Harmful Algal Blooms Along the North American West Coast Region

29 Pages·2017·1.87 MB·English

University of Nebraska - Lincoln
DigitalCommons@University of Nebraska - Lincoln
Publications, Agencies and Staff of the U.S.
U.S. Department of Commerce
Department of Commerce
2012
Harmful Algal Blooms Along the North American
West Coast Region: History, Trends, Causes, and
Impacts
Alan J. Lewitus
NOAA, [email protected]
Rita A. Horner
University of Washington - Seattle Campus, [email protected]
David A. Caron
University of Southern California, [email protected]
Ernesto Garcia-Mendoza
Centro de Investigación Científica y de Educación Superior de Ensenada, [email protected]
Barbara M. Hickey
University of Washington - Seattle Campus, [email protected]
See next page for additional authors
Follow this and additional works at:http://digitalcommons.unl.edu/usdeptcommercepub
Lewitus, Alan J.; Horner, Rita A.; Caron, David A.; Garcia-Mendoza, Ernesto; Hickey, Barbara M.; Hunter, Matthew; Huppert, Daniel
D.; Kudela, Raphael M.; Langlois, Gregg W.; Largier, John L.; Lessard, Evelyn J.; RaLonde, Raymond; Jack Rensel, J. E.; Strutton,
Peter G.; Trainer, Vera L.; and Tweddle, Jacqueline F., "Harmful Algal Blooms Along the North American West Coast Region: History,
Trends, Causes, and Impacts" (2012).Publications, Agencies and Staff of the U.S. Department of Commerce. 499.
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Authors
Alan J. Lewitus, Rita A. Horner, David A. Caron, Ernesto Garcia-Mendoza, Barbara M. Hickey, Matthew
Hunter, Daniel D. Huppert, Raphael M. Kudela, Gregg W. Langlois, John L. Largier, Evelyn J. Lessard,
Raymond RaLonde, J. E. Jack Rensel, Peter G. Strutton, Vera L. Trainer, and Jacqueline F. Tweddle
This article is available at DigitalCommons@University of Nebraska - Lincoln:http://digitalcommons.unl.edu/usdeptcommercepub/
499
HarmfulAlgae19(2012)133–159

ContentslistsavailableatSciVerseScienceDirect

Harmful Algae

journal homepage: www.elsevier.com/locate/hal

Harmful algal blooms along the North American west coast region:

History, trends, causes, and impacts

Alan J. Lewitusa,*, Rita A. Hornerb, David A. Caronc, Ernesto Garcia-Mendozad, Barbara M. Hickeyb,
Matt he w Huntere, Dan iel D. Huppe rtf, Rap ha el M. Ku delag, G regg W. Langloish, John L. L arg ieri,
Evelyn J. Lessardb, Raymo nd RaLondej, J.E. Jack Re nselk, Pet er G. S trut tonl,1, Ver a L. T rai nerm,
Jacquel in e F. Twed dlel,2

aCenterforSponsoredCoastalOceanResearch,NationalCentersforCoastalOceanScience,NationalOceanService,NationalOceanicandAtmosphericAdministration,1305EastWest

Highway,SilverSpring,MD20910,UnitedStates
bUniversi tyofW ashing ton, School ofOcea nography,Box357940,Seattle,WA98195,UnitedStates
cUniversity of SouthernCal ifornia, De partmentofBio logi calScien ces,361 6Tr ousdale Ave.,L osAngeles,CA90089,UnitedStates
dBiological Oc eanograph yDepartm ent,Centrod e Investigac io´nCientı´ ficay deEducac io´nSu per iordeEn sen ada,Km 107c arrTij-Ens,Ensenada,BajaCalifornia,Mexico
eOregonDe partmentofFi shandWildli fe,2001 M arineDrive,R oom120, A sto ria,OR971 03,Unite dS tates
fUnivers ityofWashin gt on,S choo lofMari neAff airs,37 07Bro oklynA ve.N E,Seatt le,W A981 05,Uni tedStates
gUniversity of CaliforniaSa ntaCru z, OceanS ciences andI nstitutefo rMa rine Science s,11 56Hig hStreet ,SantaCruz,CA95064,UnitedStates
hCalifornia De partment ofPubl icHea lth,Ri chmond Labo ratoryCa mp us,850 MarinaB ayPa rkway ,G165 ,Richm ond, CA 94804, United States
iUniversity ofCalifornia D avis,Bo degaM arineLabo ratory,P.O. Box247, Bod egaBay ,CA 94923,Un itedSt ates
jUniversity of AlaskaFai rbanks ,School ofFishe riesandOce anS cien ces,A laskaS eaGr ant Marine Adviso ryProgram,1007W.3rdAve#100,Anchorage,AK99501,UnitedStates
kRenselAss oc iatesAq uaticScien ces,42 09 234thSt reet N.E.,Ar lington,W A982 23, United States
lOregon StateUniv ersity,C ollegeof Ocean icand Atmos pher icSciences ,104 COAS AdminB ldg,Corvallis,OR97331,UnitedStates
mNorthw estF isheriesScie nceCen ter ,Nationa lMa rineFisheries Service,N atio nalOc eanica ndAtm ospheric Adm inistra tion,M arineBiotoxinProgram,2725MontlakeBlvd.E.,Seattle,

WA98112,UnitedStates

AR TI CLE I NFO ABS TRA CT

Articlehistory: AlongthePacificcoastofNorthAmerica,fromAlaskatoMexico,harmfulalgalblooms(HABs)have
Receiv ed21November2010 caused los seston atura lre source sandcoa stale conomi es, andhav eresulted inh umansi cknesse sand
Received in r evised form 23 June 2012 deaths fordec ad es.Rece ntreports indi cateap ossibleincre ase inthe irprevale nc eandim pactsofth ese
Accepted23June2012
eventsonlivingresourcesoverthelast10–15years.TwotypesofHABsposethemostsignificantthreat
Availableonline6July2012
to coastal ecosystems in this ‘‘west coast’’ region: dinoflagellates of the genera Alexandrium,

Gymnodinium,andPyrodiniumthatcauseparalyticshellfishpoisoning(PSP)anddiatomsofthegenus
Keywords:
Pseudo-nitzschiathatproducedomoicacid(DA),thecauseofamnesicshellfishpoisoning(ASP)inhumans.These
Alexandrium
speciesextendthroughouttheregion,whileproblemsfromotherHABs(e.g.,fishkillslinkedtoraphidophytesor
Domoicacid
Cochlodinium,macroalgalbloomsrelated toinvasivespecies,seabirddeathscausedbysurfactant-like proteins
HHeatremrofusilg malgaal blooms producedbyAk ashiwosan guinea, hepatot oxi nsfrom Microcy stis, diarr heticsh ellfishp ois oningfromDin ophysis,

Paralyticshellfishpoisoning anddinoflagellate-producedyessotoxins)arelessprevalentbutpotentiallyexpanding.Thispaperpresentsthestate-

Pseudo-nitzschia of-knowledgeonHABsalongthewestcoastasasteptowardmeetingtheneedforintegrationofHABoutreach,

research,andmanagementefforts.

PublishedbyElsevierB.V.

* Correspondingauthor.Tel.:[phone];fax:[phone].

E-mailaddresses:[email protected](A.J.Lewitus),[email protected](R.A.Horner),[email protected](D.A.Caron),[email protected](E.Garcia-Mendoza),

[email protected](B.M.Hickey),[email protected](M.Hunter),[email protected](D.D.Huppert),[email protected](R.M.Kudela),

[email protected](G.W.Langlois),[email protected](J.L.Largier),[email protected](E.J.Lessard),[email protected](R.RaLonde),

[email protected](J.E.JackRensel),[email protected](P.G.Strutton),[email protected](V.L.Trainer),[email protected](J.F.Tweddle).

1 Currentaddress:InstituteforMarineandAntarcticStudies,UniversityofTasmania,PrivateBag129,Hobart,Tas7001,Australia.
2 Current address: NAFCMa rin eCentre ,Por tArthur, Scallowa y,Shetland Z E10UN,Un itedKin gdo m.

1568-9883/$–seefrontmatter.PublishedbyElsevierB.V.

http://dx.doi.org/10.1016/j.hal.2012.06.009
134 A.J.Lewitusetal./HarmfulAlgae19(2012)133–159

1. Introduction coastHABswillthereforerequirearegionallyintegratedapproach,

and effective HAB management will depend on interstate and

Harmfulalgalblooms(HABs)areaglobalthreattolivingmarine internationalcollaborationandcoordination.

resourcesandhumanhealth.TheseeventsimpactallcoastalU.S. Severalpolicydriverscallforaregionalapproachtoaddressing

states and large portions of coastal Canada and Mexico (Taylor, marine problems (e.g., U.S. Commission on Ocean Policy, 2004;

1993;Horneretal.,1997;Mudieetal.,2002;Herna´ndez-Becerril NOAA Program Planning and Integration, 2007; NSTC Joint

et al., 2007; Anderson et al., 2008b; Band-Schmidt et al., 2010). Subcommittee on Ocean Science and Technology, 2007; Joint

Harmful algal blooms have had significant ecological and OceanCommissionInitiative,2009).The2004Reauthorizationof

socioeconomic impacts on Pacific coastal communities of North theHarmful AlgalBloomand HypoxiaResearch ControlAct also

America fordecades,andtheirprevalence andimpactsonliving acknowledgedtheneed foraregionalapproachtoHABresearch

resources in this west coast region have increased markedly in andresponsebyestablishingaprocedureforrequestingRegional

frequencyandgeographicaldistributionoverthelast10–15years AssessmentsofHABs.TheU.S.CommissiononOceanPolicy(2004)

(Andersonetal.,2008b;Kudelaetal.,2008a;Kahruetal.,2009; and the Pew Oceans Commission (2003) recommended regional

Band-Schmidtetal.,2010;Renseletal.,2010b;Garcia-Mendoza, ocean governance efforts as an effective mechanism to facilitate

unpubl.data).TheHABsthatthreatenwestcoastwaterquality,the regionalecosystemassessmentandmanagement.Recognizingthis

healthoflivingresources,andtheeconomiesofitscommunities need, the West Coast Governors’ Agreement on Ocean Health

are diverse and often extend beyond jurisdictional boundaries. (WCGA) was established in 2006 as a proactive, regional

Comprehensiveunderstandingofthecausesandimpactsofwest collaborationtoprotectandmanageoceanandcoastalresources

Table1

Reportedhumanillnessesanddeathsduetoparalyticshellfishpoisonings.Additionalillnessesareknownfromallareas,butonlythoseassociatedwithfatalitiesarereported

here.Datesvarydependingonstate,countryandwhenmonitoringbegan.

Year Cases Deaths Counties/areasinvolved Shellfishkind

AK
17991 150+ 100 Sitka,PerilStrait Bluemussels
19342 12 2 Dougl asan dAdm iraltyIslands Notk nown
19443 4 1 LikelySi tka Not known
19474 3 1 PerilS trait Butt erclams
19545 8 1 False Pass Bluem ussels
19626 27 1 Porpo iseIs land Little neckclams
19626 1 1 HawkInl et Bluemuss els
19626 1 1 Shelte rBay Butte rclams
19656 4 1 HawkI nlet Butter clams
19947 16 1 Kalsin Bay, Kodiak Bluem ussels
19977,8 9 1 Sturge onR iver,Ko diak Butte rclams,

littleneckclams
19998 1 Kodiak Notknow n
20109 5 2 Juneau andHaines Cock les,Dungeness

crabviscera

BC
179310 4 1 PoisonCove Mussels,clams
194210 3 3 Barkley Soun d Mussels, clams
196510 4 1 Theodos iaInle t Cockles
198010 7 1 HealthHa rbor, GilfordIsland Butterclams

WA
194211 9 3 Sekiu,StraitofJuandeFuca Clams,mussels

OR
193311 21 1

CA
190312 12 5 SonomaCounty Californiamussels
192713 103 6 Sonoma, Marin, SanMateo Mussels
192913 60 4 Sonoma, Marin, San Mateo Mussels,clams
193613 3 2 Ventura Mussels
193913 76 8 SantaCr uz,Monterey Mussels,clams
194313 20 4 DelN orte,H umboldt Mussels
194413 12 2 San Mateo ,SantaCru z Mussels
194613 3 1 San Mateo Mussels
194813 3 1 San Mateo Mussels
198013 98 2 Son oma,M arin Mussels,oysters,

scallops
MX
197614 7 2 PacificMexico
1979–200815 391 24 Pacific Mexico
197916 18 3 Mazatl anBay,extensivefishkill Oysters,clams
198914,17 99 3 GulfofTe huan tepec Rockyoy sters
2001–200217 600 6 Mich oa ca´nandGuer rerocoasts
2001–200217 101 6 Chiapas,Gu erre rocoasts

Sources:AK:1Tikhmenev(1979),2SommerandMeyer(1937),3Alaska’sHealth(1945),4Magnussonetal.(1951),5MeyersandHillian(1955),6Orthetal.(1975),7Ostasz
(2001),8 RaLonde(2001), 9StateofAlaskaE pide miolog yBulletin(2010) ;BC:10 Chiang(1988);WA: 11N is hitaniandChew (198 8);OR: 11Nishitania nd Ch ew(1988);CA:
12SommerandMe yer(1937),13P ric eetal. (1991);MX:1 4Saldate- Castan˜e daetal.(1991 ),15Cort e´s-Altamiranoan dSi erra-Be ltra´n(2 008),16Meeeta l.(19 86),17 Herna´nd ez-

Becerriletal.(2007).
A.J.Lewitusetal./HarmfulAlgae19(2012)133–159 135

alongthecoastsofWashington(WA),Oregon(OR),andCalifornia SymptomsofPSPareneurological,onsetisrapidandcanresultin

(CA).Harmfulalgalbloomswerehighlightedasneedingimmedi- paralysisordeaththroughrespiratoryarrest.Toxicityvarieswith

ateattentionbyallthreestates. shellfishspecies,andsomeofthewestcoastspeciesmostlikelyto

TheWCGAcalledfor‘‘aHABworkshop...toreachconsensuson becontaminatedincludemusselspecies,butterclams(Saxidomus

the present state-of-knowledge and prioritize the information giganteus Deshayes), geoduck clams (Panopea generosa Gould),

neededbydecisionmakerstolessentheimpactsoftheHABevents razorclams(SiliquapatulaDixon),andPacificoysters(Crassostrea

onhumansandcriticalmarineresources’’aspartofthestrategyto gigasThunberg);seeSection2.2.Severalotherspeciesreportedly

promoteinterstatecoordinationofHABresearchandmonitoring have also been contaminated, including northern quahogs

efforts(ActionPlanfortheWestCoastGovernors’Agreementon (Mercenaria mercenaria Linnaeus), horse clams (Tresus nuttallii

Ocean Health, 2008). The National Oceanic and Atmospheric ConradandTresuscapaxGould),Pacificlittleneckclams(Protothaca

Administration(NOAA)andthestatesofCA,OR,andWAconvened stamineaConrad),manilaclams(VenerupisphilippinarumAdams&

the West Coast Regional Harmful Algal Bloom Summit on 10–12 Reeves), varnish clams (Nuttallia obscurata Reeve), purple-hinge

February2009inPortland,Oregon,tofulfilltheWCGAcharge.A rockscallops(HinnitesmultirugosusGale)andotherscallopspecies,

WhitePaper,HarmfulAlgalBloomsintheWestCoastRegion:History, cockle species, whelk species, moon snails (Lunatia heros Say),

Trends, and Impacts in California, Oregon, and Washington, was gooseneck barnacles (Pollicipes polymerus Gmelin), Dungeness

developed by the Summit Steering Committee to summarize the crabs(MetacarcinusmagisterDana),andspinylobsters(Panulirus

scope of the HAB problem in this region, in order to provide spp.) (Shumway et al., 1990; Shumway and Cembella, 1993;

backgroundonthestate-of-knowledgeforSummitattendees.Here, Matter,1994;Shumway,1995;Deedsetal.,2008).

weexpandonthatWhitePaper,incorporatingSummitfindingsand Human deaths attributed to PSP date back to 1793 (Table 1),

consensuses, and extending the geographical coverage of HAB when four members of Captain George Vancouver’s Royal Navy

impactsonthewestcoasttoincludeAlaska(AK),BritishColumbia crewbecamesickandonediedaftereatingshellfishfromabeach

(BC),theU.S.Pacificcoaststates,andMexico. incentral BC nowcalled PoisonCove (Quayle,1969; Fig. 2). The

oldestdocumentedapparentHABincidentinAKoccurredin1799

2. Paralyticshellfishpoisoning whentheAleutcrewoftheRussianfurtrader,AlexanderBaranof,

becameillaftereatingbluemussels(MytilusedulisLinnaeus)inan

2.1. Overviewoftoxicity,historyontheNorthAmericanwestcoast areanearSitka,AK,nowcalledPerilStrait(Table1andFig.1).This

incident resulted in an estimated 100 deaths (Fortuine, 1975).

Paralyticshellfishpoisoningiscausedby a suiteofbiotoxins, Morerecently,aJune2010incidentinsoutheastAKresultedinfive

collectivelycalledparalyticshellfishtoxins(PSTs).Taxaknownto illnesses and two deaths, the first deaths in AK since 1997.

producethesetoxinsincludespeciesofthedinoflagellategenera Elsewhere on the west coast, human poisonings from PSP were

Alexandrium, Gymnodinium, and Pyrodinium. The genus typically apparentlycommoninCAinthelasthalfofthe1800s(Sommer

associatedwithtoxicoutbreaksalongtheU.S.andCanadianwest and Meyer, 1937), but the first recorded incident occurred in

coastsisAlexandrium,whileGymnodiniumandPyrodiniumspecies SonomaCounty,centralCA, in1903, when 12people became ill

are associated with outbreaks in Mexico (Ochoa et al., 1997). andfivediedaftereatingCaliforniamussels(Mytiluscalifornianus

Fig.1.Alaskacoastlineshowingsiteswithhighestconcentrationsofparalyticshellfishtoxins(numberwithnounits;unitsaremg/100gshellfishmeat)byshellfishspecies.
The re gulator ylim itfo rparalyti cshe llfish toxins is80mg/100g.

Data sources: ADHHS-ES database, 1973–2008; http://www.epi.hss.state.ak.us/bulletins/catlist.jsp?cattype=Paralytic+Shellfish+Poisoning+(PSP)), Gessner et al. (1997),

RaLonde(2001).
136 A.J.Lewitusetal./HarmfulAlgae19(2012)133–159

Fig. 2. British Columbia coast line with sites of highest concentrations of paralytic shellfish toxins (number with no units; units are mg/100g shellfish meat) and

domoicacid(ppm).

Datasources:CanadianFoodInspectionAgencydata,www.inspection.gc.ca,Chiang(1988).

Conrad; Sommer and Meyer, 1937). Paralytic shellfish poisoning distribution in some locations. For example, the frequency and

hasbeenrecognizedasaserioushealthriskinCAsince1927when geographic distribution of associated shellfish closures in Puget

amajoroutbreakinamulti-countyregionnorthandsouthofSan Sound have increased in WA since monitoring first began in

Franciscoresultedin102illnessesandsixdeaths(Table1).From the 1940s and 1950s (Trainer et al., 2003) and PST-related

1927 through 1989, PSP related illnesses totaled 511 in CA, shellfishclosureshaveincreasedontheORcoastfromthe1980s

including32deaths(Priceetal.,1991).TheearliestreportedPSP (Oregon Department of Fish and Wildlife, ODFW data, http://

poisonings in WA and the only deaths in that state occurred in public.health.oregon.gov/HealthyEnvironments/Recreation/

1942whenoneadultandtwoNativeAmericanchildrendiedafter HarmfulAlgaeBlooms/Pages/index.aspx, Strutton and Tweddle,

eatingbutterclamsandbluemusselscollectedalongtheStraitof unpubl. data). Outbreaks have decreased in other locations (e.g.,

JuandeFuca(Quayle,1969;Table1).Threedeathsalsooccurred high PSP levelsin Drakes Bay, CAhave declined since the 1980s,

further north in Barkley Sound on the West Coast of Vancouver California Department of Public Health, CDPH data, http://

Island, BC (Fig. 2). Additional incidences in BC occurred in 1957 www.cdph.ca.gov/HealthInfo/environhealth/water/Pages/

with61casesbutnodeaths,1965withfourcasesandonedeath, Shellfish.aspx).

and1980withtwoillnessesandonedeath.The1965incidentis

especially significant because it was thefirst time that a human 2.2.1. Alaska

death occurred at the same time that shellfish toxicity was ParalyticshellfishtoxinsareapervasiveprobleminAK(Figs.1

measured,andabloomofthetoxicspecies,Alexandriumacatenella and7A).Personaluseandsubsistenceshellfishharvestsaccounted

(Whedon et Kofoid) Balech was recognized as the causative for 183 confirmedPST illnesses between 1973 and 2008 (Alaska

organism(PrakashandTaylor,1966;Quayle,1969).Morerecent DepartmentofHealthandHumanServices-EpidemiologySection,

eventsinWAinclude10illnessesin1978,fiveillnessesin1998, ADHHS-ES database, 1973–2008; http://www.epi.hss.state.ak.us/

and nine illnesses in 2000, all in Puget Sound (Erickson and bulletins/catlist.jsp?cattype=Paralytic+Shellfish+Poisoning+(PSP)),

Nishitani, 1985; Trainer et al., 2003; Moore et al., 2009). PSP withmorethanhalfoftheillnessesfromconsumptionofbutter

poisoningsinORcaused20illnessesandonedeathinCoosBayin clams that can retain the toxins for more than two years

1933 (Sommer and Meyer, 1935; Halstead, 1965). In Pacific (Shumway,1990).Bluemussels,cockles(Clinocardiumsp.Keen),

Mexico,thefirstdocumentedreportofhumanshellfishpoisoning razor clams, Pacific littleneck clams, and other unknown clams

dates only to 1976, with seven cases and two deaths (Saldate- causedtheremainingillnesses.Numbersofreportedillnessesmay

Castan˜eda et al., 1991). Between 1979 and 2008, 391 poisoning be underestimated by a factor of (cid:2)10–30, due to underreported

cases were recorded with 24 deaths along the Pacific coast of minorillnesses,inaccurateandincompleteincidentrecording,and

Mexico. Of these, 34 cases with five deaths were attributed to misdiagnosis (Gessner and Middaugh, 1995; Gessner and

Gymnodinium catenatum Graham, and 357 cases with 19 deaths McLaughlin, 2008). Rural harvesters are particularly at risk

wereattributedtoPyrodiniumbahamensevar.compressum(Bo¨hm) becausetheyunderestimatethepotentialofillnessbasedontrust

Steidinger,Tester&Taylor(Corte´s-AltamiranoandSierra-Beltra´n, of traditional local knowledge to determine when to consume

2008). shellfish,includinguseofunreliableenvironmentalcuessuchas

watercolor.Furthermore,Alaskanscontinuetousethemyththat

2.2. Trendsinprevalenceandimpacts PSTsoccuronlyinmonthsthatdonothavean‘‘r’’inthespelling;

i.e.,MaythroughAugust,whentherealityisthatPSTsandillnesses

OutbreaksofAlexandriumspp.,andassociatedshellfishtoxicity canoccuryear-round.

andhumanillnesseshavebeenapersistentproblemalongthewest TheimpactsofPSTsonpublichealthareunevenlydistributed

coastfordecades.Outbreaksmay beincreasinginfrequencyand acrosspopulations;e.g.,comparedtootherAlaskans,AKNatives
A.J.Lewitusetal./HarmfulAlgae19(2012)133–159 137

livingincoastalcommunitiesarenearly12timesmorelikelyto Theintensityandfrequencyofbloomsalsovaryamonggrowing

encounter PSTs by consuming untested, subsistence-harvested areas.BaynesSoundontheeastcoastofVancouverIslanddoesnot

shellfish(GessnerandSchloss,1996).Sharingsubsistenceharvest oftenexperienceAlexandriumblooms,andthehighestlevelofPST

is common practice among AK Natives and this practice can recorded there between 1994 and 2008 was 430mg/100g in

geographically expand the risk of illness far beyond a single Californiamussels(CanadianFoodInspectionAgencydata).Areas

community.Forexample,KingCove,ontheAleutianPeninsula,has suchasBarkleySoundonthewestcoastofVancouverIslandhave

aknownhistoryofPSTillnessesandfatalities,andshellfishfrom PSTeventsnearlyeveryyear.Thenorthandcentralcoastscanhave

thisregionareoftensharedwithNativeAmericansalongtheU.S. extensiveAlexandriumspp.blooms,andatleastonePSTeventhas

westcoastandinteriorAK(Wrightetal.,2008). been recorded along the mainland coast each year (Taylor and

ThehighestPSTlevelsmeasuredtodatefromvariousshellfish Harrison,2002).Paralyticshellfishtoxinactivityislesscommonin
species in AK a re s hown in Fig. 1. Th e hig hest l evel, 20 ,600mg/ theareas monito redont heHaida Gwai i(forme rl yna medQue en

100g shellfish meat, occurred in blue mussels from Kalsin Bay, CharlotteIslands).

Kodiak Island, in late May 1994, and resulted in 16 illnesses IllnessesduetoPSParerelativelyrareinBC,withnonereported

(Ostasz,2001).ElevatedPSTsinPrinceWilliamSoundarea rare since 2005 (Canadian Food Inspection Agency data). The low

eventbecausepopulationsofbutterclams,Pacificlittleneckclams, number of PSP illnesses may be attributed to the biotoxin

andsoftshelfclams(MyaarenariaLinnaeus)aredepresseddueto monitoring program, prompt and effective closures of harvest

the1964earthquake,commercialfisheryoverharvestingofrazor areas, and education of the public to the hazards of shellfish

clams,seaotter(EnhydralutrisLinnaeus)predation,andimpacts poisoning.Themajorityofrecordedillnesseshavebeenattributed

fromthe1989ExxonValdezoilspill(Baxter,1971;Rukuyamaetal., tobutterclams.Asnotedpreviously,theseclamscanretaintoxins

2000;Thomasetal.,2002).HighPSTlevels,upto7750mg/100g, forlongerthantwoyears(Quayle,1969;Kviteketal.,2008).Dueto

existalongthesouthernshorelineoftheAleutianPeninsula,while the likelihood of high levels of PST in butter clams, this species

the northern shoreline and the Bering Sea have lower levels remainsclosedforharvestinmostareasinBC.TheimpactsofPST
ran gingfrom 135to310 mg/ 100g based onS timpso n’ssur fclam closures on th e c ommerc ia l shel lfish ind ust ry a re diffic ul t to

(Mactromeris polynyma Stimpson) viscera (Hughes and Nelson, quantify. Anecdotally, the impacts are considered extensive.

1979). Commercial fisheries exist for Pacific littleneck clams in Harvest areas can be shut down for months at a time, resulting

KachemakBay,razorclamsinlowerCookInlet,andgeoduckclams insignificantlayoffsforstaffandharvesters,andmarketscanbe

insoutheasternAK,wheremonitoringoccursduringtheharvest lost.ButterclamsarethepreferredshellfishspeciesforFoodSocial

period.Thefollowingshellfishspecieshaveshownsomerecordof CeremonialharvestingforFirstNationspeopleonthenorthcoast,
PSTsab ove theregula torylimit of80m g/100 g:blue muss el,butt er but it can b e difficult to fi nd a reas tha t can b e o pen ed for their

clam, Stimpson’s surf clam, razor clam, Pacific littleneck clam, harvestbecausetheseclamsretaintoxinsforlongperiodsoftime.

geoduck clam, scallop species, cockle species, Pacific oyster,

Dungeness crab, Tanner crab (Chionoecetes bairdi Rathbin), and 2.2.3. Washington

snow crab (Chionoecetes opilio Fabricius), particularly in the In Washington (Fig. 3), PST-related closures of recreational

Aleutian area, Kodiak Island, and in the Southeast Alaska region shellfish harvesting have been imposed since an incident

at Juneau and Ketchikan (ADHHS-ES database). Historically, the in 1942 that led to three Native American fatalities on the

toxinappearstoconstituteapersistentthreattohumanhealth,in Strait of Juan de Fuca (Trainer et al., 2003; Table 1). The

particular because while commercially harvested and farmed Washington Department of Health (WDOH; http://www.doh.

products are tested, recreationally harvested shellfish are not wa.gov/CommunityandEnvironment/Shellfish/BiotoxinsIllness

tested. Prevention/Biotoxins.aspx)imposedaharvestingclosureatthat

Paralyticshellfishtoxinsalsohavebeenmeasuredinanumberof time forallbivalve speciesexcept razorclams from Dungeness

crab species, including Dungeness, Tanner, snow, hair (Erimacrus SpittothemouthoftheColumbiaRiverfrom1Aprilto31October.

isenbeckiiBrandt),andredking(ParalithodescamtschaticusTilesius) Thecoastalclosureisreissuedeveryyear,buttheStraitofJuande

crabs (ADHHS-ES database, 1973–2008). Dungeness and Tanner Fucaclosuresarenowregulatedbytoxinmonitoring(F.Cox,pers.

crabsharvestedintheKodiakandAleutian/BeringSeafisheriesmust comm.).Routinemonitoringfortoxinsincommercialshellfishin

bekilled,cleaned,and sectionedbefore beingshippedtomarket. watersnorthandwestofAdmiraltyInletandinWillapaBayand

Testing of Dungeness crabs in the southeast AK fishery was GraysHarborbeganin1957followingasevereoutbreakofPSPin

suspendedin1996afterfouryearsofnegativePSTtests. BC(NishitaniandChew,1988).WashingtonDepartmentofHealth

recordsindicatethatPSPclosuresoccurinthesecoastalbaysonan

2.2.2. BritishColumbia irregular(sporadic)basis.

In British Columbia, PSTs are the most prevalent biotoxins Inthe1950sand1960s,PSTsoccurredinthenorthernregionsof

affecting shellfish growing areas. The frequency and intensity of Puget Sound (e.g., Sequim and Discovery bays), extending

Alexandrium blooms vary from year to year, but blooms are southward during the 1970s and 1980s to the inner Sound

expectedeachyear.MonitoringforPSTsinBCbeganin1942,asdid (Quayle, 1969; Nishitani and Chew, 1988; Rensel, 1993; Trainer

the first formal closures (Quayle, 1969). In 1982, a PST level of et al., 2003;Trainer and Hickey, 2003;Cox et al., 2008). Priorto

30,000mg/100g was recorded in California mussels in Work 1978, illnesses due to PSP were not reported in Puget Sound

ChannelonthenorthernBCmainland(Chiang,1988;Fig.2).The includingHoodCanal,andWhidbey,CentralandSouthbasins,but

highestlevelofPSTrecordedsince1994was10,000mg/100gin widespread toxicity occurred in September 1978, beginning in

musselsatEllenPointonthenortheastcoastofVancouverIslandin WhidbeyBasinandspreadingasfarsouthasDesMoines(southof

April1994(Fig.2). Seattle)intheCentralBasin(NishitaniandChew,1988;Fig.7B).

In the south coast of BC, PST events usually occur during the Toxinlevelsinbaymussels(MytilustrossulusGould)wereashigh

months of April to October, but may occur throughout the year as30,360mg/100gshellfishmeat(Fig.3).TenpeoplereportedPSP

(TaylorandHarrison,2002;CanadianFoodInspectionAgencydata, symptomsaftereatingrecreationallyharvestedmusselsandpink

www.inspection.gc.ca). Bloom initiation rarely occurs in winter scallops(ChlamysrubidaHinds),butnodeathsoccurred.Thefirst

months. The last widespread closure due to PSTs along the BC shellfishharvestclosuresintheSouthBasinoccurredinOctober

coastline occurred in 2008 when most of the main commercial 1988whentoxinlevelsinPacificoystersreached2000mg(Trainer

growingareaswereclosedforaportionofthesummer. etal.,2003).Sincethen,repeatedclosureshaveoccurredinmost
138 A.J.Lewitusetal./HarmfulAlgae19(2012)133–159

Fig.3.Washingtoncoastlinewithsitesofhighestconcentrationsofparalyticshellfishtoxins(numberwithnounits;unitsaremg/100gshellfishmeat)anddomoicacid

(ppm).Othersitesmentionedinthetextarealsoshown.

Datasources:WDOH,http://www.doh.wa.gov/CommunityandEnvironment/Shellfish/BiotoxinsIllnessPrevention/Biotoxins.aspx,Traineretal.(2003).

years throughout the Puget Sound basins, except south Hood ThefrequencyanddurationofPST-relatedshellfishclosureson

Canal, but not always in the same time or place each year (Cox the OR coast increased from 1979 to 1996 (ODFW data, http://

etal.,2008). public.health.oregon.gov/HealthyEnvironments/Recreation/

Ceremonial,subsistence,andcommercialharvestsbyWAtribal HarmfulAlgaeBlooms/Pages/index.aspx, Strutton and Tweddle,

communities have been greatly impacted by PST-associated unpubl. data, Fig. 7C). Twice as many closures occurred from

shellfish closures. The Puyallup, Suquamish, and Jamestown 1990 to 1996 as in all previous years, and most of the recent

S’Klallam tribes have experienced severe economic losses from closureslastedmorethan50days.Inthe2000s,thetotalnumber

theircommercialgeoduckfisheries,basedonfrequentandlengthy of closures, considering the northern and southern coasts

seasonal harvest closures (Wekell and Trainer, 2002). Recalls of separately,was23, comparedwith15inthe1990sand 6inthe

geoduckrelatedtoPSTeventshavecostthetribesabout$30,000. 1980s.

CommercialharvestingofPacificoystersandDungenesscrabsby

the Jamestown S’Klallam Tribe, and of manila clams, Pacific 2.2.5. California

oysters,andbasketcockles(ClinocardiumnuttalliiConrad)bythe ParalyticshellfishpoisoningeventshaveoccurredalongtheCA

Lummi Nation have also been significantly affected. Subsistence coast(Fig.5)sincebeforewrittenrecordsweremaintained,with

andceremonialharvestingbytheJamestownS’KlallamTribehave ‘‘mussel poisoning’’ being recognized by coastal tribes (Meyer

beenimpactedbyPSTtoxicityofbutter,Pacificlittleneck,horse, et al., 1928). Paralytic shellfish toxin levels have been highly

and manila clams. Beach closures have also impacted Puyallup variableandunpredictableduringthedecadesthatmonitoringhas

tribalculturebyrestrictingtheuseofclamsforceremonialdinners beenconducted,ashasthebreadthofgeographicrangeinvolved

atweddingsandfunerals. (Price et al., 1991; Langlois, 2001). Despite the temporal and

geographic variability,in everyyearsince 1999,PSP toxinshave

2.2.4. Oregon beenobservedinDrakesBayalongtheMarinCountycoast,north

IrregularmonitoringofshellfishforsaxitoxinsbeganinORin ofSanFrancisco(CDPHdata).

1958afterhighlevelsofPSTswerereportedalongtheWAcoast In general, Alexandrium is absent or constitutes a minor

(NishitaniandChew,1988).Changesinmonitoringsites,shellfish component of the marine phytoplankton community along the

species monitored, and the possibility that blooms initiated CAcoast.Thisdinoflagellatehasbeenobservedinapproximately

offshore make it difficult to compare the early data with later 3500ofthe24,000phytoplanktonsamplescollectedbytheCDPH

values (Nishitani and Chew, 1988). More consistent monitoring monitoringprogramsince1993.Ithascomprisedlessthan10%of

(conductedsince1979bytheOregonDepartmentofAgriculture, thephytoplanktonassemblagein93%ofthesesamplesand55%of

ODA; http://oregon.gov/ODA/FSD/shellfish_status.shtml) at more the observations have been at <1% relative abundance (CDPH

siteshasimprovedthecoverageandhasledtofrequentclosures, data).VisiblebloomsofAlexandriumarerarelyseenalongtheCA

primarilyofrazorclamandmusselspeciesshellfisheries.Paralytic coast,withonlyonedocumentedvisibleeventinthepast19years.

shellfish toxins have severely impacted shellfish harvests at Amassive‘redtide’duetoAlexandriumcoveredDrakesBayfora

Clatsop Beach in northern OR (Fig. 4). The severity of a PST- briefperiodinJuly1991(Langlois,2001;G.Langlois,pers.comm.).

associated HAB outbreak varies annually between northern and The greatest frequency of Alexandrium observations has been

southernORcoastalareas.In1992,aPSTeventaffectedthecentral recordedalongtheMarinCountycoast,consistentwiththegeneral

andnortherncoast,butnotthesouthernbeaches,whilein2001 pattern of PST frequency, followed by sites along the San Luis

PSTaffectedonlythesouthernbeaches. Obispo County coast (Langlois, 2001; CDPH data). Each of these
A.J.Lewitusetal./HarmfulAlgae19(2012)133–159 139

Fig.4.Oregoncoastlinewithsitesofhighestconcentrationsofparalyticshellfishtoxins(numberwithnounits;unitsaremg/100gshellfishmeat)anddomoicacid(ppm).

Data sources: ODA data, http://oregon.gov/ODA/FSD/shellfish_status.shtml, ODFW data, http://public.health.oregon.gov/HealthyEnvironments/Recreation/

HarmfulAlgaeBlooms/Pages/index.aspx,M.Hunter(unpubl.data).

regionsexperiencesmorethantwicethefrequencyofAlexandrium contained Alexandrium cells, coinciding with an increase in PSP

observationsofanyothercoastalcounty.Therewasanapparent activityintheregion(seebelow).LowabundancesofA.catenella

increaseinAlexandriumalongtheSantaBarbaracoastbeginningin weredetectedinallseasons from a weeklymonitoringprogram

1999,withthegreatestnumberofobservationsoccurringin2006; conducted in a small harbor of Santa Monica Bay from 2006 to

15 of 52 phytoplankton samples (29%) collected at Goleta Pier 2009 using a quantitative PCR method (Garneau et al., 2011).

Fig.5.Californiacoastlinewithsitesofhighestconcentrationsofparalyticshellfishtoxins(numberwithnounits;unitsaremg/100gshellfishmeat)anddomoicacid(ppm).

Datasources:CDPHdata,http://www.cdph.ca.gov/HealthInfo/environhealth/water/Pages/Shellfish.aspx,Priceetal.(1991).
140 A.J.Lewitusetal./HarmfulAlgae19(2012)133–159

Highestabundancesofthedinoflagellatecoincidedwithlowbut shellfish toxin accumulations are associated with blooms of G.

measurableconcentrationsofPSTsintheplankton. catenatumandP.bahamensevar.compressum.Theformerspecies

DatafromtheCDPHbiotoxinmonitoringprogramshowthata hasbeenobservedfromtheupperGulfofCaliforniainthenorthto

majorperiodofPSPactivityextendedthroughthe1980sinto1991 Guerrero in the south, while P. bahamense var. compressum is

(Fig.7D).Thehighesttoxinlevelsdetectedinshellfishduringthis responsible for PSP outbreaks in the southern states of Pacific

timewere26,000mg/100ginrockscallopsfromSonomaCounty, Mexico(Ochoaetal.,2002).

associated with the last documented fatality in August 1980, The dinoflagellate, G. catenatum, was first described from the
16,000mg/ 100g in C alifo rnia mussels from M arin County (July central Gulf of Califo rni a coast at cell abun dances up to 1 06/l
1980), 14,000 m g/1 00g in C alifornia muss els fro m Hum boldt (Graham ,19 43) ,butthefir stdoc um ente dPSPevento ccur red near

County(September1989)and10,000mg/100ginCaliforniamussels themouthoftheGulfin1979whenthreehumandeathsandan

fromMarinCounty(July1991)(Priceetal.,1991;CDPHdata,Fig.5 extensivefishkilloccurred(Meeetal.,1986,Table1).Toxinlevels

and Table 1). Each of the subsequent 18 years has experienced duringthateventrangedfrom<20to7640mg/100ginthetropical

significantlevelsofPSTinshellfish,butthesehavebeenwellbelow rocky oyster (Ostrea iridescens Hanley), with cell densities up to
the1980sm axim aa ndh av ebeenre stric tedin geog raphi cran geand 6.6(cid:3) 106cell s/l(Mee etal.,19 86,Fig.6 ).Add ition alblooms ha ve

duration (CDPH data, Fig. 7D). During this latter period, the occurred inBahia Mazatla´n,Colima, Guerrero,and Oaxaca.Most

concentration of PSTs has exceeded 3000mg/100g only once in blooms occur between February and May when the water

CaliforniamusselsfromMarinCounty(inAugust1998). temperaturerangesbetween17and258C(ManriqueandMolina,

The majority of PSP activity has historically occurred in the 1997;Ga´rate-Liza´rragaetal.,2004,2006).

centralandnorthernportionsofCA(Priceetal.,1991;CDPHdata). Blooms of Gymnodinium species have impacted public health.

Despitethisgeneralpattern,overtheyearsalertlevelsofPSThave The number of humans affected varies in different reports.

beendetectedinshellfishfromeachofthecoastalcounties(CDPH Herna´ndez-Becerriletal.(2007)mentioned561intoxicationsand

data).Inrecentyears,anincreaseinPSPactivityhasbeensuggested 38fatalitiesfrom1970to2004relatedtoPSTsofGymnodinium.In

in some southern CA sites, most notably in commercial shellfish contrast, Corte´s-Altamirano and Sierra-Beltra´n (2008) recognized

growingareasinSantaBarbaraandSanDiegocounties.Sampling only34intoxicationsandfivedeaths.Nointoxicationsassociated

sites in Santa Barbara experienced alert levels of PST every year with Gymnodinium have been reported recently, which may be

between2005and2008,peakingin2006(744mg/100g).Priorto attributed to increased attention by Mexican health authorities.

this recent activityand a moderate event in 1998, there had not Periodic bans on harvesting cultured or wild shellfish have been

beenalertlevelsforthesetoxinsinthisregionsincethe1980s.The imposedbyhealthauthoritiesinMexicosince2004.Themajorityof

San Diego aquaculture site experienced PST concentrations in thoseclosureswereassociatedwiththepresenceofGymnodinium

excessofthefederalalertlevelforthefirsttimein2008.Thelast species (Federal Commission for the Protection against Sanitary

timethealertlevelwasexceededanywhereinSanDiegoCounty Risks, COFEPRIS; http://www.cofepris.gob.mx/AZ/Paginas/Marea%

wasduring1985inamusselsamplefromScrippsPier(LaJolla)and 20Roja/MareaRoja.aspx).

2006insideSanDiegoBay(G.Langlois,pers.comm.). ThreemajortoxicoutbreaksofP.bahamensevar.compressum

involvinghumanpoisoninghavebeendocumentedonthePacific

2.2.6. Mexico coast of Mexico (Herna´ndez-Becerril et al., 2007). In November

Paralytic shellfish poisoning is the most important toxic 1989 in the Gulf of Tehuantepec region, three persons died and

syndromerelatedtoHABsinMexico,andPSTsaretheonlytoxins 99 persons were poisoned as a consequence of a bloom that
associated with h um an fa ta lities (Fi g. 6 and Tab le 1 ). Pa ralytic rea ched a m axim um abund an ce of 1.7(cid:3)106c ell s/l (Fig. 6 and

Fig.6.Mexicancoastlinewithsitesofhighestconcentrationsofparalyticshellfishtoxins(numberwithnounits;unitsaremg/100gshellfishmeat)anddomoicacid(ppm).

Datasources:COFEPRISdata,http://www.cofepris.gob.mx/AZ/Paginas/Marea%20Roja/MareaRoja.aspx,Garcia-Mendozaetal.(2009),Meeetal.(1986),Saldate-Castan˜eda

etal.(1991).EventsdescribedinHerna´ndez-Becerriletal.(2007)andCorte´s-AltamiranoandSierra-Beltra´n(2008).