Visually controlled head movements in perched anisopteran dragonflies

10 Pages·1995·3 MB·English

by  Miller, P L

Odonalologica24(3):301-310 SeptemberI, 1995
Visuallycontrolled headmovements
inperchedanisopterandragonflies
P.L.Miller*
The Queen’sCollege,Oxford,OX1 4AW,United Kingdom
Received January26, 1995/ ReviewedandAcceptedMarch2, 1995
Small,moving,visualtargetscommonlyexcitefastsaccadicheadmovements(head-
-cocks)in percheddragonflies.Head-cockinginresponse tonaturalstimuli hasbeen
examined byvideo-recordingperchedindividuals of7libellulid and 1gomphidspe-
cies in the field duringperiods offeedingorsexual activity. Head-cocks varied in
durationfrom40to >1000 ms(mean350ms)and theyusuallyoccurredmany times
perminute. Typicallyahead-cock consisted of3 components:afastsaccadic move-
mentin the rolling and/orpitchingplane;abriefperiodofstasis orofslow,smooth
headmovement, ofteninvolvingayawcomponentand interpretedasvisual tracking;
andfinallyafastreturn totherestposition.Aminorityofhead-cockswasfollowedby
take-off,normallyinthedirectiontowhichthehead hadbeenaimed. Inspecies which
kepttheirforelegs liftedoffthe groundwhen perched(e.g.Orthetrum),yawingwas
sometimes amplifiedby aturningoftheprothorax onthesynthorax, andalso some-
timesby rotations ofthe whole body onthelegs. Head-cocks could be evoked by
throwingorswingingstones 10-20cminfrontofapercheddragonfly,buttheirmean
durationwassignificantlyless thanthatofspontaneoushead-cocks.No head-cocking
has been seeninperched aeshnids orinthe zygopterans examined. Head-cocks are
believed to aim theacute zonesoftheeyes at atarget,andthey may also allow its
distance tobeestimatedbystereopsis sincetheaxesofsomeommatidiainaforward-
-lookingacutezoneeithersideofthe ironsconverge afew cm in front ofthe insect.
Head cocks may also determine the direction oftake-offthroughthe action of
proprioceptors in the neck.
INTRODUCTION
Dragonflies arewellknown touseoneoftwo principal strategies infeeding and
inreproductive behaviour- perchingandflying(CORBET, 1962).Fliers, such as
most aeshnids, may beon the wing continuously duringactive periods and can
search inalarge areabut, compared toperchers, they pay ahigher energetic cost
￿ Correspondenceaddress: 68Blenheim Drive,Oxford,OX28DQ,UnitedKingdom
302 P.L.Miller
andmaysuffera visualimpairmentasaresultoftheirmovement.Animalscan see
betterwhenthey areimmobile,forexample duringhovering, stalkingor perching,
andthevisualcostofforwardflighthasbeenestimatedtobeequivalent toalossof
2-3 log units of light intensity (HORRIDGE, 1977). Perching libellulidsand
gomphids usually choosesites wherethey canmaintaina high body temperature,
andfromwhichtheycan scan alargeareaandtakeoffrapidly inpursuit ofprey or
conspecifics.
Observationshaveshownthatalert,perched dragonfliesmakefrequentandabrupt
head-cocks, sometimesoflarge amplitude. Theseresemblethesaccades ofother
animalsandthey are presumed to beinresponse to moving visualtargets.Only a
smallminority ofhead-cocksis followedby take-offs. Head-cocks may allowthe
dragonfly toscrutinizea visualtargetusing theacutezones ofthecompound eyes
where visual resolution is high, and also to estimate its distance by stereopsis.
Many libellulidshave two acute zones, recognisable from the large size ofthe
pseudopupil wherethey are found:thesearea40°zone inthefronto-dorsalregion
ofthe eye comprising large-diameter ommatidia(LAND, 1989), and a smaller
forward-looking zoneoneithersideofthefronswheretheommatidiaarenarrower
(HORRIDGE, 1977).
HORRIDGE (1977) has drawnattentionto the many arthropods which make
abrupt turnsor saccadestowards visualtargets.Forexample hunting spidersmove
thewhole body roundtoface a target (LAND, 1971),mantids makefast turnsof
the head(LISKE & MOHREN, 1984;CORRETT, 1990;ROSSEL, 1991),crabs
move onlytheeyestalks (HORRIDGE, 1966),whilemanyrunning(MILLER, 1979)
or flyinginsects(COLLETT, 1980;EGELHAAF,1987)performsaccades by turn-
ing thewholebody.
Theaimofthisreportisto drawattentiontothehigh frequency ofhead-cocking
inperched dragonflies, inwhichbothasaccadic andasmooth-tracking component
can be distinguished. The marked variability ofthe take-offthresholdfollowing
head-cocks isalsoemphasised, whichperhaps gives someinsightintothe‘motiva-
tionalstate’ ofaninsect.
MATERIALANDMETHODS
Observations andvideorecordingshave been madeon6 Onychogomphusuncatus (Charp.)(ma-
ture males),4 Libellulafulva Mull, (mature males and females),4 L. quadrimaculataL, (mature
males), 1Orthetrumbrunneum (B. deFonsc.) (maturemale),15O.cancellatum (L.)(teneral,imma-
ture and maturesofbothsexes), 9O.coerulescens (Fabr.)(maturemales andfemales),4Sympetrum
danae(Sulz.)(maturemales)and 15S. striolatum(Charp.) (teneral,immatureand maturemales and
females),all when perchedin sunlightduringfeeding,and in somecasesalsowhen reproductively
activenearwater. Theyweremade between 10.00 and 16.00h. on several days duringJuly and
August, 1993and 1994,inEnglandatsitesnearOxfordandatThursleyNational NatureReserve, and
inFranceonthe River Vidourle (H6rault)and also in the vicinityofcanals intheVeniseVerte (the
easternareaoftheParcNature! RegionalduMarais Poitevin).
Video records(SONY Hi-8 x24) weremade ofheadmovementsoccurring spontaneously(pre-
Head movementsinperchedAnisoptera 303
sumed tobe tonaturaltargets)orwhichwere
evokedby small stones(ca5 mmdiameter),
thrown orattachedtoathreadand swung 10-
20cm infront ofthe perchedinsect. They
wereanalysedin singleframes at 40 msin-
tervals. Sketches ofheadpositionsweremade
ontransparent paperonthemonitorandalso
fromfrozenspecimensexaminedunderabin-
ocular microscope.
Fig.1.Thethreeplanesofheadmovements:X=pitch-
Thedragonflyheadcanbemoved inthree
planes intersectingatapointjustbehind the ing;-Y=rolling;- Z=yawing.
head, bymuscles which act onthe cervical
sclerites (cf. GORB, 1993).Theplanesaredescribedasyawing(horizontalrotations about avertical
Zaxis),pitching(upwardsmovements aboutahorizontal Xaxis),androlling(rotationsaboutalongi-
tudinalYaxis) (Fig. 1).Thepseudopupilswerephotographedin theeyesoflivingspecimenswhich
werethen preserved in 2% formaldehyde.Thick horizontal sectionsofpreserved heads weremade
with arazorbladeformicroscopic observationsontheorientation ofommatidia.
RESULTS
OCCURRENCE OFHEAD-COCKING
All libellulidand gomphid species examined in the field madefrequent, fast,
spontaneoushead-cocks whileperched. Somewereseentobemadeinresponseto
naturaltargetssuchas conspecifics, otherinsects, birdsandinone caseapparently
to vehiclesonanearby road,butinmany thetargetwas not identified(Fig. 2).
Nohead movement,except thoseaccompanying grooming or feeding, was ob-
servedinthefollowing species,allexaminedwhileperched vertically:Anaximpera-
tor,Aeshnagrandis, A.mixta, Cordulegaster boltonii.Norwerehead-cocksseenin
any ofthe following zygopteran species, observed whileperched duringperiods
when they werefeeding: Ca-
lopteryx splendens, C. hae-
morrhoidalis, Enallgma cya-
thigerum and Ischnura ele-
gans.Itcantentatively becon-
cludedthathead-cocking does
not occur inanisopteran fliers
whichperchvertically,suchas
aeshnids, norinZygoptera.
In libellulidspecies, head-
cocking didnot appearwhile
prey items were being chew-
ed, or atleast until they had
Fig. 2.Diagramtoshowhead positionsofalibellulid: (A)in
restingposition;- (B) pitchedupwards; - (C)rolledtothe been nearly consumed; nor
right. wasit seeninfemalesin tan-
304 P.L.Miller
demthough itdidoccur intandemmalesandinmales duringcopulation. Nohead-
-cocking was seen inteneralsbeforefeeding hadstarted.
FEATURES OFHEAD-COCKING
Thelibelluliddragonfliesexaminedperched duringthe dayusually withthelong
axis of the body between 0
and 45°to thehorizontalac-
cording to theperch site, and
with theheadand body level
in the rolling plane. The an-
glebetweentheheadandtho-
rax showedlittlechange with
body position except during
head-cocks. Head-cocks in-
volvedmovementofthehead
in any orall ofthe planes of
movement. Rolling rotations
ofthehead(Y axis)occurred
through up to 80°, upwards
pitching (X axis) by amaxi-
mum of50-60°, and yawing
(Z axis) to one side or the
other by 20-30°. Many re-
cordedheadmovementscom-
bined at least two of these
components(Fig. 3), butthe
videorecords usually didnot
permit amoreprecise resolu-
Fig. 3. Plotsofhead-cocksin Orthetrumcancellatum: (A) a
briefhead-cock achievedby arollingmovementtotheright; tionoftheircontributions.
-(B) alonger-lastinghead-cock broughtaboutby rollingto O. cancellatum, O. coerule-
theright (D-—□), therollpositionthen beingheldsteady scens andL. quadrimaculata
while therewasaslow pitchingupwards(O O). commonly perched with the
forelegs heldupin theflight
position and inthese species head-cocks were sometimesaccompanied by lateral
turning movements oftheprothorax on thesynthorax. Theraising oftheforelegs
appears tobe amechanismtoallow a greaterdegreeofheadmovement to occur.
Sometimes dragonflies rotatedabouta vertical axis ontheperch by moving their
legs, andthisprovided afurther meansofamplifying the headmovements in the
yawing plane.
Spontaneous head-cockswere variableindurationlastingfrom 80toexception-
ally > 1000ms,measuredfromthestartofaheadmovementuntilthereturn tothe
Headmovements inperchedAnisoptera 305
restposition. InO. cancellatumthey hadameantotaldurationof350±36ms (s.e.;
32movements from4individuals; max800 ms). Incontrast evokedhead-cocks in
response to stones whichwere thrown or swungpast perched insects were typi-
cally briefwith ameandurationof 182±11 ms(s.e.; 46 movements from 4indi-
viduals),significantly shorterthanspontaneoushead-cocks(paired t-test;Df, 31;p
=0.0002),andthey wereoftencompleted whenthestonewas stillapproaching the
dragonfly.
Head-cocks can be dividedintothree stages: firstly, afast saccade-like rolling
and/orpitching movementcausing theacutezones ofthe eyes tofacetowardsthe
target,usuallycompleted in<40ms;secondly, aperiodofnomovementorofslow,
smoothturning, assumedtobe targettracking, whichmightbebriefbutsometimes
lastedforuptoseveralhundredmsandmightincludeayawcomponent;andthirdly
afastreturn totherest position, completed in 40-80ms (Fig. 3).The majorityof
head-cocks involved mainly fast upand return movements, the prolonged mid-
-stage appearing less commonly, perhaps when the target was distantor slowly
moving.
Table I Spontaneoushead-cockscommon-
The meanfrequenciesofspontaneous head-cocks lyoccurred 10-20timesperminute,
observedin the field- [S.E. =standarderror;N = although sometimestherewere only
No.ofinsectsobserved] 1-2 per minute and the mean fre-
quenciesfordifferentspeciesranged
MMeeaann from8 to 18 min'1(Tab. I). Theval-
SSppeecciieess ffrreeqquueennccyy SS..EE,. NN
((mmiinn1')) ues probably reflect the variable
abundance of visual targets in the
OOnnyycchhooggoommpphhuussuunnccaattuuss 1177..00 -_ 11 vicinity and are unlikely to depend
LUibbeelllluullaa ffuullvvaa 1188..00 55..55 33 on intrinsic species differences, al-
LL. qquuaaddrriimmaaccuullaattaa 88..00 11..9944 55 though thepossibilityofsomespon-
OOrrtthheettrruummbbrruunnnneeuumm 1166..00 -- I1
OO..ccaanncceellllaattuumm 88..3333 11..7722 66 taneous head-cocks occurring with-
OO..ccooeerruulleesscceennss 1111..5566 11..4411 99 out astimuluscannot beruledout.
SSyymmppeettrruummssttrriioollaattuumm 99..4444 33..1122 99 ‘Investigatory’ flights are defined
asthoseinwhichthe dragonfly took
offand flew towards a target, and then quickly returned to the sameperch. In
contrast ‘alarm’flights are thoseinwhichtake-offswere followedbythedeparture
oftheinsect.Inmostdragonfliesonlyasmallproportionofhead-cocks,and some-
timesnone, wasfollowedby atake-off.Forexample oneO. uncatus,perched close
totheriver, head-cockedtoeachof40stonesthrownat3 sintervalsor swungat0.5
s'1inits vicinity,butnevertookoff.Anactively feeding S. striolatumhead-cocked
in responseto 47%ofall swungstones (n=l 12) andtookoffin responseto 10%
(11) ofthem.HoweveranimmatureO. cancellatum(a malelackingpruinescence)
head-cockedandthentookofftoinvestigate eachof20stones thrown at5-second
intervals, re-settling onthesameperch in<3 s,although inno case diditattempt
toseize thestone. Such take-offswhichledto investigatory flightswere normally
306 P.L.Miller
made in the direction to
which the head had been
cocked, flightbeinginitiated
beforetheheadhadreturned
to itsrestposition.
Repeated swings ofastone
infrontofaperched dragon-
fly sometimesevoked head-
-cocking responses which
gradually wanedinfrequency,
perhaps representing habitua-
tion of the response(Fig. 4).
Howeverthedifficultyofpre-
senting a targetidentically in
consecutiveswingsmakesthis
conclusionuncertain.LAND
(1971) found that spiders
quickly habituatedtorepeated
excitation ofoneregion ofa
lateraleye, butremainedre-
sponsive to excitation of
Fig.4.Plotsofsuccessive head-cocksin (A) O.cancellation nearby regions.
and(B)O.uncatus inresponse toastonebeingswung 15cm Observations and photo-
in front ofthe head onceevery two seconds. - [Each head- graphs oftheeyes in living
-cockisrepresentedby onepoint.Zeroreadingsindicate the O. cancellationhave shown
absence ofahead-cock].
that in the forward-looking
region eithersideofthefronsthepseudopupil isabout 1.3 mmlong and0.43mm
wide.Horizontalsections ofpreserved headsofO. cancellatumandS. striolatum,
madeattheleveloftheventralmarginofthefronswheretheeyes areseparated by
3.5mm, allowedthe positions and orientationofommatidiain thisregion to be
photographed and drawn(Fig. 5). Theommatidianearest thefronswere foundto
beinclined towards themidlineby maximally 4.5°to thelong axis ofthe body,
withvisualaxes converging about2cminfrontofthehead.Over asmalldistance
laterallyofabout5 ommatidialdiameterstheinwardtiltdeclinedanddisappeared,
buttheareaofconvergenceextendedverticallyoneithersideofthefronsforabout
1 mm. Ommatidiain themedial part ofthe eyes on thedorsal surface also have
visualaxes withasmallconvergence,but they are probably spaced too closely to
beusedeffectively forstereopsis. Ommatidiainthehindpartoftheeye are tilted
towardstheposterior andhavefieldsofvisiondirectedbehindtheinsect.
Headmovements inperchedAnisoptera 307
DISCUSSION
Saccadicbehaviour,inwhichtheeyes arerapidly switch-
edtoanewpartoftheenvironmentby body,head,eyestalk,
oreye movements,is widespread in bothvertebratesand
invertebrates(e.g. ROGERS etal., 1993).By keeping the
eyessteady, visualdiscriminationcanbeenhancedandthe
targetcan befixatedby thatpartoftheeyes best adapted
forhighresolution.During thesaccadethebrainmaycease
toanalyse visualinformation(cf. HEISENBERG& WOLF,
1979).
Themainconclusionbasedon observationsofdragon-
flies in the wild is thatactive, perched libellulidsmake
surprisingly frequent saccade-like head-cocks, often one
Rg.5. Diagramofahori- everyfewseconds, eventhough thegreatmajority arenot
zontal section ofthe head followedbyatake-off.Whentake-offdoesoccur,itis com-
ofO.cancellatum madeat monly madeinthedirectiontowhichtheheadwascocked.
the level ofthelower mar- ObservationofmaleS. striolatumperched on astick ina
ginofthe frons,showing
the orientation ofthe om- cageinthelaboratory revealedno head-cocking andIas-
matidia. Ommatidia in the sumethatallspontaneoushead-cocks inthewildoccurin
anteriorpartoftheeyehave response to moving visualtargetseventhough Ifailedto
visualaxeswhichconverge detectmany ofthosetargets.
in front ofthe dragonfly’s
Head-cocksaredivisibleintothreestages:afastsaccadic
head.
rolland/orpitchofthehead,aperiod ofvariableduration
whentheremaybe nomovement or aslowturning oftenincluding a yawcompo-
nent,and finally afastreturn to therest position. Only whentargets can bepre-
sentedundermore controlledconditionswillitbepossible torelatetheheadmove-
ments more closely to targetposition and velocity. When the perched dragonfly
keeps itsforelegs lifted, head movements intheyawing planeare sometimesam-
plified by laterally directedturnsoftheprothorax. Dragonflies mayalso turn the
whole body sideways by moving the legs. Head-cocking appearsto be inhibited
duringprey-chewing at leastuntilmost ofthefoodhasbeenconsumed,andalso
during grooming androosting, andinteneralinsectsandtandemfemales.
Someactively feeding,immatureO. cancellatumhadparticularlylowflightthresh-
olds, takingoffafterevery evoked head-cock, whereasmature dragonflies head-
-cocked as frequently but seldom tookoff. Though dragonflies respond to many
visualtargetsbyhead-cocking, acentralmechanismprobably determinesthethresh-
oldofasubsequent take-off, causing itto belowin immatureand hungry insects
but higher inthosewhichare mature andwell-fed.Thatsexually active malesre-
sponded to artificial targets with head-cocks as readily as immatureinsects but
were never then seen to takeoffto investigate them, suggestseither that experi-
ence, or possibly aninnateresponse toconspecifics, can improvethediscrimina-
308 P.L. Miller
tionof visual targets.
Atentative scheme is
presented in Figure 6
in which several fac-
tors are shown to act
onthetake-offthresh-
old.
In smooth tracking,
slow and continuous
adjustments ofeye (or
insect) position keep
theacute zonesaimed
atamovingtarget(e.g.
LAND & COLLETT,
1974; COLLETT &
LAND, 1975;LAND,
Rg. 6. Row diagramshowingthepossible effectsofvarious factors,
1992) and they over-
shown within circles,whichmay influence the head-cockingand the
take-offthresholds. - [Arrow thicknessgivesaqualitativeimpression -ride optomotor re-
ofthefrequenciesofoccurrence]. sponses which would
otherwise tend to sta-
bilise the eyes’ (and
insects’) position inspace(EGELHAAF, 1987).Theslowmovementsofthedrag-
onflyhead whichsometimesfollowedtheinitialfast saccadeareassumedtorepre-
sent visual tracking. That such activity occurred much more commonly during
spontaneoushead-cocksthaninthoseevokedby artificialtargetssuggests thatthe
dragonflycouldquickly identify stonesas targetsofnointerest, a conclusionalso
supported by thebrevity ofmostevoked head-cocks.
Head-cocking inaperched dragonfly mayserve threepossible functions.Firstly
it may aim either the dorso-frontalor forward-looking acute zones oftheeyes
towardsthetarget, thereby enhancing target discrimination.Secondly itmaypro-
vide informationabout thetarget’s distance fromthe dragonfly. Anisopterans in
flight canprobably estimatethedistanceofprey, matesor landing sites by motion
parallaxinformationas insomeotherinsects(SRINIVASAN etal., 1989;SOBEL,
1990),although stereopsismayalso play apart atshort distances. Perched dragon-
flies, however, cannot use motionparallax and probably depend on stereoscopic
visionfordistanceestimation, asdosomeoftheirlarvaeandmany otherambush
predators(COLLETT, 1987).ThefronsofS.striolatumandO. cancellatumsepa-
rates theforward-looking regions oftheeyes by about3.5 mm,slightly morethan
the separation ofthe eyes of some Calopterygidae. Forward-looking ommatidia
nearthemedialmargins ofthetwo eyes have visualaxes whichareaimedinwards
by up to about 4.5° and converge about2 cm in front of thehead. Ommatidia
placed slightly more laterally have axes which converge further in front. These
Head movementsin perchedAnisoptera 309
maypermit somestereoscopic visionto occur, allowing thedistanceofa targetto
be estimated.Informationabout target size and distance are two ofthe factors
whichmaybe used to determinewhethertake-off shouldoccur, but dragonflies
may also learntorecognise theappearanceor characteristicmovements ofpoten-
tial mates orprey. These mechanisms may combineto reducethelikelihoodof
pursuing inappropriate targetssuch as birdsor aeroplanes - or thrown stones. A
third functionofhead-cocks maybeto determinethedirectionoftake-offthrough
theasymmetrical excitationofneck proprioceptors (MITTELSTAEDT, 1957).
Thespecies ofAeshna observed together withCordulegaster were not seen to
make head-cocks when perched. This may be because such species are ‘fliers’
(CORBET, 1962), being continually on thewing when feeding and usually also
when sexually active. The absence of head-cocking inthe Zygoptera examined,
however, ismoresurprising sinceCalopteryx spp.andotherZygoptera frequently
detectpassing prey whileperched andtakeoffinpursuit. Ifhead-cocking never
occurs in thesespecies, it maybe becausetheireyes donot have well developed
acute zones, adequate informationabout targetdirectionand identity being pro-
videdby any region oftheeyes.
ACKNOWLEDGEMENT
1amdeeplygratefultoKATEMILLERforassistanceinthefield.
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