Reproductive behavior of Hypolestes trinitatis (Gundlach) in Cuba (Zygoptera: Megapodagrionidae)

2009·2.4 MB·English

by  Torres-Cambas, Y

Odonatologica38(3):247-253 SeptemberI,2009
Reproductivebehaviorof
Hypolestes trinitatis (Gundlach) in Cuba
(Zygoptera: Megapodagrionidae)
Y.Torres-Cambas and R.Fonseca-Rodríguez
DepartamentodeBiología,Facultad deCiencias Naturales,Universidad deOriente,
Ave.PatricioLumumba,SantiagodeCuba,Cuba
[email protected]
ReceivedDecember 4,2008 / RevisedandAcceptedMay18,2009
The study wasconductedatthe Dos Bocas streamnrSantiago deCuba,during
Aug.-Sept. 2007(30 d)andin May 2008 (5 d). 33 areterritorial,defendingperch-
ingsitesandreturningtothe sameplaceforseveraldays.Spermtranslocation lasted
about9sandcopulationabout7.3min. Itconsisted of2stages,recognizedfromthe
positionand movementsof3’s abdomen.StageItookca6.6minandisprobablyas-
sociatedwith spermremoval.StageIIlastedabout41.3s,involvingprobablysperm
transfer.Ovipositionlastedforjustover 1h;themaleguardinghismateduringca30
min,whereafterhereturned tohisperch.
INTRODUCTION
Compared withotherinsects,themechanismsofmatinginOdonatahavebeen
relatively wellstudiedbutthe knowledge isconfinedto asmallnumberoftaxa.
Researchonpoorly studiedfamilies is neededifwe are to makegeneralizations
ontheevolutionofreproductive behaviorwithintheorder(CORDOBA-AGUI-
LAR etal.,2003).
ThefamilyMegapodagrionidae is widespread in thetropics, butonlythebiol-
ogyof Heteragrionalienum(GONZALEZ-SORIANO &VERDUGO-GARZA,
1984)andParaphlehia quinta(GONZAlEZ-SORIANO&CORDOBA-AGUI-
LAR, 2003), bothfromMexico, hasbeendescribed.ThegenusHypolestes is the
unique representative ofthefamilyintheWestIndies.Ithastwospecies: H. clara
fromJamaicaandHaiti,andH. trinitatisfromCubaandHispaniola, whichdif-
ferin penis morphology (WESTFALL&MAY, 1996). Accordingto DUNKLE
(1991) mostHypolestes collectedinHispaniola havepenises differentfromthose
248 Y.Torres-Cambas&R.Fonseca-Rodriguez
ofCuba(H. trinitatis)andJamaica(H. clara);consequently, a thirdtaxon might
in thefutureberecognized as either athirdspecies orasubspecies ofH. trinita-
tis.DUNKLE(1991)suggests thatbehavioralandmolecularstudiesare needed
to solve these taxonomicalproblems. Thework describedhereis afirst step in
this direction.
H. trinitatisinhabitsrivers and streams atthe mountainsof the centraland
eastern Cuba (ALAYO, 1968; TRAPERO-QUINTANA & NARANJO, 2003).
Littleisknownonthebiology ofthis genus.Theaimofthispaperisto describe
thereproductive behaviorof H. trinitatisinCuba.
STUDY SITEANDMETHODS
Thestudywascarriedoutina streamatDosBocas, 12km N ofSantiagodeCuba,atapproxi-
mately200 ma.s.l.Thestreambedwidthvariesfrom 5to 10m,with abundant stonesandsand. The
riparianvegetationconsistsontreesabout15mhigh,grassesofthegenus CyperusL. andbushesof
Citrussinensis(L.)andC. nobilisAndrews,aswellascoffeetrees(CoffeaarabigaL.).OtherOdonata
speciesobservedwereProtoneura capillaris(Rambur),Neoneura maria(Scudder),Enallagmacoecum
(Hagen), Telebasis dominicana (Selys), Scapaneafrontalis (Burmeister),Dythemis rufinervis(Bur-
meister),Macrothemisceleno(SelysinSagra),Progomphusinteger(Hagen)andAphyllacaraiba(Selys).
Theareawasvisiteddailyfrom8August until 1 September 2007 (exceptdays 11; 16;17;19;29
and 30),and every two daysfrom 1 to26 September(except days2 and 16).A transectof355 m
alongthestreamedgewasselectedforthestudy, anddivided in71 5-msections. Behavioral observa-
tionswerecarriedoutfrom09:00to 15:00 h.(summertime),totalling180hours.Duringthisperiod,
the transectwassurveyedtwiceand thetypesofactivity(perching,copulation,oviposition), aswell
asthepositionofthe insects occupiedinthe transectwhen firstspottedinthe daywererecorded.
Additionally,inMayandJune 2008thereproductivebehavior wasrecorded withavideocamera.
Wemarked 146 H.trinitatisindividuals,44 femalesand 102males,usingablack inkwaterproof
marker(StaedtlerLumocolorF).Eachdamselflywasmarkedwithauniquenumberonitsrighthind-
wingand thenreleased atthesiteofcapture.Datacollected in2007and2008wereused todetermine
themeanduration ofpre-copulatory, copulatoryandpost-copulatoryevents.
RESULTS
MALE TERRITORIALITY
Themalesperch on marginalvegetation, on stones, or on drybranchesover-
hanging the stream and always in areas with rapids. Confrontations were ob-
servedamong H. trinitatis males,and between H. trinitatis, Scapaneafrontalis,
Macrothemiscelenoand Enallagma coecum males.Theaggressivebehaviortook
place whenevertheintruderflewinfrontof, orabove,themale’sperch,andcon-
sisted ofchasing them amaximumoffivemeters away, andreturning immedi-
ately to thesame perch.
Perching sitefidelity was high:60%ofmaleswereobserved at leasttwo days
inthe samesection ofthehabitat(Fig. 1).Themostfaithfulmalewas observed
atthesameperchoneachofthe20observationsbetween 12August and18 Sep-
tember2007.
Reproductivebehavior ofHypolestes trinitatis 249
COPULATION
Malesseizedfemaleswithoutprevious courtship as theyflewneartheirperch,
and settledon the riparian vegetation. Subsequently, spermtranslocationtook
place, thewholeprocess lasting9±0.14s(mean ± standarderror)(N =5).
Copulation lasted7.3±0.53min(N= 17)andfromtheposition andmovements
of themale’sabdomen, wedistinguishedtwostages. InstageI,themalemaintains
thefirstandsecondsegmentsparallel tothefemale’sninthandtenth.Hethenflexes
thethirdsegmentdorsallyinthearticulationwiththesecond, whilethefourth,fifth
andsixth segmentsremainaligned withthethird.Themalebendstheremaining
segmentsventrally
to restrain the fe-
male by her pro-
thorax(Fig. 2a).
Inthis position,
the first and sec-
ond abdominal
segments of the
male contact the
three distal seg-
ments of the fe-
male and later
separate to a dis-
tance of 1.0to 1.5
mm,due to move- Fig. 1.Frequencyofmalesobserved in thesamesection ofthehabitat
ments caused by during30days(8Aug.-26Sept.2007)atDosBocas stream,NEofSan-
both insects. This tiagodeCuba.The markedfive-metersectionsalongthestreamarecon-
sequence was re- sidered assectionsofthehabitat. An individual re-sighteditimes inthe
peated witha fre- samesection ofthe habitatwasi+1 timesobservedin thissection.
quencyof 18.3 ±0.51 min'1 (N =8),causing inand outmovements ofthe penis
inthevagina.Thisstagehadadurationof6.6±0.69min(N = 13).Inthesecond
stagethedescribedmovements ceaseandthemaleadopts anewpositionwithhis
abdomen.Heformsanobtuseangle betweenthethirdand fourthsegmentwith
the vertex directed ventrally. Themovements inthis stageconsistof flexing the
abdomendorsally inthe articulationbetweensegmentstwoandthreetoreturn
laterto theinitialposition. Thissequencewas repeated 6 to42times(N =5)and
thestagelasted41.3±6.44 s(N = 15)(Figs 2b, 3).
OVIPOSITION
Ovipositionoccurred betweenone andfivemetersfromthesiteofmatingand
always in areas offlowing water. Thesubstrataused by femalesforoviposition
250 Y.Torres-Cambas &R. Fonseca-Rodriguez
were submerged petioles andlimbsofleavesof Cyperus sp., drybranches fallen
onthewater orrootsofterrestrialplants thathang intothewater. Whenthetan-
dem settleson astone insidethe stream, the femaletouches differentplaces of
the surface, several times, withthe terminalabdominalsegments.Thisbehavior
couldbeassumedas away of checking whetherthesubstrata isappropriate for
layingeggs.
Oviposition lasted67 ± 3.95min(N = 4), withthemaleguarding the female
for32.3 ± 3.39 min(N =6),beforereturning to hisperch. Theshortest periods
of guarding was observedinamalethatcopulated three times in one hour 45
minutes:10.9min, 4.7minand 3.4min. Thelasttwo matings occurred withfe-
malesthatwere ovipositing ata distancelessthan50 cm fromtheperch.
In 2007, 12 couples were detectedin copula and 32 ovipositing. A 91% of
copulations and 100%of ovipositions detectedwere observed forthe first time
between 11;00and 15:00h(Fig. 4).
Fig. 2. Position adoptedby acoupleofHypolestestrinitatisduringmating:(a)stageI,the male’s
abdominal segments3to6remain aligned;- (b)StageII,thesegments3 and4formanobtusean-
gle.
Reproductivebehavior ofHypolestes trinitatis 251
DISCUSSION
COMPARISONWITHREPRODUCTIVEBEHAVIOROFOTHERZYGOPTERA
Territorialbehavior has been described in some otherMegapodagrionidae
species. For example, Paraphlebia quinta fromLos Tuxtlas, Mexico hastwomale
morphs, onelarge withdark wings andterritorialbehavior, andtheothersmall-
er withhialinewings and no territorialbehavior(GONZALEZ-SORIANO &
CORDOBA-AGUILAR, 2003). Territorialmalesare faithfulto theirperching
sitesanddefendthemfromallotherconspecific males. Territorialbehaviorhas
alsobeen reported in Heteragrion alienumandH. albifrons (GONZALEZ-SO-
RIANO& VERDUGO-GARZA, 1984; GONZALEZ-SORIANO, 1997).
ThemalesofHypolestes trinitatisdefendperching sites unlikesomespecies such
asPalaemnemadesiderata(Platystictidae;GONZALEZ-SORIANOetal., 1982),
Coramarina(Polythoridae; GONZALEZ-SORIANO& VERDUGO-GARZA,
1984) or Perithemismooma (Libellulidae; DE MARCO & RESENDE, 2004)
thatdefendtheoviposition site.Apparently, inHypolestes trinitatis,theterritory
provides anadvantageous position fromwhichmalescouldinterceptfemalesfor
mating. Similarargumentshavebeenusedto explain Heteragrion alienumterri-
torialbehavior(GONZALEZ-SORIANO& VERDUGO-GARZA, 1984).
Two stages of the copulatory process
have also been distinguished in P. quin-
ta, although the abdominal movements
are differentfrom those of H. trinitatis
(GONZALEZ-SORIANO & CORDO-
BA-AGUILAR, 2003). During the first
stage, P. quinta malescarry out aseriesof
abdominalelevationmovements(pumping
movements) ratherthan the flexing move-
ments described for H. trinitatisin this
paper.
Like H. trinitatis, the males of Hetera-
grionalienum guard their females in tan-
dem during oviposition, while in P. quin-
ta the guarding occurs without contact
(GONZALEZ-SORIANO & VERDU-
GO-GARZA, 1984;GONZALEZ-SORI- Fig. 3.StageIIin Hypolestestrinitatismat-
ANO& CORDOBA-AGUILAR, 2003). ing.Movements inthisstageconsistin flex-
The abilityof the males to remove the ingtheabdomen dorsallyinarticulation of
spermstoredby the femalefrom previous segments2and 3and subsequentlyreturn-
ingtotheinitial position (withcontinuous
matings is a widespread phenomenon in lines).Thepositionadoptedaftertheflexion
Odonata(CORDOBA-AGUILAR et al., isrepresentedwithdashedlines.
252 Y.Torres-Cambas &R. Fonseca-Rodriguez
2003). The first stage of mat-
ing isassociated withspermre-
moval, and theremaining ones
withinsemination(MILLER&
MILLER, 1981;CORDERO&
MILLER, 1992). The kind of
abdominalmovements thatoc-
cur during stageIof H. trinita-
tis mating and the presenceof
four distal projections covered
withspinesinthepenis(unpub-
lished data),suggest thatsperm
removaltakes place in thisspe- Fig. 4.Dailyreproductiveactivityin Hypolestestrinitatis
cies. atDos Bocasstream,SantiagodeCuba.Data weretaken
over30days(8August- 26September2007).
POST-COPULATORYGUARDING
Post-copulatory guarding presumably prevents the femalesfrommating with
othermales. Thus thelast maleto copulate with a given femaleis the one that
fertilizestheeggs(FINCKE, 1984;CORDERO & MILLER, 1992). Despite the
benefits, thetimeinvestedinthepost-copulatory guardinglimitsthemaletoob-
tainnew matings, andifamaleis territorial,compromises histerritory defense
(ALCOCK, 1982, 1994).Oviposition is prolonged in H. trinitatisand involves
contact guarding. During thisprocess the malecannot respond toothermating
opportunities unlessheabandonsthefemale.Intheory, leaving afemalebefore
shefinishesoviposition couldbeawayof minimizing thecostsofguarding. Our
results showthemalethatspenttheleasttimeintandemwithhismatewas infact
themostefficientinobtaining matings(three matingsin 1;45 h,guarded 10.9min,
4.7minand3.4min). However,thisis a unique case and moreobservationsare
neededto confirmthis hypothesis. Anotherhypothesis isthatthefemale’srecep-
tivitycoulddiminishwiththeadvanceofoviposition; oncethemalehasensured
hispaternityoversomeeggs,thiswouldreducepossible lossoffitnessshouldshe
remate (ALCOCK, 1992).
ACKNOWLEDGEMENTS
Wethank ADOLFOCORDERORIVERA, who revisedthe firstversionofthemanuscript and
providedsomeliterature.N1LIACUELLARARAUJOadvisedusontheEnglishgrammar.Wethank
alsoRODOLFO NOVELOGUTIERREZand JOHNA.ALLENfortheirvalublecomments.
ReproductivebehaviorofHypoleslestrinitatis 253
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