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CritiqueoftheDocument “InformationRegardingConcernsaboutFarmedSalmon-WildSalmonInteractions” PresentedtotheProvincialGovernmentofBritishColumbiabyGaryMarty,D.V.M.,Ph.D., Diplomate,A.C.V.P.oftheBritishColumbiaMinistryofAgriculture,AnimalHealthCentre, Abbotsford. Authorsofthiscritique: LawrenceM.Dill1,MartinKrkosek2,BrendanConnors3,StephanieJ.Peacock4, AndrewW.Bateman5,RichardRoutledge6,MarkA.Lewis7,andJohnReynolds8 1ProfessorEmeritus,DepartmentofBiologicalSciences,SimonFraserUniversity 2AssistantProfessor,DepartmentofEcologyandEvolutionaryBiology,UniversityofToronto 3SeniorSystemsEcologist,ESSATechnologies,andAdjunctProfessor,DepartmentofBiologicalSciences, SimonFraserUniversity 4PhDCandidate,DepartmentofBiologicalSciences,UniversityofAlberta 5PostdoctoralFellow,DepartmentofBiologicalSciences,UniversityofAlbertaandDepartmentofEcology andEvolutionaryBiology,UniversityofToronto 6Professor,DepartmentofStatisticsandActuarialScience,SimonFraserUniversity 7ProfessorandSeniorCanadaResearchChair,DepartmentsofBiologicalSciencesandMathematicaland StatisticalSciences,UniversityofAlberta 8ProfessorandTomBuellBCLeadershipChairinAquaticConservation,DepartmentofBiologicalSciences, SimonFraserUniversity Background Thedocument,“InformationRegardingConcernsaboutFarmedSalmon-WildSalmon Interactions,”datedMarch16,2015,waspresentedtoMinistersThompsonandLetnikof theGovernmentofBritishColumbia(BC)withtheintentionofprovidingscientific informationuponwhichtobasemanagementandpolicydecisionsregardingwildand farmedsalmoninBritishColumbia. Collectively,weareagroupofscientists,mostlyacademic,whoseresearchexpertise includessalmonandinfectiousdiseases(herewerefertoinfectiousdiseasesinthe broadestsenseasthosethatmayarisefromparasitic,viralorbacterialpathogens).Allof ushaveworkedspecificallyontheinfluenceofsalmonaquacultureondiseasesofwild salmoninBC,andtheassociatedconsequencesforthesustainabilityofbothwildand farmedsalmon.Wehavepublishedmorethan40peer-reviewedarticlesonthe interactionsbetweenfarmedsalmonandwildsalmonintheprimaryscientificliterature. Moregenerally,wehaveover150yearsofcombinedresearchexperienceandhave publishedmorethan400peer-reviewedarticlesintheprimaryliteratureinthefieldsof marinebiology,fisheriesscience,invasionbiology,epidemiology,andpopulationbiology. 1 WhileweacknowledgeDr.GaryMarty’simpressivecredentialsasafishpathologist,we havedeepconcernsthatthedocumenthepresentedtotheProvincialGovernment incorrectlyrepresentsthecurrentscienceontheecologyofdiseaseinteractionsbetween wildandfarmedsalmon.Inparticularthereareseveralerrorsofinterpretationanda selectiveuseoftheliteraturethatwebelieveleadtoabiasedconclusionthatfarmed salmonposeminimaldiseaseriskstowildsalmoninBC.Amorecompleteandbalanced assessmentofthescientificliteraturerevealsabundantevidencethatsalmonaquaculture doesposeadiseaserisktowildsalmon,althoughthereisongoingdebateabouttheextent ofthatrisk.Furthermore,theliteraturerevealsthatsalmonaquaculturecandepresswild salmonpopulationsundersomecircumstances.Forthisreason,governmentagencies, academicinstitutions,non-profitorganizations,andindustrygroupsarecurrentlyengaged inactiveresearchintodisease-mediatedinteractionsbetweenfarmedandwildsalmonin BritishColumbia. InrespondingtoDr.Marty’sopinion,wemakethefollowingsixpoints: 1. Theeffectsofdiseaseonthesurvivalofsalmoninthewildcanbemoreseverethanin captivity,particularlyforjuveniles. 2. Thereisuncertaintyaboutthecauseofdeathofmostsalmonthatdieonsalmonfarms. 3. Dr.Martymisrepresentsormisinterpretspublishedworkthatheusestosupporthis claims. 4. Dr.Martyomittedevidencethatcontradictsanumberofhisclaims. 5. Dr.Martyfailedtomentiongeneticteststhatsuggestinfectioussalmonanemiavirus (ISAv)ispresentinBC. 6. Dr.Martyfailedtoconsideremergingandevolvingdiseasesthathavethepotentialto impactwildsalmonpopulations. 1. Theeffectsofdiseaseonthesurvivalofsalmoninthewildcanbemore severethanincaptivity,particularlyforjuveniles. Itisillogicaltodrawconclusionsabouttheeffectsofdiseaseinwildsalmonbasedsolelyon theeffectsofdiseaseinfarmedsalmon.Farmedsalmondonothavetomigrate,avoid predators,orcompeteforscarcefood,unliketheirwildcounterparts.Publishedscientific evidenceshowsthatwildsalmondosufferdirectmortalityfromdisease,butdiseasealso compromisestheirabilitytogrow,tocompeteandtoavoidpredators.Farm-amplifiedsea licealonecauseanaverageof39%lossofwildsalmonreturningtoriverseveryyearin Europe(1).Theselossesoccurinthecontextofmodernfish-healthpracticesaimedto controlparasitessuchthatmortalitiesoffarmedfishduetoparasitesalmostneveroccur. MortalityofwildsalmoninBritishColumbiaduetosealicefromfarmedsalmonis estimatedtohavebeenevenhigherinsomeyears(2,3).Otherinfectiouspathogensare alsolinkedwithincreasedmortality,predationbyseabirds,andmigrationfailurefor sockeyesalmon(4). Placementofsalmonfarmsalongsalmonmigrationroutescanexposewildsalmonto pathogenspreciselywhentheyaremostvulnerable.Migratingjuvenilesalmonare 2 particularlysusceptibletotheeffectsofpathogensduetotheirsmallsize(5),highnatural mortalityduetopredation(6),stressfromsmoltification(7),andunderdevelopedscales (8).Forexample,experimentalevidenceindicatesthatsealicemakejuvenilepinkand chumsalmonmorepronetopredation(9)byreducingswimmingability(10)and increasingrisk-takingbehaviour(9).Chinooksalmonexperimentallyinfectedwith Renibacteriumsalmoninarum,thecausativeagentofbacterialkidneydisease(BKD),were almosttwiceaslikelytobeeatenbylargerfishthantheiruninfectedcounterparts(11). Fieldstudiesalsosuggestthatparasite-mediatedpredationisimportant;Milleretal.found ahigherdiversityandloadofmicroparasitesinjuvenilesockeyesalmonpredatedby RhinocerosAukletsthanthosesampledbytrawl,suggestingselectivepredationbythese seabirdsoninfectedsockeye(4). Pathogenscanalsoindirectlyaffectwildsalmonbyreducingjuvenilegrowthrates(12), whichinturncanbeanimportantdeterminantofmarinesurvivalandsubsequentreturns ofadults(13,14).Juvenilesalmonfaceatrade-offbetweenallocatingresourcestobody growthandallocatingresourcestoimmunefunction.Scientificstudiesindicatethat juvenilesockeyesalmonontheeastcoastofVancouverIslandthatareinfectedwithsea licehavereducedcompetitiveforagingabilityrelativetouninfectedconspecifics(15).This resultalignswithapublishedscientificstudythatsuggeststhesurvivalofFrasersockeyeis poorwhenfarmedsalmonareabundantalongthejuveniles’migrationrouteandthe potentialforcompetitionwithpinksalmonishigh(16). 2. Thereisuncertaintyaboutthecauseofdeathofmostsalmonthatdieon salmonfarms. Onlyasmallproportionofmortalitiesonsalmonfarmsareeverexaminedfordisease.Dr. Martywritesthat:“Lessthan1%ofBCfarmedAtlanticsalmondieofdiseasesthatmightbe infectioustowildPacificsalmon.Amongtheother99%offarmedsalmon,90%surviveand 9%dieofothercauses." Indeed,dataprovidedduringtheCohenCommissionshowthattheaveragemortalityrate basedon“freshsilvers”,orrecentlydeceasedfishthatcanprovidevaluableinformationon diseaseorothercausesofdeath,is1-5%(17,p.7).However,totalmortalityhasaveraged 9-13%perannumandhasbeenashighas30%in2003(17,p.7).Ofthismortality,just 20-25%arefreshsilversthatareexaminedforbacterialandviralpathogens.Manymore fishdieinthepensof“other”(unknown)causesandareneverexamined(17,Fig.4).Even forthefreshsilversthatareexamined,nocauseofdeathisestablishedforabout60-70%of thefishintheBCMinistryofAgricultureandLandsaudits(17,Fig.5).Therefore,theactual incidenceofpotentiallytransferablepathogensamongfarmedsalmoncouldbemuch higherthanDr.Marty’sstated1%. Dr.Martyalsomakestheassumption,withoutproof,thatasymptomaticfarmedsalmon cannotshedpathogensthatareharmfultowildfish.WecautionthatsomeofthepapersDr. Martycitestomakehiscase(e.g.,18)seemtobemisrepresented(seepoint3,below). 3 Transferofpathogensfromasymptomatichostsiscommoninterrestrialsystems(19),and thereisnoreasontobelieveitwouldnotoccurinthemarineenvironment. 3. Dr.Martymisrepresentsormisinterpretspublishedworkthatheusesto supporthisclaims. Onpage5,Dr.Martystates:“…arecentscientificpublication…reportednorelationbetween farmfishproductionintheDiscoveryIslandsandFraserRiversockeyesalmonreturns(20).” Dr.Marty’sinterpretationofthispublicationiscompletelyoppositetotheactualfindingsof thestudy.Basedonanalyzingdatafromover35sockeyepopulations,Ruggeroneand Connors(20)corroboratedthefindingsofpreviousresearch(16)showingthatthereisa negativecorrelationbetweensockeyesalmonsurvivalandthenumberoffarmedsalmon thatwildFrasersockeyemigratepastearlyinmarinelife. Onpage4,Dr.Martysays:“Datapresentedduring[theCohenCommission]didnotshowthat salmonfarmswerehavingasignificantnegativeimpactonFraserRiversockeye.”However, Dr.MartyfailstoincludethelinethatimmediatelyfollowsthisquotefromtheCohen Commissionreport,“…thestatisticalpowerofthedatabase(containingfishhealthdata from2004to2010)wastoolowtoruleoutsignificantnegativeimpact”(21,p.24).Bynot includingthisadditionalcontext,Dr.Martyleavestheimpressionthatwecanconfidently concludethatsalmonaquaculturedoesnotposeapotentialrisktoFraserRiversockeye. JusticeCohen,however,concludesthat“…net-pensalmonfarmingintheDiscoveryIslands posesariskofseriousharmtoFraserRiversockeyethroughthetransferofdiseasesand pathogens”(21,p.25). Onpage6whereDr.Martydiscussespotentialfarmedsalmonimpactsonwildsalmonin Norway,hequotesHusaetal.(22),“[t]hegoodecologicalconditionsoftheparameters studiedinthefjordshowlittleevidenceofaregionalimpactfromthefishfarmingindustry despitetheintensiveproductionlevel.”Thecitedstudydidnotmonitorwildsalmon,let alonepathogenoccurrenceinwildsalmon,butwasfocusedonalgalcommunitiesinthe fjord,andthushasnodirectbearingonthequestionofriskposedtowildsalmonby farmedsalmon. Dr.Martygoesontostateonpage6,“…nominalcatchesofwildAtlanticsalmonhave declinedinnearlyalljurisdictionsoverthepastfewdecades.However,thesedeclinesarenot greaterinNorwaythaninjurisdictionswithoutabundantsalmonfarms(23).”Hefailsto acknowledgethattheverypublicationhecitesdoesnotsupporthisassertionthat pathogensfromfarmedfishposeatmostaminimalrisktoadjacentwildsalmon populations.Rather,theauthorsstateintheabstract,“Salmonliceoriginatingfromfarms negativelyimpactwildstocksofsalmonids,althoughtheextentoftheimpactisamatterof debate”(23). Lastly,onpage11whereDr.MartyclaimsthereisevidencethatAtlanticsalmonarenot asymptomaticcarriersofdisease,hestates,“…sixscientificstudieshavebeenconductedin whichAtlanticsalmonsourcedfromcommercialfarmerswerecohabitedwithvariousPacific 4 salmonspeciesundercontrolledlaboratoryconditions(18,24–28).ThePacificsalmonnever developedunexpecteddiseasefromtheAtlanticsalmon:evidencethattheAtlanticsalmon werenotcarryinganunknowndiseaseofconcerntoPacificsalmon.”However,oneofthese studiesactuallylookedfortransferofdiseasefromPacifictoAtlanticsalmon,andclearly foundit.Andnoneofthesestudiesweredesignedtomonitororquantifytheextentof “unexpecteddisease”orasymptomaticpresenceofabroadrangeofpathogensthatmay affectwildandfarmedsalmon(e.g.,4).AlthoughmassunexplainedmortalityofPacific salmonwasnotobservedinthestudiesDr.Martycites(atleastthosethathavebeen published)thisisnotevidencethatAtlanticsalmonarenotpotentialasymptomatic carriersofdiseaseundersomeconditions. ThesemisrepresentationsormisinterpretationsshowthattheconclusionsDr.Marty reachedarebaseduponaselectiveuseofthepublishedliterature,therebycastingdoubton hisconclusionthatthereexistsminimalriskofdiseasespreadfromfarmedsalmontowild salmon. 4. Dr.Martyomittedevidencethatcontradictsanumberofhisclaims. Byignoringalargebodyofresearchthatcontradictsmanyofhisclaims,Dr.Martypresents abiasedandoverlycertainviewoftheriskposedbysalmonaquaculturetowildsalmon. Manystudiesindicatethatsalmonaquacultureisassociatedwithelevatedmortalityofwild salmon.Thesestudiesincludeanalysesofmultiplestocks(e.g.,1,29)andspecies(e.g.,30). Aspreviouslymentioned,sealicealonehavebeenshownexperimentallytocauseupto 39%mortalityofwildsalmoninEurope(1),whileobservationalstudiessuggestthis numbercanbemuchhigherforPacificsalmon(2,3,31).Furtherdataindicatethatother bacterialandviralpathogenscanalsoincreasemortalityofjuvenilewildsalmon(32–34). Althoughthesestudiesdidnotlinkwildsalmonmortalitydirectlytosalmonfarming,there ispotentialforfarmedsalmontoamplifyadiversityofpathogens. AkeycitationusedbyDr.Martytosupportthestatementthatsalmonfarmsdonotaffect wildsalmonishisownwork(35).Dr.Martyfailstomentionthathisanalysiswasnot conclusivebecauseithadlowpowertodetectaneffect(2).Indeed,areanalysisofthedata, publishedinthesamescientificjournal,revealedthatproductivityofbothpinkandcoho salmonwasnegativelyrelatedtoabundanceofsealiceonsalmonfarmsintheBroughton Archipelago(2).Werecognizethatthereiscontinuingdebateoverthemagnitudeofthe effectofsalmonfarmingonwildsalmon(23),andthattheimpactmayvaryamongspecies ofsalmon,locations,andyears(e.g.,36).However,byfailingtoacknowledgethepublished worksthatfoundparasitesfromsalmonfarmsmaynegativelyaffectwildsalmon populations(3,29,37–40),Dr.Martypresentsabiasedperspectiveonthecurrentstateof knowledgeregardingthepotentialeffectsofsalmonfarmingonwildsalmon. 5 5. Dr.Martyfailedtomentiongeneticteststhatsuggestinfectioussalmon anemiavirus(ISAv)ispresentinBC. WhilewerecognizethatnumeroussamplesofPacificsalmonhavenottestedpositivefor ISAv(e.g.,41),severallaboratorieshaveconductedteststhatindicategeneticelementsof ISAvarepresentinPacificsalmon(42).AlthoughthisisnotconclusiveevidencethatISAv ispresentinBC,itismisleadingtoignorethesetestresults.Thefollowingtestresultswere reportedtotheCohenCommissionofInquiry(43,ch.9): • Over60samplesfromtheendangered(44)CultusLakesockeyesalmonpopulation producedpositivereadingsintestsconductedinaDFOlaboratory,and • 40samplesfromthedepressed(45)RiversInletsockeyesalmonpopulation producedatleastonepositivereadingintestsconductedatfourlaboratories despitewidespreadrecognitionthatthesampleswereconsiderablydegraded. Dr.MartycontendsthatsuchresultsareallfalsepositivesbecausetheWorldOrganisation forAnimalHealth(OIE)requirementthatthevirusbeisolatedwasnotmet.However, failuretoprovidedefinitiveproofofpresencedoesnotconstitutedefinitiveproofof absence.CircumstantialevidenceofthepresenceoftheISAvirusintheNorthPacific shouldnotbereadilydismissedasfalsepositives.Indeed,intheCohenCommissionreport, JusticeCohenconcludedthat,“…theevidencedoesnotallowmetoconcludewhetherISAv oranISAv-likeviruscurrentlyexistsinFraserRiversockeye”(46,p.60). TheriskthatISAvposestowildsalmonisacombinationoftheprobabilitythatISAvis presentandtheconsequencesifitis.Conditionsincrowdednetpenscanselectformore virulentstrainsofISAv(47,48),andthevirushasalreadycausedsignificantmortalityof farmedAtlanticsalmoninEurope(49),Chile(50)andeasternCanada(51).Perhapsof greaterconcernisthatthevirushasbeenshowntocausemortalityinrainbowtrout(52, 53)andcohosalmon(54).Withsuchpotentiallysignificantconsequences,webelievethat theprecautionaryprincipleshouldbeapplied,andsurveillanceoffarmedandwildsalmon forISAvbeexpanded. 6. Dr.Martyfailedtoconsideremergingandevolvingdiseasesthathavethe potentialtoimpactwildsalmonpopulations. Evidencecontinuestoemergeofvirusesassociatedwithsalmonaquaculturethatposea potentialthreattowildsalmon,andthepotentialforcumulativeandinteractiveeffectsof multipleinfectionsbydifferentviruses(e.g.,55). Piscinereovirus(PRV)iswidelyacknowledgedaspresentandwidespreadinBritish Columbia–introutaswellassalmon(56,57).Thereisstrongevidenceofanassociation betweenPRVandthedisease,heartandskeletalmuscleinflammation(HMSI;58,59),ifnot adirectcause-and-effectrelationship(60).Dr.Marty′scommentaryonPRVfailstomention thesepapers.HisdismissalofthepotentialforPRVtocauseHSMIinwildPacificsalmonis basedonthefactthatHSMIhasnotbeenobservedinwildsalmon;however,itisimportant 6 tobearinmindthatinfectedwildfishmaynotsurviveforlongoncetheydevelopdisease (61). Thepiscinemyocarditisvirus(PMCV),associatedwithcardiomyopathysyndrome(CMS), alsowarrantsattention.CMSwasdescribedfirstinwildAtlanticsalmonin2003(62),and ithasbeensubsequentlyshownthatthemostlikelycausativeagentisPMCV(63).In addition,itispossiblethatPMCVispresentinBritishColumbiawaters;potential symptomsofCMSinBritishColumbianfarmedsalmonwasdocumentedin2002(64). Similarly,thethreatofsalmonalphavirus(SAV)onPacificsalmonandtroutshouldnotbe takenlightlygivenevidenceofimpactsofthisvirusonrainbowtrout(65). Finally,inconcludingthatpathogensfromsalmonfarmingposeatmostaminimalriskto wildsalmon,Dr.Martydidnotconsiderthepotentialforestablishedpathogenstoevolve. Parasitessuchassealicecanevolveresistancetocurrenttreatments,ashasoccurredin Europe,ChileandeasternCanada(23,66).Morevirulentstrainsofintroducedornative virusescanmultiplyinfishfarms(47,48,67),andthesecouldpotentiallyspreadtowild populations.Theseevolutionarychangesinpathogensarefavouredbythedomesticated environmentoffarmedfishandcanproduceepidemicsthataremoresevereandmore difficulttocontrol. Conclusion Wearenotopposedtosalmonaquacultureinprinciple,nordowebelievethatsalmon aquacultureisresponsibleforallthechallengesfacedbyPacificsalmonpopulationsin BritishColumbia.However,acompleteandbalancedexaminationoftheavailableevidence leadsustoconcludethattherisksposedbyaquaculturetowildsalmonarenon-negligible. Thisispreciselywhythereisextensiveongoingresearchbygovernmentagencies, academicinstitutions,non-profitorganizationsandindustrygroupsintodisease-mediated interactionsbetweenfarmedandwildsalmon. Webelievethatinordertodevelopevidence-basedpoliciesthatminimizetheriskof diseasetofarmedandwildsalmon,policy-makingmustbeinformedbyscience.Wehave deepconcernsthatthescienceadviceofferedbyDr.GaryMartytoMinistersThompson andLetnikoftheGovernmentofBCisanincompleteandbiasedsummaryofthecurrent scientificunderstandingofdiseaseinteractionsbetweenwildandfarmedsalmon.Aswe haveshown,amorecompleteassessmentofthescienceontheinteractionsbetween farmedandwildsalmonindicatesahigherriskthanDr.Martycommunicated,aswellasa higherdegreeofscientificdebateontheextentofthisrisk. 7 References 1. KrkošekM,RevieCW,GarganPG,SkilbreiOT,FinstadB,ToddCD(2013)Impactof parasitesonsalmonrecruitmentintheNortheastAtlanticOcean.ProcRoySocB 280:20122359. 2. KrkošekM,ConnorsBM,MortonA,LewisMA,DillLM,HilbornR(2011)Effectsof parasitesfromsalmonfarmsonproductivityofwildsalmon.ProcNatlAcadSci 108:14700–14704. 3. 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