Aquatic Invasive Species Vector Risk Assessments: Recreational vessels as vectors for non-native marine species in California
Final Report July 2012
Submitted to the California Ocean Science Trust Funded by the California Ocean Protection Council By: The Aquatic Bioinvasion Research & Policy Institute A Partnership between Portland State University & the Smithsonian Environmental Research Center Gail Ashton, Chela Zabin, Ian Davidson & Greg Ruiz
TableofContents
1.ExecutiveSummary...... 2 2.Introduction...... 5 2.1.TheRecreationalVesselVector...... 6 2.2.HistoryoftheVector...... 8 3.Aims...... 8 4.Methods...... 9 4.1.InvasionHistory...... 9 4.2.ContemporaryVectorOperationinCalifornia...... 12 5.Results...... 14 5.1.InvasionHistory...... 14 InvasionHistoryKeyFindings...... 24 5.2.ContemporaryVectorOperationinCalifornia...... 25 ContemporaryVectorKeyFindings...... 40 6.Discussion...... 41 6.1.InvasionHistory&Impacts...... 41 6.2.CurrentPatternsandProcessesofVectorOperations...... 42 6.3.ManagementReviewandRecommendations...... 43 6.4.Criticaldatagaps...... 52 6.5.KeyManagementRecommendationsforCalifornia...... 52 7.Acknowledgements...... 53 8.References...... 54
1
1.ExecutiveSummary
Background
TheintroductionofnonͲindigenousspecies(NIS)isrecognizedaroundtheworldasathreatto biodiversity,ecosystemservicesandhumanhealth.Californiaisahotspotfortheintroductionof marineNISinNorthAmericaaswellasglobally.Thenumberofnewmarineinvasionsdetectedper decadehasincreaseddramaticallyoverthepastcenturyinCaliforniaandalsoinotherregions.In response,managementofthevectorsofintroductionhasbeenadvancingasthemosteffectiveand efficientmechanismtocurtailthisincrease.Todate,mostvectormanagementhasfocusedon commercialvessels,whichareimportantandactivevectorsofmarineNIStransfers.Inthisregard, Californiahasbeenagloballeaderindevelopingandimplementingmanagementactionstocurbboth ballastwaterandhullfoulingmodesofintroductionbycommercialshipping.Despitethisprogress, othervectorsalsoexist,creatingadditionalopportunityfortheintroductionandspreadofmarineNIS. Thestateisnowseekingfurtherinformationaboutthesevectors,includinghowthevectorsoperate, thelikelihoodofpastandfutureintroductions,andidentificationofopportunitiesforsuccessful interventions.Here,wecharacterizethecurrentstateofknowledgeaboutrecreationalboatingasa vectorinCalifornia,includingadditionalinformationfromotherregions.
Aim
TocharacterizetheoperationandpotentialimportanceofrecreationalvesselsasvectorsforNIS introductionandcoastwisespreadinCalifornia.
Approach
WeusedhistoricalrecordsofNISintroductionsinCalifornia,alongwithrecordsofbiofoulingorganisms associatedwiththehullsandunderwatersurfacesofrecreationalboatsfromglobalstudies,toassess thestateofknowledgeandhistoricimportanceofrecreationalvesselhullfouling.Further,wecollected realͲtimedataonvesselbehaviorandfoulingcommunitiestoassessthecontemporaryandlikelyfuture roleofrecreationalvesselsinthespreadofNISinCalifornia.Finally,wereviewedbrieflysomepotential managementactionsthatcouldreducetheroleofrecreationalvesselsasvectorsofNIS.
Findings
Availabledataindicatethatrecreationalvesselshavebeenanimportantandpotentvectorforthe spreadofNISinCalifornia,aswellasotherregionsaroundtheworld,andthiscontinuestobethecase today.Theopportunitiesforspreadresultfromthelargenumberofvesselsinthestate,their movementsamongbays,andalsothebiofouling(nonindigenous)organismsassociatedwiththe underwatersurfacesofvessels.Approximately800,000900,000recreationalboatswereregisteredin Californiainrecentyears(2008Ͳ2010).Questionnaireresponsesduringthepresentstudy,andresults frompreviousstudies,indicatethat20Ͳ50%ofthesevesselstraveloutsideoftheirhomeportorbay
2 (dependingonstudyandhomebay).AmongtransientvesselsexaminedbyinͲwaterfieldsurveysduring thisstudy(n=49),86%hadfoulingspeciespresentontheirhulls,26%hadhundredsofindividualfouling organisms,andanother25%hadmorethanathousandindividualsorganismspresent.Onaverage,16 specieswereidentifiedfromtransientvesselfoulingcommunities;29%ofthespeciesidentifiedwere considerednonͲnativeinCalifornia;including3speciesthathavenotbeenrecordedfromCalifornia(or theWestCoast).
ThereisaglobalshortageofstudiesontheimpactofmarineNISwhichlimitsunderstandingofthetrue extentofecologicalandeconomicconsequencesofinvasionsduetohullfouling(aswellasother vectors).Ofthefewstudiesthatwereavailable,mostdemonstratedasignificantimpact.Further researchonimpactsiswarrantedandcriticalinsettingprioritiesformanagementresponse(eradication orcontrol),inordertofocussucheffortsonhighͲimpactspeciesofconcern.
Overall,whenconsideringthenumberofrecreationalvesselmovementsandassociatedbiofouling organismsdocumentedontransientvesselsinCalifornia,itisevidentthatrecreationalboats(a)transfer alargenumberofnonͲnativeorganismsthroughoutCaliforniaand(b)contributetothespreadofNIS intoandthroughthestate.GiventhatmanyoftheseNISmaycauseimpactsintheintroducedhabitat, thepotentialconsequencesofcontinuedintroductionandspreadareextensive.
Whereascommercialvessels(andothervectors)mayoftenbeasourceofinitialintroductionsintothe state,recreationalvesselsarelikelytobeespeciallyimportantinfacilitatingcoastwisespreadof invasions.Californiareceivesapproximately5,000Ͳ6,000commercialvesselarrivalseachyearto commercialports,arrivingmostlyfromoverseasandoutsidethestate.Incontrast,weestimatearrivals ofrecreationalvesselsareatleasttwoordersofmagnitudegreater,mostlyfromwithinthestate, providingahighlevelofconnectivity.
Importantly,smallvesselscanaccessharbors,bays,estuariesandcoastlinesthatareinaccessibleto commercialvessels,includingremoteareaswhereothervectors(aquaculture,andthetradein ornamentalspecies,livebaitandliveseafood)canberare.Itisoftennotpossibletopartitionthe sourceofbiofoulinginvasionsamongrecreational,commercial,andfishingvessels.However,the invasionofsmallbays(withoutcommercialvesseltraffic)underscoresthelikelyoverallimportanceof nonͲcommercialvesseltransferstomarineinvasionsinthestate;critically,theabsolutenumberof speciestransfersbyrecreationalvesselsisexpectedtobegreaterinlargebays,wheremorerecreational vesselsarrive,eveniftheexactroleofcommercialversusrecreationalvesselsforparticularinvasionsis notclear.
Recommendations
TherearecurrentlynoguidelinesorregulationsinCaliforniathataimtomanage(reduce)theriskof marinespeciestransfersassociatedwithrecreationalvessels.Inaddition,thereisonlylimited informationonmovementpatternsandassociatedbiotaforthesevesselsinthestate.Thecurrent approachtomanaginginvasionrisksforrecreationalvessels,whichconsistssolelyofeffortstoeducate boatersbyagenciessuchasCaliforniaSeaGrant,andthemultiͲagencyCleanMarinasprogram,which
3 focusesmostlyonreducingchemicalpollution,isinsharpcontrasttothatforcommercialships.This disparityexistsatboththestateandnationallevels.
Werecommendaleadagencybegiventheauthorityandresourcestoevaluate,advance,andassess efficacyofmanagementstrategiestoreducespeciestransfersbyrecreationalvesselsoperatingin Californiawaters.Thiscouldincludevoluntarymanagementpractices,educationandoutreach campaigns,andincentiveprograms.Inadditiontoattemptstoincreasevoluntaryefforts,regulations targetinghighͲriskvesselsatkeycontrolpointsmightbeconsidered,followingtheHazardAnalysisand CriticalControlPoint(HACCP)approach.Thismaybeespeciallyeffectiveforforeignarrivals,asa reportingandinspectionmechanismalreadyexiststhroughCustomsandBorderProtection.Examples ofsimilarprogramsfromAustraliaandNewZealandmayprovideusefulmodelsforCalifornia.
4 2.Introduction
TheintroductionofnonͲindigenousspecies(NIS)isrecognizedgloballyasathreattobiodiversity, ecosystemservicesandhumanhealth(Macketal.2000,Carlton2001,MillenniumEcosystem Assessment2005,Charles&Dukes2007).CaliforniaisahotspotfortheintroductionofNIS(Cohen& Carlton1998;Ruizetal.2011b)onthewestcoastofNorthAmerica,nationally,andglobally.Thehigh numbersofNISinCaliforniarepresentapotentialthreattothehealth,resilienceandproductivityof coastalandoceanecosystems.In2010,theNationalOceansEconomicsProgramvaluedboth Californiascoastaleconomyandoceaneconomyatmorethan$2trillion(www.oceaneconomics.org). Thisvalueincludesindustries(aquaculture,fisheries,tourism,andotherbusinesses)andwagesaccrued fromtheoceanorcoastalenvironments,butexcludesservicesthatarehardertoputavalueon, includingrecreationandhealthbenefits(KiteͲPowelletal.2008),protectionofcoastalcommunities fromstormsandfloods,andclimateregulation(Doneyetal.2009).TheCalifornianOceanProtection Act(2004)statesthat:CaliforniascoastalandoceanresourcesarecriticaltotheStatesenvironmental andeconomicsecurity,andintegraltotheStateshighqualityoflifeandculture.
ThenumberofrecognizedmarineNIShasincreaseddramaticallyinrecentdecadesaroundtheglobe (Ruizetal.2000;Hewittetal.2004),andthistrendislikelytocontinueintheabsenceofmanagement efforts,iftheratesandmagnitudeofspeciestransfersamongregionsexpandwithincreasing globalization.Whileinvasionmanagementplacesapremiumonpreventionofinvasions,asthemost costͲeffectiveanddesirableapproach(Wittenberg&Cock2005),mosteffortshavefocusedhistorically onspeciesͲbyͲspeciesmanagementinsteadofabroaderͲbasedapproachtomanagethevectors (transfermechanisms).Increasingly,scientistsandgovernmentsarerealizingthatavectorapproach allowsthepreventionofintroductionsacrossmanyspeciesgroups,canbeappliedglobally,andoncein placeshouldcontinuetopreventthespreadofNISwithminimalchangesnecessary(Ruiz&Carlton 2003).However,vectormanagementrequiresinformationabouthowthevectoroperates,the likelihoodofintroductionsviathevector,andidentificationofopportunitiesforsuccessfulintervention (managementstrategies).Toguidetheallocationofresources,anassessmentoftherelativeriskofthe vector,comparedtoothervectorsisnecessary.
SinceearlystudiesofmarineNISwerepublished,commercialshippinghasbeenrecognizedasamajor vectorforthespreadofmarinespecies(Carlton1985,Cohen&Carlton1995).Californiastateagencies havebeenamonggloballeadersdrivingguidelinesandregulationstomanageboththeballastwater andhullfoulingsubvectorsofthecommercialshippingvector.TheOceanScienceTrusthasrecognized atleastsixadditionalvectorsthatarepotentiallyimportanttotheintroductionandspreadofNISonthe coastofCalifornia:aquaculture,tradeinornamentalspecies,fishingvessels,livebaittrade,liveseafood tradeandrecreationalvessels.Noneofthesevectorshavebeenthetargetoffocusedmanagement actionsinCaliforniatodate.Inthisreport,weprovideareviewofthecurrentknowledgerecreational vesselsasvectorsforcoastalmarineorganisms,bothgloballyandinCalifornia,andpresentnewdata characterizingthecontemporaryriskofintroductionsassociatedwithrecreationalvesseltransportin California.
5 2.1.TheRecreationalVesselVector
HullfoulingistheprincipalmethodfortheintroductionofNISassociatedwithrecreationalboatsand thefocusorthisstudy.Forrecreationalvessels,speciescanalso(a)becomeentangledonanchors, lines,boatbumpers,andothergear,(b)becarriedamongfishing/divinggear,and(c)becomeentrained inwaterinintakesandothersuchlocations.WhilethesearelikelyrelativelylowͲleveloccurrences comparedwithhullfouling,relativelylittleinformationisavailableatthepresenttimetocharacterize them.
Hullfoulinginvolvestheattachmentoforganismstothesubmergedsurfacesofamarinevessel.Fouling opportunitiesonrecreationalvessels,typicallylessthan50ftlength,differfromthoseassociatedwith commercialvesselsinanumberofways(Table1).Recreationalvesselsarefrequentlyberthedor mooredforlongperiodsinshelteredmarinasandbays(Floerl2002).Thesehabitatsareconducivefor thedevelopmentoffoulingcommunities,whicharelikelytospreadontothevesselhulls(Floerl&Inglis 2003).Thiscontrastswithcommercialvessels,whichareroutinelyinportforarelativelyshortperiodof time(typically<24hrs)andspendmostoftheirtimetravelingbetweenmultipleports(Davidsonetal 2009).However,thewettedsurfaceareaofarecreationalboatismuchlessthanthatofacommercial vessel,andthesizeandintricacyofrecessednicheareas(propellers,thrusters,seachests),wherethe highestdiversitiesanddensitiesoffoulingspeciesoftenoccur,isalsogreatlyreduced.Sailingvessels aregenerallyslowermovingthancommercialvessels,whichmightretainsomespeciesthatcouldbe sloughedoffatthehigherspeedstraveledbymotorͲpoweredrecreationalboatsandcommercial vessels.Thedistancestraveledbycommercialvesselsalsotendtobemuchgreater;thuscommercial vesselsarelikelymoreimportantinmovingspeciesbetweencoasts,comparedwithsmallboats,which mayplayafargreaterroleinmovingspecieswithinaregion.Inaddition,recreationalvesselscanaccess shelteredandshallowharborsthatareinaccessibletolargercommercialvessels,potentiallyallowing transferstolocationsfarawayfrommajorinternationalports.
6 Table1.Comparisonoffactorsthatinfluencethehullfoulingcommunitiesoncommercialand recreationalvessels.
Commercialvessels Recreationalvessels Factorsdetermining Supply&demand Variable: destinations: Tourism/lackthereof Distance/proximity Cost Typically: MajorPorts Marinas/Harbors/Other Schedule: Efficient&Economical Relaxed InͲportduration: Short Long/short Speed: Fast Slow/fast Voyages: LongͲdistance Long/Short DryͲdocking: 2Ͳ5yrs,regulated AdͲhoc LayͲups: Infrequent Frequent Monitoring USCG/NBIC/CBP/Lloyds StateLicensing (Datasources)
CaliforniaisahotͲspotofrecreationalvesselactivitybecauseofitssubstantialcoastline,attractive climateandpositionattheborderwithMexicoandaccesstoandfrommoresoutherndestinations. Approximately900,000recreationalvesselsregisteredinthestateofCaliforniafrom2008Ͳ2009,andthe numberdroppedtoabout810,000in2010.WithintheUS,CaliforniaissecondonlytoFloridain numbersofregisteredboats(www.uscgboating.org).ThenumberofNISrecordedfromCaliforniaisalso high(Ruizetal.2011b).WhilemostNISarerecordedfrombayswithcommercialshippingactivity (Wassonetal.2001,Ruizetal.2009),therearemanysmallerbaysandinletswhichareinaccessibleto commercialvessels,butfrequentlyvisitedbyrecreationalvessels.Thefloraandfaunaofthesewatersis lesswellstudied,thereforethetrueextentofNISmaynotberealized(althoughseedeRiveraetal. 2005).
Hullfoulingofrecreationalvesselsisanuisancetovesseloperations,creatingdrag,blockingintakesand affectingantifoulingefficiency.Tominimizethesenegativeeffects,recreationalvesselownersusually employsomemeanstopreventordelaythegrowthoffoulingspecies.Techniquesincludekeepingthe vesseloutofwaterwhennotinuse,keepingthevesselinaninͲwatercontainmentdevice(e.g.askirtor boatͲbag),orusinganantiͲfoulantsonthehull.AntiͲfoulingpaintisthemostcommonantiͲfouling method,butotherapproachesarealsoused(e.g.,applyingzincstrips,usingsonicdevicesandmaking thehullfromafoulingͲresistantmaterial).Unfortunately,overtime,allofthesemechanismsarelikely tofail,increasingthelikelihoodthatrecreationalboatswilltransportspecies(bothnativeandnonͲ nativespecies)tonewlocations.
7
2.2.HistoryoftheVector
Sincethe1960s,Californiahasbeenrecognizedasahotspotforintroductionsofmarinenonindigenous species(Carlton1979;Cohen&Carlton1998).NewrecordsofmarineNIShavecontinuedtoincrease throughtime(Cohen&Carlton1995,1998;Ruizetal.2000)andthecurrentknownnumberof establishedmarineNISinCaliforniaisgreaterthan257(Ruizetal.2011b).Thisistwicethenumber describedinWashington(n=94)andmuchgreaterthandescribedforOregon(n=75),BritishColumbia (n=62)andAlaska(n=10)(Ruizetal.2011b).ThehistoricsuccessionofNISrecordsindicatesthat CaliforniaisanimportantpointofentryformanymarineNIStothewestcoastofNorthAmerica,with 79%ofallnewNISonthecoastbeingrecordedfirstinCalifornia(Ruizetal.2011b).
Itisoftendifficulttoassignspeciesintroductionstospecificvectors,because(a)theintroductionevent israrelyobservedand(b)multiplevectorsareoftenpossiblefordispersalofagivenspecies.Formarine andestuarinespeciesdescribedinCalifornia,apreviousanalysisattributedonly44%ofintroductionsto asinglevector,basedonlifehistorycharacteristics,locationofintroductionsandtimeofintroduction (Ruizetal.2011b);fortheremainingNIS,multiplevectorswereconsideredpossiblefortheintroduction toCalifornia.VesselshavebeenadominantvectorforintroductionsinCalifornia,boththroughballast waterandhullfouling(Fofonoffetal.2003).Morethan60%ofmarineNISinCaliforniamayhavebeen introducedviahullfouling,withthevectorsolelyresponsiblefor18%ofintroductions,andasoneof severalpossiblevectorsforanadditional42%ofintroductions(Ruizetal.2011b).
3.Aims
WeaimtocharacterizetheoperationandpotentialimportanceofrecreationalvesselsasvectorsofNIS toandalongthecoastlineofCalifornia.Ourdefinitionofrecreationalvesselsfollowsthatofthe DeparmentofMotorVehicles,i.e.,everysailͲpoweredvesselovereightfeetinlengthandeverymotorͲ drivenvessel(regardlessoflength).Theclassexcludescommercialvesselsthatmustbedocumentedby theU.S.CoastGuard,andthosevesselspropelledsolelybyoarorpaddle.Smallercraftsuchaskayaks, canoes,paddleboardsandjetskiscanpotentiallytransferspecies,buttendto1)nottravellong distancesand2)beremovedfromthewaterbetweenuses,diminishingthebuildͲupoffouling.Welimit ourstudytooperationsinmarinewaters(bays,estuariesandnearshorewaters),andfocusexclusively onhullfoulingasthepotentialvector.
WeusedhistoricalrecordsofNISintroductionsinCalifornia,alongwithrecordsofhullfoulingof recreationalboatsfromglobalstudiestoassessthestateofknowledgeandhistoricimportanceof recreationalvesselhullfouling.Further,wecollectedrealͲtimedataonvesselbehaviorandfouling communitiestoassessthecontemporaryandlikelyfutureroleofrecreationalvesselstothespreadof NISinCalifornia.Finally,weassessedmanagementactionsthatcouldbeusedtoreducetheroleof recreationalvesselsasvectorsofNIS.
8 4.Methods
4.1.InvasionHistory
4.1.1.Foulingspeciesassociatedwithrecreationalboatsglobally
WesurveyedthepeerͲreviewedandgrayliteraturefordocumentationofspeciesattachedtoor otherwisetransportedbyrecreationalvessels.ForthepeerͲreviewedliteratureweusedthesearch termsinvasi*ANDboat*,nonͲnativeANDboat*andfoulingANDboatforallyearsin BIOSIS.Wegatheredadditionalliteratureusingreferencescontainedinthesepapers.Manysuch speciesarereportedonlyincidentallyintheliterature,andarethusnotlikelytocomeupinsucha search.Wegatheredadditionalpapersandunpublishedreports(grayliterature)fromreferencesinthe literature,frompersonalknowledgeandfromdiscussionswithcolleagues.Wealsocorrespondedwith authorsforfurtherinformationnotdetailedinthepublishedliterature.Moststudiesdidnotdistinguish betweenrecreationalandfishingvessels,soweincludedallrecordsofspeciesfromsmallboats.
Speciesortaxawereenteredintoadatabasealongwiththelocationanddatewheretheywerefound. Whenavailable,wealsorecordedlifestagefound,whethertheywereonresident,visiting,recreational orfishingboats.Forthisanalysis,wedidnotattempttodeterminewhetherthereportedspecieswere nativeornonͲnativetotheregioninwhichtheywerefound,aswewishedtosimplyassessdiversity reportedonvessels.Taxawereenteredintoadatabaseandorganizedintohighertaxonomicgroups. Weusedthreeinternetsitestoassistwiththeseclassifications:AlgaeBase,IntegratedTaxonomic InformationSystem,andtheWorldRegisterofMarineSpecies.Wheretherewasdisagreement betweenthesesystems,weusedAlgaeBaseastheauthorityforthealgae,andforinvertebratesAbbott etal.1997(tunicates)andCarlton(2007).HigherͲleveltaxonomicclassificationwasbasedonPearseet al.(1987).
4.1.2.RecordsandpatternsoffoulingspeciesintroductionsinCalifornia
AsubsetoftheNationalExoticMarineandEstuarineSpeciesInformationSystem(NEMESIS)wasusedto assesshistoricrecordsofmarineNISinCalifornia.NEMESIShasbeendevelopedinternallyatthe SmithsonianEnvironmentalResearchCenter(SERC)asaresourceforinformationonnonͲnative(or exotic)speciesthatoccurincoastalmarinewatersoftheUnitedStates.Thedatabaselistsreported species(basedonstandardizedliteraturesearches),theircurrentpopulationstatus(i.e.,whether establishedornot),aswellaswhen,where,andtheputativevector(s)associatedwitheachinvasion event;italsosummarizeskeyinformationonthebiology,ecology,andknownimpactsofeachtaxa listed.VectorclassificationsforeachspeciesinNEMESISwerebasedonspeciescharacteristicsandthe operationofavectorwithinabay(SeeAppendix1fordetails).Characteristicsoffoulingspecies include:broadcastspawning;abilitytoattachtoasurfaceorbuildatubeforshelter;filterfeeding;anda toleranceofmediumͲenergyenvironments.WeusedthespeciesͲvectordesignationsassignedbySERC, asrecordedinthedatabase.Withinthedatabase,foulingwasasinglevector,anditwasnotpossible todistinguishbetweenfoulingofrecreational,commercialorfishingvesselsasvectors,exceptforsmall bayswherecommercialvesselswereabsent.
9 Previously,allrecordsofNISinCaliforniahadbeenscrutinizedandtheirlocationmoreaccurately mappedatawatershedlevelbySERC.TheseCaliforniarecordswereextractedintoaprojectdatabase. Wemadeseveralfurtheramendmentstothedatabasepriortoanalyses,andthedatawereevaluatedin anumberofways.SanPabloBay(SPB)isnotdistinctfromSanFranciscoBay(SFB)intermsofits recreationalboattraffic(alltrafficmustpassthroughSFBtoreachSPB).Acomparisonbetweenspecies recordedbyNEMESISaspresentinSPBandSFBshowedthattherewerenospeciespresentinSPBthat werenotrecordedpreviouslyinSFB.Forthesereasons,thedataforSPBwerenotincludedinanalyses. MontereyBayincludesthreeindependentmarinasystems:MontereyHarbor,ElkhornSlough(including MossLandingHarbor)andSantaCruzSmallCraftHarbor.Theseweretreatedasindependentbaysin ouranalyses;additionalresearchwasusedtodetermingspeciespresenceineachsystemandthe appropriatedateoffirstrecord.
ToexaminepatternsofspreadofNISovertimeandspace,weanalyzedtheNEMESISdatainseveral ways.ThedecadalrateofnewNISrecordsforCaliforniawascalculatedfor(a)allNIS,(b)thoseNISwith foulingasapotentialvector,and(c)thoseNISwithfoulingasasolevector.Tocomparethestrengthof thefoulingvectortononͲfoulingvectorsinaspatialanalysisamongbays,weusedthreevectordivisions (foulingasasolevector;foulingpossible;foulingnotavector)ofNISandcomparedtherelative contributionofeachvectordivisionamong42differentbaysalongthecoastlineofCalifornia.The numberofrecreationalvesselberthsinabay(determinedusinginternetsearchesandtelephoning marinas)wascomparedtothenumberoffoulingspeciesrecordedinthebayusingSpearmansrank correlation.
Toassesstheimportanceofdifferentbaysasintroductionentrypointsforthestatethroughtime,the speciesweredividedbythedecadeandlocationofthe1strecordwithinthestate,andthedecadeof1st recordwithineachbay.
SeveralanalyseswereimplementedtoassesstrendsofspreadinCalifornia.Dateoffirstrecordinabay wasusedtolinkthebaysinsequentialintroductioneventsandestimatethestrengthoftheconnection betweenbaypairs.BecauseoftherecognizedimportanceofSanFranciscoBayasanentrypointforNIS tothestate(Ruizetal.2011b)itwasusedasafocalpointtoassesswherespeciesspreadafterbeing recordedinSFB.SimilaranalyseswereperformedforSanDiegoandHumboldtBaytolookforpatterns ofnorthernandsouthernspread,respectively.Speciespresencedatawereusedtocreatea resemblancematrixofthebaysusingBrayCurtissimilarityindices,interpretedusingclusteranalysisin Primer6.
4.1.3.ImpactsoffoulingͲmediatedinvaders
WesearchedthepeerͲreviewedscientificliteratureforcrustaceanimpactsstudiesontheNEMESISlist fornonͲnativespeciesestablishedinCalifornia.AlgaeandmolluscswerereviewedbyUCDavis(UCD). Thesethreebroadtaxonomicgroupsmakeupasignificantportion(>50%)ofthenonͲnativespeciesin California.
10 BothSERCandUCDusedthefollowingapproachforthesesearches,enteringresultsintoanidentical database.SearcheswerecarriedoutbetweenNovember2011ͲMarch2012(molluscsandalgae)and FebruaryͲApril2012(crustaceans).
WeusedthefollowingsearchtermsinBIOSIS:
Topic=(AdventiveORAlien*ORBioinvasi*ORBiosecur*ORExotic*ORForeignORIntroduc* ORIncursion*ORInvad*ORInvasi*ORNonendemic*ORNonendemic*ORNonindigenous ORNonindigenousORNonnative*ORNuisance*ORPest*ORPest)AND
Topic=(speciesnameinquotes,e.g."Ficopomatusenigmaticus")ANDTimespan=1926Ͳ2011.
Searcheswerealsocarriedoutusingsynonymsforthecurrentspeciesname.WeusedWoRMS(World RegistryofMarineSpecies)forlistsofsynonyms.Weperformedaninitialsortbyreadingthroughthe returnedtitles(>95%ofpapersformostspecieswerenotrelevant).Wesortedsecondarilybyreviewing abstractsandobtainingarticles.Datafromtherelevantimpactstudieswereextracted,andpaperswere retainedforpotentialfurtherreviewandanalysis.
4.2.ContemporaryVectorOperationinCalifornia
4.2.1.Vesseltraffic:volumeandtravelpatterns
ThereisnosinglesourceofinformationonsmallͲvesseltrafficforCalifornia.Allvesselsarrivingto CaliforniafromoutsideoftheUSmustregisterwithCustomsandBorderProtection(CBP).Registration detailsincludethelastportofcall,nextportofcall,andshipcharacteristics(e.g.,type,length).A FreedomOfInformationAct(FOIA)requestwassenttoCBP,askingforallrecordsconcerningarrivalsof smallvesselstoCalifornia.Therequestincludedallarrivalsin2009and2010,bydateandarrivalport.
Tostudyvesselfluxatalocalscale,eightkeymarinasalongtheCaliforniacoastwereusedasstudy marinas.Themarinaswereselected(a)tocoverthelengthofthestate,(b)fortheirimportanceasa destinationfortransientvesselswithinabay,and(c)fortheavailabilityoftransientvesseldata(the latterinformationwasestablishedduringpreliminaryconversationswithamuchlargernumberof marinas).Studymarinaswere:thePoliceDock,SanDiego;SantaBarbaraHarbor;MontereyHarbor; PillarPointHarbor,HalfMoonBay;SouthBeachHarborandPier39Marina,SanFranciscoBay;Spud PointMarina,BodegaBay;andHumboldtBayHarbor.DatafromMonterey,PillarPoint,SouthBeach andSpudPointhadbeencollectedpreviously;theadditionalmarinaswereaskedtoproviderecordsof transientvesselarrivalswithallconfidentialinformationremoved.Mostmarinaswereabletoprovide thisinformationinanelectronicdatafile;forSanDiegoandHumboldtitwasnecessarytoenterthedata frompaperrecords.
Atleastoneyearofdatabetween2007and2011wasavailableandcollectedfromeachmarina.Data includedavesselidentifier(registrationnumberand/orvesselname),dateofarrival,dateofdeparture, vesseltype,thevesselownershomestateandzipcode(countryifoutsideoftheUS).Typicallythese
11 dataarecollectedfromvisitingboatownersuponpaymentforuseofaberth,andthusshouldbeavery accuraterecordofvisitorsstayingonenightormore.Wherepossible,vesseltypewasusedtoisolate recreationalmotorandsailvesselsfromothertransientvessels(includingfishing,patrolandresearch vessels).Unfortunatelyvesseltypewasnotprovidedreliablyacrossmarinas;forexample,SpudPoint Marinainparticularisamarinathatisrecognizedasimportantforfishingvessels,buttransientboat recordsdidnotincludevesseltype.
Thesedatawereusedtoassesstrendsintheseasonalarrivalofvessels,frequencyofvesselarrivalsfrom differentsourcelocations,durationofstays,andthenumberoftimesvesselsvisitedanygivenmarina withinthetimeperiodofthedata.Vesselidentifiersweredifferentamongmarinasandcouldnotbe usedtotrackvesselsthroughCalifornia.
4.2.2.Boaterhabits:travelandhullmaintenance
Anonlinesurveywasdeveloped,reviewedandapprovedbySmithsonianInstitution,andusedtocollect informationonboaterhabits(http://tinyurl.com/SERCsurvey).Therewere3categoriesofquestions basedonthoseusedinpreviousstudiesinCaliforniaandglobally:1)vesselinformation(type,length andhomemarina),2)hullmaintenancepractices,and3)vesseluse.Theonlineversionwasadvertised widelyanddidnotrequirethequestionnairetobemailedoutorreturnedbymail(savingcostsand resources).Thesurveywasadvertisedinmailoutsfromseveralofthestudymarinas,onsailingclub socialnetworksontheinternet,andonthewebsiteofLatitude38,apopularWestCoastsailing magazine.
Wecomparedtheresponsesinthecurrentstudytothreeearlierstudies.Davidsonetal.(2008and 2010)usedawrittenquestionnairesimilartothecurrentonetosurvey221boatersin14marinasinSan FranciscoBay.Zabinetal.2011revisedthequestionnaireslightlyandsurveyed394boatersinthree additionalSanFranciscoBaymarinas(selectedbecausetheyhadactivesailingcommunities)andat threenearbysmallcoastalharbors(SpudPointinBodegaBay,PillarPointinHalfMoonBay,and MontereyHarborinMonterey).
4.2.3.Biofoulingcommunitiesontransientboathulls
ThecontemporaryfluxoffoulingspeciesarrivingtoCaliforniaonrecreationalvesselhullswasassessed byinͲwatersamplingoftransientvessels.SantaBarbaraHarborandtheSanDiegoPoliceDockwere selectedasfocalmarinasforthesesurveys,aswehadpreviouslysampledvesselsinSanFranciscoBay andMonterey(Zabinetal.2011)andsuspectedfoulingcommunitiesandtravelpatternstodiffer betweenregionsinthestate.AlltransientvesselsarrivingwithinaoneͲweekperiod(repeatedtwo timesatSanDiego)wereinterviewedusingthequestionnairedescribedabove,andaskedwhetherthe ownerwouldpermitustodoaninͲwatersurveyusingSCUBA.Whenpermissionwasgranted(~95%of vessels),2Ͳ3diverscompletedaninͲwatersurveyofthevesselhull.Thesurveyinvolvedtakingpictures ofallunderwaterhullsurfaces,concentratingonnicheareasandlocationswherehullfoulingwas present;notesweremadetodocumenttheextentoffoulingforthewholevessel.Inaddition,all foulingspecieswerecollectedwhenpossible(asubͲsamplefocusingoncollectedorganismsthat appearedtobedifferentbasedonmorphologywastakenonthefewvesselswherefoulingwas
12 extensive).SampleswereinitiallysortedintomorphoͲtaxa,ormorphologicallydistinctiveorganisms, shortlyaftercollectionandpreservedforfurtherprocessingtospecieslevel(orlowesttaxonomiclevel possible).Certaingroupsweresenttoexperttaxonomistsforidentificationorconfirmation.
Usingthephotographsandnotes,wholeͲvesselabundanceestimatesweredescribedasoneofsix abundancecategories.ThecategorieswerebasedonalogͲscaleestimateofabundancerangingfrom1Ͳ 10organismsto>100,000organisms(individualsorcolonies).Aseventhcategoryofzerobiotawasalso included.Imagesofallnicheareaswereusedtomeasurepercentcoverofbiofoulingpernichearea. FivephotoͲquadratsofhullsurfaceswereselectedatrandomtogenerateameasureofpercentcoverof thehull.HullquadratimageswereprocessedusingapointͲcountmethodof100dotssuperimposedon theimage.
5.Results
5.1.InvasionHistory
5.1.1.Foulingspeciesassociatedwithrecreationalboatsglobally
Fewstudieshavebeendonethatfocusonthespeciestransportedbyrecreationalvessels,andmost thatdoexistonlyasreportstofundingagencies.Manymorereportsofsinglespeciescollectedfrom boatsarelikelytoexist,buttheyareburiedinthetaxonomicandotherliteratureandmanywerenot exposedduringtheliteraturesearch.Converselywefoundnumerouspapersthatsuggestedyachtsasa transportmechanismbutdidnotdocumentfoulingextentorspeciescompositiondirectly.Wefound23 papersorreportsrecording455marineorbrackishwaterorganismscollectedfromsmallvesselsfrom 12countries(includingresidentandtransientvessels;Appendix2,specieslistplusreferences).Asa group,foulingspeciesrepresentabroadspectrumoflifeformsandtrophiclevels,includingbothsessile (attached)andmobiletaxa.Insomecases,organismswereidentifiedtospecieslevel,inothercases descriptivetermssuchasgreenmacroalgaeorfishwereused.Conservatively,thiswouldappearto represent243distinctanimal,protist,andplantspeciesortaxain15phyla(Fig.1).
13 80 70 60 50 Species of
40 30
Number 20 10 0
a s) a a a a d t d es t yt i zoa o th hy hyta hyta el acles) o (fish) t rifera n p p p n icate erma o rotistao (mobile) Bry n Cnidaria P mi P r do An u od Molluscaema l lo o (barn (t n N h i yhe C Rh Anthoph oda da t p ata Chordata Ech la po P ord h Heterokonto C Arthrorthro A
Figure1.Thenumberofspeciesbybroadertaxonomicgroupreportedfromsmallvessels.
Mobilearthropodswerebyfarthelargesttaxonomicgroup,withatleast76distincttaxareported.Over halfofthesespecieswereamphipods,withsmallernumbersofisopods,decapods(exclusivelycrabs) andcopepods.Annelids,nearlyallpolychaetes,madeupthesecondlargestgroup,with34distincttaxa. Therewere33bryozoanspeciesand24tunicates.Barnaclesmadeupasignificantgroupwith17 speciesreported.Thethreehighertaxonomicgroupsofalgaecombinedrepresentedabout24distinct taxa.
ThemostͲreportedtaxonwasafolioseformofthegreenalgaUlva,whichwasrecordedsixtimes.The arborescentbryozoanBugulaneritinawasreported5times.Eachofthesemayactuallyrepresent multiplespecies,asB.neritinaisnowrecognizedasaspeciescomplex,andthereareseveralspeciesof Ulva(whichnowalsoincludesspeciesformerlyinthegenusEnteromorpha).ThetunicatesBotrylloides violaceus,BotryllusschlosseriandDiplosomalisterianum,thebarnacleAmphibalanusamphitrite,and thebryozoanWatersiporasubtorquatawereeachreportedfourtimes.
Thereareseveralpossibilitiesforbiasesotherthananorganismsabilitytoattachtoandtravelonboats thatcouldleadtodifferencesinthenumberoftaxaperphyluminthisliterature,includinggeographic locationwherestudiesweredone,taxonomicexpertiseandinterest,andthenumberofspeciesinthe phylum.EightofthestudiesweredoneinNorthAmerica,and7inEurope,withmostoftheremainder inAustralia/NewZealandorHawaii(Table2).Mostoftheresearchersalsohavetaxonomicexpertisein invertebrategroupsratherthaninalgae.
14 Noreportsevaluatedtheconditionofthespeciesreportedfromhulls,althoughsomenotedthe presenceofgravidindividuals,eggs,larvae,andjuveniles,indicatingthatatleastsomeofthespecies presentwerecapableofreproducinganddispersingintothelocalenvironment.
Table2.Locationandyearofpublicationofstudiesreportingfoulingspeciesfromsmallvessels.
Continent Geographicregion Yearofstudy(s) Europe Belgium 2002 France 2008 Netherlands 2001 Ireland 2006,2007 Italy 2006 NorthAmerica SEAlaska 2010 BritishColumbia 2011 California 2009,2010,2011 Hawaii 2004,2009 PrinceEdwardIsland 2009 SouthAmerica Brazil 2007 Curacao 2007 Australasia Australia 2005 NewZealand 2002
5.1.2.RecordsandpatternsoffoulingspeciesintroductionsinCalifornia
TheprojectͲspecificdatabaseconfirmsthatinvasionsinCaliforniahavecontinuedtoincreaseoverthe lastdecade(Fig.2).SixtynewNISwererecordedinthe1990sandthetotalnumberforthe2000s(for whichdataisincomplete)islikelyhigher.Foulingspeciesareanimportantcontributortothese numbers,bothforspecieswithfoulingasasolevector(13%ofspecies),andasoneofmultiplevectors (51%;Fig.2).TherelativecontributionoffoulingspeciestothetotalpoolofNISinCaliforniahas remainedsimilaroverthelast100years.
15 70 AllSpecies 60 Foulingpossible 50 Foulingonly
40 records NIS
30
New 20
10
0 <1900 1900s 1910s 1920s 1930s 1940s 1950s 1960s 1970s 1980s 1990s 2000s
Decade
Figure2.DecadalrateofmarineNISrecordsforCalifornia.Speciesareseparatedintothosewith foulingastheonlypossiblevector(triangles)thosewithfoulingasoneofseveral possiblevectors(circles)andallNIS(diamonds).Shadedareasindicateatimeinterval differentfrom10years(allyearspriorto1900;2000Ͳ2006).
SanFranciscoisanobviousoutlierinCalifornia(andforthewholeWestCoast)intermsofbothmarine NISandthosewithfoulingasavector(Fig.3).Therearerecordsofatleast274marineNISinSan FranciscoBay:172ofthesehavefoulingasapotentialvector,66havefoulingasasolevector.Thebays withthenexthighestnumbersofmarineNISincludethecommercialshippingbaysofHumboldt, Calleguas(PortHueneme),SanPedro(LosAngelesͲLongBeach)andSanDiego;andthosewithahistory ofbivalveimports,e.g.,TomalesBayandElkhornSlough.Regardlessofwhetherspecieshavefoulingas apotentialvector,themostNIShavebeenrecordedfrombayswithmultiplevectoropportunities. MissionandSantaMonicaaretheonlytwobayswithoutahistoryofcommercialshippingorbivalve culture,butwithmorethan50NIS.Lessthan50NIShavebeenrecordedineachoftheotherbays, whererecreationalboatingisconsideredthedominantpotentialvector.
ThenumberoffoulingNISrecordedinabayissignificantlycorrelatedtothenumberofrecreational berthsavailableinthatbay(Spearmansr<0.001forbothfoulingͲonlyandfoulingͲpossiblespecies;Fig. 4).However,mostbayswithlargenumbersofberthsalsocontaincommercialshippingports,including SanFrancisco,SanPedroandSanDiegobays.Thus,thereareseveralfactorsthatlikelycovarywiththe numberofrecreationalberths,includingthenumberofcommercialshippingvesselarrivalsandballast waterdischarge,humanpopulation,shorelinedevelopment,etc.ItisdifficultͲtoͲimpossibletodiscern betweentherelativeimportancesofthesefactors,inparticulartherelativeimportanceofcommercial versusrecreationalvesselsasavectorforfoulingspecies.
16 Forthepast100years,mostfirstrecordsofNISwithfoulingasapossiblevectorforthestatehavebeen infourbays:SanDiego,SanPedro,SanFrancisco,andHumboldt(Fig.5).Thisdistinctionislessapparent whensubsequentrecordsareconsidered(Fig.6).Yearsinwhichhighnumbersofspeciesnewtoabay arereported(asopposedtoanewrecordforthewholestate)reflectsurveyefforts,e.g.,surveysby Wassonetal.(2001)inElkhornSlough,Boydetal.(2002)inHumboldtBayandFaireyetal.(2002)and Needles(2007)inMorroBay.
Theadditionalanalysesfailedtorevealanyclearorsignificanttrendsinintroductionsequenceor speciessimilaritybetweenbays.Onlythesummaryoftheseextensiveanalyseswillbedescribedhere:
x Neighboringbaysdidnotsharethemostspecies,norwererecordsofthesamespeciesinclose succession.
x WhenusingSanFranciscoasapointsource,morespecieswerenotsharedwithbaysthatwere close,andthepatternofdecadeofrecorddidnotsuggestthatthespecieshadspreadto neighboringbaysfirst(i.e.,noevidenceofgradualspreadtobaysatincreasingdistancesfrom SanFrancisco).
x Therewasnoclearpatternofsequentialintroductionsingeographicaldirection,i.e.,eitherfrom northandsouthofthestateorfromSanFranciscoBay(SFB)asapointsource.Whenlookingat progressiveintroductionsfromthenorthandsouth,SanFranciscowassomewhatdistinguished inthatmostspeciesdidnotspreadnorthorsouthwithoutbeingrecordedinSFB,butthetrend wasdistortedbythebiasedsequenceofintroductionrecords(influencedbydatesofsurveys).
x Fewspeciesweresharedbetweenbaysinthefarnorthandsouthofthestate,butsimilarity indicesdidnotgroupthebaysbygeographicregion,presenceofalternativevector,oranyother factorthatcouldbedetermined.
Therewasnocorrelationbetweenthenumberofbaysinwhichaspecieshasbeenfoundandthe numberofvectorsthatcouldberesponsibleforitsdistribution(e.g.Watersiporasubtorquatahasbeen introducedto19baysbyfouling;CodiumfragilesspfragileisonlyinSanFranciscoBay,buthas5 potentialresponsiblevectors).
SanFranciscohadbyfarthelargestnumberofspeciesthathavenotbeenintroducedelsewhereinthe state(137of175speciesonlyreportedfromonebay,includingthosenowextinctorfailed introductions).HumboldtBayhadthenexthighestnumberofuniquespecies(n=8)followedbySan Pedro(n=6)SanDiego(n=5)andTomalesBay(n=4).
17 North SmithRiver KlamathRiver FoulingOnly MadͲRedwood FoulingPossible HumboldtBay $ * Mattole AllVectors EelRiver BigNavaroͲGarcia RussianRiver GualalaͲSalmon BodegaBay TomalesͲBodegaBay TomalesBay $ TomalesͲDrakesBay DrakesEstero $ SanFranciscoCoast(N) SanFranciscoBay $* SanFranciscoCoast(S) SantaCruz ElkhornSlough $ MontereyMarina Carmel CentralCoastal(N MorroBay $ CentralCoastal(S) SanAntonio SantaBarbaraChannel Ventura Calleguas * LosAngeles(N) SantaMonicaBay SanPedroChannel LosAngeles SanPedroBay * SantaAna NewportBay $ NewportBay(outer) AlisoͲSanOnofre SanLouisReyͲEscondido SanDiego(N) MissionBay SanDiegoBay * TijuanaEstuary South 050100150200250300 NumberofMarineNIS
Figure3.SpatialdistributionofmarineNISamongCaliforniabays(arrangednorthtosouthfromtop tobottom).Specieswithfoulingasasolevector(white),foulingasoneofseveralvectors (grey)andthosewithvectorsnotincludingfouling(black)areshownseparately.*indicate bayswithbusycommercialports;$indicatebayswithahistoryofbivalveimportsfor aquaculture.Dashedlineindicates50NIS,referredtointhetext.
18 Smallvesselberths
Ͳ30000 Ͳ25000 Ͳ20000 Ͳ15000 Ͳ10000 Ͳ5000 0 North SmithRiver KlamathRiver MadͲRedwood HumboldtBay Mattole EelRiver BigNavaroͲGarcia RussianRiver GualalaͲSalmon BodegaBay TomalesͲBodegaBay TomalesBay DrakesEstero SanFranciscoCoast(N) SanFranciscoBay SanFranciscoCoast(S) SantaCruz ElkhornSlough MontereyMarina Carmel CentralCoastal(N MorroBay CentralCoastal(S) SanAntonio SantaBarbaraChannel Ventura Calleguas LosAngeles(N) SantaMonicaBay SanPedroChannel LosAngeles SanPedroBay SantaAna NewportBay NewportBay(outer) AlisoͲSanOnofre SanLouisReyͲEscondido SanDiego(N) MissionBay SanDiegoBay TijuanaEstuary South 050100150200250300350400 MarinefoulingNIS
Figure4.DistributionofmarineNISwithfoulingasasole(white)orpossiblevector(grey)among Californiabays.Thenumbersofsmallvesselberthsinthebayareshownontherightaxes. Baysarearrangednorthtosouthfromtoptobottom.
19 1850s 1870s 1890s 1900s 1910s 1920s 1930s 1940s 1950s 1960s 1970s 1980s 1990s 2000s SmithRiver MadͲRedwood North HumboldtBay Mattole BigNavaroͲGarcia GualalaͲSalmon BodegaBay TomalesBay TomalesͲDrakesBay DrakesEstero SanFranciscoBay SanFranciscoCoast(S) SantaCruz ElkhornSlough MontereyMarina Carmel CentralCoastal(N MorroBay CentralCoastal(S) SanAntonio SantaBarbaraChannel Ventura Calleguas LosAngeles(N) SantaMonicaBay SanPedroChannelIslands LosAngeles SanPedroBay SantaAna NewportBay NewportBay(outer) AlisoͲSanOnofre SanLouisReyͲEscondido SanDiego(N) MissionBay SanDiegoBay
South TijuanaEstuary
No.newrecords 1 2Ͳ5>5
Figure5.LocationanddateoffirstrecordsofmarineNISinCaliforniawithfoulingasapossiblevector. Baysarrangednorthtosouth.
20 1850s 1860s 1870s 1880s 1890s 1900s 1910s 1920s 1930s 1940s 1950s 1960s 1970s 1980s 1990s 2000s
h SmithRiver KlamathRiver Nort MadͲRedwood HumboldtBay EelRiver Mattole BigNavaroͲGarcia GualalaͲSalmon RussianRiver BodegaBay TomalesͲBodegaBay TomalesBay DrakesͲTomalesBay DrakesEstero SanFranciscoCoast(N) SanFranciscoBay SanFranciscoCoast(S) SantaCruz ElkhornSlough MontereyMarina Carmel CentralCoastal(N MorroBay CentralCoastal(S) SanAntonio SantaBarbaraChannel Ventura Calleguas LosAngeles(N) SantaMonicaBay SanPedroChannelIslands LosAngeles SanPedroBay SantaAna NewportBay NewportBay(outer) AlisoͲSanOnofre SanLouisReyͲEscondido SanDiego(N) MissionBay h SanDiegoBay
Sout TijuanaEstuary
No.newrecords 12Ͳ56Ͳ10 11Ͳ20 20Ͳ30 30+
Figure6.LocationanddecadeoffirstrecordsoffoulingmarineNISwithfoulingasapossiblevector withineachbay(speciesmayhavebeendescribedelsewhereinCApreviously).
21 5.1.3.ImpactsoffoulingͲmediatedinvaders
LiteraturesearchesusingBIOSISwerecompletedfor94foulingspeciesandtheirsynonyms,including53 crustaceans,22molluscsand20algae(Appendix6,thelattertwogroupsprovidedbyUCD).Alldata werereportedunderthecurrentspeciesname(synonymsarelistedinAppendix6).BIOSISreturned titlesfor68species,butonfurtherreviewoftheabstractsandarticlesonly134papersconcerning22 specieswereconsideredrelevant.The22speciesincluded7algae,9crustaceaand6molluscs.The earlieststudyretrievedwaspublishedin1926(Miller1926)butalmost60%oftheimpactstudies(n=80) werepublishedinthelast5years,since2006.
Thenumberofrelevantpapersperspeciesrangedfrom1to30(30forthealgaSargassummuticum). OtherspecieswithalargenumberofsuchpapersincludethealgaCodiumfragilesspfragile(n=25),the EuropeangreencrabCarcinusmaenas(n=24)andtheshipwormTeredobartschi(n=17).
OneͲthird(34%)ofimpactpapersdescribedstudiescompletedintheUSA,andonethirdofthese(10% ofthetotal)wereconductedinCalifornia(n=14).OverhalfofallstudiesdescribedimpactsofnonͲ nativespeciesonnativespecies(56%).Impactstonativecommunities(12%)ecosystemprocesses(7%) andthewholecommunity(native/nonͲnativenotspecified,5%)werealsocommonlystudied.Almost halfofthestudies(48%)werebasedonexperimentalanalyses,includingfieldandlaboratory experiments.Theremainingstudiesweremostlymensurative(40%,measuringimpactswithno manipulation),orobservational(11%).
StudiesoftheimpactofNISvarygreatlyacrossspeciesandstudy.Forexample,theimpactsof Sargassummuticum,thefoulingspeciesforwhichthegreatestnumberofstudieswereretrieved,were firststudiedin1982inCalifornia(Ambrose&Nelson,1982).Thisisalmost40yearsafterthefirst observationofthealgaoutsideitsnativerangeinBritishColumbiain1944(Wallentinus,1999).Impact studieshavebeenreportedfromseveralcoastlinesinEurope(includingtheAtlanticandtheNorthSea) andbothcoastsofNorthAmerica.Thearticlesrangefromdescribingasingleimpactonasinglespecies orcommunity(e.g.,Ambrose&Nelson,1982),tothoseonabundance,speciesrichness,diversity, evennessandcompositionofmultipledifferentcomponentsofthecommunity(e.g.,mobileepifauna, sessileepifauna,epibiota,Harriesetal.2007).MoststudiesontheimpactsofSargassummuticumwere ofimpactsonnativespeciespopulations,butincludestudiesofbiogeochemistry,physicalhabitatand nativespeciesresponse(e.g.abehavioralorphysiologicalresponse).
Theimpactsofasecondspecies,Teredonavalis,awoodͲboringbivalve,werefirstrecordedbyMiller (1926).ThestudywasoftheeconomicimpactofthespeciesonstructuresinCalifornia.Noother relevantimpactstudiesofthisspecieswerefound.
The14studiesoffoulingspeciesimpactsrecordedfromCaliforniainclude7species(Sargassum muticum,Batillariaattramentaria,Musculistasenhousia,Mytilusgalloprovincialis,Teredonavalis, CarcinusmaenasandSphaeromaquoyanum).ThestudiesspanthecoastbetweenBodegaBayandSan DiegoBay,includingSanFranciscoBay,BolinasLagoonandSantaCatalinaIsland.Thelagbetweena speciesbeingdescribedinCalifornia,andthefirstimpactstudybeingpublishedvariedbetween10years (C.maenas)and103years(S.quoyanum);themeanlagwas41years.Theimpactedentitiesinclude
22 nativespecies(moststudies),ecosystemprocesses,communityandtheeconomy.Papersdescribeboth experimentalandmensurativestudies,inbothfieldandlabsettings.Moststudiesreportedstatistical analysestodemonstratethesignificanceofanyeffects.Mostpapers(87%,n=26)demonstrateda significantimpactonthestudiedentity.
5.1.4.InvasionsHistoryKeyFindings
x ThenumberofNISrecordedinCaliforniahascontinuedtoincreaseinrecenttime.
x Importantly,64%ofNISrecordedinCaliforniatodatemayhavebeenintroducedbyhullfouling (ofallvesseltypes).
x BayswithhighnumbersofrecreationalboatsalsohavehighnumbersofNISbutthetrendis confoundedbyotherfactors,includingmultiplevectorsactinginthesebays,highhumanpopulation densityandlargeareasofmanͲmadesubstrates.
x InCalifornia,SanFranciscoisanoutlierintermsofhighnumbersofmarineNIS,foulingNIS,and NISnotrecordedelsewhereinthestate.
x Agloballiteraturesearchrevealedonly23papersofbiofoulingorganismsonsmallvessels, recording455marineandbrackishwaterorganismscollectedfromthesevesselssampledin12different countries.
x ThereisalsoaglobalpaucityofdataconcerningtheimpactofmarineNIS,makingitdifficultto evaluateimpactsassociatedwithhullfoulingorothervectors.
x OfthestudiesavailableontheimpactsofbiofoulingNIS,87%reportedasignificantimpact,and 56%ofallstudieswereofimpactsonnativespecies.
23 5.2.ContemporaryvectoroperationinCalifornia
5.2.1.Vesseltraffic:volumeandtravelpatterns
InresponsetotheFOIArequesttoCustomsandBorderProtection(CBP),wereceivedonepageof summarydata(Appendix2).Thesedataindicatethatfrom2009Ͳ2010,2183vesselsarrivedinCalifornia fromforeignlastportsofcall.Arrivalsfollowedaseasonalpattern,beingmostfrequentfromMarchto Junewithasecondary,smallerincreaseinOctober(Fig.7).SanDiegowasthemostcommonportof registrationforthesevessels(Fig.8).Noinformationregardingthecountryofregistrationorlastportof callofforeignvesselswasprovided.
OncomparisonwithfiguresreceivedindependentlyfromLongBeachandMonterey,itwasdetermined thatthesummarydatadidnotincludeallarrivals.Afurtherrequestfortherawdatawasmetwitha propositionofreceiving24,000pagesofrawdatasheets,butmostoftheinformationwouldbeblackedͲ outundertheFederalPrivacyAct.Informationconcerningsmallvesselsisnotcollectedinan automatedorelectronicmethodbyCBP,thereforedigitalversionsofthisdatawerenotavailable.We didnotpursuetheFOIArequestfurtherandthusremainlimitedinourunderstandingofforeignvessel arrivalstoCalifornia.Wealsolearnedanecdotally,inconversationswithlocalboaters,thatmanydonot reporttoCBPwhenreͲenteringtheUS(e.g.,returningfromMexico)becausetheprocedureistootimeͲ consuming,andtheremayalsobelittleͲtoͲnoriskofbeingcaughtorreprimanded.
Wecollecteddataon9758transientvesselarrivalsfromeightmarinas.Dataincludeddateofarrival, durationofvisit,vesseltypeandownerscityand/orZIPcode.RecreationalboatingactivityinCalifornia wasgreatestduringthesummerseasonbetweenMayandSeptember(Fig.9).Thispeakwasevident bothinthenumberoftransientvesselsarrivingtomarinasandthenumberofboatsmakinglocaltrips (authorspers.obs.).FarfewertransientvesselsarrivebetweenDecemberandMarch.Theseasonal trendiscommontoallstudymarinas(Appendix3),althoughthesummerincreasewaslessapparentat SanDiegoPoliceDock,wherethenumberofarrivalsremainedhighthroughouttheyear.Thereasonfor theyearͲroundtransientboatarrivalsatSanDiegoisnotknown,butimportantfactorsmayinclude:a southernlatitudewithlessclimatevariationthancentralandnorthernCaliforniaandtheproximityto theMexicanborder,whichmakesitapopularstopforvesselsonlongerͲdistancevoyageswhichdonot followtheseasonsinthesamewayasvesselsonshorterͲdistancevoyages.
Noneofthestudymarinasaskedforthehomeportoftransientvesselsduringregistration.Weusedthe registeredhomeaddressasacoarseproxyforthehomeportofthevessel.Therelativeimportanceof differentsourceregionswascommonacrossmarinas(Appendix4)thussourceregionsforallmarinas areshowncollectivelyinFigure10.Homeaddresswasnotalwaysrecordedsohomeportcouldnotbe inferredforapproximately11%oftransientvessels(Fig.10).ThemajorityofboatswerefromWest CoaststatesandBritishColumbia(79%;Fig.10),indicatingastrongcoastͲwisevoyagetrendfor transientvesselsinCalifornia.Inparticular,morethan70%ofvesselswereonvoyagesfromhome locationswithinCalifornia(althoughtheymayhavevisitedotherlocationsonthevoyage,e.g.,Mexico).
ForhomeaddresseslistedinCentralCanada,CentralUSA,AtlanticUSAandtheCaribbean(Fig.10),it wasimpossibletodeterminethevesselshomeportandarrivalroute.Vesselsmayhavebeensailed,
24 trailered,orkeptatalocationremotefromthehomeaddress.VesselsfromNevadaandArizonamake upapproximately50%ofvesselsfromCentralUSAstates.ForvesselsfromAsia,EuropeandAustralia, theregistrationdataaccompanyingthehomeaddress(e.g.,vessellicensenumber,CustomsandBorder Protectioncertificate)suggestedthatthevesselshadsailedfromthelistedhomecountry.Vesselsfrom thesesourcesmakeuplessthan1%ofthetotalnumberoftransientvesselrecordstothestudy marinas.
Transientvesselsusuallystayinmarinasforashortperiodoftime(67%ofvesselsstayed1Ͳ2days);the southernandmoreoutercoastharborsofSanDiego,SantaBarbaraandMontereyhadmorevessels stayingforlongerthanaweekwhencomparedtomarinasinSanFranciscoBay.PillarPoint(HalfMoon Bay)andHumboldtHarborhadahighernumberofvesselsthatstayedforoverthreeweekscompared toothermarinas,thatnumberwasstilllowrelativetothosestayingfor1day.Mostvessels(>60%atall marinas)onlyregisteredatanygivenmarinaonceinthetimeperiodforwhichwehaverecords.An additional10Ͳ20%visitedamarina2Ͳ3timesandasmallpercentage(0Ͳ5%)visitedmorethan10times.
200
180 160
140 120
100 Arrivals 80 60
40 20
0 Jan Mar May Jul Sep Nov Jan Mar May Jul Sep Nov Jan Mar May
2009 2010 2011
Fig7.MonthlyarrivalsoftransientvesselsfromforeignlastportsofcalltoCalifornia,n=2535(data fromCBP).
25 Fresno
Oakland
SanFrancisco
SanJose
PortHueneme
LosAngeles
LongBeach
SanDiego
050010001500200025003000
Arrivals
Fig8.PortofregistrationfortransientvesselsfromforeignlastportsofcalltoCalifornia,n=2535(data fromCBP).
25 SD) Ͳ 20 (+/
15 arrivals of
10 percentage 5 Mean 0 JFMAMJJASOND
Fig9.VariationinmonthlyarrivalsoftransientvesselstomarinasalongtheCaliforniacoastline.Data areaverage(+/ͲSD)monthlypercentagesofasingleyearstotalarrivals,fromtheeightstudy marinas(n=6961).
26 AK BC WA OR CA Mexico HI Caribbean Central(USA) Central(Canada) Atlantic(USA) Asia Europe Australias Unknown
020 60 80 100
. Meanpercentage(+SD)
Fig10.LocationofhomeaddresseslistedbytransientvesselsarrivingtoallmarinasontheCalifornian coastline.Dataarethemeanpercentageofvesselarrivalsfromsevenstudymarinas(+SD; n=9758).
5.2.2.Boaterhabits:travelandhullmaintenance
5.2.2.1Boatuse
Ofthe349boaterswhorespondedtooursurvey,78%weresailboatowners,19%ownedamotorboat, 2%categorizedtheirboatsasother,and2%werefishermen.Justunderhalfoftherespondentswere fromSanFranciscoBay(169);44respondentswerefromelsewhereinCentralCalifornia,andthe remaining136werefromSouthernCalifornia(southofSantaBarbara).Wehadnoresponsefrom boatersnorthofSanFranciscoBay.
Threehundredsixteenboatersreportedmakingatotalof8,320tripsinthepastyear.Ofthese,81%of tripsweremadeintheboatershomebays(6,708);theremaining20%wereovernightstaysawayfrom homebaysforoneormorenights(1,612).
Onaverage,the291boaterswhoreportedhavingmadeatleastonetripintheirhomebaymadejust slightlyfewerthan2tripsamonth(23.1tripsayear,SE+/Ͳ1.45).FortyͲtwopercentofboatersmade fewerthan12tripsayear;68%made24orfewer(Fig.11).Someboaters,however,mademanytrips: 11%madebetween49Ͳ100trips;onlyafewindividualsreportedmorethan100tripsinayear. Reportedboatusagewasslightlylowerthanoneearlierreport(55%ofboatersmaking24orfewertrips
27 ayear,Davidsonetal.2008,SFBayboatersonly);butslightlyhigherthananother(76%making20or moretripsayear,Zabinetal.2011,boatersfromSFBayandsmallnearbycoastalharbors),seeTable3.
FiftyͲfourpercentofboaters(162)alsoreportedhavingmadetripsoutsideoftheirhomebaysinthelast year,witheachboateronaveragemaking11.4suchtrips(SE+/Ͳ1.33).Thispercentageishigherthan twopreviousstudiesintheSFBayarea,whichfoundthatthevastmajorityofboatersstayedexclusively intheirhomebays(Table3,24%ofboaterstraveledoutsidehomebay,Davidsonetal.2010,SFBay only;19%,Zabinetal.2011,boatersfromSFBayandnearbycoastalbays).Itispossiblethattheonline surveymethodattractedaslightlydifferentandmoreactivegroupofboatersthanthemailͲout,mail backsurveysusedinourpreviouswork.Inthepresentstudy,36%ofSFBayboatersreportedleaving thebay.TheinclusionofSouthernCaliforniaboaters,whoappeartobemoreactive,alsoincreasedthe overallaverage.SeventyͲonepercentofboaterswhoreportedmakingtripsoutsideoftheirhomebays madefewerthan12ayear;90%ofboatersmade24orfewer(Fig.12).Onlyafewindividualsreported morethan50suchtrips.
Themajorityoftripsawayfromhomewereforlessthanthreedays(62%ofallreportedtrips),andmost trips(97%)werelessthanoneweeklong(Fig.12).However,severalboatersreportedtripsofamonth orlonger.Themostfrequentlyreportedtripdurationwasoneday(24%);moreboatersreportedsingleͲ daytripsinourtwopreviousstudies(Table3).
Table3.Acomparisonofkeymetricsbetweenthepresentstudyandtwoearlierstudies.
Davidsonetal. Zabinetal. Metric Thisstudy 2008 2011 %ofboatersusing boatsmorethan2 32% 46% 24% timesamonth %ofboaterswhotravel 54% 24% 19% outsidehomebay Mostfrequently 1day(24%) 1day(51%) 1day(48%) reportedtripduration
28 boaters of Number
Numberoftripsinthepastyearinsidehomebay Numberoftripsinthepastyearoutsidehomebay
Figure11.Numberoftripsmadeinthepastyearbyboatersinsidetheirhomebays(left)andoutside theirhomebays(right).Datafromboaterquestionnaires s p Tri of Number
Figure12.Durationoftripsoutsidethehomebayofreportedbyboatersinthepastyearmonths. Datafromboaterquestionnaires.
5.2.2.2.Voyagepatterns
Boatownersprovideddestinationinformationon8,230trips.81%ofthesetripsweremadein respondentshomebays.TheChannelIslandswerebyfarthetopdestinationfortravelingboatersfrom mostbaysfromSantaBarbarasouth;410tripswerereportedthereinthepastyear,comparedto63 tripsmadetoMexicoandNewportBay,whichweretiedforthesecondͲmostvisiteddestination(Table 4).SanFranciscoCoastalSouth(whichincludesHalfMoonBay)andSanPedrowerethethirdmost frequentedharborswith37visitseach.SanDiegoBaywasalsohighlyvisited;32tripswerereported, makingitthefourthmostͲvisitedbay.
29 WiththeexceptionofthepopularityoftheChannelIslands,asageneralpattern,moretripsweremade tobaysnearaboatershomeport.Thispatternismorepronouncedwhenthenumberofboatsmaking tripsratherthanthenumberoftripsareconsidered(Table5).Forexample,theveryhighnumberof tripsfromCalleguastoNewportBaydisappearswhenboatsratherthantripsareconsidered,indicating thatasingleboatwasmakingallofthosetrips.However,therewasastrikingandsurprisingexception tothispattern:boatersfromSanFranciscomadeasmanytripstoMexicoasdidboatersfromSanDiego, withtwiceasmanyboatsfromSanFranciscoasfromSanDiegomakingthistrip.
Ourpreviouswork(Davidsonetal.2008,2010;Zabinetal.2011)indicatedthatHalfMoonBayisthetop overnightdestinationofSanFranciscoboaters,asdoesthisstudy.However,ourearliersurveys indicatedthatpointsimmediatelynorth(DrakesEstero,TomalesandBodegaBays)andinMontereyBay (SantaCruzandMonterey)werethesecondͲmostvisitedlocations.TripsfromSanFranciscotoMexico wererarelyreported.
30 Table4.Thenumberoftripsreportedbyboatersfrom15homebays(leftcolumn)tovariousWestCoastlocations(rows).Bluehighlighted cellsaretripswithinaboatershomebay.Theredtoyellowgradientindicatesthemosttoleastnumberoftripsbetweenpairsof locations.Dataarefromboaterquestionnaires. South coastal Bay Bay Escondido Coastal Ͳ Rey Onofre Drakes Bay Bay Islands Islands Ͳ Salmon Bay Bay Coastal Ͳ Estero Bay Total Pacific Monica Barbara Cruz Ͳ San Ͳ Francisco Francisco Pedro Louis Diego Farallon Bodega Drakes Tomales Tomales Gualala WA Canada HI Trans (blank) Grand Santa Calleguas Ventura Channel Santa Central Monterey Morro Santa San San Aliso Newport San Mission San Home Mexico San SanDiego 26 598 16 7 1 5 5 3 38 1 700 MissionBay 30 30 AlisoͲSanOnofre 7 11 3 252 22 11 45 2 1 1 355 NewportBay 8 154 7 43 212 SanPedro 22 41789 1674 41 272 SantaMonicaBay 2 2 3 5 8 454 87 7 568 Calleguas 1 1 2 25 212 241 Ventura 1 126 30 6 163 ChannelIslands 1 11 12 SantaBarbara 1 1 2 83 537 2 9 635 CentralCoastal 132 136 MorroBay 1 2 51 3 1 3 61 SantaCruz 663292 4 347 SanFranciscoCoastalSouth 1 1 SanFrancisco 26 15 4 1 10 4 2 1 17 1 285 11344299958721143 394519 Totallocal 598 30 252 154 178 454 212 126 537 132 51 329 4299 7352 Totaltransient 63 321612 18 63 37 19 2 8410 7 31611 1837 21958721144348885 8237 Table5.Thenumberofboatsmakingtripsfrom15homebays(leftcolumn)tovariousWestCoastlocations(rows).Bluehighlightedcellsare tripswithinaboatershomebay.Theredtoyellowgradientindicatesthemosttoleastnumberoftripsbetweenpairsoflocations. Dataarefromboaterquestionnaires. Coastal
South
North
Bay
Escondido Bay Coastal
Ͳ
Rey Onofre Bay
Drakes Bay
Islands Is Ͳ Bay Salmon
Bay Coastal
Ͳ
Estero
Bay
Total
Pacific
Monica Barbara Cruz
San Ͳ Ͳ Diego Louis Pedro Francisco Francisco
Newport Santa Mission Santa Farallon Tomales San Santa Central San Aliso Mexico San Monterey Morro WA Canada HI Trans (blank) Grand Tomales Gualala San Calleguas Ventura Channel San Home Bodega Drakes San Diego 937631 3 11131 75 Mission Bay 1 1 AlisoͲSan Onofre 34 2167 4 12 1 1 151 Newport Bay 28 3 7 20 San Pedro 21 3153 1203 21 51 Santa Monica Bay 2121220 12 2 42 Calleguas 11 11 3 7 Ventura 1 48 1 14 Channel Islands 1 3 4 Santa Barbara 11 22336 1 266 Central Coastal 33 Morro Bay 1 16 1 1 111 Santa Cruz 22 4 1 1 10 San Francisco Coastal South 1 1 San Francisco 18 9 2 1 1 3 2 1 9 1 1 6 4 7 21 278 5 3 7 3 2 1 1 4 3 7 400 Total Local 37 1 16 8 15 20 3 4 3 36 3 6 4 278 756 Total Transient 34 18 66 8 17 11 8 2 61045 2 96102 7 53732114414
32
5.2.2.3.Hullmaintenance
TwohundredninetyͲtwoboatersrespondedtoquestionsabouttheirhullmaintenancepractices.Of these,38%ofboatersreportedhavingappliedantiͲfoulingpaintwithinthepast12months.Anearly equalpercentage,35%,hadhullpaintolderthan2years.Meanpaintagewas23months,SE+/Ͳ2.21.
Sixtypercentofboaterswhoansweredquestionsaboutpainttypereportedusingcopperbasedpaints, while<2%usedTeflonorsiliconeͲbasedpaints.Sixtyindividualsreportedusinghardpaintcomparedto 70whocheckedablativeorselfͲpolishing.Ablative(orselfͲpolishing)paintsworkbysloughingoff whiletheboatisunderway.However,onaverage,boaterswhoreportedusingthistypeofpaintdidnot travelmorefrequentlythanboaterswhoreportedusingahardpaint:usersofablativepaintmade28 tripsperyear,(SE+/Ͳ3.91,meanincludes5whodidnottravel);usersofhardpaintmade29.7tripsa year(SE+/Ͳ3.21,meanincludes12whodidnottravel).
TwohundredfortyͲnineboatersansweredquestionsaboutcleaningtheirhullsinbetweenhaulͲouts: 48%ofboatershadcleanedtheirboatswithinthepastmonthand66%hadcleanedinthepast2 months;meantimesincelastcleaningwas2.2months,SE+/Ͳ0.22.InͲwatercleaningwasbyfarthe preferredmethod(86%cleanedinthisway).About40%ofrespondentsusedaprofessionalcleaning service(Fig.13).Manualcleaningusingbrusheswasthemostcommonlyreportedcleaningmethod.
FortyͲtwopercentofboatershadcleanedORpaintedinthepastmonth(of325boaterswhoanswered oneorbothofthesequestions);66%haddonesointhepast2months,and87%haddonesowithinthe pastyear.Meantimesincelastcleaningorpaintingwas5.9months,SE+/Ͳ0.81.
Figure13.Hullcleaningmethodsemployedbyboatownersrespondingtothequestionnaire. TherewasnodifferenceinmeanpaintagebetweenCentralCaliforniaandSouthernCaliforniaboaters (SouthernCalifornia=SantaBarbaraandsouth,splitbasedondifferencesinmeanwatertemperature). InSouthernCalifornia,meanpaintagewas23.7months(SE+/Ͳ2.1);itwas23.6months(SE+/Ͳ2.1)in CentralCalifornia.However,SouthernCaliforniaboaterscleanedmorefrequently(timesincelast cleaninginSouthernCaliforniawas1.38months(SE+/Ͳ0.15)vs.CentralCalifornia,whereitwas2.90(SE +/Ͳ0.40).Thisdifferenceisstatisticallysignificant(T=Ͳ3.57P<0.0005,df=156).Timesincelastcleaning orpaintingwasalsoshorter(SouthernCaliforniamean2.64month(SE+/Ͳ0.54)vs.CentralCalifornia mean8.6(SE+/Ͳ1.4),andthisdifferencewasstatisticallysignificant(T=Ͳ3.98,P<0.0005,df=222).This mayreflectdifferentratesofgrowth,possiblyvaryingwithtemperature.
AllmaintenanceintervalsreportedbyCentralCaliforniaboatersinthecurrentstudywereshorterthan twoearlierreports.Davidsonetal.(2010)foundthatmeanpaintageacross14SanFranciscomarinas was27months(SE+/Ͳ2.22),timesincelastcleaningwas3.1months(SE+/Ͳ0.82),andtimesincemost recentpaintingorcleaning(whicheverisless)was8.7months(SE+/Ͳ1.16).Zabinetal.(2011)who surveyedboatersfromSanFranciscoBayandnearbythreesmallcoastallocations,alsofoundaverage paintage,timesincelastcleaningandtimesincepaintingorcleaningtobehigher:23.2(SE+/Ͳ1.22),4.9 (SE+/Ͳ0.65)and9.6(SE+/Ͳ0.91)monthsrespectively.Again,thismayindicatethattheonlinesurvey reachedadifferentandperhapsmoreactiveboaterdemographic.
5.2.3.Biofoulingontransientboathulls
Wesampled49transientrecreationalvesselsinͲwaterusingSCUBAduring2011and2012.Twelvewere sampledinSantaBarbaraHarborand37inSanDiego(atthePoliceDock).
5.2.3.1.Biofoulingcomposition
Inthefield,anaverageof16morphoͲspecieswereidentifiedpervessel,withnumbersrangingfrom0to 72(Fig.14).Bryozoans,pericarids(e.g.,isopods,amphipods)andascidianswerethemostfrequently sampledtaxonomicgroups(Fig.15);polychaetesandcirripeds(barnacles)werealsocommonamong samples.
SERCstaffidentifiedbryozoans,cirripeds,andascidianstospecies(orgenusinsomecases).Thealgae, hydroids,pericarids,decapods,andpolychaetesweresenttotaxonomicexpertsforidentification.Alist ofspeciesidentifiedfromrecreationalboathullsinthisstudyisshowninAppendix5(n=169).39%of speciesidentifiedwerenativetoCalifornia;26%werenonͲnativebuthavebeendescribedfromthe coastpreviously;27%couldonlybeidentifiedtogenus(juvenilesorlackingtaxonomiccharactersto identifyfully)andothermembersofthatgenusareknowntobepresentinCalifornia;thebiogeography of12species(7%)isundeterminedandthesespeciesweredescribedascryptogenic.Speciesofnote areshowninTable6.WerecordedthebryozoanHippoporinaindica,whichhasnotbeenidentified fromthewestcoastofNorthAmericapreviously(L.McCannperscomm.);membersofthepolychaete genusBranchiommahaveonlyrecently(since2008)beendescribedfromtheWestCoast,inCalifornia, andanewspeciesofthisgenusisnotedhere(Branchiommasp.2Harris;thetaxonomyofthisgenus
34 needsrevisionthusnospeciesnamesareprovided,L.Harris,perscomm.).Asecondpolychaete,Syllis sp.37Harris,exhibitsanovelcombinationofpigmentpatternandmorphologicalfeaturesandappears tobenewtothearea.OtherspeciesthatareofinterestincludetheascidianBotrylloidesperspicuum andpolychaetePileolariatiaratawhichhaveonlybeendescribedfromSouthernCaliforniatodate.A smallbladeofUndariapinnatifida,alargekelpthathasinvadednumerouslocationsinCalifornia,and aroundtheworld,wasalsofoundonaboathullinSanDiego,alocationinwhichitisnotyetreportedto beestablished.Aredalga,Dasyasessilis,whichhasinvadedserveralEuropeancountriesinassociation withaquaculturepractices(Hugheyetal.2009)andhasbeendemonstratedtodecreasenativealgal diversity(WilliamsandSmith2007),wasalsorecorded.InCalifornia,thisspeciesisknownonlyfrom SouthernCalifornia.
Table6.NonͲindigenousspeciesofnotecollectedfromrecreationalboathullsduringinͲwater surveys.
Species Comments Botrylloidesperspiccum OnlyrecordedfromSouthernCaliforniatodate. Pileolariatiarata OnlyrecordedfromSouthernCaliforniatodate. Undariapinnatifida FoundonaboathullinSanDiego,alocation whereitisnotyetreportedtobeestablished. Dasyasessilis OnlyrecordedfromSouthernCaliforniatodate. Brachiommasp.1Harris OnlydescribedfromtheWestCoast,inCalifornia, since2008 Brachiommasp.2Harris NewrecordfortheWestCoast(maybeanew species) Syllissp.37Harris Exhibitsnewcolorationandappearstobenewto thearea. Hippoporinaindica NotyetrecordedfromthewestcoastofNorth America
35 14
12
10 vessels 8 of 6
Number 4
2
0 012Ͳ56Ͳ10 11Ͳ20 21Ͳ30 31Ͳ40 40Ͳ50 >50
NumberofmorphoͲspecies Figure14.MorphoͲspeciesidentifiedfromrecreationalvesselhullsinthefield(initialIDsarenot alwayscongruentwithfinaltaxonomicIDs).Numberofvessels=49.
25 Arthropoda 20 samples 15 of Algae 10 Cnidaria Mollusca 5 Percentage
0
ta te id a n n e yta r o a zoa oa a h ae di o oz anch nta yoz i ropod a ophy rripede erica sc dr Bivalve t ibr oriferaPl r i DecapodP Br A P lo C Anth Hy Gas Ch Rhodop Polych Nud Nemerte Platyhelminth Heterokontophyta Figure15.TaxonomicdiversityofsamplescollectedfromrecreationalvesselhullsinSantaBarbara andSanDiego.Numberofsamples=718.Highertaxonomicgroupingsareindicatedby dashedlines.
5.2.3.2.Biofoulingextent
Aminorityof14%oftransientvesselssampledduringthisprojecthadnodetectablemacroͲfaunaor macroͲalgae(Fig.16).Usingcategoricalabundanceestimates,wefoundthat22%ofvesselshadonly isolatedindividualsontheirsubmergedsurfaces,whileafurther12%hadbetweenelevenand100 organisms.Themostcommonextentcategoryrecordedcomprisedofboatswithbetween101and 1000organisms(26.5%ofvessels).Nearly25%oftransientvesselssampledhadmorethan1000 organisms,especiallythevesselsattheupperendofthedistributionthathadhundredsofthousandsof
36 individualsandcolonies(Fig.17).Theseextensivebiofoulingassemblagesaremoreoftenassociated withresidentorlaidupvessels(authorspersonalobservations),butweobservedfivevesselswithover 10,000organismseach,suggestingthatasignificantminorityofvesselstransportverylargequantitiesof biotafromharbortoharborontheircoastaljourneys.
Asrecordedinoursandotherspreviousstudies,biofoulingtendedtooccurmoreoftenonnicheareas ofvesselsratherthanhullsurfaces.Thiswascertainlytrueforvesselsthatwererecordedinthelower abundancecategories(1Ͳ10,11Ͳ100,101Ͳ1000organisms;Fig.18).Vesselsinthehigherabundance categories,however,tendedtohavefoulingonbothhullandnonͲhullsurfaces.Onthemostheavily fouledvessels,therewasanincreaseintheaveragepercentcoveroffoulingonhulls,butalsoawide variabilityinfoulingonhulls(Fig.18),reflectingthepatchynatureoffoulingcoveronlaminarsurfacesof heavilyfouledboats.
For46ofthe49sampledvessels,wehadcorrespondingquestionnairedatawithresponseson antifoulingpaintage.Antifoulingpainthadbeenappliedwithinthreeyearsofsamplingforamajorityof vessels(87%).Therewasasignificantcorrelationbetweenantifoulingpaintageandabundanceof foulingorganismsonhulls(r=0.521,p<0.001;Fig.19).Therewasalsoamajorityofvesseloperators reportingsomemaintenanceactivity(hullcleaningorpaintapplication)within12monthsofsampling (90%),butthecorrelationbetweenbiofoulingextentanddurationsincelastmaintenancewasnot significant(r=0.265,p>0.05).
30 n=49boats
boats 25 20
sampled 15 of 10 5 Percent 0 0 0 0 + 10 10 00 000 000 01 to to 1 0, 0, ,0 1 1 to o1 10 100 1 101 1t to 100 001 10, Categoricalabundanceestimate
Figure16.Frequencyoftransientvesselswithdifferentbiotaabundancecategories.Thisplotshows theproportionofsampledboatsthatwereassignedtooneofsevenabundancecategories. Underwaterobservationsandsubsequentassessmentsofimageswereusedtoassigneach boatintoalogͲscalecategoryoforganismabundance.
37
Figure17.BiofoulingobservedduringSCUBAsurveysoftwotransientrecreationalvesselssurveyedin SanDiego.
100 hulls on 80 cover 60
40 fouling
20 Average 0 0123456 Rankofabundancecategories
Figure18.Comparisonofbiofoulingpercentcoveronhullswithwholevesselbiofoulingextent.The categoriesoffoulingabundancecorrespondtothesevencategoriesoutlinedinFig.17(where rank1correspondstoabundance1to10,rank2toabundanceof10to100,andsoon).The percentoverofbiofoulingonhullstendstoincreaseonextensivelyfouledvessels,but variationincoveralsoincreases.
38 80
60 (months) age 40 paint
20 Antifouling 0 0123456 Rankofabundancecategories Figure19.Comparisonofbiofoulingabundancewithreportedageofantifoulingpaint.Thecategories offoulingabundancecorrespondtothesevencategoriesoutlinedinFig.17(whererank1 correspondstoabundance1to10andsoon).Therewasasignificantcorrelationbetween paintageandextentoffouling(seetext).
5.2.4.ContemporaryVectorKeyFindings
x ThereisnocentraldataresourceconcerningthemovementsofrecreationalboatsinCalifornia. Availabledatasuggestthatmorethan1000vesselsarrivetothestatefromforeignlastportsofcall annually;arrivalsofvesselsfromUSportsmaybe100timesgreater. x Morethan70%oftransientvesselsarrivingtofocalmarinasinourstudywerefromhomeports inCalifornia. x Althoughoursurveysindicated~81%ofvesseltripsremainwithintheboatershomebay,54% ofboatersreportedtravelingoutsideoftheirhomebayinthelast12months. x TheChannelIslandswerethetopdestinationfortransientvoyages;othertripswerecommonly tobaysnearaboatershomeport,withpopulardestinationsincludingMexico,NewportBay,HalfMoon BayandSanPedro. x Inoursurvey,42%ofboatershadcleanedorpaintedtheirboatinthepastmonth(87%within thepastyear),butthismaybeasignofthediligence(bias)ofthoserespondingtothequestionnaire ratherthanthegeneraltrend. x Amongtransientvesselssampledduringthisproject,only14%werecleanofmacroͲfouling.On mostvessels,wedetected100sofmacroͲfoulingorganisms,and25%hadmorethan1000ofthese organismspresent. x Biofoulingwasmostcommoninnicheareas. x Almost1/3ofspeciescollectedfromhullswereconsiderednonͲnativetoCalifornia,including newrecordsforCaliforniaandtheWestCoast.
39 6.Discussion
RecreationalvesselshavebeenanimportantandpotentvectorforthespreadofNISinCalifornia,as wellasotherregionsaroundtheworld,andthiscontinuestobethecasetoday.Boatingcontinuestobe oneofthemostpopularformsofrecreationinCalifornia,withnearlyonemillionvesselsregisteredfor useinthestateduringrecentyears(2008Ͳ2010).Manyofthesevesselstravelamongembaymentswith biofouling(nonindigenous)organismsassociatedwiththeunderwatersurfacesofvessels,expandingthe opportunitiesfordispersaloforganisms.Leftunchanged,thecurrentoperationofthisvectorwillresult inincreasingthespreadandimpactsofmarineNISinCaliforniaovertime;thishumanͲmediated dispersalincreasesimpactsbecause(a)thegeographicfootprintofinfestedareaswillincreasethrough time,(b)somesubsetofNISwillhavesignificantecologicaloreconomiceffects,and(c)thecumulative impactistheproductofperͲcapitaeffectsXareaaffected(Parkeretal.1999).
6.1.InvasionHistory&Impacts
Despitethemagnitudeofrecreationalboating,anditsroleinthespreadofNIS,theglobalknowledgeof thisvectorsactivityandassociatedNISremainssurprisinglylimited.Wefoundonly23studiesof recreationalboatfoulingcommunitieswhichdescribespeciesabundanceandcomposition.Manyof thesewerelimitedintaxonomicscopeandmostdidnotdistinguishbetweennativeandnonͲnative speciesrecorded,whethertheboatssampledwereactive,residentsorvisitors,orwhethertheboats wereyachtsvs.smallerfishingvesselsthatmightbekeptinmarinas.Thestudieswerealso geographicallyrestricted.Nonetheless,theavailableinformationdocumentsover400speciespresent onthesevessels,andthisisclearlyagrossunderestimateoftheactualspeciesdiversityinmotion.
PrimaryintroductionstoCaliforniafromoutsidethestatearegenerallyrecordedfrombayswith commercialshippingandorahistoryofaquacultureactivity.Secondaryspreadlikelyoccursby numerousvectors;unfortunatelytheresolutionofdatesofarrivalandnumberofpotentialvectorsdoes notallowustodeterminetherelativeimportanceofrecreationalboating.
Confoundingthestudyofrecreationalhullfoulingisthedifficultyinisolatingtransportviarecreational boatsfromthatofcommercialorfishingvessels.Bayswherecommercialvesselaccesswouldbe excluded(duetochanneldepthorwidth)haverarelybeensurveyedformarineNIS.Exceptionstothis inCaliforniaincludeastudyofElkhornSlough(whereoysterculturecouldhavebeenamajorvector historically;Wassonetal.2001)andastudyofNationalMarineSanctuariesandNationalEstuarine ResearchReserves(deRiveraetal.2005).Bothofthesestudiesfoundhighnumbers(ч50)ofNISin habitatswherecommercialvesselsaregenerallynotactive(arrivalsfordredging,constructionandin somelocationsfishingvesselactivitycannotbeexcluded).ThestudiesandtheNEMESISdataasa wholesuggestthatrecreationalboatshavebeenanimportantvectorinthehistoricalspreadofNISin California.
Only7specieshavebeenthesubjectofimpactstudiesinCalifornia.Mostofthese(86%,n=26) demonstratedasignificantimpact.Thelownumberofstudieshighlightsourlimitedknowledgeof marineNISimpactsgenerally(Ruizetal.1999;Ruizetal.2011a)andspecificallythoseimpactson
40 Californiaecosystems.Thisshouldbearesearchprioritywithinthestate,tobetterestablishthetrue extentofecologicalandeconomicimpactsofmarineNIS.Moreover,knowledgeaboutimpacts associatedwithcurrentandfutureinvadersmayalsobeusefulinsettingprioritiesformanagement response(eradicationorcontrol)forparticularhighͲimpactspeciesofconcern.
6.2.CurrentPatternsandProcessesofVectorOperations
BoatingcontinuestobeoneofthemostpopularformsofrecreationinCalifornia,withalmostamillion vesselsregisteredannually,operatinginbothmarineandfreshwater.Itremainsdifficulttoestimatethe proportionofthesevesselsincoastalmarineandestuarinewatersofthestate.Ofthoseoperatingin marinewaters,availabledatasuggestthat20%ofboatersmaketripsoutsideoftheirhomebay,with highlevelsofconnectivitybetweenlargeinternationalandsmallregionalharbors.Considerable numbersofboatersfromOregonandWashingtonalsovisitthestate.Inaddition,approximately1000 foreignvesselsayeararrivedtoCaliforniaduring2009Ͳ2011.Thus,thepotentialforthecontinued spreadofNISinthestateisconsiderable.
AmongCaliforniaboaters,theChannelIslands,whicharelocatedwithintheChannelIslandsNational MarineSanctuary,wereparticularlypopular.TherearetworecreationalboatmarinasonSantaCruz Island,andmanymorebayswhereboatsstayatanchorovernight.Wedonotknowofanysurveysfor marineNISormarinefoulingcommunitiesingeneralfromtheChannelIslands;howevernonͲnative algalspeciesarepresentoutsideofthemarinasettingsthere(KAMiller,personalcommunication). Giventhehighvalueplacesonthesenaturalecosystems,marinesurveysoffoulingcommunities, boatingstructures,andnearbynaturalcommunitiesintheChannelIslandsintheselocationsarehighly recommended.
ThehighnumberofvesselstravelingtoMexicofrombothSanFranciscoandSanDiegoisalso particularlyinteresting.OnlylimitedinformationexistsformarineNISfromthePacificcoastofMexico (e.g.,Okolodkovetal.2007;CONABIO2010),andthisisaseriousgapinknowledgeforbothCalifornia andthewholeWestCoastacrossallvectors(includingcommercialshipping).Otherbaysthatwere identifiedaspopulardestinationsamongrecreationalboatersincludeHalfMoonBay,NewportBay,San Pedro,MontereyBayandbaysimmediatelynorthofSanFrancisco.
Mostrecreationalboatscarriedsomebiofouling.ThirtypercentofthespeciesweidentifiedwerenonͲ native.ThebryozoanHippoporinaindica,polychaetesBaranchiommasp.2HarrisandSyllissp.37Harris areallnewrecordsforCaliforniaandsuggestthatthesespeciesarecapableofbeingtransportedby recreationalboatsandmaybecomeestablishedhere(identificationfromaboathulldoesnotconfirm establishment).BotrylloidesperspicuumandPileolariatiaratahaveonlybeenreportedfromSouthern California,andrecreationalboatingmayberesponsiblefortheirfuturespreadwithinthestate.
Itsclearthathullhusbandrypracticesvarygreatlyamongvesselsandthattheseaffecttheassociated biofoulingassemblages.Ageofantifoulingpaint,butnotmostrecenthullcleaning,wascorrelatedwith theextentoffoulingcommunitiesonashipshull.Thisislikelybecausenotallhullcleaningmethods
41 areequallyeffective,whileahaulͲoutandnewpaintapplicationisalmostguaranteedtoresetthe foulingcommunitybacktozero.Unfortunately,27%ofboatersreportedhavingpaintedtheirhulls12Ͳ 24monthspreviouslyand35%hadhullpaintolderthan2years(suggestinghundredstothousandsof foulingorganismsmaybepresent).Probablytheleasteffectivecleaningtreatmentistheuseofa scrubbingbrushfromabovewater,whenonlythesurfacelineofalgalfoulingmayberemoved,and noneofthecommonlyfoulednicheareaswillbeaffected.Themosteffectivecleaningtreatments includemooringinfreshwaterforalongperiod(>4weeks)tokillallmarinefoulingorganisms,and cleaningbyprofessionaldivers.
6.3.ManagementReviewandRecommendations
TherearecurrentlynocomprehensivemanagementstrategiesinplaceinCalifornia.Itisclearlyinthe vesselownersinterest(particularlythosewhotravelfarand/orfrequently)tomaintainacleanhull, increasingvesselperformance(includingspeed,fuelͲefficiency,andmechanicaloperation).Areviewof currentapproachestoreducehullfoulingisprovidedinTable7.However,themotivationfor maintenancewillvaryamongowners.Inoursurveys,wefoundhullfoulingorganismson86%of transientvesselssurveyed,includingdenseaggregationsonmorethan25%ofvessels.
Managementoptionscouldbeconsideredtoreducetransfersoforganismsonvesselhulls,independent (orinaddition)tothoseaimedatvesselperformance.Whenconsideringmanagementoptions,itis importanttoevaluatecosts,benefits,andefficacyofpotentialstrategies,recognizingthatthevectorin thiscaseisarecreationalactivity;inparticular,caremustbetakeninordernottoimpedethe enjoymentofboating(whichalsogeneratesasignificantcontributiontothestateseconomy($17billion in2007;DFG2008),andpublicsupportforthemaintenanceandenhancementofcoastalenvironments. Managementstrategiesshouldalsotaketheopportunitytoaddressthewholearrayofvectors associatedwithrecreationalboating,includingthosevesselsoperatinginfreshwaterandthealternative transportmechanismsdescribedintheintroduction(e.g.fishinggears,waterintakes,anchors).
42 Table7.Availablestrategiesforreducingrecreationalvesselhullfouling.Thetableshowsthe methods,benefitsandissuesrelatedtoapplicationsoftoolstodisruptabiofoulingvectortransferby recreationalvessels.
Action Method Benefits Issues
Prevent Keeptheboaton Ͳ Separatingthe Ͳ Expense species ahoistorstored vesselfromthe Ͳ Inconvenience colonization onland wateristhemost Ͳ Notavailableforallboattypes effective preventative measure Useaskirtor Ͳ Relativelysimple Ͳ Expense containeraround tool Ͳ Inconvenience vesselatberth Ͳ Allowsforvesselsto Ͳ Thistreatmentismoreeffectiveif remaininwater freshwaterorchlorineisused (e.g.boatbath) (moreconvenient insidethebath,butthishasother thanabove) environmentalimplicationsandis Ͳ Skirtalsoremainsin prohibitedinmostlocations waterforconvenient Ͳ Ifnotmaintained,theskirts replacementafter becomefouledontheoutside, voyages addingtothemaintenanceburden Maintaina Ͳ Antifoulingpaintis Ͳ Expense pristine themostcommonly Ͳ Maintenanceburden(reͲ antifouling availableprevention applicationsmaybenecessary) optionmakingit Ͳ Interimmeasuresareusually coatingwithtoxic readilyavailable required(inͲwatercleaning) agents(including Ͳ Convenience Ͳ Requiresregularvesselusage nicheareas) becausestationaryperiodscan compromiseefficacy Ͳ Toxicityissues(e.g.copper) conflictwithotherenvironmental management Prevent UseanonͲtoxic Ͳ Preventspollution Ͳ Expense species foulͲrelease Ͳ Doesnotconflict Ͳ Maintenanceburden(reͲ transferafter coating withother applications) environmental Ͳ Interimmeasuresrequired(soft colonization regulations scrubs) hasoccurred Ͳ Convenience Ͳ Partialefficacymaycontributeto NISspread(ifdislodgement doesntoccursoonafter departure) CleanhullinͲ Ͳ Straightforward Ͳ Applicationrigorvarieswidely waterbyowner Ͳ Inexpensive Ͳ Nicheareasoftenignored Ͳ Awareness/trainingusually neededtoimproveefficacy Ͳ Usuallylesseffectivethan professionalservice
43 Ͳ Releasesspecies/propagulesinto theenvironment Ͳ Mustbedoneregularly(cleanͲ beforeͲyouͲgo)toensure propagulereleasedoesnot includetransferredbiota CleanhullinͲ Ͳ Convenience Ͳ Expense waterby Ͳ Usuallymore Ͳ Applicationrigorgenerallybetter professional effectivethan thanamateurcleaningbutstill amateurcleaning varies service Ͳ Nicheareasnotalwaystargeted Ͳ Releasesspecies/propagulesinto theenvironment Ͳ Mustbedoneregularly(cleanͲ beforeͲyouͲgo)toensure propagulereleasedoesnot includetransferredbiota CleanhulloutͲofͲ Ͳ Canbeeffectiveif Ͳ Expensive water(byowner conductedproperly Ͳ Shorelinecleaning(bytraileror orprofessionally) Ͳ Allowsforother hoist)mustalsoincludea maintenanceissues containmentstrategy tobeattendedto Ͳ Drydocksmusttreatallsolidand (e.g.painttouchͲ liquideffluent(treatmentorlandͲ ups) fill)
6.3.1.Globalmanagementreview
Whilemultiplestudiesgloballyhaverecommendedmanagementofrecreationalboatsasavectorfor marineNIS(e.g.Davidsonetal.2010;ClarkeMurrayetal.2011;Zabinetal.2011),weknowofno regulationswhichhavebeenimplementedorenforcedatthenationallevelintheUStopreventthe spreadofmarineNISwithrecreationalvessels(althoughregulationsdoexistfortargetfreshwater speciesincludingthezebramussel,Dreissenapolymorpha).Twocountrieswhichhavemadeafocused efforttoaddresstherecreationalboatingvectorareAustraliaandNewZealand,whichbothhave identifiedasinglegovernmentalbodyresponsibleforthemanagementofthisvector.Byrequiring advancednotificationbyvesselsarrivingfromoverseas,bothcountrieshaveprovidedscopefor interventionofrecreationalboatsarrivingtothecountryshouldtheyposeabiosecuritythreat.
TheAustralianQuarantineandInspectionService(AQIS)requiresforeignvesselsarrivingtoamarinato registertheiranticipatedarrival12Ͳ96hrspriortotheirestimatedarrival(www.daff.gov.au/aqis, accessedApril2012).Onarrival,avesselmaybeinspectedforassessmentofbiofoulingrisks.Since 2005,AQIShasalsobeenconductingavoluntarybiofoulingmanagementregimeforoverseasvessels. Therecommendationsinclude(DAFF2011): applicationofaneffectiveantiͲfoulingcoatingsuitedtotheoperationofthevessel inspecting,andifnecessary,cleaningyourvesselincludingnicheareas(includingbutnot
44 limitedtointernalseawatersystems,seachests,rudderstockandpropellershafts),anchors, chainsandotherancillarygearimmediatelypriortoarrivalinAustralia onceinspectedandcleanedatanoverseasport,departingimmediatelyandtravellingdirectly toAustraliatominimisereͲcontamination maintainingavoyageandbiofoulingmaintenancelogandotherdocumentationthatsupports anybiofoulingmitigationactivitiesundertaken. TheAustralianGovernmentanticipatedmovingtowardsmandatoryriskͲbasedbiofoulingmanagement requirementsforalloverseasvessels.Thesehavenotbeenimplementedtodate,butwouldbe consistentwiththeaboverecommendations.InͲwaterinspectionsofvesselsnotmeetingthese recommendationswouldbeacomponentoftheregulations.
InNewZealand,theMinistryofAgricultureandForestry,BiosecurityNewZealanddivision(MAFBNZ)is responsibleforpreventingtheimportationofunwantedpestsanddiseasesandforcontrolling, managingoreradicatingthemshouldtheyarrive(MAFBNZ2010).Arrivalsfromoverseascanonlyarrive todesignatedports(unlessanalternativearrivalportisapproved)andadvancenoticeofthearrivalis required48hrsinadvance.ThefollowingarerecommendedbyMAFBNZ: Cleanhull:BeforedepartingyourlastportboundforNewZealandcleanyourhull,keeland hullfittingsoffouling.Washoutplaceswheremarineorganismsareabletolivesuchaswater inletsandoutlets,anchorwellsandcockpitareas(anyplaceswhereseawaterisretained). Ensureyourantifoulingpaintisingoodconditionandeffective. Cleanonarrival:ifyouhavenotcleanedbeforedeparture:Ifyouhavebeenunabletoaccess cleaningfacilitiespriortoyourdepartureforNewZealand,haveyourvesselcleanedwithinfour daysofarrival,particularlyifyouplantostayformorethantwoweeks.YourBiosecurity Inspectorwillbeabletodirectyoutolocalhauloutfacilities(whichcontainandtreatdischarges) atyourplaceofarrival. Donotbeach:Donotcleanyourhullbybeachingyourvesselorbycleaningitinthewater unlessthefoulingpresentisnomorethanaslimelayer. Disposal:Putfoulingorremovedsedimentmaterialintoacontaineranddisposeofitonland (ieinmarinaorportrubbishbins).Donotdischargesuchmaterialintotheseaorcoast. Onceagain,inspectionofavesselthoughttoposeaseverebiosecurityriskmaybeenforced.
Weknowofonlyonestudythatassessedthemanagementofbothforeignandlocalvesselsforalocal region,astudyofrecreationalboatsinNelsonHarbor,NewZealand(Piola&Forrest2009).Thereport recommendedacombinationofapproaches: 1.Afoulingregimethatincludesantifoulingapplicationevery12months,withtheuseofa stickertodisplaycompliance 2.RegularsurfaceandinͲwatervesselinspections 3.Ensureresourcesnecessaryforcleaningvessels(inͲoroutͲofͲwater)areavailabletoboat owners
45 4.Considerimplementingafeeforfailuretocomplywiththepoint1above(orgeneralfailureto maintainagoodhullcondition)tofundpoints2&3.Alternatively,marinafeescouldbe increasedtofundpoints2&3. InNelson,theCityCouncilandNelsonMarinaManagerwouldberesponsibleforoverseeing(or enforcing)theabovemeasures.Itwasalsohopedthatsimilarapproacheswouldbeimplementedatthe regionalandnationalscale.
6.3.2.CaliforniaManagementReview
ThereisnocoordinatedmanagementofrecreationalvesselhullfoulinginCalifornia.Noagencyhas sufficientjurisdiction,authority,andfundingtoadequatelymanagethemovementofmarineNISin associationwithrecreationalvessels.Unlikecommercialships,recreationalboatsarenotsubjectto regulationsgoverningactivitiesthatmighttransfernonͲnativespecies(otherthanafewfreshwater speciesasmentionedabove).Previousactionshavebeenlargelysporadicandmotivatedbymultiple agencies/groupswithinthestate,includingeffortstoStopAquaticHitchikersbytheANSTaskForce (protectyourwaters.net/)andvariousawarenesscampaignprojectssupportedbyagenciesincluding CaliforniaDepartmentofBoatingandWaterways,U.S.Fish&WildlifeserviceandCaliforniaSeaGrantto increaseawarenessoftheissue(e.g.,UCSGEPͲSD2006)andseveralresponsestothediscoveryofthe nonͲnativekelp,Undariapinnatifida,identifiedinCalifornianmarinas(LonhartandBunzel2009;Zabin etal.2009);.
IntheCaliforniaAquaticInvasiveSpeciesManagementPlan(2008),theDepartmentofBoatingand Waterways(DBW)waschargedwithmanagingtherecreationalboatingvectorofAISinCalifornia, although,itwasnotedthatthereisnotfundingandstaffforacomprehensiveprogram.Tothisend, DBWleadstheCaliforniaCleanBoatingNetworkacollaborationofgovernment,business,boatingand academicorganizationsworkingtoincreaseandimprovecleanboatingeducationefforts,including invasivespecieseducation,acrossthestate.Responsibilityforboatmaintenancethereforefallson individualboatowners,whomaycurrentlynotknoworcareabouttheissueofnonͲnativespeciesand measurestheycouldtaketopreventspeciestransfers.
6.3.3.ManagementoptionsforCalifornia
InCalifornia,lessthan1%oftransientvesselarrivalsbyrecreationalvesselsarefromoverseas(i.e., otherthancoastwisetraffic).MosttransientboatarrivalsfromoutsidetheStatearrivefromother regionsoftheWestCoast(78%includingBritishColumbiaandMexico).However,thevastmajorityof vesseltrafficisintrastate,and70%ofthetransitsarebyCaliforniavessels.Whileitisperhapseasyto imaginetheUSCBPrequiringforeignvesselstoregisterinadvanceoftheirarrivaltoallowassessment oftheriskofmarineNISintroductions,especiallyasareportingsystemexists,itismorechallengingto implementsimilarmanagementactionsforalldomesticandCaliforniaboaters.Yet,managementof foreignvesselswouldreachaverysmallfractionoftransientvessels,andmanagementactionsfor
46 domesticandlocalvesselsarelikelytohavethegreatestpotentialtoimpedethespreadofmarineNIS withinthestatebyrecreationalvessels.
ThereiscurrentlylimitedͲtoͲnocoordinationorauthorityamongCaliforniastateagenciestopractically managethisvector.Withadequatededicatedfundingandauthority,DBWwouldbetheobviousagency toleadandcoordinatemanagementefforts.ThroughtheCaliforniaCleanBoatingNetwork,channelsof communicationbetweenmanagementagencies,marinaoperatorsandboatersshouldalreadybein place.
SeveraloptionsformanagingtherecreationalvesselvectoratthestatelevelarepresentedinTable8; theoptionsarelistedinorderofresourcesnecessaryforimplementation.Itwouldbeparticularlyuseful toassesstheefficacyofpreviouslyimplementededucationefforts,outreachcampaignsandincentive programs.Thiswouldallowanassessmentofwhetherfutureeffortsshouldsupportsimilaractions,orif moreassertivemadatoryactions,includingatleastthethreatofpenalties,areneeded.Coordinationof suchactionsamongwestcoaststateswouldbeadvantageous.
Oneoptionforfundingmanagementstrategiesisformarinastocollectasmallfeefromresidentand visitingboaterstocontributetowardsNISpreventionstrategies.Thefeecouldalsobeaddedtothecost ofvesselregistrationwiththeDMV,althoughitshouldbenotedthatboatownersmaypreferto documenttheirvesselwithUSCGthanpaytheincreasedfeetoregisterwiththestate,andthismethod doesnotaddanyresponsibilitytovesselsfromoutͲofͲstate.
AhighpriorityforthestateshouldbetotargethighͲriskvessels(i.e.,thosewithhighlevelsofbiofouling andthosethatmaybelikelytocarryparticularhighͲimpactspeciesofconcern),focusingonkeycontrol points;thiscouldutilizetheHazardAnalysisandCriticalControlPoint(HACCP)approach,whichis becomingthestandardforaquaticinvasivespeciesmanagement(Gonzalez&Johnson2007).Key controlpointswouldbethosemarinasreceivinghighnumbersofforeignandtransientvessels.
47 Table8.Strategiesforstatewidemanagementofrecreationalvesselbiofouling.Thetabledescribesa rangeofmeasuresthatcouldbeadopted,fromtheleasttothemostresourceintensive(topto bottom)whichalsogivesanindicationofthelikelytimehorizonofthestrategy(immediateactionsat thetop).
Item Actions Outcomes
Retainthestatusquo Ͳ DonothingͲ Potentialconflictwith stakeholdersconcernedat thelackofactiononvector management Ͳ Noconflictwithrecreational boatersormarinaowners Ͳ Unintendedconsequences avoided(e.g.additional copperpollution) Ͳ Recreationalvesselinfluence onspreadofNISremains unchanged Ͳ Thedonothingoptionis notstaticandthepercapita effectofNIS×Areaaffected willexpanddramatically overtime Conductoutreachto Ͳ AttempttoincreaseawarenessofAIS Ͳ Canbescaledtosuitbudget recreationalboaters andvectorissuesamongrecreational andresourceavailability (withoutevaluationof boatersandprofessionalsworking Ͳ Mayprovideveryfavorable withboatowners(e.g.,marinastaff costͲbenefitoutcome effectiveness) andprofessionaldivers) Ͳ Theeffectsofoutreachwill belargelyunknowable Ͳ Recreationalvesselinfluence onAISspreadmaydecline Conductoutreachto Ͳ AttempttoincreaseawarenessofAIS Ͳ Canbescaledtosuitbudget recreationalboaters andvectorissuesANDdetermine andresourceavailability withscientific efficacy/behaviorchanges Ͳ Mayprovideveryfavorable costͲbenefitoutcome evaluationof Ͳ Theeffectsofoutreachwill effectiveness beassessedwithbeforeand afterpollingtodetermine efficacy Ͳ Efficacymeasurescanbe usedinadaptivestrategy andtoinformfuturepolicy directions Ͳ Higherchance(thanabove) forbeneficialeffectonAIS transfers
48 Proposevoluntary Ͳ Createandpromotebest Ͳ Maybeinexpensive guidelinesona managementpracticestoboaters Ͳ Linkingvoluntaryguidelines statewidebasis andcommercialdiversfrommarina tootherpermitting locations interactionsmayenhance vectormanagement Ͳ Addguidelinesregardingvector Ͳ Additionalmonitoring managementtomaterialsissuedby requiredtodetermine thestateDMV efficacy Ͳ Recreationalvesselinfluence Ͳ Guidelinesprovidedtoforeign onNISspreadmaydecline vesselsbyCBP Proposemandatory Ͳ Createregulationandenforcement Ͳ Amodelofstatevector rulesgoverningvector mechanismforvectormanagement managementalreadyexists management ofrecreationalvessels inthestatethatcanbe mimicked(SLCrulesfor Ͳ Couldbeimplementedatthemarina commercialvessels) levelusingresidentandvisiting Ͳ Marinas,theDMVorDBW boatercontracts wouldneedtoadopt responsibilityforgovernance Ͳ Alternatively,implementatthestate oftherecreationalvessel levelusingDMVregistration vector mechanism Ͳ Highestlikelihoodof effectivevector Ͳ Stateagentwithlegalauthority management necessarytoensureenforcement Ͳ Highandcontinuous expense Ͳ CBPresponsibleformonitoring Ͳ Highpossibilityofconflict arrivalsofforeignvessels withboatersandmarina owners Ͳ Possibilityofunintended consequences(e.g.copper pollutionorinappropriate useoffoulͲreleasecoatings)
AssuggestedinTable8,managementactionscouldbeimplementedatvariouslevelsfromindividual marinastostatewideregulation.Werecommendfurtherexplorationofthevariousapproachesand suggestthatthefollowingoptionsshouldbeamongtheideasexplored. x Inspectionofaboatsunderwatersurfacesforfoulingspeciescouldbearequirementofthe purchaseofaboat(otherthananewboatthathasnotbeenstoredinwater).Theinspection wouldneedtobecarriedoutbyaqualifiedindividualawareofbestmanagementpracticesfor NIS.TheinspectionmighttriggeraninͲwatercleaningorhauloutdependingonpercentcoverof foulingand/orthepresenceofkeyspecies. x MarinascouldincludeaclauseintheirresidentͲboatercontractthatrequiresregularcleaningof thevesselbyaprofessionaldiver.
49 x FollowingthemodelinplaceinNewZealand,Customsinspectorscouldrequirepaperwork documentinghullcleaningofvesselsarrivingfromforeignports,includingthosehomeportedin anothercountry,andUSvesselsthathavebeendockedinforeignportsformorethanafew days.Agentscouldbetrainedtocarryoutvisualinspectionsofvesselsdeemedtobehighrisk (determinationbasedariskassessmentmodel,whichwouldneedtobedeveloped).The inspectionmighttriggeraninͲwatercleaningorhauloutdependingonpercentcoveroffouling and/orthepresenceofkeyspecies. x Similarly,marinastaffcouldrequirehullͲcleaningdocumentationand/ordoavisualinspection ofvisitingboatsintendingtostayatguestberths.TheinspectionmighttriggeraninͲwater cleaningorhauloutdependingonpercentcoveroffoulingand/orthepresenceofkeyspecies; orboatscouldbeturnedawayifhighlyfouled. x Thedevelopmentoflegalauthorityforastatesagent(i.e.CDFGorDBW)undercertain circumstancestoquarantineorotherwiserestrictthemovementofaboatknowntobecarrying highͲriskspecies.Whilethereareregulationsgoverningtheintentionalimportandreleaseof nonͲnativespeciesforaquacultureandresearchpurposes,therearenorulesthatrestrictthe movementofvesselsfouledwithnonͲnativespecies.Thecurrentlackofanysuchauthority hampersattemptstoeradicateandcontrolinvasions. Regardlessofthemanagementstrategyadopted(orthecurrentscenarioofnocoordinated management),detectionandmonitoringofmarinasandharborsshouldalsobeimplemented.Thiscan indicatewhethertheprogramisworking(toreduceinvasions),providingamechanismforadapative management(Ruiz&Carlton2003).Inaddition,detectionwouldalsoallowforresponse(s)tonew incursions,especiallyfocusedontargetspeciesofconcern.Afterprevention,earlydetectionisan essentialpartofacomprehensivestrategyforNISmanagement.Smallpopulationsoforganismsthat arenotwidelydispersedand/orhavenotundergonereproductionaremoreeasilyeradicatedthan thosethathavebecomeestablishedandwidespread(Myersetal.2000;Lodgeetal.2006).Research indicatesthatharborswithhighlevelsofboateractivity(connectivitytoothermarinas)areatthe highestriskforbothreceivingandexportingNIS(Floerletal.2009).Theseareasoughttobeprioritized forfrequentmonitoring.ConsideringtheevidenceoftheinfluenceofSanFranciscoBayastheentry pointfornonͲnativespeciestothestate,manyofwhichsubsequentlyspreadtootherlocationsbothin thestateandalongtheWestCoast(Ruizetal.2011b),marinasintheBayoughttobeamongthe prioritylocationsformonitoringefforts.Morespecifically,marinasinthecentralportionofthebay oughttoreceivetoppriority,astheyhavemoreoceanicconditionsandwouldpresumablysupport speciesthatarelikelytosurvivecoastaltravel.Athoroughexaminationofthetravelpatternsof recreationalboatscouldhelpdetermineotherprioritybaysandmarinas.Basedonourdata,for example,werecommendfocusingontheChannelIslandsasanimportantlocationformonitoring efforts.
50
6.4.Criticaldatagaps
Currently,ourabilitytofullyunderstandandquantitativelyevaluatethestrengthofthisvectoris hinderedby,amongotherthings:1)thelackofanycoordinateddatagatheringofrecreationalboat traffic,especiallymovementsamongembaymentsinCalifornia,2)alackofcentralizationofdatathat aregathered,and3)improvedinformationonbioticcontentofvesselsassociatedwithspecificregions andmanagementpractices.Informationontravelpatternsofvesselsisimportanttoevaluatingthe strengthofthevector,predictingwherenewinvadersmightturnup,andfocusingeducation/prevention activities.Furtherstudiesoffactorsinfluencingthefoulingbiotaassociatedwithrecreationalvessels bothlocallyandgloballyarealsonecessary,asnotallvesselsandlocationsposeequalrisks,andsuch informationwouldallowforamorefocused,agile,andeffectivestrategyinabatingrisks.
Werecommendanexplorationofthefeasibilityofstandardizingthedatacollectedbymarinastafffrom visitingboats.Suchdatashouldataminimumincludehomeport,lastportofcall,nextportofcall, lengthofstayatamarina.Additionalkey(andstreamlined)informationonhusbandrypracticeswould beinvaluable.Ideally,astandardizedformatwouldbeused.Datacouldbereportedtoacentral locationforuseinanalysis;boatersconfidentialinformationcouldberemovedbeforedoingso.By makingthesystemautomatedandcentralized,itshouldcauseminimalinconveniencebeyondthe registrationprocessatmostmarinas.Towardsthisend,asofJanuary2012,theCBPhasimplementeda webͲbasedSmallVesselReportingSystem.Thiswillallownationalparticipantstoexpeditiouslyreport theirarrivalsfromforeignports.Theimpactofthissystemisnotyetknown,butifboaterscomply,the systemshouldimproveourfutureunderstandingofvesselmovementsfromforeignportsinto California.
6.5.KeyManagementRecommendationsforCalifornia
Insummary,ourrecommendationsforthestateareasfollows: 1)Providetheauthorityandfundingforaleadagencytoimplementamanagementstrategy, whichisurgentlyneededtopreventtheintroductionandspreadofNISbyrecreationalvessels. 2)Createacentralizedresourcetocollectdataconcerningrecreationalvesselhabitsandmeet thedatagapsidentifiedabove. 3)Assesstheefficacyofpreviouslyimplementededucationefforts,outreachcampaignsand incentiveprogramsandtheneedformandatoryregulationandenforcement. 4)Evaluateavailableoptions,includingthecostsandbenefitsofthesewithinthecontextof Californiasjurisdictionsandinterests. 5)SustainandadvanceeffortstodetectNISandevaluateimpacts,tobetterguidemanagement resourcedecisions. 6)ImplementacoordinatedmanagementapproachonastateͲwide,aswellasregional,basis. 7)Assesstheefficacyofadoptedmanagementstrategies,onacontinuedbasis,usingadaptive managementtoadapttheprogramaccordingly.
51
7.Acknowledgements
WewouldliketothankChrisBrown,DaleCalder,JeffCordell,LeslieHarris,LindaMcCannandKathyAnn Millerforspecimenidentifications.ChrisBrownalsoprovidedfieldassistanceanddiscussionofthe project.Contemporarydatawereallcollectedwiththeassistanceofharbormastersandstaffatthe studymarinas:PillarPoint,Pier39,SantaBarbaraHarbor,MontereyHarbor,SanDiegoPoliceDock, HumboldtBayHarbor,SanFranciscoMarina,SouthBeachMarina.ParticularthanksgotoJudyNeidert andTimatSanDiegoPolicedock,andKathySangsterandMickKronmanatSantaBarbaraMarina.Kim Holzer,RachelFontanaandEliotCraftonprovidedtheimpactsdata(summarizedinAppendices7and8). PFofonoffandBStevesfortheirdevelopmentofNEMESISandCaliforniaDepartmentofFishandGame fordatausedtoimproveandcreatetheCaliforniaspecificdatabaseusedinthisreport.
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55 PearseV,JPearse,MBuchsbaumandRBuchsbaum.1987.LivingInvertebrates.Blackwell/Boxwood, PacificGrove,CA:848pp. PiolaRandEJohnston.2006.Differentialresistancetoextendedcopperexposureinfourintroduced bryozoans.MarineEcologyProgressSeries311:103Ͳ114. PiolaRandBForrest.2009.OptionsforManagingBiosecurityRisksfromRecreationalVesselHubs. PreparedforNelsonCityCouncil.CawthronReportNo.1591.45pp. Ruiz,GM,FofonoffPF,HinesAHandEDGrosholz.1999.Nonindigenousspeciesasstressorsinestuarine andmarinecommunities:Assessinginvasionimpactsandinteractions.Limnologyand Oceanography,44:950Ͳ972 RuizGMandJTCarlton.2003.InvasionVectors:AConceptualFrameworkforManagement.In:RuizGM andJTCarlton(eds)Invasivespecies:vectorsandmanagement.IslandPress,Washington,DC,p 459Ͳ504. RuizGM,PWFofonoff,JTCarlton,MJWonhamandAHHines.2000.Invasionofcoastalmarine communitiesinNorthAmerica:apparentpatterns,processesandbiases.AnnualReviewof EcologyandSystematics31:481531. RuizG,AFreestone,PFofonoffandCSimkanin.2009.Habitatdistributionandheterogeneityinmarine invasiondynamics:theimportanceofhardsubstrateandartificialstructure.In:WahlM(ed) Marinehardbottomcommunitiespp.321332. RuizGM,PWFofonoff,BPStevesandADahlstrom.2011a.MarineCrustaceanInvasionsinNorth America:ASynthesisofHistoricalRecordsandDocumentedImpacts.In:GalilBS,PEClarkandJT Carlton(eds)IntheWrongPlaceͲAlienMarineCrustaceans:Distribution,Biologyand Impacts.pp215Ͳ250. RuizGM,PWFofonoff,BPSteves,SFFossandSNShiba.2011b.Marineinvasionhistoryandvector analysisofCalifornia:AhotspotforwesternNorthAmerica.DiversityandDistributions.17:362 373. TakataL,MFaulknerandSGilmore.2006.CommercialvesselfoulinginCalifornia:Analysis,evaluation, andrecommendationstoreducenonindigenousspeciesreleasefromthenonͲballastwater vector.ProducedfortheCaliforniaStateLegislaturebytheCaliforniaStateLandsCommission MarineFacilitiesDivision.76pp. UCSGEPͲSD.2006.UniversityofCaliforniaSeaGrantExtensionProgramͲSanDiegoFactSheet06Ͳ1 March2006:ManagingHullͲBorneInvasiveSpeciesonCaliforniasCoastalBoats. http://www.rimeis.org/stakeholders/docs/transportation/hullborneAIS.pdf) WallentinusI.1999.Sargassummuticum.In:Gollasch,S.,Minchin,D.,Rosenthal,H.&Voigt,M.(eds.): Exoticsacrosstheocean.Casehistoriesonintroducedspecies:theirgeneralbiology, distribution,rangeexpansionandimpact.LogosVerlag,Berlin. WassonK,CJZabin,LBedinger,CMDiazandJSPearse.2001.Biologicalinvasionsofestuarieswithout internationalshipping:theimportanceofintraregionaltransport.BiologicalConservation 102(2):143Ͳ153 WilliamsSLandJESmith.2007.Aglobalreviewofthedistribution,taxonomyandimpactsofintroduced seaweeds.AnnualReviewofEcology,EvolutionandSystematics38:327Ͳ359.
56 WittenburgRandWCock.2005. Bestpracticesforthepreventionandmanagementofinvasivealien species.In:MooneyHA,RNMack,JAMcNeely,LENeville,PJScheiandJKWaage(eds).Invasive alienspecies.IslandPress,Washington,D.C.p209Ͳ232.
ZabinCJ,GAshton,CWBrownandGMRuiz.2009.NorthernrangeexpansionoftheAsiankelpUndaria pinnatifida(Harvey)Suringar(Laminariales,Phaeophyceae)inwesternNorthAmerica.Aquatic InvasionsVolume4:429Ͳ434.
ZabinCJ,GAshton,CWBrown,IDavidson,TChestnut,RDraheim,MDSytsmaandGMRuiz.2011.Hull Fouling:CharacterizingMagnitudeandRiskofSpeciesTransfersbyRecreationalandFishing Vessels.FinalreporttothePacificStatesMarineFisheriesCommission.105pp.
57 RecreationalVesselsasVectorsofNonͲNativeMarineSpecies inCalifornia
Appendices
July2012
Submittedto
OceanScienceTrust
Submittedby
GAshton,CZabin,IDavidson,GRuiz
& Appendix1
CharacteristicsusedbyPFofonofftodefineFoulingspeciesinNEMESIS
OrganismCharacteristicsͲSessileorsedentaryorganismsfirmlyattachedtoasurface(algae,polyps, mussels,tunicates,etc),animalslivingwithinoronattachedorganisms,orinthematrixofthefouling community(isopods,amphipods,mobilepolychaetes),woodͲborers(gribbles,shipworms).Highly mobileorganismssuchasfishes,shrimps,andmysidsarelesslikely,althoughtransportoffisheggsin foulingispossible.Organismstransportedinfoulingtolerateoceanicconditions,includinghighsalinity andfluctuatingtemperatures.
ManyfoulingorganismshavelongͲlivedplanktoniclifeͲstages(larvae,medusae)andsocouldbe transportedwithroughlyequalprobabilitybyballastwaterorfouling.Historically,foulingwouldhave beenamajorvectorforCaliforniafromtheGoldRush(andmaybeearlier)tothepresent.
Seachestswerenottreatedseparately.Theydoprovideapotentialmodeoftransportforlargerand moreactiveorganismsthatwouldnottoleratehydrodynamicstressorwouldbewashedawayintransit, butmorestudyisneededtodeterminetheirimportance.
1 Appendix2cont.d
Referencesforliteraturesearchbiofoulingtaxareportedfromsmallcraft
1AshtonG,DavidsonIandGRuiz.2010.HistoryandbiofoulingofshipshullsarrivingtoKetchikan, Alaska:acasestudy.FinalreportsubmittedtoAlaskaDepartmentofFishandGame.42pp.
2ClarkeMurrayC,PakhomovEAandTWTherriault.2011.Recreationalboating:alargeunregulated vectortransportingmarineinvasivespecies.DiversityandDistributions:1Ͳ12.
3Darbyson,EA,ALocke,JMHansonandJHMWillison.2009.Marineboatinghabitsandthepotentialfor spreadofinvasivespeciesintheGulfofStLawrence.AquaticInvasions4:87Ͳ94.
4DavidsonIC,CJZabin,ALChang,CWBrown,MDSytsmaandGMRuiz.2010.Recreationalboatsas potentialvectorsofmarineorganismsataninvasionhotspot.AquaticBiology11:179Ͳ191.
5DeBlauweHandFaasseM.2001.ExtensionoftherangeofthebryozoansTricellariainopinataand BugulasimplexintheNorthͲEastAtlanticOcean(Bryozoa: Cheilostomatida).NederlandseFaunisticheMededelingen14:103Ͳ112.
6FarraperiaCMR.2011.TheintroductionofthebryozoanZoobotryonverticillatum(DellaChiaje,1822)in northeastofBrazil:acauseforconcern.BiologicalInvasions(2011)13:13Ͳ16.
7FloerlO.2002.Intracoastalspreadoffoulingorganismsbyrecreationalvessels.PhDthesis,JamesCook University,Townsville.
8FloerlOandGJInglis.2005.Startingtheinvasionpathway:theinteractionbetweensourcepopulations andhumantransportvectors.BiologicalInvasions7:589Ͳ606.
9GodwinLS,EldredgeLGandKGaut.2004.Theassessmentofhullfoulingasamechanismforthe introductionanddispersalofmarinealienspeciesinthemainHawaiianIslands.BishopMuseum TechnicalReportNo.28.August2004.114pp.
10LeonardJ.2009.HullFoulingSurveysofRecreationalBoatsinHawaii.HawaiiDepartmentofLandand NaturalResources,DepartmentofAquaticResourcesReport.32pp.
11LougheedVLandRJStevenson.2004.Exoticmarinemacroalga(Enteromorphaflexuosa)reachesbloom proportionsinacoastallakeofLakeMichigan.JournalofGreatLakesResearch30(4):538Ͳ544.
12KerckhofF.2002.Barnacles(Cirripedia,Balanomorpha)inBelgianwaters,anoverviewofthespecies andrecentevolutions,withemphasisonexoticspecies.BulletindelInstitutRoyalDesSciences NaturellesdeBelgique,Biologies,72ͲSupplement:93Ͳ104.
13MeineszA,BelsherT,ThibautT,AntolicB,MustaphaKB,BoudouresqueCͲF,ChiaveriniD,CinelliF, CottalordaJͲM,DjellouliA,ElAbedA,OrestanoC,GrauAM,IvesaL,JaklinA,LangarH,MassutiͲ PascualE,PeiranoA,TunesiL,deVaugelasJ,ZavodnikNandAZuljevic.2001.Theintroduced
15 greenalgaCaulerpataxifoliacontinuestospreadintheMediterranean.BiologicalInvasions3: 201Ͳ210.
14MineurF,MPJohnsonandCAMaggs.2008.Macroalgalintroductionsbyhullfoulingonrecreational vessels:Seaweedsandsailors.EnvironmentalManagement42:667Ͳ676.
15MinchinDandHolmesJMC.2007.ThefirstrecordofCaprellamuticaSchurin,1935(Crustacea: Amphipoda)fromtheEastCoastofIreland.TheIrishNaturalistsJournal,28(8):321Ͳ323.
6MinchinDandSidesE.2006.Appearanceofacryptogenictunicate,aDidemnumsp.foulingmarina pontoonsandleisurecraftinIreland.AquaticInvasions1(3):143Ͳ147.
17MintzCT.2001.Vesselhullsasadispersalvectorforcoastalmarineorganisms.BachelorsThesis, WilliamsCollege,Williamstown,Ma.41pp
18NevesCS,RochaRM,BettiniͲPitomboFandJJRoper.2007.Useofartificialsubstratabyintroduced andcryptogenicmarinespeciesinParanaguaBay,southernBrazil.Biofouling23(5):319Ͳ330.
19SaviniD,MarchiniA,ForniGandMCastellazzi.2006.Touristicharboursandsecondaryspreadofalien species.Biol.Mar.Medit(1):760Ͳ763.
20Zabin,CJ,ZardusJ,BettiniͲPitomboF,FreadVandMGHadfield.2007.Ataleofthreeseas:consistency ofnaturalhistorytraitsinaCaribbeanͲAtlanticbarnacleintroducedtoHawaii,Biological Invasions:9:523Ͳ544.
21Zabin,CJ,AshtonGV,BrownCW&RuizGM.2009.NorthernrangeexpansionoftheAsiankelpUndaria pinnatifida(Harvey)Suringar(Laminariales,Phaeophyceae)inwesternNorthAmerica.Aquatic Invasions4(3):429Ͳ434.
22ZabinCJ,AshtonG,BrownCW,DavidsonI,ChestnutT,DraheimR,SytsmaMDandGMRuiz.2011.Hull Fouling:CharacterizingMagnitudeandRiskofSpeciesTransfersbyRecreationalandFishing Vessels.FinalreporttothePacificStatesMarineFisheriesCommission.105pp.
16 Appendix3
DatareceivedfromCustomsandBorderProtectioninresponsetoFOIArequests:
AtableofsmallvesselsarrivingbyseafortheperiodofJanuary2009topresent;whichhaveregistered withU.S.CustomsandBorderProtection(CBP),specificallyintheportsofSanDiego,Eureka,Port Hueneme,Monterey,SanFrancisco,aswellasallotherportsofentryinCaliforniathatdealwiththe arrivalsofsmallvessels.
17 Appendix4
PoliceDock (SanDiego) SantaBarbara 180 250 160 2010 2010 140 2011 200 2011 120 150 100 80 100 60 40 50 20 0 0 JFMA MJ J A SOND JFMA MJ J A SOND
MontereyMarina PillarPoint(HalfMoonBay) 140 250 2006 120 2007 2007 200 100 2008 80 150 60 100 40 20 50
0 0 JFMA MJ J A SOND JFMA MJ J A SOND
SouthBeach (SF) Pier39(SF) 180 100 2008 160 90 2010 2009 140 80 2011 120 70 100 60 80 50 40 60 30 40 20 20 10 0 0 JFMA MJ J A SOND JFMA MJ J A SOND
SpudPoint(Bodega Bay) Humboldt 300 400 2008 2010 250 350 300 2011 200 250 150 200 100 150 100 50 50 0 0 JFMA MJ J A SOND JFMA MJ J A SOND
MonthlyrecordsoftransientvesselarrivalstomarinasalongtheCaliforniacoastline.Shadingisusedto distinguishbetweendifferentyears(indicatedbylegends).NotedifferentscalesontheyͲaxes.
18 Appendix5
PoliceDock(SanDiego) SantaBarbara MontereyMarina AK AK AK BC BC BC WA WA WA OR OR OR CA n=2123(77%) CA n=894(81%) CA n=921(72%) Mexico Mexico Mexico HI HI HI Caribbean Caribbean Caribbean Central(USA) Central(USA) Central(USA) Central(Canada) Central(Canada) Central(Canada) Atlantic(USA) Atlantic(USA) Atlantic(USA) Asia Asia Asia Europe Europe Europe Australias Australias Australias Unknown Unknown Unknown
0 100 200 020406080 020406080100
PillarPoint(HalfMoonBay) SouthBeach(SF) Pier39(SF) AK AK AK BC BC BC WA WA WA OR OR OR CA n=666(54%) CA n=721(59%) CA n=791(93%) Mexico Mexico Mexico HI HI HI Caribbean Caribbean Caribbean Central(USA) Central(USA) Central(USA) Central(Canada) Central(Canada) Central(Canada) Atlantic(USA) Atlantic(USA) Atlantic(USA) Asia Asia Asia Europe Europe Europe Australias Australias Australias Unknown n=469(38%) Unknown n=424(35%) Unknown
010203040 010203040 01020304050 SpudPoint(BodegaBay) AK BC WA OR CA n=519(59%) Mexico HI Caribbean Central(USA) Central(Canada) Atlantic(USA) Asia Europe Australias Unknown
020406080100
AppendixFig2ͲLocationofhomeaddresseslistedbytransientvesselsarrivingtokeymarinasontheCalifornian coastline.Dataarecountsofvessels.NotedifferentscalesonthexͲaxes.
19 Appendix6
Listofspeciesidentifiedfromrecreationalvessels.Numbersindicatenumberofvesselsthatthespecieswas sampledfrom.LettersindicatestatusofthespeciesinCalifornia:NͲNative,IͲIntroduced,CͲcryptogenic,GͲ couldnotbeidentifiedtospecies,buttherearenativemembersofthisgroup.*indicatesspeciesnotyet recordedfromCA.
Algae 1 N Gonothyraealoveni 1 N Blidingiaminima 5 N Obeliadichotoma 1 N Chaetomorphaaerea 8 N Obelialongissima 1 I Colpomeniaperegrina 1 N Plumulariasetacea 1 N Dasyasessillis 1 I Lomentariahakodatensis Arthropods 1 N Myriogrammespectabilis 1 G Allorchestessp. 1 N Polyneuralatissima 1 C Ampithoeplumulosa 1 N Polysiphoniapacifica 1 G Aoroidessp.juvenile 1 N Pterosiphoniadendroidea 1 N Cancergracilis 1 N Pterothamnionpectinatum 11 N Caprellacalifornica 1 N Ulvaclathrata 10 C Caprellaequilibra 1 N Ulvaintestinalis 3 N Caprellakennerlyi 3 G Ulvasp. 15 I Caprellamutica 1 I Undariapinnatifida 1 I Caprellasimia 2 G Corophiidaejuveniles Ascidians 2 I Elasmopusrapax 6 N Ascidiaceratodes 9 C Erichthoniusbrasiliensis 1 N Ascidiaparatropa 2 C Erichthoniussp.juveniles 1 G Ascidiasp. 1 G Gammarideajuvenile 2 I Ascidiazara 1 G Grapsidae 6 N Botrylloidesdiegensis 1 G Harpacticoida 2 I Botrylloidesperspicuum 7 I Jassamarmorata 3 G Botrylloidessp. 11 N Jassaslatteryi 14 I Botrylloidesviolaceus 1 G Jassasp.juveniles 19 I Botryllusschlosseri 1 N Jassastaudei 9 I Cionaintestinalis 9 N Laticorophiumbaconi 1 I Cionasavignyi 1 G Leucothoesp.juveniles 1 I Molgulacf.manhattensis 1 I Leucothoespinicarpa 1 I Molgulaficus 8 I Monocorophiumacherusicum 6 I Molgulasp. 1 I Monocorophiuminsidiosum 1 G Riterellasp. 1 I Monocorophiumuenoi 4 I Styelaclava 1 N Pachychelesrudis 10 I Styelaplicata 14 N Paracerceissculpta 8 G Styelasp. 11 N Paranthuraelegans 1 N Podoceruscf.cristatus Hydrozoans 2 N Pugettiagracilis 3 N Aglaopheniadiegensis 1 G Sphaeromatidaejuveniles 1 N Amphisbetiafurcata 1 G Stenothoidae,unidentified 2 I Bougainvilliamuscus 2 G Xanthidae 1 G Bougainvilliidae(blank) 8 N Zeuxonormani 3 N Campanulinidae(blank) 7 G Zeuxosp.juveniles 2 G Clytiasp. 1 G Corynesp. 2 N Ectopleurasp.
20 Bryozoans Polychaetes 2 G Diaperoformasp. 5 N Paleanotusbellis 13 G Bowerbankiasp. 1 G Cirratulidae 32 I Bugulaneritina 1 C Dorvilleamoniloceras 23 I Bugulastolonifera 1 G Nereididae 17 N Celleporariabrunnea 2 I Alittasuccinea 1 N Celleporellahyalina 1 N Nereislatescens 1 G Celleporellasp. 1 N Nereismediator 1 G Celleporinasp. 1 N Nereisvexillosa 1 I Conopeumcf.tenuissimum 6 N Platynereisbicanaliculata 2 G Conopeumsp. 1 N Eualiaquadrioculata 1 N Crisiacf.occidentalis 3 N Halosydnabrevisetosa 2 G Crisiasp. 1 N Halosydnajohnsoni 1 G Crisidaesp. 1 C Harmathoeimbricatacomplex 3 G Crisuliporasp. 1 C Thormorajohnstoni 14 I Cryptosulapallasiana 1 C Bispirasp.7Harris 1 G Electracf.crustulenta 1 I Branchiommasp.1 2 G Electrasp. 3 I Branchiommasp.2Harris 1 I Hippoporinaindica* 1 N Eudistyliapolymorpha 3 N Membraniporavillosa 1 G Eudistyliasp. 1 N Microporellasetiformis 1 C Megalommacoloratum 4 I Schizoporellajaponica 2 N Paradialychoneecaudata 2 G Schizoporellasp. 4 I Parasabellafullo 2 N Scrupocellariabertholetti 2 N Pseudopotamillaocellata 8 N Thalamoporellacalifornica 1 G Serpulidae 2 N Tricellariaoccidentalis 2 I Ficopomatusenigmaticus 1 N Tubuliporacfpacifica 1 I Hydroidescrucigera 3 I Watersiporaarcuata 1 I Hydroidesdiramphus 21 I Watersiporasubtorquata 9 I Hydroideselegans 5 I Zooobotryonsp. 6 N Hydroidesgracilis 2 G Hydroidessp. Cirripeds 9 C Salmacinatribranchiata 5 I Amphibalanusamphitrite 1 I Boccardiellahamata 8 I Amphibalanuseburneus 2 N Polydoranarica 5 I Amphibalanusimprovisus 3 G Spirorbidae 1 G Amphibalanus(blank) 10 N Pileolariamarginata 11 N Balanuscrenatus 1 N Pileolariatiatara 3 N Balanusglandula 3 G Autolytinae 1 G Balanussp. 1 C Syllisgraciliscomplex 9 N Balanustrigonus 2 I Syllissp.37Harris 1 N Conchodermaauritum 2 G Trypanosyllissp. 1 G Conchodermasp. 1 N Eupolymniaheterbranchia 1 N Lepasanatifera 2 N Lepaspacifica 2 G Lepassp. 3 C Megabalanuscftanagrae 3 N Megabalanuscoccopoma 1 G Megabalanussp. 1 G Megabalanussp.A 1 G Megabalanussp.B 2 N Megabalanustintinnabulum
21 Appendix7 ResultsofBIOSISsearchesforimpactstudies.NotethatthenumberofBiosisAbstractsreturnedoftenincludes duplicatesandisunreliable.Onlyarticlesthatcouldbesourcedandassessedforrelevanceareincludedinthe finalcolumn.
BIOSIS Title Taxonomic Abstracts suggests Article Group Class Species returned relevance relevant Algae Chlorophyta Bryopsishypnoides 2 2 0 Codiumfragilesspfragile 137 68 25 Heterokontophyta Cutleriacylindrica 1 0 0 Sargassumhorneri 4 2 0 Sargassummuticum 132 71 30 Undariapinnatifida 116 50 9 Rhodophyta Aglaothamniontenuissimum 0 0 0 Antithamnionhubbsii 3 0 0 Antithamnionpectinatum 6 0 0 Caulacanthusustulatus 8 0 0 Ceramiumkondoi 1 0 0 Chondriaarcuata 0 0 0 Dasyasessilis 4 1 1 Gracilariavermiculophylla 34 14 6 Grateloupialanceolata 6 0 0 Grateloupiaturuturu 32 9 2 Lomentariahakodatensis 5 1 0 Neosiphoniaharveyi 18 4 2 Pikeayoshizakii 0 0 0 Polysiphoniadenudata 1 0 0
22
BIOSIS Title Taxonomic Abstracts suggests Article Group Class Species returned relevance relevant Arthropoda Amphipoda Abludomelitarylovae 0 0 0 Ampeliscaabdita 14 3 0 Ampithoe 9 4 0 Ampithoelongimana 3 0 0 Ampithoevalida 3 0 0 Aoroidessecunda 0 0 0 Calliopiellasp. 0 0 0 Caprelladrepanochir 0 0 0 Caprellamutica 42 11 2 Caprellascaura 7 1 1 Caprellasimia 0 0 0 Cheluraterebrans 1 0 0 Corophiumheteroceratum 2 0 0 Eochelidium 0 0 0 Eochelidiummiraculum 0 0 0 Grandidierellajaponica 8 0 0 Incisocalliopederzhavini 0 0 0 Jassamarmorata 7 1 0 Melitanitida 9 4 0 Microdeutopusgryllotalpa 2 1 0 Monocorophiumacherusicum 8 3 0 Monocorophiuminsidiosum 8 3 0 Monocorophiunuenoi 0 0 0 Paracorophiumlucasi 2 1 0 Paradexamine 0 0 0 Stenothoevalida 0 0 0 Cirripede Amphibalanusalbicostatus 4 2 0 Amphibalanusamphitrite 100 11 1 Amphibalanuseburneus 3 2 0 Amphibalanusimprovisus 51 10 3 Amphibalanusreticulatus 18 2 0 Balanustrigonus 13 1 0 Copepoda Mytilicolaorientalis 10 6 5 Cumacean Nippoleuconhinumensis 1 1 0
23 BIOSIS Title Taxonomic Abstracts suggests Article Group Class Species returned relevance relevant Crustacea Decapoda Carcinusmaenas 394 149 24 cont.d Rhithropanopeusharrisii 74 13 3 Isopoda Caecijaerahorvathi 0 0 0 Dynoidesdentisinus 0 0 0 Eurylanaarcuata 4 1 0 Iaiscalifornica 0 0 0 Ianiropsisserricaudis 0 0 0 Limnoriaquadripunctata 3 0 0 Limnoriatripunctata 10 0 0 Paranthurajaponica 2 1 0 Pseudosphaeromasp. 1 1 0 Sphaeromaquoianum 14 4 2 Sphaeromawalkeri 10 0 0 Sphaeromasp. 45 6 3 Synidotealaevidorsalis 11 8 0 Uromunnasp. 0 0 0 Ostracoda Aspidoconchalimnoriae 0 0 0 Redekeacalifornica 0 0 0 Tanaid Sinelobusstanfordi 4 0 0
24
BIOSIS Title Taxonomic Abstracts suggests Article Group Class Species returned relevance relevant Mollusca Bivalvia Crassostreagigas 415 42 12 Geukensiademissa 26 0 0 Ischadiumrecurvum 5 0 0 Lyroduspedicellatus 6 0 0 Musculistasenhousia 56 13 8 Mytilusgalloprovincialis 278 62 17 Teredobartschi 5 1 0 Teredofurcifera 5 0 0 Teredonavalis 16 7 1 Gastropoda Anteaeolidiellafoulisi 0 0 0 Babakinafestiva 0 0 0 Batillariaattramentaria 14 4 4 Catrionarickettsi 0 0 0 Crepidulaconvexa 5 4 0 Crepidulaplana 1 1 0 Cuthonaperca 1 0 0 Eubranchusmisakiensis 0 0 0 Guildfordiayoka 0 0 0 Okeniaplana 1 0 0 Potamopyrgusantipodarum 136 21 2 Sakuraeolisenosimensis 1 0 0 Tenelliaadspersa 2 0 0
25 Appendix8 SynonymslistedinWoRMS(WorldRegisterofMarineSpecies;www.marinespecies.org)usedassearch termsinBIOSIS.Currentrecognizednomenclatureislistedinbold,synonymsfollow. Mollusca Anadaraovalis:Arcaamericana,Arcacampechiensis,Arcacanalicostata,Arcacayenensis,Arcacostata,Arca declivis,Arcaholmesii,Arcaindica,Arcaovalis,Arcapariaensis,Arcapectinoides,Arcapexata,Arca semidentata,Lunarcaovalis Anadaratransvers:aAnadarademiri,Arcaamygdalum,Arcasulcosa,Arcatransversa,Scapharcademiri Anomiasimplex:Anomiaacontes,Anomiaglabra Anteaeolidiellaindica:Anteaeolidiellafoulisi,Aeolidiellaindica,Aeolidiellatakanosimensis,Aeolisfoulisi, Anteaeolidiellaindica Arcticaislandica:Arcticavulgaris,Cyprinaislandica,Pectunculuscrassus,Venusbuccardium,Venusferröensis, Venusislandica,Venuspitar Crassostreagigas:Crassostreaangulata,Crassostreatalienwhanensis,Dioeciostreahispaniola,Gryphaea angulata,Lophaposjetica,Ostreaangulata,Ostreacomplanata,Ostreacymbaeformis,Ostreagigas, Ostrealaperousii,Ostreaposjetica,Ostrearostralis,Ostreavirginicavar.lusitanica, Crassostreavirginica:Dioeciostreaamericana,Ostreaborealis,Ostreacanadensis,Ostreafloridensis,Ostrea procyon,Ostreareniformis,Ostrearostrata,Ostreatriangularis,Ostreavirginiana,Ostreavirginica Crepidulaconvexa:Crepidulaacuta,Crepidulaglauca Crepidulafornicate:Crepidulariisei,Crepidulavirginica,Cryptadensata,Cryptanauturum,Patellafornicata Crepidulaplana:Crepiduladepressa,Crepidulalamina,Crepidularhyssema Eubranchusmisakiensis:Leostyletusmisakiensis Gemmagemma:Cyrenapurpurea,Gemmafretensis,Gemmatottenii,Parastarteconcentrica,Venusgemma, Venusmanhattensis Geukensiademissa:Brachidontesdemissus,Brachydontesclava,Modiolaplicatula,Modiolasemicostata,Modiolus demissus,Mytilusdemissa Haminoeajaponica:Haminoeacallidegenita Ilyanassaobsolete:Buccinumnoveboracensis,Buccinumoliviforme,Nassaobsoleta, Ischadiumrecurvum:Mytiluscarolinensis,Mytilushamatus,Mytilusrecurvum,Mytilusstriatus Littorinalittorea:Littorinaarmoricana,Littorinabartonensis,Littorinacommunis,Littorinaparva,Littorinarudis, Littorinasphaeroidalis,Littorinavulgaris,Turbobicarinatus,Turbocarinatus,Turboelongatus,Turbo litoreus,Turbolittoreus,Turbosulcatus,Turboustulatus,Turboventricosus Littorinasaxatilis:Litorinagroenlandica,Litorinaincarnata,Litorinamarmorata,Litorinasulcata,Littorina castanea,Littorinadanieli,Littorinaneglecta,Littorinanervillei,Littorinanigrolineata,Littorinapalliata, Littorinarudis,Littorinasaxoides,Littorinasimplex,Littorinatenebrosa,Littorinazonaria,Neritarustica, Turboobligatus,Turborudis,Turborudissimus Lyroduspedicellatus:Teredoarabica,Teredocalmani,Teredochlorotica,Teredodagmarae,Teredodiegensis, Teredofloridana,Teredofranziusi,Teredohawaiensis,Teredohelleniusi,Teredohibicola,Teredo honoluluensis,Teredoindica,Teredokauiensis,Teredolamyi,Teredolinaoana,Teredolomensis,Teredo madrasensis,Teredomalaccana,Teredomidwayensis,Teredonodosa,Teredopedicellata,Teredo
26 pertingens,Teredopochhammeri,Teredorobsoni,Teredosamoaensis,Teredosiamensis,Teredo taiwanensis,Teredotateyamensis,Teredotogoensis,Teredotownsendi,Teredotristis,Teredoyatsui Melanoidestuberculatus:Melanoidestuberculata Mercenariamercenaria:Mercenariacancellata,Mercenariafulgurans,Mercenariarutila,Mercenariaviolacea, Venuscyprinoides,Venusmercenaria,Venusnotata,Venusobliqua,Venuspraeparca,Venus submercenaria,Venusziczac Meretrixlusoria:Cythereaformosa,Cythereagraphica,Meretrixvirgatula,Venuslusoria Musculistasenhousia:Arcuatulasenhousia,Modiolaaquarius,Modiolabellardiana,Modiolasenhousia Myaarenaria:Myaacuta,Myaalba,Myacommunis,Myacorpulenta,Myadeclivis,Myaelongata,Myahemphilli, Myajaponica,Myalata,Myaoonogai,Myasubovata,Myasubtruncata,Spheniaovoidea Myosotellamyosotis:Ovatellamyosotis Mytilusgalloprovincialis:Mytilusdilatatus,Mytilusedulisdiegensis,Mytilusedulisgalloprovincialis,Mytilusedulis zhirmunskii,Mytilusflavus,Mytilushesperianus,Mytiluslamarckianus,Mytilusorbicularis,Mytilus sagittatus,Mytilussuccineus Nuttalliaobscurata:Nuttalliasolida,Psammobiaolivacea,Soletellinaobscurata Ocinebrellusinornatus:Ocenebrainornata,Murexcrassus,Murexendermonis,Murexinornatus,Murexjaponicus, Murextalienwhanensis,Pteropurpurainornata,Ocinebrellusinornata,Tritoniumsubmuricatum,Fusus submuricatum,Trophonincompta Okeniaplana:Okeniaeolida,Doriseolida Ostreaedulis:Monoeciostreaeuropa,Ostreaadriatica,Ostreaboblayei,Ostreacorbuloides,Ostreacristata,Ostrea cumana,Ostreacyrnusi,Ostreadepressa,Ostreaexalbida,Ostreahippopus,Ostrealamellosa,Ostrea leonica,Ostreaparasitica,Ostrearostrata,Ostreasaxatilis,Ostreascaeva,Ostreastriatum,Ostrea sublamellosa,Ostreataurica,Ostreavulgare Petricolariapholadiformis:Gastranellatumida,Petricolacarolinensis,Petricolaflagellata,Petricolafornicata, Petricolapholadiformis,Petricolarogersi Philinejaponica:Philineorientalis,Philineargentata,Philinestriatella Philineorientalis:Philineargentata,Philinestriatella,Philinejaponica Potamopyrgusantipodarum:Hydrobiajenkinsi,Paludestrinajenkinsi,Potamopyrgusjenkinsi Tenelliaadspersa:Embletoniapallida,Eolisventilabrum,Tenelliapallida,Tergipesadspersus Teredobartschi:Teredoaegyptia,Teredobalatro,Teredobatilliformis,Teredofragilis,Teredogrobbai,Teredo hiloensis,Teredoshawi Teredofurcifera:Teredoaustralasiatica,Teredobensoni,Teredofurcata,Teredofurcillatus,Teredokrappei,Teredo laciniata,Teredoparksi Teredonavalis:Pholasteredo,Serpulateredo,Teredoaustini,Teredobatavus,Teredobeachi,Teredobeaufortana, Teredojaponica,Teredomarina,Teredomorsei,Teredonovangliae,Teredopocilliformis,Teredosellii, Teredosinensis,Teredovulgaris Urosalpinxcinerea:Fususcinereus,Urosalpinxfollyensis Venerupisphilippinarum:Paphiabifurcata,Ruditapesphilippinarum,Tapesphilippinarum,Tapesbiradiata,Tapes denticulata,Tapesducalis,Tapesindica,Tapesjaponica,Tapessemidecussata,Tapesviolascens,Venus philippinarum,Venustessellata
27 Algae Aglaothamniontenuissimum:Aglaothamnionbyssoides,Callithamnionarachnoideum,Callithamnionarnottii, Callithamnionbyssoides,Callithamnionfurcellariae,Callithamnionhiemale,Callithamniontenuissimum (Bonnemaison),CeramiumtenuissimumBonnemaison Antithamnionpectinatum:Antithamnionnipponicum,Antithamnionapplicitum,Antithamnioncristirhizoph,um, Callithamnionapplicitum,Callithamnionpectinatum,Herpothamnionpectinatum,Ptilothamnion pectinatum Ascophyllumnodosum:Ascophyllalaevigatum,Ascophyllumlaevigatum,Ascophyllummackayi,Ascophyllum mackayif.robertsonii,Ch,dariasc,pioides,Fucodiumnodosum,Fucusmackayi,Fucusnodosus,Fucus sc,pioides,Halicoccusnodosus,Halidryssiliquosa,Ozothallianodosa,Ozothalliavulgaris Caulacanthusustulatus:Caulacanthusdivaricatus,Caulacanthusindicus,Caulacanthusokamurae,Caulacanthus spinellus,Fucusacicularisvar.ustulatus,Gelidiumustulatum,Gigartinaustulata,Laurenciadivaricata, Rhodomelaspinella,Sphaerococcusustulatus Caulerpataxifoli:,Fucustaxifolius Codiumfragilesspfragile:Codiumfragilefragile,Codiumfragilecapense,Codiumfragilessptomentosoides Gelidiumvagum:Gelidiumgrubbae Gracilariavermiculophylla:Gracilariaasiatica,Gracilariopsisvermiculophylla Grateloupialanceolata:Aeodeslanceolata,Pachymeniopsislanceolata Grateloupiaturuturu:Grateloupiad,yph,a Lomentariahakodatensis:Lomentariasinensis Neosiphoniaharveyi:Polysiphoniaargentinica,Polysiphoniahavanensisvar.insidiosa,Polysiphoniainsidiosa, PolysiphonianovaͲangliae,Polysiphoniaharveyi Polysiphoniadenudate:Hutchinsiabiasolettoana,Hutchinsiavariegata,Polysiphonialeptura,Polysiphonia variegata,Polysiphoniavidovichii Sargassumhorneri:Sargassumh,neri,Fucush,neri,Sargassum(Bactrophycus)h,neri,Sargassumspathulatum SargassummuticumSargassumkjellmanianumf.muticum Undariapinnatifida:Alariapinnatifida,Ulopteryxpinnatifida Crustacea Caprellamutica:Caprellamacho Orientomysisaspera:Acanthomysisaspera Orientomysishwanhaiensis:Acanthomysishwanhaiensis Hyperacanthomysislongirostris:Acanthomysislongirostris Caecidotearacovitzai:Asellusracovitzai AmphibalanusAmphitrite:Balanusamphitrite Amphibalanusimprovisus:Balanusimprovisus Amphibalanusreticulates:Balanusreticulatus
28 Carcinusmaenas:Cancergranarius,Cancergranulatus,Cancermaenas,Cancerpygmeus,Cancerrhomboidalis, Cancerviridis,Carcinusgranulatus,Carcinusmoenas,Megalopamontagui Caprellascaura:Caprellacornuta,Caprellanodosa Cheluraterebrans:Cheluracambrica,Cheluranesaeoides,Chelurapontica,Cheluraxylophaga Eurylanaarcuata:Cirolanaarcuata Monocorophiumacherusicum:Corophiumacherusicum Monocorophiuminsidiosum:Corophiuminsidiosum Dynoidesdentisinus:Dynoidellaconchicola,Dynoidesconchicola Synidotealaevidorsalis:Edotialaevidorsalis Amphibalanusalbicostatus:Fistulobalanusalbicostatus Upogebiaaffinis:Gebiaaffinis Eriocheirsinensis:Grapsusnankin,Grapsusnankin Iaiscalifornica:Janiropsiscalifornica Exopalaemonmodestus:Leanderczerniavskyi,Leandermacrogenitus,Leandermodestus Exopalaemoncarinicauda:Leanderlongirostris,Palaemoncarinicauda,Exopalaemoncarinicauda Lernaeacyprinacea:Lernaeacarassii,Lernaeaelegans,Lernaeaesocina,Lernaearanae,Lernaeatentaculis, Lernaeoceracyprinacea,Lernaeoceragasterostei Sinocalanusdoerrii:Limnocalanussinensisdoerrii Microdeutopusgryllotalpa:Microdeutopusbidens,Microdeutopusgrandimana,Microdeutopusminax, Microdeutopussalenskii Mytilicolaorientalis:Mytilicolaostreae Transorchestiaenigmatica:Orchestiaenigmatica Rhithropanopeusharrisii:Panopeuswurdemannii,Pilumnusharrisii Pseudosphaeromasp.:Paradynamenopsissp. Callinectessapidus:Portunusdiacantha Stenothoevalida:Proboliumpolyprion,Stenothoeassimilis,Stenothoemegacheles,Stenothoeornata,Stenothoe polyprion Eusarsiellazostericola:Sarsiellatricostata,Sarsiellazostericola Pseudodiaptomusforbesi:Schmackeriaforbesi Corophiumalienense:Sinocorophiumalienense Corophiumheteroceratum:Sinocorophiumheteroceratum Sphaeromaquoianum:Sphaeromaquoyanum
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