Postcopulatory guarding behaviour in a territorial damselfly, Pseudagrion p. pilidorsum (Brauer), for submerged ovipositing females (Zygoptera: Coenagrionidae)

2005·1.5 MB·English

by  Matsubara, K

Odonatologica34(4):387-396 December I,2005
Postcopulatory guardingbehaviour
ina territorial damselfly,
Pseudagrionp. pilidorsum(Brauer),
for submergedovipositing females
(Zygoptera: Coenagrionidae)
K. Matsubara¹* andNM.Hironaka²
1DepartmentofAppliedBiologicalSciences,Faculty ofAgriculture,SagaUniversity,
Honjo1,Saga,840-8502,Japan
2 DepartmentofBiology,Faculty ofMedicine,HamamatsuUniversitySchool ofMedicine,
Handayama1-20-1,Hamamatsu,Shizuoka,431-3192,Japan
ReceivedSeptember29, 2004/RevisedandAcceptedApril22, 2005
Thepostcopulatorymateguardingbehavioursbyterritorial andnon-territorial 33
forsubmergedovipositing $9wereinvestigatedinthefield.Aftercopulations,9 9in
tandem begantoovipositatthewatersurfaceandthereaftertheyusuallysubmerged
completelyunderwater.The 9 oftenrepeatedthesubmergenceandemergenceatsev-
eraloviposition sites.Whenthe 9submergedcompletely,the 3 released herwithout
submergenceandrested abovethewatersurface duringoviposition(non-submerged
guarding), orthe 3 submergedcompletely and remained intandem,whether only
atfirstorforthe durationoftheoviposition(submergedguarding).Territorial 33
alwaysperformednon-submergedguardingwhen the 9ovipositedinsidetheir ter-
ritories. Thenon-submergedguardinginside theterritorymightallow theterritorial
3bothtoguardtheovipositing 9 andtomaintain histerritory.On theother hand,
when the 9 ovipositedinside another 3’s territories, territorial and non-territorial
33 exhibited bothnon-submergedguardingand submergedguarding.Thus, P.p.
pilidorsum66 mayadopteither submergedguardingornon-submergedguarding
inresponse tochangeintheprobabilityofatakeoveroftheemerged 9byrival 33
insideanother 3’s territory.
INTRODUCTION
Inmany insects, the maleprolongs its relationship with its mate beyond the
timeit takesto transfera sufficientnumberof gametesto fertilizeallofthefe-
*Correspondingauthor:Tel&Fax: [phone];- e-mail:[email protected]
388 K. Matsubara &M.Hironaka
male’seggs(ALCOCK, 1994).Mostprolongedassociationswithmates havede-
veloped to assure paternity underthe conditionthatthelastmaleto inseminate
a femaleis morelikely than previous malesto fertilizetheeggs. Postcopulatory
mate guarding, seen inmany species of dragonflies and damselflies, is one of
themostfamiliarexamplesofhowamalepreventsothermalesfromcopulating
with his partner(WAAGE, 1984;ALCOCK, 1994;CORBET, 1999). In these
species, postcopulatory mate guarding is aparticularly effectivemeans, because
spermremovalordisplacement gives thelast malea fertilization advantage (see
WAAGE, 1984).
Dragonflies and damselflies exhibit two manners of postcopulatory mate
guarding: contact guarding (tandemoviposition), inwhichthemalestays physi-
cally attachedto thefemale(e.g. B1CK&BICK, 1963),andnon-contact guard-
ing. inwhichthemaleremainsnearthefemaleandchasesawayothermales(e.g.
WAAGE, 1973). Although contact guarding offersbettersecurity against take-
over ofhismate(SAKAGAMletah, 1974;WAAGE, 1984),themalemaybeun-
abletomatewithotherfemalesas longas heisattachedtotheovipositing female
(ALCOCK, 1979;UEDA,1979;WAAGE, 1984).On theotherhand,non-contact
guardingallowsthemaleto acquirenewmateswhileguardingtheovipositing fe-
maleandto simultaneously defendhisterritory(ALCOCK, 1979;UEDA, 1979;
SHERMAN,1983;WAAGE, 1984),buttherisk thatthefemalewillre-mate may
begreater(UEDA, 1979;ALCOCK, 1982;CONVEY, 1989).
Submerged oviposition byfemales is foundonly inthe Zygoptera (WAAGE,
1984).Whenafemalecommencessubmerged oviposition, herpartnerguards her
by hovering orperching abovethewatersurface (e.g. Hetaerina vulnerata, AL-
COCK, 1982; Enallagma hageni, FINCKE, 1982).On the otherhand, m some
genera(e.g. Paracercion, ARAI, 1977;Erythromma, WINSLAND, 1983;Lestes,
ANDO,1969;Pseudagrion FURTADO, 1972,MESKIN, 1986, 1989;andXan-
,
thocnemis,CRUMPTON, 1975),theguardingmalesubmergescompletely andin
tandemwiththefemale.However,theadaptive significance ofsubmerged guard-
ing by males hasnot beenfullyanalyzed.
InP.p.pilidorsum, themale formsaterritorynearoviposition sites, andthefe-
malefrequently performs submerged oviposition(AZUMA, 1987;ISHIDA etah,
1988).Inordertoelucidatetheadaptive significance ofsubmerged guarding, we
investigated postcopulatory guarding behavioursby territorialandnon-territorial
malesforsubmerged ovipositing females Wediscuss themating tacticsofterrito-
rialandnon-territorialmalesassociated withpostcopulatory mate guarding.
METHODS
STUDYSITE, —The studywascarriedoutattheupperpartofastreamontheSenbaru campus
oftheUniversityoftheRyukyusinNishihara,thesouthernpart ofOkinawaIsland,Japan(26°14'N,
127°45'E).Atthe studysite,theriverwasabout3rawide and 0,5m deep,andaboveitsbanks stood
agrove ofleucaena Leucaenaleucocephalaand anevergreenforest.Damselflies rarelyappearedat
PostcopulatoryguardinginPseudagrionpilidorsum 389
thestudysiteintheearlymorningorevening,when thewatersurface wasshaded. Thereproductive
behaviourwas observedata 15m lengthoftheriver inthe studysite. Intheobservation area,there
weretwosandysitesontheriverbank,one3mlongand theother 5m.Thesesiteswerecoveredwith
grasses,andsomeofthestemsandrootswereunderwater.Female damselfliesusedtheseunderwater
stemsand rootsasovipositionsubstrates,
OBSERVATIONOFREPRODUCTIVEBEHAVIOUR. - Althoughdamselfliesappearedsuc-
cessivelyatthesitefromearlyApriltolateNovember,theobservationwasconductedintwoperiods,
JulyandSeptember1996,whenmanydamselfliesappeared.Intwodaysbeforeeachobservationpe-
riod,wecollected asmanymaleandfemaledamselflies aspossibleatthe studysite andsurrounding
area, andindividuallymarked them with paintmarkers (MitsubishiPaint MarkerPX-21®)onthe
thorax andabdomen.Furthermore,ifanyunmarked individuals werefoundduringobservationpe-
riod,theyweremarkedandreleased. The behaviourofdamselflies didnotappeartobe affectedby
markingthemonthe thoraxandabdomen. Wecarriedoutcontinuous observation principallyfrom
0900to 1500h,exceptonrainyorovercast days(observationtime: 114hin July,69 hinSeptember).
Weexamined thetimeandlocation inwhichreproductivebehaviours byindividual damselflies were
observed.The time andduration ofthese behaviours weremeasured with theuseofastopwatch.
Intotal,149malesand46females(July: 77malesand31 females;September:72 malesand15fe-
males)wereindividuallydistinguishedbymarking.
TERRITORIALBEHAVIOUR
Territorieswere usuallyestablishedaroundoviposition sitesthatcontainedtwo
orthreelocationsofoviposition substrates, elongated stemsandroots ofgrasses
underwater, andeach territoryalways containedatleastone perch onstems or
leavesofgrassesprotruding 10-15cmabove thewater surface.Territorialmales
defendedagainst intruding conspecific males by the chase display and/or the
elaborateconfrontation-chasedisplay(FURTADO, 1972;MESKIN,1986,1989,
1993).Territorial malesalmost always succeededin defending theirterritories;
intrudersousted defending malesfromtheirownterritoryonly 3times(1.4%) in
220observedinteractions.Territorysize, as definedby thedistanceatwhichthe
ownerreactedto anapproaching male,was quite variable,ranging from 1-4m.
Territorialmaleswere residentat thesameoviposition sitefrom 1-8 days(mean
± SE =2.33 ± 0.43, n=21). Thesocial statusofmalessometimeschanged from
territorialto non-territorialorvice versa.
MATINGBEHAVIOUR
Neitherterritorialnor non-territorialmalescourtedfemales.Whena territo-
rialmalediscoveredafemaleapproaching anoviposition siteinsidehisterritory,
heimmediately grasped thefemalewithhisanalappendages. Thenon-territorial
male, ontheotherhand, usually stayed aroundanothermale’sterritory untila
femaleapproached anoviposition site, whereupon it quickly seizedthe female.
Aftera territorialor non-territorialmale had seizeda female, the couple flew
immediately intandemto a nearby plant and perched onit.Themale simulta-
neously raisedandcurved hisabdomento bringthe primary gonoporein con-
390 K.Matsubara&M.Hironaka
tact withthe secondary genitalia, presumably translocating sperm. Copulation
ensuedimmediately. Themean(±SE) copulation durationwas 17.42± 1.75min
(range =4.08-50.30,N =29).
OVIPOSITION BEHAVIOUR BY FEMALESAND
POSTCOPULATORY BEHAVIOURS BYMALES
Inthe 85(91.4%) of93tandempairs thatappeared atthe observationsite, the
femaleperformed submerged oviposition. In theother 8 tandempairs (8.6%),
the femaleoviposited onthewatersurfaceandthenflewaway fromtheobserva-
tionsite.Thus,whentandempairsappeared attheobservationsite, mostfemales
performed submerged oviposition atleastonce.
Figure 1 is a flow chart of the successive postcopulatory behaviours. After
copulation, the maleand femalein tandemflewto anoviposition site nearthe
water’s edge. Thefemalelandedonthe siteandbent herabdomen, andherovi-
positor contacted the oviposition substrates.The maleresponded by adopting
an“upright tandemposture”in whichhisbody stoodvertically onthetipofhis
abdomen(his analappendages remaining interlockedwiththe female’sthorax),
andflapped andvibratedhis wings. Oviposition began at thewater surfaceand
usuallywas completed underwater.Insurfaceoviposition, onlythefemale’sovi-
positor was immersed, whilethe male maintainedthe upright tandemposture.
Whenthe femalesubmerged by movingbackwards along thesite in tandem(n
= 107), the maleoften released the femalewithoutsubmerging with her(non-
submerged guarding, n =74), or the maleremainedin tandemandsubmerged
eitherforashortmoment atfirst(n= 10)orforthedurationofthefemale’ssub-
mergence(n =23) (submerged guarding, n =33). Malesthatsubmerged only at
firstreturnedto thesurfacetorest abovetheoviposition site.Anyindividualwas
abletoperform bothsubmerged andnonsubmerged postcopulatory guardingfor
submerged ovipositing hispartner.
Afterthemalereleasedthe submerged ovipositing femaleandperched onveg-
etationabovethefemale, heusuallyrecaptured thefemaleoncesheemerged, and
thetandempair began searching foranotheroviposition site.Whenthemalere-
mainedsubmerged withthe femalethroughout oviposition, theirsearch foran-
othersiteresumedpromptly uponemergence. Thefemaleoftensubmerged and
emerged atseveraloviposition sites(theaveragenumberofovipositions (n,mean
± SE.): n= 17,2.2±0.4, range = 1-7).
Themean(±SE) durationofsubmerged oviposition by femalesandthemean
(±SE) durationofsubmerged guarding bymaleswhen themaleadapted either
thesubmerged guardingor thenon-submerged guardingare showninTableI.
Afemalewithanonsubmerged malehadasimilaroviposition timeas thatof
afemalewithanat-firstsubmerged maleor withafullysubmerged male(signifi-
cantpost hoc Mann-Whitney Utest(Padjusted to0.0167 toreducethechance
PostcopulatoryguardinginPseudagrionpilidorsum 391
of committing a type Ierror), vs. a femalewith anat-first submerged male, z
= -1.400, P = 0.1615; vs. a femalewitha fullysubmerged male, z = -1.847, P =
0.0647). Thedurationofsubmerged oviposition by a femalewas shorterwhen
the maleremainedsubmerged withherthroughout oviposition than when the
male was submerged only at first (significant post hoc Mann-Whitney U test
(P adjusted to0.0167 toreducethechance ofcommitting a typeI error),z = -
2.663, P =0.0077). Thedurationofsubmerged oviposition byfemaleswas sig-
nificantly longer thanthatof submerged guarding by males(Wilcoxon signed
ranks, afemalewithanat-firstsubmerged male,n=7, z =-2.366, P =0.0180; a
femalewith afullysubmerged male, n= 17, z = -3.621, P - 0.0003). Thedura-
tionofsubmergence by males didnotdifferbetweenmalesthatsubmerged only
Fig. 1.The flowchart ofthesuccessivepostcopulatorybehaviours inP.p.pilidorsum. — [Aquadri-
lateralshows aparticularevent.Figures inparenthesisindicatesamplesize]
392 K. Matsubara& M.Hironaka
atfirstandthosethatremainedsubmerged throughout (Mann-Whitney Utest,
z = -0.896,P = 0.3704).
Tandempairswereofteninterferedbyalonemales. Theinterferencefrequently
resultedin anoticeablechange offlightor oviposition behavioursby thepair.
TERRITORIALITYAND POSTCOPULATORY MATE
GUARDING BEHAVIOURS
Aftercopulating withaterritorialmale, thefemaleoviposited underwaterin-
sidehisterritoryor inanothermale’sterritory.
Figure 2 shows the proportions of submerged guarding and non-submerged
guarding by territorialmaleswhenfemalesoviposited insidetheirterritoriesor
anothermale’s territory,andthoseproportions by non-territorialmaleswhenfe-
malesoviposited insideanothermale’sterritory.
When thefemaleperformedsubmerged oviposition insideherpartner’s terri-
tory, the territorialmalealwaysreleasedthefemaleandrestedonthewater sur-
faceduringoviposition. On theotherhand,whenthefemaleoviposited underwa-
terinsideanothermale’s territory,themaleowning theterritoryexhibitedeither
submerged guarding ornon-submerged guarding; theproportion ofsubmerged
guarding was higher than thatof non-submerged guarding (Fisher’s exacttest,
P =0.0021, Fig. 2a).
Of 12 territorialmales performing non-submerged guarding forhis partner
inside their territories, only one maleacquired an additional femalethat had
emerged from underwater, by eliminating the non-territorialmaleperforming
non-submerged guardingforhispartner.
Non-territorialmalesalso performed both submerged and nonsubmerged
postcopulatory guardingwhen thefemaleoviposited underwaterinsideanother
male’s territory, andthe proportion ofsubmerged guardingwas similarto that
of nonsubmerged guarding (chi-square goodness-of-fit test, x2= 3.13, df = 1,
P>0.05, Fig. 2b).
TableI
The mean(± SE)duration(min)ofsubmergedovipositionbyfemalesandthemean(+SE)duration
(min)ofsubmergedguardingbymales whenthemaleadaptedeitherthesubmergedguardingorthe
non-submergedguarding[Figuresinparenthesisindicatesamplesize]
Duration ofsubmerged Duration ofsubmerged
ovipositionbyfemales guardingbymales
Non-submergedguarding 21.2313.24(42)
Submergedguarding
Afemalewith anatfirstsubmergedmale 33.2518.25(7) 8.4212.08 (9)
Afemalewith afullysubmergedmale 8.5811.35(18) 6.1411.09(20)
PostcopulatoryguardinginPseudagrionpilidorsum 393
DISCUSSION
FemalesP.p.pilidorsumbeganoviposition onthesurfacebutusually completed
it underwater. Submerged oviposition hasbeenfoundin P.perfuscatum, P. mi-
crocephalum(FURTADO, 1972),P. hagenitropicanum (MESKIN, 1986),P. cit-
ricola, P.i. inconspicuum andP.salisburyense (MESKIN, 1989). Thus, submerged
oviposition mightbe ubiquitous inthegenusPseudagrion.
Whenthefemalesubmerged deeply, themaleeitherreleasedthefemalewithout
submerging orthemalesubmerged completelyandremainedintandem,whether
onlyatfirstorforthedurationoftheoviposition. Similarpostcopulatory behav-
ioursbymaleshavebeenfoundinP.perfuscatum andP. microcephalum. FURTA-
DO(1972) reported anexample inwhichamaleofP. microcephalum submerged
withanovipositing femaleintandembutthenseparatedaftertwominutes,float-
ing to thesurfacetorest onthenearest perch. FURTADO (1972) reported two
otherexamples inmalesofP.perfuscatum: inone, themale submerged withthe
ovipositing femalefor 15minutes,andin theother, the malehoveredabove the
ovipositing femalewithoutsubmerged guarding. InthegenusPseudagrion, there-
fore,thepostcopulatory behavioursbymalesforsubmerged ovipositing females
maybeflexible, depending onhowlong thefemalesare submerged.
Submerged oviposition sometimes lasts more than an hourand may incur
considerableenergycostsand predation risks for the female(WAAGE, 1984).
Furthermore, FINCKE (1988)
and MILLER (1990) consid-
ered that submerged oviposit-
ing females suffer costssuch as
waterloggingandimpaired vigor
upon surfacing. Therefore, it is
likely that submerged guarding
has the same effects on males,
and the cost may be far larg-
er than that of non-submerged
guarding. Flowever, submerged
guardingmaybemoreadvanta-
geousto themalethannon-sub-
mergedguarding,sincethereisa
higherrisk thatothermaleswill
takeover theemergentfemaleif
the guarding male did not sub- Fig. 2,Theproportionsofsubmergedguardingandnon-
-submergedguardingbyterritorial males when females
merge. ovipositedinsidetheirterritoriesoranothermale’sterri-
Whena femaleoviposited in- tory(a), and thoseproportionsby non-territorial males
side her partner’s territory, the when females oviposited inside anothermale’s territory
maleowing thatterritoryalways (b). — [Figuresincolumnsindicatesamplesize]
394 K. Matsubara&M.Hironaka
releasedthefemalewithoutsubmergence andrestedabovethewater surfacedur-
ing oviposition (non-submerged guarding, Fig. 2a). Two hypotheses have been
proposed toexplain theadaptive significance ofnon-contact guardingbytheter-
ritorialmale insidehisterritory (ALCOCK, 1979,UEDA, 1979,SHERMAN,
1983). ALCOCK(1979) andUEDA(1979) suggested thatnon-contact guarding
is reproductively advantageous because it allowsamaleboth to guard the ovi-
positing femaleand to acquire newmates(multiple mating hypothesis). On the
otherhand,SHERMAN(1983)andWAAGE(1984) suggested thatnon-contact
guarding isreproductively important becauseitallowsamalebothto guard the
ovipositing femaleandto maintainhisterritory (territorymaintenancehypoth-
esis).Of 12territorialmalesperforming non-submerged guarding forhispartner
insidetheirterritories,only one malecould acquire anadditionalfemale.From
thisresult, we could not necessarily discard themultiple mating hypothesis, be-
causeofshortageofthedata.SHERMAN(1983) posited thatamaleintandem
wouldhavedifficultyfightingoff intrudersandthattandemmateguardingcould
reduceamale’sability tomaintainhisterritory.Inthisstudy, although theterrito-
rialmalein tandemdidnot eliminateintruders fromhis territory,the territorial
malewhenalone prevailed inmostmale-maleinteractions. Therefore,non-sub-
merged guardingallowsterritorialmalesbothto guardtheovipositingfemaleand
tomaintainhisterritory,supporting theterritorymaintenancehypothesis.
Whenafemaleoviposited underwaterinsideanothermale’sterritory,bothsub-
merged guardingandnon-submerged guardingbytheterritorialmalewerefound,
andtheproportionofsubmerged guardingwas higherthanthatofnon-submerged
guarding (Fig. 2a). Non-territorialmalesalsoexhibitedbothtypes of guarding
whenthefemaleoviposited underwaterinsideanothermale’sterritory(Fig. 2b).
UEDA (1979)showedthatSympetrumparvulummalescouldadoptbothcontact
guardingandnon-contact guarding, changing fromoneto theotherinresponse
to changes intheprobability ofatakeover. InP.p. pilidorsum, malesalso adopt
eithersubmerged or non-submerged guardingforthe samereason.
Theterritorialmaleoftenlefthisterritorytoaccompany amate to anovipo-
sitionsiteelsewhere.Sinceamaledidnot always detectthepresenceofafemale
ovipositing in his territory, theprobability thathe wouldtakeover a femaleovi-
positingwithanintruding malemightbelow.Therefore, amalemightnotalways
engageinsubmerged guardingevenwhenthey are inanothermale’sterritory.
CONVEY (1989) reported thatSympetrumsanguineum malesdecidedwhether
ornot to switch fromcontact to non-contact guardingbasedontheirassessment
ofmaleharassmentearlyinanoviposition bout.Suchharassmentby othermales
may affectthe male’schoicebetween submerged andnon-submerged guarding
in P.p.pilidorsum, but this remainstobeelucidated.
Whenamalesubmerged intandemforthedurationofoviposition, thefemale
completed heroviposition fasterthanwhenthemaleremainedsubmerged only
at first. The maleremainedunderwaterthe same amount of timewhether his
Postcopulatory guardingin Pseudagrionpilidorsum 395
submergence was only atfirst or fortheduration(Tab. I).Therefore, malesmay
ceasesubmerging whenthefemale’ssubmergence isprolonged, partiallybecause
themalecannot stay underwateras long as thefemale.
Submerged guarding mayhaveevolvedincloseassociationwiththemannerof
oviposition, inwhichthefemalefrequently repeatssubmergence andemergence,
laying eggs atseveral sites. Ifafemaleoviposits almostallof hermature eggs at
asingle site, she maythenbetakenover by anothermaleatno cost to herpart-
ner, sinceshewillnot produce mature eggs again forseveral days.On theother
hand, if afemaleoviposits eggs at several sites byrepeated submerged oviposi-
tioning, such as Hetaerinavulneratafemalesdo(ALCOCK, 1982),herpartner’s
submerged guarding maysubstantially benefithimbypreventing anothermale
from taking her. Therefore, submerged guarding by P. p. pilidorsum males may
haveevolved by thefemales’frequent, repeated submergence to lay eggs at dif-
ferent sites untilalmostallofher eggs are gone.
ACKNOWLEDGEMENT
WethankProf.N.SUZUKI, DepartmentofAppliedBiologicalSciences,FacultyofAgriculture,
SagaUniversity, forvaluable suggestionsandcriticallyreadingthemanuscript.
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