Biting in dragonfly fights

2013·0.57 MB·

by  Georg Rüppell

InternationalJournalofOdonatology,2013
Vol.16,No.3,219–229,http://dx.doi.org/10.1080/13887890.2013.804364
Biting in dragonfly fights
GeorgRüppella andDagmarHilfert-Rüppellb*
aAnderWasserfurche32,D-38162Cremlingen,Germany;bInstitutfürFachdidaktikder
Naturwissenschaften,TechnischeUniversität,Braunschweig,Germany
(Received6March2013;finalversionreceived8May2013)
SlowmotionfilmsoffightbehaviouroffivedifferentspeciesofOdonatawereanalysed.Inallcasesbiting
playedamajorrole.Thebitingdurationdependedonthedurationofastableconnectionbetweenthe
twoopponents.Sittingodonatesshowedmuchlongerbitingthanthosethatwereflying.InfightsofAnax
juniusandCalopteryxsplendenslongbitingbetweenmalesledtoseriousinjuriesanddeath.Twomales
ofAnaximperator biteachotherbyveryshortstrikesduringloopingflightstogether,betterdescribed
ashack-biting.Thishack-bitingwasseenintwootherfights:afemaleofLibellulaquadrimaculatabita
harassingmaleonthehead,immobilizinghim,andduringamale–malefightinC.splendensflyingnearly
onthespot.Loops,verybriefbutrelativelystableflightpositions,wereusedforbitinginthreecases.The
significanceofbitingininter-andintrasexualcompetitioninOdonataisdiscussed.
Keywords: fightbehaviour;inter-andintrasexualcompetition;dragonflyflight;looping;mandibleuse;
hack-biting
Introduction
Contestsamongindividualsovermatingopportunitiesarecommonacrossdiversetaxa,yetphys-
icalconflictisrelativelyrare.Duetothepotentiallyfatalconsequencesofphysicalfighting,most
animalsemploymechanismsofconflictresolutioninvolvingsignallingandritualisticassessment
(Umbers,Tatarnic,Holwell,&Herberstein,2012).Asaconsequence,physicalfightsininsects
havebeeninvestigatedonlyrarely.Duetotherateofresultsandtotheirunimpededbehaviourin
laboratoriesthiswasdonemostlyinOrthoptera(Briffa,2008;Gwynne&Bailey,1999;Shackleton
etal.,2005;Tachon,Murray,Gray,&Cade,1999;Umbersetal.,2012).Ontheotherhand,adult
Odonatadonotlendthemselvestolaboratorystudies,becausetheyshowtheirfullbehavioural
spectrumonlyinnatureandmostlyinflight.
InOdonata,fightshavebeendescribed(Corbet,2004;Marden&Waage,1990;Pajunen,1962,
1966;Waage, 1988;Wildermuth, 2008) but not analysed.There are frequent reports of injured
specimen of different Odonata species (Corbet, 2004), and the injuries have been taken as an
indicationofthedegreeofaggressivebehaviourinpopulationsofdifferentlatitudes(Calopteryx
splendens;Hilfert-Rüppell,2004;Hilfert-Rüppell&Rüppell,2008).
SinceadultOdonatararelyencounterrelatives,oratleastdonotrecognizethem,bothsexes
behaveselfishly.Consequently,duetotheasymmetriesofthenumbersofmaleandfemalegametes
there is intense competition among male Odonata for mates (Alcock, 1993). At reproduction
*Correspondingauthor.Email:[email protected]
©2013WorldwideDragonflyAssociation
220 G.RüppellandD.Hilfert-Rüppell
sitesoperationalsexratiosareusuallystronglymale-biased,somalesfightforlimitedresources
suchasterritoriesorfemales(Emlen&Oring,1977).Maleswithcolouredwingsmostlyshow
threateningflights,butathighdensities–aspredictedingeneralbyAlcock(1993)–maleswith
clearwingsfightwithphysicalcontact(Hilfert-Rüppell&Rüppell,2013).Intersexualfightsalso
may occur: female Odonata try to refuse some males. Although females show special refusal
behaviour(Corbet,2004;Hilfert,1998),sometimestheyfightagainstharassingmalesphysically
(Rüppell&Hilfert-Rüppell,inprep.).Older16mmslow-motionfilmshintthatlegsandbiting
mayplayaroleinfights(Rüppell,1984).Inmorethan30fieldseasonswithmanyobservation
hoursweonlyhadthechancetofilmaroundadozenfights.Onlynow,bymeansofdigitalslow
motion filming which allows recording for several minutes (Rüppell & Hilfert-Rüppell, 2009),
hasitbeenpossibletocatchimagesofbitinginflight.InthispaperweanalysebitinginOdonata
forthefirsttimeanddiscussitsroleinfightsindifferentsituations,withapproximateanddefinite
conclusions.
Materialandmethods
FilmingwasdonenearBraunschweig(52◦26(cid:3)N,10◦23(cid:3)E)inNorthernGermanyinsummer2011
and 2012 at ponds (Anax imperator, Libellula quadrimaculata and Coenagrion puella), and in
1984(Orthetrumcancellatum),andin1984and2011(Calopteryxsplendens)attheriverOker.
This medium-fast running river is 14–18m wide. In 1987 we filmedAnax junius nearWaco in
Texas(31◦33(cid:3)N,97◦9(cid:3)W),USA.Theolderfilmswerereanalyzedwithspecialattentiontobiting.
Allfightshappenedundersimilarclimaticconditions–sunnyweatherat25–35◦C.Fightswere
filmedinslowmotionat200–400framespersecondusinga16mmfilmcameraLOCAM(model
51) (1984, 1987 and 1988) and at 300 and 600f/s using a digital camera (Casio EX F1) in all
otheryears.Becauseofthehighflightspeedandtheunpredictableflightpathoftheinsects,the
camera was moved parallel to their movement and was triggered without viewing through the
viewfinderwithaprefocusedlens.Drawingsweremadebytakingthepositionsofthebodiesand
extremitiesfromsingleframesfromtheslowmotionfilmsaswellasdetailsofstructuresfrom
photosanddeadspecimens.
Results
BitinginZygoptera
AthighdensitiestwomalesofCoenagrionpuellafoughtforrareperchesbystrikingwiththeir
legs(filmedseveraltimes)andbyobviouslybiting,touchingtheopponentwiththemouthparts.
Thistouchingcouldbefilmedononlyoneoccasionandlasted0.05s.
InfightsofCalopteryxsplendens,whichoccurredathighdensitiesinwhichterritorialitybroke
downbecauseofveryhighintrusionratesamongterritoryholders,bitingwasfrequent.Inflight,
theopponentsgraspedeachother(Figure1)andtriedtoreachtheother’sbody,wingsorextremities
withtheirmouth.Thiswaslikewrestlingwhileflyingnearlyonthespot.Inthissituation,biting
lasted0.27s.Anotherinstanceofshortbitingwasobservedinflight,whentwomalesfoughtfor
afemale.Whenthefemaleleft,onemalebittheotherontherightforewing(Figure2),andboth
crashedontothewater.Thisbitinglasted<0.12s.Bitingwaslongerinanothercasewhenboth
malesrolled,flutteringtheirwingsoverthewater’ssurface,performingfiveturnovers.Duringthis,
onemalepresseditsmouthpartscontinuouslyontotheothermale,obviouslybitingortryingto
biteforabout1s(Figure3,Table1).AnotherbitinginC.splendensoccurredwhenamalelanded
ontherival,whichwasalreadyexhaustedandinjured.Thefirstmalebitfor4scontinuouslyinto
Bitingindragonflyfights 221
Figure 1. Inordertoreachthebodyorextremitiesoftheopponent,malesofCalopteryxsplendensgrapplewiththeir
legs(left).Onlyaftergettingcontactwiththeirlegsaretheyabletobiteeachother(right).Redrawnfromhigh-speedfilm
images.
Figure 2. AmaleofCalopteryxsplendensbitingintothewingofarival,leadingtoacrash.Bitinginflightisverybrief.
(Supplementarymaterialisavailableviathearticlewebpage).
Figure 3. FightbetweentwomalesofC.splendenswithbitingduringafive-loopmanoeuvre(beginningatthetopleft).
Fromfilm300f/s.
222 G.RüppellandD.Hilfert-Rüppell
Table 1. BitingbehaviouroffiveOdonataspeciesindifferentsituations.
Event Numberof Duration
Speciesand Locationand duration bitesor ofone
participants activity (s) strikes strike(s) Outcome Figure
Coenagrionpuella; Inair;dashingagainst 0.05 1 Unknown
male–male eachother
Calopteryxsplendens; On water; on 0.9 Continuedfightinair
male–male submergingfemale (nextrow)
C. splendens; Inair;flutteringnearly 0.27 Separated Figure 1
male–male onspot
C. splendens; Onwater;bothfive 1.1 1 Unknown Figure 3
male–male loopsforward
C. splendens; Onwater;opponent 4 1 Deathofattacked Figure 4
male–male lyingonwater male
C. splendens; Inair;afterafemale <0.12 1 Bittenmaleleft Figure 2
male–male escaped
Anaximperator; Inair;bothlooping 2 0.02 Unknown Figure 7
male–male forward
A.junius;male–male Onwater;bitingafter 1.17 1 Deathofattacking Figure 5,6
beingseparated male
Libellulaquadri- Inair;harassedfemale 0.2 3 0.03 Deathofattacking Figure 8
maculata; bitmale male
female–male
Figure 4. MaleCalopteryxsplendensbitingintotherightforewingofarival.Bitinginsuchastablepositioncanlast
severalseconds.Redrawnfromhigh-speedfilmimages.
theleadingedgeoftherightforewing(Figure4).Thisledtoimmobilityoftheloser,whothen
wascaughtbyafrog.
BitinginAnisoptera
Anax
Male–male competition of Anax junius was very intense in Texas, due to the hot climate and
thescarcityofwaterbodies.Malestriedtograspfemalesandfoughtwithothermales.Onone
occasionamaleseizedafemaleandgeneratedatandem,anothermaleplungedontothetandem
Bitingindragonflyfights 223
andbitintoitsconnection,causingittosplit.Theoriginaltandemmaleturnedaroundandbitthe
newtandemmaleinthebasalareaoftherighthindwing.Thislastedforabout1sandendedvery
suddenlybeforetake-offoftheattackingmale.Thenewtandemtookoff,too,buttheleadingmale
wasunabletobeatitsinjuredrighthindwingeffectively.Immediatelythetandemwasattacked
Figure 5. AtandemofAnaxjuniuswaspursuedandseizedbyanothermale.Theaggressorsplitthetandemmaleby
biting.Theseparatedmalebitback,thendeparted,whilethenewtandemmalecoupledtothefemalebutfailedtofight
offtheattackofathirdmale.Thepairdrowned.Behaviourfollowsthearrowsbeginningattop.Malesarenumbered.
224 G.RüppellandD.Hilfert-Rüppell
Figure 6. Theseparatedtandemmale(Anaxjunius)bitbacktheattacker,sittingonhim.Thefemale’sheadisshownat
reducedcontrast.Thisbitinginjuredtherighthindwinginthebasalregion(wingjoint),whichimpedednormalflapping.
Bothredrawnfromhigh-speedfilmimages.
Figure 7. AfightoftwomalesofAnaximperator.Aftergrasping,themaleshiteachotherwiththeirmouths.Thebody
axes(depictedonlyforthelowermaleasabrokenline)werebent(solidlineindrawingright)veryquickly(within0.007s
to48◦).Bothredrawnfromhigh-speedfilmimages.
byathirdmale,andtheycrashedontothewaterwheretheydrowned(Figure5,6).Theywere
eatenbywaterbeetles(Dytiscus).
Fightsinmid-airoccurredregularlyinmalesofAnaximperator.Mostlytheypursuedeachother,
but sometimes they clashed together. In such a situation, slow motion film (600f/s) revealed
biting during a forward loop (Figure 7). This biting began with opened mouth and was very
short. Two strikes lasting about 0.02s each were exhibited, which means the male reached a
strikingfrequencyof50Hz.Thisstriketimeconsistedofthreeequalparts:movementofthehead
towardstheopponent =0.006s,contacttime=0.006sandmovementbackwardstotheinitial
position=0.007s.AsdepictedinFigure7themouthwasopenedatthebeginningofeachstrike.
Whetherthiswasthecaseduringthewholestrikeisnotclearduetothechangingperspectiveof
theshiftinghead.
Bitingindragonflyfights 225
Figure 8. FemaleLibellulaquadrimaculatabitingamalewhowaslatereatenbyafrog(fromleft).Largedrawing
showsthemomentjustbeforebiting.Thefemalecontinuedovipositionnearby(right).Redrawnfromhigh-speedfilm
images.
Libellulaquadrimaculata
Athighdensities,malespursuedfemalesforpairings.Asamaleseizedanovipositingfemale,the
femalemanagedtogetabovehiminflight(Figure8).Inthispositionshebithiminthehead:first
for0.2scontinuously,andthenwithaseriesofthreeveryshortstrikes(seeTable1).Themale
triedtodislodgeherbyshakinghisbodylaterally(fourtimes,0.02seach).Thefemalereleased
themale0.75saftergraspinghim,andhetumbledontothewater,whereheremainedmotionless.
After25safrogswallowedhim.Thefemalecontinuedovipositionnearby.
Discussion
CompetingmaleOdonatabiteeachotherinfights.DeadandinjuredspecimensofOdonatacanbe
found,especiallyinplaceswithahighlymale-biasedoperationalsexratio.InnorthernGermany
theflightperiodsareshortduetothecoolandchangeableclimate;hereHilfert-Rüppell(2004)
foundmoreinjuredspecimens(damagedwingsorlossoflegs)ofC.splendens(345injuredmales
outof1911=18.05%)thaninthewarmerconditionsofsouthernFrance(111injuredmalesout
of856=13%;chi-square-test:χ2 =10.26;p =0.001).Itseemsfightsaremainlyresponsible
forinjuries,althoughothercausessuchasaccidentsmayplayaminorroleindamage(personal
observations).
InfightsOdonatausefourdifferentweaponstodamagetherival:thelegs,whichareequipped
withmanyspines;themouthparts;arammingdeviceconsistingoftheprominentfrontalpartsof
thehead–frons,clypeusandlabrum(especiallyinAeshnidae);andclashingwings.Inthispaper
226 G.RüppellandD.Hilfert-Rüppell
Figure 9. ThetoothedmandiblesofamaleAeshnacyanea,thebitingorgans(length=ca.3mm).
wereportonlyonbiting.Thebitingweaponsofinsectsarethemandibles(Briffa,2008;Emlen,
2008;Judge&Bonanno,2008).Odonatapossessveryprominenttoothedmandibles(Figure9)
withwhichtheyareabletocutthehardsclerotizedcuticleofprey,hencebitingwiththemshould
alsobeveryeffectiveinfights.Infights,however,bitingmovementsofthemandiblesarehard
to recognize, even in slow motion films. We only can describe biting as contact of the mouth
partswiththeopponent’sbody,becausetheinteriormovementsofthemandiblesarehidden.But
damage,asfoundforexampleinawingofabittenmaleafterthecontact,indicatesrealbiting.
Bitingcantakeplaceanywhere–inair,onthesurfaceofwater,onthegroundorinvegetation.
Inordertobite,astablepositionofthebodyisneededtoinsertthemandiblesintotheopponent’s
surfaceandtoproceedwithoutbeingdislodgedbybodymovements.Stablepositionsarehardto
maintainbecauseoftheopponent’sdefensivemovements,anddependonthecontactsituation.The
longerstablecontactlasted,thelongerwasthedurationofthebiting.Weobservedbitingdurations
of1-4swhentheattackerwassittingonthewater’ssurface.InC.splendensbitinginflightlasted
for relatively long periods, however, probably due to the outstanding flight manoeuvrability of
this species (Rüppell 1985, 1989). Dashing together is a too short manoeuvre to allow biting,
but flying a loop together, which seems to be a controlled flight manoeuvre, requires a longer
periodandrendersbitingpossible.Odonataoftenflyloops(unpublishedslowmotionfilms).We
previouslyfoundbitingduringloopsinOrthetrumcancellatum(Rüppell,1984),andinthisstudy
inC.splendenswhileturningoverfivetimesonthewatersurface,andinoneloopbyA.imperator.
Inthelatterspeciesbitingtimewasveryshort.Itishighlyimprobablethatthemouthpartscan
performrealbitinginthisshorttime.Duetotheshortcontacttimeofonly0.006sinonestrike
weassumethatthemandiblesstaymotionlessrelativetothecraniumandareusedtohackatthe
opponent.Anotherargumentforthatinterpretationisthatapreciseandsynchronizedclosingof
themouthpartsseemstobeimpossible.Within0.006sthedragonflyprobablycannotpredictthe
exactmomentofhittingtheopponent’ssurface,soastoclosethemandiblesforbiting.
Theactioninsuchbriefencountersshouldbecalledhack-biting(Figure10).Themusclesofthe
mandiblesofOdonatahavetoberelativelylargeandstrongtosucceedinrapidlycuttingupthe
chitinouscuticleofpreyduringeating.Becauseoftheinverserelationshipbetweencontraction
velocityandmaximumforce,andthefactthatthemechanicalarrangementofthemandiblesis
probablyadaptedforhighforceproductiontocrushthepreycuticle,itisunlikelythatcontraction
velocityishigh.
Bitingindragonflyfights 227
Figure 10. ViewintotheopenedmouthofanAnisoptera(Aeshnacyanea).Upperrow:themouthparts(mandibles
superior,maxillaebelow)aredrawnback(left)atthebeginningand,wesuggest,close(right)duringnormalbiting.
Lowerrow:themouthpartsprobablyremainopenduringhackbiting.
Wefoundthishack-bitinginaweakerforminC.splendens,anddistinctlyinL.quadrimaculata,
anotherspeciesofAnisoptera.Thefrequencyofhack-bitingrangedfrom33to50Hz(C.splen-
dens,L.quadrimaculataandA.imperator).Thesehighfrequencieswereperformedfortwo(A.
imperator,C.splendens)orthreestrikes(L.quadrimaculata)(Table1).
In view of the brevity of individual encounters in Odonata it is not surprising that mutual
assessmentmayplayonlyaminorroleindecisionsaboutwhetherornottofight,asdescribed
forslowersystems(Arnott&Elwood,2008;Parker,1974).
Duetothefrequencyofbitingeventsandtheelusivenessofthecombatantswedonotknow
the prior condition of the participants, such as residency or their preceding success in fights or
pairings. Both conditions are important for the explanation of fight outcomes (Hilfert-Rüppell,
2004; Jennions & Backwell, 1996; Kemp & Wiklund, 2004). We can only state that serious
damage resulted from long biting, but not from short events. The mandibles in short bitings
in flight impinged on the opponent haphazardly but often first on the legs because of defence
reactions.Thismightexplainthelossoflegsoftenseenindragonflies(unpublishedobservations;
Hilfert-Rüppell,2004).
Longbitinginfights,intwocases,wasdirectedatthewingsofthecombatant,causingreduced
mobility.Longbitingledtoimmobilityofmalesintwocasesandtosubsequentdeathbyafrog’s
attackandtodrowningafterdamagetoawing.Thusitcanbeaveryeffectivebehaviourpatternto
winadispute.Despitethepaucityofdocumentationitprobablyoccursverycommonlyinfightsof
Odonata.Bitesseemtobeanimportantweaponinintra-andintersexualcompetition,whichare
particularlysevereinOdonata(Corbet,2004;Córdoba-Aguilar&CorderoRivera,2005;Pajunen,
1962,1966).
228 G.RüppellandD.Hilfert-Rüppell
Anumberofquestionsareraisedbyourobservations:
(1) Thereseemstobearelationbetweenfightingwiththelegsandmouth.IsittruethatOdonata
withlongandfragilelegs,e.g.Calopterygidae,tendtobiteonly,whereasAnisopterainten-
sively strike with their solid and well-armed legs or ram each other with their prominent
frontalpartsoftheirheads?Moregenerally,arefightingtechniquesreflectedindifferences
inmorphology,especiallyofthelegsandhead?
(2) Although after being separated from the female the male of A. junius had no chance of
regainingthefemale,hebitbackattheattackingmale.Hedidthisveryeffectively,sothat
thebittenhindwingwassubsequentlynearlyuseless.Wasthispurelyself-defensive,orwas
heattemptingtoresumethetandemwiththefemale?
(3) WhatdidthefemaleL.quadrimaculatagainbybitingtheattackingmaletoimmobilityrather
thansimplyflyingaway?
(4) Howfrequentandimportantisbitinginintraspecificconflictsingeneral?
Weareconvincedthatbitingoccurseverydayandeverywherewhenhighdensitiesofdragonflies
produce intense competition, reported in general by Knell (2009), and with digital recording
techniquesitcouldbefilmedmoreofteninslowmotion.Morestudiesofbitingareneeded–not
only for answering proximate, mechano-physiological questions but also for clarification of its
adaptivevalue.
Acknowledgements
WethankHansruediWildermuthandFrankSuhlingforencouragementandGeorgSeifertforinitialhelpwiththeEnglish
and for comments. Mike May, Richard Rowe andAndreas Martens helped to clarify the manuscript with important
questionsandcomments.
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