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MarinePollutionBulletin552007282 ID: 204391

MarinePollutionBulletin55(2007)282

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Correspondingauthor.Tel.:+441314552633;fax:+441314552291.E-mailaddress:p.tett@ichrachan.u-net.com(P.Tett).www.elsevier.com/locate/marpolbul MarinePollutionBulletin55(2007)282…297 ofthesemeasuresextendbeyondtheissuesofsewagetreat-mentandnitratefertilizeruse,toincludetheneedtocon-trolnutrientreleasebyagriculture,aquaculture,transportandurbandevelopmentingeneral.UKwatersconsideredtobeatriskfromeutrophicationhaveuntilrecentlybeenidenti“edmainlybymeasurementsofwinterconcentrationsofnitrateandphosphateandsum-merconcentrationsofphytoplanktonchlorophyll,whichwerecomparedwiththresholdssuchasthe10mgchlminsummerorthe12MwinterDissolvedAvailableInor-ganicNitrogen(DAIN)proposedbytheCSTT(1994)However,nutrientenrichmentandacceleratedalgalgrowtharenotinthemselvesharmful,andbecausethesebulkmea-surementsprovidelittleinformationontheextentofchangeinthebalanceoforganisms,theycannotadequatelyidentifyharmfulconsequencesofnutrientenrichment.TheUKDepartmentofEnvironment,FoodandRuralAairs(Defra)thereforecommissionedastudyaimedatproviding(i)ascienti“callybasedde“nitionofundesirabledisturbanceinthecontextofmarineeutrophicationand(ii)amonitor-ingstrategyfordetectingdisturbanceandunambiguouslydiagnosingeutrophication.Thispapersummarizesandupdatesthestudys“ndings,whicharereportedindetailAnon(2004)2.Thescienti“cbasis:atheoryofundesirabledisturbanceUndesirableDisturbanceStudyTeam(UDST)withUKmarineecosystemsfromanestuarineinnerlimitwherethe”oraandfaunaceasetohaveasubstantialmar-inecomponent,totheedgeofthecontinentalshelf.Theseecosystemsincludethoseinwhichthecharacteristicpri-maryproducersareseaweeds,seagrassesormicrophyto-benthosaswellasthosedominatedbyphytoplankton.UndesirableDisturbancewasde“nedasaperturbationofamarineecosystemthatappreciablydegradesthehealthorthreatensthesustainablehumanuseofthatecosystem.EcosystemisusedinthesenseofOdum(1959)meaninganyareaofnaturethatincludeslivingorganismsandnonlivingsubstancesinteractingtoproduceanexchangeofmaterialsbetweenthelivingandnonlivingpartsalthoughthisfactualde“nitionlacksthenormativeimpli-cationsassociatedwiththeideaofecosystemhealthAccordingtoCostanza(1992),ahealthyecosystem,likeahealthyhumanbody,isasystemthatfunctionswellandisabletoresistorrecoverfromdisturbance.Thisismorethanametaphor,becauseecosystemhealthhasquan-ti“ablecomponentsoforganizationresistancedisturbance,andresilienceMageauetal.,1995ofanecosystemliesinitsbiologicallymedi-ated”uxesofenergyandmaterialsaswellasitsabilitytorecoverfromdisturbancebymeansofrecolonizationandpopulationgrowth.Althoughtheseprocesses,andthefoodsupplyavailabletohigherlevelsinmarinefoodchains,dependonprimaryproduction,therelationshipbetweenproductionandecosystemhealthisnotlinear(Fig.1Exceedingamoderatesupplyoforganicmattercanresultinastateinwhicheukaryoticconsumersfailtodealeec-tivelywithorganicinput.Itis,however,notsomuchthesizeoftheinputastheuncouplingbetweenproductionandusethatcanleadtotheproblemsassociatedwitheutrophication:HarmfulAlgalBlooms(HABs);thespreadofopportunisticmacroalgae;andthedeoxygenationofdeepwaterorsedimentresultingfromthedeathanddecayofexcessbiomass.Theproblemstateisthatwhichisnowcommonlycalled,butsuchlabellinggoesagainsttheGreeketymology(nourishing,healthyLiddellandScott,1940))andoriginalmeaningoftheGermanscienti“ctermeutraphent Fig.1.Ecosystemhealthandundesirabledisturbance.Theprimarycomponentsofaregoodandoptimum.Theseliebehindtheecosystemsresistancetopressureanditsrecoveringfromdisturbance.Part(a)ofthisconceptualdiagramrelateshealthtovigourasthelatterincreaseswithnutrientenrichment;part(b)showstheresponseofstructuretopressure.Thetwopartsofthediagramshouldbereadtogethertounderstandwhytheprocessof(anthropogenic)eutrophicationisnowunderstoodtoimplyachangefortheworse:increasingpressurefromnutrientenrichmentmightovercomeecosystemresistanceandsoresultinaP.Tettetal./MarinePollutionBulletin55(2007)282…297 EcologicalQualityStandards(EQSs)toprovidethresholdstoundesirabledisturbance.Table2presentsEQSsintheformofEcologicalQualityObjectives(EcoQOs)whichrequireindicatorvaluestobewithinade“nedrangeunlesstheecosystemistobeconsidereddisturbed.Aswillbecon-sideredlater,theactualdiagnosisofundesirabledisturbancereliesontheaccumulationofevidence;atransgressionofasingleEcoQOwillrarelybeconclusive.3.1.BulkindicatorsChlorophyllconcentration,acommonmeasureofphyto-planktonbiomassandphotosyntheticpotential,ismuchusedasanindicatoroftrophicstatusinfreshwatersOECD,1982)andthesea(Paintingetal.,2005).However,assessmentofchangeshouldtakeseasonalvariationintoaccount,perhapsusingthemethodofcomparisonwithareferenceenvelopeshowninFig.2.Increasedchlorophyllconcentrationdecreasestransparencyandthusimpactsonthephytobenthosinshallowwaters.TransparencycanberoughlyestimatedfromSecchidepth,andithasbeenclaimedthatdecreasingSecchidepthtrackseutrophicationintheBaltic(Kratzeretal.,2003;SandenandHakansson,)).Opportunisticgreenandbrownseaweeds,withanannuallifecycle,canbeeasilydistinguishedfromperennialseaweedsandseagrasses,andtheircoverimpactsdirectlyonthenaturalfucoid,laminarianorseagrass”ora.Coverorbiomassofopportunisticseaweedshavethusbeenpro-posedbytheUKMarinePlantsTaskTeam(MPTT)asindicatorsofeutrophicationinshallowwaters.Acentury-longtime-seriesshowingdecreasingdeep-wateroxygenhasbeenusedasevidenceofeutrophicationintheBalticSea(FonseliusandValderrama,2003;JanssonandDahl-berg,1999),andregularmeasurementsofdissolvedoxygenshouldbemadebeneaththepycnoclineofpersistentlystrati“edwatersthatmightbeatriskfromnutrientenrichment.3.2.FrequencystatisticsHarmfulAlgalBlooms(HABs)arenaturalphenomenathatcanberenderedmorefrequentbynutrientenrichment,asexempli“edintheInlandSeaofJapan(Nakanishietal.,1992;Prakash,1987).However,thereismuchconfusionaboutwhattheyare.AlthoughtheacronymHABhasbecomewidelyused,someHABsarenotharmful,othersarenotalgal,andsomearenotsea-discolouringbloomsAndersonandGarrison,1997).Itisthususefultodistin- Table1(continuedEcohydrodynamicwatertypeSubcategoryandnotesthatcanbeusedtoshowdisturbance(seeTable2forEcoQOs);seemaintextforfurtherofthefollowingchangewithnutrientincreaserequiresfurtherstudyandcontributestoadiagnosisofeutrophicationwhenthereisevidenceofundesirabledisturbanceRegionsofFreshwaterIn”uence(ROFIs)withvariablebloomsofphytoplanktonSedimentandbenthoshighlyphysicallydisturbedbytidalandwind-wavestirring,andsobenthicindicatorsnotproposedIndicators4.1…4.4.sameasCorrelationssameasthosefor3.1…3.44.5Occurrenceormagnitudeofbloomsorbeach-foamIncreasingfrequencyormagnitude4.6.FrequencyandextentofanoxicsedimentordeathofmacrobenthosIncreasingfrequencyorextentRegionsofRestrictedExchangewherephytoplanktonabundancedependson”ushingSemi-enclosedtransitionalandcoastalwatersfallintothiscategory,forwhichitisnecessarytotakeaccountof”ushingrateaswellasopticalconditions.Insomefjords,halinestrati“cationmaypersistthroughoutyear,andthe”ushingofbasindeepbecomesanimportantissueTreatastype1…4ifappropriate,withfollowing(a)LargeRREsofEHDtype33.5.maybecome5.5:meanorpre-”ushingminimumoxygenconcentrationinbasindeepwaterDecreasingconcentration(b)SmallRREsofEHDtypes3or4:listofindicatorssimpli“edininterestsofcost-eectiveness,butoptionofusingmorecompletelistremainCouldusereducedlist,i.e.,3.1and3.2,plus5.5incaseofBasinDeepWaterIndicator3.1couldbereplacedby:MaximumsummerchlorophyllcalculatedbyCSTTmodel(Unlessthesystemislight-or”ushinglimited,maximumpredictedchlorophyllwillautomaticallyincreasewithnutrientloading)P.Tettetal./MarinePollutionBulletin55(2007)282…297 annualproduction,andthesuggestedbulkindicatorsinvolvingcoverofopportunisticalgaeseemsucient.Incontrastthebiomassofplanktonicalgaetypicallyturnsovereveryfewdays,andrepeatedmeasurementsareneededtoestimatetheirannualproduction.Thestateoftheartinthemeasurementofpelagicpro-ductionisdiscussedinarecentbook(Williamsetal.,).Techniquesincludefree-waterbudgetsofnutrientremovaloroxygenproduction,andtheuseofremotesens-ing,numericalmodelsandsophisticatedopto-electronics.Despitethedevelopmentofnewinstruments,coremethodsremainthoseinvolvingtheincubationofwatersamplescontainingphytoplankton,eitherinthesea,onthedeckofashipundernaturallightconditions,orinthelabora-toryundercontrolledillumination.Themethodinvolvesmeasuringtheincorporationoflabelledbicarbonateintoparticulateorganicmatter.Shortincubations(1…3)hoursarethoughttomea-grossprimaryproduction(GPP)„i.e.,thetotalorganicmattermadeduringphotosynthesis,beforeanyislosttorespiration.Inthelightanddarkbottleoxygenmethod,GPPcanbeestimatedfromthedierencebetweenthechangesinoxygenconcentrationintransparentandopa-quebottles.NetprimaryproductionisGPPlessrespirationandcanbeestimatedfromthechangeinoxygenovertimeinatransparentbottle.Becausewatersamplesalsoincludebacteriaandprotozoathatconsumeproductsofphotosyn-thesisanduseoxygen,whatismeasuredinsuchincuba-tionsisbestcallednetmicroplanktonproduction(NMP,shortenedfromthenetmicroplanktoncommunityproduc-WilliamsandRaine(1979).LongertermCincu-bations(eitherfromdawntoduskor24h),giveresultsthatarelessthanGPP(becausesomeoftheClabelisreturnedtothewaterbywayofalgalandmicrohetero-trophrespiration)butmorethanNMP.Resultsfromshortincubationscanbegraphedagainstirradiancetoobtaina(photosynthesis…irradiance)curveandvaluesofthephotosyntheticparametersthatde“nethecurve(JassbyandPlatt,1976;LedermanandTett,1981).Theparametervaluescanbeusedwithsolarradiation,watertransparencyandchlorophylldatatoesti-matehourlyanddailywatercolumnproductioninmgcar-bonmHermanandPlatt,1986).Theseestimatesthencanbescaleduptogiveanestimateofannualproduction.Thereisa“nalcomplication.Mucheuphoticzonepro-ductionisfuelledbyrecyclednitrogenexcretedbyzoo-planktonfeedingonphytoplankton(Dugdale,1967newproduction,supportedbynitrogen(mostlynitrate)introducedfromoutsidetheeuphoticzone,canbeexported(EppleyandPeterson,1979).Inthecontextofundesirabledisturbanceduetonutrientenrichment,onlythisfractionofproductionhasthepotentialtocausedis-turbance.Methodsexistfortheestimationofnewproduc-tionfromtheuptakeofisotopicallylabelednitrate,buttheirreliabilityinshelfseas,wheresomenitratemayberecycledandsomeammoniamaybenew,isunclear.Thealternativemethodofestimatingtheconsumptionofwin-ternitratealsohasdicultiesbecausethelinkbetweenNassimilationandorganiccarbonproductionisvariable.Itmaybethatonlymodelssoundlybasedinalgaltheorycanadequatelyestimatenewproductionincoastalwaters.Forthepresent,isinourviewbestindicatedbymea-surement-derivedestimatesofannualGPPandNMP.GPPcomesclosertotheideaofvigourasapotentialforgrowthandactivity,whereasNMPindicatespotentialforundesir-abledisturbance.Bearinginmindalltheseissues,wesuggestatwo-stepmethoddrawnfromseveralsources(GowenandBloom-“eld,1996;HermanandPlatt,1986;JointandPomroy,1993;Tettetal.,1988).Inthe“rststep,watersamplesareincubated(a)withunderalightgradient,for1…3h,tomeasurecarbon“xationand(b)indarknessfor24htoestimatemicroplanktonrespirationbyoxygenchange.Theresultsareusedtoestimatechlorophyll-relatedphotosyntheticandrespiratoryparameters.Inthesecondstep,theparametervaluesareusedwithverticalpro“lesofchlorophyllandsubmarinelight,takingaccountofdielchangesinsea-surfaceirradiance,toestimateeuphoticzoneGPPandNMP.Thesedailycolumnproductionvaluesareregresseduponeuphoticzonechlorophyllandtheregres-sionusedwithchlorophyllmapsobtainedduringrepeatedsurveystoestimateannualGPPandNMP.Suchregres-sionsexplainedupto70%ofthevarianceinproductionintheNorthSeaandIrishSea(GowenandBloom“eld,1996;JointandPomroy,1993).Improvementsinaccuracycouldbemadebyusingadditionalchlorophylldata(e.g.,fromremotesensingandmooredorship-mounted”uo-rometers)andbytakingaccountofday-to-dayvariationsinsea-surfaceandsubmarinelightusingaccessorymodels.Inthelongrun,thebestestimatesmightbeobtainedbyassimilatingbio-physicalmodelstoobservedchlorophyllandlocalproductivities.Finally,thereisevidence(PearsonandRosenberg,1978thatorganicenrichmentresultsinashallowingofthedepthoftheRedoxPotentialDiscontinuity(RPD)insoftsedi-ments,asbenthicorganismsconsumeoxygenfasterinrela-tiontoitsdiusionoritsbiologicalpumpingintothesediment.Thisaspectofvigour(withitspotentialforover-loadingthecapacityofasedimenttoassimilateorganicmatter)canbeestimatedbyRedoxprobesorbySedimentPro“leImaging(NilssonandRosenberg,19973.4.IndicatorsofecosystemstructuralhealthTheimpactoforganicmatteronthemacrobenthosoftemperateshelfseasiswellunderstood(PearsonandRosenberg,1978;Rosenberg,2001),andtoassesstheresultingchangeincommunitystructureincludetheInfaunalTrophicIndex(ITI)(Word,1990),andtheAZTIMarineBioticIndex(AMBI)(Borjaetal.,2000,2003aAlthoughAMBIhasbeenassessedagainstseveralsourcesofdisturbance(Borjaetal.,2003b),itandITImayproveinsensitivetothelow-level,widearea,organicenrichmentthatmaybeexpectedtooccurduringeutrophication.InP.Tettetal./MarinePollutionBulletin55(2007)282…297 anycase,itisthecommunitystructureoftheprimarypro-ducersthatholdsthekeytodiagnosingeutrophication,becausealgaeandcyanobacteriaprovidetheinitialresponsetonutrientenrichment.Itisthusunfortunatethatindicatortoolsforchangeinseaweedcommunitiesorthephytoplanktonarelessdevelopedthanthoseformacroben-thicchange.Inthecaseofseaweeds,themainindicatorsproposedbytheUKMPTTarethoseofbulkcoverbyopportunisticseaweeds.However,speciesrichnessandthebalancefunctionalformgroupsecologicalstatusgroupsOrfanidisetal.,2001)havealsobeenconsidered.Inthecaseoffreshwaterphytoplankton,shiftsfromdesmids,chrysophytesordiatomstocyanobacteriaareknowntobeassociatedwithnutrientenrichment(Hutchinson,1969;TallingandHeaney,1988).Incontrast,andexcept-ingtheBalticSea,whereblue…greenbacteriahaveincreasedwithnutrientenrichment(Finnietal.,2001themarinesituationislessclear.IncreasesintheratioofNtoSimaycauseincreasesintheproportionofnon-silic-i“edalgae(Gillbricht,1988;Tettetal.,2003b),andthishasledtoproposalsforindicatorsbasedontheratioofdia-tomstodino”agellates.Caremustbetakenintheuseofsimple,growth-season-averaged,ratiosofthissort,sincetheycanunderestimatetheeectofnutrientpressureonwell-stirredwaterswherediatoms,includingresuspendedbenthicdiatoms,arenaturaldominants.SettingEQSsfromsuchratiostendstore”ecttheviewthatdiatomsaregoodand”agellatesordino”agellatesarebad,whichmisunderstandsthemultiplerolesthateachgroupplaysinmarineecosystems.Forexample,dino”agellatelipidscanmakeimportantcontributionstothedietofcrustaceanzooplankton.Moregenerally,itisapparentthatthephyto-planktonencompassesawiderangeofbiochemical,taxo-nomicandfunctionaldiversity(Delwicheetal.,2004;JereyandVesk,1997;Tettetal.,2003b),anditseemsunwisetoignorethisdiversityinassessingthehealthoftheplankton.Itisalsodesirabletotakeintoaccountthenatural,especiallyseasonal,variabilitythatisanessentialpartofphytoplanktonecology.Toolsknowgenericallyas(marine)PhytoplanktonCommunityIndices(PCIs)arebeingdevelopedtosatisfytheserequirements.Allstartwiththeideaofde“ningeco-systemstateintermsofvaluesofstatevariables,whichcanbeplottedintoamultidimensionalstatevariablespace.Fig.3(a)illustratesthisintwodimensions,wheretheaxesarethestatevariables,.Theshadeddoughnutregionincludesallthosestatesoftheecosystemthatarenormalforthetype-speci“cconditions,takingaccountofseasonalandinterannual,variationandspatialpatchiness.Thesystemishealthywhileitsstateremainswithin,oriscapableofreturningrapidlyto,thedoughnut.Sustainedmovementawayfromthedoughnut,constitutesanunde-sirabledisturbance.Themaindicultyisthatofidentifyingstatevariables.Graphsinaphytoplanktonspeciesabundancespacecon-tainingdozensofdimensionswouldbetoocomplextobeuseful.Oneroutetosimpli“cationinvolvesempiricalmul-tivariateanalysistoextractafewkeydimensions(repre-sentinggroupsofregularlyco-occurringspecies)thatincludemostofthevariationincommunitycomposition.Asecondrouteinvolvestheuseoflifeformsbasedonfunctionandtaxonomy(Tettetal.,2003b).Thisroute y2 - state variable 2y1 - state variable 1 stippled region shows 'normal' domain 2 3 4 5 6 7 0 1 2 3 4 5 6 (log) dinoflagellates/Litre(lo g winterautumn Fig.3.Ecosystemstate.Part(a)isageneralizeddiagramshowingastate-spacede“nedbytwovariables;anormalorreferencedomainisshownbytheshareddoughnutregion,andadisturbanceisamovementoutsidethisregion.Part(b)providesaconcreteinstanceofastate-spacediagrambyplottingPortErinMarineLaboratorydatafromtheCyprisstationnearthecoastoftheIsleofManintheIrishSea.Thedataareinvertedmicroscopecountsofcellsineachcategory,averagedoveramonth.Resultsfrom10yearsofsampling(1995…2004)havebeenplotted,andanenvelopedrawntoinclude95%ofthepoints.Resultsfrom2005arealsoplotted,toshowhownewdatacanbeassessedagainstapreviouscondition.TheproposedPCIwillbebasedontheproportionofnewpointsoutsidetheenvelope,comparedwiththe5%expectation.P.Tettetal./MarinePollutionBulletin55(2007)282…297 oreutrophication.AnincreaseinthegreencolourdetectedbytheContinuousPlanktonRecordersurvey,whichwasat“rstinterpretedasevidenceofeutrophicationintheNorthSea,wassubsequentlyshowntobesowide-spreadthatclimatechangeisamorelikelyexplanationEdwardsetal.,2001).Thediatom:”agellatebalanceinshelfseasiscontrolledbyphysicalprocessesandselectivegrazingasmuchasbynutrientelementratios(Tettetal.,).AlthoughincreasesintheabundanceofPhaeo-spp.intheWaddenSeahavebeenassociatedwitheutrophication(andHegeman,1986),NorthSeapopulationshaveshownlong-term”uctuationswhichappearunrelatedtonutrientenrichment(GieskesandKraay,1977).Inthecaseofthephytobenthos,thereplace-mentofdominantwracksorseagrassesbyopportunisticgreenorbrownalgaecanoccurforavarietyofreasonsinadditiontoeutrophication(Fletcher,1996;MorandandBriand,1996Sofarasvigourisconcerned,ithasbeensuggestedthatalakeispollutedeutrophicifitsannualproductionexceeds350gCmRodhe,1969)andthatamarinewaterishypertrophicabove500gCmNixon,1995).Inrela-tiontoourownde“nitionsofproduction,itcanbearguedthatpelagicGPPprovidesthedesiredindicatorofeutrophi-cationbecauseitrespondsdirectlytonutrientenrichment.Ittakesaccountofecohydrodynamicconditionswhichdimin-ishlightforphotosynthesisorkeepbiomasslowbyhigh”ushing.However,itislikelytobeapoorpredictorofdisturbancebecauseofthesensitivityoforganicimpacttoecohydrodynamictypeandtheeciencyofcoupling.NPPmaybeabetterpredictoriftheargumentthatpelagicprotozoansarethemostimportantcontrolonbiomassformation(Tettetal.,2003a),iscorrect.Butotherpressures,suchastoxicpollution,mayharmtheprotozoancommunityandsoincreaseNPP,andinanycasewethinkitdesirablethatEcoQOsforNPParesetonthebasisofEHDtype.Thisisalsothecaseforproductionsproxy,chlorophyll.Thusweconcludethatthereappeartobenounambig-uousanduniversalindicatorsofdisturbanceduetomarineeutrophication,eitheramongstspecies,lifeforms,”uxesorbulkorfrequencyindicators,andhencenosingle,preciseEcoQOcanbeproposed.Instead,amulti-stepmethodisneededtodiagnoseundesirabledisturbanceduetoeutro-phication.Thestepsare:1.Identifyecohydrodynamictype,andthus,inprinciple,referenceconditions.2.Assessnutrientloadingandidentifywaterbodies/eco-systemswherethereispotentialforundesirabledistur-banceinthecontextofeutrophication,becausesuchwater-bodiesaresucientlywell-illuminatedtoallownutrienttobeconvertedintoprimaryproducerbiomass,”ushingissucientlylowtoallowbloomstodevelop,and,insomecases,strati“cationallowsorganicaccumu-lationandoxygenconsumptionindeepwater.3.Usethesimpler,bulkandfrequency,indicators,incom-parisonwithreferenceconditions,todetectatrendtowardsdisturbanceor,withreferencetoanEHD-type-speci“cEcoQO,tomakeaprovisionaldiagnosisofundesirabledisturbance. Good ate pressurestructural indicator nutrient loading vigourdisturbance nutrient loading oxygen 2) B Fig.5.Identifyingundesirabledisturbanceinthecontextofeutrophication.Thediagramassumesthatthewaterbodyandecosystemunderinvesti-gationisabletosuereutrophication,andthatnutrientenrichmentistheonlysigni“cantanthropogenicpressure:thehorizontalaxisin(c)islabelledpressuretoremindthereaderthattheremaybeothercausesofdisturbance.Part(d)isasuggestedmappingbetweentheecosystemhealthapproachtoundesirabledisturbanceandWFDAnnexVqualitycatego-ries.Inordertousethemethodology,speci“cmonitoringvariablesandEcoQOsneedtobeidenti“edforeachecohydrodynamicwatertype.Bulkindicators(exempli“edbychlorophyllanddissolvedoxygeninpart(a))andfrequencyindicatorsshouldberoutinelymonitored;productionmeasurements(partb)andindicatorsofstructure(partc)aremoreexpensive,andthearrowsAandBshowtheapplicationofstep5(measuringproductionandstructure)oftheproposedmonitoringstrategywhenconcernhasbeentriggeredbytrendsintheindicatorsofpart(a).TheverticalarrangementofthefourpartsshouldbereadassuggestingthatbreachofEcoQOsinpart(a)necessarilyimpliesbreachesinparts(b)and(c)orthatwaterbodyecologicalqualityin(d)hasnecessarilyfallenbelowWFDP.Tettetal./MarinePollutionBulletin55(2007)282…297 4.Usecorrelationbetween(adverse)trendsintheseindica-torsandinnutrients,aidedbypurpose-mademodelssuchasthatoftheUKCSTT(CSTT,1994,1997;Tettetal.,2003a;Paintingetal.,2006)torelatethetrendordiagnosistonutrientenrichment.5.Whenthereisasuchaprovisionaldiagnosis,andthecostsofreductioninnutrientloadingjustifyfurtherwork,monitorecosystemhealthbymeasurementofpri-maryproduction(indicatingvigour)andofcommunityandspeciesindicatorsofplanktonicandbenthicstructure.Step2isintendedtoincreasethereliabilityoftheOSPARscreeningprocedureforidentifyingpotentialprob-lemareas.Thealternativetostep5isofcoursetoapplytheprecautionaryprinciplefollowingtheprovisionaldiagnosisofsteps3…4,andtakestepstoreducenutrientloadingwith-outfurtherstudy.Weargueagainstthisasastrategybecausetheenrichedecosystemmayinfactbeinorclosetoanoptimumcondition,supportingmaximumbiomass,diversityand“sheriesyield.Fig.5summarizessteps3…5pictorially,andismeanttoimplythata“rmdiagnosisofundesirabledisturbanceduetoeutrophicationfollowsfromthefollowingcombinationofelements:ahighGPPthatcanbeshown(bycorrelationornumer-icalmodelling)toresult,inwholeorsubstantialpart,fromanthropogenicnutrientenrichment;NMPalargefractionofGPP,whichsuggestspoorpro-tozoancontrolofmicro-algalgrowthandhencethepotentialforexceptionalbloomsandexcessofsinking,potentiallyoxygen-consuming,organicmatterifcou-plingtomesozooplanktonormacrobenthosfails;markeddeviationsfromreferenceconditionsinbulkandfrequencyvariables,inparticularthosewhichareconsid-eredtobeparticularlyimportantforagivenEHDtype,suchasdeep-wateroxygenlevelsinstrati“edwaters;markedincreasesinabundanceofEHD-type-speci“cindicatororganisms,suchasPhaeocystisspp.,oroppor-tunisticseaweeds,whicharedeemedtorespondtonutri-entloading;asigni“cantdecreaseinthestructuralhealthofthepela-gicandbenthiccommunities,asshownbychangesinthevaluesofappropriatecommunityindicesanddecreasesintheabundanceorhealthofEHD-typespe-ci“cindicatororganismssuchasNephropsorsea-grasses.6.DiscussionandconclusionsTorecapitulate,thetheoryandmethodologysetoutherefortheidenti“cationofundesirabledisturbanceinthecontextofeutrophication,involve:theequationofundesirabledisturbancewithananthro-pogenicallycauseddeteriorationinecosystemhealthrecognizedinparticularbychangesincommunitystructurethemeasurementoftheprimaryproductioncomponentofecosystem(oritsproxies)inordertorelatedis-turbance(whichmayresultfromseveralpressures)spe-ci“callytonutrientenrichment;anecohydrodynamictypologywhich:distinguishesthedierentsensitivitiesandresponsesofecosystemstonutrientenrichmentandsoallowsappropriateindica-torstobeselected;andguidestheidenti“cationoftype-speci“creferenceconditionsforthepartofthemethodologywhichconcernschangefromtheseconditions.Attheheartoftheundesirabledisturbancetheoryistheinteractionbetweentheandthestructureofecosys-tems.Wehavesupposedthatoptimumvigourinecosys-temsmayoccurwhenorganicproductionisgreaterthanthatofanoligotrophicreferencecondition.Figs.1(b)and(c)showsastructuralindicatorchangingslightly,astheoptimumisapproached,fromitsvalueatthezero-pressureorreferencecondition.Beyondtheoptimum,excessofvig-ourleadstopolutrophy,andstructuredeteriorates:theeco-systemgoesoverthecli,eitherintoastatefromwhichrecoverymaybesloworintoanewstablestate.Itisthere-foreessentialthatamonitoringprogrammebeabletodetectatrendtowardsthecli,anditisforthisreasonthatmeasurementsofprimaryproductionare,inmanycases,essential.ThereisadierenceinourconceptualframeworkandthatoftheWFDinitsAnnexV.Thelatterseesallchangefromareferenceconditionasadegradationofecologicalquality,whereastheconceptofecosystemhealthimpliesthatsomechangemaybegoodifitistowardswhatwehavecalleda(nutrient-driven)optimum.Nevertheless,thetwoapproachescan,wethink,bereconciledFig.5(d)).WFDecologicalstatus,whichequateswithsmallchangesfromthereferencecondition,canbeequatedwiththesmallchangesfromreferenceconditionstructurewhichequateinourschemewiththeapproachtoanoptimumvigour,duringwhichtheecosystemremainswellwithinitsresistancetopressure-induceddisturbance.WeequatetheregioninFig.5(c)thatisclosetotheedgeofthestructuralcliwithWFDmoderatestatus:thatis,withasystemthatappearsonlylittlechangedbutisapproachingthelimitsofitsresistancetopressureFig.1(b)),andsocouldeasilybesentoverthecliintoadegradedstatewhichequateswithWFDquality.SomeoftheEcoQOsinTable2explicitlyequateanundesirablydisturbedstatewithWFDpoororbadThebasisoftheecohydrodynamictypologythatwehavepresentedhereiscompatiblebothinprincipleandpracticewiththatsuggestedbyOSPARsStrategy,whichtakesaccountofhydrodynamic/physicalfeaturesandotheraspectssuchaszooplanktongrazing,assupportingenviron-mentalfactors,overadomainthatextendsfromthepointoffreshwaterpenetrationatlowtidetotheouteredgeoftheP.Tettetal./MarinePollutionBulletin55(2007)282…297 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