Differences in larval emergence chronotypes for sympatric Rhagoletis brncici Frías and Rhagoletis conversa (Bréthes) (Diptera, Tephritidae)

RevistaBrasileiradeEntomologia63(2019)195–198

REVISTA

BRASILEIRA

DE

Entomologia

Short

Communication

Differences

in

larval

emergence

chronotypes

for

sympatric

Rhagoletis

brncici

Frías

and

Rhagoletis

conversa

(Bréthes)

(Diptera,

Tephritidae)

Daniel

Frías-Lasserre

_,

_Andrea

_Luna

_S

_,

_Cristian

_A.

_Villagra

b_{UniversidadAutónomadelEstadodeMorelos,FacultaddeCienciasAgropecuarias,CuernavacaMorelos,Mexico}

a

r

t

i

c

l

e

i

n

f

o

Articlehistory: Received18August2018 Accepted26April2019 Availableonline18May2019 AssociateEditor:LeonardoBarbosa Keywords: R.conversa R.brncici Sympatry Chronotypes Emergence Larvae

a

b

s

t

r

a

c

t

IncentralChile,RhagoletisbrnciciandR.conversa,canbefoundinsympatry,associatedwiththefruit oftheirnativehostplants:SolanumtomatilloandS.nigrum(Solanaceae),respectively.Third-stage lar-vaemustemergefromitshostinsearchofpupationsites,andduringthisperiodlarvaemustfindan appropriatepupationmicrohabitatwhileavoidingpredationandadverseabioticfactors.Inthisstudy, weexploredwhetherthesesympatricspeciesdifferintermsofthetimingoftheirlarvalexitfromthe hostfruitinsearchofpupationsites.Field-collectedfruitsfromhostplantswerecheckeddailyforlarval emergence,within24h,underlaboratoryconditions,inordertodeterminethetimeoftheevent.We foundthatthesespeciesdifferedsignificantlyintheirdiellarvalemergence.ForR.brncici,mostlarvaeleft thehostfruitbetweenlateeveningandpastmidnight,meanwhilelarvaefromR.conversaconcentrated theirpeakofemergencenearmidnightandearlymorning.Wediscussthesefindingsintermsofthe ecologicalandevolutionaryimplicationsofthetemporalseparationoflarvalemergenceregardingthe useofpupationsites,abioticstressandriskofpredationforthesesympatricspecies.

PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeEntomologia.Thisisanopen accessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/by-nc-nd/4.0/).

Nichepartitioningthroughtheuseofdifferentresourcesisa factorthatpromotesthecoexistenceofecologicallysimilarspecies insympatry(LevineandHilleRisLambers,2009).Ininsects,such divergencemaybeexpressedasallochronicbehaviors:differences inthetimingofactivitypeaksthatpromotespeciesspatialoverlap (Schoener,1974;WernerandGilliam,1984).Temporal segrega-tioninforagingbehaviorfacilitatesthesympatriccoexistenceof insectspeciesfromanoak-defoliatingassemblage(Kalapanidaand Petrakis,2012).Allochronicbehavioraldifferencesinpopulations ofthesamespecies couldpromotea sympatricspeciation.Four sympatric species of ants fromthe Australian genusMyrmecia, forexample,arecapableofsharingforagingresourcesandspace by being active at different times of the day (Narendra et al., 2016).Inthesamefashion,ithasbeenfoundthatinthe dragon-flyspeciesAnax imperatorLeach,1815andA.parthenope(Sélys, 1839)(Odonata:Aeshnidae),immaturesselectsimilarsubstratesas supporttocarryoutecdysis,buttheyemergefromthewater asyn-chronouslytodoso,contributingthistemporaldifferentiationto thesympatriccoexistenceofthesespecies(Boucennaetal.,2018).

∗ Correspondingauthor.

E-mail:daniel.frias@umce.cl(D.Frías-Lasserre).

In thecase of tephritidflies(Diptera),despitemany species havingbeencarefullystudiedduetotheirimportanceaspestson severalfruitcommodities(Uchôa,2014),theinformationregarding larvalbehaviorisscarce,andresearchconcerningtemporal pat-ternsoflarvalactivityisevenlessabundant(butseeAlujaetal., 2005).

However,consideringavailablestudiesin tephritidflies, itis proposedthatamonglarvaebehaviors,thelast-stage larvalexit fromthehostfruittofindpupationsitesinthesoilisoneofthe mostcriticaleventsofthisperiod.Attheendofdevelopment,the larvaemustfindasuitablepupationmicrohabitatwithspecificsoil, temperatureandhumiditycharacteristics(Thomas,1995).

Moreover,wanderinglarvaemustavoidadverseabiotic condi-tions,suchaselevatedtemperaturesthatmaykillthemthrough dehydration(Alujaetal.,2005;Schwerdtfeger,1976).Ontopof allthis,whilelookingforpupationsite,larvaemustevadeactive predatorsandparasitoids(Fernandesetal.,2012;Thomas,1993, 1995).Ithasbeenfoundthatlarvaesearchingforpupationsites mayeventrytopreventpotentialpredationand/orparasitation duringpupation(Bressan-Nascimento,2001;WangandMessing, 2004).Thisimplies covering asmuchdistanceas possiblefrom thehost fruit’skairomones (usedby parasitoidsto findnearby pupae)andalsofromotheralreadyestablishedpupationsites,as https://doi.org/10.1016/j.rbe.2019.04.003

0085-5626/PublishedbyElsevierEditoraLtda.onbehalfofSociedadeBrasileiradeEntomologia.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense(http:// creativecommons.org/licenses/by-nc-nd/4.0/).

196 D.Frías-Lasserreetal./RevistaBrasileiradeEntomologia63(2019)195–198

larvalaggregationsarealsopreferentiallypredatedandparasitized (Guillénetal.,2002).

The genus Rhagoletis Loew (Diptera: Tephritidae), with 65 speciesdistributedintheNearctic,PelearcticandNeotropicalzones (Foote,1981;Thompson,1999;WhiteandElson-Harris,1994),has beenmostly studiedregarding theirreproductive behavior and ovipositionmechanisms(Frías-Lasserre, 2015;Rullet al.,2016). Littleinformationisavailableregardingotherkeylifecycleevents relatedtothelarvalstages,suchasthetimingoflarvaerhythmic behaviors.

Sofar,itisknownthatafterfemales fromRhagoletis species deposittheireggsinsidehost’sfruits,larvaehatchandfeedonthe mesocarpandseeds,requiringanapproximateminimumoftwo weeksinside theparasitized fruittogrowthand develop(Duso andLago,2006;Frías,1986).Followingthat,thethird-instar lar-vaeleavethefruitandenterthesoiltopupateandoverwinterfor severalmonthsindiapause(BollerandProkopy,1976;Bush,1992, 1966;ChristensonandFoote,1960;Frías,1992).Despitethe rele-vanceofthistemporalevent,dielpatternsoflarvalemergenceare unknownformanyRhagoletisspecies.

IntheNeotropic,mostRhagoletisspeciesareassociatedwith Solanaceae(Foote,1981;Fríasetal.,2006;Frías,2001).Incentral Chile,forexample,RhagoletisbrnciciFríasandR.conversa(Bréthes) (Diptera,Tephritidae)overlaptheirdistributionsassociatedtothe phenologicalcycleoftheirrespectivehostplants:Solanumtomatillo andS.nigrum(Solanaceae)(Fríasetal.,1984).Inthisshortpaperwe explorethecircadianclocksforlarvalemergenceintwosympatric andclosely-related species:We evaluateifthere is a diverging dielpatternforlarvaeleavingthehostplant’sfruitsanddiscuss emergencetrendsinoverlappingclosely-relatedholometabolous insects.

Observationsoflarvalemergencewerecarriedoutunder labo-ratoryconditionsat21±1◦C,65%relativehumidityand14h:10h L(3600lx):DphotoperiodatInstitutodeEntomologíaUniversidad MetropolitanadeCienciasdelaEducación,Santiago,Chile.The lar-vaeofR.brnciciandR.conversawereobtainedwiththefruitsof theirrespectivehostplants,S.nigrumandS.tomatillo(Solanaceae), inthetownofPirque(33◦3800S70◦3300W)intheCordillera Province,located21.3kmsoutheastofSantiago,atanaltitudeof 697m.a.s.l.

BetweenOctober andDecember 2017,sixperiodic fruit col-lections were made using plastic screw-top jars that had a fine mesh lid to ensure good ventilation. During this period, a total of approximately 6000 fruits of S. nigrum and 2000 fruitsofS.tomatillowerecollected.Thesefruitsweretransferred to the laboratory and placed on a thin grid on a plastic tray (40cm×35cm×8cm).Thegridallowedonlythepassageofthe larvae that left the fruits, which fell onto the plastic tray and thuscouldbecounted.Duringthe24-hlarvalemergence,records weretakenattimeintervalsof 5h(Table1);consideringdawn (06:00–11:59); midday (12:00–17:59), dusk (18:00–23:59) and

night (00:00–05:59) time intervals (CLST, Chile Summer Time, UTC/GMT −3h). Thisobservation wasrepeated22 times for R. brncici and 10 for R. conversa. For each species, at each inter-val,thelarval emergencepercentagewasdetermined.Withthe informationobtained,thepercentageoflarvaethatemergedwas estimated.

Circularstatisticalanalysiswasconductedinordertotestthe occurrenceofagivendielpatternofemergenceforthesespecies (dosSantosetal.,2017;Fisher,1993).Totesttheprevalenceof emergencetimingona24hrclockfortheRhagoletisspecies,we usedaRayleigh(z)testinordertospecifythesignificanceofmean anglefortheoccurrenceofthisbehavior.Weconsideredasanull hypothesis time intervalsfor emergence that were evenly dis-tributedaroundthedielclock.Alternatively,therecouldbeamean timeintervalwherefliesemergencesarebeingconcentrated. Fur-thermore,wecompareddielemergencebetweenR.brnciciandR. conversausingWatson–William equaldirectionstest (Morellato etal.,2010).

Therewasacleartendencyofthelarvaeofboththestudied species toemergein a timerange from18:00 PMto5:59AM. Eighty-threepercent ofR. brnciciand 77% of R.conversa larvae emergedduringthiswindow.Despitethesimilarityofthese emer-gencetimes,thelarvaeofthesespecies,duringthespecifiedtime window,displayeddifferencesintheproportionoflarvaeexiting fruitatdifferenttimes.InR.conversa,thehighestpercentageof larvaeexitingfruitwasbetweenthehoursof00:00to5:59(65% emergence),whenonly39%ofR.brncicilarvaeemerge.Between thehoursof18:00to23:59,12%ofR.conversalarvaeemerged, whiletheemergenceofR.brncicilarvaeinthesameperiodwas 44%.Duringdaylighthours(6:00–5:59),thepercentageemergence ofthelarvaeofbothspeciesdecreased(18%inR.brnciciand23%in R.conversa)(Table1A).

Themeantimeoflarvalemergenceshowedamarkeddiel pat-ternforeachRhagoletisspecieswithrcorrespondingto0.5and 0.7forR.brnciciandR.conversarespectively.Thenull hypothe-sisofuniformdistributionforbothspecieswasrejected(Table1B, Fig.1).Furthermore,R.brnciciandR.conversaalsoshowed statisti-caldifferences,disprovingthenullhypothesis(Watson–Williams test,F=168.873;p<0.0001).

ThesympatricRhagoletisspeciesR.brnciciandR.conversahave a marked diel pattern of larval eclose from their hosts’ fruits. Moreoverthecircadianrhythmsforthisactivitywerestatistically different betweenthese two closely-relatedtaxa, perhaps as a productofselectionproducedbyhostplantsthatoccupydifferent habitats.

Extrapolatingourexperimentaldatatowhatcouldhappenin nature,thescarceemergenceoflarvaeofbothspeciesduring day-timemayallowthemtoavoidthehighertemperaturesrecorded for thesetimesin thefield (reaching around30◦C),duringthe spring–summerseasonintheMatorralofcentralChile(Armesto etal.,2007;Rundel,1981),thusavoidingdehydration.

Table1

A:Larvalemergence(percentageandsamplesize)inrelationtodieltimeintervalsforRhagoletisbrnciciandR.conversa.B:Circularstatisticsuniformdistributionshowing samplesize,Raleighttestvalueandstatisticalsignificanceforbothsympatricspecies.

(A) (B)

Species TimeIntervals Larval Emergence

SampleSize MeanDirection Circular Deviation

Lengthofmean vector(r)

Rayleigh’sStat. Rayleigh’sProb.

R.brncici 00:00–05:59 39%(335) 867 23.189 4.191 0.548 558.957 <0.001 06:00–11:59 8%(69) 12:00–17:59 10%(84) 18:00–23:59 44%(379) R.conversa 00:00–05:59 65%(194) 299 2.593 3.391 0.674 302.355 <0.001 06:00–11:59 22%(66) 12:00–17:59 1%(4) 18:00–23:59 12%(35)

D.Frías-Lasserreetal./RevistaBrasileiradeEntomologia63(2019)195–198 197

Rhagoletis brncici Rhagoletis conversa

18 6 ₁₈ 12 12 0 379.0 189.5 379.0 194.0 194.0 97.0 97.0 194.0 97.0 .0 194.0 379.0 379.0 189.5 189.5 189.5 6 0

Fig.1. CircularhistogramroseplotshowingRhagoletisbrnciciandR.conversalarvalemergencefromfruitina24-hclock.Forbothgraphs,thearrowshowsthemeantime ofemergence.Mainnumbersinsectionscorrespondtotimeinhours.Numbersaccompanyingcircumferencesrefertonumberofindividuallarvaereplicates.

Ithasbeendocumentedthat predationatthetimeof third-instaremergencefromfruitsisoneofthefactorsthataffectslarval survival(Alujaetal.,2005).Theotherfactor thatmayinfluence larvalemergencebehaviorinthespeciesstudiedistheevasionof potentialdiurnalpredatorsthathavebeendescribedfor Tephri-tidaelarvae,suchasmice(Thomas,1993,1995),antsandwasps (Alujaetal.,2005),andalsoseveralparasiticmicrohymenopteran species(Maier,1981; Ovruskiet al.,2000;Bomfim etal.,2007; Hernández-Ortizetal.,1994;Sivinskietal.,2001,1997;Tairaetal., 2013).

Moreover,theinterespecificallochronydetectedinlarvae emer-gence,forbothRhagoletisspecies,maybealsoberelatedtothe differencesingeographicaldistributionfoundinthesespecies;R. brncicitendstoinhabitcoolerplacesinthesub-Andeanregionof centralandsouthernChile,whereasR.conversaisdistributedin warmerlocalitiesincentralandnorthernChile(Fríasetal.,1984; Frías,2001).Thiskindofpatternhasbeenfoundinspeciesofother generaofThephritidaesuchasBactrocera(Danjumaetal.,2014) andCeratitis(DuyckandQuilici,2002).

Asafinalremark,wecancommentthatitisnecessaryto fur-therstudylarvalexittimingdifferencesinthesetwo Rhagoletis species in allopatric populations, considering climatic variables andtheirrespectiveSolanumhostplants,inordertotestif tem-poral differencebetween R. conversa and R. brncici larvae may fit to potential physiological adaptations of these flies within theirdistribution. Moreover, it would alsobe of great interest tocomparethiswithsympatricpopulationsinorder totest for differencesinemergenceregardingallopatricpopulations.These comparisonsmayallowustodisentanglewhetherchangesin lar-valexitevolvedasanisolatingmechanismwhenthesetwospecies overlap.

Conflictsofinterest

Theauthorsdeclarenoconflictsofinterest.

Acknowledgments

ToAdrianaMoctezumaOcampo(UAEM),fortheirsupportinthe fruitcollectioninthefield.

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