FRI-UW-8808February1988FISHERIESRESEARCHINSTITUTESchoolofFisheriesUniversityofWashingtonSeattle,WA98195NOAATECHNICALREPORTSERIESOCRM/MEMDBENTHICPRIMARYPRODUCTIONINTHEEELGRASSMEADOWATTHEPADILLABAYNATIONALESTUARINERESEARCHRESERVE,WASHINGTONbyRONALDM.THOMU.S.DEPARTMENTOFCOMMERCENATIONALOCEANOGRAPHICANDATMOSPHERICADMiNISTRATIONNATIONALOCEANSERVICEOFFICEOFOCEANANDCOASTALRESOURCEMANAGEMENTMARINEANDESTIJARINEMANAGEMENTDIVISIONWASHINGTON,D.C.ThisworkistheresultofresearchsponsoredbytheU.S.DepartmentofCommerce,NationalOceanographicandAtmosphericAdministration,NationalOceanService,OfficeofOceanandCoastal ResourceManagement,MarineandEstuarineManagementDivision,under contractNA86AA-D-CZ027.ApprovedF)~Date_________________________________RobertC.Francis,DirectorThisreportwaspreparedasanaccountofgovernment-sponsoredworkandhasbeenapprovedfordistribution.Approvaldoesnotsignifythatthecontentsnecessarilyreflecttheviewsandpoliciesofthegovernment,nordoesmentionoftradenamesorcommercialproductsconstituteendorsementorrecommendationforuse.~fl~72-mlREPORTDOCUMENTATION1.REPORTNO.2.3.Recipient~sAccessionNo.PAGE4.TitleandSubtitle5.ReportDateBenthicPrimaryProductionintheEelgrassMeadowatthePadill12—87BayNationalEstuarineResearchReserve, Washington7.Author(s)8.PerformingOrganizationRept.No.RonaldN.Thom9.PerformingOrganizationNameandAddressio.Project/Task/WorkUnitNo.FisheriesResearchInstituteSchoolofFisheries,WH1O11.Contract(C)orGrant(G)No.UniversityofWashington(C)Seattle,WA98195(G)NA86AA—D—CZ02712.SponsoringOrganizationNameandAddress13.TypeofReport&PeriodCoveredNOAA/OCEN/MENDPadillaBayN.E.R.R.~..FinalReport6/86—12/87l82~ConnecticutAveNWWAStateDept.ofEcologyUniversalBuilding1043Bayview—EdisonRd.14.Washington,D.C.20235Mt.Vernon,WA9827315.SupplementaryNotes16.Abstract(Limit:200words)Thespatialpatternsofstanding stockandproductivityofbenthicautotrophiccomponents (ZosteramarinaandZosterajaponica,epiphyticalgae andbenthicsedimentassociatedalgae)oftheeelgrassmeadowinPadillaBay,Washington,werestudiedseasonallyforoneyear. Eelgrassextendedfromapproximatelyl.OmaboveMLLWdowntosubtidaldepths.However,standingstockdecreasedatdepthsbelow-0.5rnMLLW.Z.japonicaformedabandatupperelevations,andmixedwithZ.marinaatabout0.3mto 0.6mMLLW.Epiphyticalgaewereabundantinthemeadow,and reached greateststandingstockbetween0.3and-0.4mMLLW.Sedimentassociatedalgaewere abundantatallelevationsasindicatedbychlorophyllaconcentrations.Thestandingstockofallcomponentsvariedseasonally.Sedimentalgaereachedpeakabundanceinearlyspring,followedbyrapidgrowthofepiphyticmacroalgaeinearlysummer.Eelgrass biomasswas greatestinearlytolatesummerdependingupondepth.Annualnetprimaryproductivity(NPP)forthesystemwas351gCrn2.Epiphyticalgae, Z.japonicaandZ.marinawereresponsiblefor50,2and48%ofthisproduction,respectively.NPPbysedimentalgaewasnegligibleduetohighsedimentassociatedrespirationrates.Totalannualproductionfromthe3,000ha systemwasapproximately28,000mtdryplantmatter.17.DocumentAnalysisa.Descriptorseelgrass,primaryproduction,standingstock,seasonaldynamics,epiphyteproduction,estuarineprimaryproductionb.ldentiflers/Open.EndedTermsc,COSATIField/GroupSecurityClass(ThisReport)EllabliltYStatement21.NootPagesOPTIONALFORM272(4-77)(FormerlyNTIS—35)Departmentof Commerce(See ANSI—Z39,18)SeeInstructionsonReverse-IlTABLEOFCONTENTSLISTOFFIGURESiiiLISTOFTABLESivPREFACEviiINTRODUCHON1STUDYAREADESCRIPTION3MATERIALSANDMETHODS5SamplingSites5StandingStockSampling5ProductivityMeasurements6Eelgrass6BenthicAlgae7SystemProductivityCalculations8RESULTS9EelgrassMorphometrics9DensityandStandingStock9Eelgrass9Epiphytes14Sediment Microalgae14Productivity14ProductiontoBiomass20ComparisonofMethods25DISCUSSION26REFERENCES31ifiLISTOFFIGURESFigurePage1.LocationofPadillaBay22.PadillaBayand thestudysites43.Eelgrassmeandensityvs depth114.Eelgrassmeandensityatthreedepthsvstime125.Eelgrassmeanbiomassvs depth136. Eelgrass meanbiomassatthreedepthsvstime157.Epiphytemeanbiomassvsdepth168.Epiphytemeanbiomassatthree depthsvstime179.Meansedimentplantpigmentconcentrationsvsdepth1810.Meansedimentchlorophyllaconcentrationatthree depthsvstime1911.NPPvsdepth2112.Eelgrassshootweightvsannual systemNPP24ivAs~isApnis~pwsi~onpoidAi~mud~qiaoj(q:J~J}~J)op~issumotqo~uoiionpoadpui~aai~.i‘(s)sslrnIoTqj~nuu~~J~AVlz~81~P~ ~flUTdcTh~I~OTJO~oTsi~iunu~dou~moqthowss~i~p~iojsuo!ssaT~1i~urjs~rrnvi10isriPREFACEIgratefullyacknowledgetheassistanceofI.Hampel, D.Groebecker,K.Li,D.Olden,L.HallumandD.Shrefflerinthefield.3.Hampel,A.Shaffer,D.ShrefflerandL.Hallumprocessedmostofthe samples.A.Shafferenteredalargeproportionofthe dataonto computerfiles.3.Shaplanddrewthe maps.T.Stevensprovidedthedepthdeterminationsforthestudysites.ThestaffatthePadillaBaySanctuarywasveryhelpfulinprovidingequipment,logisticalsupportandovernightaccommodationsduringfieldtrips.IespeciallythankT.Stevens,DirectorofthePadillaBayReserve,forhelpandsupport.R.Nakatani,T.Stevensandananonymousreviewerprovidedhelpfulcommentsthatconsiderablyimprovedthemanuscript.M.Dukedid fmaleditingofthemanuscript.TheworkreportedhereindocumentsthedistributionandproductionofthedominantprimaryproducersintheReserve.Thisinformationis neededtounderstand theecologicalimportanceandcontributionofthemajorprimaryproducerswithinthereserve.Thedatacomplimentsworkonthedistributionoffishprey(C.Simenstad)andDungenesscrab (D.Armstrong)intheBay,andresearch on thenutrientdynamics(S.Williams)andfoodwebsupport(R.Wissmar)on theflats.ResearchwhichdocumentsthetotaldisthbutionofseagrassesintheBay(T.Mumford,B. Webber)willutilizethe presentdatatocalculatethetotalprimaryproductionintheBay.FY87researchfocusingonprimary productionintheremainingbenthichabitats,i.e.mucifiats,gravelbeds(R.Thom)andmarshes(M.Burg),willbecoupledwiththeseagrassdata todocumenttherelativeandabsolutecontributionofbenthicplantstothefoodweboftheBay.vINTRODUCTIONSeagrassesareamongthemostcommonplantsinhabitingshallowcoastalecosystems.Eelgrass(Zosteraspp.)isthemostcommonseagrasstaxoninestuariesandembaymentsalongtemperate regionsofNorthAmerica(Phillips1984).Therelativelygreatimportanceofautotrophiccomponentsofseagrasssystemstonearshorefoodwebsisproveninseveralareas(e.g.,Stoner1980,Fry1984).Further,thesystems canactautonomouslyintermsofproductionandconsumptionprocesses(AsmusandAsmus1985).Seagrasssystemsareutilizedashabitatandnurseryareasbymanyanimals(e.g.,HeckandThoman1984:Heijs1985:VirnsteinandCurren1986).Althoughdominantandecologicallyimportant,fundamentalinformationoneelgrassdistributionandproductionislimitedforthePacificcoast.Recently,KentulaandMclntire(1986)showedthatZosteramarinaL.inNetartsBay,Oregon,exhibitedamean annualproductionrateof383gCnr2.Thetotalproductionfromthe 176habed amountedto3,200mty1.Ofsignificancewasthefactthatthebiomasswasreplaced10timesduringthegrowingseason,whichindicatedsubstantialexportoforganicmattertosurroundinghabitats.Thom(1984)estimatedthateelgrassaccountedforover50%oftheannualprimaryproductioninGraysHarbor,acoastalestuaryinWashington.Seaweedsanddiatomsepiphyticorcloselyassociatedwithseagrassescanformasignificantproportionofthetotalprimaryproductioninthesystem.Penhale (1977)calculatedan18%contributionbytheepiphyticfloratothetotalproductivityoftheeelgrasssysteminNewJersey.Kentula(1982)foundthatmaximumstandingstockofepiphytesoneelgrassinNetartsBayexceededseagrassleafbiomassby2.3timesduringspring.The highimportanceofseagrassassociatedalgaehasbeenprovenforonefoodwebinhabitingestuariesofHoodCanal,Washington(SimenstadandWissmar1985).Thepurposeofthisworkwastodescribethespatial patternsandseasonaldynamicsofstandingstockandproductivityofthemajorbenthicintertidalplantsinPadillaBay(Fig.1).Anattemptwasmadetopartitiontheproductionamongthemajorcomponents(i.e.,twoeelgrassspecies, seaweedsandsedimentmicroflora), providedatafromwhichpredictionsofproductioncouldbemadeinunsampledareas,andcalculateafirstorderapproximationoftotalannualprimaryproduction(i.e.,theamountofcarbonfixedbyplantsduringphotosynthesis)intheBay.2CanadaVancouverIslandPADILLABAYOlympic PeninsulaFigure1.LocationofPadillaBay.3STUDYAREADESCRIPTIONPadillaBayisashallowembaymentlocatedonnorthernPuget Sound(Fig.1).TheBaycoversapproximately4,200ha,and issurroundedbyagriculturallands,foresteduplandsandnarrowfringingmarshes(Fig.2).ThebroadintertidalflatsintheBayaredissectedbyshallowchannelswhichdraintheflatsduringfallingtides.Themeantiderangeandmean springtidalrangefortheareaare1.55and2.56m, respectively.RiverineinputisprimarilyfromtheSkagitRiverviaSwinomishchannel, andsecondarilyfromsmallsloughsdraininglocaluplands.SalinityintheBayrangesfrom15pptto30pptdependinguponriverflowandtidalinfluences(CassidyandMcKeen1986andunpublisheddata).Watertemperature variesfrom7°CinDecember-Februarytoashighas25°Cinlargepooisofstandingwateron theflatsduring warm mid-summer(July)days.Inorganicnitrogenvaluesaretypically lowthroughouttheyear.Nitrateconcentrationrarelyexceeds5jiMandisusuallylessthan1jiM.(unpublisheddata).Lownitrogentophosphorousratios(range3-6)existinspringandsummerinthewater overtheseagrassmeadow(Wissmar1986).Themostconspicuousautoirophiccomponentoftheintertidalareaiseelgrass,whichoccupiesapproximately3,500ha,and representsoneofthelargestcontiguouseelgrassmeadowsonthePacificcoastofNorthAmerica.TheeelgrassspeciespresentinPadillaBayareZosteramarinaandZosterajaponicaAschers.&Graebn. Z.japonicaisanannualspecies,and isbelievedto havebeenintroducedtotheregioninadvertentlywiththeimportationofoysterseedfromJapaninthe1930s(Harrison1976).Thislatterseagrassspeciesis generallysmallerinsizeandoccupieshigherintertidalelevationsascomparedtoZ.marina(Harrison1982a).4Figure2.PadillaBayandthestudysites.TheinsetshowsdepthsofsitesrelativetoMLLW.ThelinedelineatingchannelsandflatswithintheBay indicatestheapproximateseawardextentoftheintertidalzone(-l.OmMLLW).The outlineofeelgrassis alsoapproximate.Littleinformationexists onthedistributionofeelgrassinthechannels.5MATERIALSANDMETHODSSamplingSitesEightstudysiteswerelocatedinthemidportionoftheBay(Fig.2).ThesitescoveredadepthgradientthatspannedfromthelandwardedgeofZ.japonicatotheedgeofasubtidalchannel.Thedepthsofthesites,relativetoMLLW,were 0.8m,0.6m, 0.5m,0.3m,0.im,-0.im,-0.2mand-0.4m.Thesiteat-0.2mwaslocatedinthemiddleofashallow, narrow(ca.15mwide)channel,andthesite at-0.4mwaspositionedattheedgeofawiderchannelthatextendedtosubtidaldepths.Waterflowedrelativelyrapidlythroughthesechannelsduringfallingtides.Preliminaryobservationsshowedthatthe siteswererepresentativeoftherangeofseagrassstandingstockandmorphologyintheBay.EachsiteconsistedofalOmtransectlinepositionedparalleltotheedgeofthewater.Thesiteswere markedbywoodenstakesplacedateachendofthelOm line.Samplingwascarried outusing0.1m2quadrat placedatrandompointsalongeithersideoftheline.DensityandStandingStock SamplingEelgrassshootswithinthequadratwereharvestedby cuttingattheirbase.Theplantmaterialwas placedinlabelledplasticbags.Asmallplastictubewasusedtoextractasedimentcore(1cm diameterx1cmdeep)fromthequadratforanalysisofchlorophyllaandphaeopigmentconcentrations.Allsampleswerefrozeninthedarkforlateranalysis.Ingeneral,threequadrats(onewasalsousedforproductivitymeasurements,seebelow)weresampledateachsite.Samplingwasconductedon9and 23June,22July,5and18Augustand7October1986, and26 January,25February,16Apriland1May1987.AllsitesweresampledduringtheJune,July,AugustandMayvisits.Threesites(i.e.,0.6,0.1,-0.4m)representativeofthetwomainhabitats(i.e., Z.japonicaand Z.marina)weresampledduringallvisits.Frozensamplesofmacrophytes were thawedinthelaboratory,rinsedgentlyintapwatertoremovesediments,and separatedbyspecies.Theepiphytes,consistingofseaweedsandfilamentousandtubedwellingdiatomswerecarefullyremovedfromtheseagrassleavesbyscrapingwithaspatula.Thefreezingprocessfacilitatedeasyremovaloftheepiphytes.Thenumberofshootsofeacheelgrassspecieswasrecordedforeachsample.Theweightofeachspecies wasrecordedfollowingdryingat90°Cforatleast48hours.Todescribemorphologicaldifferencesineelgrasspopulationsamongthesites,the6length,width,leafareaanddryweightweredeterminedforfiverandomshootsfromeachsamplecollectedinJune 1986.Chlorophyllaandphaeopigmentconcentrationsweredeterminedfrom90%acetoneextractionsofsedimentsusingafluorometer (StricklandandParsons1972).ProductivityMeasurementsEelgrassNetshootprimary productivity(NPP)ofZ.marinawas measuredusingamodificationofthemethodofKentulaandMclntire(1986).A0.1m2areawasmarkedateachsitecontainingthisspeciesbyanchoringaquadratusingstiffwire(i.e.,clothes hanger)pushedintothesediment.Ashootwasmarkedbypokingahypodermicneedlethroughtheleavesatapointimmediatelyabovetheyoungestsheath.Differentdiameterneedleswereuseddependingon thewidthoftheleavesnotonlytominimizedamagetotheplantbut toalsoassurerelocationofthemarksatalaterdate.Themajorityofshootswithinthequadratweremarked.Allvegetationinthequadratwasharvestedduringthenextvisittothesite,andfrozenforlateranalysis.Inthelaboratory,thesamplesweretreatedexactlylikethesamplesforstandingstock.However,themarkedshootswereseparatedfromtheremainderofthesample.Theshoot wascutatthelevelofthemarkintheoldestleaf.Next,theportionofleafdistaltothemarkon thatleafwasremoved.Thematerialbetweenthelevelofthemarkontheoldestleafandthedistalmarkconsistedofthebiomassproducedduringthetimebetweentheoriginalmarkingandtheharvesting.Itwasassumedthatnoleaflossoccurredduringthe13-15dayintervals.Lossoftheoldestleafwasapparentinafewcasesinthatamarkwasfoundinthebasalportionoftheoutersenescentleaf,buttheupperportionoftheleafwaslost.Inaddition,usingthemarkintheoldestleafas abaselineassumedthatnogrowthtookplaceintheoldestleaf.Verylittle(<10%)oftheannualZ.marinaNPPwas duetogrowth intheoldestleafinNetartsBay(MaryKentula,personalcommunication,1986).Thedry weightofthenewmaterialproducedduringthegrowthintervalwasrecorded.Finally,thedataonshootdensityandbiomassofcomponentplantsfromthequadratwereincludedasathirdreplicatesampleofstandingstockfromeachsite.ProductionexperimentswerecarriedoutduringJune,JulyandAugust1986,andApril-May1987;aperiod coveringthegrowingseasonfortheplants(KentulaandMclntire1986,Harrison1982a).7TheshootmarkingtechniquewasattemptedonZ.japonicaemployingveryfmeneedlesandpins,butprovedunsuccessfulduetodifficultiesinconfidentlyrelocatingmarksintheverynarrow (<2mm)leaves.Inaddition,damageto theleavesappearedsignificant,evenwiththesmallestdiameterpin.Thus,changeinmeanbiomasswasusedasanindicatorofNPP. Z.japonicaisanannual,and isvirtuallyabsentfromtheBayinwinter. Thisfact,coupledwiththerelativelyshortintervalsbetweensamplingsduringthegrowingseason,minimizedtheerrorinestimatingNPPusingbiomasschanges.Limitedexperimentswereconductedwithbotheelgrass speciesusing oxygenflux(seebelow)to provideacomparisonofmethods measuringNPPusing oxygenfluxversusshootmarkingandbiomasschanges.Becauseofevidencefromphysiologicalandenvironmentalwork,theuseofoxygenfluxtomeasurenetproductionwasstronglydiscouragedbyZiemanandWetzel(1980). Therefore,IusedleafmarkingandbiomasschangestoestimateeelgrassNPPinPadillaBay.BenthicAlgaeTheNPPofalgaeepiphyticontheeelgrasswas measuredusingstandardlightanddarkbottleincubationsfollowingthemethodologyinLittlerandArnold(1985).HealthyspecimensofepiphyticalgaewerecollectedfromthesitesandtransportedtolaboratoryfacilitiesatthePadillaBay InterpretiveCenter.Portionsofspecimens were placedin300ml BODbottlescontainingwatercollectedfromtheBay.Theinitialdissolvedoxygen(DO)wasmeasuredusinganoxygenmeter(YSIdissolvedoxygen metermodel58).Thebottles were placedinawaterbathheldatambientseatemperature,andincubated underambientmid-daylightfor1-3hours.Bottles containingwateronlywererun toaccountforplanktonmetabolism.Followingtheincubation,thefmalDOwasrecorded.Thespecimenswere removedfromthebottles,driedandweighed.NPPwascalculatedforeachspeciesusingtheformulasinLittlerandArnold(1985).Two-fourreplicateswererunforeachspecies.Theexperimentstookplaceon9June, 23 June,22Julyand18August1986, and30April1987.Shootsofbothseagrassspecieswereincubatedinasimilarmannerduringsomeexperiments.SedimentNPPwasmeasuredinclear plexiglasscylinders.The cylinderswere20cmlongand hadaninsidediameterof10cm.Anundisturbed sedimentcore(5cmdeep)wascarefullyremovedfromwithinonerandom0.1m2 standingstockquadratateachsiteusingthecylinder.Thebottomwas sealedwitharubberbung.The topofthecylinderwasclosedwithaplexiglass plateexceptforahole(1.3cm diameter)throughwhichtheoxygen8probecouldbeinserted.Thisholewassealedwitharubberstopperduringincubations.ThesedimentswereincubatedunderthesameconditionsastheepiphytesintheBODbottles.SystemProductivityCalculationsTheZ.marinagrowthdata wasextrapolatedto NPP perunitareabymultiplyingmeanNPPpershootbythemeanshootdensity.Z.japonicaproductionwascalculatedasthedifferenceinmean biomass betweensuccessivecollectiondates.Epiphyteproductionperunitareawasdeterminedbymultiplyingmeanproductionpergoftissuebymeangdryweightoftissueperunitarea.Sedimentproductionwasdirectlymeasuredperunitareaofsediment.Epiphyteandsedimenthourlyproductionwasexpandedtodailyratesbymultiplyinghourlyratesby8tosimulatethedurationofnon-lightlimitedphotosynthesis(unpublisheddata).Total dailyNPPforasitewasthesumofperunitarearatesforthespeciesoccurringatthesiteduringthesamplingperiod.Afactorof0.38gC=1gdrywtwasusedtointer-convertplantdryweightwithcarbon content (Westlake1963),9RESULTSEelgrassMorphometricsCoefficientofdeterminationvaluesbasedonlinearregressions showedthatpairsofmorphornetricparametersweremore strongly relatedforZ.marinaascomparedtoZ.japonica(Table1).Shootlengthandleafareaofbothspeciesincreasedwithincreasingdepth,althougharelativelywiderangeinshoot lengthsforZ.marinaespeciallyatthedeepestsitesresultedinarelativelyweakrelationship(Table1).Non-linearmodelsappliedtothedatadidnotyieldappreciablygreaterR2valuesover thatofthelinearmodel.DensityandStandingStockEelgrassShootdensityforbothspeciesshowedastrongrelationshiptodepthduringthegrowingseason(Fig.3a,b),withZ.japonicareachingpeakdensitybetween0.5and0.8mdepthandZ.marinahavingpeakdensityat-0.2mdepth. Basedonthedensity vsdepthcurves,thedepthofmaximumoverlapofthetwospecieswasatabout0.3rn.The dramaticseasonalityofZ.japonicaistypifiedbythe changeinmeandensityfromamaximuminJuneofapproximately3200shootsrn-2toaminimumoflessthan100shootsrn-2inwinteratthesiteat0.6rndepth (Fig.4).Seasonal changesinthedensityofZ.marinawasmuchlesspronounced (Fig.4).Meanbiomasswasstronglyrelated todepthalso(Fig.5a,b).ForZ.japonica,biomass wasgreatestatdepthsbetween0.3 and0.8m.Aninterestingshiftinbiomassisevidentduringthegrowingseason,however.At0.6m,biomasswaslowest inMay,greatestinJuneandintermediateinAugust.ThedifferencebetweenMayandAugustvaluesat0.5rnisalsorelativelygreat.Seasonaldifferencesattheotherelevationsarelesspronounced.PeakbiomassofZ.marinaoccurredatthelowestdepth(-0.4m)inMayandJune,andatamuchshallowersite(0.lm)inAugust.Therelativelygreatleafareaofplantsat thelowestelevation explainsthehighbiomassatrelativelylowdensity(Fig.3b)conditionatthelowestelevation.Aswithdensity,the greatestoverlapofthetwospecieswithregardtobiomasswas atthe0.3rndepth(Fig.5a,b).Althoughpeakdensitieswerequitedissimilarbetweenthetwospecies(Fig.3a,b),themaximummean biomassmeasuredwassimilar(Fig.5a,b).10Table1.Linearregressionsforseagrassmorphometricparameters.formY=a+bX.R2=coefficientofdetermination-V5~_)ThemodelisoftheaSpeciesZ.japonicashootwt.(mg)length(cm)3.320.600.49leafarea(cm2)length(cm) 1.892.500.46shootwt.(mg)leafarea(cm2)1.75-3.000.32length(cm)depth(m)a-6.437.260.55Z.marinashootwt.(mg)length(cm)43.86-362.610.74leafarea(cm2)length(cm)19.31-120.410.78shootwt.(mg)leafarea(cm2)2.00-59.100.85length(cm)depth(m)a-13.8415.810.26aRelativetoMLLW.c3(n\InI00IIn0zB)Z.MAl~INAaA)11Z.JAPONICA-~‘~-MAY•+JUNE--AUGUSTI0IninI.00IIn0zCX1000)4S210—0.5I.I.I.I..7-I’I’I’.1~•I’7”‘.4-00.5DEPTHCm)1-*-MAYCX1001-.4-JUNE-AUGUST40—0.S00.5DEPTHCm)Figure3.Eelgrassmeandensityvsdepth.A)Z.japonica;B)Z.marina.CX1000)d(I)(I)I—00IU)4d1-*-ZJ-‘-O.Sm•+ZM-‘-0.imJFMAMMONTHC19B6—1~87)Figure4.Eelgrassmeandensityatthreedepthsvstime.ZJZ.japonica;ZM=Z.marina.12S2--ZM—O.Bm++0JJAS0ND300250200UU)150>-a:o100500—0.5300250I200UU)\150>-a:o100500—0.513A)Z~JAPONICATI’I’I~-*~~MAY.+JUNE--AUGUSTI00.5DEPTHCm)B)Z.MARINA-~-MAY•+JUNE-.AUGUST00.5DEPTHCm)Figure5.Eelgrassmeanbiomass vsdepth.A)Z.japonica;B)Z.marina.14Theseasonalshiftinbiomassforbothspecieswas evident,withmaximumbiornassoccurringinearlysummerforZ.japonica(Fig.6).Z.marinabiomasspeakedinspringatthelowestelevationandinlatesummerinthehighelevationsite(O.lm).Thesiteat-O.4mmaintainedthe greatest biomassthroughoutthewinter.EpiphytesMaximummeanepiphytebiornass,whichincludedbothseaweedsandfilamentousandtubedwellingdiatomsepiphyticoneelgrassandassociatedwiththebaseoftheeelgrassshoots,occurredat thesiteat0.lmdepthinJune(Fig7).Therewasapronouncedpeakofrelativelyshortdurationofepiphytebiornassduringearlysummer(June)atthethreeintensivelystudiessites(Fig.8).TheJunepeakwasdominatedbydiatoms,theredalgaCeramiumpacjficumandthe greenalgaUlvafenestrata. Diatombiomasswasgreatestat0.lm(248.9gdrywtrn-2).ThebiornassofC.pac~cumwasgreatestat-0.2m(45.6gdrywtrn2).U.fenestratabiomasswasgreatestat-O.lm(34.2gdrywtrn-2).ThegreenalgaEnteromorphaintestinaliswasabundantinlateJune, andreachedatpeakmeanbiomassof113.6 gdrywtrn-2at-0.4mduringthis period.OtherspeciesrecordedintheepiphytesamplesincludedthegreenalgaCladophorasp.,thebrownalgaLaminariasaccharinaandtheredalgaGracilariapac~fica.C.pac~ficum,U.fenestrataandG.pac~ficawere commonmembersoftheunderstoryassemblageinthe Z.marinaportionofthebed.SedimentMicroalgaeTherewasno apparenttrendinsedimentchlorophyllaconcentrationrelativetodepthduringanyofthesamplingsinspring-summer (Fig.9a).Concentrationsdidchangeamongthemonths,andthischange appearedmostpronouncedatthehighestsite.Phaeopigmentconcentrationwasgreatestat7ofthe8sitesin MayascomparedtoJune andAugust(Fig.9b).Phaeopigmentconcentrationshowedlittlerelationshiptodepthduringthelattertwomonths.Chlorophyllaconcentrationwashighestatthethreeintensivestudysitesinlatewinterthroughearlyspring(i.e.,February-April)(Fig.10).Thispeakprecedestheearlysummerincreaseinseagrass(Fig.6)andseaweed(Fig.8)biomass.ProductivityCalculationofNPPwasdividedintospring(i.e.,April-June)andsummer(i.e.,JulyAugust)to coverthegrowingseasonandtoemphasizeapparentseasonaldifferencesin15Zi-*-0.SmI.I.I.0/4I.—.—— ——/-—— —JJAS0N DJFMAMMONTH<1980—1967)Figure6.Eelgrassmeanbiomassat threedepthsvstime. ZJZ.japonica;ZMZ.marina.+ZM-s-0.lrnZM—O~.4mTIU,\I—>03002502001.50100Sc0+II‘Ii.+0~+16EPIPHYTES—N—MAY•+JUNE300AUGUST1•2502000U)1500-4.50DEPTHCm)Figure7.Epiphytemeanbiomassvsdepth.17-*---.-oSmEPIPHYTES•+-‘-0.lm300—--—O.4m-~250—IciU)\150—.>-a:0100—;:,~,—I••~..Lj50—.~—~Tb— — ——+0..~t.1i~i—_~I~J JA S0N DJFMAMMONTHC1~B6—1~B7)Figure8.Epiphytemeanbiomassatthree depthsvs time.181UU)(514003002001000—0.5A)CHLOROPHYLL~-~-MAY•4.JUNE--AUGUST.4.112001000$00f-IU)500\(5I4002000—0.5B)PHAEOPIGMENTS00.51DEPTHCm)Figure9.Meansedimentplant pigmentconcentrationsvs depth.A)Chlorophylla;B)Phaeopigments.+O0.5DEPTHCm)-II-MAY.4.JUNE- -AUGUST+IciU)\ICHLOROPHYLL~MONTHC1~6e—1~a7)194-0.8m•+-1-0.im--—O.4mBOO8004002000—7’.—‘——74///S.S.+..-1-.+J JAS0NDJFMAMFigure10.Meansedimentchlorophyllaconcentrationatthree depthsvstime.20NPPamongmajorcomponentautotrophs.Inspring, NPPwasdominatedby epiphytesatsitesbetween0.3 and-0.2m elevation(Fig.1la).Assemblage NPPwasgreatestbetweenelevations0.1and -0.im.Z.marinaNPPwas greatestatthetwolowestelevations,andZ.japonicaNPPpeakedat0.6m.insummer,epiphyte NPPexceededseagrassproductivityonlyatthelowestelevation(Fig.1ib).GreatestNPPforZ.marinashiftedtohigherelevationsascomparedtospring.Incontrast,maximumNPPforZ.japonicashiftedtoalowerelevationascomparedtospring.NPPdeclinedatallsitesbetweenspringandsummerexceptat 0.5and-0.2m. NPPdeclinedtozeroatthetwohighestelevations(Z.japonicadominatedsites)insummer.AnnualNPPvariedwithdepth,withamaximumNPPat-0.lm(Fig.1lc).SeaweedNPPpredominated,onanannualbasis,atintermediateelevations.MaximumNPPbyZ.marinaandZ.japonicaoccurredat-0.2and0.5m elevations,respectively.MeanNPPbysedimentassociatedmicroflorawasnegativeduringallsamplingsandisnotpresented.Veryhighoxygendemand(unpublisheddata)associatedwiththesedimentsaccountedforthenegativevalues.TotalannualNPP estimatedfromthePadillaBayeelgrasssystem was10,557xl0~kgC(Table2).Ninety-sevenpercentofthisproductionoccursinthe Z.marinabedatelevationsbelow0.3m.Atotalof50%oftheproductioninthesystemwasattributedtoepiphytes. TheaverageannualNPPforthemacrophytecomponentofthesystemwas351gCm2(=924gdrywtm2).ProductiontoBiomassEpiphyteannualNPPtoaverageannualbiomassratiowasgreatestamongallcomponentsatallsitesexceptthehighesttwo(Table3).Thesehighvaluesareexplainedbytherelativelylowannualbiomassofepiphytesduetotheir markedlyseasonalappearance(Fig.8).TherewaslittlevariationinNPP:Bfortheseagrassspeciesoverthedepth gradient.Theturnoverratefortheentiresystem,calculatedbydividingtotalaverageannualNPP by totalaverageannualbiomass,was9.2.Thismeansthattheentirebiomassofthesystemwasreplacedapproximately9timesduringtheyearofstudy.Therelationshipbetween meanshootweight(regardlessofspecies)forthesamplinghavingthegreatestmeaneelgrassstandingstock(August)andannualNPPislinearforshootweightsuptoapproximately300mg(Fig.12).Highershootweightsappearedto21IaLia)>-ciIa14\LIa)>.ci\1a140-0.5C)ANNUALNPPFigure11.NPPvsdepth.A)April-June;B) July-August;C)AnnualNPP.A)NPPAPRIL—JUNE.-*—Z.JapanIcc-÷Z.martno--EpipHy~~Total54320—0.500.5DEPTHCm)9)NPPJULYAUO.—*—Z.Japonica.*Z.marina—-Epip~~yt—~—TatOl430—0.500.5DEPTHCm)•oo—W—Z.Joponica•4.Z.martno-—Epiphyt..—4.—Total400200O0.5DEPTHCm)22Table2.EstimateoftotalNPPintheeelgrass system.Averagesarefor12months.Totalintertidalarea=4176ha.TotalZosteraarea=72%ofintertidalarea=3007ha.TotalZ.japonicaarea=16%ofZosteraarea=481ha.TotalZ.marinaarea=84%ofZosteraarea=2526ha.AverageNPPAreaTotalNPPPercentComponentandDepth(gC/m2/yr)(ha)(xl0~kgC/yr)ofTotalZ.japonica(0.8to0.3m)44.74812152Epiphytes(0.8to0.3m)21.34811021Z.marina(0.3to -0.4m)199.72526504448Epiphytes(0.3to -0.4m)205.72526519649Total=1055723Table3.Averageannualbiomass(B),NPPandproductionto biomassratio(NPP:B)fortheprimaryproducersatthe studysites.PercentageoftotalNPPforeachsiteisgiveninparentheses.Averagebiomasswascalculatedona12monthbasisusinginterpolationformonthswithnodata.ZJ=Z.japonica;ZMZ.marina;E=epiphytes.DepthAverngeAnnual(m)BiornassNPPAnnual(grn2)(gdrywtrn-2)NPP:BZJZMBTot.ZJZMBTot.ZJZME0.82 00.22.215.800.816.67.9-4.0(95) (0)(5)0.62200.722.7138.900.5139.4 6.3-0.7(100) (0)(<1)0.54900.7 50.6230.0017.1247.14.7-353.0(93)(0)(7)0.32433865.085.5159.0206.1450.63.64.825.8(19)(35)(46)0.1093211140520.2746.81267.0-5.635.6(0)(41)(59)-0.10102131150698.41037.1 1735.5-6.879.8(0)(40)(60)-0.20115131280807.7271.11078.8-7.020.9(0)(75) (25)-0.40118151330440.6443.4884.0-3.729.6(0)(50)(50)24900*L600N\*U3)400*a.*0~zI<200I-*0F0.111111IIii1111111 1111111024881012CX100)ZOSTERAMEAN SHOOTWTCm9/h~~t)Figure12.EelgrassshootweightvsannualsystemNPP.ShootweightsaremeansfromsamplescollectedinAugust1986.25haveanegativeaffecton annualNPP.Shootweightispositivelyrelatedtoleafarea(Table1),andthe sitewiththegreatest meanshootweightwaslocatedatthelowest elevationsampled.ComparisonofMethodsLimitedcomparisonsofoxygenfluxdatawithshootmarkingandbiomasschangeestimatesofNPPshowedthatoxygenfluxresultedingreaterNPP valuesforbotheelgrassspeciesandepiphyticalgae.DailyNPPforZ.marina(at0.lmMLLW)estimatedbyoxygenfluxwas4.37and1.30timeshigherthantheestimatefromshootmarking inJuneandAugust,respectively.ForZ.japonica(at0.5mMLLW)inAugust,oxygenfluxproducedadailyNPPvaluethatwas3.66timesthat calculatedonthebasisofchangeinbiomass.Incomparison,totaldailyepiphyte NPP estimatedbyoxygenfluxat0.6mMLLWwas2.50timesthatestimatedbybiomass changeduringtheperiodofApril-June.Theratioofestimatesbasedonthetwomethodsat0.lmMLLWwas2.78duringthesameperiod.26DISCUSSIONPadillaBayisanexampleofanexpansiveshallowestuarineembaymentinwhichthebenthic environmentisdominatedbyadenseseagrasssystem.MyobservationsintheBayanddatafromotherresearch(T.Mumford,unpublished)indicate thattheresultsfromthepresentstudyareroughlyapplicabletothesystemingeneral.Thestudysitesspannedagradientinseagrassleafdimension, densityandplantbiomassandNPPthatcorrelatedwithdepth.PeakstandingstocksofZ.japonicaand Z.marinawerecenteredatabout0.5mandMLLW,respectively. ThedensitiesanddepthdistributionatPadillaBaywassimilartothat reportedforanexpansiveeelgrasssysteminRobertsBankinsouthernBritishColumbia(Harrison1982).Incontrast,theupperlimitofdepthdistributionofZ.marinainNetarts Bay,Oregon,wasmuchshallower.KentulaandMclntire(1986)sampledthatsystemat1.1to1.4mMLLW;anelevationrangethatspannedtheintertidalportionofthebed.The upperlimitofZ.marinaatPadillaBaywasabout0.3mMLLW(i.e.,0.8mdeeperthanatKentulaandMclntire’sdeepeststudysite).Apossibleexplanation ishighertemperatureson theflatsinPadillaBayduringlowtidesinsummer(Bulthius1987).Harrison(1982b)showedexperimentallythattheupwardlimitofdistributionofZ.marinaisregulatedbylowresistancetodesiccationincomparisontoZ.japonica,andthatZ.japonicacanoutcompeteZ.marinaforthisreasonatupperelevations.Kentula(1982)didnotreportZ.japonica fromNetartsBay,althoughitisknowntooccurinestuariesnorthandsouthofNetartsBay (Harrison1982b;Thom1984 andpersonalobservation).PondsformonPadillaBayflatsduringlowtides.Pondingwasmost evidentinsummerwhenstandingstocksofeelgrasswasgreatest,whichsuggeststhatthemassofplantmaterial functionsasaspongeininhibitingtherateatwhichtheflatsdrainduringebbingtides.Thedeepestsite(at-0.4m)wasunder0.3mofwaterevenduringextremelowtidesof-l.3mMLLW.Siteslocatedinareasofpondingatupperelevations(i.e0.3to0.6m)containedthedenseststandsofZ.japonica.Thesite(0.8m) thatwasdryatlowtidehadaverylowstandingstockofplantsinlatesummer;atimewhenNPPwasnegligible.Inwinter,whenstandingstockintheentiresystemwasthe least,verylittlepondingwasevident.This furthersupports the spongeeffecthypothesis.Ponclingwas notedby Harrison(1982a) onRobertsBank,KentulaandMclntire(1986)inNetartsBayandinEnglandby27Wyeretal.(1977).Theecological significanceofbiologicallymediatedpondingthatvariesseasonallymaybegreat,andrequiresstudy.Z.marinadensitychangedrelativelylittleseasonally,whereas thedensityofZ.japonicaexhibitedwidefluctuationsbetweenanearlysummermaximumtoamid winterminimumnearzero.SomeindividualsofZ.japonicawerepresentduring winter,andtheseweremostevidentatthesitesatthelowerendofitsdistribution.Thebiomassofbothspecieschangedwithseason.ThemostrapidincreaseoccurredbetweenAprilandJune,when NPPwasgreatest.Duringthistimelightenergyreachesmaximumandwatertemperatureisincreasingrapidlyintheregion.Lightenergyatnooninmid-June(i.e.,thetimeofthesummersolstice)canbeashighas4000p.Ern-2s1.Mid-winternoonvaluesarecommonly below100~iErn-2sd-.Severalpreviousstudies (Sand-Jensen1975,Jacobs1979,KentulaandMclntire1986,Dennison1987)haveconcludedthatlightenergywasanimportantfactorcontrollingshoot netproduction. TheexperimentalworkofDennisonandAlberte(1982) showedthatvariationsinlightintensityexhibitedsignificant controlofeelgrassphotosynthesis.Peakshoot biomassoccurredinJune-August,whichis thesameperiodasreportedforothernorthtemperatesystems(Phillips1972,Sand-Jensen1975,Wyeretal.1977, Jacobs 1979).Inaddition,peakshootdensitycoincidedwithpeakbiomass.In PadillaBay,seasonalbiomasspeaksvaried bydepth.Seasonalshiftsinthelocationofthesepeaksmayberelatedinitiallytohowlightenergyrequirementsaremetatthevariousdepths.Theincreaseinbiomass,especiallyevidentinZ.marina,was duelargelytoanincreaseinleafarea.Plantshadrelativelynarrowleavesinmid-winterandnoticeablywiderleavesinsummer.KentulaandMclntire(1986)andothershaveshownthatZ.marinaplantshavemoreandlargerleavesinspringandsummerascomparedtowinter.Thislatterconditionisinresponsetoincreasedlightenergyandphotosyntheticrate, andperhapsdecreasedleafexportrate,insummer.AnnualNPPinPadillaBaywas351gCm2wassimilartodatafromothertemperatesystems(seeZiemanandWetzel1980).However,theepiphyteswere responsiblefor50%oftheNPP,indicatingthatNPPbyeelgrasswas,onaverage,relativelylow(ca.175gCrn2).EpiphyteNPPhasbeennotedtobesignificant inmanyseagrasssystems.Typicalvaluesforepiphyteproductionarebetween7and58%(MorganandKitting1984).Thehigh relativeimportanceoftheseasonalappearanceofthehighlyproductiveepiphytetaxawithsubstantialturnoverratestoanimalsassociatedwithseagrasswasprovenbystable28carbonisotopedatainestuarinesystemsinHoodCanal,locatednearPadilla Bay(SimenstadandWissmar1985).Fry(1984),alsousingstablecarbonisotopes,showedthat algal epiphytesinaSyringodiumfihiformemeadowinFloridawerethedominantsourceofcarboninthatseagrassecosystem.LimitedexperimentsshowedthatcomparingNPPonthe basisofthetwomethodsemployedmustbe donewithcaution.Substantiallyhighervalueswere obtained usingoxygenfluxmethodsforeelgrass andepiphytesascomparedtovaluesobtainedusingbiomasschanges.Theaveragedifferencefactorforeelgrassduringthegrowingseasonwas3.11.Usingthis factor,theestimateforeelgrassannualNPPwouldbeincreasedfrom175to546gCm-2.TotalannualNPPforthesystemwouldbe722gCm-2,ofwhichepiphyticalgaewouldcomprise24%insteadof50%ofthetotal.Recently,theargumentsofZiemanandWetzel(1980)againsttheuseofmetabolictechniquesformeasuring NPPinrootedaquaticmacrophyteswasexaminedbyKempetal.(1986)usingPotamogetonperfoliatusL.They foundthattheprimaryreasonsgivenfornotusingmetabolictechniques(i.e.,problemsassociatedwiththe storage,recyclingandtranslocationofmetabolic02andC02)werenotsignificantsourcesoferror.Obviously,thesetypesofstudiesneedtobecarried outforeelgrassinordertobetterestimateeelgrasssystemproductivity.Epiphytebiomass,althoughsubstantiallyexceedingseagrassbiomassatsome sitesduringearlysummer,comprisedonly11%ofthetotalaverageannualbiomassinthesystem.ValuesreportedforseagrasssystemsinNewJersey(Penhale1977),NetartsBay(Kentula1982)andsouthTexas(MorganandKitting1984)were23,25 and47%,respectively.Greatesttotalsystem andepiphyteannual NPPwasrecordedat-0.lmdepth.Thissitewaslocatedinthecenterofasmallchannelthroughwhichwaterfromsurroundingflatsdrainedatduringebbingtides.Thissitealso had thegreatestepiphyteproductiontobiomassratiowithintheZ.marinaportionofthemeadow.Inotedonseveralvisitsthatwatercurrents wereswifterthroughthischannelascomparedtothesurroundingflats,andthatfloatingmatterwasrapidlyremoved.Basedonlimiteddatafromnearthesesites(unpublished)inorganicnitrogenconcentrationsarequitelowduringthegrowingseason.Itmaybethattherapidtransportofwaterpastthestudysiteinthechannelissupplyingtheplantsinthechannelwithaconstant,althoughlow,amountofinorganicnutrients.Thisrelativelyhighfluxofnutrientspasttheepiphyticalgaeandseagrassmayberesponsiblefor29therelativelyhighproductionratesthere(FonsecaandKenworthy1987).NitrogenwasshowntobelimitingtoZ.marinagrowthinChesapeakeBay(Orth1977).Inaddition,ShortandMcRoy(1984)haveshownthatZ.marinacanuptakeandutilizenutrientsthroughitsleaves.Further,therelativelyhigh currentratesinthechannelmayexplaintheloweraverageannualepiphyteandseagrassbiomassatthissite (Fonseca andKenworthy1987).Nutrientfluxratesareareknowntobeimportantwithregardtototalnutrientsupplyavailableto support algalgrowth(seereviewby Hanisak1983).Sedimentassociatedmicroalgae,asmeasuredbychlorophyllaconcentration, werepresent.Arapidincreaseinchlorophylladuringlatewinterandearlyspring,priortotheperiodofrapidmacrophyte growth,suggeststhat thesedimentmicrofloraisbetteradaptedforrapidgrowthduringthelowtemperaturesandlowerlightconditionsduringthelatewinter.Competitionfornutrients,andlight,andphotoinhibition,alongwithspeciessuccessionmaybefactorsslowingthegrowthofthisassemblageinsummer(MillsandWilkerson1986).HighsedimentassociatedoxygendemandresultedinlowornegativecalculationsofNPP.Thesedatasuggestthatgrossprimary productivity(GPP)forsedimentassociatedassemblagesmaybesubstantial,andasignificantsourceofcarbontothelocalsedimentfoodweb,andthatthesedimentsarehighlyheterotrophic.GPPinaZ.marinabedinChesapeakeBaybythesedimentwas225gCrn2onanannualbasis,whichaccountedfor14%oftheannualGPPofthebed(MurrayandWetzel1987).Incomparison,respirationmeasurementsmadeoneelgrassindicatethatrespirationislowrelativetoNPPduringthegrowingseason(unpublisheddata).Respirationratesofepiphyteson theseagrasswereusually<10%oftheNPPfortheseplants.RecentresearchinPadilla Bay(Thom,inpreparation)focusedon theproductiondynamicsofsedimentmicrofloraonmudflatsinPadilla Bay,andwillcoupletheworkfromseagrasssedimentproductionstudiesinevaluatingtheimportanceofthiscomponenttototal productionintheBay.ThevaluesforsedimentchlorophyllaconcentrationmeasuredinPadilaBaywereontheorderofthosereportedforNetartsBay(DavisandMclntire1983)andhigherthanthosereportedfortheColumbiaRiverestuary(MclntireandAmspoker(1986).Sedimentphysicalcharacteristics,andbiologicalandphysicalprocesseshaveastrongbutpoorlyunderstoodinfluenceonthebenthicmicroflora(DavisandMclntire1983).Meanshootweight,regardlessofeelgrassspecies,inJune(asanindicatorofleafarea)anddepthappearedtobegood predictorsofannualNPPforthesystem.OfsignificancewasthethresholdofannualNPPreachedatapproximately300mgdrywtshoot1anda30depthof-0.2m.HighershootweightsandincreaseddepthresultedinlowerNPP.Lightpenetrationmaybestexplainthisthresholdresponse(Dennison1987).ThepresentdatashowthatZ.japonicahasalowerannualNPPascomparedtoZ.marina,andexhibitsdifferentpatternsbyseasonintermsofdensitydistributionandgrowth.Theselatterdifferencesprobablyonly pointoutafewoftheecologicalconsequencesoftheinvasionoftheintroducedspecies.Ofnote isthefactthatZ.japonicaisverynewtotheareaingeologicalandevolutionarytimescales.Finally,atotalofapproximately28,000mtofdryplant matterwasproducedinPadillaBayseagrasssystemduringthe oneyearstudy.ValuesfromNetartsBayandGraysHarborwere3,200mt(KentulaandMclntire1986) and98,000mt(Thom1984),respectively. Althoughtheestuariesdifferinsize anddistributionofeelgrass,thesevaluesindicatethattheamountoforganicplantmatterproducedonanannualbasis andpotentiallyavailableforutilizationinestuarineand nearshoremarinesystemsissubstantial.31REFERENCESAsmus, H.and R.Asmus.1985.Theimportanceofgrazingfoodchainforenergyflowandproductioninthreeintertidalsandbottom communitiesofthenorthern WaddenSea.HelgolanderMeeresunters. 39:273-301.Buithius,D.A.1987.Effectsoftemperature onphotosynthesisandgrowthofseagrasses.Aquat.Bot. 27:27-40.Cassidy,P.M.andG.L. McKeen.1986.PadillaBaybaselinewaterqualityrecord.NOAATechnical ReportSeriesOCRWDMEM,U.S.Dept.ofCommerce,Washington,D.C.65pp.Davis,M.andC.D.Mclntire.1983.Effectsofphysicalgradientson theproductiondynamicsofsediment-associatedalgae.Mar.Ecol.Frog.Ser.13:103-114.Dennison,W.C.1987.Effectsoflightonseagrassphotosynthesis,growthanddepthdistribution.Aquat. Bot.27:15-26.Dennison,W.C.and R.S.Alberte.1982.PhotosyntheticresponsesofZosteramarina L.(eelgrass)toinsitumanipulationsoflightintensity.Oecologia(Ben.).55:137-144.Fonseca,M.S.andW.J. Kenwonthy.1987.Effectsofcurrentonphotosynthesisanddistributionofseagrasses.Aquat. Bot. 27:59-78.Fry,B.1984.‘3C/’2Cratiosand thetrophicimportanceofalgaein FloridaSyringodiumfil~formeseagrassmeadows.MarineBiology.79:11-19.Harrison,P.G.1976.ZosterajaponicaAschers.&Graebn.inBritishColumbia,Canada.Syesis.9:359-360.Harrison,P.G.1982a.Spatialandtemporalpatternsinabundanceoftwointertidalseagrasses,ZosteraamericanadenHartogandZosteramarinaL.AquaticBotany.12:305-320.Harrison,P.G. 1982b.ComparativegrowthofZosterajaponicaAschers.&Graebn.andZ.marinaL.under simulatedintertidalandsubtidalconditions.AquaticBotany.14:373-379.Hanisak,M.D.1983.Thenitrogenrelationshipsofmarinemacroalgae.Pages699-730InE.J.CarpenterandD.G.Capone(eds.),NitrogenintheMarineEnvironment.AcademicPress,NewYork.Heck,K.L.andT.A.Thoman.1984.ThenurseryroleofseagrassmeadowsintheupperandlowerreachesoftheChesapeakeBay.Estuaries7:70-92.Heijs,F.M.L.1985.TheseasonaldistributionandcommunitystructureoftheepiphyticalgaeonThalassiahemprichii(Ehrenb.) Aschers.fromPapauNewGuinea.AquaticBotany. 21:295-324.Jacobs,R.P.W.M.1979.Distributionandaspectsoftheproductionandbiomassofeelgrass,ZosteramarinaL.,atRoscoff,France.AquaticBotany.7:151-172.Kemp,W.M.,M.R.LewisandT.W.Jones.Comparisonofmethodsformeasuringproductionbythesubmersedmacrophyte,PotamgoetonpeifoliatusL.Limnol.Oceanogr.31:1322-1334.32Kentula,M.1982.Production dynamicsofaZosteramarina L.bedinNetartsBay,Oregon. Ph.D.Dissertation,OregonStateUniversity,Corvallis.158pp.Kentula,M.E.andC.D.Mclntire.1986.Theautoecologyandproductiondynamicsofeelgrass(ZosteramarinaL.) inNetartsBay,Oregon.Estuaries. 9:188-199.Littler,M.M.andArnold.1985.ElectrodesandChemicals.Chapter17,pages349-375J~M.M.LittlerandD.S.Littler(eds)HandbookofPhycologicalMethodsEcologicalFieldMethods.Macroalgae.CambridgeUniversityPress,NewYork.617pp.Mclntire,C.D.andM.C.Amspoker.1986.EffectsofsedimentpropertiesonbenthicprimaryproductionontheColumbiaRiverestuary.AquaticBotany.24:249-267.Mills,D.K.andM.Wilkerson.1986.Photosynthesisandlightinestuarinebenthicmicroalgae.BotanicaMarina.29:125-129.Morgan,M.D.andC.L.Kitting.1984.ProductivityandutilizationoftheseagrassHalodulewrightiianditsattachedepiphytes.Limnol.Oceanogr.29:1066-1076.Murray,L.andR.L.Wetzel.1987.Oxygenproductionandconsumptionassociatedwithmajorautotrophiccomponentsintwotemperateseagrasscommunities.Mar.Ecol.Prog.Ser.38:231-239.Orth,R.J. 1977.Effectofnutrientenrichmentongrowthofthe eelgrassZosteramarinainthe ChesapeakeBay,Virginia,USA.MarineBiology.44:187-194.Penhale,P.A.1977.Macrophyte-epiphytebiomassandproductivityinaneelgrass(ZosteramarinaL.)community.J.ExperimentalMar.Biol.Ecol.26:211-224.Phillips,R.C.1972.TheecologicallifehistoryofZosteramarinaL.(eelgrass)inPugetSound,Washington.Ph.D.Dissertation,UniversityofWashington,Seattle.Phillips,R.C.1984.TheecologyofeelgrassmeadowsinthePacificNorthwest:Acommunity profile.U.S.FishWildi.Serv.FWS/OBS-84/24.85pp.Sand-Jensen,K.1975.Biomass,netproductionandgrowthdynamicsinaneelgrass(ZosteramarinaL.)populationinVellerupVig,Denmark.Phelia.14:185-201.Short,F.T.andC.P.McRoy.1984.NitrogenuptakebyleavesandrootsoftheseagrassZosteramarinaL.BotanicaMarina.27:547-555.Simenstad,C.A.andR.C.Wissmar.1985.d13Cevidenceoftheoriginsand fatesoforganiccarboninestuarineandnearshorefoodwebs.Mar.Ecol.Prog.Ser.22:141-152.Stoner,A.W.1980.Theroleofseagrassbiomassintheorganizationofbenthicmacrofaunalassemblages.Bull,ofMarineScience.30:537-551.Strickland,J.D.H.andT.R.Parsons.1972.Apracticalhandbookofseawater analysis.Fish.Res.Bd.CanadaBull.167.3llpp.Thom,R.M.1984.PrimaryproductioninGraysHarborestuary,Washington.Bull.SouthernCaliforniaAcademySciences.83:99-105.Virnstein, R.W.andM.C.Curren.1986.Colonizationofartificialseagrassversustimeanddistancefromsource.Mar.Ecol.Prog.Ser.29:279-288.Westlake,DY.1963.Comparisonsofplantproductivity.Biol.Rev.38:385-425.~‘T~°A‘~N‘SS~1JJAJ~JJ~S~PU1~IJ1~9~X0l0?E1ssv.t8vdgfo~yooqpuvj—j‘(spa)~(ojoy~dDpu~sdijjnijcni~TcIT-L8S~ds~upu~spo~~~m:s~ss~i~~sUi~C1TAnonpOJJ0861pz1~~‘~y}Jput~~yf‘iwui~izLzz-cTv~TaInlJn3vnbykr~n1sQs~u~iJJ~J~nootpin~JOuor~nqu~sip~ipuos~tpnigLL6TSJ~1i~M)Jpui~UIini.iOO~~“AVU‘~PAdd9j~xa‘uoi~u~qsi~‘~at~mwoD~d~Usn‘vv~uJwaDos~u~guod~>j~°“J°~J~VVON-‘~~1‘T°I~t~U0~N‘~I~fflP~dJOsq~poojinu~o~iuoTu~aojos~i~jpu~su~.io~qiJoUO~T~UTPU9861 ~Y’d‘~A~