Evaluating the potential efficacy of invasive lionfish (Pterois volitans) removals

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Evaluating the potential efficacy of invasive lionfish (Pterois volitans) removals
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Barbour, Andrew B.
Allen, Micheal S.
Frazer, Thomas K.
Sherman, Krista D.
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The lionfish, Pterois volitans (Linnaeus) and Pterois miles (Bennett), invasion of the Western Atlantic Ocean, Caribbean Sea and Gulf of Mexico has the potential to alter aquatic communities and represents a legitimate ecological concern. Several local removal programs have been initiated to control this invasion, but it is not known whether removal efforts can substantially reduce lionfish numbers to ameliorate these concerns. We used an age-structured population model to evaluate the potential efficacy of lionfish removal programs and identified critical data gaps for future studies. We used high and low estimates for uncertain parameters including: length at 50% vulnerability to harvest (Lvul), instantaneous natural mortality (M), and the Goodyear compensation ratio (CR). The model predicted an annual exploitation rate between 35 and 65% would be required to cause recruitment overfishing on lionfish populations for our baseline parameter estimates for M and CR (0.5 and 15). Lionfish quickly recovered from high removal rates, reaching 90% of unfished biomass six years after a 50-year simulated removal program. Quantifying lionfish natural mortality and the size-selective vulnerability to harvest are the most important knowledge gaps for future research. We suggest complete eradication of lionfish through fishing is unlikely, and substantial reduction of adult abundance will require a long-term commitment and may be feasible only in small, localized areas where annual exploitation can be intense over multiple consecutive years.
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This publication was supported by a grant from the NOAA National Sea Grant College Program, and the National Science Foundation Graduate Research Fellowship under grant No. DGE-0802270 to ABB, the NOAA Aquatic Invasive Species Program, the NOAA National Centers for Coastal Ocean Science, and the National Marine Fisheries Service’s Southeast Fisheries Science Center. Publication of this article was funded, in part, by the University of Florida Open- Access Publishing Fund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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EvaluatingthePotentialEfficacyofInvasiveLionfish ( Pteroisvolitans )Removals AndrewB.Barbour 1 ,MichaelS.Allen 1 ,ThomasK.Frazer 1 ,KristaD.Sherman 2 1 FisheriesandAquaticSciencesProgram,SchoolofForestResourcesandConservation,TheUniversityofFlorida,Gainesville,Florida,UnitedStat esofAmerica, 2 Parks andScience,TheBahamasNationalTrust,Nassau,TheBahamas Abstract Thelionfish, Pteroisvolitans (Linnaeus)and Pteroismiles (Bennett),invasionoftheWesternAtlanticOcean,CaribbeanSea andGulfofMexicohasthepotentialtoalteraquaticcommunitiesandrepresentsalegitimateecologicalconcern.Several localremovalprogramshavebeeninitiatedtocontrolthisinvasion,butitisnotknownwhetherremovaleffortscan substantiallyreducelionfishnumberstoamelioratetheseconcerns.Weusedanage-structuredpopulationmodelto evaluatethepotentialefficacyoflionfishremovalprogramsandidentifiedcriticaldatagapsforfuturestudies.Weusedhigh andlowestimatesforuncertainparametersincluding:lengthat50%vulnerabilitytoharvest( L vul ),instantaneousnatural mortality( M ),andtheGoodyearcompensationratio( CR ).Themodelpredictedanannualexploitationratebetween35and 65%wouldberequiredtocauserecruitmentoverfishingonlionfishpopulationsforourbaselineparameterestimatesfor M and CR (0.5and15).Lionfishquicklyrecoveredfromhighremovalrates,reaching90%ofunfishedbiomasssixyearsaftera 50-yearsimulatedremovalprogram.Quantifyinglionfishnaturalmortalityandthesize-selectivevulnerabilitytoharvestare themostimportantknowledgegapsforfutureresearch.Wesuggestcompleteeradicationoflionfishthroughfishingis unlikely,andsubstantialreductionofadultabundancewillrequirealong-termcommitmentandmaybefeasibleonlyin small,localizedareaswhereannualexploitationcanbeintenseovermultipleconsecutiveyears. Citation: BarbourAB,AllenMS,FrazerTK,ShermanKD(2011)EvaluatingthePotentialEfficacyofInvasiveLionfish( Pteroisvolitans )Removals.PLoSONE6(5): e19666.doi:10.1371/journal.pone.0019666 Editor: HowardBrowman,InstituteofMarineResearch,Norway Received February25,2011; Accepted April2,2011; Published May10,2011 Copyright: 2011Barbouretal.Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense,whichpermits unrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited. Funding: ThispublicationwassupportedbyagrantfromtheNOAANationalSeaGrantCollegeProgram,andtheNationalScienceFoundationGraduate ResearchFellowshipundergrantNo.DGE-0802270toABB,theNOAAAquaticInvasiveSpeciesProgram,theNOAANationalCentersforCoastalOceanScien ce, andtheNationalMarineFisheriesService'sSoutheastFisheriesScienceCenter.Publicationofthisarticlewasfunded,inpart,bytheUniversityo fFloridaOpenAccessPublishingFund.Thefundershadnoroleinstudydesign,datacollectionandanalysis,decisiontopublish,orpreparationofthemanuscript. CompetingInterests: Theauthorshavedeclaredthatnocompetinginterestsexist. *E-mail:snook@ufl.edu Introduction InvasiveIndo-Pacificlionfishes, Pteroisvolitans (Linnaeus)and Pteroismiles (Bennett),areestablishedintheoffshorewatersofthe SoutheastUnitedStates,Caribbean,andarepresentlyinvading theGulfofMexicoandSouthAmerica[1,2,3,4].Thelionfish invasionisconcerningduetothedangerofhumanhealthrisksby venomouslionfishspinesandbecauseofnumerouspotential ecologicaleffectsonnativehard-bottom,mangrove,seagrass,and coralreefcommunities.Forexample,lionfishhavebeenshownto reducenativefishrecruitmentonexperimentalpatchreefsinThe Bahamas[5]andreductionsinreeffishrecruitmentmaybe exacerbatedbylionfishpredationuponjuvenilenativefishin importantnurseryhabitatssuchasmangrovesandseagrassbeds [6]possiblylimitingthesupplyofeconomicallyimportantreeffish recruits[7]. Throughthesemechanismslionfishmaybecontributingto widespreadregime-shiftsonCaribbeancoralreefsbyconsuming herbivoresresponsibleforcontrollingmacroalgalproduction [5,6,8].Theeffectsofthelionfishinvasionwilllikelycontinueto spread,aslionfishhaveextensivedispersalcapabilities[7,9]and arethoughtonlytobelimitedinrangebytemperaturesbelow 10.0 u C[10].Furthermore,knowninstancesofpredationupon lionfishintheWesternAtlanticarerareandlimitedtoincidental naturaloccurrencesofpredationbysuchspeciesasgroupers (Serranidae)[11]andgreenmorayeels, Gymnothoraxfunebris (Ranzani)(KDSherman,pers.obs.).Moreover,predationon juvenilelionfishbycommonreefpredatoryspeciesinlaboratory trialssuggestslowpredationvulnerability[12].Thissuggests lionfishpopulationslackatop-downcontrolmechanismto regulatetheirpopulationsizeintheirinvasiverange. Asaresultofthisestablishedanddestructiveinvasion,many countrieshaveinstitutedlionfishremovalprograms.These programsincludeinitiativessuchascreatingaspeciallicenseto allowthespearingoflionfishonnearshorereefsandlionfishkill ordersintendedtoinvolvethegeneralpublicinremovalefforts [13].Thelargestinitiativesinvolveusingrecreationaldiversto removelionfishduringderbyevents,andfocusingcommercial diversandfishersonharvestinglionfishasafoodfish[7]. Developinglionfishasacommercialorrecreationalfisheryhas beenproposedasapotentiallong-termsolution[7],butitisnot yetfullyunderstoodwhatlevelofexploitationmightberequiredto controllionfishpopulations. Todate,onlyoneevaluationhasexploredthelevelofharvest requiredtosubstantiallyreducelionfishpopulationsize.Thisstudy [14]utilizedastage-basedmatrixlionfishpopulationmodeland indicatedthatdecreasinglionfishabundancewouldrequire monthlyremovalsof27%oftheadultlionfishpopulation.The studyalsoreportedthatthisrequiredadultexploitationratecould besignificantlyreducedifjuvenileswereremovedfromthe PLoSONE|www.plosone.org1May2011|Volume6|Issue5|e19666

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population[14].Theirmodelwasdensity-independent,whichis appropriateforarecentlyintroducedlionfishpopulation.Thus, themodelassumednocompensationinrecruitmentafterfishing oraftertheparticularpopulationreachedalevelwheredensitydependencewouldoccur,aswouldbeexpectedforamaturing andwell-establishedinvasivespeciespopulation.Lionfishhave nowbeenintheAtlanticbasinforover10yearsandhavereached highdensities( 450fishperhectare)insomelocations[7,15], however,populationassessmentsofabundancearegenerally lacking.Neverthelesslionfishrecruitmentperadultwouldbe expectedtoincreaseasadultabundanceisreducedbyremoval effortsviarecruitmentcompensationasistypicalofestablishedfish populations[e.g.16].Thus,itisessentialthatremovalpractices andpoliciesbeevaluatedforscenarioswhererecruitment compensationoccurs. Inthisstudyweusedanage-structuredpopulationmodelto evaluatethepotentialforremovalprogramstooverfishlionfish populations,whileidentifyingkeydatagapstoguidefuture research.Existinglionfishlifehistoryinformationwascompiledto developthemodel,andvariousharvestrateswereappliedto evaluatetheefficacyofharvestasatop-downcontrolmechanism. Harvestrateswereevaluatedforupperandlowerestimatesof uncertainandunknownparameters.Theresultsofthemodelcan beusedtoinformthebestpossiblemanagementstrategiesunder currentknowledgewhileguidingfutureworktoreducekey uncertainties. Methods ModelDescription Onlysmallnumbersof Pteroismiles havebeendocumentedalong theSoutheastUnitedStates[17]withnocapturestodateinThe Bahamas[18].Lionfisharehereafterreferredtoasinclusiveof both P.miles and P.volitans .Forthepurposeofthismodeling exercise,lifehistoryparameterswerederivedprimarilyfrom P.volitans .Weassumedthatgiventhetaxonomicsimilarity between P.volitans and P.miles (twocloselyrelatedsympatric species),therewouldbenosubstantiallifehistorydifferences[see 19]betweenthetwospeciesthatmightaffecttheoveralloutcome ofthisstudy. Thepopulationmodelstructurewasidenticaltothatpublished previously[20,21],anditpredictedequilibriumrecruitmentand age-specificabundanceunderavarietyofharvestrates.Survival schedulesincorporatednaturalandharvestmortalities.Harvest wasdrivenbyastatedexploitationrateandlength-based vulnerabilitytoremovalefforts.Fecunditywasexpressedasa functionoffishweightandthecollectivefecundityforagivenyear wasreducedbyallmortalitysources.Themodelincludedages1 20andwasconstructedinExcel H EquilibriumrecruitmentwascalculatedusingaBotsford modificationofaBeverton-Holtstockrecruitmentfunction [22,23,24]asdescribedelsewhere[20].Thissimpleformulation predictsequilibriumrecruitmentasafunctionofthefishing mortalityrate.Themodelpredictedtheequilibriumage-1recruits (R eq )ofanexploitedpopulationandissummarizedas[20] R eq ~ R 0 CR { ( W 0 = W f ) CR { 1 1 where R 0 isthenumberofage-1recruitsoftheunfished populationatequilibrium,and CR istheGoodyearcompensation ratio[25].Itisunknownifthecurrentpopulationisnearthe asymptoticunfishedabundance,however,becauselionfishpopulationshavebeenestablishedforovertenyearsintheAtlantic coastalwaters,weinitiatedthesimulationatunfishedequilibrium. Thisissupportedbysimulationrunsinitializedatverylow populationsize,whichreachedequilibriumrecruitmentinfourto sixyearsdependinguponthevaluefor CR .The CR isdefinedas theratiooftherecruitsperspawneratverylowpopulationabundancerelativetotherecruitsperspawnerintheunfishedequilibriumcondition[25].Theparameter R 0 istheunfishedage-1 recruitmentatequilibriumandissimplyascalingparameterthat doesnotinfluencemodelpredictions. Themodelusedsurvivorshipcurvestocalculatethesurvivors perrecruittoeachage.Survivorshiptoage a intheabsenceof fishingwasfoundas l a ~ S a l a { 1 2 where S a istheage-specificfiniteannualnaturalsurvival(i.e., e 2 M ). Oursurvivorshipschedulesinthefishedconditionincorporated naturalmortalityandharvestas l fa ~ l fa { 1 S a (1 { UV a { 1 ), 3 where l fa isthesurvivorshipinthefishedcondition, U isthefinite annualexploitationrate,and V a istheage-specificvulnerabilityto harvest.Wespecifiedtheproportionoffishvulnerabletoharvest as V a ~ 1 1 z e { ( TL { L vul ) SD vul 4 where TL isthemeantotallengthatage a ascalculatedfromthe vonBertalanffygrowthmodel, L vul isthetotallengthat50% vulnerabilitytocapture,and SD vul isthestandarddeviationofthe logisticdistributionfor L vul .Theterm V a modelsincreasing vulnerabilitywithlength,and SD vul specifiesthesteepnessofthe curve.Age-specificabundance( N a )wasestimatedastheproductof thenumberofage-1recruits( R eq )andtheage-specificsurvivorship schedule. Meanfishweight-at-agewasusedasanindexoffecundity(egg production)asfecundityisdirectlyproportionaltoweight-at-age. Theage-specificfecundity( f a )wassettozeroifweight-at-agewas lessthanweight-at-maturity.Toaccountforthecumulativeeffects offishingonthereproductivecapacityofthepopulation,weused theincidencefunctionfortheunfished( W 0 )andfished( W f )egg productionperrecruit[20].Theseincidencefunctionswere calculatedas W o ~ X a f a l a and 5 W f ~ X a f a l fa 6 where f a representsage-specificfecundity,and l a and l fa arethe survivorshipschedulesoftheunfishedandfishedstates.Weused theweightedspawningpotentialratio(SPR)toevaluatetheextent towhichfishingmortalitycanreducereproductiveoutputof lionfish SPR ~ W f R W o R o 7 OverfishingLionfish PLoSONE|www.plosone.org2May2011|Volume6|Issue5|e19666

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where W 0 and W f aredefinedinEqs.(5)and(6),and R isthe recruitmentatequilibriuminthefishedcondition.Theweighted SPRmeasuresthepopulationforagivenleveloffishingmortality relativetotheunfishedcondition,whichisacommonlyused referencetoassessfisheriessustainability[26].Recruitment overfishingisgenerallytermedtooccurwhenSPRisbelowabout 0.4[27].Forthisstudy,wedefinerecruitmentoverfishingas occurringwhenSPR # 0.35. ParameterEstimates Parameterestimatesusedinthemodelsimulationareshownin Table1.Duetoalackofempiricaldataon CR forlionfish,we selectedtwovaluesfor CR ,5and15.Thesevaluesrepresented biologicallyreasonablehighandlowestimatesforspecieswith similarlifehistorytraits(e.g.,relativelyshortlivedpredators), baseduponpastmeta-analyses[16,28]. Ageandgrowthdatatodeterminevaluesfor L and K (Table1) wereobtainedfromlionfishcollectedinoffshorewatersofNorth Carolinabyspearfishing,handnets,hookandline,andtrapping during20042009(dataprovidedbyJ.Potts,NMFS[29]). Collectionsitesrangedbetween2745mdepthandwere characterizedashard-bottomhabitatcomprisedofrockyoutcroppings.Sagittalotolithswereremoved,dried,andembeddedin epoxy.Otolithswereseriallysectionedonalow-speedsaw.The resultingsectionswereadheredtomicroscopeslidesandcovered withaliquidcover-slip. Opaquezoneswereenumeratedforeachfishandwidthofthe marginwasnoted.Opaquezonecountswereconvertedto calendaragesbasedontimingofopaquezonecompletingand dateofcapture.Atotalof774fishwereagedbyasingleperson. Qualityassurancewasassuredusingasecondblind''readerto maintain 95%agreement.AvonBertalanffygrowthcurvewas fittedusingmaximumlikelihoodestimationofthenormal distribution(Figure1),butwefixed t o at 2 0.5becauseoflikely overestimationofmeanlengthatage-0duetogearbias.Thefitted valueof L =425mmisconsistentwithdatareportedpreviously; forexample,apaststudy[30]collected 1,000lionfishwiththe largestfishmeasuring424mmTL;andReefEnvironmental EducationFoundation's(REEF)lionfishderbies,whichhave resultedinthecollectionofn=2,349lionfish,indicatethatthe largestfishmeasured434mmTL. Topredictfishweightfromlength, a and b parameterswere estimatedfromthedatasetof774lionfishcollectedfromthe offshorewatersofNorthCarolina.Usingmaximumlikelihoodof thenormaldistribution,valuesof2.89 6 10 2 5 and2.89were estimatedforthe a and b growthparameters(Figure2).Lionfish sizeat50%maturityhasbeenestimatedat100mmTLformales (n=927)and175mmTLforfemales(n=718)through examinationofgonadaltissue[12].Ageat50%maturitywas specifiedasage-1,whichcorrespondedtoamodel-predictedtotal lengthof159mmandaweightat50%maturity( W mat )of0.07kg (Table1). Instantaneousnaturalmortality( M )isunknownforlionfish.We usedvaluesof0.2and0.5for M (Table1).Avalueof M =0.5is typicalofshort-livedfishandwassimilartothevalueusedinapast study[14].Thevalueof M =0.2istypicaloflonger-livedspecies andwouldbeindicativeofafishwitha1520yearlifespan:in captivity,themaximumlifespanoflionfishhasbeenrecordedas thirtyyears[29].Weincludedthisrangein M duetouncertainty inlionfishmaximumage.Littledataexistforlionfishintheir nativerange,andtheyhavenotbeenpresentintheinvadedrange forenoughtimetoallowestimationofmaximumage,andthus naturalmortality. Thetotallengthat50%vulnerabilitytoremovalefforts( L vul )has notbeenstudied.Weassumedthatsmallfishwouldbelessvisible andlesslikelytobespottedduringremovaleffortsthanlarger animals;alargerfishbiasistypicalofnearlyallfishinggears. Lionfishareeasilyspeared,butdifficulttocatchonhook-and-line. Itisalsodifficulttospearsmalllionfish,meaningmostcaptureof juvenileswillrequirehandnettingorothermethods.Therefore, weevaluatedharvestscenariosundertwopossiblelengthsat50% vulnerability:159mmTL(age-1)and259mmTL(age-2, Table1. Parametersusedinthesimulationmodel. Parameter ValueDataSource NaturalMortality M instantaneousadultnaturalmortality(yr 2 1 )0.2and0.5Inferred FishingMortality U annualharvestexploitationrate0.00to1.0 Vulnerability L vul lengthat50%capturevulnerability(mm)159(age-1)and259(age-2)Inferred SD low standarddeviationof50%capturevulnerability10%of L vul Inferred Growth L asymptoticlength(mm)425Thisstudy K metaboliccoefficient(yr 2 1 )0.47Thisstudy Length-Weight a length-weightcoefficient2.89 6 10 2 5 Thisstudy b length-weightexponent2.89Thisstudy Recruitment R o averageannualunfishedrecruitment100Scalingparameter CR Goodyearcompensationratio5and15Inferred W mat weightatmaturity(kg)0.07EmpiricalData doi:10.1371/journal.pone.0019666.t001 OverfishingLionfish PLoSONE|www.plosone.org3May2011|Volume6|Issue5|e19666

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Table1).Fishrecruitedtoremovaleffortsaccordingtothelogistic functioninthemodel(Eq.4),andfullyvulnerablefishwere harvestedattherateofannualexploitation( U ). SimulationProtocol Toevaluatetheefficacyoflionfishharvestasaremovaltool,we simulatedarangeofexploitationrates( U =0.051.0in0.05step increments).Weappliedtheseexploitationratestoavarietyof scenariosinordertomodelthefullrangeofuncertaintiesinmodel parameters.First, L vul wassetateither159mmTL(age-1)or 259mmTL(age-2).Then,valuesfor M (0.2or0.5)and CR (5or 15)wereselected.Allpossiblecombinationswereevaluated,and theequilibriumoutputmetricwastheannualfiniteexploitation rate( U )requiredtorecruitmentoverfishthestock( U SPR 0.35 ).For eachscenariowecalculatedthenumberofyearstolionfish recoveryfollowingtheremovalofharvest,definedasareturnto 90%oftheunfishedbiomass.Calculatingrecoverytimeis importantasmanyinvasiveremovalprogramsarefundedonly forshortperiodsoftime.Additionally,todeterminethesensitivity ofSPRtouncertaintyinmodelparameters,wemodeledtheeffect ofa10%increaseinindividualparameterestimatesonSPR. Results Themodelindicatedahighdegreeofvariabilityintheannual finiteexploitationrate( U )requiredtocauseoverfishinginlionfish Figure1.LengthatageforlionfishcollectedfromNorthCarolina. ThevonBertalanffygrowthcurveisshownascalculatedbytheequation: TL a ~ 425 : 2(1 { e { 0 : 47( a z 0 : 5) ) doi:10.1371/journal.pone.0019666.g001 Figure2.Lionfishlength-weightrelationshipforlionfishcollectedfromNorthCarolina. Lionfishtotallength(mm,xaxis)andtotalweight (g,yaxis)relationshipandestimatesof a (2.89 6 10 2 5 )and b (2.89)growthparameters.Model predictedvaluescalculatedas: TW ~ (2 : 89 | 10 { 5 ) TL 2 : 89 doi:10.1371/journal.pone.0019666.g002 OverfishingLionfish PLoSONE|www.plosone.org4May2011|Volume6|Issue5|e19666

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populations.Thisvariabilitydependedontheuncertainparameter valuesof L vul M ,and CR (Table2).Oftheunknownparameters, L vul hadthelargestimpactonexploitationratesthatachieved overfishing(Table3).Lower L vul valuesresultedinasubstantially lower U beingrequiredforoverfishingthanhighervaluesof L vul (Table2).Thus,fishinggearsthatselectsmalllionfishwouldbe moreeffectiveatcausingoverfishingthanthoseremovingonly largefish.Instantaneousnaturalmortality( M )hadthesecond largestimpact(Table3),withahigh M of0.5requiring considerablyhigher U than M =0.2.Thisoccursbecausewhen naturalmortalityislow,exploitationstronglychangesabundance. Whennaturalmortalityishigh,fishnaturallydieatahighrate,so exploitationhasadampenedeffectontotalabundance[20]. Therewasconsiderablevariabilityinyearstorecoveryafterthe cessationofexploitation.Lionfishpopulationsrecoveredfairly quickly(67years)when M andrecruitmentcompensation( CR ) werehigh(0.5and15).Recoverytook1525yearswhenlower parameterestimates( M =0.2and CR =5)wereused.Ifthehigher parameterestimatesrepresentrealisticconditionsforlionfishinthe invadedrange,highlevelsofsustainedfishingmortalitywillbe requiredtocauseoverfishing.Giventhattheoldestlionfishagedin thisstudywasage-8,itislikelylionfishareshort-livedpredators andthatourestimatesof M =0.5and CR =15areappropriate. Withtheseparametervaluesandan L vul of159mmSL,anannual exploitationofatleast35%wouldberequiredtocause recruitmentoverfishing.Atan L vul of259mmSL,a65%annual exploitationwouldberequiredtocauserecruitmentoverfishing. Resultsofthesensitivityanalysisshowedthatuncertaintyin L L vul M ,and K hadthegreatesteffectonSPR(Table3).Thisstudy hadestimatesof L and K fromage-growthinformation,butno dataexiston L vul or M .Thevalueof L vul islargelydependenton thetypeofremovaleffortsused.Speargunsareselectiveforlarger lionfish(S.Green,pers.comm.),andatruefisherywouldbebiased towardslargerlionfishduetohighermeatcontent.Thesesize biasesmightbemitigatedwithtargetedhandnettingofsmall lionfish,ascatchesoflionfishwithacombinationofspearingand handnettinghasbeenfoundtoconcurwithvisualestimatesof lionfishsizedistribution(S.Green,pers.comm.).Anothersource ofuncertaintyistheGoodyearcompensationratio( CR ),but sensitivityanalysissuggestsonlyaminorchangeinSPRwitha 10%increasein CR (Table3). Discussion Modelresultssuggestedthatahighlevelofsustainedremoval wouldberequiredtoreducelionfishpopulationsizesbelowthe SPRthresholdofrecruitmentoverfishing.Scalingtheannual exploitationratetoalionfishperhectareremovalfigurebased uponpublisheddataonlionfishdensity[7,15],suggestsayearly removalof157293lionfishperhectarewouldberequiredto causerecruitmentoverfishingforapopulationbasedon M and CR valuesof0.5and15.Thus,thecontroloflionfishpopulations throughtargetedremovaleffortswillbecostly,anderadication throughremovaleffortsishighlyunlikely.Intensiveremovalsare probablyonlyfeasibleatrelativelysmallspatialscaleswherevery highexploitationrates(i.e., 50%)canbeobtained[14]. Resourcemanagersmaybeabletocontroltheinvasionina waythatlimitstheimpactoflionfishonpreyspeciesandprotects ecosystemfunctionality,therebyprotectingbiodiversityand fisheriesatlocalscales.However,beforeanyremovalprogramis implemented,measurablegoalsandtargetexploitationrates shouldbeclearlydefined,andpilotstudiesshouldbeconducted todetermineifthedesiredresultsareattainable. Localandlarge-scalemethodsofexploitinglionfishcurrently exist,butneedfurtherdevelopment.Onalocalscale,lionfish removaleventsintheUnitedStatesandvariouscountriesofthe Caribbeanhavebeenhighlysuccessfulatinvolvingthepublicand generatingawareness,butestimatingtheexploitationratefrom theseeventsisneededtomeasureefficacy.Onalarge-scale,the creationofafisherywithahighexploitationratemayproduce sustainableandmeasurableresults,buttheinfrastructureand demandforsuchafisherydoesnotcurrentlyexist.However,the efficacyoffisheryremovalswouldbedependentonthesizeat vulnerability.Furthermore,suchalionfishfisherywouldbelimited toshallowwater( 30m)spearfishingandhandnettingaslionfish havealowvulnerabilitytocapturebyhookandline[7].Thisgear anddepthlimitationprovidespotentialrefugiafromfishing, potentiallymakingremovaleffortslesseffective.Lionfisharebeing capturedregularlyasbycatchinreeffishtrapfisheries[7],but feasibilityofalionfishspecifictrapcapableofremovinghigh densitiesoflionfishwithouthighbycatchofnativespeciesis questionable. Thisstudyrevealedkeyknowledgegapsthatshouldguidefuture datacollection.Changesinasymptoticlength( L )andlengthat 50%vulnerabilitytoharvest( L vul )causedthegreatestchangein SPR.Weobtaineddatafor K and L fromNorthCarolina,but Table2. Modelresultsforallcombinationsofpossible L vul M and CR parametervalues. L vul (mm)MCR U SPR 0.35 Recovery(yrs)after U SPR Fishing 1590.5150.356 1590.550.310 1590.2150.2012 1590.250.1516 2590.5150.656 2590.550.509 2590.2150.2511 2590.250.216 Modeloutputsinclude:(1) U SPR ,definedasthefiniteannualexploitationrate( U ) requiredtoreduceSPRtoorbelow0.35;and(2)recovery(inyears)after U SPR doi:10.1371/journal.pone.0019666.t002 Table3. Modelsensitivitytoincreasinggivenparametersby 10%. ParameterSPR%Change M 8% L vul 11% SD vul 0.0% CR 1% K 2 6% a 0% b 2 3% L 2 12% W mat 0.0% Sensitivityanalysisperformedwithstartingvaluesof L vul =159; M =0.5; CR =15; and U =0.35(Table2). doi:10.1371/journal.pone.0019666.t003 OverfishingLionfish PLoSONE|www.plosone.org5May2011|Volume6|Issue5|e19666

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growthparametersforlionfishcoulddifferatmoresouthern latitudes,andthus,moreageandgrowthinformationisneeded throughouttheSouthAtlanticandbroaderCaribbeanregion.No dataexistfor L vul ,andourvalueswerebasedonalogical frameworkforfishesofthissize,aswellaspersonalexperiencesin capturinglionfish.Taggingstudiesshouldbeconductedto evaluatethevulnerabilityoflionfishtovariousfishingand collectionefforts,anditislikelythatvulnerabilitywilldifferby region(e.g.NorthCarolinaversusTheBahamas)aswellashabitat type(e.g.mangrovesversusreefversusartificialstructure).Our modelclearlyshowedthatremovaleffortsshouldfocuson methodstocollectsmalllionfish,whichisinagreementwith othermodels[14]. Ourmodelresultswerealsosensitivetochangesinnatural mortality( M )andtheGoodyearcompensationratio.Nodataexist onlionfishnaturalmortality;therefore,uncertaintysurrounding the M parameterestimateishigh.Thisstudyfollowedpast examples[14]inusingthegeneralliteratureon M tochoosea valueforthemodel.Gatheringdataon M isaclearneedand researchpriority.Estimatesof M couldbeobtainedwithtagging studiesorfromagecompositiondata(i.e.catchcurves)inareas wherelionfisharefullyestablishedbutremovaleffortshavenot occurred(i.e.totalmortality=naturalmortality).Additionally, thereisaneedfordataontheGoodyearcompensationratio( CR ). Althoughthisparameterdidnotaffectthemodelpredictionsas stronglyastheparametersM,L ,and L vul ,nolionfish CR data exist,introducingfurtheruncertaintyinthemodelresults. Themodelwasbasedonasimplifiedviewoflionfishlifehistory, whichincreasedsimulationuncertainty.Lionfishareabletospawn almostcontinuously[7,12,19],andexploitedpopulationsmay receiverecruitsfromdistantsourcepopulationsduetolonglarval duration[7,9,31].Oursimulationdidnotincludecontributionsof larvalsupplyfromareasoutsideofthelocalpopulationtargetedby removalefforts;therefore,populationrecoverycouldoccurmore rapidly.Thesource-sinkdynamicsofthelionfishinvasionneedto bebetterunderstood,asrecruitmentoverfishingwillnotbe possibleifrecruitscomefromsourcepopulationsthatarenot fished.Inthecurrentmodel,thisoccurswhensmalllionfishwith lowvulnerabilitytoharvestareabletospawnbeforecapture. Additionally,thiscouldoccurwithalackofremovalsfromlarge spatialareas,orifsourcepopulationsexistinareasthatare inaccessibletoremovaltechniques(e.g.lionfishlivingatdepths 100m:M.Lesser,pers.comm.). Colonizationfromdistantsourceshasbeendemonstratedbythe successofthelionfishinvasiontodate[2].Recolonizationby removedinvasivespeciesistypicallyrapidandlikelylinkedtotheir reproductivesuccess[32],resultingincostlylong-termcontrol programs,suchaswiththemelaleucatree, Melaleucaquinquenervia (Cavanilles)[33],andzebramussel, Dreissenapolymorpha (Pallas) [34].Conductingconcurrentremovalprogramsinallinvaded areaswouldmitigatethiseffect,butwouldrequirelarge investmentsandmaybeinfeasibleduetotheexpansiveand highlyconnectedinvadedrange. Becauseofthedifficultyofsubstantiallyreducinglong-term lionfishabundancethroughremovals,theeffectsandgoalsof removalprogramsshouldbedeterminedbeforeproceeding.It cannotbeassumedthatanyleveloflionfishremovalwillbe beneficialtonativeaquaticcommunities.Forexample,nobenefits tonativefisheswerefoundafteradecadeofnorthernpike Esox lucius andchannelcatfish Ictaluruspunctatus removalsinthe ColoradoRiverandaninvestmentofseveralmilliondollars [32].Additionally,adultremovalsmaycauseashifttosmaller, morenumerousinvasivepredatorswiththeabilitytoconsume nativefishatearlierlifestages[32,35].Ifthisshiftweretooccurin lionfishoncoralreefs,post-settlementmortalityofnativefish wouldlikelyincrease,potentiallydrivingfutureabundancesdown duetothepopulationstructuringeffectofpost-settlement mortality[36,37,38].Studiesonthebiologyandecologyof lionfish,interactionsintheinvadedcommunity,andtheefficacyof removaleffortsmustbeconductedbeforecommittingresourcesto potentiallyineffectiveremovalprograms. Areasonableandmeasurablegoalforlionfishremovaleffortsis toincreasegrowthand/orabundanceofnativepopulationsthat havebeennegativelyimpactedbytheinvasion.Lionfishare knowntoconsumeandcompeteforfood[30]andpossiblyshelter [6]withnativefishes.Althoughnoresearchontheeffectoflionfish onnativefishgrowthrateshasbeenpublished,itislikelythatthe presenceoflionfishreducespopulationand/orindividualgrowth fornativefishes.Onestudydocumentedincreasedpopulation growthinendangeredCaliforniaclapperrail Ralluslongirostris obsoletus followinginvasiveredfox Vulpesvulpes removal,suggesting thatremovaleffortscanbeeffectiveatreversinganegative populationgrowthratetrajectory[39].Lionfishremovalefforts couldpotentiallyimproveabundanceofnativefaunabyreduced predationandcompetition. Thecomplexityoftheecosystemsinvadedbylionfishmustalso beconsideredbeforeenactingremovalprograms.Ontogenetic habitatshiftsbynativereeffishleadtotheuseofmultipleessential habitattypes[40,41,42]andmakeprotectionofecosystem functionalityanimportantgoal.Manyreeffishspeciesuse seagrassandmangroveasjuvenilehabitat[43,44,45].Lionfishin ajuvenilenurserymayreducetherecruitmentpoolavailableto colonizereefsthroughpredationorcompetition[6]actingin concertwithlionfishpredationoncoralreefs[5,30]tofurther stressreeffishpopulations.Additionally,lionfishmaydifferentially usehabitatsthroughouttheirontogeny.Lionfishinmangrove habitat,forexample,maybesmallerthaninreefhabitat[6], suggestingmangrovesmayfunctionaslionfishnurseries.Iftrue, targetinglionfishinmangrovehabitatwouldfocusremovalsonthe importantjuvenilestage,whilealsoreducingpredationstresson nativesusingthehabitatasanursery.Thisstudycouldbeusedas aguidetodeveloptargetsforsuchcontroleffortsbeforeagencies investinremovalprograms. Acknowledgements WethankK.Shertzer,E.Williams,andP.Marraroandtwoanonymous reviewersformanuscriptreviewandtheCapeEleutheraInstituteand DiscoveryDivingforuseofboatsandequipment,andP.Whitfieldandthe manyNOAAdiversthatassistedwithlionfishcollections.Theviews expressedarethoseoftheauthorsanddonotnecessarilyreflecttheviewof theseindividualsororganizations. AuthorContributions Conceivedanddesignedtheexperiments:ABBMSL.Performedthe experiments:ABBMSL.Analyzedthedata:ABBMSLTKFKDS. Contributedreagents/materials/analysistools:ABBMSL.Wrotethe paper:ABBMSLTKFKDS. References 1.WhitfieldPE,GardnerT,VivesSP,GilliganMR,CourtenayWR,Jr.,etal. (2002)BiologicalinvasionoftheIndo-Pacificlionfish Pteroisvolitans alongthe AtlanticCoastofNorthAmerica.MarEcolProgSer235:289297. 2.SchofieldPJ(2009)Geographicextentandchronologyoftheinvasionofnonnativelionfish( Pteroisvolitans [Linnaeus1758]and P.miles [Bennett1828])inthe WesternNorthAtlanticandCaribbeanSea.AqInv4:473479. 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