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Frontiers in Zoology Frontiers in Zoology This Provisional PDF corresponds to the article as it appeared upon acceptance. Fully formatted PDF and full text (HTML) versions will be made available soon. A cuckoo in wolves' clothing? Chemical mimicry in a specialized cuckoo wasp of the European beewolf (Hymenoptera, Chrysididae and Crabronidae) Frontiers in Zoology 2008, 5:2 doi:10.1186/1742-9994-5-2 Erhard Strohm ([email protected]) Johannes Kroiss ([email protected]) Gudrun Herzner ([email protected]) Claudia Laurien-Kehnen ([email protected]) Wilhelm Boland ([email protected]) Peter Schreier ([email protected]) Thomas Schmitt ([email protected]) ISSN 1742-9994 Article type Research Submission date 30 May 2007 Acceptance date 11 January 2008 Publication date 11 January 2008 Article URL http://www.frontiersinzoology.com/content/5/1/2 This peer-reviewed article was published immediately upon acceptance. It can be downloaded, printed and distributed freely for any purposes (see copyright notice below). Articles in Frontiers in Zoology are listed in PubMed and archived at PubMed Central. For information about publishing your research in Frontiers in Zoology or any BioMed Central journal, go to http://www.frontiersinzoology.com/info/instructions/ For information about other BioMed Central publications go to http://www.biomedcentral.com/ © 2008 Strohm et al., licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Acuckooinwolves’clothing?Chemicalmimicryina specializedcuckoowaspoftheEuropeanbeewolf (Hymenoptera,ChrysididaeandCrabronidae) ErhardStrohm1,2,JohannesKroiss1,2,§,GudrunHerzner1,2,ClaudiaLaurien-Kehnen3,4, WilhelmBoland5,PeterSchreier6,ThomasSchmitt2,7 1UniversityofRegensburg,InstituteofZoology,D-93040Regensburg,Germany 2UniversityofWürzburg,DepartmentofAnimalEcologyandTropicalBiology,Am Hubland,97074Würzburg,Germany 3UniversityofBonn,ZoologicalInstitute,PoppelsdorferSchloss,53115Bonn,Germany 4presentaddress:UniversityofBielefeld,BehaviouralBiology,33501Bielefeld,Germany 5MaxPlanckInstituteforChemicalEcology,DepartmentforBioorganicChemistry,07745 Jena,Germany 6UniversityofWürzburg,DepartmentofFoodChemistry,AmHubland,97074Würzburg, Germany 7UniversityofFreiburg,InstituteofBiologyI(Zoology),Hauptstr.1,79104Freiburgi.Br., Germany §Correspondingauthor Emailaddresses: ES:[email protected] 1 JK:[email protected] GH:[email protected] CLK:[email protected] WB:[email protected] PS:[email protected] TS:[email protected] 2 Abstract Background Host-parasiteinteractionsareamongthemostimportantbioticrelationships.Hostspecies shouldevolvemechanismstodetecttheirenemiesandemployappropriatecounterstrategies. Parasites,inturn,shouldevolvemechanismstoevadedetectionandthusmaximizetheir success.FemalesoftheEuropeanbeewolf(Philanthustriangulum,Hymenoptera, Crabronidae)huntexclusivelyhoneybeeworkersasfoodfortheirprogeny.Thebroodcells containingtheparalyzedbeesareseverelythreatenedbyahighlyspecializedcuckoowasp (Hedychrumrutilans,Hymenoptera,Chrysididae).Femalecuckoowaspsenterbeewolfnests toovipositonparalyzedbeesthataretemporarilycouchedinthenestburrow.Thecuckoo wasplarvakillsthebeewolflarvaandfeedsonitandthebees.Here,weinvestigatedwhether H.rutilansevadesdetectionbyitshost.Sincechemicalsensesaremostimportantinthedark nest,wehypothesizedthatthecuckoowaspmightemploychemicalcamouflage. Results Fieldobservationssuggestthatcuckoowaspsareattackedbybeewolvesinfrontoftheirnest, mostprobablyafterbeingrecognizedvisually.Incontrast,beewolvesseemnottodetectsigns ofthepresenceoftheseparasitoidsneitherwhenthesehadvisitedthenestnorwhendirectly encounteredinthedarknestburrow. Inarecognitionbioassayinobservationcages,beewolffemalesrespondedsignificantlyless frequentlytofilterpaperdiscstreatedwithacuticularextractfromH.rutilansfemales,than tofilterpaperdiscstreatedwithanextractfromanothercuckoowaspspecies(Chrysis viridula).ThebehaviortopaperdiscstreatedwithacuticularextractfromH.rutilansfemales 3 didnotdiffersignificantlyfromthebehaviortowardsfilterpaperdiscstreatedwiththe solventonly. Wehypothesizedthatcuckoowaspseithermimicthechemistryoftheirbeewolfhostortheir host'sprey.WetestedthishypothesisusingGC-MSanalysesofthecuticlesofmaleand femalebeewolves,cuckoowasps,andhoneybeeworkers.CuticleextractsofHedychrum nobile(Hymenoptera:Chrysididae)andCercerisarenaria(Hymenoptera:Crabronidae)were usedasoutgroups.Therewaslittlecongruencewithregardtocuticularcompoundsbetween H.rutilansfemalesandhoneybeesaswellasfemalesofC.arenariaandH.nobile.However, therewasaconsiderablesimilaritybetweenbeewolffemalesandH.rutilansfemales. Beewolffemalesshowastrikingdimorphismregardingtheircuticularhydrocarbonswithone morphhaving(Z)-9-C25:1andtheothermorphhaving(Z)-9-C27:1asthemajorcomponent. H.rutilansfemalesweremoresimilartothemorphhaving(Z)-9-C27:1asthemain component. Conclusions WeconcludethatH.rutilansfemalescloselymimicthecompositionofcuticularcompounds oftheirhostspeciesP.triangulum.Theoccurrenceofisomericformsofcertaincompounds onthecuticlesofthecuckoowaspsbuttheirabsenceonbeewolffemalessuggeststhat cuckoowaspssynthesizethecuticularcompoundsratherthansequesterthemfromtheirhost. Thus,thebehavioraldataandthechemicalanalysisprovideevidencethataspecialized cuckoowaspexhibitschemicalmimicryoftheodorofitshost.Thisprobablyallowsthe cuckoowasptoenterthenestwithareducedriskofbeingdetectedbyolfactionandwithout leavingtraitorouschemicaltraces. 4 Background Theinteractionbetweenhostsandparasitesorparasitoidsisoneofthemostimportantforces drivingevolutionaryandecologicalprocesses(e.g.[1]).Inordertoreducetheimpactof parasitoids,hostspeciesmayevolvemechanismstodetecttheirenemiesandemployadequate counterstrategies(e.g.[2-5]).Parasitoids,inturn,areselectedtoevolvemechanismsthat reducetheprobabilityofbeingdetectedbytheirhoststocircumventsuchcountermeasures. Thissetsthestageforrepeatedcyclesofadaptationsandcounteradaptations(“evolutionary armsrace”;seee.g.[6-10])betweenhostsandparasites,especiallyiftheparasitoidishighly specializedonasinglehostspeciesandhasalargeimpactonhostfitness[2,11,12]. Progenyofbroodcaringbeesandwaspsareparticularlysusceptibletoparasitism[13-15]. Femalesofthesespeciesstorelargeamountsofvaluablenutrientsaslarvalprovisionsin broodcells.Thesevaluableresourcesattractavarietyofbroodparasites,either cleptoparasitesthatreducetheamountofresourcesavailabletothehost’sprogenyor parasitoidsthatobligatorilykillthehostlarvae.Mostly,femalesoftheseparasiticspecies havetoenterthenestorthebroodcelltodepositeggsorlarvae.Thus,thetracesthatareleft byfemalebroodparasitesmightbedetectedbythehost.Asaresult,thehostsmightabandon thenestsorremoveordestroyeggsofbroodparasites[5,16].Broodparasitesmightalsobe encounteredinthenestbythehostandmightbedrivenaway,injured,orevenkilled(E. Strohm,unpubl.observations).Sinceinsectsheavilyrelyontheirchemicalsensesforany kindofrecognitionorlocalizationprocess[1,17,18],concealmentofabroodparasite's actualorpreviouspresencewillrequirechemicalcamouflage(compoundssequesteredfrom thehostorthehost’snest)orchemicalmimicry(compoundssynthesizedbythemimic, definitionssensu[19]).Inthisstudy,weinvestigatedtheinteractionbetweenahuntingwasp, 5 theEuropeanbeewolf,Philanthustriangulum(Hymenoptera,Crabronidae)anditshighly specializedbroodparasitoidHedychrumrutilans(Hymenoptera,Chrysididae).We investigatedthefollowingquestions:Arecuckoowasps(H.rutilans)detectedandrecognized bybeewolffemalesatall?Isthereadifferenceinhostresponsetowardsthecuckoosoutside andinsidethenestanddothecuticularhydrocarbonsplayaroleforthedetectionofthe cuckoowaspsinsidethenest?Isthechemicalcompositionofthecuticularhydrocarbonsof H.rutilansfemalessimilartotheirhostortotheirhost’sprey? FemalesoftheEuropeanbeewolfhunthoneybeeworkers(Hymenoptera,Apidae)asfoodfor theirprogeny.Severalparalyzedbeesaretemporarilycouchedinthemainburrow(upto1m long)oftheundergroundnest(see[20]fordetailsonnestarchitecture).Eventually,the femaleclosesthenestentrance,excavatesasideburrowandaterminalbroodcell,bringsin onetosixparalyzedbees,andovipositsononeofthebees[21].Thereupon,shecarefully closesthesideburrowandsubsequentlyhasnocontacttoherprogeny. Thecuckoowasp,H.rutilans,isaspecializedbroodparasitoidofthegenusPhilanthus[16, 22].However,sinceinCentralEuropeonlyonememberofthegenus,P.triangulum,isfairly abundant,H.rutilansiseffectivelymonospecificinthisregion.Thisconsiderabledegreeof specializationisexpressedbytheuniqueovipositionstrategyofH.rutilans.Mostchrysidid waspsovipositintothebroodcelloftheirhostsatadefinedstageoftheprovisioningcycleor afterthebroodcellhasbeenfinallyclosed[22].Inbeewolves,however,thebroodcellis excavatedonlyafterthefemalehasbroughtinthebeesandthenestentrancehasbeenclosed. Thus,thenestisblockedupandthefemaleisattendantuntilthebroodcellisfinallyclosed. Thisleaveslittleopportunityforacuckoowasptodepositanegginthebroodcell.Asa consequence,H.rutilansfemalespursuetwoalternativestrategies.Eithertheyrapidlypounce 6 andovipositonaparalyzedbeewhenthefemalealightswithitspreyandenterstheburrow ([23],E.Strohmunpubl.observation),orH.rutilansfemaleswaitinfrontofthenestuntilthe hostfemaleleavestoforageandthenentertheburrowandovipositontheparalyzedbeesthat
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