Reproductive behavior of Enallagma coecum (Hagen) in Cuba (Zygoptera: Coenagrionidae)

2009·1.3 MB·English

by  Trapero-Quintana, A

Odonatohgica38(1): 7-13 March I.2009
Reproductive behavior
ofEnallagma coecum(Hagen) inCuba
(Zygoptera: Coenagrionidae)
A.Trapero-Quintana*,A.Cabrera+Anaya,Y.Torres+Cambas
& L. Rodríguez+Montelier
DepartamentodeBiología,Universidad deOriente,PatricioLumumba s/n,
CU-90500 SantiagodeCuba,Cuba
ReceivedJuly20, 2008/Revised andAcceptedDecember 4,2008
Thereproductivebehavior isdescribedfrom2populationsontheoutskirtsofSan-
tiagodeCuba,between June 2005and May 2006. 33 startedarrivingatthewater
body in themorningnearly2h before 99.Spermtranslocation wasbrief(lessthan
30s),and thedurationofcopulationaveragedabout 18min. Duringovipositionthe
9 was guardedintandem bythe 3,except when shesubmergedunderwater, when
non-contact guardingwasobserved.Themeanduration ofovipositionwasabout 10
min. Abioticfactorsthatinterfered withthereproductionwerewind,absenceofsun,
and rain;and thebiotic interactions included conspecific33,spiders ofthegenus
Dolomedes,Gambusia punctatafishesandthe lizardAnolissagrei.
INTRODUCTION
Theodonateshaveacomplex reproduction (CORBET, 1999),andthisaspect
oftheirbiology hasbeenespecially wellstudiedinthetemperatezones(NOVE-
LO& GONZALEZ, 1984).ThegenusEnallagma constitutesapproximately 40
species (MAY, 2002), fourofwhichare foundinCuba. Of these, E. coecum has
the largest areaof distribution, and is characteristicof slow-moving and tree-
linedrivers andstreams.Thespeciesalso occurs in Jamaica, LaEspanola, Puerto
Rico, theLesserAntilles(ALAYO, 1968),and FloridaandAlabamaintheUSA
(WESTFALL & MAY, 1996).
*Correspondingauthor:[email protected],[email protected]
8 A.Trapero-Quintanaetal.
MATERIALANDMETHODS
Thestudywascarriedoutattwo sitesbetween June 2005 andMay 2006, Onesite isa streamat
“LosGomez”farm,locatedNorth ofSantiagodeCuba between75°49’ 18”Nand20°02’52”W,and
at 90masl.Thesecond site is onthe Sevilla river,located East ofthe citybetween 75°45’56”N and
20°00’54”W and atanaltitude of62 masl.Theobservations(total:176hours)weremadedailybe-
tween08:00a.m.and 16:00a.m.Thefirstsiteisanopenstream50cmindepthwithamuddybottom.
Herbaceous vegetationwith CyperusrotundasL.predominatesandthedominantaquaticvegetation
consistsofthe shrubsDichrostachyssinerea (L.)Wight,Arn.CabombapiauchiensisL.and Hydro-
cotyleumbellata L.TheSevillariveris20cmdeep,itsbottomiscomposedofrocksand sand,andit
ispartiallycovered with largesizetrees such asSterculia apetala(Jacq.)Karst.,besides herbaceous
vegetationwith C.rotundas and H.umbellata. Watertemperaturein bothsitesoscillatedbetween 23-
28°C.
Theduration ofthereproductiveprocesseswasregisteredwithadigital63-1126 chronometer and
the temperaturewithadrybulb thermometer.
OtherOdonataspeciesseenintheareawere:Enallagmacivile(Hagen),Ischnuracapreolus(Hagen),
I. ramburii (Selys), Telebasis dominicana (Selys),Neoneura maria(Scudder), Coryphaeschnaadnexa
(Hagen),AphyllacaraibaSelys,Cannaphilainsularis (Kirby), Crocothemisservilia(Drury), Dythemis
rufinervis(Burmeister),Erythemisplebeja(Burmeister),E. simplicicollis(Say),Erythrodiplaxjustiniana
(Selys),E.umbrata(L.),Macrothemisceleno(Selys), Miathyriamarcella (Selys),Micrathyriaaequalis
(Hagen),Orthemis discolor(Burmeister),O.ferruginea(Fabricius),Pantalaflavescens(Fabricius) and
Perithemis domitia(Drury).
RESULTS
DAILY ACTIVITY
Thefirst malestoarriveweredetectedat08:15a.m.,perching closeto thewa-
terandflying amongthe vegetation. Thiscombinedactivitywas maintainedun-
til09:50a.m.During flight somemalesmaintainedtheabdomenslightly curved
downwardswithsegmentseightandnineslightly expanded. Confrontationswere
observed witha durationof6 ± 1.6s (4.3-9.0s, N = 16),among 11 nonspecific
males andamongE. coecum and fiveIschnuracapreolus. Theseinteractions in-
volved short flights inaposition always inferiorto theintruderuntil thelatter
hadmovedfor atleast40cm fromtheperching site.
REPRODUCTIVEBEHAVIOR
Arrivaloffemalesbegan atabout 10:00a.m.Whenamaledetectedafemalehe
grabbed herwithitslegs to formaprecopulatory tandemwithoutany apparent
preceding courtship. Inbothlocationsthe suddenrupture of the precopulatory
tandemwas observedon fiveoccasions, possibly dueto nonreceptive behavior
bythefemales.Sperm translocationoccurred onherbaceousvegetation exposed
to thesunandhadanaveragedurationof22 ± 13s(14-50s,N = 7).During this
event,themale’sabdominalsegments4-6formedanangleof90°(Fig. 1).Ontwo
occasions, duringprecopulatory tandemandbeforetranslocation,thefemalewas
Reproductivebehavior in Enallagmacaecum 9
observedswingingherabdomenandmakingcontact withthesecondary genita-
liaofthemalefor oneor two seconds(cf.“genital touching” of ROBERTSON
& TENNESSEN, 1984).
Copulation occurred immediatelyaftertranslocation.Itwas observedbetween
10.00a.mand04.00p.m.andhadanaveragedurationof 18± 10min(2-32 min,
N =23). Whileinprecopulatory tandemthe femalebegan aseriesof waveswith
Figs 1-5.ReproductivebehaviourinEnallagmacoecum:(1)spermtranslocation;—(2)stageIofcop-
ulation; —(3)stageIIofcopulation; - (4)oviposition; — (5)aggregationsforoviposition.
10 A.Trapero-Quintanaetal.
herabdomenuntilmakingcontact withthesecondary genitalia ofthemale.The
male’sabdomenformedanarc (Fig.2)thatcorresponds toStage Iofcopulation,
during whichspermremoval fromthebursaand/orspermatheca frompreceding
copulas probably occurs. Thisfirststagehadanaveragedurationof 14± 5.1 min,
andthetransferenceofspermpresumably began shortly afterwards, withanav-
eragedurationof7 ± 1.6min(4-9 min,N =9)(Fig. 3). Attheendofthisstage,
the malearchedhis abdomenas in Stage I.Thecouple remainedintandemfor
afew minutes, usually in theplace wherethey hadcopulated, beforeheading to
the water to oviposit.
Oviposition underwater tookplace in tandemandlastedon averageof 10 ±
8,7 min(3-40 min, N =39). Thesubstrata were theplants of H. umbellataand
C.piauchiensis (Fig. 4),wheresomefemales(N =7)submerged underthewater
forup to 12 min.Thetandemseparated when thewater reached themale’stho-
rax andthemaleflewto abranchcloseto theimmersionsite,recapturing the fe-
malewhensheleftthewater.Remaining ovipositionswere inC.piauchiensis and
roots ofC.rotundus,wherenoimmersionwasobserved.Communalovipositions
ofa durationof 17min(Fig. 5)involving upto fivecouples wereobserved(8-26
min, N - 5).
According to the classification of WAAGE (1984) on the variation in the
postcopulatory behaviorinodonates, E. coecum is classifiedas categoryA“ovi-
position intandem”withtheexception insomecases ofasecondary behaviorof
solitary submerged oviposition. Afteroviposition somecouples (N = 4) stayed
intandemforapproximately 90minuteswithoutapparentsexualintercourse, far
fromthewater andamongthevegetation. Majorreproductive activity inE. cae-
cum is concentratedinhoursaroundnoon(Fig. 6).
Someclimatic factors seemed to interferein the reproduction of E. caecum,
amongthemwind,whichcouldresultintheseparationofthetandem.Partialor
totalabsenceof sunmadethedamselfliesinactive, andraincausedthemtoaban-
Fig.6,CopulafrequencyanddailyovipositioninEnallagmacoecum.
Reproductivebehavior inEnallagmacaecum 11
donmating altogether. Biotic factors such as competition of nonspecific males
forthefemales(N= 11)orheterospecific interactions(N = 10),lastedonlya few
seconds, butwereobservedto slowdownthesequenceofreproductive behaviour.
Thefish, GambusiapunctataPoey,wasobserved(N = 7)tobiteoffthedistalpart
ofthe abdomenduring a spawn, andalso to jump out ofthewater to eat indi-
vidualsincopula or in tandemnearthe water. Spiders ofthe genusDolomedes
wereobservedfeeding onfemales(N =5)thatwereincopula previously, and 12
deadspecimens ofthis speciesandofTelebasis dominicanumwere foundintheir
webs.Alizard, the CubanBrownAnole, Anolissagrei (Dumeril& Bibron), was
alsoobserved (N = 8)feeding onindividualsincopulation.
DISCUSSION
Themeandurationofspermatictranslocationin E. coecum(22 ±13 s) islong
compared withthatknown forotherspecies inthegenus.InE. civileitlasts 16s
(BICK&BICK, 1965),in E. aspersum17.8 sandinE. exsulans25.2 s(BICK&
HORNUFF,1966)(Tab. I). Copulation inE. caecum hasanaveragedurationof
18minwhichissimilartothoseofE. civile(18.7 min)(BICK &BICK, 1965),E.
aspersum(13.5min)(BICK& HORNUFF, 1966),E. hageni(22.4 min),butdif-
ferentfromE.exsulans(75.8 min),andotherspecies intheCoenagrionidae (Tab.
I). Prolonged reproductive events in E. caecum couldreducethe chancesofthe
femalemating withothermales.
Stages I and II ofcopula couldbe related to sperm removal fromprevious
copulaandinsemination, respectively, as ithasbeendemonstratedforotherspe-
ciesofthegenus.For example, inE. cyathigerumremovalofspermwas observed
during thefirstpartofcopula, whilethelast 200 swere destinedto insemination
(MILLER& MILLER, 1981).InE. hagenithemalecouldeliminate87%ofthe
storedspermfromthespermatic bag (FINCKE, 1984).
TableI
Duration ofsperm translocation (inseconds) andcopulation(inminutes)in speciesofthe genera
EnallagmaandIschnura
SSppeecciieess RReepprroodduuccttiivveepprroocceessss RReeffeerreennccee
SSppeerrmmttrraannssllooccaattiioonn CCooppuullaattiioonn
EEnnaallllaaggmmaaccooeeccuumm 2222 1188 TThhiiss ssttuuddyy
EE..aassppeerrssuumm 1177..88 1133..55 BBIICCKK&& HHOORRNNUUFFFF,, 11996666
EE..cciivviillee 1166 1188,,77 BBIICCKK&& BBIICCKK,, 11996655
EE.. eexxssuullaannss 2255..22 7755..88 BBIICCKK&& HHOORRNNUUFFFF,, 11996666
EE..hhaaggeennii 2222..44 FFIINNCCKKEE,, 11998822aa
IIsscchhnnuurmaddeennttiiccoolllliiss 3322 CCOORRDDOOBBAA,, 11999922
II..eelleeggaannss 332244 MMIILLLLEERR,,11998877
II..ggrraaeellllssiiii 7744 CCOORRDDEERROO,, 11998899
II..rraammbbuurriiii 220022 RROOBBEERRTTSSOONN,, 11998855
12 A.Trapero-Quintanaetal.
As in E. coecum, E. hageni females submerge to oviposit; oviposition in the
latter species always takes place underwater,with themaleremaining closefor
safekeeping (FINCKE, 1982b, 1984). Submergence couldbe hazardous for fe-
males, foron occasions they have been known to die(FINCKE, 1984),butit
has theadvantage ofreducing thechancesoftheeggs desiccatingas aresultofa
lowering of thewaterlevel(FINCKE, 1984)andavoidsinterferencewithmales
(FINCKE, 1984;WAAGE, 1984). Conspecific maleswere observedin the area
wherethefemaleswere submerged.
Thetendency toformcongregations during oviposition hasbeennotedinvari-
ous species ofthesuborder, andsomeauthors suggestthatthisbehaviorreduces
the risk ofpredation by amphibians (REFIFELDT, 1990). In thepresent study
the observed congregations mightreducethe risk ofpredation by Anolissagrei
lizards (MACMILLAN, 2000). Theconcentrationof the reproductive activity
toward hoursof themidday apparently related to airtemperature,as hasbeen
foundin Protoneuracapillaris(Rambur) intheformofapositive correlationbe-
tween temperatureandoviposition frequency (TRAPERO etal.,2005).
ACKNOWLEDGEMENTS
WethankNIL1ACUELLARARAUJO,BERNARDOREYESTURandBEATRIZGONZALEZ
(UniversidaddeOriente,Cuba)fortheir helpduringthis investigation. Wealso thank ENRIQUE
GONZALEZ-SORIANO(InstitutedeBiologia,DepartamentodeZoologia,Universidad Nacional
Autonoma deMexico),RODOLFONOVELOGUTIERREZ(InstitutedeEcologia,Xalapa,Mex-
ico) and ADOLFOCORDERO(Departamentode Ecoloxia eBioloxia Animal,Universidade de
Vigo,Espana)fortheirsupportwith literature andadvice, and NATALIAVONELLENRIEDER
(IBiGeo,Universidad Nacional deSalta,Argentina),JOHNA.ALLEN(UniversityofSouthamp-
ton,UK) forthe criticalreview ofthemanuscript.
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