Download Critique Dr. Gary Marty

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.
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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
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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).
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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
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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.
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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
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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.
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