%(65%inbrown Movies 1and2).Thewingsopenedonceairborneflapping particularly inthepitchplane( jumps inwhichthelongitudinalbodyaxisremainedstable, from the115 jumpsby17lacewingsthatwereanalysed.First this time.Two broadcategories ofjumpscouldbedistinguished could notthereforehavecontributedanyforcetoajumpbefore Kinematics of thejump Kinematics of In bothgreenandbrownlacewings,thelateralwallsofmeso The orientationoflegswassuchthatthehindmovedclose The sequenceoflegmovements wasessentiallythesameinall 2A). Thefemoraandtibiaeofallthreepairslegswerelong The JournalofExperimentalBiology(2014)doi:10.1242/jeb.110841
2D,E). 1E). Thetrochanterawereshortandableto
deg abouttheirrespectivecoxae.Theywere
1E). Thefrontlegsweretheshortestofall
2B,C). Whensoftinternaltissuehad 5–7; supplementarymaterialMovie is3–5;supplementarymaterial Figs
1B, Fig.
1A, Fig. 3). Thecoxaeofthe 3). Themiddleand
1). Thehindlegs
ms and 4253
1E,
The Journal of Experimental Biology horizontal (head pointingdownwards)was Thebodyangleattake-off relativetothe maximum rateof22Hz. propulsive phaseandonce airborne continuedtorotateata 7) lacewings thebodypitcheddownwardsduring (Fig. of themiddleandhindlegs. jump fromthegroundwasthus entirely propelledbythemovements jumps wherealandingsitewasencounteredsoonaftertake-off. A flight. Theexceptiontothisopeningofthewingsoccurredin those a fewmillisecondsaftertake-off, sothatsuchjumpsleddirectlyto contact bythehindtarsi).Thewingsfirstopenedandstartedto flap movements ofthemiddleandhindlegsuntillossground acceleration phaseofthejump(thetimefromfirstpropulsive a discernibleeffect onthestability ofajump. with theheadpointingupwardsmoreoftenthandownwardswithout horizontal, buttherewaslarge variationbetweendifferent jumps angle ofthebodywasthusonaverageafewdegreeseitherside of and 13.7±7 take-off was− the groundandlacewingbecameairborne.Thebodyangleat outstretched. Atthispointthetipsofhindtarsilostcontactwith reached thefullextentoftheirmovementsbybecomingfully propelling thelacewingupwardsandforwards,untiltheytoo by thehindlegs.Thelegscontinuedtodepressandextend, middle legsandthatforthefinalfewmillisecondswasappliedonly clearly thatthrustwasinitiallyappliedbythetwohindand ground. Thesetimingsvariedbyafewmillisecondsbutshowed maximal depressionandextension,theyalsolostcontactwiththe second, oncethemiddlelegswerefullyoutstretchedbyreaching short frontlegslostcontactwiththeground4–6 gradually raisedthebodyandthishadtwoconsequences;first depression ofthetrochanteraandextensiontibiae degrees whilethehindtibiaecontinuedtoextend.Theprogressive extension movementthemiddletibiaethenflexedthroughafew The tibiaealsobegantoextendatthesametime,butafterasmall body, becauseeachsmalltrochanterwascloselyattachedtoafemur. most apparentasachangeintheangleoffemurrelativeto 5A,B).Insideviewsofthelacewing,thesemovementswere (Fig. their respectivecoxaethatoccurredwithin1 were adepressionofbothhindandmiddletrochanteraabout jumping. Fromthisinitialposture,thefirstpropulsivemovements tibia aboutafemurbyfullflexionwereessentialprerequisitesof neither lockingofatrochanteraboutcoxabyfulllevation,or 4254 RESEARCH ARTICLE instead typicallyadoptedanangleof~90 middle andhindtibiaewerenotfullyflexedabouttheirfemora,but joints, butnotnecessarilytotheirmaximalextent.Similarly, the the hindandmiddlelegswerelevatedattheircoxo-trochanteral (Fig. left columns. mean valuesgiveninfour number ofindividualsfromwhichthemeasurementsweretaken.Thevaluesintworight-handcolumnsarecalculated thefrontlegs;N Body massandlength,lengthsofthehindfemoratibiaearemeans±s.e.m.Theratiolegisgivenrelativeto Table Green lacewing( Brown lacewing( Micromus variegatus Chrysoperla carnea ntescn aeoyo up ybt re Fg 6)andbrown In thesecondcategoryofjumps bybothgreen(Fig. The wingsremainedclosedanddidnotmovethroughoutthis )adbon(i.4)lacewingsbeganfromapostureinwhich 3) andbrown(Fig. 1. Bodyformofgreenandbrownlacewings deg (meanof23jumpsbyninebrownlacewings).The 7±8 N N 7 .±. 030419012601112175 2.7 55 1.7 1.2 1 2.6±0.1 1.9±0.1 10.3±0.4 9.0±1.1 =7) 7 .±. .±. .±. .±. . . 02.5 70 2.1 1.5 1 1.6±0.1 1.1±0.1 5.3±0.3 3.6±0.4 =7) deg (meanof22jumpsbyeightgreenlacewings) group oyms Bd egh idlg Hindleg, (mm) Hindleg, Bodylength (mg) Body mass
deg. Thisimpliesthat −
37±3deg ingreen 37±3deg ms beforetake-off;
ms ofeachother eu m)tba(m rn ideHn eghbodymass length Hind Middle Front tibia(mm) femur (mm) t lacewings. Thetimesarestatisticallysignificantlydifferent ( 55 (0.5±0.01 fastest jumpsrangedfrom5.6 lacewings aforceof6.3 would requirea poweroutputofonly274 found inotherjumpinginsects (Burrows,2006a),thefastestjump muscles ofthetwohindlegs constitutes ~10%ofbodymass,as brown lacewings.Onthebasis thatthetrochanteraldepressor significance ( lacewing didachievethehighesttake-off velocityof1 of 39 not observedinanindividualbrownlacewing.Meanaccelerations t significantly different fromthoseadoptedbyeithergreen( in thesecondcategoryofunstablejumpswerestatistically lacewings and− 15.2±0.9 2).Themeanaccelerationtimeforgreenlacewingswas (Table enabled thefollowingaspectsofperformancetobecalculated An analysisofallthejumpsbygreenandbrownlacewings achieved bygreenlacewings(0.6±0.04 body massofthegreenlacewings.Similartake-off velocitieswere to thelongertimethatittakesaccelerate2.5timesheavier that wereresponsibleforthetrajectory(Fig. propulsive movementsofthelegswhileincontactwithground the pitchplanewingsremainedfoldedsothatitwas depressed (Fig. 8A,B).Duringjumpsinwhichthebodyrotated of theabdomenslowedonlytoincreaseagainaswingswere once airborne;asthewingswereelevated,upwarddisplacement abdomen wereaffected bytheelevationanddepressionofwings progressively upwardsandforwardswhilethemovementsof against time(Fig. abdomen wereplottedinthe clearly seenwhenmovementsoftheheadandtip rotation. Similarly, iftheheadpointedupwards,smallerwasangular relative tothehorizontal,greaterwasangularrotation. downwards andthusthemorenegativeangleitsubtended oftheairbornetrajectory. Themoretheheadpointed first 10ms the angularrotationofbodyrelativetohorizontalduring ones showedacorrelationbetweentheangleofbodyattake-off and brown lacewingsinboththemorestablejumpsandless the firstcategoryofstablejumps.Poolingalldataforgreenand green lacewingsexperienced aforceof5.5 Jumping performance 19 15 =3.65, =6.70, The contrastbetweenthesestableandunstablejumpswasmost m
s m − 2
s in thelighterbrownlacewings.Intheirfastestjumps P − ms (N P<0.0001) andthe1.6timesdifference canbeattributed 2 m =0.002) orbrown(t Ratio ofleglengths The JournalofExperimentalBiology(2014)doi:10.1242/jeb.110841 were reachedintheheaviergreenlacewingsrisingto
s − t 1 -test: ). Thesemeansbarelyreachlevelsofstatistical 35±4deg inbrownones.Thesebodyanglesadopted 35±4deg =8) and9.3±0.2
8B,D). Instablejumpstheheadmoved t 15 =2.25,
g . Theenergy requiredtogeneratethe -test: x P μJ ingreenlacewingsto0.7 =0.040), butanindividualgreen and
ms (N t 20 y fbd Length(mm)/ % ofbody Hind leglength =4.04, oriae Fg 8A,C),or coordinates (Fig. =9) takenbythebrown
W
m
kg
8C,D). P s − =0.001) lacewingsin − 1 ) andbrownones 1
g . Thisvaluewould and thebrown
m indicates the
s − 1 , avalue 1/3 t μJ in t -test: -test: (mg)
The Journal of Experimental Biology each rowofphotographs. and metathoracicridgesinA.Notethearrowsindicatingorientation of illumination. Thediagonallinesofbluefluorescencecorrespondtothemeso- (B,C) andinner(D,E)surfacesofthethoraxagreenlacewingunder UV metathoracic segments.(B–E)Bluefluorescencevisibleonboththeouter ridges runfromthecoxaetowinghingesonbothmeso-and similar shape,butthefrontcoxaisnarrowerandmoreelongated.Prominent side ofthethorax.Theproximalpartsmiddleandhindlegsare take-off. Estimates ofthedistance( measured becauseoftheintervention offlappingflightsoonafter The distanceandheightgenerated bystablejumpswerenot were almostverticalwithsome evenmovingslightlybackwards. ones (valuesnotstatisticallysignificantly different), sothat most horizontal of94±10 contributed anequalamount. be halvedifthemusclesofmiddlelegsweresimilarmass and lacewing Micromusvariegatus Fig. RESEARCH ARTICLE D B ridge Meso Trochanter ridge Meta A Coxa leg Hind The trajectoriesofjumpshad ameananglerelativetothe Femur
.Toai tutr n h rsneo eii inthebrown Thoracicstructureandthepresenceofresilin 2. Hind leginside Hind legoutside idwn Frontwing Hind wing ridge Meta ridge Meta
deg ingreenlacewingsand95±7 leg Middle . (A) Photographofalateralviewtheright Coxa Trochanter otro Dorsal Posterior C Femur E Ventral s) andheight( Middle leginside Middle legoutside Anterior 500 µm ridge Meso leg Front Coxa Femur ridge Meso Posterior h) thatcouldbe Anterior
deg inbrown Dorsal Ventral Dorsal Ventral Tibia Tarsus 200 Anterior Posterior µm backward distances wouldbeonly4–5 lacewing toaheightof13 height of18 Selected imagesfromajumpcapturedatrateof1000 where inert body(Alexander, 1968): according toEqns1and2below, whichdescribethemotionofan reached, ifajumpprovidedtheonlypropulsion,were made Fig. 0 propulsive middleandhindlegsfromtheirbeginninguntiltake-off attime arranged intwocolumns.Theyshowtheprogressivemovementsof spatial referencepoint.ThesameconventionsarefollowedinFigs triangles inthebottomlefthandcornerofeachimageindicateaconstant with whiteheadsandthehindlegs(LH,RH)byarrowspinkheads. The indicated byarrowswithyellowheads,themiddlelegs(LM,RM) then ledtoflappingflight.Thefrontlegs(LF, leftfront; RF, rightfront)are
ms. Wingmovementsbeganonlywhenthelacewingwasairborneand On thisbasis,ajumpispredicted topropelagreenlacewing
.JumpbyagreenlacewingoftheChrysoperlacarnea 3. v RH RH LH LH is thevelocityattake-off and of legs First movement The JournalofExperimentalBiology(2014)doi:10.1242/jeb.110841 mm, orapproximatelytwiceits body lengthandabrown RM Take-off RM sv = RF RF LF h –10 ms
cos mm, or2.5bodylengths.Forward or 0 –8 –2 –4 –6 = () Θ v 9.81 2 sin × ⎝ ⎜ ⎛ 2sin Θ v 9.81
mm fromtake-off anglesclose Θ 2 isthetake-off angle. Θ ,(2) ⎠ ⎟ ⎞ ,(1)
images LH RH
s group. − LM 1
4,6,7. are RM RF 5 mm +10 +15 +5 ms 4255
The Journal of Experimental Biology 4256 RESEARCH ARTICLE requires power outputsnogreaterthan192 Calculations fromthekinematic analysesindicatethatjumping mechanisms tostoretheenergy ofthemusclecontractions. contraction ofthelegmuscles withouttheuseofcomplex of legs.Theforcesgenerated couldbeproducedbythedirect jumps bythesimultaneousmovementsofmiddleandhind pairs This papershowsthatbothgreenandbrownlacewingspropel their to 90 Fig. Power outputfor jumping DISCUSSION off. Thewingsbegantoopen 10 rotate duringthemovementsofmiddleandhindlegsthatpropelled take- height attheexpenseofforward(orbackward)distance. considered intheseestimates.Naturaljumpsthusfavourgreater and thebodyremainingstable.
Take-off of legs First movement HRM RH .Jumpbyabrownlacewing 4. deg relativetothehorizontal.Theeffect ofwindresistanceisnot –2 –4 –6 –1 –8 ms 0 RF
ms aftertake-off withflapping flightensuing to flap and begin Wings open Micromus variegatus RH LH
RM W
LM kg . The bodydidnot − 5 mm 1 by brown LF RF +10 +20 +15 +5 ms lacewings and274 The yellowbarshowswhenthelacewingbecameairborneattake-off. first startedtomoveandwhenthemiddlelegslostcontactwithground. represented byfilledsymbols.Theverticalgreybarsindicatewhenthelegs squares) intherightmiddleleg.(B)Thesameangleshindlegare angle; blackopentriangles),andthefemoro-tibialangles(pink between thebodyandfemur(representingchangesincoxo-trochanteral a greenlacewing. Fig. energy storage, however, thesidesofmeso-andmetathorax have pre-requisite forjumping.Although thereisnorequirementfor before thelegsmovedrapidly, asinacatapultmechanism,is nota engaged toallowmusclecontractions togenerateandstoreenergy these jointsintoapositionatwhich lockingmechanismscouldbe legs heldatarangeofdifferent angles.Thissuggeststhat moving trochanteral orfemoro-tibialjoints ofthepropulsivemiddleandhind accommodate muchmusclemass.A jumpstartedwiththecoxo- femora indicatesthatthereislimitedspaceavailable to the extensortibiaemuscles,butthintube-likeshapeof the within thethorax.Someadditionalpowermayalsobegenerated by contraction ofthepower-producing trochanteralmuscles located implies thatjumpingbylacewingscouldbeproducedthe direct 1985; Josephson,1993;Weis-Fogh andAlexander, 1977).This range ofdifferent animals (Askew andMarsh,2002;Ellington, capabilities of250to500 their bestjumps.Suchoutputsarewellwithintheactivecontractile
.Angularchangesofmiddleandhind legjointsduringajumpby 5. Joint angle (deg) 100 140 180 100 140 20 60 20 60 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.110841 B A movements First leg (A) Plotofthetimecoursechangesinangle 2 1 +10 0 –10 –20
W
kg − 1 Wkg by theheaviergreenlacewings,evenin off ground Middle legs –1 found fornormalmusclefroma Time (ms) Take-off Femoro-tibial angle Femoro-tibial angle Body/femur angle Body/femur angle Middle legs Hind legs
The Journal of Experimental Biology performance compare withthoseofotherinsects? Fromasurveyof How doesthejumpingmechanism oflacewingsandtheir contractions. the thoracicstructuretoitsnatural shapeafterpowerfulmuscle to providegreaterflexibility the cuticleunderstrainandtoreturn when thetrochanteraldepressormusclecontracts,soitsrolemay be resilin isclearlylocatedinaregionthatwillbeplacedunder strain been linkedwithcuticulardevicesthatstoreenergy. Inlacewings, (Andersen andWeis-Fogh, 1964;Weis-Fogh, 1960)thathasoften fluorescence hasthepropertiesofelasticproteinresilin ridges thatfluorescebrightblueunderultravioletlight. The open orflapinthissequence. a trajectorythatwasupwardsandslightlybackwards.Thewingsdidnot began 4 plane. Fig. RESEARCH ARTICLE Jumping mechanisms
.Jumpbyagreenlacewinginwhichthebodyrotatedpitch 6. LH LH A downwardpitchofthehead(directionindicated byblackarrows)
ms beforetake-off andcontinued oncetheinsectwasairbornewith LM of legs First movement RH RH Take-off RM LM RF RM RF –12 –16 ms –2 –4 –8 0 +60 +30 +10 ms 5 mm contact withtheground.Thewingsdidnotopenorflapduringthissequence. that theantennaewerepressedagainstground5 depression andextension.Therotationofthewholelacewingcontinuedso arrows) occurredjustbeforetake-off asthehindlegswerereachingfull body rotated. Fig. 2012). Bycontrast, inhemipteranbugs,thejump ispropelledbyshort distortions ofthehindlegs(Bennet-Clark, 1975;BurrowsandSutton, generated bylarge extensortibiaemusclesisstoredin cuticular arranged atthesidesofbody. Forexample,inlocusts,the energy grasshoppers (Brown,1967), the propulsionisprovidedbylegs and Lucey, 1967),fleabeetles(BrackenburyandWang, 1995)and of insectscanberecognised.In insectssuchasfleas(Bennet-Clark and themusclesusedtopowertheirmovements,twobroadcategories movements ofthelegs.Basedonorientationpropulsive legs the skeletonandthenreleasedsuddenlytopropel rapid energy theygenerateisstored indistortionsofspecialisedregions strong jump.Thepower-producing musclescontract slowly, the amplification tomeetthehugerequirementsdemandedofarapid and that useacatapultmechanism.Suchmechanismsprovidepower relative tobodylengthachievedinajumparegeneratedbyinsects 3). the followingconclusionscanbedrawn(Table the jumpingmechanismsthathavesofarbeenrevealedininsects, First, thefastesttake-off speeds andgreatestdistancesheights LH
.Jumpbyabrownlacewing 7. RH RH LH The JournalofExperimentalBiology(2014)doi:10.1242/jeb.110841 of legs First movement A downwardpitchofthehead(directionindicatedbyblack LM RM RM ake- ff -o e k Ta RF RF –6 –1 –2 –8 ms –4 0 Hemerobius humulinus
ms afterthelegslost +20 in whichthe 5mm +10 +15 +5 ms 4257
The Journal of Experimental Biology Formula 4258 RESEARCH ARTICLE a columns ontheright arederivedfromthesemeasured data.Acc.,acceleration. ( ofthreejumpsbyeach The jumpingperformanceofthelacewings analysed.Datainthefourcolumnsonleftaregrandmeans fortheperformance Chrysoperla carnea Units are exceptionallylong,asinbushcrickets(Table high take-off velocitiescanbeachievedonlyifthepropulsivelegs levated aboutthecoxae(Burrows,2006a;Burrows,2006b). Burrows, 1977)andinfroghoppersthehindtrochanteramustbefully the hindtibiaemustbefullyflexedaboutfemora(Heitlerand jumping isthatthelegsmuststartfromaparticularposition;inlocusts arches (Burrowsetal.,2008).Inalloftheseinsectsapre-requisitefor trochanteral depressormusclesisstoredinthemetathoracicpleural arranged underneaththebodyandenergy generatedby legs, andthuswithaccelerationtimesoflessthan1 Table Micromus variegatus of similarlyshapedgrasshoppersthatuseacatapultmechanism than thebody, bushcricketsstillcannotmatchthetake-off velocities legs thatare4.6timeslongerthanthefrontand1.5 N N Best Mean (N Best Mean (N ) individualsofeachspecies;thebest performance(definedbytake-off calculatedvaluesinthesix velocity)ofaparticularindividualisalsogiven.The =7 forthiscategory. y distance (mm) Second, whenusingdirectmusclecontractionstopowerajump, 10 15 20 25 10 15 20 25 0 5 0 5 2 04 0–002 06 0100 80 60 40 20 0 –20 60 40 20 0 –20 2. Jumpingperformanceoflacewings A BD 0 6 =8) =9) 18 51015200 5101520 Take-off Take-off 36 Abdomen position Head position Stable jump mg ms m oyms Ac ie aeof Take-off Take-off ( Acc.time Body mass 071 1.0 19 10.7 m 9.0±1.1 . 00.6 10 3.5 3.6±0.4 0 Wings elevate 6 )( 18 49 Take-off 36 a a x distance(mm) 49 52090600 41 9401.6 4.0 39 94±10 0.6±0.04 15.2±0.9 t .±. .±.19± 5560.5 5.6 55 95±7 0.5±0.01 9.3±0.2 velocity( ) Time (ms) 10 15 20 25 25 10 15 20 5 0 5 C Take-off Take-off
s
3). Evenwithhind − 1 Jump withspin v
angle( ) ms, thatare 2 2630.7 6.3 62 120 3 4555.6 5.5 54 137 e m deg Take-off Θ Acc.(f ) f = 1 ants achievemoremodesttake-off velocitiesofgenerallylessthan contractions topowerjumping,suchasflies,stickinsectsandsome than thoseoffroghoppers.Otherinsectsthatusedirectmuscle longer thanthoseofgrasshoppersandmore30times long propulsivelegs,sothataccelerationtimesforbushcricketsare come attheexpenseofmuchlongertimeittakestomove (Burrows andMorris,2003).Theseconsiderableachievementsalso apparently usesbothacatapultmechanismandfourpropulsive legs 1994) alsousetwopairsoflegs.Ofthese,onlythesnow flea (Burrows, 2013a)andanant(Myrmecianigrocincta hyemalis) (Burrows,2011), afly(Hydrophorus alboflorens ) pairs oflegstogethertopropeljumping.Thesnowflea(
v
s m / − Third, thelacewingsanalysedhere,movemiddleandhind t 2
s ) − 1 (Table g g g = oc Energy( force f The JournalofExperimentalBiology(2014)doi:10.1242/jeb.110841 /9.81
Fig. open orflap.(A,C)Thechanging whole bodyrotatedinthepitchplane,butwingsdidnot lacewing inwhichtheheadpitcheddownwardsand correspond towingelevation.(C,D)Jumpbyagreen take-off. Notetheplateauxinabdominalpositionsthat propelled take-off. Thewingsopenedandflappedonlyafter lacewing inwhichthebodyremainedstableaslegs coordinates areplottedagainsttimeevery2 bars inB,D. arrows andyellow-filledsymbolsinA,Cbyverticalyellow on thegraphs.Take-off time(0 superimposed onthecorrespondingpoints(showninpink) In C,threeimagesfromthevideoofthisjumpare curved blackarrowsshowthedirectionofwingmovements. times (correspondingnumbersandpinksymbols).The cartoons inA showthepositionofwingsatparticular are plottedevery2 head (opencircles)andtipoftheabdomen(filledtriangles) 3).
.Trajectories ofjumps. 8. E Jm NW mN mW µJ =0.5mv E 2 Power( )
ms. Inthebottomtwographs(B,D) . . 117 0.4 0.1 . . 192 0.2 0.1 . . 140 0.2 0.1 . . 274 0.6 0.3 p = E / t p Force(F )
(A,B) Jumpbyagreen ms) isindicatedbyblack x andy F = fp/(0.1m mf coordinates ofthe musclemass )
ms. The ) (Tautz etal., Power/ kg − Boreus 1 ) y
The Journal of Experimental Biology use onlythemiddleandhindlegstogeneratetake-off. Lacewings donotmovethewingsuntiltheyareairborne,so they that is84%shorterthantake-off poweredonlybythewings. have atake-off velocitythat is 168%fasterandanaccelerationtime of thelegs.Nevertheless,jumpspoweredbybothlegsandwings moves itslegsandinsometake-offs makesonlysmallmovements Catapult mechanism 1994); Direct musclecontraction airborne phase. Thepropulsivemovementsof thelegstherefore off whenthewingsbegantoopenseveralmilliseconds intothe the bodyremainedstableduring take-off anddidnotspinafter take- strategy (59%ofjumpsingreen lacewings,65%inbrownlacewings) strategies wererecognised.Inthe firstandmostcommonlyobserved In jumpsbybothgreenandbrown lacewings,twodifferent jumping contrast, fleas arewinglessandmustrelyonlyonthelegsforpropulsion. By only wayofgeneratingenoughpowertolaunchintotheair. Snow and therebydoublingthemusclemassusedforjumping,maybe the alboflorens surface ofwater(Burrows,2013a).Second,snowfleas, snow (Burrows,2011) andtheflyH.alboflorens lacewings tojumpfromflexibleleaves,snowfleas insects ofasimilarmassusingcatapultmechanism.Thisenables a longertimebecauseaccelerationtimesareslower, comparedwith be distributedoveralarger areaprovidedbythefourtarsiandover Two reasonscanbeadvanced.First,thegroundreactionforceswill at thesametimeremainstobeexplained. (Burrows, 2011). Howallfourlegsaremovedtodelivertheirpower 8 1 contractions. Meandatavaluesaretakenfromthispaperandpaperslistedbelow. Take-off foreachspecies. velocitiesarethehighest recorded bydirectmuscle The insectslistedaredividedintotwogroups;thosewhichhavejumpsinvolvingacatapultmechanism,andwithpowered Animal RESEARCH ARTICLE Table Two jumpingstrategies (Burrows, 2012); (Sutton andBurrows,2011); Bush cricket( Brown lacewing( Ant (Myrmecianigrocincta Flea (Archaeopsylluserinacei Stick insect( Green lacewing( Prosartharia teretrirostris Locust (Schistocercagregaria Treehopper ( Planthopper ( Leafhopper ( Stick insect( Fly (Hydrophorusalboflorens Bush cricket,male Snow flea( Jumping plantlice( Shore bug( Hackeriella veitchi Froghopper ( Why doesthisthirdgroupofinsectsusefourpropulsivelegs? 3. Lacewingjumpingmechanismsandperformanceinthecontextofotherinsects 15 (Burrows andMorris,2002); H. alboflorens Boreus hyemalis and lacewingsallhavethinlegssothatusingtwopairs, Saldula saltatoria Sipyloidea Timema chumash Aphrodes makarovi Entylia carinata Philaenus spumarius Issus coleoptratus Pholidoptera griseoaptera 9 (Burrows, 2011); Chrysoperla carnea Micromus variegatus 12 (Coleorrhyncha) Psylla alni sp.), male , male ) 14 2 moves itswingsatthesametimeasit ) (Burrows, 2006a); ), female , ) ) ) ) 13 7 ), female female , 1 ) 11 16 female ), male ) 3 15 10 ) 2 6 16 (Bennet-Clark, 1975); (Burrows, 2008). 9 ) 5 ) 8 10 4 ) , female 3 (Burrows, 2007a); 12 to jumpfromthe ide363 150 35 Hind Middle 3.6 Hind Hind legs rplie oyms %o oy ffot ceeain Take-off Acceleration %offront %ofbody Bodymass Propulsive Middle 9 ide4710140 – Hind 170 Hind Middle andhind Middle 4.7 Hind Hind 140 130 Hind Hind Hind Middle 4.2 Hind Hind Hind Hind Hind Hind Hind Hind 11 (Burrows andWolf, 2002); 4 (Burrows, 2009a); H. (mg) 0010320 100 1540 2000 1 5 420 460 164 152 158 415 600 755 150 57 47.5 120 220 150 65 84 66 21.5 18.4 12.3 second category inwhichthebodyspunbut wingsdidnotflap. after take-off) tooklongertoreachaparticularheightthan those inthe that jumpsinthefirstcategory(no spinbutflappingwingmovements correlation betweenbodyangleand spinrate.A furtherdifference was was reflectedindifferent jumpsinwhichtherewasa strong where thethrustisappliedmust determinetheamountofspin.This presumably theresultingposition ofthecentremass,relativeto jumping strategiessothatthedifferent angleofthebody, and spin). Thelegmovementswereapparentlythesamein two to generatejumpsthatareeitherstable(nospin)orunstable (with conclude thatthetwotypesoflacewingsbothusesamestrategy used bythetwotypesoflacewingwhenjumpingwithspin. We spin. Similarly, therewasnosignificantdifference inthebody angle adopted byeitheragreenorbrownlacewingwhenjumpingwithout however, nosignificantdifference inthebodyangleattake-off angles whentheyjumpedwithspinandwithoutspin.There was, were significantlydifferent (see Results);eachadopteddifferent body and brownlacewingsthebodyanglesfortwojumpingstrategies pointed downwardssothatthebodysubtendedanangleof brown lacewings,13.7±7 ground orpointedjustabovebelowit(greenlacewings, at take-off. Inthefirststrategy, thebodywasclosetoparallelwith the twocategorieswasangleofbodyrelativetohorizontal lacewing didthewingsopen.Themostobviousdifference between rates ofupto22 brown lacewings),thebodyspuninpitchplaneonceairborneat In thesecondstrategy(41%ofjumpsingreenlacewings,35% launched thelacewingintoairandledsmoothlytoflappingflight. (green lacewings)and . 1120 180 110 160 61 90 65 86 190 2.8 2.1 1.3 5.9 154 0.7 5 12 (Burrows, 2013b); (Burrows andMorris,2003); The JournalofExperimentalBiology(2014)doi:10.1242/jeb.110841 7 140 170 eghlglnt ie(s velocity(ms time(ms) leglength length 7 187 170 Hind leglength 0210 70 5170 55 – 8120 38 2260 62 410100 100 64 Hz andinonlyoneofthejumpsbyeachtype − 6 (Burrows etal.,2007); 35±4
deg). Inthesecondstrategy, theheadalways – deg (brownlacewings).Forbothgreen 13 (Burrows, 2013a); 15 52 0.6–0.7 15–25 21.1 30 20 30.6 32.6 12 9 6.6 0.8 4.4 0.8 1.7 4 1.5 1.2 1.2 7 (Burrows, 2009b); 14 (Tautz etal., 0.6 1 1.6 2.5 3.2 0.6 1.5 2.1 0.9 0.9 5.5 2.9 4.7 2.7 1.8 1.5 2.1 1.9 − − 37±3 7±8 4259 deg; deg − 1 )
The Journal of Experimental Biology 4260 RESEARCH ARTICLE their songpatterns (Henryetal.,2002).A fewspecimens ofthebrown green lacewings to thelevelofsiblingspecies,for example,accordingto August andSeptember2013.Noattempt wasmadetoidentifyindividual variegatus et al.,2001;Tauber andTauber, 1973) andbrownlacewings Green lacewingsoftheChrysoperlacarnea survival chancesinthepresenceofapredator. tumbling motionaddsfurtherunpredictabilitythatmayimprove to aparticulartarget. Inother orientations,anunstablejumpwitha which thebodyremainsstablemaygenerateadirectedmovement jumps fromanuprightposture,orinresponsetocertainstimuli in to different typesofjumping behaviour(Card,2012).Inlacewings, tumbling jumps.Inflies,forexample,different stimuliclearlylead elicit jumpsandwhethersomeleadtostableothers to undersides ofleaves.Itis,however, notknown whatnaturalstimuli orientations, frequentlyemerging fromhidingplacesonthe lacewings jumpreadilyfromleavesandstemswithmanydifferent these analysesoflacewings.Intheirnaturalhabitat,however, insects, onlythejumpsfromahorizontalsurfacewereconsideredin To allowreadycomparisonwiththejumpingperformanceofother in planthoppersarebetween40and90 21 to187 and Picker, 2010).Infleabeetlestheforwardspinratesrangefrom jumps giventhattheirneighboursaredangerouspredators(Burrows suggested tobeamechanismforaddingunpredictabilitythe advantages. Jumpinginsectswiththehighestspinrates(480 relative tothepointwhereforceisappliedcanleadother for manyjumpinginsects,buttheabilitytoadjustcentreofmass translating ittoforwardmovement,wouldseembeadvantageous each elevationofthewings. two typesofjump(Fig. strategy butonly42 For example,toreachaheightof22 MATERIALS ANDMETHODS thejump of Biology moving fromoneplacetoanotheramongstvegetation. mechanism ofescapefrompredatorsandafastefficient wayof the highestvelocityofajumpandargue thatjumpingisbotha these mustoutweighthosewherealltheenergy isputintoachieving a predatorwillbemadeevenharder. Suchsurvivaladvantagesas catch aninsect.Second,ifthespinratecanbevaried,thentaskof subsequent siteforlandingandthusmakeitharderapredatorto it willaddtotheunpredictabilityoftrajectoryajumpand mole crickets,spinbackwardsatratesabove100 head pointsupwardsattake-off thenthespinrateisreduced.Pygmy same adjustmentofthebodyangleattake-off asinlacewings.Ifthe although muchlesscommon(2%ofitsjumps),resultsfromthe Nevertheless, Psyllidsalsohaveasecondjumpingstrategy, that (Burrows,2012),or15timeshigherthan inlacewings. 336Hz rotation tothebodyandspinratesinpitchplaneashigh arranged atthesidesofthorax,asinlacewings,impartaforward off, sothatthepropulsivemovementsofhindlegs,whichare Sternorrhyncha, Psyllidae)theheadagainpointsdownwardsattake- spin. InmostjumpsbyPsyllids(jumpingplantlice:Hemiptera, and seeminglyleaveslittlescopeforadjustmentthusavoiding This pointofforceapplicationisdistantfromthecentremass propel themselvesbyextendingafurcaattheendoftheirabdomen. the pitchplane)arespringtails(Collembola)(Christian,1979).They Avoiding spin,andhencethelossofenergy torotationinsteadof What evolutionaryadvantagecouldspinningaddtojumping?First, Hz indifferent species(BrackenburyandWang, 1995) and (Fabricius, 1793)werecaughtin Girton,Cambridge,UKin
ms usingthesecond,a38%decreasebetween 8). Thegaininheightwasclearlyslowedat
mm ittook58
group, (seeHenry, 1985;Henry Hz (Burrows,2009a).
ms usingthefirst
Hz, whichis Micromus
Hz in ranged from22to25°C. Measurements aregivenasmeans ± s.e.m.Temperatures inallexperiments Only jumpsfromthefloorof the chamberwereanalysedindetail. were recorded.A minimumoffivejumps wererecordedforeachlacewing. five jumpsbyeightgreenlacewingsand60ninebrown and thevaluespresentedareforfinalmillisecondbeforetake-off. Fifty- rolling threepointaverageofmeasurementstakenfromsuccessiveimages, acceleration time.Peakvelocitywascalculatedasthedistancemoved ina the legsandtake-off time wouldresultina10%errormeasuring legs untiltake-off. A one-frameerror inestimatingboththefirstmovementof defined astheperiodfromfirstdetectable,propulsivemovement of the allowed different jumpstobe compared.Theaccelerationtimeofajumpwas legs lostcontactwiththegroundandlacewingbecameairborne thus Take-off time,designated ast=0 camera software(RedlakeImaging,Tucson, AZ,USA)orwithCanvas14. front ofthechamber. SelectedimagefileswereanalysedwithMotionscope from thosecapturedunderneathasalacewingjumpedthevertical measurements. Changesinjointanglesweremeasuredfromtheseimagesand up to30 werenotincludedintheanalysis.Thosethatdeviatedby by morethan30deg possible tothisplane.Jumpsthatdeviatedfromtheimageplaneofcamera from jumpsthatwereparalleltotheimageplaneofcamera,orasclose image planeofthecamera.Measurementsdistancesmovedweremade middle ofthischamber, theshapeofwhichconstrainedmostjumpsto 100 Watkins andDoncaster, Cranbrook,Kent,UK).The camera,fittedwitha which thelacewingscouldjump,weremadeofhighdensityfoam(Plastazote, Systems InternationalInc.,Seattle,WA, USA). of thesameregionsthoraxweresuperimposedwithCanvas14(ACD edged bandpassfilteranddichroicbeamsplitter. UV andbrightfieldimages collected atwavelengthsfrom413nmto483throughasimilarlysharp- band from350 (Semrock, Rochester, NY, USA)withasharp-edged(1%transmissionlimits) conditioned byaSemrockDAPI-5060BBrightlineseriesUV filterset series 120metalhalidelightsource(EXFO,ChandlersFord,UK)was compound microscope(OlympusUK,London,UK).UV lightfromanX-cite objective lenses,underUV orwhiteepi-illuminationonanOlympusBX51WI lacewings wereviewedthroughOlympusMPlan5×/0.1 tests wereappliedassumingequalvariance. normally distributedbyusingtheShapiro–Wilk testandthenparametric morphological andkinematicalexperiments,dataweredeterminedtobe (Beaumont Leys,Leicester, UK).To makestatisticaltestsonboththe 55 with a100 μmsilverwire,inchambermadeofopticalqualityglass(width, occurred spontaneously, orwereelicitedbydelicatemechanicalstimulation 1024×1024 pixels,werefeddirectlytoacomputerforlateranalysis.Jumps (Europe) Ltd,West Wycombe, Bucks.,UK).Theimages,witharesolutionof exposure timeof0.5 determined toanaccuracyof0.1 projected ontoalarge screenfromthesamemicroscope.Bodymasseswere were measuredtoanaccuracyof0.1 microscope (Wetzlar, Germany).Lengthsofthelegsfixedspecimens a NikonDXM1200digitalcameraattachedtoLeicaMZ16stereo or in50%glycerol,werealsoanalysed.Colourphotographstakenwith and subsequentstoragein70%alcohol;fixationalcohol, and drawnthosepreservedbyfixationin:5%buffered formaldehyde lacewings andninebrownlacewings.Intactwerephotographed family ChrysopidaeandthebrownonestoHemerobiidae. these lacewingsbelongtotheorderNeuroptera,green place, werefilmedbuttheirmorphometricsnotanalysedindetail.All lacewing M.B. tocatchthegreen lacewings.We alsothank ourCambridgecolleaguesfor We are gratefultoMaxMcArthurforfinding the brownlacewingsandforhelping Acknowledgements Sequential imagesofjumpswerecapturedatrates1000 To searchforthepossiblepresenceofrubber-like proteinresilin, The anatomyofthehindlegsandmetathoraxwasanalysedin10green mm; height,55 mm microTokina lens,ora60 deg werecalculatedtoresultinamaximumerrorof10%the Hemerobius humulinus The JournalofExperimentalBiology(2014)doi:10.1242/jeb.110841 nm to407
mm; depth,27
ms withasinglePhotronFastcamSA3camera(Photron nm. Theresultingbluefluorescenceemissionwas
ms, wasdefinedasthetimeatwhichall
mg withaMettlerToledo AB104balance
Linnaeus 1761,alsocaughtinthesame mm). Thefloor, sidesandceilingfrom
mm MicroNikkorlens,pointedatthe
mm witharulerplacedonimages
NA and10×/0.25
s − 1 and an
NA t -
The Journal of Experimental Biology http://jeb.biologists.org/lookup/suppl/doi:10.1242/jeb.110841/-/DC1 Supplementary materialavailableonlineat commercial, ornot-for-profitsectors. This researchreceivednospecificgrantfromanyfundingagencyinthepublic, Both authorscontributedequallytoallaspectsofthepaper. The authorsdeclarenocompetingfinancialinterests. comments onthemanuscript. their manyhelpfulsuggestionsduringthecourseofthisworkandfor RESEARCH ARTICLE se,G .adMrh R.L. Marsh, and G.N. Askew, T. Weis-Fogh, and S.O. Andersen, Alexander, R.M.(1968). References Supplementary material Funding Author contributions Competing interests urw,M. Burrows, entCak H.C. Bennet-Clark, urw,M. Burrows, M. Burrows, M. Burrows, R.H.J. Brown, urw,M. Burrows, E.C.A. Lucey, and H.C. Bennet-Clark, Burrows, M. Burrows, M. Burrows, urw,M. Burrows, M. Burrows, M. Burrows, rcebr,J n ag R. Wang, and J. H. Brackenbury, Hunt, and J. Brackenbury, cuticle. Adv. In.InsectPhys. Auchenorrhyncha, Membracidae). 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The Journal of Experimental Biology