SHIFTSINLIFEHISTORYASARESPONSETO PREDATIONINWESTERNTOADS(Bufoboreas)

DOUGLASP.CHIVERS,l,*JOSEPHM. KIESECKER,2

ADOLFOMARCO,3ERICAL.WILDY,4 andANDREWR.BLAUSTEIN4

‘Departmentof BiologicalSciences

UniversityofMaine

Orono,Maine04469-5751

2School of Forestryand EnvironmentalStudies

Yale University

New Haven,Connecticut06511

3Departamentode BiologiaAnimal Universidadde Salamanca Salamanca,37071,Spain

4Departmentof Zoology OregonState University Corvallis,Oregon97331

Abstract—Larval westerntoads(Bufoboreas)areknowntoexhibitantipreda­ torbehaviorinresponsetobothchemicalalarmcuesreleasedfrominjured conspecificsandchemicalcuesofpredatoryinvertebrates.Inthisstudy,we testedwhetherlong-termexposuretopredator andalarmcuesresultedinan adaptiveshiftinlifehistorycharacteristicsofthetoads.We raisedgroupsof tadpolesinthe presenceof:(1)predatorybackswimmers(Notonectaspp.)that were fedtoadtadpoles,(2)nonpredatorywaterboatman(Corixidae),and(3) chemicalalarmcuesofinjuredconspecifics.Tadpolesraisedinthepresenceof bothchemicalalarmcuesandcuesofpredatorsfedtadpolesmetamorphosedin significantlyshortertimethanthoseraisedinthepresenceofthenonpredator control.Reducingtimetakentoreachmetamorphosiswouldreduceexposure toaquaticpredators.Therewasnodifferenceamongtreatments inthesizeat metamorphosis.Ourresultssuggestthatthisshiftinmetamorphiccharacter­ isticsmay representafacultativealterationinlife history.

KeyWords—Predation,lifehistory,chemicalcues,alarmcues, amphibians,

westerntoads,Bufo boreas.

*To whom correspondence should be addressed at Department of Biology, University of

Saskatchewan,112SciencePlace, Saskatoon,Saskatchewan57N5E2,Canada.

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INTRODUCTION

Predationisastrongselectiveforceinfluencingthebehavior,morphology,and lifehistoryofpreyspecies(Sih, 1987;LimaandDill,1990; ChiversandSmith,

1998).Moststudiesofpreydefenseshaveconcentratedonbehavioralormor­ phologicaldefenses.Fewerstudieshaveexaminedtheeffectsofpredationon alterationsinlifehistorycharacteristics(patternsofgrowthandreproduction).

Amphibiansprovideamodelsystemforstudyingtheeffectsofpredation onlifehistoryshifts(seeWerner,1986).Forexample,Skelly(1992)foundthat graytreefrog(Hyla versicolor)tadpoleshadreducedgrowthanddevelopment rateswhenexposedtocagedlarvaltigersalamanders(Ambystomatigrinum). SkellyandWerner(1990)demonstratedthatlarvalAmerican toads (Bufoamer­ icanus)metamorphosedatasmallersizeinthepresenceofdragonfly(Anax junius) predatorsthanintheirabsence.VanBuskirk(1988)andWilburand Fauth(1990)documentedthatAmericantoadtadpolesmetamorphosedearlier andatasmallersizeinthepresence ofdragonflypredators.

Fewstudieshaveexaminedtheimportanceofchemicalcuesassignals

inducing changesinamphibian lifehistorytraits(KatsandDill,1998).Inone study,SihandMoore(1993)demonstratedthatsalamanders(Ambystomabar­ bouri)delayedhatchinginthepresenceofchemicalcues ofpredatoryflatworms (Phagocottusgracilis),butnotinresponsetocuesofnonpredatory isopods (Lirceusfontinalis).Inanotherstudy,larvallong-toedsalamanders(Ambystoma macrodactylum)exhibitedslowergrowthandanincreaseintimetoreachmeta­ morphosisinthepresenceofconspecificpredatorsfedacannibaldietovercon- specificsfedaninvertebratediet(Wildy etal.,1999).

Behavioralresponsesoflarvalamphibiansto chemicalcuesarewidespread (reviews ChiversandSmith,1998;KatsandDill,1998).Forexample,several bufonidtadpoles,includingthoseofthewesterntoad,exhibitantipredatorbehav­ iortochemicalalarmcuesreleasedfrominjuredconspecifics(Pfeiffer,1966; HewsandBlaustein,1985;Hews,1988;Petranka,1989).Thespecificchemi­ calthatactsasthealarmcueforbufonidtadpolesmaybebufotoxin(Kulzer,

1954).Bufonidtadpolesalsorespondtochemicalcuesofpotentialpredators.For example,Kieseckeretal.(1996)demonstratedthatwesterntoadtadpolesexhibit antipredatorbehaviorinresponsetochemical cuesofpredatorybackswimmers (Notonectaspp.),giantwaterbugs(Lethocerusamericanus),andgartersnakes (Thamnophissirtalis).Chemicalcuesareofprimeimportanceinrecognitionof insectpredatorsbywesterntoadtadpoles.Tadpolesrespondto chemicalbutnot visualcuesofpredatorybackswimmersandgiantwaterbugs(Kieseckeretal.,

1996).

Inthisstudy,weexaminedtheeffects ofpredationriskonlifehistory char­ acteristicsofwestern toads (Bufo boreas).Weraised tadpolesinthepresenceof predatorybackswimmers,nonpredatorywaterboatman,orchemicalcues from

injuredconspecifics totestwhetherthetadpoleschangecharacteristicsoftheir lifehistoryin responsetopredationcues.Specifically,wetested whethertherisk ofpredationaltersthetimeittakestadpolestoreachmetamorphosisorthesize theindividualsattainuponreachingmetamorphosis.

METHODSANDMATERIALS

WecollectedlarvaltoadtadpolesfromLostLake,LinnCounty,Oregon (44°26’42”N,121°55’30”W)inthesummer of1996.Thetadpolesweretrans­ portedtoOregonStateUniversityfortesting.Priortobeginningexperiments, tadpolesweremaintainedin37-literglassaquariaona14L:1ODphotoperiod atapproximately20°C.Thetadpoleswerefedadlibitumwithgroundalfalfa pellets.

Wedivided12glassaquariawidthwisewithafiberglassmeshscreento

createtwocompartments,eachmeasuring25x30x25cm.Twelverandomly selectedtadpoleswereplacedontoonesideofeachofthe12testtanks.All tadpoleswereatthesamestageofdevelopment(Gosnerstage25)(Gosner,

1960)atthebeginningoftheexperiment.Anadditionalthreetadpoleswere placedontotheoppositesideofeachtankfromwherethetesttadpoleswere placed.Ourexperimentconsistedofraisinggroupsoftadpolesunder threedif­ ferenttreatmentsin a randomizedblockdesignwithfourreplicatesofeachtreat­ ment.Treatment1wasapredatortreatment.Inthistreatmentweplacedthree predatorybackswimmersintoeachaquarium.Thepredatorswereplacedatthe stimulusendofthetank(i.e.,theendopposite fromwherethe12testtadpoles werehoused).Treatment2wasanonpredatortreatmentinwhichweplacedthree nonpredatorywaterboatmanintothestimulusendofeachaquarium.Treatment

3consistedofexposingtesttadpolestoalarmcuesfrominjuredconspecifics.

Throughoutthecourseoftheexperimentwe ensuredthattherewerethree livetadpolesonthestimulusendofeachaquariumeachday.Thesetadpoles servedaspreyforthebackswimmers.Placementoftadpolesonthestimulus endintheothertreatmentscontrolled foranyeffectsrelatedtothepresenceof preytadpolesinthebackswimmertreatment.Wepreparedthealarmcuestimulus bygrindingasingletadpolewithamortarandpestlein60mlofdistilledwater. Theresultingsolutionwasfilteredthroughafinemeshnetand10mlofthe solutionwasaddedtoeachofthealarmcuetreatmentcontainers.Alarmcues wereaddedtotheaquariathreedaysperweek. Onalloccasionsthecueswere introducedintothestimulusendofthetank.

Throughoutthecourseoftheexperimentwefedthetadpolesadlibitum withgroundalfalfapellets.Theaquariawerecleanedonceperweek.Wemoni­ toredtheexperimentalaquariadaily.Alltestanimalsthatreachedmetamorphosis (Gosner stage41)(Gosner,1960)wereremovedfromtheaquariaandweighed.

Foreachaquariumwecalculatedthemeantimetadpolestooktoreachmeta­ morphosis,andthemeanmassatmetamorphosis.Tankmeanswereusedinall statisticalanalyses.Weusedamultivariateanalysisofvariance(MANOVA) toexaminetheeffectsofthetreatment conditionsonmetamorphic characteris­ ticsofthetoads(TabachnickandFidell,1989).After MANOVA,weuseduni­ variateanalysisofvariance(ANOVA)oneachoftheresponsevariables (time takentoreachmetamorphosis,sizeuponreachingmetamorphosis,survivalto metamorphosis)toassesswhichvariableswereresponsibleforsignificantmain effects.Posthoccomparisons(Tukeytests)wereperformedtotestfordiffer­ encesbetweenmeansamongthestimulipresented.

RESULTS

MANOVArevealedthattherewasanoveralleffectofthetreatmentcon­ ditionsonthelifehistoryparametersthatwemeasured(Table1).Asubse­ quentANOVAshowed thattimetakentoreachmetamorphosiswassignificantly affectedbythetreatmentcondition.Tukeytestsrevealedthattadpolesmetamor­ phosedfasterinthepresenceofalarmcuesthaninthenonpredatorcontrol(P

0.029).Similarly,tadpolesmetamorphosed fasterinthepresenceofpredator cuesthaninthepresenceofnonpredatorcontrolcues(P=0.025).Therewasno differenceintimetometamorphosisbetweenthepredator andalarmcuetreat­ ments(P0.95).Neithermassatmetamorphosisnorsurvivaltometamorphosis wasinfluencedbythetreatmentconditions(Figure1).Percentageofsurvival (mean±SE)tometamorphosiswas66.7±8.3,64.5±10.5,and60.4±8.6in thepredator,nonpredatorandalarmcuetreatments,respectively.

TABLEI.RESULTSoFMANOVAFOROVERALLEFFECTSOFTREATMENTCONDITIONS ONMETAMORPHICTRAITSOFWESTERNTOADSANDANOVAsFOREACHRESPONSE VARIABLEa

F / df / P
MANOVA / 14.909 / 9,17 / <0.001
ANOVA Time / 6.800 / 2,9 / 0.016
Mass / 1.764 / 2,9 / 0.226
Survival / 0.121 / 2,9 / 0.888

aResponsevariablesaretimetoreachmetamorphosis(time),massatmetamorphosis(mass),and survivaltometamorphosis(survival).

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AlarmPredator Non-Predator

CueCueCue

FIG.1.Mean(+SE)timetoreachmetamorphosis(days)andmeanmassatmetamorpho­ sis(grams)fortadpolesexposedtochemical cuesofinjuredconspecifics,cuesofpreda­ torybackswimmers,andcuesofnonpredatorywaterboatman.Differentlettersdenote significantdifferencesatP0.05,basedonpost-hocTukeytests.

DISCUSSION

Theresults ofourstudydemonstratethatwestern toads altercharacteristics oftheirlifehistory inresponsetocuesthatindicatepredation.Tadpolesdecrease time taken toreach metamorphosisinthe presenceofpredatorcues and alarm cues whencomparedtononpredator cues.Bydecreasingtimetakentoreach metamorphosis,toadslikelybenefitbyreducingthetimetheyareexposedto predationby aquatic predators.Nevertheless,this type of shift in life history may have potentialcosts. For example,early metamorphosismay exposetoads toahigherlevelofterrestrialpredation.Further experimentsareneeded tounder­ stand potentialcosts ofearly metamorphosis.

Kieseckeretal.(1996) showedthat western toad tadpolesdo not respond to visual cues of invertebratepredators(backswimmersand giant waterbugs), butdo respondtochemicalcues ofthe same predators.Inthis experimentwe fed the backswimmerstadpolesinthe experimentalaquaria.Consequently,our

predatorstimulus likelyresultedin acomplexstimulusthatincludedbothvisual andchemicalcuesofthepredatorandinjuredpreycues.Weknow thatboththis complexpredator stimulusandtheinjuredprey(alarm)cuesalonewillinduce thechangeinlifehistory.Itisimportanttostressthatwedonotknowwhether cuesfromthepredatorintheabsenceofalarmcues(bufotoxin)ofthepreywill inducethischangeinlifehistory.Theresponsetothepredatorstimulusthatwe observed maybeadirectresponsetothealarm cuesofinjuredpreyandnota responsetothepredatorperse.

Additionalstudiesdesignedatexaminingthenatureofthechemicallyin­

ducedlifehistorychangesarewarranted.Forexample,futurestudiesshould manipulatetheconcentrationandfrequencyofexposuretoalarmcuesinorder to assesswhetherthechangeinlifehistory isanall-or-nothingresponseorinstead isagradedresponsethatreflectstheintensityofpredation.Moreover,weshould morecloselyexaminethenature ofthechemicalcuesthatinducethechanges, notonlythechemistryofthestimulusbutalsoitsperceptionandthemecha­ nismofresponsebythetadpoles.Weknowthatalarmcuesalonewillinduce ashiftinlifehistory.Theresponsetothepredatorstimulusinourstudymay havebeena responseto thepredatorstimulusalone,it mayhavebeena response toalarmcuesreleasedwhenthepredatorcapturedtheprey,oralternativelyit maybearesponsetoalarmcuesreleasedinthepredator’sdiet.Severalbehav­ ioralstudiesindicatethatprey speciesmayonlyrespondtochemicalcuesofa predatorwhenthepredatorisfedadietthatcontainsconspecifics oftheprey (e.g.,MathisandSmith,1993;WilsonandLefcort,1993;Chiversetal.,1996). Similarresultsareknowninstudiesofmorphologicaldefenses.Forexample, StabellandLwin(1997)showed thatcrucian carp(Carassiuscarassius)exhibit anadaptivechangeinbodymorphologyinresponsetopredatorsfedcarpbut notpredatorsfedadifferentdiet.

Inourexperimenttheresponseofthetoadswasto decreasethetimetaken toreachmetamorphosis.Wefoundnoevidencethattadpolesmetamorphosedata differentsizeinthepresenceofthepredatororalarmcuesthanin thepresenceof nonpredatorcues.VanBuskirk(1988)andWilburandFauth(1990)showedthat Americantoadtadpolesdecreasedboth thetimetakentoreachmetamorphosis andthesizeatmetamorphosisinresponsetodragonflypredators.Inanother study,SkellyandWerner(1990)foundthatAmericantoadsmetamorphosedat asmaller size inthepresenceoflarvaldragonflies.Theyfoundnoevidencethat toadtadpolesreducedthetimetakentoreachmetamorphosis.

Long-termshiftsinlifehistorymayresultfromseveralfactors.Forexam­ ple,numerousauthors(e.g.,DodsonandHavel,1988;Skelly,1992;Balland Baker,1996)havedemonstratedthatlifehistoryshiftsmayresultasby-products ofantipredatorbehavior.Specifically,timeandenergydevotedtoantipredator responseshaveacostintermsofa reductionin growthand/ordevelopmentrate. Suchreductionsingrowthand/ordevelopmentratecouldinfluencethetiming

oflifehistoryswitchpoints,forexample,byeitherdecreasingsizeatmeta­ morphosisorincreasingtimetometamorphosisorboth.Long-termshiftsinlife historymayalsorepresent facultativealterationsindevelopmentrate,whereby animalsincreasetheirdevelopmentratewhile maintainingthesame growthrate (e.g.,MinchellaandLoverde,1981;CrowlandCovich,1990;WilburandFauth,

1990).Thistypeofchangewouldlikelydecreasethetimetakentoreachmeta­

morphosis.

Changesintimingofmetamorphosisorsizeatmetamorphosiscanoccur evenintheabsenceofafacultativeincreaseindevelopmentrateoradecrease ingrowthand/or developmentrateassociatedwithantipredatorbehavior.For example,iftadpoleshavereachedaplateauontheirgrowthcurveandifthe conditionsintheterrestrialenvironmentareharshorunpredictable, theninthe absenceofaquaticpredators,tadpolesmaynottransformeveninanaquatic environmentthatprovideslittleornogrowthopportunities.Ifthiswasthecase, thecostsofstayingintheaquatic environment andnotgrowingmustoutweigh costsintheterrestrialenvironment.Itmaybecommontohavetemporaryperi­ odsduringwhichgrowthand/orsurvivalislowerintheterrestrialenvironment thantheaquaticenvironment.Suchconditionscouldoccur,forexample,ifthe probabilityofdesiccationishighorifterrestrialpredatorsareconcentratedat theedgeofthewater(DeVitoetal.,1998).

Inour experimentwedocumentedthattadpoleswerethesamesizeatmeta­ morphosis,butmetamorphosedfasterinthepresenceofthealarmandpredator cuesthaninthepresenceofthenonpredatorcues.Wedonotknowwhether tadpolesinthedifferenttreatmentsexhibitedthesamegrowthand/ordevelop­ mentratethroughouttheexperiment.Itispossible thatdifferencesinthetiming ofmetamorphosisthatweobservedcouldresultfromafacultativeincreasein developmentrate.Alternatively,thetadpolesmayhavehadthesamegrowthand developmentratebutalteredtheirtimingofmetamorphosistoreflectdifferences incostsandbenefitsoftransforming.Futurestudiesareneededtodifferentiate thesepossibilities.

Acknowledgments—Wethank Lisa Belden,Roger St. Luc, Rob Linski,NicholasTudor, and JanineTudorforproviding technicalassistance.FundingwasprovidedbytheUniversilyofMaine, theUniversity ofSaskatchewan,Oregon StateUniversityDepartmentofZoologyResearchFunds, theInstituteofBiosphericStudiesatYaleUniversity, theNaturalSciencesandEngineeringResearch Councilof Canada,theMinistryofEducationandScience of Spain,andtheNationalScienceFoun­ dation(grantDEB-9423333).

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