Bionomics and seasonal occurrence of Larinus filiformis Petri, 1907 (Coleoptera:
Curculionidae) in eastern Turkey, a potential biological control agent for
Centaurea solstitialis L.
L. Gültekin,1 M. Cristofaro,2,3 C. Tronci3 and L. Smith4
Summary
WeconductedstudiesonthelifehistoryofLarinus filiformisPetri,1907(Coleoptera:Curculionidae:Lixinae)todetermineifitisworthyoffurtherevaluationasaclassicalbiologicalcontrolagentofCentaurea solstitialisL.(Asteraceae:Cardueae),yellowstarthistle.ThespeciesoccursinArmenia,Azerbaijan,TurkeyandBulgaria.AdultshavebeenrearedonlyfromC. solstitialis.IneasternTurkey,adults were active from mid-May to late July and oviposited in capitula (flower heads) of C. solsti-tialisfrommid-Junetomid-July.Inthespring,beforefemalesbeginovipositing,adultsfeedontheimmature flower buds of C. solstitialis,preventingthemfromdeveloping.Larvaedevelopinabout6weeksanddestroyalltheseedsinacapitulum.TheinsectisunivoltineineasternTurkey,andadultshibernatefrommid-Septembertomid-May.
IntroductionCentaurea solstitialis L. (Asteraceae:Cardueae),yel-lowstarthistle,isanimportantinvasivealienweedinrangelands of the western USA (Maddox and Mayfield, 1985;Sheleyet al.,1999;DiTomasoet al.,2006).Al-thoughsixspeciesofinsectshavebeenintroducedtotheUSAforbiologicalcontrolofthisweed,thereisstillinterest to find additional prospective agents (Balciu-nas,1998;Smith,2004a;Pitcairnet al.,2006).GreeceandTurkeyareconsideredtobethegeographiccentreofdiversityofC. solstitialis(Wagenitz,1975;Dostál,
1976).RecentexplorationscarriedoutinEasternTur-key revealed the presence of Larinus filiformis Petri,1907 (Coleoptera: Curculionidae), a weevil strictlyassociatedwithC. solstitialis(Cristofaroet al.,2002,2006;Gültekinet al.,2006).L. filiformiswasoriginallydescribedfromAraxValley(Armenia)andisincludedin theLixinaesubfamily (Petri,1907;Ter-Minassian,1967).However, nothing isknownabout its biology.Thegoalof thisworkwas toclarify this insect’s lifehistory,includinghostrange,seasonaloccurrenceandgeographicdistributioninTurkey.
Methods and materialsField surveys and observations were conducted fromearly spring through summerduring2003.Thegoalswere to collect live adults forbiological experimentsand to observe hibernation places, initiation of adultactivity in the spring, adult feeding,mating, oviposi-tion,larvalfeedinganddevelopment,hostplants,ovi-positionpreference,seasonofoccurrenceofdifferentdevelopmentalstagesandtocollectassociatedparasit-oids.TheprincipalstudysiteswerelocatedinBingöl
Province (from35kmnorth-eastofBingöl to15kmwest of Bingöl) and in Iğdır Province, (from 6 km east of Tuzluca to 7 km east of Iğdır). Both provinces are temperateregions.TheBingölregionischaracterizedby Quercus forest with open areas, including aban-doned fields where C. solstitialis commonly occurs.Iğdır Province contains the Aras river valley and Ağrı mountain lowland area (Iğdır Plain). The Aras valley is quite desertified and eroded and dominated mainly bysemi-desertvegetation.Whenwefoundasitewithat least100C. solstitialisplants,wesearchedyellowstarthistleplantsforsignsofL. filiformis(e.g.feedingandovipositiondamageandpresenceofadults).Dur-ing1997to2006,whileconductingasurveyofLarinusbiodiversity,theleadauthorrecordedhostplantasso-ciationsineasternTurkeybyexaminingmanyplantsinthe tribe Cardueae (Asteraceae). Mature flower heads were collected and held to rear adult insects fromknownhostplants.
Results and discussionInsect morphology
Adult body length is 4.5 to 6.5 mm. The body isblack,thescape,funicleandtarsiarechestnut-brown,and the tibia and apex of femur are brownish-black (Figure1).Goldencolourhair-likescalesarescatteredsparselyonpronotaldiscandbody.Elytraareclothedwithbifurcateshortwhitish-greyscales,whicharemoredense on second to fourth intervals (where the first in-tervalisthelongitudinalstripeclosesttothecenterofthe insect when wings are folded) and on the lateralmargins.Therostrumiscylindrical,weaklycurved,1.0to1.5timesaslongaspronotumandisdistinctlylongerandmoreshinyinfemalesthanmales(Figure1).Elytraareparallelsidedat thebasalhalfandthengraduallycurvedtowardtheapex.
Life historyFirstadultactivityinthespringwasrecordeddur-
ingthethirdweekofMay.BytheendofMay,mostofthe insectshademerged fromhibernation.Early sea-son field collections suggest that males become active earlier than females.Matingwasnotobserved in thefield until the end of May, but it continued throughout theadultlifespan.Adultsfeedonyoungbuds,onthecentralgrowingtipoftheplantandonleavesofC. sol-stitialis.Laterintheseason,theyfeedontheinternalreceptacle tissue and flower parts of immature and ma-ture flower heads. Adults were active in the field from 19Mayto3August2003.
Based on our observations in the field and cage studies,threeconditionswerenecessarytobeginovi-position: temperature above 25°C, feeding for about20daysandavailabilityofmatureC. solstitialis flower heads. In the field, oviposition was recorded from mid-Junetomid-July.Femaleschewedanovateholewiththeir rostrum in the lowerpart ofmature, rarelypre-flowering flower heads and laid a single egg into the receptacle tissue.Theovipositionhole is then closedwithasecretion.Eggshatchedinabout13daysunderlaboratoryconditions.
In the field survey, the first larvae were found at the beginningofJulyin theBingölregion(1,000masl).Thelarvaefedonreceptacletissueenlarginganiche,eventually consuming all the flower parts and recep-tacle. Larvae fastened together remaining flower parts and frass to form a hard cell inside the flower head. Pupation occurs inside the flower head, about 3 days aftermature larvaeceasedfeeding.LarvaewereseenfromthebeginningofJulytomid-September.Attackedflower heads can easily be distinguished because they dried prematurely without flowering.
First adult emergence was recorded in late July inIğdır region. The adults waited inside flower heads about
1 week before exiting from the top of the flower. New adults were recorded in the field until mid-September at the Iğdır site. Hibernation started in mid- to late September:Adults generally hide under rocks, dry plantpartsordebrisingroupsoftwotothreeindividuals.
Geographical distribution and host plant range
L. filiformis occurs from easternArmenia, Nakhi-chevanautonomous regionofAzerbaijanand inTur-key,fromtheeastborderthroughcentralAnatoliaandnearthesouthernMediterraneancoast(Figure2).OnespecimenwasdeterminedfromBulgaria,whichwasanewrecordforEurope(Gültekinet al.,2006).
Three years of extensive field observations, collec-tionsandlaboratoryrearing,carriedoutbyourgroupinTurkey,indicatethatL. filiformisismonophagousonC. solstitialis.
Natural enemiesSix hymenopteran parasitoid species were reared
from larval and pupal stages of L. filiformis: Bracon urinator(F.),Bracon tshitsheriniKok.,Exeristes robo-rator F., Aprostocetus sp. and two unidentified wasp species belonging to the families Eurytomidae andOrmyridae.
ConclusionsOurresultsindicatethatL. filiformisiscloselyassoci-atedwithC. solstitialis in the field in eastern Turkey.
TheinsectwasverycommononC. solstitialisandwasneverfoundfeedingonothernearbyplants.Theadultsdestroy many immature flower heads, and larvae de-stroy all the seeds within flower heads that they infest. ThisdamageisverysimilartothatcausedbyLarinus minutusGyll.onspottedanddiffuseknapweeds,Cen-taurea stoebeL.andCentaurea diffusaL.;L. minutusGyll.isabiologicalcontrolagentthatappearstobere-ducingpopulationsofthesetwoweedsinNorthAmer-ica (Smith, 2004b; Seastedt et al., 2007). Therefore,L. filiformiswarrants furtherevaluationasaprospec-tivebiologicalcontrolagentforthisweed,especiallyifitdoesnotinterferewiththeotherseedheadinsectsthatarealreadyestablished(Pitcairnet al.,2004;2005).
AcknowledgementsWearesincerelygratefultoProfessorVladimirI.Doro-feyev(KomarovBotanicalInstitute,RussianAcademyof Sciences, St. Petersburg, Russia) for identification ofplants;DrS.V.Belokobylskii,DrD.R.Kasparyan,Dr K. Dzhanokmen (Zoological Institute, RussianAcademyofSciences,St.Petersburg,Russia)foriden-tification of parasitoid wasps; Dr Boris A. Korotyaev (Zoological Institute, Russian Academy of Sciences,St.Petersburg,Russia) for years of supervision, sup-portandtrainingoftheseniorauthorinweeviltaxon-omy.TheseniorauthorwassupportedbygrantsfromCollaborative Linkage Grants no. 978845 and NR-CLG-981318oftheNATOLifeScienceandTechnol-ogyProgramme;BBCAresearchgrantandTUBITAK-TOVAG-105O038.
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