REYKJAVÍK SEPTEMBER 2020 Burrowing behaviour in ocean quahog (Arctica islandica) in situ and in the laboratory HAF-OG VATNARANNSÓKNIR MARINE AND FRESHWATER RESEARCH IN ICELAND

Abstract

REYKJAVÍK SEPTEMBER 2020Burrowing behaviour in ocean quahog (Arctica islandica) in situ and in the laboratory

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REYKJAVÍK SEPTEMBER 2020
Burrowing behaviour in ocean quahog (
Arctica islandica
) in
situ and in the laboratory
Stefán Ragnarsson og Guðrún G. Þórarinsdóttir
HAF- OG VATNARANNSÓKNIR
MARINE AND FRESHWATER RESEARCH IN ICELAND
HV 2020-43
ISSN 2298-9137



Burrowing behaviour in ocean quahog
(
Arctica islandica
) in situ and in the laboratory
Stefán Ragnarsson og Guðrún G. Þórarinsdóttir

Haf‐ogvatnarannsóknir
MarineandFreshwaterResearchinIceland
 
Upplýsingablað

Titill:Burrowingbehaviourinoceanquahog(Arcticaislandica)insituandinthelaboratory
Höfundar:StefánRagnarssonogGuðrúnG.Þórarinsdóttir
Skýrslanr.
HV2020‐043
Verkefnisstjóri:
StefánRagnarsson
Verknúmer:
11515
ISSN
2298‐9137
Fjöldisíðna:
20
Útgáfudagur:
28.september2020
Unniðfyrir:
Hafrannsóknastofnun
Dreifing:
Opin
Yfirfariðaf:
KlaraJakobsdóttir
Ágrip
Íþessarrirannsóknvoruárstíðabundnarsveiflurílóðréttrihreyfingukúfskelja(Arctica
islandica)íbotnsetiogskelstærðkönnuðíEyjafirðisemogírannsóknarstofu.Niðurstöður
sýnduaðskeljarvorugrafnardýpraísetiyfirveturensumar,semvæntanlegaskýristaf
minnafæðuframboðioglægrahitastigiáþeimárstíma.Íljósiþessavarathyglisverthversu
skeljarvorudjúptgrafnarísetiíseptember2003.Daganafyrirsýnatökuvarmjöghvasstsem
gætihafaorsakaðmiklahreyfinguábotnsetinuogorðiðtilþessaðskeljrnargrófusigniður
íleitaðskjóli.Tölfræðilegurmunurvarámeðaldýpiskeljaísetiíjúníbæðirannsóknarárin
semerfitteraðskýra.Marktækfylgnifannstámilliskellengdarogdýpisínokkrumsýnatöku
mánuðum.Íathugunumsemfóruframárannsóknarstofufannstekkertsamræmiámilli
einstakingaísetdýpi.Þaðerljóstaðskeljarsemvorumeðþykkavírinnáttuerfittmeðað
grafasigniður.

Abstract
Thisstudyexaminedtheseasonalvariationinburialbehaviourandshelllengthofocean
quahogs(Arcticaislandica)inEyjafjörðurandduringdirectobservationsinlaboratory.The
buryingbehaviourofoceanquahogswasstronglyseasonal,withclamsburrowingmore
deeplyduringwintercomparedtosummer,mostlikelyduetoreducedfoodavailabilityand
lowerseawatertemperatures.Itwasofinteresthowdeeplyburrowedtheclamswerein
September2003,giventhatbothfoodsupplyandtemperatureshouldhavebeenfavourable
atthattimeofyear.Itislikelythatthehighwindspeedsthedayspriortosamplingcaused
sedimentdisturbancesthatinducedoceanquahogstoburrow.Therewerealsodifferences
inburialdepthsinJuneinbothyearsinvestigatedwhicharedifficulttoexplain.Significant

relationshipswerefoundintheburrowingdepthandshelllengthforseveralsampling
months.Inthelaboratorystudy,noclearsynchronyinburrowingbehaviourwasfound
amongindividuals.Itwasclearthatthoseclamsfittedwiththethickwirehadproblems
burrowing.

Keywords:Arcticaislandica,oceanquahog,burrowing,shelllength
Undirskriftverkefnisstjóra:


Undirskriftforstöðumannssviðs:



i

Efnisyfirlit         Bls.

Introduction.................................................................................................................1
Materialandmethods.................................................................................................3
Fieldstudy.................................................................................................................3
Laboratorystudy.......................................................................................................5
Statisticalanalysis.....................................................................................................7
1.Temporaltrendsinburyingactivityofoceanquahogs.........................................7
1.1.Environmentalvariables..................................................................................7
1.2.Burialdepth.....................................................................................................9
1.3.Shelllength....................................................................................................11
1.4.Burialdepthandshelllength........................................................................12
2.Laboratorystudy.................................................................................................13
2.1.Mortalityratesandburrowingactivity..........................................................13
Discussion..................................................................................................................15
Acknowledgements...................................................................................................18
References.................................................................................................................18


Tables
Table1.Numberofoceanquahogs,survivalandmortalityrate,burialbehaviour,anddepth
inthecontrolsandwithclamsfittedwiththin(1.6mm)andthick(3mm)wire24,48and72
h.
Tafla1.Fjöldikúfskelja,yfirlifunogdánartíðni,hreyfingíbotnsetiogdýpihjá
viðmiðunarhópi,skelmeðþunnan(1,6mm)ogþykkan(3mm)vírárannsóknartímabilinueftir
24,48og72kls.


Figures
Figure1.Siphonopeningsofoceanquahogs(A.islandica)insandybottom.(Photo/Ljósm.
StefánRagnarsson).
1.mynd.Inn‐ogútstreymisopkúfskelja(A.islandica)ísandbotni.
Figure2.SamplingsiteinEyjafjördur,NorthIceland.
2.mynd.RannsóknarsvæðiðíEyjafirði,norðurland.
Figure3.Samplingofoceanquahogswithinarectangleof1m2.Therightphotoshowsthe
siphonopenings.(Photo/Ljósm.KarlGunnarsson).
3.mynd.Einsfermetrarammitilafmörkunarsýnatökusvæðis.Tilhægrisjástinn‐og
útstreymisopkúfskeljainnanrammans.

ii
Figure4.Oceanquahogs(A.islandica)withwireexposedwhilegluewasdrying.
(Photo/Ljósm.StefánRagnarsson).
4.mynd.Kúfskeljar(A.islandica)meðvíráþurruámeðanlímiðþornar.
Figure5.Oceanquahogs(A.islandica)withandwithoutwirelocatedinthetankatday1(a)
andday2(b).Aclamwithawirestartingburrowinginthesediment(c)andburieddeeply
(d).(Photo/Ljósm.StefánRagnarsson).
5.mynd.Kúfskeljar(A.islandica)meðogánvírsítankiádegi1(a)ogdegi2(b).Skelað
grafasigniður(c)skellangtniðurgrafiníbotnlagiðogaðeinshlutivírssjáanlegur(d).
Figure6.Anoceanquahog(A.islandica)fittedwithwirestartingburrowingintothe
sediment.(Photo/Ljósm.StefánRagnarsson).
6.mynd.Kúfskel(A.islandica)meðvíraðgrafasigniðuríbotnlagið.
Figure7.ReconstructedseawatertemperatureinHjalteyri.Thetemperaturedatawere
reconstructedduetomissingdatabyusingthemeandifferencesintheseawater
temperatureinthenearbylocatedGrímseyislandbetween2000and2006(forwhichthere
wasacompletetemperaturerecord)andHjalteyri.Thedatesonthex‐axisshowthe
samplingoccasions.
7.mynd.Endurgerður(reconstructed)sjávarhitiviðHjalteyri.Hitagögninvoruendurgerð,þar
semgögnvantaði,meðþvíaðnotameðalmuníhitaviðGrímsey(2000‐2006)ogHjalteyri.
Söfnunardagarerusýndiráx‐ás.
Figure8.a)Maximumsustainedwindspeed(m/sec)for10minperiodinHjalteyri(May
2003‐July2004).Thedatesonthex‐axisshowthesamplingoccasions.
8.mynd.Mesti10mínútnameðalvindraði(m/sek)áHjalteyri(maí2003‐júlí2004).
Söfnunardagarerusýndiráx‐ás.
Figure9.BoxplotshowingmeanburialdepthsofoceanquahoginJuneandSeptember2003
andFebruaryandJune2004.Theboxrepresents25‐75%quantiles,thewhiskersthe1.5*
interquantilerangesandthedotstheoutliers.
9.mynd.Kassaritsemsýnirmeðaldýpikúfskeljaísandbotnifebrúar2004,júníbæðiárinog
september2003.Kassinnsýnir25‐75%hlutfallsmörk,skeggineinaoghálfakassalengdog
punktarnirútgildi.
Figure10.FrequencydistributionofoceanquahogburialdepthsinJune(J03)andSeptember
2003(S03)andFebruary(F04)andJune2004(J04).Notethedifferencesinthescaleofthe
y‐axisbetweensamplingmonths.
10.mynd.Dýpikúfskeljaísandbotniíjúní(J03)ogseptember2003(S03),ogfebrúar(F04)og
júní2004(J04).Athugiðmismunandiskalaáy‐ás
Figure11.Boxplotofmeans,25‐75%quantiles(box)and1.5*interquantileranges
(whiskers)ofoceanquahoglengthsinJuneandSeptember2003andFebruaryandJune
2004.Theboxrepresents25‐75%quantiles,thewhiskersthe1.5*interquantilerangesand
thedotstheoutliers.
11.mynd.Kassaritsemsýnirmeðallengdkúfskeljaísandbotnifebrúar2004,júníbæðiárin
ogseptember2003.Kassinnsýnir25‐75%hlutfallsmörk,skeggineinaoghálfakassalengdog
punktarnirútgildi.
Figure12.Relationships(LOESS;locallyweightedsmoothing)betweenburialdepthandshell
lengthofoceanquahogsinJuneandSeptember2003andFebruaryandJune2004.
12.mynd.Samband(LOESS)dýpisskeljaíbotniogskellengdaríjúníogseptember2003og
febrúarogjúní2004.

iii

Figure13.Oceanquahogswithoutawirestartingburrowingintothesediment.Thefootis
clearlyvisible.(Photo/Ljósm.StefánRagnarsson).
13.mynd.Kúfskeljaránvírsaðgrafasigniðuríbotnlagið.Fóturinnséstgreinilega.
Figure14.Sedimentburialdepthoffiveoceanquahogsfittedwiththinwireafter24,48and
72hours.
14.mynd.Lóðrétthreyfingfimmkúfskeljaísetimeðgrannanvíreftir24,48og72
klukkustundir.


1
Introduction
Thefactorsthatgoverntheburrowingbehaviourofinfaunalbivalvesarepoorly
understood.Infaunalbivalvesthatareburrowedatthesediment‐waterinterfaceare
indirectcontactwiththeoverlayingseawatertotakeupoxygenandfilterfood.
Manyinfaunalbivalvespeciescanburydeeperintothesedimentstoescapeadverse
conditionsandsurvivewithoutoxygenbymeansofanerobicrespiration,oftenfora
considerableduration.Thisphysiologicaladaptionenablesthemtolower
considerablytheirenergycosts(Taylor1976,Oeschger1990).Whilemostinfaunal
bivalvescanundergoshort‐termanaerobiosis,especiallyintheintertidalzone(de
Zwaan1977,Siebenaller1979,Holwerdaetal.1983,Sicketal.1983,Fieldsand
Storey1987,Tallqvist2001),relativelyfewspeciescanremainburiedandrespire
anaerobicallyforseveralmonths(Oeschger1990).Thefactorsthathavebeen
suggestedtoinfluenceburrowingactivityincludereducedfoodsupply(Edelaar
2000),lowsalinity(Haideretal.2018),lowtemperature(JohnandFernandez1989,
Davisetal.1999),highpredatoroccurrence(Tallqvist2001,Edelaar2000,Griffith
andRichardson2006,ZwartsandWanink1989),increasedstormintensity(Poseyet
al.1996),presenceofalgalmats,driftingalgaeandtidallytransportedsandinducing
hypoxicconditions(Nashimotoetal.1986,NorkkoandBonsdorff1996)anddredge
inducedstress(Chicharoetal.2003).
Theoceanquahog(A.islandica),iscommonlyfoundinpartsoftheN‐Atlantic,
sometimesinveryhighdensities.Itpossessesshortpairedinhalantandexhalant
siphons.Duringfeedingactivity,itispositionedatthesediment‐waterinterfaceand
thesiphonopeningscanbevisibleonthesedimentsurfaceascylindricalholes.The
diameteroftheholesmadebytheinhalantsiphonisalwaysslightlylargerthanthat
oftheexhalantone(Fig.1).



2



Figure1.Siphonopeningsofoceanquahogs(A.islandica)insandybottom.Photo/Ljósm.:StefánRagnarsson.
1.mynd.Inn‐ogútstreymisopkúfskelja(A.islandica)ísandbotni.

Theoceanquahogisanexampleofaspeciesthatiscapableoflonger‐term
anaerobiosiswhereit“hibernates”foralongtimedeeplyburrowed.Whiletheexact
environmentalstimulitotriggerthisbehaviourispoorlyknown,itisclearlya
responsetoadverseenvironmentalconditions(Taylor1976).Oceanquahogs
appearstobemoreresistanttooxygendeficiencyandcansurvivelongerthanmany
otherinfaunalbivalvespeciessuchasAbraalba(WeigeltandRumohr1986)and
Cerastodermaedule(Theedeetal.1969).Predationhasbeensuggestedtobea
majorburrowingelicitorinbivalves(GriffithandRichardson,2006).Weigeltand
Rumohr(1986)showedthatjuvenileoceanquahogisanimportantfoodresourcefor
benthicandpelagicfish.Adultsarebelievedtobelessaccessibleforpredationdue
tolargersize,thickershellsandgreaterburrowingdepth(ArntzandWeber1970).
However,Thorarinsdóttiretal.(2009)showedhowdislodgedclamsofdifferentsize
range,lyingonthesedimentsurfacebecameaneasypreyforopportunistic
invertebrateandfishpredators.Manyofthesevalvespartiallyopen,giving
predatorseasieraccesstoitssoftparts.
Theenvironmentaleffectsofshellfishdredginghavebeenwelldocumentedfor
manybivalvespecies(e.g.Chicharoetal.2003,Ragnarssonetal.2015).InIceland,
commercialfishingforoceanquahogswithhydraulicdredgestookplace

3
intermittentlybetween1987and2009(Hafrannsóknastofnun2019).Thedredge
penetratesthesedimentasmuchas10cm(Thorarinsdóttiretal.2002).Thefishing
efficiencycanbeashighas92%forshellsthatare107.5mmorlonger
(Thorarinsdottiretal.,2010).Someclamsarenotcaughtbythedredgeandremain
inthetrackoraredisplacedoutofit(Thorarinsdottiretal.2009).Thesurvivalof
theseclamsislikelytodependuponpredatordensity,thedegreeofshelldamage
andtheirabilityofself‐repairandtoreburrow.Ragnarssonetal.(2015)estimated
thatoutoftheoriginaloceanquahogbiomassbeforefishingtookplace,thedredge
captured82%whilethe18%oftheremainingbiomassrepresentedclamsthatwere
eitherdisplacedoutofthetrackorremainedwithinthetracks.
Furthermore,dredgingcaninducestresstotheclams,affectingboththeir
behaviouralandphysiologicalresponsesandcanincreasetheburrowingtimein
bivalves(Chicharoetal.2003).
Theobjectiveofthisstudywastoinvestigatetheburrowingbehaviourofocean
quahogsundernaturalconditionsatdifferenttimesoftheyearandinthelaboratory
at7°Cwatertemperature.Undernaturalconditionsweinvestigatedwhetherthe
burrowingactivitywasseasonaland/orfunctionofbodysize.Underlaboratory
settings,theburrowingactivityofclamswasmonitoredoveradurationof74hours.

Materialandmethods
Fieldstudy
Thestudywasconductedonasandybottomat10mdepthinEyjafjörður,North
Iceland(65°47.8'N,18°3.8'W)withhighdensitiesofoceanquahogs(Fig.2).
Samplingtookplaceon5thJuneand30thSeptember2003and11thFebruaryand30th
June2004.Theseawatertemperatureandthephytoplanktonconcentrationwere
notmeasuredatthestudysitebutthemeanmonthlyseatemperatureinEyjafjördur
between1987‐2000was7.5°C,8°Cand1.5°CinJune,SeptemberandFebruary,
respectively(Jónsson2004).Thephytoplanktonconcentrationfromnearlocalityin
June,andFebruarywere0.9and0.03mgchl/m3respectively(Kaasaand
Gudmundsson1994).


4

Figure2.SamplingsiteinEyjafjördur,NorthIceland.
2.mynd.RannsóknarsvæðiðíEyjafirði,norðurland.


Ateachsamplingdate,diverscollectedallclams>8mmSLwithintwo1m2frames
thatwererandomlylaidontheseafloordowntothesedimentdepthof20cm,using
anunderwatersuctionsampler(Fig.3).Whentheburrowopeningswerevisibleon
theseafloortheburrowingdepthwasconsideredzero.Forclamsthatdidnothave
visiblesiphonopenings,thedepthofburial(thedistancebetweenthesediment
surfacetotheclamedge)wasmeasuredwitharulertothenearest0.5cm.Allclams
sampledfromthesediment(110,93,65and130inJuneandSeptember2003and
FebruaryandJune2004respectively)wereenumeratedandtakentothelaboratory
wheretheshelllengthwasmeasuredwithverniercalliperstothenearest0.1cmand
weighted.


 
Figure3.Samplingofoceanquahogswithinarectangleof1m2.Therightphotoshowsthesiphonopenings.
Photo/Ljósm.:KarlGunnarsson.
3.mynd.Einsfermetrarammitilafmörkunarsýnatökusvæðis.Tilhægrisjástinn‐ogútstreymisopkúfskeljainnan
rammans.

5
Laboratorystudy
Oceanquahogswerecollectedwithadrydredgefrom20mdepthinFaxaflóiBay,
SW‐Iceland,inMarch2004.Theclamsweretransportedimmediatelytothe
mariculturelaboratorylocatedcloseby,7kmwestofGrindavík,inwhichmanytypes
ofexperimentsinvolvingcultureofmarinefishandechinodermshavebeencarried
out(https://www.hafogvatn.is/en/about/branches/grindavik).Seventyclams(60‐80
mmshelllength)weretransportedfromthefishinggroundtothelaboratoryin
Grindavík.Theexperimentalsetupconsistedofa500ltankwithrunningseawater
pumpedfrom50mdepthwithaconstanttemperatureof7°Cand30pptsalinity.
Thetankhad30cmlayeroffinesand.Fulllightwasinthelaboratorythroughoutthe
experiment.
Inthelaboratory,atotalof36oceanquahogswereusedfortheexperiment.Apiece
ofthingalvanizedwireoftwodifferentdiameters(1.6and3mm)and20cmlong,
wasattachedtoeachshellnexttothesiphon‐openingsusinganepoxyadhesive
(Reefconstruct,Aquamedic,Bissendorf,Germany).Thewireprotrudedabovethe
sedimentsurface,enablingdirectmeasurementoftheburrowingdepth.Fourteen
clamswithoutawire(controlgroup),werekeptinseawaterandplacedinthe
laboratorytankimmediatelyuponarrival.Eightindividualswithathinwire(1.6mm)
and14withthickwire(3mm)wereexposedwhiletheepoxygluewasdrying,for3
and1hourrespectively(Fig.4).


Figure4.Oceanquahogs(A.islandica)withwireexposedwhilegluewasdrying.
Photo/Ljósm.:StefánRagnarsson.
4.mynd.Kúfskeljar(A.islandica)meðvíráþurruámeðanlímiðþornar.



6
Photographsweretakentolocatetheanimalsinthetankatthestartandthrough
theexperiment(Fig.5).Dailyobservationsweremadefor3days.Forshellsfitted
withwire,theburialbehaviouranddepthwererecorded.Theburialdepthwas
determinedbymeasuringthelengthofwireprotrudingabovethesedimentsurface
(Fig.5d).Buryingactivitywasconsideredtohaveinitiatedwhentheclamhadlifted
itselftoanuprightpositionandshowingclearsignittobeburrowingintosediments
(Fig.6).Thetotalburrowingtimewasrecordedastheinstanttheshellissupported
verticalbythefoottoacompleteburialbelowthesurfaceofthesubstratum
(Stanley1970).




Figure5.Oceanquahogs(A.islandica)withandwithoutwirelocatedinthetankatday1(a)andday2(b).Aclam
withawirestartingburrowinginthesediment(c)andburieddeeply(d).Photo/Ljósm.:StefánRagnarsson.
5.mynd.Kúfskeljar(A.islandica)meðogánvírsítankiádegi1(a)ogdegi2(b).Skelaðgrafasigniður(c)skel
langtniðurgrafiníbotnlagiðogaðeinshlutivírssjáanlegur(d).


a b
c d

7

Figure6.Anoceanquahog(A.islandica)fittedwithwirestartingburrowingintothesediment.
Photo/Ljósm.:StefánRagnarsson.
6.mynd.Kúfskel(A.islandica)meðvíraðgrafasigniðuríbotnlagið.


Statisticalanalysis
Testsonmeanburialdepthsandonmeanlengthsoftheclamsbetweensampling
monthsweremadewithone‐wayANOVAonlog‐transformeddata.Forsignificant
tests,subsequentTukeymultiplecomparisontestswerecarriedouttoidentifythose
meansthatdifferedsignificantly.Two‐sampleKolmogorov‐Smirnov(k‐s)testswere
usedtotestfordifferencesintheclamburialdepthfrequencydistributions.

Results
1.Temporaltrendsinburyingactivityofoceanquahogs
1.1.Environmentalvariables
ThetrendsinreconstructedsurfaceseawatertemperaturesinHjalteyriisshownin
Fig.7.Theestimatedseawatertemperaturesatthetimesofsamplingwere8.2°C(5th
ofJune2003),9.1°C(30thofSeptember2003),2.6°C(12thofFebruary2004)and
11.4°C(30thofJune2004).DataonwindspeedsbetweenMay2003andJuly2004

8
wereobtainedfromthemeteorologicalofficefortheAkureyriweatherstation.The
metricforwindspeedused(maximumwindssustainedfor10minutesinm/sec)
decreasedfromMay2003onwardsbutroseintheautumnof2003andremained
highoverwinteruntildecreasinginsummer2004(Fig.8).Highestwindspeedsduring
thestudyperiodwereobservedinendofSeptember2003,precedingthesampling
onthe30thofSeptember.Between20thand22ndofSeptember,theaverage
windspeedssustainedfor10minuteswereover10m/secperdaywhiletherewere
individualobservationswithwindspeedsbetween20–30m/secandasinglegust
over31m/sec.Thedaybeforesampling(Septemberthe29th),therewerethree
instanceswhenthewindspeedsexceeded15m/sec.




Figure7.ReconstructedseawatertemperatureinHjalteyri.Thetemperaturedatawerereconstructeddueto
missingdatabyusingthemeandifferencesintheseawatertemperatureinthenearbylocatedGrímseyisland
between2000and2006(forwhichtherewasacompletetemperaturerecord)andHjalteyri.Thedatesonthex‐
axisshowthesamplingoccasions.
7.mynd.Endurgerður(reconstructed)sjávarhitiviðHjalteyri.Hitagögninvoruendurgerð,þarsemgögnvantaði,
meðþvíaðnotameðalmuníhitaviðGrímsey(2000‐2006)ogHjalteyri.Söfnunardagarerusýndiráx‐ás.






9

Figure8.Maximumsustainedwindspeed(m/sec)for10minperiodinHjalteyri(May2003‐July2004).Thedates
onthex‐axisshowthesamplingoccasions.
8.mynd.Mesti10mínútnameðalvindraði(m/sek)áHjalteyri(maí2003‐júlí2004).Söfnunardagarerusýndirá
x‐ás.



1.2.Burialdepth
Themeanburialdepthsofclamsdifferedsignificantlyamongsamplingmonths(one‐
wayANOVA,F=217,P<0.0001),(Fig.9).Themeanburialdepthwasgreatestin
February(mean=8.5cm,SD=1.7,range4‐12cm),followedbySeptember2003
(mean=8.0cm,S.D=2.8,range2‐15cm)andlowestinthetwoJunesampling
occasions(2003;mean=2.4,SD=2.2,range=0‐10;2004;mean=3.2,SD=1.3,range=0‐
6.5).TheresultsfromtheTukeymultiplecomparisontestsshowthattheonlynon‐
significantdifferenceinthemeanburialdepthsbetweensamplingoccasionswas
betweenSeptember2003andFebruary2004(Padj.0.46).Itwasofinterestthatthe
burialdepthsinJune2004weresignificantlygreatercomparedtoJunetheprevious
year(Tukeymultiplecomparisontest(padj=0.008).Thedifferencesinmeans
betweenallothersamplingoccasionswerehighlysignificant(padj<0.0001).


10

Figure9.BoxplotshowingmeanburialdepthsofoceanquahoginJuneandSeptember2003andFebruaryand
June2004.Theboxrepresents25‐75%quantiles,thewhiskersthe1.5*interquantilerangesandthedotsthe
outliers.
9.mynd.Kassaritsemsýnirmeðaldýpikúfskeljaísandbotnifebrúar2004,júníbæðiárinogseptember2003.
Kassinnsýnir25‐75%hlutfallsmörk,skeggineinaoghálfakassalengdogpunktarnirútgildi.

Theproportionofclamsburiedbelow7cmdepthwas79%inFebruaryand53%in
Septemberbutwasalmostclosetozeroduringsummermonths(2%and0%inthe
twoJunesamplings,respectively)(Fig.10).Theshapeoftheclamburialdepth
frequencydistributionsdifferedsignificantlybetweenthefollowingsamplingmonths
whenindividuallytestedinapairwisefashionwithatwo‐sampleKolmogorov‐
Smirnov(k‐s)tests;J03vsS03(D=0.27,p=0.001),J03vsJ04(D=0.28,p<0.001),S03vs
F04(D=0.38,p<0.001)andF04vsJ04(D=0.36,P<0.001).Nosignificantdifferences
werefoundbetweenJ03vsF04,J03vsF04andS03vsJ04).



11


Figure10.FrequencydistributionofoceanquahogburialdepthsinJune(J03)andSeptember2003(S03)and
February(F04)andJune2004(J04).Notethedifferencesinthescaleofthey‐axisbetweensamplingmonths.
10.mynd.Dýpikúfskeljaísandbotniíjúní(J03)ogseptember2003(S03),ogfebrúar(F04)ogjúní2004(J04).
Athugiðmismunandiskalaáy‐ás


1.3.Shelllength
Theshelllengthdifferedsignificantlybetweensamplingmonths(one‐wayANOVA,
F=13,P<0.0001).TheoutputsfromtheTukeymultiplecomparisontestsrevealed
thatthemeanlengthsdifferedsignificantlyinallpairwisecomparisonofsampling
months,exceptbetweenFebruary2004andJune2003andbetweenJune2004and
September2003.Asanexample,themeanclamlengthinFebruary2004(78.0,
SD=18mm)wassignificantlygreatercomparedtoSeptember2003(58.0mm,
SD=25.6mm)(P=0.001)andJune2004(57.5mm,SD=26.7mmand(P<0.0001),
(Fig.11).


12

Figure11.Boxplotofmeans,25‐75%quantiles(box)and1.5*interquantileranges(whiskers)ofoceanquahog
lengthsinJuneandSeptember2003andFebruaryandJune2004.Theboxrepresents25‐75%quantiles,the
whiskersthe1.5*interquantilerangesandthedotstheoutliers.
11.mynd.Kassaritsemsýnirmeðallengdkúfskeljaísandbotnifebrúar2004,júníbæðiárinogseptember2003.
Kassinnsýnir25‐75%hlutfallsmörk,skeggineinaoghálfakassalengdogpunktarnirútgildi.


1.4.Burialdepthandshelllength
Therelationshipsbetweenburialdepthandshelllengthforeachsamplingmonthis
showninFig.12.ThenonparametricLOESSregressionwasusedtofitasmooth
curvethroughthesamplingpoints.Significantlinearregressions(usinglog‐
transformeddata)werefoundbetweenburrowdepthandshelllengthforJune2003
(p=0.0024)September2003(p=0.012)andJune2004(p=0.0008)butnotinFebruary
2004(p=0.46).




13


Figure12.Relationships(LOESS;locallyweightedsmoothing)betweenburialdepthandshelllengthofocean
quahogsinJuneandSeptember2003andFebruaryandJune2004.
12.mynd.Samband(LOESS)dýpisskeljaíbotniogskellengdaríjúníogseptember2003ogfebrúarogjúní2004.


2.Laboratorystudy
2.1.Mortalityratesandburrowingactivity
Themortalityofclamsafter72hourswaslowestforshellsincontrols(nowire)or
29%butwas60%and38%forshellswiththickandthinwire,respectively.Mostof
themortalityoccurredwithin24hrs(Table1).Theshellsinthecontrolgroup(n=10)
displayedvarietyinburrowingbehaviouroverthecourseofthestudy.Thefirstclam
tostartburrowingbelongedtothecontrolgroup,initiating30minutesafter
placementinthetank(Fig.13).Fiveoftheclamsinthecontrolswerefullyburied
after24hours(nosiphonopeningsvisible)whiletheremainingfiveremainedonthe
sedimentsurface(Table1).At48and72hours,noclamsinthecontrolswerelying
onthesedimentsurface,butwereeitherhalf‐buried,buriedjustbelowthesediment
surface(siphonsvisible)orfullyburied.

14



Figure13.Oceanquahogswithoutawirestartingburrowingintothesediment.Thefootisclearlyvisible.
Photo/Ljósm.:StefánRagnarsson.
13.mynd.Kúfskeljaránvírsaðgrafasigniðuríbotnlagið.Fóturinnséstgreinilega.

Alltheclamsinthethin‐wiregroupthatsurvivedthefirst24h,remainedcompletely
burrowedafter24hours,withnosiphonopeningsbeingvisibleonthesediment
surface(i.e.noevidenceoffeedingactivity).Therewasnooverallpatternin
burrowingbehaviourwithrespecttoburyingdepthandverticalmovements(Fig.14,
Table1).Allclamsinthethin‐wiregroupwereorientedvertically.



Figure14.Sedimentburialdepthoffiveoceanquahogsfittedwiththinwireafter24,48and72hours.
14.mynd.Lóðrétthreyfingfimmkúfskeljaísetimeðgrannanvíreftir24,48og72klukkustundir.

Onlyoneclamfittedwithathickwiremanagedtofullyburrow,reachingthebottom
ofthetankafter48hrs.After72hrsthissameclamhadmovedupwardsto3cm
beneaththesedimentsurface.Theremainingclamsremainedhalf‐buried
throughoutthestudyandwereorientedobliquely.

15
Table1.Numberofoceanquahogs,survivalandmortalityrates,burialbehaviouranddepthinthe
controlsandwithclamsfittedwiththin(1.6mm)andthick(3mm)wire24,48and72h.
Tafla1.Fjöldikúfskelja,yfirlifunogdánartíðni,hreyfingíbotnsetiogdýpihjáviðmiðunarhópi,skelmeðþunnan
(1,6mm)ogþykkan(3mm)vírárannsóknartímabilinueftir24,48og72kls.

 ControlThinwireThickwire
Number(no)14810
After24h

5onsedimentsurface



4half‐buriedwithwireoriented
obliquely,

 5reburied 1half‐buried
Survivingclams(no)1055
Deadclams(no)4 3 5
Burialdepth(cm) 3,16,2,4,20 
After48h2halfburied
4half‐buriedwithwireoriented
obliquely.

5withvisiblesiphon
openings 
 3reburied 
Survivingclams(no)1055
Deadclams(no)000
Burialdepth(cm) 3,3,3,1,1320
After72h

2half
‐
buried



3half‐buriedwithwireoriented
obliquely.


3withvisiblesiphon
openings


Survivingclams(no)54
Deadclams(no)001
Burialdepth(cm)20,20,20,5,53,3,3,13,173



Discussion
Thefindingsfromthisstudyshowthattheburrowingbehaviourofoceanquahogs
wasstronglyseasonal,withindividualsmoredeeplyburiedduringwintertoescape
adverseconditionswhilemostwereactivelyfeedingatthesediment‐waterinterface
duringsummer.ItislikelythatthedeepburrowingdepthofclamsinFebruarywasin
responsetocombinationofcoldertemperatures,reducedphytoplanktondensities
andincreasedstormfrequency.Lowseawatertemperaturesduringcoldseasons
havebeensuggestedtoinducedeeperburrowingandmetabolicarrest(hibernation)
inbivalves(Morleyetal.2007).Foodshortagecanforcebivalvestoburydeeperinto
sedimentsandrespireanaerobically,whichenablesthemtosaveenergyuntilfoodis
availableagain(Edelaar2000).Theglycogenstoreswillthuslastmuchlongerwhen
respiringanaerobicallythanwouldbethecaseduringaerobicrespirationwhenthe
clamsareatriskofstarvation,ashasbeenshownbycalorimetricmeasurements
(Oeschger1990).Thismayhavedevelopedasanevolutionaryadvantagewhere

16
savingsintotalenergybudgetaremadeattimeswhenfoodresourcesarescarce,as
pumpingseawaterissoenergydemanding(Taylor1976).
Sometrendsintheburialbehaviourwereunexpected.Themeanburialdepthof
clamsinFebruaryandSeptemberwasquitesimilarorabout8cm,butintuitivelyone
wouldexpectshellsinSeptembertobeclosertothesurfaceactivelyfeedingatthe
sediment‐waterinterface,similarasinJune.InSeptember,theseawater
temperaturewasrelativelyhigh(~9°C),similartothatofJune(~8°C),butmuch
highercomparedtoFebruary(~2.5°C).Onewouldalsoexpectthattheproductivity
ofphytoplanktontoremainhighinSeptemberasinvestigationsintheareabetween
1988and1991haveshown(GuðrúnG.Þórarinsdóttir,1993).Throughoutthestudy
period,thewindspeedswerehighestintheweeksprecedingthesamplingin
September.Itisplausiblethatthesewindspeedsweresufficienttocreateintense
waveinducedsedimentdisturbancesthattriggeredburrowingofshellsdeeperinto
sediments.DuringsamplinginSeptember,thediversnotedrippledsediment
surfaces,indicatingrecentwaveinducedsedimentdisturbances.Storminduced
wavedisturbancesareknowntohaveeffectonsurvival(YeoandRisk1979,Garcia‐
de‐Lomasetal.2019)andburrowingbehaviour(Nashimotoetal.1986,Haideretal.
2018)forvariousbenthicinvertebrates.Redjahetal.(2010)showedthatclams
burieddeeperintosedimentsinresponsetoincreasedcurrentvelocityinan
experimentalbenthicflume.Anotherfactorthatmayplayaroleisspawningactivity.
WithinIcelandicwaters,oceanquahogscanspawnalltheyeararound,butthemain
spawningactivityisbetweenJuneuntilAugust(Thorarinsdottir2000).During
spawning,clamsiphonsneedtobepositionedatthesediment‐waterinterface,while
followingspawningtheymaymovedeeperintosediments,andthismaypossibly
explainmoreofthedeeperburrowingofclamsinSeptember.
ThedifferencesinthemeanburialdepthsinJuneinthetwoyearsinvestigatedwas
about0.8cm,butneverthelessthisdifferencewassignificant.Itshouldbenoted
thatthestatisticalpoweroftestswashighduetothelargesamplesize(110and130
shellsinJune2003andJune2004respectively).ThetimeofsamplinginJunethetwo
yearsdifferedby25days,butitisunclearhowthismayhaveaffectedtheresults.
Theaveragesizeofclamswassimilaroverthestudyperiodbutwassomewhatlower
inSeptemberandJune2004.Theshelllengthwasonthreeoutoffoursampling
datesfoundtobepositivelyrelatedwithburrowingdepth,supportingfindingsfrom
severalotherstudies(e.g.ZaklanandYdenberg1997).Increasingthetimespent
burroweddeeplymayenhancesurvivalratebecauseofreducedpredationbutatthe

17
costofdecreasedfoodavailability.Forsomebivalvespecies,juvenileshavebeen
observedtoburrowfasterthanadults(JohnandFernadez1989,Davisetal.1999,
Nashimotoetal.1986,delaHuzandLopez2002,Haideretal.2018)whichcanbe
advantageoustoescapepredation.Theoceanquahogsinthepresentstudywere
mostly>25mm,butitispossiblethatsmallerclamscanburrowfaster.
Inthelaboratoryexperiment,noobviousrhythmicitywasobservedinburying
activity.Theperiodspentbeneaththesedimentsurfaceandtheburialdepthswere
variablewithlittlesynchronyamongtheclamsineithertheonsetofburrowingor
movementinthesediment.Allclamsthatmanagedtoburythemselvesremained
buriedthroughoutthestudywheretheyundertookverticalmovementsbutnever
emergedtothesedimentsurface.Taylor(1976)similarlyfoundthattheburrowing
behaviourtobenon‐rhythmicwithclamsremainingbelowthesedimentsurface
from1‐7dayswithnosatisfactoryexplanationfortheburyingbehaviour.
Thehighmortalityofclamsinthelaboratoryexperiment,30,37and50%inthe
control,thethinwireandthethickwiretreatmentgrouprespectivelymighthave
hadsomeinfluenceonthereliabilityoftheresults.Thestressrelatedtocapture,
transportation,andshortdurationoftemperatureacclimation(temperatureatsite
ofcapturewasabout2°Cbutintanks7°C)mighthavecontributedtomortality.
ResultsfromalaboratorystudyonadultC.islandicafromIcelandicwatersshowed
thatsuddenchangesintemperaturehadsignificanteffectontheirsurvival(Jónasson
etal.2004).Itisalsoclearthatthewirethicknessaffectedsurvivalrates.Mostofthe
shellsfittedwiththethickwirehadproblemsburrowingdeeplyinthesedimentsand
thismayhaveaccountedforthereducedsurvival.Whileallsurvivingclamscarried
outsomeburrowingactivity,20%remainedhalf‐buriedthroughoutthestudy.All
clamsfittedwiththethinwireshowedapatternofintermittentburrowingandwere
orientedvertically.Onlyoneclamfittedwithathickwiremanagedtofullyrebury,
withthewireorientedobliquely.Itisthusclearthatthethickwireinterferedwith
theburrowingactivityoftheclamswhilethethinwiremaynothave.Themaximum
burialdepthofoceanquahogsisstillunknown.Theresultsfromthepresentstudy
indicatethattheycanburrowatleastdownto20cm(thesedimentdepthinthe
tanks),butmayhaveburroweddeeperifthesandlayerwouldhavebeenthicker.
Thereislimiteddataonburrowingtimeofoceanquahoginsitubutthevarious
stressexposedtotheclamsinthepresentlaboratorystudymayhavedelayedonset
ofburrowingactivity.Thefirstclamtoreburyinthelaboratorystudy(withouta
wire)startedburrowing30minutesafterbeingplacedinthetankandtheburrowing

18
timewasthreehours.Itisdifficulttoknowwhetherclamslocatedinsituwould
burrowfaster.Oeschger(1990)showedthatmostoceanquahogsmanagedto
reburywithintwohoursafterbeingexperimentallymovedfromanoxic
environmentstosubstrateswithaeratedseawater.Anexampleofaslowburroweris
Myaarenaria,whichtakesabout100minutestoburrowbelowthesedimentsurface
(ChecaandCadée1997).ThereburialtimeforSpisulasolidaincreasedwith
increasingaerialexposure.Individualsthatwereexposedfor3hourstook50
minutestoreburycomparedtoonly15minutesintheinsitucontrols,asdetermined
bydivers(Chícharoetal.2003).

Acknowledgements
WethankthediversKarlGunnarssonandErlendurBogasonforsupportduringthe
fieldworkinEyjafjörðurandthestaffattheFMRImarinestationinGrindavíkforall
assistanceinthelaboratory.KlaraJakobsdóttirreadthedraftreportandgetsthanks
forgivinggoodadvice.

References
Arntz,W.E.andWeber,W.(1970).CyprinaislandicaL.(Molluska,Bivalvia)alsNahrungvonDosrch
undKliescheinKielerBucht.Ber.Dtsch.Wiss.Komm.Meeresforch.21.193‐209.
Checa,A.G.andCadée,G.C.(1997).HydraulicburrowinginthebivalveMyaarenariaLinnaeus
(Myoidea)andassociatedligamentaladaptations.J.Moll.Stud.,73,157‐171.
Chicharo,M.A.,Amaral,A.,Condinho,S.,Alves,F.,Regala,J.andGaspar,M.(2003).Adenylic‐derived
indicesandreburyingtimeasindicatorsoftheeffectsofdredging‐inducedstressontheclamSpisula
solida.MarineBiology,142,1113‐1117.
Davis,J.P.,Barenburg,C.andPederson,D.(1999).Burrowingresponseofjuvenilegeoducks(Panopea
abrupta)tochangesintemperatureandsalinity.J.ShellfishRes.,19,p.689.
delaHuz,R.andLopez,J.(2002).Theinfluenceofsedimentgrainsizeonburrowing,growthand
metabolismofDonaxtruculusL.(Bivalvia:Donacidae).JournalofSeaResearch,47,85‐95.
deZwaan,A.(1977).Anaerobicenergymetabolisminbivalvemolluscs.Oceanogr.Mar.BiolA.Rev.
15,103‐197.
Edelaar,P.(2000).PhenotypicplasticityofburrowingdepthinthebivalveMacomabalthica;
experimentalevidenceandgeneralimplications.GeologicalSocietySpecialPublications,177,451‐
458.
Fields,J.H.A.andStorey,K.B.(1987).Tissue‐specificalanopinedeyhydrogenasefromgilland
strombinedehydrogenasefromthefootmuscleofthecherrystoneclam,Mercenaria,mercenaria
(Linn.).J.Exp.Mar.Biol.Ecol.,105.175‐185.

19
Garcia‐de‐Lomas,J.,Payo,A.,Cuesta,J.A.andMacias,D.(2019).Morphodynamicstudyofa2018
mass‐strandingeventatPuntaUmbriabeach(Spain):EffectofAtlanticstormEmmaonbenthic
marineorganisms.J.Mar.Sci.andEng.,7,344;doi:10.3390/jmse7100344.
Griffith,C.L.andRichardson,C.A.(2006).Chemicallyinducedpredatoravoidancebehaviourinthe
burrowingbivalveMacomabalthica.J.Exp.Mar.Biol.Ecol.,331,91‐98.
GuðrúnG.Þórarinsdóttir.(1993).Tilraunaeldiáhörpudiski,Chlamysislandica(O.F.Muller),í
Breiðafirði.IIVöxtur.Náttúrufræðingurinn62,157‐164.
Haider,F.,Sokolocv,E.P.andSokolova,I.M.(2018).Effectsofmechanicaldisturbanceandsalinity
stressonbioenergeticsandburrowingbehaviourofthesoft‐shellclamMyaarenaria.J.Exp.Biol
(2018)22l,jeb172643.doi:0.1242jeb.172643.0.1242jeb.172643.
Hafrannsóknastofnun.(2019).KÚFSKEL–Arcticaislandica.MFRIAssessmentreport2019.7bls.
Holwerda,D.A.,Veenhof,P.R.,vanHeugten,H.A.A.andZandee,D.I.(1983).Modificationofmussel
pyruvatekinaseduringanaerobiosisandaftertemperatureacclimation.Mol.Physiol.,3,225‐234.
John,L.andFernadez,T.V.(1989).Influenceofenvironmentalfactorsontheburrowingbehaviourof
anestuarinebivalve,VilloritacyprinoidesfromVeliLake.S.W.coastofIndia.J.Ecobiol.1,137‐148.
Jónasson,J.P.,Thórarinsdóttir,G.G.,Eiríksson,H.andMarteinsdóttir,G.(2004).Temperature
toleranceofIcelandscallop,Chlamysislandica(O.F.Müller)undercontrolledexperimental
conditions.AquacultureResearch,35,1405‐1414.
Jónsson,S.(2004).Sjávarhiti,straumarogsúrefniísjónumviðstrendurÍslands.
Hafrnnsóknastofnunin,fjölrit,111,9‐20.InIcelandic.
Kaasa,Ö.AndGuðmundsson,K.(1994).SesonalvariationinphytoplanktoncommunityinEyjafjördur,
NorthIceland.ICESC.M.L;24,p15.
Morley,S.A.,Lloyd,S.P.,Miller,A.J.andPörtner,H.‐O.(2007).Hypxiatoleranceassociatedwith
activityreductionisakeyadaptationforLatermulaellipticaseasonalenergetics.Ecophysology153,
29‐36.
Nashimoto,K.,Kojima,T.andSato,O.(1986).BurrowingbehaviourofJapanesesurfclams.Bull.Fac.
Fish.HokkaidoUniv.,37,171‐180.
Norkko,A.andBonsdorff,E.(1996).Rapidzoobenthiccommunityresponsestoaccumulationsof
driftingalgae.Mar.Ecol.Prog.Ser.,131,143‐157.
Oeschger,R.(1990).Long‐termanaerobiosisinsublittoralmarineinvertebratesfromtheWestern
BalticSea:Halicryptusspinulosus(Priapulida).AstarteborealisandArcticaislandica(Bivalvia).Mar.
Ecol.Prog.Ser.,59,133‐143.
Posey,M.,Lindberg,W.,Alphin,T.andVose,F.(1996).Influenceofstormdisturbanceonanoffshore
benthiccommunity.Bull.Mar.Science,59,523‐529.
Ragnarsson,S.A.,Thorarinsdóttir,G.G.andGunnarsson,K.(2015).Shortandlong‐termeffectsof
hydraulicdredgingonbenthiccommunitiesandoceanquahog(Arcticaislandica)populations.Marine
EnvironmentalResearch.109,113‐123.DOI10.1016/j.marenvres.2015.05.003
Redjah,I.,Olivier,F.,TremblayR.,Myrand,B.,Pernet,F.,Neumeier,U.andChevarieL.(2010).The
importanceofturbulentkineticenergyontransportofjuvenileclams(Myaarenaria).Aquaculture,
307(1‐2),20‐28.
Sibenaller,J.F.,(1979).RegulationofpyruvatekinaseinMytilusedulisbyphosphorylation‐
dephosphorylation.Mar.Biol.Lett.,1,105‐110.

20
Sick,J.M.,deZwann,A.anddeBont,A.M.T.(1983).AnoxicmetobolicrateinthemusselMytilusedulis
L.Estimatdbysimultanjoursdirectcalorimetryandbiochemicalanalysis.Physiol.Zool.,56,56‐73.
Stanley,S.M.(1970).RelationofshellformtolifehabitsoftheBivalvia(Mollusca).TheGeological
SocietyoftheAmericaMemoir,125,1‐295.
Tallqvist,M.(2001).BurrowingbehaviouroftheBalticclam,Macomabalthica:effectsofsediment
type,hypoxiaandpredatorpresence.Mar.Ecol.Prog.Ser.,212,183‐191.
Taylor,A.C.(1976).BurrowingbehaviourandanaerobiosisinthebivalveArcticaislandica(L).J.Mar.
Biol.Ass.U.K.,56,95‐109.
Theede,H.,Ponat,A.,Hiroki,KandSchlieper,C.(1969).Studiesontheresistanceofmarinebottom
invertebratestooxygen‐deficiencyandhydrogensulphide.MarineBiol.2,325‐337.
Thorarinsdóttir,G.G.(2000).Annualgametogeniccycleinoceanquahog,Arcticaislandicafromnorth‐
westernIceland,2000.J.Mar.Biol.Ass.U.K.,80,661‐666.
Thorarinsdóttir,G.G,Ragnarsson,R.ÁandGunnarssonK.(2002).Theimpactofhydraulicdredgingon
oceanquahogpopulation.ICESCM2002/V:28.pp.30
Thorarinsdóttir,G.G.,Jacobson,L.,Ragnarsson,S.Á.,Garcia,E.G.andGunnarsson,K.(2009).Capture
efficiencyandsizeselectivityofhydraulicclamdredgesusedinfishingforoceanquahogs(Arctica
islandica):simultaneousestimationintheSELECTmodel.ICESJournalofMarineScience,67,345‐354.
Thorarinsdóttir,G.G.,Gunnarsson,K.andBogason,E.(2009).
Massmortalityof
oceanquahog,Arcticaislandica,onhardsubstratuminLonafjördur,north‐eastern

Icelandafterastorm,2009.JMBA2‐BiodiversityRecords,3pp.Publishedonline.
Weigelt,M.andRumohrH.(1986).Effectsofwide‐rangeoxygendepletiononbenthicfaunaand
demersalfishinKielBay1981‐1983.Meeresforsch,31,124‐136.
Zaklan,S.D.andYdenber,R.(1997).Thebodysize‐burialdepthrelationshipintheinfaunalclamMya
arenaria.J.Exp.Mar.Biol.Ecol.,215,1‐17.
Zwarts,L.andWanink,J.(1989).Siphonsizeandburyingdepthindeposit‐ andsuspension‐feeding
benthicbivalves.MarineBiology,100,227‐240.
Yeo,R.K.andRisk,M.J.(1979).Intertidalcatastrophes:effectofstormsandhurricanesonintertital
benthosoftheMinasBasin,BayofFundy.J.Fish.Res.BoardofCanada,36,667‐669.


46