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ExposureRisks&HealthEffectsofDomoicAcidinMarineWildlife&
Humans
KathiLefebvreNorthwestFisheriesScienceCenter
h6p://www.nwfsc.noaa.gov/research/divisions/efs/warrnwest/
PrevalenceofAlgalToxinsinAlaskanMarineMammalsForaginginaChangingArcCcandSubarcCcEnvironment
HarmfulAlgae55(2016)
KathiA.Lefebvre1*,LoriQuakenbush2,ElizabethFrame1,3,KathyBurekHunMngton4,GaySheffield5,RaphaelaSMmmelmayr6,AnnaBryan2,PrestonKendrick1,HeatherZiel7,TraceyGoldstein8,Jonathan
A.Snyder9,TomGela67,FrancesGulland10,Bobe6eDickerson7,VerenaGill9,11
• NorthwestFisheriesScienceCenter• AlaskaDepartmentofFishandGame,ArcMcMarineMammalProgram• AlaskaVeterinaryPathologyServices(AVPS)• UniversityofAlaskaFairbanks,AlaskaSeaGrant,MarineAdvisoryProgram• NorthSlopeBoroughDepartmentofWildlifeManagement• MarineMammalLaboratory,AlaskaFisheriesScienceCenter,NOAA• OneHealthInsMtute,SchoolofVeterinaryMedicine,UniversityofCalifornia,Davis• U.S.FishandWildlifeService,MarineMammalsManagement• TheMarineMammalCenter• AlaskaNaMveOrganizaMons:Western&NorthernCoastalcommuniMes,AlaskaEskimo
WhalingCommission,NaMveVillagesofGambell&Savoonga,TribalgovernmentofSt.PaulIsland,whalingcaptainsandsubsistencehuntersofBarrow.
Table1:Listofspecies,collectionstatus,periodandlocations,andtotalnumberofmarinemammalssampled.
Species Collectionstatus
Collectionperiod
CollectionlocationsinAlaska
(AK)
Totalnumber
ofanimals
Humpback Stranded July2007toSept.2011
Kodiak,TheAKPeninsula,Southeast
8
Bowhead Harvested Spring&Fall2006to2011
Barrow 25
Beluga Stranded&Harvested
Sept.2005toOct.2012
CookInlet,HooperBay
15
HarborPorpoise
Stranded Aug.2008toJuly2011
CookInlet 5
NorthernFurSeal
Harvested&LiveCapture
2010 SaintGeorge&SaintPaulIslands
179
StellerSeaLion
Stranded May2004toMarch2013
GulfofAK 42
HarborSeal
Stranded May2008toAug.2012
GulfofAK,Egegik 9
RingedSeal
Harvested Nov.2006toNov.2012
Barrow,ChukchiSea,BeringSea
113
BeardedSeal
Harvested Oct.2007toJune2013
Barrow,ChukchiSea,BeringSea
55
SpottedSeal
Harvested&SnowUrine
Nov.2006toNov.11
Barrow,ChukchiSea,BeringSea
158
RibbonSeal
Harvested&SnowUrine
May2009toOct.2012
Barrow,ChukchiSea,BeringSea,
Yakutat
21
PacificWalrus
Harvested May&Junein2012&2013
SaintLawrenceIsland
82
NorthernSeaOtter
Stranded&LiveCapture
April2004toMay2011
GulfofAK 193
SummaryofOpportunisMcSamples(n=905)
• 905marinemammalswerecollectedbetween2004-2013andtestedforthepresenceofalgaltoxins.
• Algaltoxinswerepresentin
AlaskanmarinemammalsfromSEAlaskatotheArcMcOcean.
• ThedatarevealthatAKfoodwebscontainalgaltoxinsatlevelsthataredetectableintoppredators.
• Mostlevelswerelowand
healthimpactswerenotconfirmed.
!Table!1:!!Summary!of!the!number!of!domoic!acid2positive!individuals!from!13!species!of!Alaskan!marine!mammals,!including!the!sample!matrix!with!the!highest!concentration.!F!=!Feces,!SC!=!Stomach!Contents,!S!=!Serum,!IC!=!Intestinal!Contents,!U!=!Urine.!!
Species! Sample!number!
Number!positive!
%!!positive!
Max!conc.!(ng/g!or!ml)!
Sample!Matrix!
Cetaceans! ! ! ! ! !Humpback!whale! 8! 3! 38%! 51! F!Bowhead!whale! 25! 17! 68%! 359! F!Beluga!whale! 15! 2! 13%! 7! SC!Harbor!porpoise! 5! 2! 40%! 15! F!Otariids! ! ! ! ! !Northern!fur!seal! 179! 8! 5%! 13.8! S!Steller!sea!lion! 44! 12! 27%! 7! SC!Phocids! ! ! ! ! !Harbor!seal! 9! 6! 67%! 8! F!Ringed!seal! 113! 19! 17%! 127! F!Bearded!seal! 55! 14! 25%! 48! IC!Spotted!seal! 158! 5! 3%! 40! SC!Ribbon!seal! 21! 5! 24%! 7! F!Odobenids! ! ! ! ! !Pacific!walrus! 82! 34! 41%! 6,457! SC!Mustelids! ! ! ! ! !Northern!sea!otter! 172! 43! 25%! 162! U!! ! ! ! ! !
SEAFOODRegulatorylimit=20ugDA/gor20,000ng/g
Table&2:!!Summary!of!the!number!of!saxitoxin2positive!individuals!from!13!species!of!Alaskan!marine!mammals,!including!the!sample!matrix!with!the!highest!concentration.!F!=!Feces,!SC!=!Stomach!Contents,!IC!=!Intestinal!Contents,!U!=!Urine;!na!=!not!applicable.!
Species& Sample&number&
Number&positive&
%&&positive&
Max&conc.&(ng/g&or&ml)&
Sample&Matrix&
Cetaceans& ! ! ! ! !Humpback!whale! 8! 4! 50%! 62! F!Bowhead!whale! 25! 8! 32%! 63! F!Beluga!whale! 12! 1! 8%! 4! F!Harbor!porpoise! 5! 0! 0%! na! na!Otariids& ! ! ! ! !Northern!fur!seal! 179! 8! 5%! 42! F!Steller!sea!lion! 42! 4! 10%! 7! F!Phocids& ! ! ! ! !Harbor!seal! 8! 0! 0%! na! na!Ringed!seal! 110! 15! 14%! 172! F!Bearded!seal! 44! 6! 14%! 15! IC!Spotted!seal! 145! 1! 1%! 3! SC!Ribbon!seal! 7! 0! 0%! na! na!Odobenids& ! ! ! ! !Pacific!walrus! 82! 23! 28%! 240! IC!Mustelids& ! ! ! ! !Northern!sea!otter! 163! 37! 23%! 45! U!! ! ! ! ! !
SEAFOODRegulatorylimit=80ugSTX/100gor800ng/g
Exposurerisk,butwhatabouthealthimpactstomarinemammals?
Fecesrange:4to182,000ngDA/gUrinerange:0.6to253ngDA/ml
ClassicDomoicAcidToxicosis
CSL
Humpback
Bowhead
Beluga
Harbor P
orpoise
Northern
Fur
Steller
Sea Lion
Harbor S
eal
Ringed
Beard
ed
Spotted
Ribbon
Walrus
010203050
100150200
2520050200
Dom
oic
Aci
d C
once
ntra
tion
(ng/
g Fe
ces
or G
I con
tent
s)CSL
Harbor P
orpoise
Steller
Sea Lion
Harbor S
eal
Ringed
Beard
ed
Spotted
Ribbon
Sea O
tter
0.00.51.01.52.0
5203550
100200300
Species
Dom
oic
Aci
d C
once
ntra
tion
(ng/
ml U
rine)
A
B
Feces
Urine
Algaltoxinimpairssealionmemory&hippocampalconnecCvity,withimplicaConsfor
strandingsPeterF.Cook1,2,*,ColleenReichmuth2,AndrewA.Rouse2,LauraA.Libby3,SophieE.Dennison4,OwenT.
Carmichael5,KrisT.Kruse-Ellio64,JoshBloom4,BaljeetSingh3,VanessaA.Fravel6,LorraineBarbosa6,JimJ.Stuppino4,WilliamG.VanBonn7,FrancesM.D.Gulland6,CharanRanganath3
PeterCook&Ronan
EffectsofChronicLowLevelExposuretoDomoicAcid(NIH/NSFRO1)
UniversityofWashington
DonSmithYiZuoEmmaHiolski
UniversityofCalifornia,SantaCruz
DaveMarcinekPrestonKendrick
RegulatoryLimit=20ppm
BridgetFerriss
MicewereIPinjected1Xperweekwith0.6ppmdomoicacidfor25weeks(doseis30%ofEC50).
A`er6monthsofexposure,miceweretestedforlearning&memoryviaaRadialWaterMazetest(n=20control&20exposedmice).
RadialWaterMazeTesCngApparatus
SignificantLearningDeficitsinExposedMice!
6monthsofexposure
LearningImproveda`er9wkRecoveryPeriod!
9weekrecoveryperiod
0 1 2 3 4 5 12
20406080
100
Day (0 = First Trial Only)
% S
ucce
ss o
f thr
ee tr
ials
(m
ean ±
SEM
, n =
20)
ControlExposed
TestDay 5
TestDay 12
0 1 2 3 4 5 12
20406080
100
Day (0 = First Trial Only)
% S
ucce
ss o
f thr
ee tr
ials
(m
ean ±
SEM
, n =
10)
ControlExposed
TestDay 5
TestDay 12
0 1 2 3 4 5 12
20406080
100
Day (0 = First Trial Only)%
Suc
cess
of t
hree
tria
ls
(mea
n ±
SEM
, n =
10)
ControlExposed Test
Day 5 Test
Day 12
• Exposedonceaweekfor≈9months• 3to12monthsofage
• TestedatthreeoldageMmepoints;
• 18months(Earlyoldage)• 24months(Midoldage)• 28months(Oldoldage)
• Noexposurefor6,12,and16months
EarlyOldAge
MidOldAge
OldOldAge
DoeschronicexposureearlyinlifeimpactcogniCvedeclinewithage?
Organotypic Brain Slice Cultures Mouse
(A) Photomicrograph (x4 magnification; scale bar = 200 µm) of a representative brain slice culture (red staining = NeuN+ neurons). White box highlights the region covered by the 512-electrode array, and electrophysiologically identified neurons (circles) are overlaid. Green circles = hippocampal neurons; blue circles = cortical neurons
(excluded from analyses). (B) Mean (± SE) number of active hippocampal neurons in control (n=14) and domoic acid-exposed (n=15) brain slice cultures. * p < 0.05 (random effects ANOVA).
EmmaHiolski
#ofAcCveNeurons
ConnecCvityDensity
PercentInhibitoryNeurons
Electrophysiologicaleffectsofdomoicacidexposureontheneuralnetworksoforganotypicbrainslicecultures
Modelofdomoicacid-inducedchangesinorganotypicbrainslicecultures
• Lossofinhibitoryneuronswithchronicexposure• IncreasedconnecCvity&excitatoryenvironment
HealthImpactsofDomoicAcid
• Highexposures:seizures,death,spaMalmemory/learningdeficits(permanent)
• Lowexposures:SpaMalmemory/learningdeficits,hyperacMvity(reversible)
• PotenCalconsequences:
– DecreasednavigaMonalskills,strandingimpacts?– Increasedvulnerabilitytoshipstrikes,hunters,predaMon?– Compromisedforagingability,starvaMon?– CompromisedimmunefuncMon,vulnerabilitytoinfecMousdisease?
WARRN-West
WARRN-WestPartners
• NOAANorthwestandSouthwestFisheriesScienceCenters,
• AlaskaSeaLifeCenter,• CascadiaResearchCollecCve,• MarineMammalInsCtuteOregon
StateUniversity,• PortlandStateUniversity,• UniversityofWashington,• UniversityofAlaskaFairbanks,• UniversityofCaliforniaDavisOne
HealthInsCtute.
• NOAAWestCoast&AlaskaMarineMammalStrandingNetworks&OfficeofProtectedResources,
• NorthSlopeBoroughDepartmentofWildlife,• AlaskaDepartmentofFishandGame,• TheMarineMammalCenter,• WashingtonStateDepartmentofFishandWildlife,• AlaskaSeaGrant,• TheWhaleMuseumofFridayHarbor,• USGSNaConalWildlifeHealthCenter,• AlaskaUSFishandWildlifeService,• AlaskaVeterinaryPathologyService.
FundingprovidedbyNOAAFisheries,WARRN-WestPartners,NorthPacificResearchBoard,NIHandNSF
ALASKANATIVECOMMUNITIES