A Phylogenetic Approach to Understanding Rattlesnake Evolution. By Bradley Allf

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1 A Phylogenetic Approach to Understanding Rattlesnake Evolution By Bradley Allf Senior Honors Thesis Biology Department University of North Carolina at Chapel Hill./ April 6, 2015 David Pfennig, Thesis Advisor, Reader, Reader

2 INTRODUCTION Oneofthebiggestquestionsofevolutionarybiologyishownoveltraitsariseand fixateinapopulation.rattlesnakes(amonophyleticgroupwithinviperidaeareequipped withakeratinizedtailtipofoverlappinghollowsegmentsthatmakessoundwhenvibrated. Thisstructureisuniquetorattlesnakes,whichuseitforaposematicsignaling(Greene 1988.Abetterunderstandingofhowthisnovelstructureevolvedcouldshedlightonhow noveltraitsariseingeneral. Thoughmanyresearchershavepostulatedhypothesesabouttheevolutionary originsoftherattlesnakerattle(forexample,roweetal.2002;klauber1972;youngand Brown1995,itisstillunclearwhatexactlyledtotheevolutionofthisuniquestructure. Someauthorssupporttheideathattherattleevolvedtoenhancethesoundproducedby tailqvibratinginanextinctrattlesnakeancestor(klauber1972;roweetal.2002;moon 2001.TailQvibratingisadefensivesignalwhereasnakevibratesitstailrapidly,often againstasubstrate,producingabuzzingsound.thiswidespreadbehavioralmostcertainly servesasawarningand/ordistractiontoapotentialpredator,thoughthishasneverbeen testedspecifically.tailqvibratingisusedinasimilarcontextasrattlesnakerattling,andthe movementitselfisstronglyreminiscentofrattlesnakerattling,themajordifferencebeing thattherattlesnaketailisheldvertically,whiletailqvibratingsnakesholdthetail horizontally.fortheseandotherreasons,manyresearcherscitetailqvibrationasthemost likelysignalprecursortorattlesnakerattling. However,otherresearchershavespeculatedthattherattlesignalcouldhave evolvedfromadifferentsnaketailbehaviorcalled caudalluring (Schuettetal Caudalluringisafeedingbehaviorwhereasnakemovesits(oftenbrightlycoloredtailin

3 aslow,waveqlikemannerinordertoattractpreyspeciesthatpotentiallymistakethetail foraninvertebratefoodsource(tiebout1997;sazima1991;lealandthomas1994. Accordingtothishypothesis,anincipientrattlemaynothaveincreasedsoundproduction becauseofthehighamountofstructuralspecificityrequiredforsuchastructureto function(i.e.aseriesoflooselyoverlappinghollowsegmentsofkeratininmakingnoise.if thatincipientstructuredidnotincreasesoundproduction,thenitwouldapparentlyhave nofunctioninenhancingtailqvibration(schuettetal.1984.suchanincipientrattlemight, however,haveincreasedtheeffectivenessofcaudalluringifthetailmodificationresulted inmoreeffectiveluring forexample,ifthetailbetterresembledanarthropodhead (thoughseesiskandjackson1997.selectionforamodifiedtailtoenhancecaudalluring couldhaveledtotheevolutionoffurtherelaborationofthestructure,eventuallyresulting inasoundqproducingrattle. However,thishypothesisrunsintoanumberofproblems,themostobviousbeing parsimony.veryfewmodernrattlesnakescaudallurewhileallrattlesnakespeciesusethe rattlefordefensivesignaling(moon2001;roweetal.2002.thus,ifcaudalluringwerethe signalprecursorfortherattlesnakerattle,thesignalwouldhavehadtoswitchfroman offensivetoadefensivecontext.nosuchjumpisrequirediftailqvibrationwerethesignal precursor. Thesecondmajorproblemwiththecaudalluringhypothesisisthatboth rattlesnakesandtheirclosestrelatives(thegenusagkistrodonhaveelevatedoxidative capacitiesintheirtailmusculature(moon2001.rapid,sustainedtailqvibrationisa demandingmovementforanectotherm,especiallycomparedtocaudalluring,which almostcertainlyrequiresmuchlessenergy.withthisinmind,itwouldseemmorelikely

4 thatsuchspecializedtailmusclesinrattlesnakesandtheirclosestrelativeswouldhave evolvedtoenhanceademandingmovementliketailqvibration,notcaudalluring. Thusweareleftwithtwohypothesesabouttheevolutionaryoriginofthe rattlesnakerattle the tailqvibrationassignalprecursorhypothesis andthe caudal luringassignalprecursorhypothesis. Thepurposeofthisstudyistousedistributionsof tailbehaviorsacrossmodernspeciesofnewworldpitviperstobetterunderstandthetail behaviorsthatancestralrattlesnakesmighthavehad.thiswillinformthesignalprecursor debateandwillmoregenerallyleadtoabetterunderstandingofrattleevolution.sucha phylogeneticapproachtounderstandingrattlesnakeevolutionhasnotyetbeenpublished intheliterature.thefirststepinthisprojectwastomapobservationsofcaudalluringand tailqvibrationindifferentnewworldpitviperspeciesacrosstheentirephylogeny.ifoneof thesebehaviorswereclusteredincloserattlesnakerelativeswhiletheotherwas concentratedinmoredistantrelatives,itcouldsuggestsomethingaboutthelikely behaviorsdisplayedbyancestralrattlesnakes.ifancestralrattlesnakesdidnotdisplayone ofthetailbehaviors,thenitwouldofcoursebeexceedinglyunlikelythattherattlesnake rattleevolvedtoenhancethatsignal. Thesecondstepinthisprojectwasmorecloselyanalyzingthespecificsofoneofthe behaviorsandhowitchangesacrossthenewworldpitviperphylogeny.tailqvibratingwas examinedbecausethereiswidersupportintheliteratureforthatbehaviorbeingthesignal precursor.differentnewworldpitviperspeciesservedasproxiesfortheevolutionary historyoftherattlesnake,dependingonhowcloselyrelatedeachspeciesistorattlesnakes. Inthisway,ifthebehaviorchangedinanyspecificwayincloserrattlesnakerelatives,it couldinformhowthatbehaviorchangedalongtheancestralrattlesnakelineage.

5 METHODS First,aliteraturereviewwascarriedoutinorderassesshowwidespreadbothtailQ vibratingandcaudalluringareinnewworldpitvipers.datawereobtainedfromjournal articles,fieldguides,personalcommunicationwithresearchers,andpersonalobservations bytheauthor.thisinformationwasthenmappedontoancestralstatereconstructions createdusingmesquite2gb.thephylogeniesusedtobuildtheseancestralstate reconstructionswerebasedonthephylogenyofpyronetal.(2013,whichisthemost recentcomprehensivephylogeneticreconstructionavailableforthisclade. Withtheknowledgeofthegeneralpresenceorabsenceofthesetraitsinspecies withintheclade,amorespecificanalysisofthebehaviorswasthencarriedout.this analysiscomparedthetailqvibrationofspeciesacrossnewworldpitviperstoexamine whetheritchangedinanypersistentwayincloserrattlesnakerelatives.snakesfrom museums,zoos,andprivatecollectionswerefilmedwithahighspeedcasioexilimexq ZR700cameraat480framespersecond.Thishighframerateallowedforananalysisofthe rattlingspeedofeachindividual.tailqvibrationwasfilmedforapproximately30secondsto 2minutes. TailQvibrationwasinitiatedbyapproachingthesnakeor,ifthatdidnotsufficiently provoketheanimaltodisplaydefensively,astuffedanimalheadmountedonapairoftongs waspresentedtothesnake.thiswassurprisinglysuccessfulininitiatingadefensive responseintheanimals,potentiallybecauseofthetoy sresemblancetoamammalian predator.onlymaximumrecordedrattlespeedswereusedinanalysestoadjustfor potentialdifferencesinthestateofdefensivearousalofeachindividualsnake.nodatawas usedinanalysesforsnakesbeingbrumatedorotherwisebeingkeptatatypicallylow

6 temperatures,whichhasbeenshowntodecreaserattlingspeedinrattlesnakes(martinand Roland1972.VideoswereanalyzedusingAdobePremierePro,whichallowedforframe byframeanalysisofthevideossothatthenumberoftailvibrationspersecondcouldbe recorded.onerattle/vibrationwasdefinedasafullcompletionoftheentiremovement, wherebythetailflexesinonedirection,flexesintheoppositedirection,andthenreturns backtotheoriginaldirection. RESULTS InformationwasfoundonthetailbehaviorofnearlyeverygenusofNewWorldpit vipers(appendixb,excludingrattlingbehaviorinrattlesnakes.bothcaudalluringand tailqvibrationwerewidespreadthroughthecladeandneitherbehaviorwassignificantly moreconcentratedincloserrattlesnakerelatives(figures1and2.thus,itappearslikely thatancestralrattlesnakesexhibitedbothtailqvibrationbehaviorandcaudalluring behavior. TailQvibrationwasfilmedin65individualsacross27speciesand11genera.Snake groupsfilmedincludedcolubrids(outgroup,rattlesnakes,andnonqrattlesnakenewworld pitvipers.thisthirdgroupwasfurtherdividedintocloserattlesnakesrelativesandmore distantrattlesnakerelatives(figure3toseehowtailqvibratingchangedacrossthenew Worldpitviperclade.

7 MaximumLikelihoodReconstructionofCaudalLuringinNewWorldPitViperGenera Figure1:GenusQlevelancestralstatereconstructionofNewWorldpitvipers.Blackdotsrepresent generacontainingatleastonespeciesknowntocaudallure.whitedotsrepresentgenerawithout speciesknowntocaudallure,thoughtheabsenceofsuchanobservationdoesnotnecessarilymean speciesinthatgenusdonotperformcaudalluring.rattlesnakescomprisethetwogeneracrotalus andsistrurus.thisphylogenyisbasedonpyronetal.2013.

8 MaximumLikelihoodReconstructionofTailQVibratinginNewWorldPitViperGenera Figure2:GenusQlevelancestralstatereconstructionofNewWorldpitvipers.Blackdotsrepresent generacontainingatleastonespeciesknowntotailqvibrate(rattlesnakerattlingwasconsidereda formoftailqvibrationinthisfigure.whitedotsrepresentgenerawithoutspeciesknowntotailq vibrate,thoughtheabsenceofsuchanobservationdoesnotnecessarilymeanspeciesinthatgenus donotperformtailqvibration.rattlesnakescomprisethetwogenerasistrurusandcrotalus.this phylogenyisbasedonpyronetal.2013.

9 Figure3:Thisfigureshowshowtaxaaredividednumericallyintheanalysesofrattlingspeedinthe figuresbelow.rattlesnakes,theredtaxa,representgroup 0. Group 1 representsthegreengenus Agkistrodonshownabove.Nodatawasobtainedfromtaxaintheblackgenera.Thebluetaxaare themoredistantlyrelatednewworldpitvipersandarerepresentedbygroup 2. Importantly, tailqvibrationwasnotfilmedinallthegeneraintheblueclade(seeappendixa.thebrown Colubridoutgroupwillberepresentedbygroup 3.

10 Averagerattling/vibratoryspeedsamongthesegroupswerecomparedusinga TukeyQCramermeanscomparison.Rattlesnakeswerefoundtorattlesignificantlyfaster thananyothergrouptailqvibrated.thecloserrattlesnakerelatives(group1tailqvibrated fasterthangroups2and3onaverage(table1,butthetukeyqcramercomparisondidnot findthisdifferencetobesignificant(figure4. Group Numberofindividuals Averagerattling/vibratory recorded speed rattles/second 1 12* 33.65vibrations/second* vibrations/second rattles/second Table1:AveragetailQvibrating/rattlingfrequenciesamongthedifferentgroupsofsnakesoutlined infigure3.(*indicatesdatathatchangesinfigure5,witha.,piscivorus,dataremoved.average vibratoryspeedincreasesto37.11rattles/secondandthenumberofindividualsrecordedis reducedto10. However,onespeciesinGroup1islikelyresponsibleforthis Agkistrodon, piscivorus.,thetwooutliersingroup1 sdatainfigure4thataredramaticallylowerthan anyothervibratoryspeedsinthegroupbelongtotheonlytwoa.,piscivorus,individuals filmed.a.,piscivorus,istheonlyknownaquaticpitviperintheworld(campbelletal.2004 anditispossiblethatconstraintsfromthishabitatledtothelossofafasttailqvibratory speed,perhapsduetomorphologicalchangesinthetailtomakeitamoreeffective swimmingstructure.ifa.,piscivorus,isremovedfromthedata,therattlingspeedsfrom Group1becomesignificantlyhigherthanthoseofGroups2and3(Figure5,whileGroup0

remainssignificantlyfasterthananyothergroup.thus,accordingtothisdatarattling speeddoesincreaseincloserrattlesnakerelatives.

group0(rattlesnakesrattlesignificantlyfasterthananyothergroup. Group1(Agkistrodon,sp.

11 remainssignificantlyfasterthananyothergroup.thus,accordingtothisdatarattling speeddoesincreaseincloserrattlesnakerelatives. Figure4:TukeyQKramercomparisonoftailQvibrating/rattlingspeedamongthefourgroupsof snakesoutlinedinfigure3.group0(rattlesnakesrattlesignificantlyfasterthananyothergroup. Group1(Agkistrodon,sp.tailQvibratesfasterthanGroups2and3buttheseresultsarenot significant(p=0.0023and0.0129,respectively.notethetwoa.,piscivorus,outliersingroup1that haverattlingspeedsdramaticallylowerthananyotherdatapointsinthegroup.

DISCUSSION Theancestralstatereconstructionsobtainedinthisresearchsuggestthatancestral rattlesnakeslikelytailqvibratedandcaudallured.

12 Figure5:TukeyQCramercomparisonofthegroupsoutlinedinFigure3,withA.,piscivorus,data removed.groups0and1arebothsignificantlydifferentfromallothergroupsandgroup1is intermediaryinrattlingspeedbetweengroup0andgroups2and3. DISCUSSION Theancestralstatereconstructionsobtainedinthisresearchsuggestthatancestral rattlesnakeslikelytailqvibratedandcaudallured.hadoneofthetailbehaviorsbeen significantlymoreconcentratedincloserrattlesnakerelatives,itwouldhavebeen particularlyinformativeinthedebateoverwhatthesignalprecursorwastorattlesnake rattling.butbecausebothbehaviorsarespreadfairlyevenlythroughtheclade,this approachdidnotbolstereitherhypothesis.

13 However,thedataobtainedinthesecondpartofthisresearchsupportsthe hypothesisthattailqvibrationprovidedthesignalbasisfortheevolutionoftherattlesnake rattle.thedatashowsthatrattlesnakesrattlefasterthananyothergrouptested.italso showsthat,withtheexceptionofa.,piscivorus,,speciesinthegenusmostcloselyrelatedto rattlesnakestailqvibratefasterthanmoredistantlyrelatedpitvipers.thissuggeststhat tailqvibrationwasmodifiedinancestralrattlesnakesduringrattleevolutiontobecome faster,aselevatedvibratoryspeedisalsoatraitofextantrattlesnakes.onewouldnot necessarilyexpectthisstepwisemodificationoftailqvibrationthroughevolutionarytimeif caudalluringwerethesignalprecursor. Thisresearchalsosuggestssomepotentialhypothesesfortheevolutionary pressuresthatledtotheevolutionoftherattle.withtheexceptionofa.,piscivorus, Agkistrodon,speciestailQvibratesignificantlyfasterthanmoredistantlyrelatedpitvipers. Whileitremainsunclearwhy,suchanincreasedvibratoryspeedwouldbeselectedforin thisgenus,theresultsofthisselectioncouldhaveactuallyfacilitatedrattleevolutionifthis increasedvibratorycapacityledtotaildamage.rattlesnakesarethoughttohaveoriginated inrockyoutcropsincentralmexico,andvibratingathighfrequenciesagainstsuchahard substratecouldhaveledtotaildamageinfastqvibratingancestralrattlesnakes.iknowfrom personalcommunicationwithstaffatthekentuckyreptilezoothatsomeindividualsofthe genusbothrops,intheircollectionhavefracturedtheirtailsintheprocessoftailqvibrating. Ifastructureevolvedinancestralrattlesnakesthatprotectedthetailduringvibration perhapssomesortofkeratinousbulbattheendofthetail itcouldhavebeenselectedfor andtheneventuallymodifiedintotheuniquesoundqproducingstructurethatmodern rattlesnakesareequippedwith.thishypothesisthattheoriginalpurposeofincipient

14 rattleswasforprotectionofthetailhasbeenraisedbefore(tiebout1997butthisisthe firstresearchtofindpotentialsupportfortheideathroughanactualempiricalstudy. Inmovingforward,thishypothesisthatincipientrattlesfirstevolvedtoprotect againsttailqdamagesustainedduringtailqvibrationshouldbeinvestigatedmore specifically.thiscouldpotentiallybedonebyinvestigatingwhetherfastertailqvibrating specieshaveahigherincidenceoftailbreakagethanslowervibratingspecies.onecould alsoinvestigatewhethertailfracturesaremorecommonintailqvibratingspeciesthatlive inhabitatswithhardsubstrates.anotherpotentialwaytomoveforwardwiththisresearch wouldbetoinvestigatewhyagkistrodon,andforthatmatterrattlesnakes,evolvedsuch elevatedrattlingspeeds.isahigherrattlingspeedindicativeofhealthierindividualsmore capableofdeliveringatoxicbitetoawouldqbepredator?arepredatorsmorelikelyto avoidfasterqrattlingindividuals? Amorecomprehensiveexaminationofvibratoryspeedsacrosspitviperswould bolsterthesignificanceofthisresearch.inparticular,gettingdatafortheonespeciesof Agkistrodon,(A.,taylorinotincludedinthedataisimportantinordertobettersubstantiate theclaimthatvibratoryspeediselevatedinthisgenuscomparedtoothernonqrattlesnake pitvipers.obtainingdatafromthecladecontaininglachesis,,ophryacus,,mixcoatlus,,and Bothriechis,wouldalsobeinformativeinunderstandingwhereintheevolutionary sequenceelevatedvibratoryspeedbegan.itisalsoimportanttonotethatelevated vibratoryspeedisapparentlynotuniquetorattlesnakesandthegenusagkistrodon.two differentspeciesofcolubrid(pituophis,melanoleucus,andelaphe,obsoleta,lindheimeriboth vibratedatspeedstypicalofaslowrattlingrattlesnake(appendixa.yetneitherofthese speciesarepartoflineagesthatevolvedanysortofmodifiedtailstructure.whywoulda

15 rattleevolveinfastvibratingrattlesnakeancestorsbutnotinfastvibratingcolubrid ancestors?hopefully,futureresearchwillbeabletoaddresssomeofthesequestionsin ordertobringusclosertounderstandinghowtherattlesnakerattleevolvedand,thereby betterunderstandhownoveltraitsariseinpopulationsingeneral. Acknowledgements IwouldliketothankAliLyoob,TheCapeFearSerpentarium,TheKentuckyReptileZoo, ColdQBloodedEncounters,AlligatorAdventure,andtheLastPlaceonEarthpetstorefor allowingmetofilmthesnakesintheircollections.iwouldalsoliketothankdr.david PfennigandtherestofthePfennigLabfortheirvaluableadviceandencouragementinthis project. BIBLIOGRAPHY Campbell,JonathanA.,WilliamW.Lamar,andEdmundD.Brodie.The,venomous,reptiles,of, the,westen,hemisphere,,vol.1.no.2.ithaca:comstockpub.associates,2004. Greene,HarryW. Antipredatormechanismsinreptiles. Biology,of,the,Reptilia,16.1 (1988:1Q152. Klauber,LaurenceMonroe.Rattlesnakes:,Their,Habits,,Life,Histories,,and,Influence,on, Mankind.,Berkeley,Calif.:Univ.ofCalifornia,1972.Print. Leal,Manuel,andRichardThomas."NotesontheFeedingBehaviorandCaudalLuringby JuvenileAlsophisPortoricensis(Serpentes:Colubridae."Journal,of,Herpetology 28.1(1994:126Q28.Print. Martin,JamesH.,andRolandM.Bagby."TemperatureQfrequencyrelationshipofthe rattlesnakerattle."copeia(1972:482q485. Moon,BradR."MusclePhysiologyandtheEvolutionoftheRattlingSystemin Rattlesnakes."Journal,of,Herpetology(2001:497Q500.Web.

16 Pyron,R.Alexander,FrankT.Burbrink,andJohnJ.Wiens."Aphylogenyandrevised classificationofsquamata,including4161speciesoflizardsandsnakes."bmc, evolutionary,biology13.1(2013:93. Rowe,MatthewP.,TerrenceM.Farrell,andPeterG.May."RattleLossinPygmy Rattlesnakes(SistrurusMilairius:Causes,Consequences,andImplicationsfor RattleFunctioninRattleEvolution."Biology,of,the,Vipers(2002:385Q404.Web. Sazima,Ivan."CaudalLuringinTwoNeotropicalPitvipers,BothropsJararacaandB. Jararacussu."Copeia1991.1(1991:245Q48.Print. Schuett,GordonW.,DavidL.Clark,andFredKraus."FeedingMimicryintheRattlesnake SistrurusCatenatus,withCommentsontheEvolutionoftheRattle."Animal, Behaviour32.2(1984:625Q26.Print. Sisk,NormanR.,andJamesF.Jackson."TestsofTwoHypothesesfortheOriginofthe CrotalineRattle."Copeia1997.3(1997:485Q95.Print. Tiebout,HM."CaudalLuringbyaTemperateColubridSnake,ElapheObsoleta,andIts ImplicationsfortheEvolutionoftheRattleamongRattlesnakes."Journal,of, Herpetology31.2(1997:290Q92.Print. Young,BruceA.,andLlonaP.Brown."ThePhysicalBasisoftheRattlingSoundinthe RattlesnakeCrotalusVividisOreganus."Journal,of,Herpetology29.1(1995:80Q85. Web.

17 AppendixA:Rattling/VibratorySpeedsofSnakesFilmed Species MaximumRattles/ Second PhylogeneticGroup (accordingtofigure 3 Othriophistaeniurus Othriophistaeniurus Bothropscolombiensis Elapheclimacophora Lampropeltisgetula Agkistrodonpiscivorus Bothropscaribbaeus Bothropsmoojeni Bothropsmoojeni Bothropscolombiensis Lampropeltisgetulagetula Bothropsmoojeni Bothropsmoojeni Lampropeltiscalligaster Bothropsmoojeni Bothropsatrox Bothropsmoojeni Bothropscolombiensis

18 Agkistrodonpiscivorus Bothropsmatogrossensis Porthidiumophryomegus Bothropsmoojeni Rhinocerophusalternatus Rhinocerophusalternatus Rhinocerophusalternatus Rhinocerophusalternatus Rhinocerophusalternatus Rhinocerophusalternatus Rhinocerophusalternatus Agkistrodoncontortrix Atropoidesmexicanus Agkistrodonbilineatus Agkistrodonbilineatus Agkistrodonbilineatus Agkistrodoncontortrix Agkistrodoncontortrix Agkistrodonbilineatus Agkistrodoncontortrix Agkistrodoncontortrix

19 Agkistrodoncontortrix Pituophismelanoleucus Crotalushorridus Elapheobsoleta Crotalusbasilicus Crotalushorridus Crotalusatrox Crotalusatrox Crotaluscerberus Crotalusdurissus Crotalusdurissus Crotalusdurissus Crotalusdurissus Sistrurusmilairius Crotaluslepidus Crotalusmitchellii Sistrurusmilairius Crotaluscerberus Crotalusdurissus Crotalusdurissus Crotalusdurissus

20 Crotalusornatus Crotalushorridus Crotaluslepidus Crotalusadamanteus Crotalusdurissus AppendixB:RecordedInstancesofTailQVibratingandCaudalLuringinNewWorld PitVipers Species TailQVibrating CaudalLuring Reference Sistrurus Yes(hasrattle Yes Pers.com.withTMFarrell(Stetson milairius U.;Palmer1993;Campbelland Lamar2004 Yes Yes Pers.com.withJACampbell(Uof Texas,Austin;Neill1960 Agkistrodon bilineatus Lachesissp. Yes Yes Pers.com.withTimTroutatDenver Zoo;pers.com.withDeanRipaat CapeFearSerpentarium. Lachesis stenophrys Yes Pers.com.withFinnSpaerenof RainforestAnimalsRescueGroup Bothropsasper Yes Yes Pers.com.withJACampbell(Uof Texas,Austin;Tryon1985 Agkistrodon piscivorus Yes Yes HeatwoleandDavison1976;Werler anddixon2000 Agkistrodon contortrix Yes Yes Neill1948;Pers.com.withCFSmith (WoffordU.;Moon2001 Crotalus Yes(hasrattle Yes Kauffeld1943 Lepidus Porthidium hespere Yes Pers.com.withJRVelasco(Uof Texas,Austin Sistrurus Yes(hasrattle Yes Reiserer2002 catenatus Bothropoides jararaca Yes Yes Sazima1991;Pers.Com.withJim HarrisonatKentuckyReptileZoo Bothrops Yes Yes Sazima1991;Pers.commwithJim

21 jararacussu HarrisonatKentuckyReptileZoo Bothropsatrox Yes Yes Sazima1991;Pycraft1925;Siskand Jackson1997 Bothriopsis Yes GreenandCampbell1972 bilineata Atropoides nummifer Yes Yes Neill1960;pers.com.withJim HarrisonatKentuckyReptileZoo; Pers.Com.withGustavEloyatNajil Bothriechis schlegalii Bothriechis lateralis Bothriechis bicolor Crotalus cerastes Bothrops moojeni Bothrops leucurus Bothropoides neuwiedi Bothriopsis taeniata Crotalus willardi Rhinocerophis ammodytoides Bothrops colombiensis Bothrops carribaeus Rhinocerophus alternatus Cerrophidian godmani Kaan Yes Yes Neill1960;Pers.com.withFinn SpaerenofRainforestAnimals RescueGroup;Pers.com.with AdrianAcevedoofSouthwest FloridaVenomFarm Yes MurphyandMitchell1984. Yes MurphyandMitchell1984 Yes Reiserer2002 Yes Yes Martinsetal.2002;Andradeetal. 1996;pers.com.withJimHarrison atkentuckyreptilezoo Yes Yes Martinsetal.2002;Pers.com.with ViniHansserfromBrasCubas University Yes Yes Martinsetal.2002;Pers.com.with ViniHansserfromBrasCubas University Yes Martinsetal.2002 Yes(hasrattle Yes Greene1992 Yes Greene1992 Yes Yes Pers.com.withJimHarrisonat KentuckyReptileZoo Yes Pers.com.withJimHarrisonat KentuckyReptileZoo;Pers.obs. Yes Pers.com.withJimHarrisonat KentuckyReptileZoo;Pers.com. withvinihansserfrombrascubas University Yes Pers.com.withJimHarrisonat KentuckyReptileZoo;Pers.com.

22 Atropoides mexicana/ nummifer Rhinocerophus withgustaveloyfromnajilkaan Yes Pers.com.withJimHarrisonat KentuckyReptileZoo;personal observation Yes Pers.com.withJimHarrisonat KentuckyReptileZoo sp. Atropoidessp. Yes Pers.com.withJimHarrisonat KentuckyReptileZoo;Pers.com. withgustaveloyfromnajilkaan Porthidiumsp. Yes Pers.com.withJimHarrisonat KentuckyReptileZoo Bothrops venezuelensis Bothrops marmoratus Atropoides olmec Ophryacus undulatus Porthidium ophryomegus Bothrops matogrossensis Bothropoides insularis Yes Pers.obs. Yes Pers.com.withViniHansserfrom BrasCubasUniversity Yes Pers.com.withGustavEloyfrom NajilKaan Yes Pers.com.withGustavEloyfrom NajilKaan Yes Pers.com.withGustavEloyfrom NajilKaan;Pers.obs. Yes Pers.obs. Yes Andradeetal.2010 BibliographyofSourcesfromAppendixBnotcitedinPrimaryBibliography Andrade,DenisV.,etal."TailLuringbytheGoldenLancehead(Bothropsinsularis,anIsland EndemicSnakefromSouthQEasternBrazil."South,American,Journal,of,Herpetology5.3 (2010:175Q180. Greene,HarryW."Theecologicalandbehavioralcontextforpitviperevolution."Biology,of,the, Pitvipers10(1992:7Q118. Greene,HarryW.,andJonathanA.Campbell."Notesontheuseofcaudalluresbyarborealgreen pitvipers."herpetologica(1972:32q34. Heatwole,Harold,andElizabethDavison."Areviewofcaudalluringinsnakeswithnotesonits occurrenceinthesaharansandviper,cerastesvipera."herpetologica(1976:332q336.

23 Kauffeld,CarlF."GrowthandfeedingofnewbornPrice'sandgreenrockrattlesnakes."American, Midland,Naturalist(1943:607Q614. Martins,M.,MarquesOAV,andSazimaI."Ecologicalandphylogeneticcorrelatesoffeedinghabits inneotropicalpitvipersofthegenusbothrops."biology,of,the,vipers(2002:307q328. Murphy,J.B.,andL.A.Mitchell."Miscellaneousnotesonthereproductivebiologyofreptiles.6. ThirteenvarietiesofthegenusBothrops(Serpentes,Crotalinae."Acta,Zoologica,et, Pathologica,Antverpiensia,,Antwerpen,(78(1984:199Q214. Neill,WilfredT.,"Thecaudallureofvariousjuvenilesnakes."Quart.,J.,Florida,Acad.,Sci23(1960: 173Q200. Neill,WilfredT."Theyellowtailofjuvenilecopperheads."Herpetologica4.5(1948:161Q161. Palmer,WilliamM.Reptiles,of,North,Carolina.UnivofNorthCarolinaPress,1995. Pycraft,WilliamPlane.Camouflage,in,nature.Hutchinson&Company,1925. Reiserer,R.S.2002.Stimuluscontrolofcaudalluringandotherfeedingresponses:Aprogramfor researchonvisualperceptioninvipers.pp.361q383.ing.w.schuett,m.hoggren,m.e. Douglas,andH.W.Greene(Eds.,BiologyoftheVipers.EagleMountainPublishing,LC, EagleMountain,Utah,U.S.A. Sazima,Ivan."CaudalLuringinTwoNeotropicalPitvipers,BothropsJararacaandB.Jararacussu." Copeia1991.1(1991:245Q48.Print. Tryon,B.W."Bothropsasper(terciopelo.Caudalluring."Herpetol.,Rev16.28(1985:561. Werler,JohnE.,andJamesR.Dixon.Texas,snakes:,identification,,distribution,,and,natural,history. UniversityofTexasPress,2000.

Behavioral Plasticity and the Origins of Novelty: The Evolution of the Rattlesnake Rattle

vol. 188, no. 4 the american naturalist october 2016 Natural History Note Behavioral Plasticity and the Origins of Novelty: The Evolution of the Rattlesnake Rattle Bradley C. Allf,* Paul A. P. Durst, and