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Environmentaltolerancesoffree-livingcorallinealgae(maerl):implications

Correspondingauthor.Tel.:+44-0-28-90-272265;fax:+44-0-28-90-E-mailaddress:c.maggs@qub.ac.uk(C.A.Maggs).Presentaddress:SchoolofBiologicalSciences,UniversityofWisconsin-Milwaukee,P.O.Box413,Milwaukee,WI

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Environmentaltolerancesoffree-livingcorallinealgae(maerl):implications




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Presentation on theme: "Environmentaltolerancesoffree-livingcorallinealgae(maerl):implications"— Presentation transcript:

Environmentaltolerancesoffree-livingcorallinealgae(maerl):implicationsforEuropeanmarineconservationSianWilson,CharmaineBlake,JohnA.Berges,ChristineA.MaggsSchoolofBiologyandBiochemistry,QueensUniversityBelfast,97LisburnRoad,BelfastBT97BL,NorthernIrelandReceived27June2003;receivedinrevisedform29January2004;accepted5March2004Maerlisageneraltermusedforloose-lyingsubtidalbedsofnodularcorallineredalgae.Maerlbedssupporthighassociatedinvertebrateandalgalbiodiversity,andaresubjecttoEuropeanandUKconservationlegislation.PreviousinvestigationshaveshownEuropeanmaerltobeecologicallyfragileduetogrowthratesofapproximately1mmperyear.However,theseveryslowgrowthrateshavehamperedattemptstodeterminethekeyecologicalrequirementsandsensitivitycharacteristicsoflivingmaerl.Inthisstudy,photosyntheticcapacitydeterminedbypulseamplitudemodulated(PAM)”uorometrywasusedasadiagnosticofstresscausedbyvariousenvironmentalconditions.Maerlspecieswereexposedtoarangeoftemperatures,salinitiesandlightlevelsandtoburial,fragmentation,desiccationandheavymetaltreatment.Maerlwasnotassusceptibleaspreviouslyassumedtoextremesofsalinity,temperatureandheavymetalpollution,butburial,especiallyin“neoranoxicsediments,waslethalorcausedsigni“cantstress.Thesedataindicatethatthemainanthropogenichazardforlivemaerlandtherichcommunitiesthatdependonthemissmotheringby“nesediment,suchasthatproducedbytrawlingormaerlextraction,fromsewagedischargesorshell“shand“shfarmwaste,andsedimentationresultingfromdisruptiontotidal”ow.2004ElsevierLtd.Allrightsreserved.Maerl;Pulseamplitudemodulated”uorometry;Temperature;Light;Salinity;Fragmentation;Burial;Metalcontamination;Conservation;Sewagedischarge;Fishfarmwaste1.Introduction1.1.MaerlbedsThetermmaerlreferstocalci“edmarinealgae(Rhodophyta,Corallinales)thatgrowunattachedandusuallylackarticulatedjoints.Maerl(Fig.1)canaccu-mulatetoformlargebedsofliveanddeadmaterialunderfavourableconditionsintemperateandtropicalwaters.Thebranchedtwig-likethallilocktogetherintoalatticewhichprovidesecologicalnichesforadiverserangeofseaweedandinvertebratespecies,someofwhichmaybecon“nedtothemaerlhabitat(Keegan,1974;Bosence,1976;Foster,2001;Stelleretal.,2003).Maerlhastraditionallybeenusedanasoilcondi-tioneronasmallscaleinGalicia(Spain),Brittany(France)andwesternIrelandandScotland,butmorerecentlyithasbeenindustriallyextractedbydredginginBrittany,Cornwall(England)andBantryBay,Ireland(GrallandHall-Spencer,2003).Legislationhasbeenproposedtominimizethedestructionofmaerlbeds(reviewedbyDonnanandMoore,2003).Twomaerl-formingspecies,Phymatolithoncalcareumandthamnioncorallioides,areincludedinAnnexVoftheECHabitatsDirective(CouncilDirective92/43/EEC),asspeciesofcommunityinterestwhosetakinginthewildandexploitationmaybesubjecttomanagementmea-sures.WithintheUK,maerlbiotopesareprotectedasakeyhabitatundertheJointNatureConservationCommitteesinterpretationoftheHabitatsDirective,inthecategorysandbanksslightlycoveredbyseawateratalltimes.TheUKBiodiversityActionPlan(BAP)in-cludesahabitatactionplanformaerlbeds(UKBiodi-versityGroup,1999).FouroftheUKscandidate Correspondingauthor.Tel.:+44-0-28-90-272265;fax:+44-0-28-90-E-mailaddress:c.maggs@qub.ac.uk(C.A.Maggs).Presentaddress:SchoolofBiologicalSciences,UniversityofWisconsin-Milwaukee,P.O.Box413,Milwaukee,WI53201,USA.0006-3207/$-seefrontmatter2004ElsevierLtd.Allrightsreserved.doi:10.1016/j.biocon.2004.03.001 BiologicalConservation120(2004)283…293www.elsevier.com/locate/biocon BIOLOGICALCONSERVATION marineSpecialAreasofConservation(SACs)includemaerlandone,theSoundofArisaig,wasdesignatedprimarilyforitsmaerlbeds.InFrance,maerloccursin14outof28Natura2000sitesproposedalongtheBretoncoast(GrallandHall-Spencer,2003).Maerlisconsideredanon-renewableresourceduetoitsveryslowgrowthrate,approximately1mm(0.5…1.5mm)peryear(BosenceandWilson,2003;BlakeandMaggs,2003),comparedtoharvestsofthousandsoftonnesperannuminBrittany(Briand,1991).ExtensivedeadmaerlbedsinAtlanticEuropeanwaterssuggestthatenvironmentalconditionsmaypreviouslyhavebeenmoresuitableformaerlgrowth.ThemostcommonandwidespreadspeciesinEurope,P.calcareum,isnever-thelessassumedtohavefairlynarrowecologicalre-quirements,judgedbyitsdistributioninrelationtocontrollingenvironmentalfactors(Bosence,1976).Al-thoughthemostsigni“cantthreatstothefunctionallydiverseandspecies-richinfaunalcommunitiesofmaerlbedshavebeenevaluated(Barberaetal.,2003;Hall-Spenceretal.,2003),ecologicalsensitiviesofthemaerlspeciesthemselvesareverypoorlyknownduetothedicultiesofworkingwiththeseslow-growingcalci“edalgae(Birkettetal.,1998).Livingmaerlisessentialtothesurvivalofmaerlbedsandtheirassociatedhighbiodiversity(Barberaetal.,2003),soitisimportanttounderstandtheenvironmentalfactorsthatpermitmaerlthallitosurviveandgrow.Theaimofthepresentstudywasto“llgapsintheunderstandingofkeyecologicalrequirementsandsen-sitivitycharacteristicsoflivingmaerlthatisneededforcompliancewiththeHabitatsDirective,tomeettheUKBAP,toinformconservationmanagementofSACsandfortheOsloandParisConvention(protectingthema-rineenvironmentofthenorth-eastAtlantic).Wereviewthemostimportantenvironmentalfactorsandpotentialthreatsin”uencingsurvivalandgrowthofmaerl.WepresentPulseAmplitudeModulated(PAM)”uorometrydataforphotosyntheticcapacity,aproxyforstresslevels,ofmaerlspeciesunderawiderangeoflaboratoryconditions.Finally,weevaluatetheimplicationsofthesedataformaerlbedconservationinEurope.1.2.Environmentaltolerancesofmaerl1.2.1.TemperatureTemperaturehaslongbeenknowntobetheprimarydeterminantofgeographicaldistribution,becausetheboundariesofbiogeographicalregionsareassociatedwithisotherms(Luning,1990).Maerlbiotopesoccurinawiderangeoftemperatureregimes,fromthetropicstonorthernNorway,butthespeciescompositionofthemaerlbedsisgreatlyin”uencedbytemperature.AdeyandAdey(1973)showedthatthedistributionofcoral-linealgalspeciesintheNorthAtlanticcouldbecorre-latedwithtemperature/habitatboundaries.Anobvioustemperature-relatedmaerlphenomenonintheUKistheabsenceofLithothamnioncorallioidesfromScotland,eitherbecausewintertemperaturesoccasionallydropbelowtheminimumsurvivaltemperatureofthisspecies(between2and5C)orbecausetemperaturesdonotremainhighenoughforlongenoughtosupportsu-cientannualgrowth(AdeyandMcKibbin,1970).Lab-oratorystudiesonSpanishmaerlshowedthatP.calcareumsurviveddownto2C,dyingat0.4C,andtheoptimumtemperatureforgrowthwas15C(AdeyandMcKibbin,1970).L.corallioideshadahigherminimumsurvivaltemperature,dyingat2Candsur-vivingwithoutgrowthat5C(AdeyandMcKibbin,1970).Temperatureappearstocon“neLithothamnionglacialetonorthernpartsoftheBritishIsles,possiblybecausereproductiveconceptaclesareonlyproducedinwinterwhenwatertemperaturesarebelow9C(Hall-Spencer,1994),althoughmaerlspeciesareknowntopropagatemainlybyfragmentation.1.2.2.SalinityMaerlbedswerepreviouslythoughttooccurwheresalinitywasdepressed(Joubin,1910),butalthoughthesurfacesalinityinthevicinityofmaerlbedsinFranceandIrelandisoftenlow,thebottomwaterisgenerallyfullysaline(Bosence,1976).KingandSchramm(1982)foundthatgrowthofP.calcareumisimpairedatsalin-itiesbelow24(practicalsalinityscale)whereasL.glac-ispresumedtobetolerantoflowsalinitiesbecauseitoccursinScottishsealochs(Connoretal.,1997).1.2.3.IrradianceIrradiancerequirementsofmaerlspeciesarenotknown(Birkettetal.,1998).Manycorallinealgaearelow-light-adapted.Thisholdsbothforjointed,erectspecies(Haderetal.,1996)andforcrustoseforms(Kuhletal.,2001;Robertsetal.,2002).Forexample,inthe Fig.1.ThalliofP.calcareummaerlfromStrangfordLough,NorthernIreland,labelledwithbeadsattachedby“shingline.S.Wilsonetal./BiologicalConservation120(2004)283…293 crustoseArcticspeciesPhymatolithonfoecundum,thecompensationirradiancewasonly1.6molpho-tonsm,andphotosyntheticsaturation,determinedusingPAMtechniques,wasatabout40molpho-tonsm(Kuhletal.,2001).Bycontrast,however,thetropicalreefspeciesHydrolithononkodessaturatingirradiancevaluesof200…600molpho-tonsm,dependingonthedegreeofphotoaccli-mation,andphotoinhibitionwasobservedonlyat1600molphotonsm(Payrietal.,2001).1.2.4.DesiccationBedscontaininglivethalliarefoundonlybelowas-tronomicallowwatermark,somaerlispresumedtobehighlysensitivetodesiccationandunabletowithstandemersion(Birkettetal.,1998).1.2.5.BurialandsedimentationWatermovementisakeyfactorconcerningthedis-tributionofmaerl.Extensivemaerlbedsarefoundinareaswheretherearemoderatetostrongseabedcur-rents,orinrelativelyopen,yetsheltered,areaswithsucientwaveaction,suchascoastalbaysorinlets(Bosence,1979).Ithasthereforebeensuggestedthatmaerlbedsrequirebothshelterfromwaveactiontopreventburialofthalliandenoughwatermovementtopreventsmotheringwithsilt(Hall-Spencer,1998).ScallopdredginginScotlandburiedmaerlupto8cmdeepandlateraplumeofsedimentsettledoutonthesubstratum(Hall-SpencerandMoore,2000).Dredgingreducedthenumberoflivemaerlthallibymorethan70%,withnosignofrecoveryafterfouryears.Com-mercialextractionofmaerllikewisereleases“neparti-clesthatsettleonthecommunitiescausingdegradation(DeGraveandWhitaker,1999;GrallandHall-Spencer,2003).Thelossoflivemaerlfollowingburialorsedi-mentationisthoughttoresultfromitsdeathduetolackoflightwhenburied(StellerandFoster,1995;Hall-SpencerandMoore,2000),butactualexperimentaldataarelacking.OrganicinputandheavymetalpollutionfromsewagedischargesinBrittanyhavereportedlyre-ducedthethicknessof,orentirelykilled,livemaerlcover(GrallandHall-Spencer,2003).1.2.6.FragmentationDemersal“shingpractices,suchasscallopdredging,cancrushtheopenlatticestructureofmaerlbeds,leavinglessinterstitialspace(Hall-SpencerandMoore,2000).IntheFirthofClyde,Scotland,maerlbedssub-jecttoscallopdredgingoverthepastcenturyconsistofsigni“cantlysmallerthallithanadjacentcontrolbeds(Hall-SpencerandMoore,2000).1.2.7.HeavymetalcontaminationTherehavebeennopreviousstudiesontheresponseofmaerltoheavymetalexposure;wearenotawareofanyexperimentsonothercorallinealgae.Elevatedconcentrationsofheavymetalsarequitecommoninmanycoastalhabitatswheremaerlisfound(CullinaneandWhelan,1982;Rainbowetal.,2002),andthuslikelytobearelevantenvironmentalstress.1.3.MeasurementofstressinmarinealgaeChlorophyll”uorescenceanalysishasbecomeoneofthemostpowerfulandwidelyusedtechniquesavailabletoplantphysiologists(MaxwellandJohnson,2000).PAMtechnologyisnowusedwidelyinstudiesofpho-tosyntheticratesinmarinealgae,particularlyforin-vestigationsofstressconditions(Haderetal.,1996;Beeretal.,2000;Parkhilletal.,2001;Kuhletal.,2001;Ivorraetal.,2002).Comparedwithtraditionalmeasurementsofphotosyntheticrates,itisanon-invasive,non-de-structivetechnique,soalthoughitonlyyieldsrelativephotosyntheticratesitiswidelyapplicableandversatile.Theprincipleofchlorophyll”uorescenceanalysisisthatlightenergyabsorbedbychlorophyllmoleculescanbeusedtodrivephotosynthesis(photochemistry),dissi-patedasheat(non-photochemicalquenching)orbere-emittedaslight(”uorescence)(Schreiberetal.,1986,1994).Thethreeprocessesoccurincompetitionwitheachother,sochlorophyll”uorescenceyieldsinforma-tionaboutchangesinphotochemistryandheatdissi-pation(MaxwellandJohnson,2000).TheoptimalquantumyieldofphotosystemII(PSII)istheratioofvariabletomaximal”uorescence(Thevariable”uorescence()representsthedierencebetweenthemaximal”uorescence(),whichisthe”uorescencefromthesamplewhenallPSIIreactioncentresarereduced(andthusactive),andtheinitial”uorescence(),whenallthePSIIreactioncentresareoxidized(orclosed)(BuchelandWilhelm,1993;Hanelt,1998;Gomezetal.,2001).Aratioofthevariabletomaximal”uorescencerepresentsthequantumeciencyofthatplant,whichcanthenbecomparedtootherreadings.Theratiocanbeusedtoevaluatere-ductionsinPSIIactivitycausedbystressessuchashightemperatureorbyphotoinhibition(Ludlow,1987;DemmigandBjorkman,1987;SchreiberandBigler,1987).Adecreaseinthevaluerepresentsare-ductioninthepotentialforadditionalphotochemistry.2.Materialsandmethods2.1.CollectionandacclimationofmaerlSamplesofcorallinealgaewereobtainedfromsub-tidallocationsinStrangfordLough,NorthernIreland,atleastfourweeksbeforetheiruseinexperiments.P.calcareumwascollectedatadepthof10…12mbySCUBAdivinginCastlewardBayon4October2001S.Wilsonetal./BiologicalConservation120(2004)283…293 and20May2002.L.glacialewascollectedonstonesat3…4mdepthatRaineyIslandon15June2002.Con-spicuousmacrofaunawasremoved.ThalliwerethenheldeitherinrunningseawateratambienttemperatureattheQueensUniversityMarineLaboratory,Porta-ferry(in2001),orin10litretanksofaeratedseawaterinaconstanttemperatureof9C,underaphotoperiodof16hlight:8hdark,ataphotonirradianceofca.13molphotonsm(in2002).TheseawaterwassourcedfromanintakeintheStrangfordLoughNar-rowsneartheMarineLaboratory,wheresalinityisap-proximately33atsitesmonitoredbyAgricultureandFoodSciencesNorthernIreland(AFSNI;http://www.afsni.ac.uk/services/coastalmonitoring/default.htmSeawaterwassand-“lteredandUV-treatedtoeliminatetoxinsandunicellularorganismsassociatedwithsea-water.Salinityandtemperatureweremonitoredregu-larlyandkeptconstant.P.calcareumwastestedunderallenvironmentalconditionsdescribedbelow.L.glaci-wasusedonlyinsalinityexperiments.2.2.Experimentalconditionsandprocedures2.2.1.TemperatureTheeectsoftemperatureonphotosyntheticcapacitywereinvestigatedintwosetsofexperiments.Alltreat-mentswereataphotoperiodof16hlight:8hdark,underaphotonirradianceofca.13molpho-tonsm.In2001,controlthalliweremaintainedatC,andtenthalliweretransferredto25Cfor5weeks.In2002,wefocussedoncomparingphotosyn-theticcapacityatrealisticwinter(9C)andsummer(17C)temperaturesdeterminedatsitesnearlocalP.cal-bedsmonitoredbyAFSNI.Temperaturewascontrolledconstantlyusingthermostats(Digitherm,Algarde,Pinxton,Nottinghamshire)and50Waquar-iumheaters(Eco-therm,Aquariumsystems,Padova,Italy),checkedregularlyandmonitoredwithmaximum-minimumthermometers.InitialPAMmeasurementsweretakenafteracclimationbutpriortothetreatments,andthereaftermeasurementsweremadeweeklyfor4or5weeks.Inshort-termexperimentscarriedoutat40PAMmeasurementsweremadeatthestartandevery15minupto90min.2.2.2.SalinityTanksweresetupatsalinitiesof3,15,33and40.Thereducedsalinityconditionswereobtainedbyaddingdistilledwatertothetankscontainingseawater,andincreasedsalinitywasobtainedbyaddingseasalttonormalseawater.Salinitywithinthetankswasmeasuredusingahand-heldrefractometercross-checkedwithaconductivitymeter.Theaeratedtanksweretightlysealedwithelectricaltape,andregularlymonitoredtopreventunwantedsalinitychanges.BothP.calcareumL.glacialeweresubjectedtosalinitytreatments.PAMwasmeasuredeveryhourforthe“rst12hineachsalinitycondition,andthereaftereveryweekfor5weeks.Resultswereevaluatedrelativetothecontrolcondition(salinityof33).2.2.3.IrradianceThreeirradianceconditionsweresetup:(1)completedarkness,(2)brightlightof140molphotonsm(16hlight:8hdark)and(3)controlambientlightofmolphotonsm(16hlight:8hdark).PAMmeasurementsweremadeafter12and48h,andthere-aftereveryweekfor5weeks.2.2.4.DesiccationFifteenthalliwereremovedfromholdingtanksandplaceduncoveredatroomtemperatureandambienthumidity.PAMmeasurementsweretakenafter5,10,15and30min,andat24h.2.2.5.BurialTreatmentsinvolvedburialofmaerlatthreedepthsinthreedierentsedimenttypes:(1)coarsecleanmaerlgravel(diameter1…10mm)collectedfromamaerlbeachatCarraroe,Co.Galway,Irelandandwashedcarefullyinseawaterbeforeuse;(2)coarsecleansand(diameter0.3…1.0mm;PlaySand,EarlyLearningCentre,Swin-don,England);and(3)muddysandfrombelowtheredoxlayer,blackincolourandsmellingofhydrogensulphide,collectedatDundrumBeach,Co.Down,NorthernIreland.Ineachconditionthereplicateswereallkeptinthesametankandthesedimentwasassumedtobehomogeneousincomposition.Groupsoftenthalliwerestrungonlineandtheirvaluesrecordedbeforeburial.Tenthalliwereplacedateachof0,4and8cmdepthsinseparatetanksofmaerlgravelandcleansand.Inthemuddysandtreatment,tenthalliwereplacedonthesurfaceandatdepthsof0.25and2cm.Tencontrolthalliforeachtreatmentwerekeptinseparatetankswithoutsedimentbecausethallionthesedimentsurfacebecamecoveredwitha“nelayerofsandduetoaerationofthewater.Maerlthalliwereburiedatthespeci“eddepthsforatotalof5weeks(2weeksforthemuddysandtreatment).Attheendofthetreatment,thalliwerecarefullyremovedandPAMmeasurementsweremade.2.2.6.FragmentationThetreatmentswere(1)breakingmaerlthalliinhalfor(2)breakingoonebranchfromathallus.OnlyonePAMmeasurementwasmadeoneachfragmentofthemaerlduetotheirsmallsize.PAMmeasurementsweretakenweeklyfor2weeks.2.2.7.HeavymetalcontaminationTreatmentsweresetupusingastandardmodeleuentsolution(Mellor,2002)in5litreglasscontainers.S.Wilsonetal./BiologicalConservation120(2004)283…293 Zn:Pb:Ni:Cu:Cdwereprovidedintheratio37:16:14:11:1,atarangeofconcentrationswithCdvaryingfrom0.174to174ppb.AtaconcentrationwithCdat1.74ppbthissolutionisconsideredtobethatofastandardindustrialeuent.TenthalliofP.calcareum,weighingapproxi-mately10g,wereexposedtoeachtreatment.PAMmeasurementsweretakendailyovera7-dayperiod.2.3.Pulseamplitudemodulated”uorometryAllmeasurementsweremadeinatemperature-controlledroomat9C,andmaerlwasdark-adaptedfor30minpriortomeasurement.Chlorophyll”uores-cencewasmeasuredwithaPAM-2000portablepulsemodulation”uorometer(HeinzWalz,Germany),at-tachedtoacomputerwhichdisplayedtheAdecreaseinvaluesindicatesareductioninthePSIIactivity;ifthisdecreaseisaresponsetoanenvi-ronmentalfactor,itcanbeassumedthatthisfactorhadanegativeeectonthephotosyntheticapparatusofthesample(Gentyetal.,1989).Changesintheeciencyofheatdissipationalsooccur(non-photochemicalquenching),inadditiontochangesineciencyofpho-tochemistry.Thesechangesarere”ectedasvariationwhichcannotbeinhibitedtotally,andallestimationsofnon-photochemicalquenchingarestrictlyrelativetosomedark-adaptedpoint.Thereforeadark-adaptedperiodwasdesignedintoPAMexperiments.The“breopticbundleofthePAMwasplacedonthesampleatananglesothealgawasnotshaded,andafterdarkadaptationPAMreadingweretakenimmediatelyinambientlight.Thelengthofthesaturatingpulseswas0.6s.Initialinvestigationsshowedthatthetipsofthethalligavemorerepeatablereadingsthanthecentresorbranchesofthethalli,presumablybecausethemoreevensurfaceformeasurementprovidesgreateraccuracy.Thereafter,readingswereobtainedonlyfromthetipareasofthethalli.Observationssuchaschangesinthecolourofthethalluswerealsonotedasthewererecorded.Anycolourchangescouldbeassociatedwiththelossofaccessorypigments,indicatinganega-tiveresponseinthephotosyntheticapparatusofthethallus.Foreachthallusthreemeasurementstakenondierenttipswereconsideredreplicates.Theemersiontimewasminimisedtoensurethatthevalueswerenotaectedbydesiccation,andthemeasurementonlylastedaround40s.2.4.StatisticalanalysisDatawereanalysedusingvariousstatisticaltests.TwowayAnalysisofVariance(ANOVA),incorporat-ingnormalitytests,wasperformedwithSigmaStat(forWindows,v2.03,SPSSInc.Chicago)toidentifysig-ni“cantdierencesinvaluesbetweenconditions.Signi“cancelevelofalltestswassetat05.Tukeystestwasusedformultiplecomparisonswithineachoftheconditions,toisolatethoseconditionsthatweresigni“cantlydierentfromeachother.Tukeystestde-terminesifthereisasigni“cantdierencebetweentworesultsbasedupondierencesintheleastsquaremeans.Errorbarspresentedarestandarderrors.3.Results3.1.PAMvaluesofcontrolsvaluesforcontrolsofabout0.50.1wereobtainedforbothmaerlspecies.Undertheseconditions,therewasgoodconsistencybetweenreplicatemeasure-ments,andbetween9Ccontrolsin2001and2002(Fig.2(a)).Ingeneral,asmorestressfulconditionswereapplied,variabilitybecamemuchgreater.3.2.Experimentaltreatments3.2.1.TemperatureP.calcareum,therewerenosigni“cantdierencesvaluesbetweenthe9CcontrolsandeithertheCor25Ctemperaturetreatmentsoverperiodsof4or5weeks.Therewasnosigni“cantchangeatanytemperatureoverthecourseoftheexperiments(Fig.2(a)).At40valuesdroppedsigni“cantlywithin15minandcontinuedtodeclineuntilat90minthemeanwas0.003,andthethalliwerejudgedtobedeadbycomparisonwithresultsofthedesiccationex-periment(Fig.3(b)).3.2.2.SalinityP.calcareum(Fig.2(b)),valuesat40psuwerenotsigni“cantlydierentfromthoseofthe33psucontrolsthroughouttheexperiment.At15psu,valuesdroppedsigni“cantlylowerthanthecontrolduringthe“rstweek,butthenrecoveredandwerenotsigni“cantlydierentfromthecontrolfromweek2onwards.Valuesforthe3psutreatmentshowedasigni“cantdropinvalueswithinthe“rstweek,asinthe15psutreatment,butfailedtorecover.Theyremainedsigni“cantlylowerthanthecontrolthrough-outtheexperiment,althoughallthalliremainedaliveduringthe5weekperiod,withanvalueofaboveL.glaciale(Fig.2(c)),thevaluesforthe3psutreatmentdroppedsteadilyforthe“rst3weeks,andweresigni“cantlylowerthanthoseofthecontrolfortheentire5-weekperiodoftheexperiment.AswithP.cal-,allthalliremainedalive.Noneoftheothertreatmentsshowedsigni“cantlydierentvaluesfromthecontroloverthe5-weekperiod,exceptforthe15psuconditionwhichproducedsigni“cantlylowervaluesthanthecontrolinweek5(Fig.2(c)).S.Wilsonetal./BiologicalConservation120(2004)283…293 3.2.3.IrradianceAt140molm(brightconditions)thevaluesforP.calcareumweresigni“cantlylowerthaninthecontrolafter24h,andtheycontinuedtodropthroughoutthe4-weekperiod.Thevaluesinthedarktreatmentweresigni“cantlylowerthanforthe13molmcontrolafter336h(2weeks),andremainedsigni“cantlyreducedforthedurationofthe4-weekex-periment(Fig.3(a)).Valuesforthedarktreatmentneverthelessweresigni“cantlyhigherthanforthebrightconditions.3.2.4.DesiccationTherewasasigni“cantdecreaseinthemeanvaluesoftheP.calcareummaerlwhenthethallihadbeenoutofwaterforlongerthan5min.Thevaluessteadilydeclinedovera30-minperiod(Fig.3(b)),toapointwherethethalliweredeterminedtobedead,becausenofurtherchangeoccurredwhenthedesiccationperiodwasextendedto24h(notshown;valueswere0.001…0.008).3.2.5.BurialvaluesofP.calcareumthallionthesurfaceandburiedatbothdepthsinboththegravelandsandconditionsweresigni“cantlylowerthanthoseofthesediment-freecontrols(001inallinstances)(Fig.4(c)).Inthegraveltreatments,after4weeksthere 0.10.20.30.40.50.6012345Fv/FmFv/Fm 0.1012345 0.00.10.20.30.40.50.6012345Fig.2.(a)…(c)Theeectoftemperatureandsalinityonphotosyntheticcapacityofmaerl.(a)TheeectoftemperatureonvaluesofP.calcareumgrowninaeratedtanks,ataphotoperiodof16hlight:8hdark,underaphotonirradianceofca.13molm.The25treatmentandits9Ccontrol,bothshownwithdashedlines,werecarriedoutin2001,andthe17Ctreatmentandits9Ccontrolin2002.Symbolsrepresent:diamonds,9Ccontrolfor17Ctreatment;squares,17Ctreatment;triangles,9Ccontrolfor25Ctreatment;,25Ctreatment.AllvaluesaremeansandSEsofthreePAMmeasurementsoneachoftenthalli.(b)Theeectofsalinity(dia-monds,3;opensquares,15;triangle,33;opencircles,40)onvaluesofP.calcareumgrownat9C,withotherconditionsasde-scribedpreviously.(c)Theeectofsalinity(diamonds,3;opensquares,15;triangle,33;opencircles,40)onvaluesofL.glacialegrownat9C,withotherconditionsasdescribedfor(a). 0.10.20.30.40.50.60100200300400500600700800 0.10.20.30.40.50.605101520253035Fig.3.(a)and(b)TheeectofirradianceanddesiccationtreatmentsonthephotosyntheticcapacityofP.calcareum.(a)Theeectofphotonirradiancelevelsoninmaerlgrownat9C,withotherconditionsasdescribedforFig.2a.Bright(diamonds)was140molm(16hlight:8hdark);control(squares)was13molm(16hlight:8hdark)asprovidedduringthepre-experi-mentalacclimationperiod,anddarktreatments(triangles)werekeptaeratedinthedark.(b)Theeectofdesiccationon(diamonds)ofP.calcareumremovedfromtanksandkeptuncoveredatroomtemperatureandambienthumidity.S.Wilsonetal./BiologicalConservation120(2004)283…293 wasnosigni“cantdierencebetweenthethallionthesurfaceofthesediment,whichhadbecomelightlycov-eredby“negravel,andthoseatdepthsof4and8cm.Inthesandtreatments,after4weekstherewasnosigni“-cantdierencebetweenthethalliatdepthsof4and8cm,butthallionthesurfaceofthesubstratumhadsigni“cantlyhigher.Allthalliinbothtreatmentsremainedalive.Inthemuddysandtreatments,afteroneweekthethalliburiedat2cmwereaverypalepinkwhilethethallionthesedimentsurfaceandthoseburiedunder0.25cmwereastrongerpink.Allthallihadbecomewhitebytheendofthesecondweek,whentheyweredeadasjudgedbyPAMvalues(Fig.4(c)).3.2.6.FragmentationFragmentationhadnosigni“canteectonmaerl(Fig.5).3.2.7.HeavymetalsAsigni“cantdecreaseincomparedtothecontrolwasobservedinalltreatmentsafter24,48and72h.Themostmarkeddropwasatthehighestmetalconcentrations(120mll).Recoverythenoccurred,andnoneofthevalueswassigni“cantlylowerthanthecontrolsafter1week(Fig.6). 0.10.20.30.40.50.6012345 0.10.20.30.40.50.6 0.00.10.20.30.40.50.6Fig.4.(a)…(c)TheeectonvaluesofP.calcareumofburialunderdierentconditions.(a)Theeectofburialatthreedepthsinmaerlgravel(diamonds,0cmdepthbutpartiallycoveredbygravelasaresultofwatermotioninthetanks;squares,4cm;triangles,8cm;)intanksat9C,withotherconditionsasdescribedinFig.2(a).Controlswerekeptinaseparatetank.(b)TheeectofburialatdierentdepthsincoarsecleansandontheP.calcareum(diamonds,0cmdepthbutpartiallycoveredbysandasaresultofwatermotioninthetanks;squares,4cm;triangles,8cm;controls,intanksat9C,withotherconditionsasdescribedinFig.2(a).Controlswerekeptinaseparatetank.(c)Theeectofburialinanoxicmuddysandatdepthsof0.25cm(opensquares),2cm(opentriangles),and0cmbutcoveredwithscatteredsedimentbythewatermotion(opendiamonds);allotherconditionsasdescribedforFig.2(a). 00.511.522.5Fig.5.Theeectoffragmentationofmaerlthalliintohalves(triangles,)orbybreakingobranches(twigs,squares)fromthalli(dia-monds)onthePhymatolithoncalcareum.AllotherconditionswereasdescribedforFig.2(a). 0.10.20.30.40.50.6050100150200Fig.6.Theeectofvariousconcentrationsofaheavymetalmodeleuent(expressedasmlofeuentperlitreofseawater:diamonds,control;squares,0.12;triangles,1.2;,12;star,120)upontheP.calcareumat9C;allotherconditionsasdescribedforFig.2(a).S.Wilsonetal./BiologicalConservation120(2004)283…293 4.Discussion4.1.EvaluationofphotosyntheticcapacityinmaerlusingTheoptimalquantumyielddiersbetweentaxa.Expectedforredalgaeisnormallyconsideredtobearound0.5…0.6(Dringetal.,1996),socontrolvaluesof0.6wereanticipated.However,ourcontrolresultsformaerlwereconsistentlyintherange0.4…0.5,evenwhenthallihadbeenverycarefullyprotectedfromexcessiveirradianceorotherstressandhadbeenacclimatedtocontrolledtemperatureconditionsforfourweeks.Itispossiblethatthecalcareousmatrixofmaerlaectsop-timumquantumyields,butthiswasnotinvestigatedfurthersincewewereinterestedonlyinthevaluesobtainedduringstresstreatmentscomparedtotheircontrols.4.2.Evaluationofphysiologicalstressinmaerlusing4.2.1.TemperaturePreviousstudiesoftemperatureeectsonmaerlhaveexaminedgrowthoverlongperiodsnecessitatedbytheslowrates.InP.calcareumtheoptimaltemperatureforgrowthwasinferredtobe12…13C(AdeyandMcKibbin,1970).Therapidlethaleectsofthe40treatmentshowhoweectivethePAMsystemisfordeterminingmaximumsurvivaltemperatures.Thedemonstrationherethatvaluesdidnotdierbetween9C(winter)and17C(summer)areinaccordwithourprevious“ndingsthattemperaturehadnodetectableeectonP.calcareumincomparisonsofgrowthratesat10,14and18C(BlakeandMaggs,2003).However,anacclimationperiodofupto5monthsmaybenecessaryaftertemperatureshifts(AdeyandMcKibbin,1970),soitispossiblethatchangesinoptimalquantumyieldwouldbedetectedafterlongerperiodsofacclimation.Theseasonalityofgrowthwillalsobein”uencedbydaylength,foul-ingandshadingbyotherspeciesinadditiontotemperature.Thelackofdetectablestressat25CindicatesthatP.calcareumtolerateshightemperaturesbetterthanmostsubtidalredalgaefromthetemperatezone,manyofwhichdieabove23C(Luning,1990;table7.1).P.calcareumiswidelydistributedinEurope,fromnorthernNorwaytonorthernSpainandtheMediter-ranean(IrvineandChamberlain,1994).Temperaturesurvivalresponsesarelikelytobemoresigni“cantneartheedgesofitsrange,butbiogeographiclimitsarenotsetbyrequirementsforreproductionasthisspeciesreproducesprincipallybyfragmentation(IrvineandChamberlain,1994).4.2.2.SalinityBothmaerlspeciesweretolerantofincreasedsalinityupto40psu,showingnodecreaseinphotosyntheticcapacity.Althoughmostsubtidalseaweedscansurviveupto50psu,andsometropicalcrustosecorallinealgaecangrowatevenhighersalinities(BarryandWoelker-ling,1995),photosyntheticratesdropslightlyabove30psu(Luning,1990;p.336).Thedierencebetweenthetwomaerlspeciesintheirresponsestodepressionofsalinitywascontrarytopre-dictionsbasedon“eldobservations(Birkettetal.,1998).WhereasithadpreviouslybeensuggestedthatL.glacialewasmorelikelytobetolerantoflowsalinitythanothermaerlspecies(Birkettetal.,1998),itwassigni“cantlylesstolerantofboththe3psuand15psuconditionsthanP.calcareum.Althoughthephotosyn-theticcapacityofP.calcareumwasdepressedinitiallyinbothlowsalinitytreatments,acclimationtocontrolvaluesoccurredat15psu.Thissalinityisatthelowerextremeoftolerancesobservedinothersubtidalalgaeuning,1990),andislowerthansalinitiespreviouslyseentoimpairgrowth(KingandSchramm,1982).Maerlbedsoftenoccurinthevicinityofestuaries(Joubin,1910)sotolerancetoreducedsalinitymayberequiredundersomehydrodynamicconditions.4.2.3.IrradianceThereductionintheabilityofP.calcareummaerltoperformadditionalphotochemistryunderhighirradi-anceconditionsshowsthatthisspecies,likemanyothercorallines,isadaptedtolowphotonirradiances.Crus-tosespeciessuchasPhymatolithonfoecundumPhymatolithontenueshowedeectiveadaptationtolowirradianceunderseaice(Kuhletal.,2001;Robertsetal.,2002).Variousnorth-westAtlanticcorallinealgaegrewbestunderlowirradianceconditionsof0.7…20molm(Johansen,1981).Theerectjointedcoral-CorallinamediterraneaJaniarubensarealsoadaptedtolowirradiancelevelsandHaderetal.(1996)showedthatphotosynthesiswasinhibitedbyexposuretoexcessiveradiation.Theextentofphotoinhibitioncanalsoberelatedtowhetherthealgahasexperiencedshadeorsunexposure(Payrietal.,2001),sotheprioracclimationofmaerltolowirradiancemayhaveaectedthedegreeofstressobserved.AlongerexperimentwouldberequiredtodeterminewhetherP.calcareumcanacclimatetohighirradiance.Maerlshowedlittlestressafterbeingkeptinthedarkfor4weeks.ThemaintenanceofoptimalquantumyieldsoveranextendedperiodofdarknesshasalsobeenobservedintheAntarcticredseaweedPalmariadecipi-ensduringa6-monthsimulatedwinterindarknessuderetal.,2002).valuesforP.decipiensmainedhighforthe“rst2monthsinthedarkbeforedroppingsuddenlyandthendecreasingmoregraduallytolessthan0.05.PhotosyntheticcapacityrecoveredveryS.Wilsonetal./BiologicalConservation120(2004)283…293 rapidlyfollowingilluminationinthearti“cialspringuderetal.,2002).Althoughweinvestigatedarela-tivelyshortdarkperiod,itisverylikelythatmaerlcansurviveseveralmonthsofdarknesswithoutdeleteriouseects.4.2.4.DesiccationIngeneralcorallinealgaearenottolerantofdesic-cationandrarelyoccurinareaswhichareexposedatlowtide(Johansen,1981).Expectationsthatmaerlwouldbeintolerantofdesiccationwereborneoutbyourexperiments.Theveryrapidlethaleectsofdesic-cationonmaerlmayberelatedtoitslowwatercontentandlackofaprotectivemucilagecoatingasfoundinmanyothermarinealgae4.2.5.BurialWeexaminedthallisubjectedtoperiodsofdarknessaswellastoburialincoarse,“neandorganic-richmuddysediment.Darknessaloneorburialincoarsesedimenthadlesssevereeectsonthealgaethanperiodsofburialin“nesediment.Inthe“nesediments,reduc-tionofwatermovementaroundthethalliprobablylimitsgaseousexchangewithdetrimentaleectsonthealgae.ChapmanandFletcher(2002)consideredthattheeectsonembryosofburialinsedimentsprobablyresultfromtheaccumulationofmetabolicproductsaroundthealgaeduetoreduceddiusion.Thesedataareconsistentwiththedistributionofmaerlbedsinareasofhighcurrentortidal”ow,suchasthemouthsofsea-lochs,orheadlands,wherethereisreducedsedi-mentation(Birkettetal.,1998).Burialbyashallowlayerofmuddysandcontaininghydrogensulphidewasquicklydetrimental,andevenmaerlonthesurfaceofthesedimentwasdeadwithintwoweeks.Sedimentchemistry,particularlythelevelofhydrogensulphide,hasrecentlybeenfoundtobepar-amountindeterminingthesurvivalofburiedFucusembryos(ChapmanandFletcher,2002).A1mmlayeroforganicallyrichbiodepositskilled90%ofFucusembryosevenwhentheoverlyingseawaterwasoxy-genated.Thetoxiceectsonmaerlof“neorganicsed-imentandassociatedhydrogensulphideexplaintheobserveddetrimentaleectsofCrepidulafornicataBrittany.FaecesandpseudofaecesproducedbyhighdensitiesoftheseinvasivegastropodshavedamagedBretonmaerlbeds(Chauvaudetal.,2000;GrallandHall-Spencer,2003).Similarly,sewageoutfallsandaquacultureraftsandcagescanalsoheavilyimpactmaerlbedsbysmotheringwithorganic-richdischarges,faecesandunused“shfood(GrallandHall-Spencer,Burialofmaerlthalliin“nesedimentbyscallopdredginghaspreviouslybeenidenti“edasaseverethreatintheFirthofClyde,Scotland,byHall-SpencerandMoore(2000).However,deathofburiedmaerlwasin-terpretedasresultingfromalackoflight(Hall-SpencerandMoore,2000),whereasourdataindicatethatitismorelikelytobeprimarilyduetootherphysicalandchemicaleectsofthesediment.4.2.6.FragmentationThishadnoeectonthephotosyntheticcapacityofmaerl,asexpectedbecausemaerlpropagationintheBritishIslesisprimarilybyfragmentation(IrvineandChamberlain,1994).Althoughtrawlingbreaksthemaerlthalli(Hall-SpencerandMoore,2000),sub-sequentdeathofmaerlismorelikelytobeduetore-ductionofwatermovementaroundthemaerlcausedbycompactionorsedimentation.4.2.7.HeavymetalcontaminationTherehavebeennopreviousstudiesonheavymetalcontaminationofmaerlorothercorallinealgae.Inthisclosedsystemexperimentthealgaeweresubjectedtoonedoseofpollutantsandmonitoredforaweekafter-wards.Atallconcentrationsthealgaewereinitiallynegativelyaected,butafteroneweektheyappearedtohaveassimilatedallthecontaminationandrecoverednormalphotosyntheticvalues.Recoveryisprobablyduetotheabsorptionofheavymetalsontothewallmatrixorsomeothernon-metaboliccomponentofthealgae.Sequestrationofmetalsbyalgaeisawell-knownphe-nomenon,withalgaebeingwidelyusedforbiomoni-toringandbioremediationofmetals(Hamdy,2000;StirkandVanStaden,2002).Metalsaretakenupbothpassivelyandactivelybyalgae(LobbanandHarrison,1994).Inthenaturalenvironment,however,thealgaemightbeaectedworsebychronicpollutionthanbyasingleevent.Thelowestconcentrationofeuentusedappearedtoincreasephotosynthesisofthethalliafteroneweek,suggestingthat,atthislevel,addedmetalshadsomenutritionalbene“t.5.ConclusionsWehaveshownthatPAM”uorometrycanbeusedasanon-invasive,rapid,repeatablemeasureofstresslevelsinmaerlcorallinealgae.Itisparticularlyusefulinthisgroupbecausegrowthratesofmaturethalliaresoslowastoprecludeshort-termexperimentsinvolvinggrowth.OurresultswillcontributetomeetingtherequirementoftheUKBAPtomakeprovisionby2005forthemaintenanceoftheextentandhealthofmaerlbedcommunitiesinmanagementplansforSACs(UKBiodiversityGroup,1999).Theselaboratorystudieshavecon“rmedthatP.cal-,themostabundantmaerlspeciesinEurope,isextremelyintolerantofdesiccation.Itisalsodeleteri-ouslyaectedbyhighirradiances.P.calcareumhowever,unexpectedlytolerantofrapidchangesinS.Wilsonetal./BiologicalConservation120(2004)283…293 salinity,beingbetterabletoacclimatetobothhighandverylowvaluesthanL.glaciale.ThephotosyntheticcapacityofP.calcareumwasmaintainedoverawidetemperaturerange,9…25C.Thisspecieswasnotaf-fectedbytreatmentwithahighdoseofsimulatedin-dustrialeuent,butthepresenceof“nesedimentwithahighorganicloadandhydrogensulphidecontentwasrapidlylethal.Thisinvestigationofawiderangeofthreatstomaerlhasdemonstratedthatthemainanthropogenichazardformaerlalgaeandtherichcommunitiesthatdependonthemissmotheringby“nesediment,producedbytrawlingormaerlextraction,orresultingfrombarrierstonormaltidal”ow,suchascausewaysandbarragesinWesternScotland(UKBiodiversityGroup,1999).Sewagedischarges,andshell“shand“n“shfarmwastearelikelytobeparticularlydamagingduetothein-creasedoxygendemand.Ourstudycon“rmstherec-ommendationintheHabitatActionPlanformaerlbeds(UKBiodiversityGroup,1999)thatcoastalzoneman-agementplansinvolvingmaerlbedsshouldfocusonpreventingactivitiesthatwouldcausetheirsmotheringoreutrophication.AcknowledgementsWethankProf.M.J.DringandDrM.P.Johnsonforadviceandassistancewithstatisticalanalysis.DrA.Mellorkindlyprovideduswiththesimulatedindustrialeuent.WearegratefultoS.VizeandG.Hinojosaforcollectingthemaerl,andtoJanetKforcommentsonthemanuscript.WeacknowledgestudentshipsfromtheDepartmentofEducationandLearning(forC.B.)andtheBritishPhycologicalSociety(forS.W.).ReferencesAdey,W.H.,Adey,P.J.,1973.StudiesofthebiosystematicsandecologyoftheepilithiccrustoseCorallinaceaeoftheBritishIsles.BritishPhycologicalJournal8,343…407.Adey,W.H.,McKibbin,D.L.,1970.StudiesonthemaerlspeciesPhymatolithoncalcareum(Pallas)nov.comb.andLithothamnionCrouanintheRiadeVigo.BotanicaMarina13,100…Barbera,C.,Bordehore,C.,Borg,J.A.,Glemarec,M.,Grall,J.,Hall-Spencer,J.M.,DelaHuz,C.,Lanfranco,E.,Lastra,M.,Moore,P.G.,Mora,J.,Pita,M.E.,Ramos-Espla,A.A.,Rizzo,M.,Sanchez-Mata,A.,Seva,A.,Schembri,P.J.,Valle,C.,2003.ConservationandmanagementofnortheastAtlanticandMedi-terraneanmaerlbeds.AquaticConservation…MarineandFresh-waterEcosystems13,S65…S76.Barry,G.C.,Woelkerling,W.J.,1995.Non-geniculatespeciesofCorallinaceae(Corallinales,Rhodophyta)inSharkBay,WesternAustralia…Biodiversity,salinitytolerancesandbiogeographicanities.BotanicaMarina38,135…149.Beer,S.,Larsson,C.,Poryan,O.,Axelsson,L.,2000.Photosyntheticratesof(Chlorophyta)measuredbypulseamplitudemodu-lated(PAM)”uorometry.EuropeanJournalofPhycology35,Birkett,D.A.,Maggs,C.,Dring,M.J.,1998.Maerl,vol.V.AnoverviewofdynamicandsensitivitycharacteristicsforconservationandmanagementofmarineSACs.ScottishAssociationforMarineScience.(UKMarineSACsProject),116pp.Blake,C.,Maggs,C.A.,2003.Comparativegrowthratesandinternalbandingperiodicityofmaerlspecies(Corallinales,Rhodophyta)fromnorthernEurope.Phycologia42,606…612.Bosence,D.W.J.,1976.EcologicalstudiesontwounattachedcorallinealgaefromwesternIreland.Palaeontology19,365…395.Bosence,D.W.J.,1979.Liveanddeadfaunasfromcorallinealgalgravels,Co.Galway.Palaeontology22,449…478.Bosence,D.,Wilson,J.,2003.Maerlgrowth,carbonateproductionratesandaccumulationratesinthenortheasternAtlantic.AquaticConservation:MarineandFreshwaterEcosystems13,Briand,X.,1991.SeaweedharvestinginEurope.In:Guiry,M.D.,Blunden,G.(Eds.),SeaweedResourcesinEurope.Wiley,Chich-ester,pp.259…308.Buchel,C.,Wilhelm,C.,1993.Invivoanalysisofslowchlorophyll”uorescenceinductionkineticsinalgae:progress,problemsandperspectives.PhotochemistryandPhotobiology58,137…148.Chapman,A.S.,Fletcher,R.L.,2002.DierentialeectsofsedimentsonsurvivalandgrowthofFucusserratusembryos(Fucales,Phaeophyceae).JournalofPhycology38,894…903.Chauvaud,L.,Jean,F.,Ragueneau,O.,Thouzeau,G.,2000.LongtermvariationoftheBayofBrest:benthic…pelagiccouplingrevisited.MarineEcologyProgressSeries200,35…48.Connor,D.W.,Brazier,D.P.,Hull,T.O.,Holt,R.H.F.,Northen,K.O.,Sanderson,W.G.,1997.MarineNatureConservationReview:marinebiotopeclassi“cationforBritainandIreland,vol.2.Sublittoralbiotopes.Version97.06.JNCCReportNo.230.JNCC,Peterborough.Cullinane,W.P.M.,Whelan,P.,1982.Copper,cadmiumandzincinseaweedsfromthesouthcoastofIreland.MarinePollutionBulletin13,205…208.DeGrave,S.,Whitaker,A.,1999.Benthiccommunityre-adjustmentfollowingdredgingofamuddy-maerlmatrix.MarinePollutionBulletin38,102…108.Demmig,B.,Bjorkman,O.,1987.Comparisonoftheeectofexcessivelightonchlorophyll”uorescence(77K)andphotonyieldofOevolutioninleavesofhigherplants.Planta171,171…184.Donnan,D.W.,Moore,P.G.,2003.Specialissue:InternationalWorkshoponTheconservationandmanagementofmaerl-23…27February,2001,UniversityMarineBiologicalStation,Millport,IsleofCumbrae,Scotland,Introduction.AquaticConservation…MarineAndFreshwaterEcosystems.Dring,M.J.,Wagner,A.,Boeskov,J.,Luning,K.,1996.SensitivityofintertidalandsubtidalredalgaetoUVBradiation,asmonitoredbychlorophyll”uorescencemeasurements:in”uenceofcollectiondepthandseason,andlengthofirradiation.EuropeanJournalofPhycology31,293…302.Foster,M.S.,2001.Rhodoliths:Betweenrocksandsoftplaces…Minireview.JournalofPhycology37,659…667.Genty,B.,Briantais,J.M.,Baker,N.R.,1989.Therelationshipbetweenthequantumyieldofphotosynthetice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