T IS WELL KNOWN THAT NOT ALL BUTTERFLY SPECIES are equally acceptable food items to bird predators some are readily eaten while others may be rejected presumably due to their nasty taste Poulton 1902 Swynnerton 1915a b 1919 Chai 1986 General observa ID: 79141
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176DeVries E-mail:tmale@hawaii.edu BIOTROPICA34(1):176±1812002DifferentialWingToughnessinDistastefulandPalatableButter¯ies:DirectEvidenceSupportsUnpalatableTheoryKeywords:Nymphalidae;butter¯ypalatability;wingtoughness;wingpatterns;predatordefenses.TISWELLKNOWNTHATNOTALLBUTTERFLYSPECIESareequallyacceptablefooditemstobirdpredators;somearereadilyeaten,whileothersmayberejectedpresumablyduetotheirnastytaste(Poulton1902;Swynnerton1915a,b,1919;Chai1986).Generalobservationsshowthatpalatablebutter¯iestendtohavecrypticcolorationanddependuponrapid¯ighttoevadepredators,whereasdistastefulbutter¯iesminimizepredationbyadvertisingnoxiousqualitiesassociatedwithadistinctivecolorpatternandaslow¯ight(summarizedinTurner1984,1987;Chai1986,1996).Theseobservationsarecentraltounder-standingthefunctionofbutter¯ycolorationandbehavior,learningbybutter¯ypredators,andthetheoriesofunpalatabilityandmimicry(Marshall1902;Poulton1908;Eltringham1910;Swynnerton1915a,b,1919;Carpenter1932,1942;Brower1958a,b;Fisher1958;Turner1984;Bowersetal.Chai1986,1996).Thebasictheoryaccountingfortheevolutionofunpalatabilityandwarningcolorationrequiresthedifferentialsurvivalofsomeindividualbutter¯iesfollowingattacksandtastingbypredators,andthattheexperiencebememorabletopredators(Fisher1958).Asimpleextensionofunpalatabletheorysuggeststhatnaturalselectionshouldfavoraposematicphenotypespossessingaphysicaltoughnessthatmakesthemresistanttohandlingbypredators.Indeed,thefactthatbodiesofunpalatablebutter¯ytaxatendtobemoreresilienttohandlingthanpalatableoneshaslongbeenrecognizedbyentomologists(Poulton1908,Piepers&Snellen1909±1918,DeVries1987).Therefore,toughnessappearstobeanessentialcomponentofbutter¯ysurvivalfrombirdattacks;however,theonlystudyofdifferentialtoughnessamongpalatableandunpalatablebutter¯iesisthatofCarpenter(1941)showingthatthenumberofbeakmarksonunpalatablemuseumspecimenswassigni®cantlygreaterthanpalatableones.Fromthisstudy,heinferredthatunpalatablebutter¯iessurvivingbirdattackshadtougherwingsthanpalatableones,thusprovidingtheonlyempiricalevidenceinsupportoftoughnessasacorollaryofunpalatability.Thereisalargeanddiversebodyofliteratureexploringtheevolutionofbutter¯ycrypsis,unpalat-ability,mimicryandassociatedwingtraits,andbehaviors(Poulton1902;Blest1957;Robbins1981;Turner1984,1987;Wourms&Wasserman1985;Chai1986,1996;DeVries1987;Chai&Srygley1990;Srygley1994;Steppan1996;Beccaloni1997;DeVriesetal.1999;Mallet&Joron2000andreferencestherein).Consideringthebreadthofthisliterature,itisthereforesurprisingthatdifferentialwingtoughnessamongpalatableandunpalatablebutter¯ieshasneverbeenmeasureddirectly.Accord-ingly,thisstudyaskswhetherornotunpalatablebutter¯ieshavetougherwingsthanpalatableonesbyexperimentallyestimatingtheforcenecessarytotearthewingsofrepresentativeAfricanbutter¯ies. Received8September2000;revisionaccepted19January2001. Notes177Thestudywasconductedfrom12to25September1999,inthewesternUsambaraMountainsofnortheasternTanzaniaattheAmaniExperimentalFieldStation(5,38),whichhasalonghistoryofvarioushumanactivities(summarizedinIversen1991).Consequently,theareaaroundAmaniisMaesopsiseminiiEngl.(Rhamnaceae)plantation,secondgrowthforest(invadedextensivelybyM.eminii),otheragriculturalareas,teaplantations,andassociatedriparianedges.Fiveabundantandwidespreadnymphalidbutter¯ieswereselectedtorepresentpalatableorunpal-atablespecies.Palatabilitywasassessedonthebasisoftheirnaturalhistory,colorpattern,¯ightbehavior,taxonomicaf®nity,andassessmentbynaturalpredatorsofthe®vespeciesortheircloserelatives(Marshall1902;Swynnerton1915a,b;Carpenter1941;Ackery&Vane-Wright1984;Brower1984;Turner1984;Ackery1987,1988;Larsen1991).Basedonthesecriteria,allavailableevidencesuggestedthatJunoniatereaDrury(Nymphalinae)andBicyclussa®tzaHewitson(Satyrinae)representpalatablespeciesandAmaurisniaviusLinnaeus(Danainae),AcraeainsignisDistant,andA.johnstoniGodman(Acraeinae)representunpalatablespecies.Anexperimentalbirdbillwasfashionedfromasmallmetalelectricalclip(jaws10.0mmlong3.68mmwide).Asmallplasticweighingdishwastiedtotheendoftheclipoppositethejawswith6cmofsilkthread.Thisapparatusishereafterreferredtoastheclipassembly.Abutter¯ywaskilledbyapinchtothethorax,thenimmediatelysecuredinthejawsofawoodenclothespegthathadbeenattachedtoastiffwirerigidlysuspendedfromthecenterpostbelowthelegsofaphotographictripod.Allindividualsweresecuredwiththewingsclosedinanaturalrestingpositionsuchthattheclothespeggrippedallfourwings.Theclipassemblywasthencarefullyattachedtothehindwingdistalmarginsofthebutter¯ysuchthatthejawsgrippedthewingsbetweenveinsCuand2A,apositionthatcloselyapproximatesthatofbeakmarksmadebybirdsattackingrestingbutter¯ies(Carpenter1932,1937,1938,1941;DeVries,pers.obs.).Thecenterpostofthetripodwasthenraisedslowlyuntiltheweighingboatwasfreelysuspended20mmaboveareceptacle.Oncesuspended,suf®cientdrysandandsmallmetalweightswereslowlyaddedtotheweighingdishuntiltheentireassemblysuddenlytorefreeofthewingandfellintoacollectingreceptaclebelow.Theclipassemblyandalladditionalweightswerethenweighedtothenearest0.001gonamodelPB53Mettler-Toledoelectronicbalance.Thisweightestablishedtheforcenecessarytoteartheclipassemblyfreeofthehindwings,thusprovidingameasureofrelativewingtoughnessforeachindividualspecimen.Toavoidpotentialeffectsofwingconditiononmeasuresofrelativewingtoughness,noindividualbutter¯ytestedhadanywingdamageorfadedwingpatternsthatdenotedoldage;,allindividualshadentirewingmarginsandwereingoodcondition.BecauseforewinglengthisawidelyusedmeasureofbodysizeinLepidoptera(Dudley2000),thedistancefrombasetoapexofonewingwasmeasuredwithdialcaliperstothenearesttenthofamillimeterforallspecimenstoprovideanestimateofbodysizeforeachspecies.Differencesinwing-tearweightsandlengthsamongspeciesweretestedusingaone-wayANOVA.Thepotentialrelationshipbetweentearweightandwinglengthwastestedforeachspeciesusinglinearregression.Signi®cancelevelsformeanwingtearweightandlengthinpairedspeciescomparisonswereadjustedfornonindependenceusingthesequentialBonferroni-Dunnmethod(Rice1989).Wing-tearweightswereevaluatedusingaone-wayANOVAforpooledpalatableandunpalatablespecies.Meanwing-tearweightsdifferedsigni®cantlyamongtheindividualspecies(0.0001,df4),andtheranksbyspeciesshowedthatA.niaviushadthetoughestwings,followedbyA.insignis,thenA.johnstoni,whileB.sa®tzaJ.tereatiedfortheleasttoughwings(Fig.1a).Examinationofspeciespairsshowedthatthereweresigni®cantwing-tearweightdifferencesamongspecies(Table1a).Winglengthsdifferedamongspecies(Table1b)andthesedifferencesweresigni®cant,withthelargestA.niavius,included(0.0001,df4)orexcludedfromanalysis(0.0001,df3).Whenconsideredasagroup,unpalatablebutter¯ieshadgreatermeanwinglengthsthanpalatableones,bothwithA.niavius0.0001,df1)andwithoutit(0.0001,df1).Eventhoughthelargestspecies(A.niavius)hadthehighesttearweight(Fig.1),regressionanalysisshowednosigni®cantrelationshipbetweenwinglengthandtearweightamongspecies;allprobabilityvalueswerebetween0.8235and0.3397,andallvalueswerebetween0.003and0.070.Asagroup,unpalatablebutter¯ieshadsigni®cantlyhigherwing-tearweightsthanpalatableones(Fig. 178DeVries FIGURE1.Boxplotcomparisonsofwing-tearweights.Eachboxspansthe®rsttothirdquartile;themedianisshownasthehorizontallinewithineachbox;andtheverticalbarsextendtothemaximumandminimumvaluesofthesample.(A)Comparisonofwing-tearweightsforallspecies.Samplessizesareasfollows:AmaurisniaviusAcraeainsignisAcraeajohnstoniBicyclussa®tza22),andJunoniaterea18).(B)Comparisonofwing-tearweightsofallspeciesgroupedbypalatableandunpalatablecategories.(C)Comparisonofwing-tearweightsofpalatableandunpalatablespeciesexcludingthelargestspecies,A.niavius 1b,c),bothwhenthelargestspecies(A.niavius)wasincluded(0.0001,df1),andexcludedfromanalysis(0.001,df1).Whencomparingspeciespairs,tearweightsdifferedamongunpalatablebutter¯ies,butnotpalatableones(Table1a);however,itisofconsiderableinterestthatthewing-tearweightofA.johnstonidifferedfromotherunpalatablespeciesbutnotfromeitherpalatablespecies(Table1a).Ecologicalobservationsandbasicunpalatabilitytheoryforbutter¯iessuggestthataposematicspeciesshouldevolvephysicalattributesthatmakethemresistanttohandlingbypredators(Poulton1908,Fisher1958).Usingthefrequencyofbeak-markedmuseumspecimens,Carpenter(1941)inferredthatunpal-atablebutter¯iesweremoreresistanttobirdattacksthanpalatableones.Thepresentwork,however,providesthe®rstdirectexperimentalevidencethatsomeunpalatablebutter¯yspecieshavesigni®cantlytougherwingsthansympatricpalatablespecies(Fig.1b,c;Table1a).InconcertwithCarpenter(1941),thisstudysupportstheorybysuggestingthatatoughenedwingintegumentmaybeageneraltraitassociatedwiththeevolutionofdistastefulnessinbutter¯ies.Theobviousnextstepwillbetotestthephylogeneticrelationshipbetweenthesetraitsthroughalargecomparativestudythatexploresawiderangeofbutter¯ywinglengths,includingtheeffectsof¯exuralstiffness(Steppan1996).Birdseatadultbutter¯iesandalmostcertainlyin¯uencetheevolutionofbutter¯ywingtraits(Poulton1902;Carpenter1932,1937,1938;Brower1958a,b;Wourms&Wasserman1985;Chai1986,1996).Twoobservationsmakeitlikelythattheexperimentalmethodsusedinthisstudysimulatedwingdamagein¯ictedbyanaturalbirdbill.First,theexperimentalclipassemblyusedhereapproximatedthebillsizesoffourspeciesofAmanibulbulsknowntoeatbutter¯ies:AndropadusgracilisA.masukuensisShelley,A.milanjensisShelley,andA.nigricepsShelley(Pycnonotidae).Second,theformofwingdamagein¯ictedexperimentallycloselyresembleddamageknowntoresultfrombirdattacksinthewild(DeVries,pers.obs.;seealsoillustrationsinCarpenter1932,1937). Notes179 TABLE1.(A)Wing-teardifferencesamongspeciespairs.(B)Winglengthdifferencesamongspeciespairs.Bonferroni-Dunncomparisonsaresigni®cantat0.005.Abbreviations:*signi®cant;NSnotsigni®cant. MeanwingCriticaldifferenceSigni®cance tereatereatereatereatereatereatereaterea AvailableevidencesuggeststhatallspeciesofAfricanAcraeaareunpalatable(Eltringham1910,1912;Swynnerton1915b,1919;Owen1971;Nahrstedt&Davis1981;Pierre1984).Inhisreviewofnym-phalidhostplants,Ackery(1988)foundtwomajorhostplantthemesthatre¯ectthecladisticanalysisAcraeabyPierre(1984)ÐageneralViolalesfeedinggroupandanUrticalesfeedinggroup.AlthoughAcraeaaresuspectedtocontaincyanidecompounds(Owen1971,Nahrstedt&Davis1981),Ackery(1988)notedthatonlyspeciesfromtheViolalesfeedinggrouptestedpositiveforcyanideproduction;howevernonefromtheUrticalesgrouphadbeenexamined.OneresultfromthisstudysuggeststhatassessingpalatabilitywithinAcraeamaybemorecomplexthanpreviouslythought.ThespeciesexaminedhererepresentbothfeedinggroupsÐA.insignisonViolalesA.johnstonionUrticales.Wingtoughness,however,differedbetweenA.insignisA.johnstonibutnotbetweenA.johnstoniandthepalatablespeciesB.sa®tzaJ.terea(Table1a).Ifwingtoughnesscanbeusedasameasureofrelativepalatability,thentheseobservationsopenthepossibilityofdifferentialpalatabilityamongspeciesinthetwoAcraeafeedinggroups.Ventralmarkingsatthehindwingdistalmarginofpalatablebutter¯ies,suchastheeyespotsintheSatyrinaeor``false-head''intheLycaenidae,haveevolvedtofunctionastargetsthatdivertpredatorattacksawayfromvitalbodyareas(Blest1957,Robbins1981,Wourms&Wasserman1985).Inessence,theattackedbutter¯ymayescapewhilethepredatorisleftwithonlyapieceofwing.Theseobservationsincombinationwiththepresentstudyprovideanimpetusforaskingifthereisadifferentialtoughnessbetweenthetargetarea(,eyespots)andotherareasofthehindwinginpalatablebutter¯ies.Speci®cally,hasnaturalselectionresultedinhindwingtargetareasthataremorefragilethanthewingareassurround-ingthem?Thisquestioncanbeaddressedusingthemethodsdescribedhere.Insummary,byextendingunpalatabletheorythisstudyprovidesaprecedentforconductingalargecomparativestudyondifferentialwingtoughnessasanevolutionarycorrelateamongmanyspeciesofpalatableanddistastefulbutter¯ies.Inasimilarmanner,thisstudyalsosuggestsnewwaysofassessingpalatabilityamongmembersofAcraeaandothergroupsofbutter¯iesthataretraditionallyconsideredtobedistasteful.Finally,theresultshereprovideamotiveandameansforaskingwhetherornotthetargetpatternsonpalatablebutter¯iesformtheweakestportionofthehindwing.IthankP.R.AckeryforinsightintoAcraeabiology,W.Newmarkforbillmeasurementsandinfor- 180DeVriesmationontheecologyofAmanibirds,andL.Fishman,N.Martin,andT.R.Wallaforstatisticalconsultation.Iamgratefulforthestudentandfacultyinteractionsonthe1999TropicalBiologyAsso-ciationcourse,andofferspecialthankstoRosieTrevelyanforsomecriticalTuskermoments.IamindebtedtoG.Beccaloni,R.Dudley,B.Hawkins,R.Lande,N.Martin,C.M.Penz,R.Watkins,A.Young,andtwoanonymousreviewersforcommentsonpreviousdraftsofthismanuscript.ThisstudywassupportedinpartbytheNationalScienceFoundation(NSFDEB980679)andisdedicatedtotheinspiringtoughnessofL.FriedlanderandS.Lacy.CKERY,P.R.1987.DiversityandphantomcompetitioninAfricanacraeinebutter¯ies.Biol.J.Linn.Soc.30:291±ÐÐÐ.1988.Hostplantsandclassi®cation:areviewofnymphalidbutter¯ies.Biol.J.Linn.Soc.33:95±203.ANDR.I.VRIGHT.1984.Milkweedbutter¯ies:theircladisticsandbiology.BritishMuseum(Nat.Hist.),Entomology,London,England.ECCALONI,G.W.1997.Verticalstrati®cationofithomiinebutter¯y(Nymphalidae:Ithomiinae)mimicrycomplexes:therelationshipbetweenadult¯ightheightandlarvalhost-plantheight.Biol.J.Linn.Soc.62:313±341.LEST,A.D.1957.ThefunctionofeyespotsintheLepidoptera.Behaviour11:209±256.OWERS,M.D.,I.L.BROWNANDD.W.1985.Birdpredationasaselectiveagentinabutter¯ypopulation.Evolution39:93±103.ROWER,J.V.Z.1958a.ExperimentalstudiesofmimicryinNorthAmericanbutter¯iespart1.Themonarch,Danaus,andtheviceroy,Limenitisarchippusarchippus.Evolution12:32±47.ÐÐÐ.1958b.ExperimentalstudiesofmimicryinNorthAmericanbutter¯iespart3.DanausbereniceLimenitisarchippus¯oridensis.Evolution12:273±285.ROWER,L.P.1984.Chemicaldefensesinbutter¯ies.Symp.R.Entomol.Soc.Lond.11:110±134.ARPENTER,G.D.H.1932.Attacksofbirdsonbutter¯ies.Trans.R.Entomol.Soc.Lond.81:21±26.ÐÐÐ.1937.Furtherevidencethatbirdsdoattackandeatbutter¯ies.Proc.Zool.Soc.Lond.A1937:223±247.ÐÐÐ.1938.Theattacksofbirdsuponbutter¯ies.Proc.VIIIInternationalOrnithologicalCongress,Oxford.1934,pp.265±276.Oxford,England.ÐÐÐ.1941.Therelativefrequencyofbeak-marksonbutter¯iesofdifferentedibilitytobirds.Proc.Zool.Soc.Lond.AIII:223±230.ÐÐÐ.1942.ObservationsandexperimentsbythelateC.M.F.Swynertononwildbirdseatingbutter¯iesandthepreferencesshown.Proc.Linn.Soc.Lond.154:10±46.,P.1986.FieldobservationsandfeedingexperimentsontheresponseofRufousTailedJacamars(Galbularu®cauda)tofree-¯yingbutter¯iesinatropicalrainforest.Biol.J.Linn.Soc.29:166±189.ÐÐÐ.1996.Butter¯yvisualcharacteristicsandontogenyofresponsestobutter¯iesbyaspecializedtropicalbird.Biol.J.Linn.Soc.59:37±67.ANDR.B.SRYGLEY.1990.Predationandthe¯ight,morphology,andtemperatureofNeotropicalrain-forestbutter¯ies.Am.Nat.135:748±765.RIES,P.J.1987.Thebutter¯iesofCostaRicaandtheirnaturalhistory.PrincetonUniversityPress,Princeton,NewJersey.ÐÐÐ,R.LANDED.MURRAY.1999.Associationsofco-mimeticithomiinebutter¯iesonsmallspatialandtemporalscalesinaNeotropicalrainforest.Biol.J.Linn.Soc.62:343±364.UDLEY,R.2000.Thebiomechanicsofinsect¯ight:Form,function,evolution.PrincetonUniversityPress,Princeton,NewJersey.LTRINGHAM,H.1910.Africanmimeticbutter¯ies.ClaredonPress,Oxford,England.ÐÐÐ.1912.AmonographoftheAfricanspeciesofthegenusAcraea,Fabr.,withasupplementonthoseoftheOrientalregion.Trans.Entomol.Soc.Lond.1912:1±374.ISHER,R.A.1958.Thegeneticaltheoryofnaturalselection.2ndedition.Dover,NewYork,NewYork.,S.T.1991.TheUsambaraMountains,NETanzania:phytogeographyofthevascularplantfauna.Sym.Bot.Ups.29:1±234.ARSEN,T.B.1991.Butter¯iesofKenyaandtheirnaturalhistory.OxfordUniversityPress,Oxford,England.,J.B.L.,ANDM.JORON.2000.Evolutionofdiversityinwarningcolorandmimicry:polymorphisms,shiftingbalance,andspeciation.Annu.Rev.Ecol.Syst.30:201±233.ARSHALL,G.A.K.1902.Fiveyearsobservationsandexperiments(1896±1901)onthebionomicsofSouthAfricainsects,chie¯ymimicryandwarningcolours.Trans.Entomol.Soc.Lond.1902:287±584.,A.,R.H.DAVIS.1981.TheoccurrenceofcyanoglucocideslinamarinandlotustralininAcraeaHeliconiusbutter¯ies.Comp.Biochem.Physiol.68B:575±577.WEN,D.F.1971.Tropicalbutter¯ies.OxfordUniversity.Press,Oxford,England.IEPERS,M.C.,P.C.T.S.1909±1918.TheRhopaloceraofJava.TheHague,TheNetherlands.IERRE,J.1984.SysteÁmatiqueevolutivecladistiqueetmimeÁtismechezlesleÁpidopteÁresdegenreAcraea.DScthesis.UniversityofParis,Paris,France.OULTON,E.B.1902.Thecoloursofanimals.InternationalScienti®cSeries67.Appleton,NewYork,NewYork.ÐÐÐ.1908.Essaysonevolution.ClaredonPress,Oxford,England.,W.R.1989.Analyzingtablesofstatisticaltests.Evolution43:223±225. Notes181OBBINS,R.K.1981.The``falsehead''hypothesis:predationandwingpatternvariationoflycaenidbutter¯ies.Am.Nat.118:770±775.RYGLEY,R.B.1994.Locomotormimicryinbutter¯ies?Theassociationsofpositionsofcentersofmassamonggroupsofmimetic,unpro®tableprey.PhilosophicTrans.R.Soc.Lond.B343:145±155.TEPPAN,S.J.1996.Flexuralstiffnesspatternsofbutter¯ywings(Papilionoidea).J.Res.Lepid.35:61±77.,C.M.F.1915a.Abriefpreliminarystatementofafewresultsof®veyearsspecialtestingonthetheoriesofmimicry.Proc.Entomol.Soc.Lond.1915:21±33.ÐÐÐ.1915b.Birdsinrelationtotheirprey:experimentsonWood-Hoopoes,SmallHornbillandaBabbler.J.SouthAfr.Ornithol.UnionPretoria11:32±108.ÐÐÐ.1919.Experimentsandobservationsbearingontheexplanationofformandcolouring,1908±1913,Africa.J.Linn.Soc.Lond.Zool.33:203±385.,J.R.G.1984.Mimicry:thepalatabilityspectrumanditsconsequences.Symp.R.Entomol.Soc.Lond.11:ÐÐÐ.1987.Theevolutionarydynamicsofbatesianandmuellerianmimicry:similaritiesanddifferences.Ecol.Entomol.12:81±95.OURMS,M.K.,F.WASSERMAN.1985.Butter¯ywingmarkingsaremoreadvantageousduringhandlingthanduringtheinitialstrikeofanavianpredator.Evolution39:845±851.P.J.DeVriesCenterforBiodiversityStudiesMilwaukeePublicMuseumMilwaukee,Wisconsin,53233,U.S.A. 176DeVries BIOTROPICA34(1):176±1812002DifferentialWingToughnessinDistastefulandPalatableButter¯ies:DirectEvidenceSupportsUnpalatableTheoryKeywords:Nymphalidae;butter¯ypalatability;wingtoughness;wingpatterns;predatordefenses.TISWELLKNOWNTHATNOTALLBUTTERFLYSPECIESareequallyacceptablefooditemstobirdpredators;somearereadilyeaten,whileothersmayberejectedpresumablyduetotheirnastytaste(Poulton1902;Swynnerton1915a,b,1919;Chai1986).Generalobservationsshowthatpalatablebutter¯iestendtohavecrypticcolorationanddependuponrapid¯ighttoevadepredators,whereasdistastefulbutter¯iesminimizepredationbyadvertisingnoxiousqualitiesassociatedwithadistinctivecolorpatternandaslow¯ight(summarizedinTurner1984,1987;Chai1986,1996).Theseobservationsarecentraltounder-standingthefunctionofbutter¯ycolorationandbehavior,learningbybutter¯ypredators,andthetheoriesofunpalatabilityandmimicry(Marshall1902;Poulton1908;Eltringham1910;Swynnerton1915a,b,1919;Carpenter1932,1942;Brower1958a,b;Fisher1958;Turner1984;Bowersetal.Chai1986,1996).Thebasictheoryaccountingfortheevolutionofunpalatabilityandwarningcolorationrequiresthedifferentialsurvivalofsomeindividualbutter¯iesfollowingattacksandtastingbypredators,andthattheexperiencebememorabletopredators(Fisher1958).Asimpleextensionofunpalatabletheorysuggeststhatnaturalselectionshouldfavoraposematicphenotypespossessingaphysicaltoughnessthatmakesthemresistanttohandlingbypredators.Indeed,thefactthatbodiesofunpalatablebutter¯ytaxatendtobemoreresilienttohandlingthanpalatableoneshaslongbeenrecognizedbyentomologists(Poulton1908,Piepers&Snellen1909±1918,DeVries1987).Therefore,toughnessappearstobeanessentialcomponentofbutter¯ysurvivalfrombirdattacks;however,theonlystudyofdifferentialtoughnessamongpalatableandunpalatablebutter¯iesisthatofCarpenter(1941)showingthatthenumberofbeakmarksonunpalatablemuseumspecimenswassigni®cantlygreaterthanpalatableones.Fromthisstudy,heinferredthatunpalatablebutter¯iessurvivingbirdattackshadtougherwingsthanpalatableones,thusprovidingtheonlyempiricalevidenceinsupportoftoughnessasacorollaryofunpalatability.Thereisalargeanddiversebodyofliteratureexploringtheevolutionofbutter¯ycrypsis,unpalat-ability,mimicryandassociatedwingtraits,andbehaviors(Poulton1902;Blest1957;Robbins1981;Turner1984,1987;Wourms&Wasserman1985;Chai1986,1996;DeVries1987;Chai&Srygley1990;Srygley1994;Steppan1996;Beccaloni1997;DeVriesetal.1999;Mallet&Joron2000andreferencestherein).Consideringthebreadthofthisliterature,itisthereforesurprisingthatdifferentialwingtoughnessamongpalatableandunpalatablebutter¯ieshasneverbeenmeasureddirectly.Accord-ingly,thisstudyaskswhetherornotunpalatablebutter¯ieshavetougherwingsthanpalatableonesbyexperimentallyestimatingtheforcenecessarytotearthewingsofrepresentativeAfricanbutter¯ies. Received8September2000;revisionaccepted19January2001. 176DeVries BIOTROPICA34(1):176±1812002DifferentialWingToughnessinDistastefulandPalatableButter¯ies:DirectEvidenceSupportsUnpalatableTheoryKeywords:Nymphalidae;butter¯ypalatability;wingtoughness;wingpatterns;predatordefenses.TISWELLKNOWNTHATNOTALLBUTTERFLYSPECIESareequallyacceptablefooditemstobirdpredators;somearereadilyeaten,whileothersmayberejectedpresumablyduetotheirnastytaste(Poulton1902;Swynnerton1915a,b,1919;Chai1986).Generalobservationsshowthatpalatablebutter¯iestendtohavecrypticcolorationanddependuponrapid¯ighttoevadepredators,whereasdistastefulbutter¯iesminimizepredationbyadvertisingnoxiousqualitiesassociatedwithadistinctivecolorpatternandaslow¯ight(summarizedinTurner1984,1987;Chai1986,1996).Theseobservationsarecentraltounder-standingthefunctionofbutter¯ycolorationandbehavior,learningbybutter¯ypredators,andthetheoriesofunpalatabilityandmimicry(Marshall1902;Poulton1908;Eltringham1910;Swynnerton1915a,b,1919;Carpenter1932,1942;Brower1958a,b;Fisher1958;Turner1984;Bowersetal.Chai1986,1996).Thebasictheoryaccountingfortheevolutionofunpalatabilityandwarningcolorationrequiresthedifferentialsurvivalofsomeindividualbutter¯iesfollowingattacksandtastingbypredators,andthattheexperiencebememorabletopredators(Fisher1958).Asimpleextensionofunpalatabletheorysuggeststhatnaturalselectionshouldfavoraposematicphenotypespossessingaphysicaltoughnessthatmakesthemresistanttohandlingbypredators.Indeed,thefactthatbodiesofunpalatablebutter¯ytaxatendtobemoreresilienttohandlingthanpalatableoneshaslongbeenrecognizedbyentomologists(Poulton1908,Piepers&Snellen1909±1918,DeVries1987).Therefore,toughnessappearstobeanessentialcomponentofbutter¯ysurvivalfrombirdattacks;however,theonlystudyofdifferentialtoughnessamongpalatableandunpalatablebutter¯iesisthatofCarpenter(1941)showingthatthenumberofbeakmarksonunpalatablemuseumspecimenswassigni®cantlygreaterthanpalatableones.Fromthisstudy,heinferredthatunpalatablebutter¯iessurvivingbirdattackshadtougherwingsthanpalatableones,thusprovidingtheonlyempiricalevidenceinsupportoftoughnessasacorollaryofunpalatability.Thereisalargeanddiversebodyofliteratureexploringtheevolutionofbutter¯ycrypsis,unpalat-ability,mimicryandassociatedwingtraits,andbehaviors(Poulton1902;Blest1957;Robbins1981;Turner1984,1987;Wourms&Wasserman1985;Chai1986,1996;DeVries1987;Chai&Srygley1990;Srygley1994;Steppan1996;Beccaloni1997;DeVriesetal.1999;Mallet&Joron2000andreferencestherein).Consideringthebreadthofthisliterature,itisthereforesurprisingthatdifferentialwingtoughnessamongpalatableandunpalatablebutter¯ieshasneverbeenmeasureddirectly.Accord-ingly,thisstudyaskswhetherornotunpalatablebutter¯ieshavetougherwingsthanpalatableonesbyexperimentallyestimatingtheforcenecessarytotearthewingsofrepresentativeAfricanbutter¯ies. Received8September2000;revisionaccepted19January2001. 176DeVries BIOTROPICA34(1):176±1812002DifferentialWingToughnessinDistastefulandPalatableButter¯ies:DirectEvidenceSupportsUnpalatableTheoryKeywords:Nymphalidae;butter¯ypalatability;wingtoughness;wingpatterns;predatordefenses.TISWELLKNOWNTHATNOTALLBUTTERFLYSPECIESareequallyacceptablefooditemstobirdpredators;somearereadilyeaten,whileothersmayberejectedpresumablyduetotheirnastytaste(Poulton1902;Swynnerton1915a,b,1919;Chai1986).Generalobservationsshowthatpalatablebutter¯iestendtohavecrypticcolorationanddependuponrapid¯ighttoevadepredators,whereasdistastefulbutter¯iesminimizepredationbyadvertisingnoxiousqualitiesassociatedwithadistinctivecolorpatternandaslow¯ight(summarizedinTurner1984,1987;Chai1986,1996).Theseobservationsarecentraltounder-standingthefunctionofbutter¯ycolorationandbehavior,learningbybutter¯ypredators,andthetheoriesofunpalatabilityandmimicry(Marshall1902;Poulton1908;Eltringham1910;Swynnerton1915a,b,1919;Carpenter1932,1942;Brower1958a,b;Fisher1958;Turner1984;Bowersetal.Chai1986,1996).Thebasictheoryaccountingfortheevolutionofunpalatabilityandwarningcolorationrequiresthedifferentialsurvivalofsomeindividualbutter¯iesfollowingattacksandtastingbypredators,andthattheexperiencebememorabletopredators(Fisher1958).Asimpleextensionofunpalatabletheorysuggeststhatnaturalselectionshouldfavoraposematicphenotypespossessingaphysicaltoughnessthatmakesthemresistanttohandlingbypredators.Indeed,thefactthatbodiesofunpalatablebutter¯ytaxatendtobemoreresilienttohandlingthanpalatableoneshaslongbeenrecognizedbyentomologists(Poulton1908,Piepers&Snellen1909±1918,DeVries1987).Therefore,toughnessappearstobeanessentialcomponentofbutter¯ysurvivalfrombirdattacks;however,theonlystudyofdifferentialtoughnessamongpalatableandunpalatablebutter¯iesisthatofCarpenter(1941)showingthatthenumberofbeakmarksonunpalatablemuseumspecimenswassigni®cantlygreaterthanpalatableones.Fromthisstudy,heinferredthatunpalatablebutter¯iessurvivingbirdattackshadtougherwingsthanpalatableones,thusprovidingtheonlyempiricalevidenceinsupportoftoughnessasacorollaryofunpalatability.Thereisalargeanddiversebodyofliteratureexploringtheevolutionofbutter¯ycrypsis,unpalat-ability,mimicryandassociatedwingtraits,andbehaviors(Poulton1902;Blest1957;Robbins1981;Turner1984,1987;Wourms&Wasserman1985;Chai1986,1996;DeVries1987;Chai&Srygley1990;Srygley1994;Steppan1996;Beccaloni1997;DeVriesetal.1999;Mallet&Joron2000andreferencestherein).Consideringthebreadthofthisliterature,itisthereforesurprisingthatdifferentialwingtoughnessamongpalatableandunpalatablebutter¯ieshasneverbeenmeasureddirectly.Accord-ingly,thisstudyaskswhetherornotunpalatablebutter¯ieshavetougherwingsthanpalatableonesbyexperimentallyestimatingtheforcenecessarytotearthewingsofrepresentativeAfricanbutter¯ies. Received8September2000;revisionaccepted19January2001.