Table Of ContentOdonatologica39(2):141-148 JuneI.2010
SHORTCOMMUNICATIONS
Theprocess of moultingduringfinal emergence
of the dragonflyPantala flavescens(Fabricius)
(Anisoptera: Libellulidae)
R.J.AndrewandN.Patankar
DepartmentofZoology,HislopCollege,Civillines,Nagpur-440001,India
[email protected]
ReceivedAugust6,2009/ RevisedandAcceptedFebruary1,2010
ThechainofeventsoccurringduringemergenceinP.flavescensisdescribedinde-
tail.The moultingprocessisdividedinto 3stages.Thelarvaclimbs outofthewater
afew hoursaftersunset.Ifdisturbedwhile climbing,itexhibits thanatosis i.e.death
feigningandcrab-likeside-wayscrawling.Itstopsatasuitable verticalemergentsup-
port.Manipulationfromverticaltohorizontal ofthissupportstopscommencementof
ecdysis. —StageIstartsfromthemomentthelarvafinds asuitable site formoulting.
Soon,itstartsshuddering,quiveringandshakingitsbodyinasynchronizedpattern.
Theimagoinsidetheexuviae exertspressure onthethoracictergitesuntilthecuticle
splits.This stagevariesfrom8to20min and occupies 16%ofthemoultingperiod.
— DuringstageII,thehead and thoraxoftheimagoemergeoutofthe splitthorac-
iccuticle. Theimagoexhibits anantero-posteriorhumpingmovement andthebody
hangsoutdownwards with folded legs.Thehalf suspended,upturnedimagostarts
‘breathing’heavily. Unfoldingofthelegsand movementsofthepackedwingstakes
placeinacharacteristicmanner.Theimagoturnsupwards,gripstheheadoftheexu-
viaeandjerksouttheremainingterminal portionoftheabdomen fromtheexuviae.
This stagetakes 18to35min and occupies 31%ofthemoultingtime.Pigmentation
oftheheadregioniscompletedduringthis stage. — InstageIII,theimagoisreleased
fromtheexuviae,it startshardeningitscuticle and extendingthewings.Theimago
movesafewinchesabovetheexuviae.Theabdomenispalegreenandcurvedupwards.
Thewingsexpandbut areopaque.Simultaneously,pigmentationofthebody starts
aroundthe thoracicregionandthe terminal tip ofthe abdomen.Within 10-14min
the wholebody ofthe imagodevelopsaspecies-specificteneral patternofcoloura-
tion.Meanwhile,theexpandingwingsunfold and separateout andtheteneraladult
isreadyforflight.Thisstagetakes 40-55minand occupies53%ofthetotalmoulting
period.Observationsonincompletemetamorphosisindicate thatgravitationalforce
isresponsibleforuniformwingexpansion.
142 R.J.Andrew &N.Patankar
INTRODUCTION
Moultingduring finalemergence,or finalmetamorphosis, is oneofthe most
spectacular eventsinthelifehistoryofa dragonfly(MILLER, 1995).Thisprocess
hasbeenobserved anddiscussedbyvariousworkers(TILLYARD. 1917;COR-
BET. 1951; PAJUNEN. 1962; TROTTIER. 1966; BULIMAR, 1971). Moult-
ing isa highlycomplexprocess inwhichmanydifferenttypesofrhythmic move-
ments participate.
CORBET (1999) notedthatitwas noteasy to determinestage IandstageIV
of metamorphosis in Odonata.Thelarvaeofmanyspecies leavethewater part-
ly or wholly andintermittently, days or even weeks beforeemergenceand it is
noteasyto timestageIVinOdonatabecause variousextrinsic factorslikedawn,
twilight andtemperatureandevenendothermicwarmingcontrolthefirstflight,
whichconcludesstageIV.
MATERIALANDMETHODS
ThecityofNagpur(21°10’N/79°12’E)liesatthesouthernfringeoftheSatpudamountainrange
incentral India. Itislocatedonanundulatingplateauwithaltituderangingbetween 274-305mabove
meansealevel. The collection sitewasa 15m longstretch ofa 120mlongopen cementdrain run-
ninginawest-eastdirection. Ithasawidthof34inchesandadepthof32inches. Depthofwaterof
about5inchesaccumulatesatthebottomduetothepresenceofasinglebrick layerplacedacrossthe
floorofthedrain. Thedrain islocated atthe largegrass coveredplaygroundsurrounded by shrubs
and fewtrees oftheSt John’s Schoolinthe centreofthecity.
MatureF-0larvaewerecollected fromthissite andkeptinbucketsandplasticcontainers,partially
filledwith thewaterfromwhere theywerecollected. Woodensticks, twigsandbranches wereplaced
inthecontainersasemergencesupports.Naturalconditionsweremaintainedbykeepingthecontain-
ersinaveranda,nearlargeopenwindows.With thehelpofanaim-n-shoot 35mm Yashicacamera
(model:EZX-105,38/105mm)thevarious stagesoftheprocess ofmoultingduringfinal metamor-
phosiswerephotographed.
Allthemovementsofthelarva/emergingpharateweredocumented andaNokia 1100cellphone’s
stopwatchwasusedtorecordthetime(oneofthemajormeritofusingthiscell phonewastheinbuilt
tinycooltorchwhich was ofgreathelpduringtherecording ofobservations inthedark).
RESULTS
Thefollowing documentationis ofone complete sessionof moulting during
the finalemergenceof Pantalaflavescens, which was observed onthe nightof
15th April2004.
Thelarvarestedwithitsheadandthoraxoutofwater sinceearlyevening(6:25
pm.).At 11:10pm,itmovedoutofthewaterandclimbed13inches, stopping at
asuitableemergent support(driedbranches, stick).
Stage I(Figs 1-2). — Afterarest of96 seconds, thelarva startedjerking
its head sideways ’leftand rightT9 times. Then it pushed theheadand thorax
Moultingduringfinalemergence ofPimtalaflavescens 143
upwards seven timeswithlegs spread and theposterior region ofthe abdomen
firmly pressed against the base. Thelarva moved the head sideways twiceand
curvedup theabdominaltip once. Itreset thegripof its legs and pushed upthe
headandthoraxbuttheabdomenlay pressed against thebase.Theheadmoved
sideways eight times, slowly rising withevery move(as iftaking a deep breath).
Itre-grippedandrepositioned itslegs andslightly elevatedthethorax.Thefore-
legs startedtwitching, while thehindlegs re-positioned themselves.Theforelegs
startedquivering without losingtheirgrip. At this stage, theterminalendof the
abdomenwas firmlypressed against the base. Thehead liftedandthe forelegs
displayed clawingmovements whichstopped aftereight seconds. Theheadand
thoraxjerked up anddown 14 times.Theright wing pad elevatedslightly insix
tinyjerksbut returnedto itsoriginal position. A darksplitappeared inbetween
thewingpads. Thisstageconcludedat 11:35pm.
Figs 1-9.Pantalaflavescens,final metamorphosis:(1-2)stage I; —(3-6)stageII; — (7-9)stage III.
144 RJ. Andrew&N.Patankar
Stage II(Figs 3-6). — Thelarvaremainsmotionlessbuttherightwingbuds
exhibitedslight lateralmovement whichstopped after 28secondsandthe larva
againbecamemotionless.
At 11:40pmthe wingbuds rose while the thoraxlifted.Theheadand thorax
of the adult emerged out of the split. Initially, the thorax emerged, followed
by the head.It didnot wrigglebutmoved upand down.By 11:45pmthe head
andthoraxhung outandjerked once. Theabdomenoftheadultlay trapped in
theexuviaeof thelarva. Thelegs, whichwere foldedagainst the thorax, started
twitchingbutina foldedposition. Thebody ofthe adulthanging outexpanded
andrelaxed as if ’breathing1 heavily. Itstarted an antero-posterior conspicuous
’humping1movement,tryingto loosenitsskin fromthelarvalexuviae. Thebody
ofthe pharate was filledwithhaemolymph andappeared green.Thelegs were
stillfoldedagainst thethoraxbutnowthey startedmoving. Thefirst pair oflegs
was foldedbut startedto jerk at the tibia-femurjoint. Thejointmoved upand
downalong theneckregion. Thefoldedlegs startedjerking atarate of2-3jerks
persecond. Thesecondpair of legs unfolded(just theangle offemurandtibia
increasedfrom10 to 40degrees aroundthe neck). The 1stand2ndpairs oflegs
startedtwitching. Thetwitching intensity ofthe 1stpair oflegs was muchhigh-
er then the2ndpair. Thehindwing pads,which initially lay parallel to the body,
now hung outwards anddownwardsperpendicular to the abdomen.The fore-
wings layparallel andcloseto theabdomen.Thepharateturnedupward, gripped
theheadoftheexuviae andatthesametimepulled outthe abdominaltip from
theexuviae, endingstage IIofmetamorphosis at 12:06am.
Stage III(Figs 7-9). — Thepharate gripped the headofthe exuviaewith
the 1stand2ndpair oflegs. The2nd pair grippedfirmly butthe 1stpair triedto
getabetterholdbyre-grippingthehead.The3rdpair oflegshungdownwithout
touchingany substrate.Theabdomenandwings startedtostretch. By 12:18 am,
the opaquewhitewingswere completely stretchedbut still stuckto each other,
whiletheabdomenwas still curvedbutby 12:24am,theabdomenwascompletely
elongated, straight andstartedto sclerotize.Simultaneously, thewingsstretched
out completely andbecametransparent. Pigmentation of thebody startedfrom
thethoraxandtheterminaltip
TableI oftheabdomen(theheadwas
Pantalaflavescens:theduration(minutes)ofthethreestages alreadypigmented by theend
ofthefinal metamorphosisin threeobserved moultings ofstageII).Theteneralmoved
2.5inches above the exuviae.
Specimen StageI StageII StageIII Total
Afterforty minutessinceturn-
1 12 18 42 72 ingupward, by 12:36am,the
2 20 25 55 100 wings became unstuck from
3 08 37 40 85
eachother, separatedandnow
Average% 16% 31% 53% 100%
lay perpendicular tothebody.
Moultingduringfinal emergence ofPantalaflavescens 145
Theabdomenbecamecompletely sclerotizedandwas colouredwithitsspecies-
-specificpattern. Thisendedstage IIIof metamorphosis.
Thetimedurationofthe threestagesforthreeobservedfinalecdysis is illus-
tratedin Table1.
THANATOSIS
One larva was resting on the outer surface ofthe bucket, we caught it and
placed it horizontallyon therim so thatthebody was parallel to theground. It
stiffenedandstraightenedallthreepairsoflegsalongthesideofits abdomenand
dropped outsideontheground. For morethen 15 seconds, itexhibitedthanato-
sis (acted dead), thendartedquickly upthe sideofthe bucketand, afterclimb-
ing up only three inches, it quickly started the process of eclosionwithinfour
minutes. It was 11:45pm. Themainsurvival valueofthis thanatosisbehaviour
is probably to avoid furtherattack by alarge predator. Theemerging larva of
P.flavescens isprone toattack from landpredatorsand itis only physical stim-
ulithatcan excitethis behavioursincemoulting takesplace indarkness. ARAI
(1987) reported thatthanatosisorrefleximmobilizationcanoccurshortly before
ecdysis andbefore emergence. It is strongly exhibited if the larvais grasped by
thethoraxoutofwater,thusresponding to physical stimuliratherthanvisualas
foundinthe presentstudy.Thehastetomoultalmostimmediately afterexhibit-
ing thanatosisbehaviourin P.flavescens shouldbenotedas asurvivalinstinctas
foundinHemigomphus heteroclitus, whichcompleted ecdysis within 10minutes
beforeanimpending storm(TILLYARD, 1917). At 2:00 am,acompletely scle-
rotized, motionlessadultwas resting onthe exuviae, legs clutching the exuviae
head.
Generally wefindthatthepharate adult,just afterfinalecdysis, is foundafew
inchesaboveits exuviae. Since extra energywas spentbefore moulting(inpre-
tendingthanatosis), itmaybepossible thatnow thepharate has noenergyleftto
moveafewinchesabovethe exuviaeas notedin normalcircumstances.At 6:00
am,wegently carried the bucketout; theadult flewupwards(18-20inches) and
dartedaway towards theEast.
ANGLEOFECDYSIS
Aeshnajuncea cancomplete ecdysis at0 degree(vertical) (MAITLAND, 1967)
whereas Stylurus annulatus canbe forced toemergeat 180 degrees on amesh
net. Orthetrumalbistylum speciosum couldnotdosoat0degree(INOUE, 1964).
HEYMER(1972) foundthata Calopteryx larvatriedto regain its verticalpo-
sitionwhenthe angleof theverticalsubstratewas manipulated. Invertedemer-
gence occurs in Xanthocnemissinclairiand three species of Ischnura (ROWE,
1987;CORBET, 1999) whilehorizontalemergenceis commoninZygoptera and
146 R.J.Andrew&N.Patankar
Gomphidae. Wemanipulated the position ofalarvareadyforecdysis fromver-
tical tohorizontalby placingit onaflatsurfacebutthelarva didnotmoultbut
always re-orienteditself in thevertical position, by darting quickly towards an
erect verticalsubstrate. Ifaphysical obstaclewas kept in itspath, itmovedside-
ways crab-like, withoutchanging the orientationofitsbody. As faras isknown
thisisthefirsttimethatsuchcrab-likeside-ways locomotionofamatureodonate
larva onlandhasbeenreported.
PHARATETRAPPEDATSTAGEII
On 11thApril2004 at 10:40pm, one pharate adultwas foundhanging down
fromits exuviae. Ittried desperately to arch upwards so as to catch the head
oftheexuviaeandreleaseitself,but
could not succeed. It hung down,
legsthrashing, butitcouldonlyturn
uphalf-way andthenfellback toits
hanging position.
Soon, the wings startedexpand-
ing inthehanging positionand90%
ofthe wings spread lengthwise but
pointing downwards.Itstayed inthis
position for morethan 30minutes.
Then it again tried to up-right its
position and, afterfourattempts, it
Fig. 10.Pantalaflavescens:pharatetrappedatstage caught holdof the emergent sup-
II.— Notetheforwardly directedwingsand theun- porttowardsthe leftoftheexuviae
evenstretchingofthe wingsonthe left-compared butcould not proceed furthertore-
totherightside. gain the natural symmetrical posi-
tion.Itheld this positionwiththeabdominaltipstilltrappedintheexuviae. The
wingscontinuedstretchingevenwhiletheimago washeldimmovableinthislop-
sidedposition. Withinten minutes, thewings hardenedand were nowpointing
upwards. The pharate was still struggling toremove its trapped abdominaltip
fromthe exuviaebutcouldnot succeed. Later, at2:00 am,wefoundthepharate
floating on thewater surface withitsabdomenalmost stretchedandtannedand
withitswings pointingforward andexhibiting asymmetrical stretching. A close
examinationofthewingsrevealedthatthe fore-andhindwings oftherightside
hadstretchedmorethanthewings oftheleftside(Fig. 10).
DISCUSSION
EDA(1963) distinguished two typesofpostureduringemergence,theupright
typefoundinmostCoenagrionidae, Gomphidae, Lestidae,Petaluridae, Platycne-
Moultingduringfinal emergence ofPantalaflavescens 147
mididaeandPseudolestidaeand thehanging typereported inAeshnidae,Calop-
terygidae, Coruliidae,Epiophlebiidae, Libellulidaeand sometimesinPetaluridae,
and proposed that thisreflected the larva’staxonomic position. In theupright
type,thelarvacompletes moulting withthe angleof0degreebetweenbody and
exuviaeduring stageII whereasinthe hanging typeas foundin P.flavescens the
angle isbetween 90-130degrees. Theothermajor differenceis in theexpansion
ofthewings, whichinthe uprighttypestartsfromthebasewhereasin thehang-
ing typetheyexpand uniformly.
CORBET (1999)notedthatitwas not easy to determinestageI andstage IV
ofmetamorphosis inOdonata.Thelarvaeofmanyspecies leavethewater partly
orwholly andintermittently,daysor evenweeksbeforeemergence.Theyusually
leavethe water by climbing emergent vegetation or by walking onto the shore
and, whenemergencesupportsare few,someindividualswalkupto 30mto find
anemergencesupport.Thusitisdifficultto measure thetimeofstageIbecause
it is directly dependent upon the distance and/or the presenceof an available
emergence support. The present paperproposes that the timeperiod of stage
Ishould thereforestart from thetimethe larvafinds a suitablespotforecdysis
rather than the timeit leaves thewater. Further it is proposed toend the proc-
ess of metamorphosis in Odonataat stageIIIsince, by theend ofstageIII, the
individualhasattainedall themorphological charactersofapharate adultand
Fig. 11.Proposedstages ofmoultingduringfinalemergence.
148 R.J.Andrew &N. Patankar
alsobecauseit isnot easy to time stageIVinOdonatabecause variousextrinsic
factorslikedawn, twilight, temperatureandevenendothermicwarming control
thefirst flight,whichconcludesstage IV(CORBET, 1999).
Thechanges proposed inthestages demarcatedduring thefinalmoultofOdo-
nataare compared andillustrated in Figure 11.
From thepresentobservationsofforwardly directed, asymmetrical stretching
andspreadingofthewings,itappearsthatgravitationalforceplaysanimportant
roleinuniformwingexpansion of dragonflies adoptingthehanging typeposture
duringemergence.
ACKNOWLEDGEMENT
Partialfinancial support fromthe UniversityGrantsCommission, Pune,Indiaunder theMinor
Research Projectscheme (47-1041/09WRO)isherebyacknowledged.
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