Egg maturation egg resorption and the costliness of transient egg limitation in insects - PDF document

Eggmaturation,eggresorptionandthecostlinessoftransientegglimitationininsectsJayA.Rosenheim1*,GeorgeE.Heimpel2andMarcMangel31DepartmentofEntomology,UniversityofCalifornia,OneShieldsAvenue,Davis,CA95616,USA2DepartmentofEntomology,UniversityofMinnesota,StPaul,MN55108,USA3DepartmentofEnvironmentalStudies,UniversityofCalifornia,SantaCruz,CA95064,USAAlthoughthereiswidespreadagreementthatthecostofovipositionunderliesselectiveovipositionininsects,thereisnoconsensusregardingwhichfactorsmediatethecostofoviposition.Modelshavesuggestedthateggcostsareoftenparamountinthoseinsectsthatdonotcontinuetomatureeggsduringtheadultstage(pro-ovigenicinsects).Hereweaddressthehypothesisthateggcostsaregenerallylesssigni¢cantinsynovigenicinsects,whichcanreplenishoocytesuppliesthroughcontinuouseggmaturation.Adynamicoptimizationmodelbasedonthebiologyofahighlysynovigenicparasitoid,Aphytisaonidiae,suggeststhatthemaximumrateofeggmaturationisinsu¤cienttobalancethedepletionofeggswhenopportunitiestoovipositareabundant.Transientegglimitationthereforeoccurs,whichimposesopportu-nitycostsonreproducingfemales.Thus,whereasthemostfundamentalconstraintactingonthelifetimereproductivesuccessofpro-ovigenicspeciesisthe¢xedtotalnumberofeggsthattheycarryateclosion,themostfundamentalconstraintactingonasynovigenicspeciesisthemaximumrateofoocytematura-tion.Furthermore,theabilityofsynovigenicspeciestoreversethe£owofnutrientsfromthesomatooocytes(i.e.eggresorption)hasadramaticin£uenceonthecostofoviposition.Whereasfemalesinhost-richenvironmentsmayexperienceoviposition-mediatedegglimitation,femalesinhost-poorenviron-mentsmayexperienceoosorption-mediatedegglimitation.Bothformsofegglimitationarecostly.Contrarytoinitialexpectations,the£exibilityofresourceallocationthattypi¢essynovigenicreproduc-tionactuallyappearstobroadentherangeofconditionsunderwhichcostlyegglimitationoccurs.Eggcostsappeartobefundamentalinmediatingthetrade-o¡betweencurrentandfuturereproduction,andthereforeareanimportantfactorfavouringselectiveinsectoviposition.Keywords:costofreproduction;costofoviposition;currentversusfuturereproduction;egglimitation;timelimitation;eggresorption1.INTRODUCTIONHerbivorousandparasiticinsectsareselectivewhenchoosinghostsuponwhichtodepositeggs.Hoststhato¡eranon-zeroprobabilityofsupportingsuccessfulo¡springdevelopmentbutwhicharesuboptimalinsomewayareoftenrejected.Why?Williams(1966)wasthe¢rsttorecognizethepivotalimportanceofthecostofreproduction,andspeci¢callythetrade-o¡betweencurrentandfuturereproduction,totheevolutionofreproductivestrategies.ThereiswidespreadagreementthatWilliams'thesisexplainsselectiveovipositionininsects:thebene¢tsfromovipositingonamarginal-qualityhostcanbetoosmalltoo¡setcostsintheformofdecreasedopportunitiesforfuturereproduction.Butwhatfactorsmediatethetrade-o¡betweencurrentandfuturereproductionininsects?Heretherehasbeennoconsensus.Extensiveresearchhasbeendevotedtodevelopingamechanisticunderstandingofthecostofreproductionindi¡erentgroupsofanimals(Clutton-Brock1991;Ylo«nenetal.1998).Theexactnatureofsuchcostsoftendependscriticallyuponthespeci¢cbiologyoftheanimalbeingconsidered.Forinsects,whichgenerallydonotexhibitparentalcarefollowingoviposition,di¡erentschoolsofthoughthaveemergedregardingthefactorsmediatingthecostofreproduction,andinparticularthe`costofoviposition',whichincludesonlythosecoststhatareincurredbyacceptingahostandavertedbyrejectingahost(Rosenheim1996,1999a;Sevensteretal.1998).Oneschoolhasarguedthatthesecostsaremediatedentirelybythetimerequiredtodepositeggs(e.g.Charnov&Skinner1984;Visseretal.1992;Glaizot&Arditi1998;Kraaijeveld1999).Anotherschoolhasarguedthatthe¢nitelifetimesupplyofeggsisalsooftenimportantinmediatingthecostofoviposition(e.g.Iwasaetal.1984;Mangel1989;Mangeletal.1994;Collier1995a;McGregor1997).Ineithercase,thecostofovipositioncanbeviewedasanopportunitycost:timeoreggsthataredevotedtoexploitingacurrenthostcannotbeusedinthefuturetoexploitanother,potentiallyhigher-quality,host.Inanattempttoresolvethedi¡erencesbetweenthesetwocompetingschools,Rosenheim(1999a,b)developedmodelsthatplacethetimeandeggcostsofovipositioninacommoncurrency(foregonefuture¢tnessreturns)sothattheirrelativemagnitudescouldbedirectlycompared.Themodelsshowedthatevenwhenonlyasmallfractionofindividualsinapopulationexhausttheirlifetimesupplyofeggs,eggcostsoftencontinuetomakeanimportantcontributiontotheoverallcostofoviposi-tion.Timecosts,however,maystillbeimportant,espe-ciallywhenhostsarescarceandthereforevirtuallyallfemaleshavemoreoocytesthantheywilleverhaveachancetodeposit.Thus,thegeneralconclusionthatemergedwasthatbothtimeandeggscanmakeimportantProc.R.Soc.Lond.B(2000)267,1565^15731565©2000TheRoyalSocietyReceived8February2000Accepted23March2000 *Authorforcorrespondence(jarosenheim@ucdavis.edu).doi10.1098/rspb.2000.1179 contributionstothecostofoviposition,witheggcostspredominatingwhenhostsareabundantandtimecostspredominatingwhenhostsarerare.Forthesakeofmaximumtransparency,thesemodelsassumedthateggmaturationwaspro-ovigenic,i.e.thatalloocytematurationoccurspriortoadulteclosion.Pro-ovigenyisalife-historypatternthatincorporatesarigidone-timeallocationofresourcesbetweensomaticmain-tenanceandreproduction.Manyinsects,however,continuetomatureoocytesduringtheadultstage(i.e.synovigeny;Volko¡&Daumal1994;Boggs1997a,b;Rivero&Casas1999a).Anaturalobjection,therefore,totheearlieranalysesisthatmanyinsectsretainsubstantial£exibilityinallocatingresourcestoreproductionversussomaticmaintenanceduringtheadultstage,therebyminimizingtheriskthateggsupplieswouldbeexhausted,evenwhenhostsareabundant.Insectsarenoteworthyrelativetomanyotheranimalsforthespeedwithwhicheggscanbefullyprovisionedwithyolkandreadiedfordeposition(Papaj2000).Noinsect,however,canmatureoocytesinstantaneously.Furthermore,somesynovigenicinsectshavelimitedabilitiestostorematureoocytesand,therefore,maycarryonlyafewmatureeggsintheirovariesatanytime(Iwata1964).Therefore,evensynovi-genicinsectsmayexperiencetransientboutsofegglimita-tion,whentheyexhausttheirsupplyofmatureoocytesandmustawaitfurthereggmaturationbeforetheycanresumereproduction(Charnov&Skinner1988;Heimpel&Rosenheim1998;Casasetal.2000).Thepurposeofthispaperistoanalysethecostofovipositionforaninsectthatexhibitsaveryhighlevelof£exibilityinreproductiveallocations,theparasitoidAphytisaonidiae.A.aonidiaefeedsasanadultonhostandnon-hostfoods,andcanusethenutrientsobtainedtherebytocontinuetomatureeggs.Furthermore,likemanysynovigenicinsects,Aphytisspp.canreversetheallocationofnutrientstoreproductionbyresorbingoocytesduringtimesofmetabolicstress(Collier1995b;Heimpel&Rosenheim1995;Heimpeletal.1997).Speci¢-cally,weaskthefollowingquestions:(i)Doessynovigenyeliminatetheopportunitycostsofdepositingeggs(or,onthecontrary,doopportunitycostsremainbecauseofconstraintsontherateofeggmaturationandthecapacitytostoreeggs),and(ii)doestheabilitytoresorboocytesin£uencetherelativeimportanceoftimeversuseggcosts?2.METHODSWeuseadynamicoptimizationmodeltoanalysethecostofovipositioninA.aonidiae.Thismodelhasbeendescribedindetailelsewhere(Heimpeletal.1998),sowebeginwithonlyasynopsisofitsprimaryfeatures.Wethendescribehowthemodelwasmodi¢edtoestimatethetime-andegg-mediatedcostsofoviposition.Finally,weincorporatethedynamicsofeggresorp-tionintothemodeltoexploretheirin£uenceonthetrade-o¡betweencurrentandfuturereproduction.(a)ThedynamicoptimizationmodelAmodelofthefeedingandovipositionbehaviourofA.aonidiaewaspreviouslydevelopedtoexplorefactorslimitingthelifetimereproductivesuccessinthisminuteparasitoidwasp(Heimpeletal.1998).Thekeyfeaturesofthemodelareasfollows.Parasi-toidsemergeasadultswithbothmatureoocytesandproteinreservesderivedfromlarvalfeeding.Adultparasitoidsthensearchintheenvironmentforhosts,thearmouredscaleQuadraspidiotusperniciosus,uponwhichtheycanfeed(toaugmenttheirproteinreserves,whichareusedtomatureadditionaleggsandforsomaticmaintenance)oroviposit(garneringreproduc-tivesuccess).(Notethatamodelwithmoreparameterswouldbeneededforaparasitoidthatfeedsononesetofhostsandovipositsonadi¡erentsetofhosts.)Hostencounterisrepre-sentedasastochasticprocess.Hostsexistinthreequalityclassesde¢nedbythenumberofeggsadaughterdevelopingonthathostwouldcarryatemergence(7,10and12eggs,respectively;wewillrefertotheseas`grand-eggs').Mortality,dueentirelytopredation,isalsorepresentedasastochasticprocess.Themodelfollowsthelifetimeofafemaleparasitoid,calculatingtheoptimalbehaviourateachtimestepasafunctionoftheparasi-toid'sage,proteinreservesandsupplyofmatureeggs(`eggload').Themodelalsocalculatestheexpectationoffuturerepro-ductioninunitsofgrand-eggsproduced,F(x,y,t,T,d),forfemaleswithxeggsandyunitsofproteinreservesatagiventime-step,t,ondayd,whereTisthemaximumfemalelong-evity.Parametervaluesdescribingecologicalprocessesweremeasuredin¢eldstudies(Heimpeletal.1996;Heimpel&Rosenheim1998)andparametersdescribingphysiologicalprocessesweremeasuredinlaboratorystudiesofacongenericspecies,Aphytismelinus(Collier1995b;Heimpel&Rosenheim1995;Heimpeletal.1997).Hereweadoptthecentralestimatesofallparametervalues(seeHeimpeletal.1998)asourbasesetofparameters(table1).Theeggloadandprotein-reservelevelsofnewlyemergedadultA.aonidiaearenotknown.AsdiscussedinHeimpeletal.(1998),simulationsinwhichinitialeggloadsweredistributeduniformlybetween0and10(themaximumeggcapacity)producedanegg-loaddistributionthatcloselyapproximatedthedistributionobservedinthe¢eld,soweagainadoptthisassumptionhere.Initialproteinreservesweresetat15minustheinitial-egg-loadtore£ecttheobservationthatadultparasitoidscanmatureapproxi-mately15totaleggswithoutanyadditionalproteinmeals(Heimpeletal.1997;see}2(c)).Althoughthereissomeuncertaintyregardingtheegg-loaddistributionatemergence,theegg-loaddistributionsbecomelesssensitivetoinitialassumptionsastheparasitoidsforageoverthecourseofafewdays;thus,wereportresultsforthe¢rstovipositionofthethirddayoftheparasitoid'slife(see½2(b)).Thequalitativeresultsofthemodelare,however,extremelyrobusttowhichovipositioneventisexamined.(b)CalculatingtheopportunitycostsoftimeandeggsA.aonidiaegenerallydepositsasingleeggperhostattacked,andovipositionrequiresanaverageofca.10min(twotime-stepsinthemodel).Toinspectandrejectahostofmarginalqualityrequiresanaverageofca.5min.Thus,eachhostthatisacceptedincursopportunitycostsofoneeggand5min(thedi¡erencebetweenhostacceptanceandrejectiontimes).Thedynamicopti-mizationmodelcanbeusedtotranslatethesetwocostsintotermsofforegonefuture¢tnessreturns,bycomparingappropriatevaluesofF(x,y,t,T,d).Thiswasdonewithacomputer`experi-ment',inwhichthreetreatmentswereestablishedforfemalepara-sitoidsthatwereabouttoacceptahost.Ignoringforamomentthechangesineggloadandproteinreservesduetoeggmatura-tionand/orresorption(whicharetreatedin½2(c)),femalesinthe`control'groupperformedanormaloviposition,whichchangestheexpectationoffuture¢tnessreturnsfromF(x,y,t,T,d)to(e72·)£F(x71,y,t+2,T,d).The¢rstterminthisexpressionis 1566J.A.RosenheimandothersThecostlinessoftransientegglimitationProc.R.Soc.Lond.B(2000) theprobabilityofavoidingpredationduringtwotime-steps(·isthepredationrate).Femalesinthe`notimecost'treatmentexperi-encedthenormaleggcostofoviposition(oneegg)butdidnotincurthetimecost;thustheirfutureexpectationof¢tnessreturnsafterovipositionwas(e7·)£F(x71,y,t+1,T,d).Femalesinthe`noeggcost'treatmentexperiencedthenormaltimecostofovipo-sition(anextra5min)butdidnotincurtheeggcost;thustheirfutureexpectationof¢tnessreturnsafterovipositionwas(e72·)£F(x,y,t+2,T,d).Forthebaseparameterset,these`treat-ments'wereappliedtofemalespreparingtoaccepttheir¢rsthostontheirthirddayofforaging.Thedistributionsoffemaleage,eggloadandproteinreservesforfemalesencounteringthe¢rsthostonthethirddayofforagingwereobtainedwithaMonteCarlosimulationinwhichthephysiologicalstatesoffemales(1000perreplicate;nˆ5replicateruns)thatexpressedtheoptimalbeha-viouridenti¢edbythedynamicmodelwerefollowedovertheirlifetimes(seeMangel&Clark1988;Rosenheim1999b).TheMonteCarlosimulationusedparametervaluesidenticaltothoseusedinthedynamicoptimizationmodel.Timecostcouldthenbecalculatedasthedi¡erencebetweenexpectedfuturereproductioninthe`notimecost'treatmentandthe`control'treatment,andeggcostcouldbecalculatedasthedi¡erencebetweenthe`noeggcost'treatmentandthe`control'treatment.(c)OocytematurationandresorptionAphytisspp.parasitoidsare£exibleintheirallocationofmeta-bolicresourcesbetweenthefunctionsofsomaticmaintenanceandoocytematuration.Thehostscaleinsectisthesolefoodresourceforthedevelopingparasitoidlarva,andlarvaestoreproteinsandothernutrients,whichcansubsequentlybeusedduringtheadultstagetomatureapproximately15eggswithoutanyadditionalproteinmeals.Theadultparasitoidmayhaveaccesstotwoprimarytypesoffoodsintheenvironment.First,adultsmayfeedonsugar-richfoods,including£oralnectar,extra£oralnectar,orhoneydew.Sugarssupportsubstantialadultlongevity,suggestingthatmostoftherequirementsforsomaticmaintenancearemetbysugars,butcarbohydratesareinsu¤-cientforeggmaturation.Carbohydrate-richfoodsmaybeabun-dantinsomehabitatsbutscarceorinaccessibleinothers(Jervisetal.1996).Second,adultfemalesmayfeedonhostscaleinsects(`hostfeeding')byprobingthescalewiththeovipositorandthendrinkingthehaemolymphthatexudesfromthepuncturesite.Hostfeedingprovidesadultparasitoidswithaprotein-richmeal,thenutrientsfromwhichsupportongoingeggmaturation.Hostfeedingalsoextendslongevitybeyondthatobservedonadietrichinsugarsonly,suggestingthatsomeaspectsofsomaticmaintenancerequiretheexpenditureofprotein.Hostinsectsmaybeabundantinsomeenvironments,providingessentiallyunlimitedproteinresources.However,inenvironmentswherehostsarerare,proteinreservesmaydwindleunderthedualdemandsofsomaticmaintenanceandeggmaturation.Inthesecases,femalescanhalteggmaturationandresorbeggstoreclaimproteinsandothernutrientsneededforsomaticmainte-nance.Protein-starvedAphytisadultsresorbeggsuntiltheireggsupplyisexhausted,anddeaththenrapidlyensues(Collier1995b);thisobservationforAphytissupportsthegenerallyheld(butdi¤culttotest)viewthatoneofthekeyfunctionsofoosorptionistoavertstarvationduringtimesofnutrientstress(Bell&Bohm1975;Boggs&Ross1993;Ohgushi1996).Insomeinsects,resorptionmayalsoservetomaintainaconstantsupplyoffreshlymaturedeggs(e.g.Rivero-Lynch&Godfray1997)butwedonotexaminethisfunctioninthisstudy.Weexploredthreescenariosfornutrientdynamics(table1).(i)Noeggresorption.Thisscenariowasincludedasapointofcomparisononly,giventhattheabilitytoresorbeggsappearstobewidespreadamonghighlysynovigenicinsects(Bell&Bohm1975;Boggs&Ross1993;Ohgushi1996; ThecostlinessoftransientegglimitationJ.A.Rosenheimandothers1567Proc.R.Soc.Lond.B(2000) Table1.ModelparametersdescribingthedynamicsofeggmaturationandresorptionintheparasitoidA.aonidiae(Scenario(i)(noeggresorption)isincludedonlyasapointofreference.Scenario(ii)(sloweggresorption)isappropriateforpopulationsthatconsumesugar-richfoodsasadults,andthereforecanusesugarstosupportmostoftheirsomaticmaintenancerequirements.Scenario(iii)(rapideggresorption)isappropriateforpopulations,liketheonestudiedinaCaliforniaalmondorchard(Heimpeletal.1998),thatdonotfeedonsugars,andthereforemustuseproteinreserves(pr)tosupportmoreofthecostsofsomaticmaintenance.)parameterestimateallscenariosmeggsmaturedpertime-step0.011preggproteinreservesusedpertime-stepforeggmaturation0.00878scenario(i):noeggresorptionprsomaproteinreservesusedpertime-stepforsomaticmaintenance0.00222scenario(ii):sloweggresorptionprsomaproteinreservesusedpertime-stepforsomaticmaintenance0.00222prthreshthresholdlevelofproteinreservesbelowwhicheggmaturationceasesandeggresorptionbegins2.0reggsresorbedpertime-step0.00347prresproteinreservesaccruedpertime-stepfromeggresorption0.00222scenario(iii):fasteggresorptionprsomaproteinreservesusedpertime-stepforsomaticmaintenance0.0148prthreshthresholdlevelofproteinreservesbelowwhicheggmaturationceasesandeggresorptionbegins4.0reggsresorbedpertime-step0.0232prresproteinreservesaccruedpertime-stepfromeggresorption0.0148 Lopez-Guerrero1996).Eggmaturationoccurredatratesobservedinlaboratoryand¢eldstudies(Collier1995b;Heimpeletal.1997;Casasetal.2000;table1).Oneunitofstoredproteinwassu¤cienttomatureoneegg(aneggwasassumedtocontain0.8unitsofprotein)andtoful¢ltheproteindemandsofsomaticmaintenanceincurredoverthetimerequiredtomatureoneegg(0.2unitsofprotein).Eggmaturationcontinuedregardlessofproteinreservesoreggloads.(ii)Carbohydrate-richfoodspresent;sloweggresorption.Whenparasitoidpopulationshaveampleaccesstosugar-richfoods,oosorptionoccursslowly(approximatelyoneeggperday)whenfemalesareproteinstarved(Collier1995b;Heimpel&Rosenheim1995;Heimpeletal.1997;table1).Weassumethatparasitoidsmatureeggswhenproteinreservesareaboveathreshold(whichwesetattwounitsofprotein)andceaseeggmaturationandinitiateeggresorptionbelowthisthreshold.Parasitoidsstarvetodeathiftheirproteinreservesfallbelowoneunit.Weassumethattherecoveryofproteinfromresorbedeggsis80%e¤cient(i.e.theeggyields0.64unitsofprotein)andthattheobservedrateofeggresorptionprovidesproteinresourcesthatsatisfymetabolicdemands.AlthoughthisscenarioisnotappropriateforthepopulationofA.aonidiaethatwestudied,becausetheyapparentlydidnothaveaccesstosugar-richfoodsinthe¢eld,itshoulddescribetheovariandynamicsofotherAphytispopulationsthatfeedasadultsonsugaryfoods.Wenote,however,thatbecausethephysiologyofeggresorptionisstillpoorlyunderstood,aspectsofourdepictionofresorptioninthemodel(e.g.thethresholdsforinitiationofresorptionandthee¤ciencyofnutrientrecovery)arenecessarilysomewhatspeculative.(iii)Carbohydrate-richfoodsabsent;rapideggresorption.WhenAphytisspp.cannotconsumesugar-richfoods,theyresorbeggsrapidly(approximately6.7eggsday71;Heimpeletal.1997)tostayalive.DirectobservationsandbiochemicalassaysofA.aonidiaeforagingonalmondtreessuggestthattheseparasitoidsareunableto¢ndsugar-richfoodsintheirenvironment(Heimpeletal.1998;G.E.Heimpel,unpublisheddata).Therefore,thisscenarioistheonethatbestdescribesourfocalpopulation.Thee¤ciencyofproteinrecoverywasmaintainedat80%.Thethresholdlevelatwhicheggmaturationceasedandresorptionbeganwasraisedtofourunitsofprotein(sothatfemaleswouldnotneedtoswitchfromeggmaturationtooosorptionduringasinglenight-timerestingperiod).Inallscenarios,eggmaturationorresorptionoccurredduringbothdayandnighthoursandeggsmaturedinexcessofabdominalcapacity(teneggs)wereassumedtobelost.3.RESULTS(a)Modelwithouteggresorption:baseparametersetfortheobserved¢eldpopulationThebaseparametersetre£ectedakeyfeatureoftheecologyoftheobservedA.aonidiaepopulation:therateofhostencounter(1.00hosth¡1)wassubstantiallyinexcessoftherateofeggmaturation(0.132eggsh¡1).Mostoftheencounteredhostswereacceptedforoviposition,leadingtoasubstantialfrequencyoftransientegglimitation:manyfemalesexhaustedtheirsuppliesofmatureoocytesduringeachday'sforagingperiodandmaturedadditionaloocytesduringtheovernightrestingperiod(Heimpeletal.1998).Undertheseconditions,andassumingthatthereisnoopportunitytoresorbeggs,thetotalcostofovipositionishigh(4.92§0.03grand-eggs;¢gure1a)andaverylargefractionofthistotalcostiscontributedbythecostoftheegg(97.56§0.04%;¢gure1b).Thisisnottosaythatnofemalesweretimelimited;becausepreda-tionrateswerehigh(Heimpeletal.1997),somefemaleswerekilledbeforetheycouldexhausttheireggsupply.Nevertheless,timecostscontributedonlytheremaining2.44%ofthetotalcostofoviposition.Underthesecondi-tionsfemalereproductivesuccessisstronglyconstrainedbyeggsupply,thustheopportunitycostsofdepositinganeggarehigh.Eggcoststhusappeartobemuchmoreimportantthantimecostsforthe¢eldpopulationofA.aonidiaethatwasstudiedinCalifornia.Thisresultfromthedynamicoptimizationmodelreinforcesandextendstheresultofasimpler,analyticalmodel(Rosenheim1999a).Optimizationmodelsthatconsideronlytime-mediatedcostsofoviposition,includingmanyrate-maximizationmodels,wouldnotbeappropriateforanalysingthereproductivebehaviourofthisparasitoid(b)Modelwithouteggresorption:sensitivityanalysisforhostdensityParasitoidsintheobservedpopulationforagedinanalmondorchardwithamoderatelyhighdensityofscaleinsecthosts(Heimpel&Rosenheim1998).BecausepreviousmodelshaveemphasizedtheimportanceofhostdensityindeterminingtherelativeimportanceofeggversustimecostsandbecausemanyalmondorchardsharbourmuchlowerdensitiesofthehostscaleinsectQ.perniciosus(J.A.Rosenheim,personalobservation),weperformedasensitivityanalysisinwhichtherateofhostencounterwasvaried.Boththetotalcostofovipositionandtheproportionalcontributionofeggcoststotheoverallcostofovipositiondecreasedashostencountersbecamelessfrequent(¢gure1a,b).Thisresultparallelsthatobtainedforpro-ovigenicinsects(Rosenheim1999b).Whenhostsareabundant,eggsbecomethelimitingresourceandeggcoststhereforedominatethecostofoviposition.Thetotalcostofovipositionishigh,andthereforeinsectsarepredictedtobehighlyselectiveinchoosinghosts(Iwasaetal.1984;Mangel1989).Whenhostsarerare,timeto¢ndhostsbecomesthelimitingresource,andtimethereforedominatesthecostofovi-position,atleastinthissimplemodelwithouteggresorp-tion.Thetotalcostofovipositiondecreaseswhenhostsarerare,andthereforeinsectsarepredictedtobemorecatholicinhostacceptance.(c)ModelwitheggresorptionThein£uenceofeggresorptiononthecostofovipositionvariedwithhostavailability(¢gure1).Atveryhighhostdensities,neitherthetotalcostofovipositionnortheproportionalcontributionsofeggandtimecostsweresensitivetotheinclusionofeggresorptioninthemodel.Thisisnotsurprisingbecausewhenhostsareabundanthostfeedingopportunitiesarealsoabundant,andthere-foreproteinreservesdonotfallbelowthethresholdatwhichresorptionisinitiated.However,whenhostsarescarce,theinclusionofeggresorptioninthemodel 1568J.A.RosenheimandothersThecostlinessoftransientegglimitationProc.R.Soc.Lond.B(2000) elevatedthetotalcostofovipositionandhadadramaticin£uenceontherelativeimportanceofeggandtimecosts.Whyisthisresultobserved?Hastheinclusionofeggresorptionsomehowchangedthefundamentalchallengefacedbyparasitoidsthatmustspendtimeinextensivesearchingforrarehosts?No.Eggresorptioninsteadallowsparasitoidstotranslateeggresourcesintoaddi-tionalsearchtime.Theproteinthatcanberecoveredfromasingleeggthroughresorption(0.64unitsofprotein)representsasubstantialamountofsearchtime(uptoamaximumof43time-steps,or3.6hwhenparasi-toidsaresugarstarved,and288time-steps,or24hwhenparasitoidscanfeedonsugars).Thus,theopportunitycostsassociatedwithdepositinganeggcanbelargeiftheeggwouldotherwisesupportadditionalsearchtime.Theamountoftimeatstakeislargerelativetotheimmedi-atelyincurredcostofthe5.0minrequiredtodeposittheegg.Acloserexaminationofthemodeloutputcanhelptoexplainwhyslowoosorptionhadamoremodestin£uenceonthecostofovipositionthandidfastoosorption.The¢eldpopulationofA.aonidiaethatwestudiedinCali-forniawassubjecttointensepredationpressuresfromacomplexofgeneralistpredators(Heimpeletal.1997),thus,expectedlongevitieswererelativelyshort(1.3days).Underscenario(ii),parasitoidshaveaccesstosugar-richfoods;therefore,metabolicdemandsplacedonproteinreservesaremodest.Undertheseconditions,evenifopportunitiestohostfeedarerare,proteinreservestakeseveraldaystodwindletothedangerouslylowlevelsatwhicheggresorptionisinitiated(¢gure2a).Forexample,aparasitoidthatemergeswithanaverageproteinreserve,tenunits,andfailstosecureanyhost-feedingmealsstillhasenoughproteintosupporteggmaturationandsomaticmaintenancefor2.53daysbeforeshedrawsherproteinreservesdowntothethresholdatwhichresorp-tionbegins(twoproteinunits).Eveninfrequenthost-feedingmealswilldelaytheonsetofeggresorptionfurther.Furthermore,eggresorptionmustnotonlybeinitiatedbutmustcontinueforlongenoughthattheeggsupplycanactuallybeexhaustedbeforethebulkoftheopportunitycostofdepositinganeggis¢nallyrealized.Femaleswithaccesstosugarsresorbeggsslowly(approxi-matelyoneeggday¡1),thus,eggloadisdrawndowngradually(¢gure2b).Thus,whenpredationpressureisintenseanddemandsonproteinresourcesarelight,fewindividualslivelongenoughtoinitiateeggresorptionandproduceasigni¢cantriskofoosorption-inducedegglimitation(¢gure2c).Thereforeeggresorptionhasarela-tivelysmallin£uenceonthecostofovipositionwhenparasitoidshaveaccesstosugar-richfoodsandoosorptionisthereforeslow.Whenparasitoidsaresugarstarved,however,themetabolicdemandsmadebythesomaonproteinreservesareintense.Proteinreservescannowbedepletedmorequickly(¢gure2a).Aparasitoidemergingwithtenunitsofproteincannowreachthethresholdatwhicheggresorptionisinitiated(fourproteinunits)in0.88days,andtherapidoosorption(6.67eggsday¡1)thatensueswhenreservesreachdangerouslylowlevelscanquicklyleadtooosorption-inducedegglimitation(¢gure2b,c).Thus,whenhostdensitiesdeclinetolevelsatwhichhostfeedingcannotmaintainproteinreserves,manyfemalesresorballtheireggsandstarvetodeathbeforetheyarekilledbypredators,andeggcostsarethereforehigh.Thedetailsoftheresultsdisplayedin¢gure1are,therefore,sensitivetothepotentialforfemalelongevity,opportunitiesforfemalestofeedandoviposit,andthemagnitudeofproteindemandsforeggmaturationandsomaticmaintenance.Ourgeneralconclusion,however,isthatwhenfemalesmustresorbeggstoavoidstarvation,eggresourcesbecomecritical,andthereforetheegg-mediatedcostscandominatethecostofoviposition. ThecostlinessoftransientegglimitationJ.A.Rosenheimandothers1569Proc.R.Soc.Lond.B(2000) 10.80.20.40.600.1(b)0.01host availability (probability of hostencounter in 5 min of search) e g g - m e d i a t e d c o s t o f o v i p o s i t i o n ( p r o p o r t i o n o f t o t a l ) 0.001 6240(a) t o t a l c o s t o f o v i p o s i t i o n no oosorptionslow oosorptionfast oosorption Figure1.In£uenceofhostavailabilityonthetotalcostofovipositionandtheproportionofthetotalcostthatiscontributedbytheeggcost.Hostavailabilityismeasuredastheprobabilityofencounteringahostduringasingle5-mintime-step;theverticallineindicatesthelevelofhostavailabilityobservedinthe¢eld(probabilityofhostencounterduring5minofsearchˆ0.08).(a)Totalcostofoviposition,measuredintermsofthenumberofeggscarriedbytheemergingadulto¡springofthefocalfemale(`grand-eggs').Toputtheabsolutevaluesofthesecostsintoperspective,notethattheexpected`bene¢t'ofovipositiononalow-qualityhostequalstheproductoftheprobabilitythatthedepositedeggwilldevelopsuccessfullytotheadultstage(0.61)andtheexpectedfecundityoftheresultingdaughter(7.0),or4.27grand-eggs.Theexpectedbene¢tsofovipositingonamedium-andhigh-qualityhostare6.1and7.32grand-eggs,respectively.(b)Theproportionalcontributionofeggcoststothetotalcostofoviposition(theremainingproportioniscontributedbythetimecostsofoviposition). Becauseoosorptionisageneralfeatureofsynovigenicinsects,itappearslikelythateggcostsmakeasubstantialcontributiontotheoverallcostofoviposition,evenwhenhostsarerare.4.DISCUSSIONWedrawtwoprimaryconclusionsfromouranalysis.First,althoughtheparasitoidA.aonidiaecancontinuetomatureeggsasanadult,the¢nitemaximumrateofeggmaturationstillmeansthattransientegglimitationcanoccurwhenhosts,andthereforeopportunitiestooviposit,areabundant.Whentheeggsupplyistempora-rilyexhausted,femalesmusthaltreproductiontoawaitthematurationofadditionaleggs.InourmodelofA.aonidiae,ahaltinreproductionimposesacost,becausethereisariskofmortalityduringthewaitingperiod.Moregenerally,ahaltinreproductioniscostlybecauseofimmediaterisksofmortality,theprogressionofsenescenceand,insomecases,lossofopportunitiestoovipositonhostresourcesthatareavailableonlyforashorttime.Thus,ashasbeenemphasizedbyotherauthors,whereasthemostfundamentalconstraintactingonthelifetimereproductivesuccessofpro-ovigenicspeciesisthe¢xedtotalnumberofeggsthattheycarryasanewlyemergedadult,themostfundamentalconstraintactingonasynovigenicspeciesistheirmaximumrateofoocytematuration(Charnov&Skinner1988;Rosenheim1996;Casasetal.2000).Bothoftheseconstraintsmeanthatthereisariskofoviposi-tion-mediatedegglimitation,whichispermanentinthecaseofapro-ovigenicspeciesbutpotentiallytransientinthecaseofasynovigenicspecies.Second,theabilityofsynovigenicspeciestoreversethe£owofnutrientsfromthesomatooocyteshasadramaticin£uenceonthecostofoviposition.Whereasfemalesinhost-richenvironmentsmayencounteroviposition-mediatedegglimitation,femalesinhost-poorenviron-mentsmayencounteroosorption-mediatedegglimitation.Bothformsofegglimitationarecostly.Theresorptionofeggsallowsfemalestosupporttheirbasicmetabolicrequirements,therebytranslatingeggresourcesintoaddi-tionalsearchtime.Thesearchtimegainedfromresorbinganeggmaybelargecomparedtothetimecostsasso-ciatedwithdepositinganegg;ovipositiontimerequire-mentsaregenerallysmall(typicallyintheorderofsecondstominutes),whereaseggsareoftenprovisionedwithabundantnutrients,sothataresorbedeggcansupportthefemale'smetabolicdemandsforasigni¢cantlengthoftime(typicallyintheorderofhourstodays)(Godfray1994;Rosenheim1999a).Eggsarethereforeavaluableresourceevenwhenhostsarerare,becausefemaleswhoresorbtheirentiresupplyofeggsfaceimmi-nentdeathduetostarvation.Eggs,therefore,appeartomakeimportantcontribu-tionstotheoverallcostofovipositionforhighlysynovi-genicinsects,justastheydoforstrictlypro-ovigenicinsects.Contrarytoinitialexpectations,the£exibilityofresourceallocationthattypi¢essynovigenicreproductionactuallyappearstobroadentherangeofconditionsunderwhichcostlyegglimitationcanoccur.Whereasforpro-ovigenicinsectseggcostspredominateonlywhenhostsareabundant,forsynovigenicinsectseggcostsmaypredominatewhenhostsareabundantorrare.Eggcostsappeartobefundamentalinmediatingthetrade-o¡betweencurrentandfuturereproduction,andarethusbasictotheunderstandingofwhyinsectsarechoosyaboutwheretheyoviposit. 1570J.A.RosenheimandothersThecostlinessoftransientegglimitationProc.R.Soc.Lond.B(2000) 10.80.40.20.60987time (days) p r o p o r t i o n e g g l e s s 1 6 5 4 3(c) 2 1084260 e g g l o a d (b) 10842fast oosorptionslow oosorption60 p r o t e i n (a) Figure2.In£uenceofslowversusfastoosorptionon(a)theproteinreserves,(b)eggloadsand(c)proportionoffemaleswhohaveexhaustedtheirsupplyofmatureoocytes.DataarefromMonteCarlosimulations(1000femaleparasitoidssimulatedperreplicate;nˆ5replicateruns)offemaleA.aonidiaethatexpressedtheoptimalbehaviouridenti¢edbythedynamicmodel.Thesimulationsusedthebaseparameterset(seeHeimpeletal.1998;table1)exceptthathostavailability(theprobabilityof¢ndingahostduringa5-mintime-step)wassetat0.005,avaluethatiswellbelowthevalueobservedinthe¢eld(0.08).Atthislowlevelofhostavailability,host-feedingoppor-tunitiesarerare,andeggresorptionmaythereforeoccurtosatisfymetabolicdemands.Whenparasitoidscanfeedonsugar-richfoodsintheenvironment,oosorptionisinitiatedwhenproteinreservesfalltotwounits,andoosorptionisslow(scenario(ii)intable1);whensugar-richfoodsareabsent,oosorptionisinitiatedwhenproteinreservesfalltofourunits,andoosorptionisfast(scenario(iii)intable1).Shownaremeans§s.e.m. (a)Egg-loaddynamicsintwohighlysynovigenicHowgeneralizableisourresultthatahighlysyno-vigenicspeciesmaystillfaceacostlyriskofexperiencingtransientegglimitationinthe¢eld?AlthoughwefeelthatA.aonidiaeexhibitstraitsthataretypicalofhighlysyno-vigenicinsects,additionalcasestudieswouldcertainlyhelpustoassessthegeneralityofabasicconstraintimposedbythemaximumrateofeggmaturation.Tworecentlycollecteddatasetsprovideusefulinsights.Casasetal.(2000)studieda¢eldpopulationofanotherAphytisspecies,Aphytismelinus.Simplebutingeniousmanipulationsshowedthatduringtheperiodofactiveforaging(10.00^16.00)therateofeggmaturation(measuredundersemi-¢eldconditions)was0.25eggsh¡1,whereastherateofovipositionwas0.58eggsh¡1.Thus,justaswasobservedforA.aonidiae,therateofovipositiongreatlyexceededtherateofeggmaturation,andtheresultwasthatasubstantialfraction(theyestimatedbetweenone-thirdandone-halfofallfemales)experi-encedegglimitationatsometimeeachday.Thedistribu-tionofeggloadsforfemalescollectedattheendofthedailyforagingperiodcon¢rmedthisinference:manyfemaleshadnomatureoocytesintheirovaries.Theiranalysisalsosuggestedthatasfemalesdepletedtheireggsupply,theyslowedtheirrateofoviposition,apatternthathasbeenobservedforAphytisspp.inthelaboratory(Rosenheim&Rosen1991;Heimpel&Rosenheim1995)and¢eld(Heimpeletal.1996)andthatispredictedbyoptimalitymodels(Mangel1987).Althoughacouplingoftherateofovipositionwitheggloadcancertainlyreducethelikelihoodofcompletelyexhaustingtheeggsupply,itappearsnottoeliminatethispossibility(Mangel&Heimpel1998;Rosenheim1999b).A¢eldexperimentbyK.R.Hopper(personalcommu-nication)showed,however,thatapopulationoftheaphidparasitoidAphelinusasychisexhibitednoegglimitation:noneofthe92sampledfemaleshadexhaustedtheirsupplyofeggs.Themodaleggloadwas14,whichisapproximatelythemaximumeggloadforthisspecies,andonlyonefemalehadasfewastwomatureoocytes.Thus,forthefemalesinthispopulation,eggmaturationappearstohavebeenmorethanadequatetoo¡setovipo-sitionandoosorption.Theavailabilityofhostsandhoneydew,asugar-richfood,tofemaleparasitoidsinthispopulationprovidesacontextforunderstandingthisresult.Theparasitoidswereforagingina¢eldwhoseaphidpopulationhadrecentlydeclinedfromhighlevels.Thus,hosts,andhenceopportunitiestooviposit,wererelativelyrare(theestimatedtotalnumberofprogenyproducedperfemalewaspwasthreeto¢ve).Honeydewproducedbyaphidsduringtheearlierdenseaphidpopulationcanpersistonprotectedleafsurfaces(K.R.Hopper,personalcommunication),sothatfemaleshadampleaccesstosugarmeals.Inthelaboratory,femalesheldwithouthostsbutwithaccesstohoneyshowedlittlechangeineggloadfor¢vedays,andeggloaddeclinedonlymodestly,fromanaverageoftwelveeggstoeighteggs,overthenexttendays(Sanchez1994).Inthisspecies,eggresorptionmayoccuratthesametimeaseggmaturationiffemalesareheldwithouthosts;inthestudied¢eldpopulation,however,theremayhavebeenlittleornonetdeclineineggloadduetoresorptionbecausefemaleshadaccesstobothhoneydewandaphidsuponwhichtheycouldhostfeedtoreplenishproteinreserves.Thus,thispopulationofA.asychistheimportanceofunderstandinghowlocalecologicalconditions,includingtheavailabilityofhostsandnon-hostfoods,interactwithparasitoidphysiologytodeter-minelevelsofegglimitation.Papaj(2000)hasarguedcogentlythatmodelsthattreattherateofeggmaturationasaconstantareoverlookinganimportantaspectofinsectbiology,namelyplasticityinthelevelofvitellogenicactivity.Weconcur.Althoughwehaveattemptedtoincorporatesome£exibilityofovariandynamicsintoourmodelbyincorporatingbotheggmaturationandresorption,westillsimplifyovarianfunc-tionbytreatingeggmaturationasaone-speedprocess.However,wenotethatbothA.aonidiaeandA.melinusdisplayedhighlevelsofegglimitation(Heimpeletal.1996;Heimpel&Rosenheim1998;Casasetal.2000);thus,ourexpectationisthattheseparasitoidsweredisplayingtheirmaximumattainablerateofeggproductionfortheenvir-onmentalconditionsthattheyexperienced.Itappears,then,thattheseparasitoidpopulationsexperienceafunda-mentalphysiologicalconstraint,onewhichtheyareincap-ableofcircumventingthroughshort-termmetabolicadjustments.Populationssubjecttosuchintenselossesofreproductiveopportunityduetoegglimitationmightbeexpectedtorespondoveralongertime-framethroughevolutionofincreasedfecundityoracceleratedeggmatura-tion(Rosenheim1996;Sevensteretal.1998).(b)TransientversuspermanentegglimitationinsynovigenicinsectsAfactorthathasastrongin£uenceontherateofeggmaturationinsynovigenicfemalesisage.Asfemalesage,theirrateofeggmaturationgenerallydeclines(e.g.Shirotaetal.1983;Ho¡mannetal.1995;Boggs1997b);whetherthisdegradationofovarianfunctionincreasesthelikelihoodofexhaustingtheeggsupplydependsontheextenttowhichsenescencemightalsodiminishtheabilityoffemalestoforagesuccessfullyforsuitableovipositionsites.Inmanyspeciesofherbivorousandparasiticinsects,vitellogenesisceasesentirelyinoldfemaleswhohaveexperiencedrichopportunitiestooviposit(e.g.Dunlap-Piankaetal.1977;Jervisetal.1994;Lopez-Guerrero1996).Thus,highlysynovigenicspecies,incommonwithpro-ovigenicspecies,canexperienceapermanentformofegglimitation,whichwouldaugmenttheegg-mediatedcostofovipositionassociatedwithtransientegglimitation.Age-dependentdeclinesinovarianfunctionhavebeendocumentedinthelaboratory,andopportunitycostsofpermanentegglimitationhavebeenanalysedwithmodels(Rosenheim1999b),but¢eldstudiesofage-dependentchangesinfemaleforagingability,ovarianfunctionandlevelsofegglimitationareneededbeforetherelativeimportanceoftransientandpermanentegglimitationwillberesolvedforhighlysynovigenicspecies.(c)EnvironmentalheterogeneityandthefunctionofeggresorptionOurmodelunderscoresthevalueofeggsasasourceofnutrientsthatcanbeminedduringtimesofmetabolicstress.Wefeel,however,thatthetruevalueofeggresorption(andthereforethecostsassociatedwithegg ThecostlinessoftransientegglimitationJ.A.Rosenheimandothers1571Proc.R.Soc.Lond.B(2000) limitationduringtimesofnutrientstress)mayoftenbegreaterthanindicatedbyourmodel.Thereasonisthatourmodelassumesconstantenvironmentalconditions(i.e.constantavailabilityoffoodsandhosts),whereasnatureischaracterizedbybothtemporalandspatialheterogeneity.Afemalewhoexperiencesashortperiodofhostorfoodscarcity,andwhosubsequentlyexperiencesconditionsrichwithopportunitiestoreproduce,mayrealizeverylargeincreasesinlifetimereproductivesuccessifshecansurvivethroughtheperiodofscarcitybyresorbingeggs(e.g.Ohgushi1996).Additionalwork,includingperhapsboth¢eldstudiesandmodellinge¡orts,areneededtoexplorethispossibility.(d)Physiology,behaviouralecologyandlife-historyevolutionWeclosebyechoingapointrecentlyadvancedbySinervo&Svensson(1998)intheirstudiesofthecostofreproductioninvertebrates:adeeperunderstandingofreproductivebehaviourandthelong-termevolutionarytrajectoriesoflife-historytraitsislikelytoemergefromanenhancedunderstandingofthephysiologicalbasisofthecostofreproduction.Ourmodelhashighlightedtheimportanceofunderstandingnotonlytheecologyofreproductiveopportunity(e.g.theavailabilityofovi-positionsitesandfoodsinthelocalenvironment,andtheintensityofmortalityfactors)butalsothephysiologyofbi-directional£owsofproteinsandothercompoundsbetweenthesomaandthedevelopingoocytes.Mechan-isticstudiesofovariandynamics(e.g.Boggs1997a,b;Rivero&Casas1999a,b;Papaj2000)willcontributegreatlytoourunderstandingofinsectlife-historyevolution.Forhelpfulinputonanearlierdraftofthismanuscript,wethankJ.Casas,R.G.Colfer,K.R.Hopper,B.Inouye,E.H.Nelson,N.Underwoodandananonymousreviewer.J.A.R.thanksN.E.PierceandtheDepartmentofOrganismalandEvolutionaryBiology,HarvardUniversity,fortheirgracioushospitalityduringthepreparationofthemanuscript.ThisworkwassupportedinpartbyUSDAgrants9202357and9702217andUSDARegionalResearchProjectW-185.REFERENCESBell,W.J.&Bohm,M.K.1975Oosorptionininsects.Biol.Rev.50,373^396.Boggs,C.L.1997aReproductiveallocationfromreservesandincomeinbutter£yspecieswithdi¡eringadultdiets 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