Polychaete/amphipod ratios: An approach to validating simple benthic indicators

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Polychaete/amphipod ratios: An approach to validating simple benthic indicators

Jean-Claude Dauvin, H. Andrade, J.A. De-La-Ossa-Carretero, Y.

Del-Pilar-Ruso, R. Riera

To cite this version:

Jean-Claude Dauvin, H. Andrade, J.A. De-La-Ossa-Carretero, Y. Del-Pilar-Ruso, R. Riera. Poly-

chaete/amphipod ratios: An approach to validating simple benthic indicators. Ecological Indicators,

Elsevier, 2016, 63, pp.89 - 99. �10.1016/j.ecolind.2015.11.055�. �hal-01537662�

ContentslistsavailableatScienceDirect

Ecological Indicators

jou rn al h om ep a g e :w w w . e l s e v i e r . c o m / l o c a t e / e c o l i n d

Polychaete/amphipod ratios: An approach to validating simple benthic indicators

J.C. Dauvin

, H. Andrade

, J.A. de-la-Ossa-Carretero

, Y. Del-Pilar-Ruso

, R. Riera

aNormandieUniversity,France

bUNICAEN,LaboratoireMorphodynamiqueContinentaleetCôtière,UMR6143M2C,24ruedesTilleuls,F-14000Caen,France

cCNRS,UMR6143M2C,24ruedesTilleuls,F-14000Caen,France

dAkvaplan-niva,FramCentreforClimateandtheEnvironment,9296Tromsø,Norway

eDepartmentofMarineSciencesandAppliedBiology,UniversityofAlicante,Ap99E-03080Alicante,Spain

fAtlanticEnvironmentalMarineCentre(CIMASL),SanCristobaldeLaLaguna,Spain

a r t i c l e i n f o

Articlehistory:

Received25August2015 Receivedinrevisedform 25November2015 Accepted28November2015 Availableonline22December2015

Keywords:

Polychaete/amphipodratio TaxonomicSufficiency Indicators

Oilspill Sewagepollution Brine

Aquaculturefarms

a b s t r a c t

Amongthemacro-invertebratesusedfortheassessmentofsoft-bottomcommunities,mostpolychaetes areclassifiedastolerant/opportunistictopollutionwhileamphipodsareconsideredassensitive.These taxahavebeenusedinseveralecologicalindices,suchasthesimpleabundanceratiobetweenPolychaeta andAmphipodaortheBenthicOpportunistAnnelidsAmphipods(BO2A)index,toassesstheEcological QualityStatus-EcoQs-ofsoft-bottomcommunities.IntermsofTaxonomicSufficiency(TS),thepoly- chaete/amphipodratio(i.e.attheleveloftheclass/order)hasbeenprovedtobeeffectiveinidentifying majorchangesinbenthiccommunitiesfollowingdisturbances.However,anunderlyingissueistoassess theacceptableTSlimitvalueneededtostateaccuratelythequalityofthebenthicenvironment.Wetested threeindicesusing18seriesofobservationscarriedoutinfivenorth-easternAtlanticandMediterranean zonesimpactedbyoilspills,oilandgasproduction,brineandurbansewage,harboursandaquaculture farmswithinimpactedandcontrolareas.SimilarresultstoBO2AwereobtainedwhenlimitingtheTS atthelevelofPolychaeteopportunisticfamilies,whichrequiredalowerdegreeoftaxonomicexpertise, andclassifyingallamphipodsassensitivetaxa.InsuchawaythattheEcoQsgivenbytheBPOFA(Benthic PolychaeteOpportunisticFamiliesAmphipods)wasverysimilartothosegivenbytheBO2A(Benthic OpportunisticAnnelidsAmphipods).

©2015ElsevierLtd.Allrightsreserved.

1. Introduction

The development of benthic biological indicators that were abletoidentifyenvironmentalstatusandpotentialanthropogenic impacts(Diazetal.,2004)hasrecentlyattractedmuchresearch effortinEurope.TheEuropeanWaterFrameworkDirective(WFD;

2000/60/EC) spurred the development of innovative ecological indicators(Devlinetal.,2007),mostlyforthequalityassessment ofsoft-bottommacrobenthiccommunities(seeBorjaetal.,2009;

Pintoetal.,2009;Martinez-Haroetal.,2015).In2008,theMarine

∗ Corresponding author at: Laboratoire Morphodynamique Continentale et Côtière, UMR 6143 M2C, 24 rue des Tilleuls, F-14000 Caen, France.

Tel.:+33231565722;fax:+33231565757.

E-mailaddresses:jean-claude.dauvin@unicaen.fr (J.C.Dauvin),hector.andrade@akvaplan.niva.no(H.Andrade),

ja.ossa@ua.es(J.A.de-la-Ossa-Carretero),yoana.delpilar@ua.es(Y.Del-Pilar-Ruso), rodrigo@cimacanarias.com(R.Riera).

StrategyFrameworkDirective(MSFD;2008/56/EC)reinforcedthe needtodevelopecologicalindicatorstoassesstheQualityStatus ofEuropeanmarinewaters(seeVanHoeyetal.,2010;Rombouts etal.,2013).Mostecologicalindicatorsarebasedonthelongestab- lishedprincipleoftolerant/sensitivespecies(i.e.speciesfavoured bypollution/speciesaffectedbypollution).Reish(1959)firstsug- gestedthisprincipleinthe1950s,whilePearsonandRosenberg (1978)establishedthisconceptintheirreviewoftheresponseof benthicspeciesandcommunitiestoorganicmatterenrichment.

Later,accordingtothePearsonandRosenberg(1978)paradigm, GlémarecandHily(1981)andGrallandGlémarec(1997)proposed classifyingmacrobenthicspeciesinfiveecologicalgroupsinterms ofdefiningsensitive/tolerant/proliferatingspeciesinresponseto organicmatterenrichment.Borjaetal.(2000)adoptedthesame representation of species proportions, arranged in five ecologi- calgroups, forcalculating theAZTIMarineBioticIndex(AMBI), whichwasdevelopedfortheEuropeanWaterFrameworkDirec- tive(WFD).Inthesameway,SimbouraandZenetos(2002)also proposedanewindex(BENTIX)developedfortheMediterranean http://dx.doi.org/10.1016/j.ecolind.2015.11.055

1470-160X/©2015ElsevierLtd.Allrightsreserved.

Sea.Thisindexwasbasedontherelativepercentagesofthreeeco- logicalgroupsofspeciesgroupedaccordingtotheirsensitivityor tolerancetodisturbancefactorsandweightedproportionatelyto obtainaformularenderingafivestepnumericalscaleofecological qualityclassification.

Amphipodsareanabundantcomponentoftheestuarineand marinesoft-bottomsand areknowntobesensitivetopolluted sediments;theydisappearedfrombenthiccommunitiesimpacted bypollutionand couldreappearwhen environmentalcondition recover(Réetal.,2009;de-la-Ossa-Carreteroetal.,2012a).Sim- ilartotheknownresponsesofbenthicspeciestoorganicmatter enrichment,other sources of pollution, suchas oil spills, have allowedresearcherstoobservethesensitivityortoleranceofben- thicspeciestohydrocarbonsinthewatercolumnand/orsediments (Gomez-GesteiraandDauvin,2000,Gomez-Gesteiraetal.,2003).

Crustaceans,especiallyamphipods,seemedtobeaffectedbylow levelsofhydrocarbons,whileotherspecies,suchaspolychaetes, were mostly tolerant to high levels of hydrocarbons (Gomez- Gesteira and Dauvin,2000; Gomez-Gesteira et al., 2003). Since hydrocarbonpollutionwassimilartoanorganicmatterincrease (i.e.availablecarbon),bothproducedthesameresultsinbenthic communities:theselectionandproliferationofasmallnumberof opportunisticspecies,suchasoligochaetesandpolychaetes,anda decreaseofsensitivespeciessuchasamphipods.Amphipodsensi- tivityhavebeenhighlightedbyseveralauthorssincethebeginning ofthe1980s(Bellan-Santini,1980)andcontinuedtobediscussed (Réet al.,2009;de-la-Ossa-Carreteroetal.,2012a).Thesestud- ieshaveledtothedevelopmentofbenthicqualityindicesbased ontheratioofsensitiveamphipodstootherfaunamainlycom- prisedofopportunisticpolychaetesorannelids(Gomez-Gesteira andDauvin,2000;DauvinandRuellet,2007,2009).Moreover,the amphipodabundancesandopportunisticcapitellids,ortheabun- danceof sensitivespeciescompared withtolerantspecies,have beenincludedin severalmultimetricapproaches suchas those usedfortheBenthicIndexofEnvironmentalConditionoftheGulf ofMexicoestuaries(Pontietal.,2009)ortheMacrobenthicIndex ofShelteredSystemsdevelopedbyLavesqueetal.(2009)forthe ZosteranolteibedsintheArcachonBasin(FrenchAtlanticcoast).

The indices BOPA (Benthic Opportunistic Polychaetes Amphipods; Dauvin and Ruellet, 2007) and BO2A (Benthic Opportunistic Annelids Amphipods; Dauvin and Ruellet, 2009) were obtainedas the log₁₀ of the ratio between opportunistic polychaetes (or annelids) and amphipod frequencies (i.e. the totalnumberofopportunisticpolychaetes(orannelids)andtotal numberofamphipodsdividedbytheoverallabundanceaccounted in a sample). Andrade and Renaud (2011) employed a general polychaete/amphipodratiotoassesstheimpactofoffshoreoiland gasproductiononbenthicfaunaalongtheNorwegiancontinental shelf. Theyfoundthat theratiobetweentolerant (polychaetes) and sensitive (amphipods) species decreased across a distance gradientfromtheproductionfacilitytothelessimpactedstations.

Toconsidera polychaete/amphipodratio(i.e.attheclass or orderlevel)asanindicatorofbenthosqualityintermsofTaxonomic Sufficiency(TS)(Ellis,1985), itis required:(1)anidentification levelhigherthanthespecies(i.e.genus,family,order,class),and (2)theuseofamphipodsandpolychaetesassurrogatesforben- thicassessments(Dauvinetal.,2003;Gomez-Gesteiraetal.,2003;

Terlizzietal.,2003;Bevilacquaetal.,2009;Tatarannietal.,2009;

Muscoetal.,2009,2011;Soares-Gomesetal.,2012;de-la-Ossa- Carreteroetal.,2012b;Aguado-Giménez etal.,2015).Although theTSwasoftenpresentedasbeingcost-effective(Tataranniand Lardicci,2010;AndradeandRenaud,2011;Dimitriouetal.,2012), manyauthorshavedisregardeditsusearguingthatuntilnow,no studieshavecompareddirectlytheTSlevelrequiredtoeffectively assessbenthicenvironmentalquality.Thegoalofthepresentstudy wastocomparetheeffectivenessofthreeindicesemployingTS,

theOpportunisticAnnelidsAmphipodsindex(BO2A)(Dauvinand Ruellet,2007,2009),theBenthicPolychaeteOpportunisticFamilies Amphipodsindex(BPOFA)andtheBenthicPolychaetesAmphipods index (BPA), todetect changes of environment quality in soft- bottomcommunities.Forthispurpose,weanalyseddatacollected atdifferentlocationsacrossalargelatitudinalgradientunderdiffer- entanthropogenicpressures.Thelocationsextendedfromcoastal zoneswithhighinputofcontinentalorganicmattertooffshore oligotrophiczonesinthenorth-easternAtlantic,includingtheNor- wegiancontinentalshelf,Brittany(NWFrance)andGalicia(NW Spain),aswellastheCanarianarchipelagoandthewesternbasinof theMediterraneanSea(Castellóncoast,NESpain).Anthropogenic pressuresincludedoilspills(BrittanyandGalicia),offshoreoiland gasproduction(Norway),urbansewage(Castellóncoast),fishcages andharbourconstruction,aswellasbrineandsewagedischarge (CanarianArchipelago).Theunderlyingissuewastoidentifythe limitofacceptableTStoassessaccuratelythequalityoftheben- thicenvironmentusingmacrofauna,i.e.polychaetes(orannelids) andamphipods.

2. Materialsandmethods

Datapreviouslycollectedduringdifferentsamplingcampaigns wereusedtotest thethreeindices. Atotal of18 selectedsites locatedalongalatitudinalgradientinthenorth-easternAtlantic Ocean and the western basin of the Mediterranean Sea was selected.

2.1. Studysites

Thedatacamefrom:

-Three oil and gas production fields (Ekofisk 2/4B&K (hereby Ekofisk),StatfjordAandHeidrun)locatedinthecontinentalshelf offNorway.Thesefieldsweresampledaspartofanenvironmen- talmonitoringprogrammefrom1990to2009.Thebenthicdata includesspeciesabundancescollectedevery3yearsalongadis- tancegradient,fromtheproductionfacilitytoreferencestations locatedatleast10,000maway.Abundancedataweregrouped infivedistancecategories(0−250m;250−500m;500−2000m;

2000−5000m,and>10,000mrespectively)[forfurtherinforma- tionseeAndradeandRenaud(2011)andreferencestherein].

-Twosites(RivièredeMorlaix,RMandPierreNoire,PN)froma longtermsurvey(1977−1996)intheBayofMorlaix(Brittany coastofwesternEnglishChannel,NWFrance)pollutedbyhydro- carbonscomingfromtheAmocoCadizwreckinApril1978[for furtherinformationseeDauvin(1998)andDauvin(2000)].

-Fivesitesfromtwodifferentsectors intheAres-BetanzosRía, Galicia,NWSpainsampledafterthespill oftheGreektanker AegeanSea(December1992−November1996)[forfurtherinfor- mationGomez-GesteiraandDauvin(2000,2005)].

-Four sitesat two distances fromthe discharge outfall(0 and 1000m)affectedbysewagedischargealongtheCastellóncoast (MediterraneanSea,NESpain)andsampledforfiveconsecutive summers(2004−2008)[forfurtherinformationseedelaOssa Carreteroet al.,2008; Del-Pilar-Ruso etal., 2009;de-la-Ossa- Carreteroetal.(2008,2009and2010)].

-Four sites from the Canarian Archipelago, being subjected to different anthropogenic disturbances: fish cages (Barranco Hondo,April2007−December2008),turbidityandsedimentload (Calero harbour,November 2004−June 2006), brine (LasBur- ras,May2008−January2009),brineandsewage(Tarajalillo,May 2008−January2009)[forfurtherinformationseeRieraandde-la- OssaCarretero(2013)].

2.2. Dataanalysis

Thethreeindicesweredefinedasfollows:

1)BO2A(BenthicOpportunisticAnnelidsAmphipods)(Dauvinand Ruellet,2009):

BO2A=log₁₀[ foa

fsa+1+1]

wherefoaisthefrequencyofopportunisticannelids(Clitellata andPolychaeta)(i.e.numberofopportunisticpolychaetescorre- spondingtotheEcologicalGroupsIVandVofGrallandGlémarec (1997)andusedforcalculatingAMBI(Borjaetal.,2000),plusthe OligochaetaandHirudinea,dividedbytheoverallabundancein asample),fsawasthesensitiveamphipodfrequency(i.e.num- berofamphipods,excludingtheopportunisticJassaamphipods, dividedbytheoverallabundanceinasample),andfoa+fsa≤1.

2)Anewindex,designatedasBPOFA(BenthicPolychaeteOppor- tunisticFamiliesAmphipods):

BPOFA=log₁₀[ fpof

fa+1+1]

wheref_pofwasthefrequencyofopportunisticpolychaetefam- ilies(i.e. Capitellidae,Cirratulidae,Dorvilleidae,Pectinariidae andSpionidae)andf_awasthefrequencyofallamphipodsinclud- ingJassa.ToobtainresultsthatwerecomparablewithBO2A,the BPOFAindexwascalculatedwiththesameequationofBO2A.

3)TheBPAaBenthicPolychaetesAmphipodsratio:

BPA=log₁₀[ fp

fa+1+1]

wherefpwasthepolychaetefrequency andfa istheamphi- podfrequency.Thisindexcorrespondedtotheratiobetween thepolychaeteabundanceinasampleandthetotalamphipod abundance;BPAindexwascalculatedwiththesameequation ofBO2A.

AsthecomputationofBO2Awasnotrecommendedforsamples containing≤20individuals(DauvinandRuellet,2009),thesame thresholdwasrequiredforBPOFAandBPA.AccordingtoDauvin andRuellet(2009)BOPAvalueswereintherangefrom0tolog₁₀ 2=0.301;thisrangewasalsoconsideredforBPOFAandBPA.

The stations for each locality were classified in two levels:

impactedandcontrolstations.ForthecontinentalshelfofNorway, impactedstationscorrespondedtostationsneartheproduction facility(<2000m),andcontrolstationstothestationslocatedat leastat5000mfromtheproductionfacility(AndradeandRenaud, 2011).For theBayofMorlaix,theRivièrede Morlaixstationin theinner partoftheBaycorrespondedtotheimpactedstation, whilethecontrolstationwasPierreNoire.InGalicia,theimpacted

Table1

ThresholdsforestablishingEcoQstatusbyeachindex.Values<0.025→HighStatus;

Values0.025−0.130→GoodStatus;Values0.130−0.199→ModeratedStatus;Values 0.199−0.255→PoorStatus,andValues>0.255→BadStatus.

BO2A BPOFA BPA

High-Good 0.025 0.031 0.135

Good-Moderate 0.130 0.126 0.211

Moderate-Bad 0.199 0.187 0.260

Poor-Bad 0.255 0.237 0.300

stationswerelocatedintheinnerpartofthería,whilethecontrol stationswereinthecentralzoneofthería.InCastellón(western Mediterranean),theimpactedstationscorrespondedtothestations nearthedischarges,whilecontrolstationswereat1000mfrom thedischarges.FinallyfortheCanarianArchipelago,theimpacted stationswherethoseaffectedbyhumanactivities,whilethecon- trolstationscorrespondedtostationsunaffectedbythesediverse humanactivities.

Ananalysisofvariance(ANOVA),withafixedfactorwiththis twolevels,impactand control,wasusedinordertotestdiffer- encesin thethree indices.PriortoANOVA,thehomogeneityof variance wastestedusing Barlett’stest. Dataweretransformed whenvariancesweresignificantlydifferent.Ifvarianceremained heterogeneous,untransformeddatawereanalysedsinceANOVA isrobusttoheterogeneityofvariances,particularlyforlargebal- ancedexperiments(Underwood,1997).Wesetamoreconservative significance level of 0.01 to reduce theprobability of a Type I error.

Pearson’scorrelation coefficientrwas usedtotest the rela- tionshipsbetweenthethreeindices(BO2A,BPOFAandBPA),i.e.

thecouplesBO2A-BPOFA,BO2A-BPAandBPOFA-BPA.Thelevelof agreementbetweentheindiceswillbedeterminedbythestrength of correlation(r=-1,1). Highervalues of rwill ledtoa higher agreement.Besides,thresholdshavebeenprovidedforestablish- ing EcologicalStatus of each site, which ledusto evaluatethe consequences of choosinganyof theseindices for assessingan impact.

Thresholds, presented by de-la-Ossa-Carretero and Dauvin (2010)forBO2A,wereusedforestablishingEcologicalStatusof eachsamplefromapristineecosystemstatetohighlydegraded state:high,good,moderate,poororbad(Table1).Thresholdsof BPOFAandBPAwereobtainedfromtheseBO2Athresholdsbya regressionusingthewholedataset(Table2).WeightedKappaanal- ysis(Cohen,1960;LandisandKosch,1977)wasusedtoevaluate theagreement,employingthemethodologyproposedbyBorjaetal.

(2007).TheequivalencetablefromMonserudandLeemans(1992) wasusedtoestablishthelevelofagreementofthetwoindices.In addition,sincetheimportanceofmisclassificationisnotthesame betweenclosecategories(e.g.betweenhighandgood,orpoorand bad)asbetweendistantcategories(e.g.betweenhighandmod- erate,orhighandbad),wechosetoapplyFleiss–Cohenweights (FleissandCohen,1973).

Table2

ResultsofANOVAforBPA,BPOFAandBO2Avaluesbetweenimpactandcontrolstationsforeachstudysite.Df:degreesoffreedom,F^p:Fratioandp-value.

Norway BayofMorlaix Galicia Castellón CanaryArchipelago

Df F^p Df F^p Df F^p Df F^p Df F^p

BPA IC 1 31.77^<0.001 1 127.5^<0.001 1 171.2^<0.001 1 29.16^<0.001 1 64.48^<0.001

Res 267 38 54 38 175

BPOFA IC 1 67.13^<0.001 1 76.12^<0.001 1 0.033^0.875 1 15.69^<0.001 1 28.85^<0.001

Res 267 38 54 38 175

BO2A IC 1 75.48^<0.001 1 73.13^<0.001 1 0.8161^0.358 1 15.59^<0.001 1 1.341^0.248

Res 267 38 54 38 175

3. Results

3.1. Valuesoftheindicesincontrolandimpactedstations

Impactedstationspresentedhigherindicesvaluesthancontrol stationsformostofthesites,i.e.lowerecologicalstatus(Fig.1).

Inacomparableway,thevaluesofBPAwerehigherthanthoseof

thetwootherindicesBPOFAandBO2Awhichshowedverysimilar valueswiththepointsoftensuperposed(Fig.2),inparticularfor theBayofMorlaix,GaliciaandCastellóncoastsites.

For the continental shelf Norway, the three indices showed similarpatternsinsucha waythatsignificantdifferenceswere detectedbetweenimpactandcontrolstations(Table2).Theywere higheratimpactedstationsclosertotheproductionfacilitythan

Fig.1.Polychaete/Amphipodratiosvaluesforeachlocality.Stationsweregroupedinimpactandcontrol.ContinentalshelfofNorway,Impact:stationsat<2000mfromthe productionfacility,Control:stationsatleast5000mfromthenearestproductionfacility.BayofMorlaix,Impact:RivieredeMorlaixstation,Control:PierreNoirestation.

Galicia,Impact:stationsintheinnerpartofthería.Control:stationsinthecentralzoneofthería.CastellónCoast.Impact:stationsat0mfromthedischargeControl:stations at1000mfromthedischarge.CanarianArchipelago:Impact:impactedstations,Control:controlstations.

Fig.2. ScatterplotsbetweenpairofvaluesofeachPolychaete/Amphipodratios.

stationsdistanttothem. FortheEkofiskfield,BO2AandBPOFA indicesshowedclearer trendswhencomparedwithBPAvalues, which,in2005,showedamaximum(Fig.1).In1996,theBPOFA andBPAindicesshowedapeakintheimpactedstations.Forthe Heidrunfield,thethreeindicesshowedgenerallythesamepat- ternofdecrease towardsvaluesof thecontrolstation.In1997, theBPAindexshowedapeak.By2009,thethreeindices atthe impactedstationshadreachedsimilarvaluestothosefoundatthe controlstations.FortheStatfjordAfield,BPAremainedhighobtain- ingalesscleartemporalpatternwhilstBO2AandBPOFAshowed aclearerdecreasingtrendsince1999.Thenumberofamphipods usedtocalculatethethreedifferentindicesforHeidrunandStat- fjordAremainedconstantsincenotolerantspecieswererecorded inthesesites.ForEkofisk,fewtolerantamphipodswererecorded (genusJassa,n=14outof1033).Differencesinthesesitescanbe thereforebeprimarilyascribedtothenumbersofpolychaetesused intheindexcomputations.

IntheBayofMorlaix,bothBO2AandBPOFAindicesshowed similartemporalpatterns,withhighervaluesandvariabilityatthe impactedRMstationthanatthecontrolPNstation(Fig.1).Signif- icantdifferenceswerealsodetectedbetweenimpactandcontrol

stationsforthethreeindicesinthissite(Table2).Atthecontrol site,therewasalargeincreaseoftheindicesinparticularBPAat thebeginningofthesurvey,andlatelyageneraltrendtodecreasing values.TheBPAindexremainedveryhighthroughoutthesurvey periodintheRMimpactedstation.

InGalicia,bothBO2AandBPOFAshowedsimilarpatternswith fluctuatingpeaks,whichdidnotfollowadistincttemporaltrend.

Therewasnoindicationoftheimpactofthe‘AegeanSea’oilspill andthetemporalchanges weresynchronous,withoutanyclear differencesbetweenimpactedandcontrolstations(Fig.1,Table2).

Thevaluesofbothindicesremainedrelativelylow(<0.15).How- ever,significantdifferencesweredetectedinBPAindexbetween impactandcontrolstations,withhighervaluesinimpactedsta- tions. This index showed a general decrease at the impacted stationsfromthepeaksofJune1993toJune1995whilstvalues incontrolstationsweremorestable,rangingfrom0.15to0.20.

OntheCastellóncoast,thethreeindicesshowedaclearresponse to the discharge, with lower values in control stations than impactedsitesclosertothesewagedischarge,whereamphipod abundancedecreasedandpolychaeteabundanceincreased(Fig.1, Table 2).AtBenicarló, there wasa greater differenceof values betweenimpactedandcontrolstation,especiallyin2007and2008.

MarkeddifferencesfortheBPAindexwereobservedinotherloca- tions,suchasPe ˜níscola(2006)orAlcocebre(2007).

IntheCanarianArchipelago,thethreeindicesshowedverylow valuesincludingahighnumberofzeroresultsduetotheabsence ofopportunisticspecies.Significantdifferencesweredetectedin BPAand BPOFAbetweencontrol andimpactstations (Table2).

ThesedifferencesweremorenoticeableinCaleroHarbour,whilean increasecouldbeidentifiedattheLasBurrasdesalinationplantsite (Fig.1).AttheBarrancoHondofishcages,BPOFAandBO2Aindices showedverylowvalues.Highervalueswereobservedmainlyatthe impactedstations,withmaximumvaluesattainedinApril2007and December2008.

3.2. Relationshipsbetweenthethreeindices

ThePearsoncoefficientsbetweenthethreeindicesshowedsig- nificantcorrelationsatmostofthesites(Table3).Exceptforthe Canarianarchipelagodataset,wherethemajorityofthePearson coefficient values between pairs of indices were low and non- significant(threeoutof15possible).Nevertheless,thestrength ofthesesignificantcorrelationsvariedbetweenindices.Thecor- relationsbetweenBPAandbothotherindiceswereweakerthan

Table3

Pearsoncoefficientvaluesbetweencouplesofindicesforeachareaandsite.Inbold, thenon-significancelevel(p>0.05).

BO2A/BPOFA BO2A/BPA BPOFA/BPA

Norway Total 0.960 0.490 0.483

Ekofisk2/4B&K 0.932 0.322 0.346

Heidrun 0.974 0.698 0.690

Statfjord 0.978 0.670 0.689

BayofMorlaix Total 0.998 0.798 0.811

PierreNoire 0.998 0.795 0.812

RivièredeMorlaix 0.996 0.513 0.51

Galicia Total 0.952 0.337 0.281

Innerpart 0.982 0.355 0.336

Centralpart 0.937 0.489 0.577

Castellón Total 1.000 0.844 0.845

0m 1.000 0.857 0.859

1000m 0.997 0.679 0.677

Canary Archipelago

Total 0.390 0.216 0.365

BarrancoHondo 0.073 0.640 0.118

LasBurras 0.448 0.330 0.971

CaleroHarbour 0.467 0.398 0.481

Tarajalillo 0.469 0.136 0.692

thosebetweenBO2AandBPOFA(Table3).Scatterplotsallowed foravisualinspectionoftherelationsbetweenpairsofvaluesof thethreeindices(Fig.2).TherelationbetweenBO2AandBPOFA waslinear,showingthatthereisahighagreementbetweenboth indices.TherelationbetweenBPAandtheotherindiceswasless clearwithahighdispersionofvaluesbetweenBO2AandBPAand betweenBPOFAandBPA(Fig.2).

3.3. Ecologicalstatus

TheFig.3givesthedistributioninpercentageofeachEcoQSta- tus(EcoQS)ofeachsiteforimpactandcontrolstations.

BO2AandBPOFAclassifiedcontrolstationsashighandgood status,exceptinCanarianArchipelagowhere7%ofcontrolstations wereclassifiedasmoderate,poororbadbyBPOFA.Bothindices tendedtoassignedworseEcoQstoahigherpercentageofimpact stationswithrespecttocontrolstations,beingBPOFAstricterin mostoftheareas.OnlyinthecaseofGalicia,differencesbetween impactandcontrol stationswerenot detectedusingBO2A and BPOFA.RegardingtoBPA,itassignedworseEcoQs(moderate,poor orbad)toahigherpercentageofimpactstationsincomparison withcontrolstations.However,thisratioalsoclassifiedcontrolsta- tionsasmoderateorpoorinNorwayandGalicia.Kappaanalysis showedahighagreementbetweenBO2AandBPOFAinmostofthe areaswiththeexceptionofGaliciaandtheCanarianArchipelago wherelevelofagreementwaslow(Table4).Theothercomparisons

Table4

KappavalueswithagreementlevelsinparenthesesfortheEcologicalStatusclas- sificationbetweeneachindices(levelofagreement:AP–‘Almostperfect’;VG-‘Very good’;G–‘Good’;M–‘Moderate’,L-‘Low’,N-‘Null’).

BO2A/BPOFA BO2A/BPA BPOFA/BPA

Total 0.7715(VG) 0.3203(L) 0.4479(M)

Norway 0.9018(AP) 0.2825(L) 0.3186(L)

BayofMorlaix 0.9435(AP) 0.7007(VG) 0.7774(VG)

Galicia 0.3408(L) 0.0315(N) 0.0330(N)

Castellón 0.9940(AP) 0.7610(VG) 0.7472(VG) CanaryArchipelago 0.251(L) 0.122(L) 0.5843(G)

withBPAshowedworselevelofagreementexceptinthecaseof CanarianArchipelagowherethehighestagreementwasobtained betweenBPOFAandBPA.

Insummary,theindicesindicate:(i)aworseEcoQSinimpact stationsthanincontrolstationswhenwetakeintoaccountthe threeindices,and(ii)theBPAgivesamoresevereclassification thanthetwootherindices.

4. Discussion

AverystrongcorrelationbetweentheBO2AandBPOFAindices weredetectedinthisstudy,exceptfortheCanarianarchipelago, where verylow indices were detected(Table3).Consequently, these indices might be unsuitable for assessing environmental

Fig.3. PercentageofsamplesclassifiedineachEcoQStatusforimpactandcontrolstationsofeacharea.Stationsweregroupedinimpactandcontrol.Continentalshelfof Norway,Impact:stationsat<2000mfromtheproductionfacility,Control:stationsatleast5000mfromthenearestproductionfacility.BayofMorlaix,Impact:Rivierede Morlaixstation,Control:PierreNoirestation.Galicia,Impact:stationsintheinnerpartofthería.Control:stationsinthecentralzoneofthería.CastellónCoast.Impact:

stationsat0mfromthedischargeControl:stationsat1000mfromthedischarge.CanarianArchipelago:Impact:impactedstations,Control:controlstations.

qualityatthisandothersimilarlocations.Inthislocation,indices were very low probably due tothe oligotrophic nature of the AtlanticOceanintheCanaries,whichmightdissipateperturba- tionsbroughtabouttheanthropogenicdisturbancesanalysedin thisstudy(Rieraandde-la-Ossa-Carretero,2013).

Man-inducedperturbationsintheCanarianarchipelagoarespa- tiallylimitedandcharacterizedbyalowintensityintheimpacted area,beingclassifiedcoastalwatermassesasinverygoodcondi- tion(Rieraetal.,2009).Pollutionfromsewage anddesalination plantsisrapidlydilutedinthewatercolumnbecauseofthecontin- uouscoastalcurrents.Thus,macrofaunacommunityisnotheavily affectedbythisperturbation,andthecompositionofpolychaetes andamphipodsnotdifferconsistentlyfromimpactedtocontrol stations(Rieraetal.,2012).Thissituationoccursinoffshorefish cages,withahighdispersionofparticulatematerial,e.g.faecesand uneatenpellets,togetherwiththepresenceoffishaggregatesthat incorporatethisfoodsourceasamainpartoftheirdiet(Rieraetal., 2014).Thethreeindices(BO2A,BPOFAandBPA)showedconsistent effectsinPuertoCalero,insideaharbourwherehydrodynamicsare limitedandnotexposedtothemaincurrent.Impactedstationsin PuertoCalerowerecharacterizedbyopportunisticpolychaetesthat dominatethemacrofaunacommunity,withalackofamphipods (Rieraetal.,2011).Consequently,theseindicesmightbeunsuit- ableforassessingenvironmentalqualityatthisandothersimilar locations.

ThemaximumvaluesoftheBPAindex(Fig.1)alwaysseemed higherthan bothof theotherindices.In fact,thesevalues cor- responded to two distinct situations: (i) the absence or low abundanceofamphipodsand(ii)highabundanceofpolychaetes thatwerenotclassifiedamongopportunisticannelids,suchason thecontinental shelfofNorway.FortheEkofisksiteBPAvalues wereheavilyinfluencedbytheepisodicpresenceofthepolychaete Galathowenia oculata in 2005 and 2008. Thispolychaete is not accountedforBO2AandBPOFAcalculations. In2008,G.oculata wasbyfarthemostabundantbenthicorganismintheregionand showedlargefluctuationsinabundancebetweenenvironmental surveys(Cochraneetal.,2009).In1996,theBPOFAandBPAindices showedapeakintheimpactedstationsmainlyduetoincreased abundancesofthegenusSpiophaneswhich isnotaccountedfor BO2A.In1997,fortheHeidrunfield,theBPAindexshowedapeak partiallyduetohighabundancesofthepolychaeteEuchoneincolor.

By2009,thethreeindicesshowedadecreaseduetodecreasing abundances of the polychaete Chaetozone sp., one of themost dominanttaxain2003and2006(Mannviketal.,2010).In2009, however,thestations neartheproductionfacility wereconsid- ereddisturbedbyhighabundancesofthebivalveThyasiraequalis, whichwasregardedasanindicatorspecieswhenpresentedinlarge numbers(Mannviketal.,2010).ForStatfjord,BPAremainedhigh duetotheincreaseabundanceofthepolychaeteDitrupaarietinain thestationsneartheproductionfacility.Highabundancesofthis specieshadbeenpreviouslyattributedasanindicatorofpollution (Vassendenetal.,2009).

IntheBayofMorlaix,thehighvaluesofBPAintheimpactedRM stationwasrelatedtothehighabundanceofsomeopportunistic species,suchasChaetozonegibber(Cirratulidae)orSpiodecoratus andPseudopolydorapulchra(Spionidae)(Dauvin,2000).Thesetwo spionids,S.decoratusandP.pulchra,alsorepresentedalargepro- portionoftheopportunisticpolychaetes,explainingcomparable trendsofbothBO2AandBPOFAatthecontrolsite.Atthecontrol PNsite,thedisappearanceofthedominantamphipodAmpelisca after theAmoco Cadiz oil spill in the spring of 1978 matched foralargeincreaseoftheindices,inparticularBPA.Then,there wasageneraltrendtodecreasingvaluesinrelationtothecolo- nizationofsensitiveAmpeliscaspecies,whichoccurred10years afterthespill(Dauvin,1998).TheBPAindexremainedveryhigh throughoutthesurveyperiodintheRMimpactedstationdueto

thehighdensitiesofopportunisticpolychaetes.Thisobservation correspondedto the‘EstuarineQuality Paradox’(Dauvin,2007;

ElliottandQuintino,2007;DauvinandRuellet,2009),wherebyit wasdifficulttodetectanthropogenicallyinducedstressincluding the”AmocoCadiz”oilspill.In fact,inestuariesthatwerenatu- rallyorganicallyrich,thebiotawasconsequentlysimilartoareas withanthropogeniceutrophication,andpolychaetesproliferated naturallywithoutsupplementaryorganicpollution.

In theGalician Rías, differences in index values werecloser thanthoseobservedintheBayofMorlaiximpactedstationswhere opportunisticpolychaetesdominatedthroughoutthestudyperiod.

However,inthisarea,theabundanceofopportunisticpolychaetes afterthe“AegeanSea”oilspillwasrelativelylow.

OntheCastellóncoast,therewasanincreaseoftheabundance ofpolychaetefamilies,which,despitenotbeingconsideredoppor- tunistic,exhibitedtypicaltolerancepatterns(Del-Pilar-Rusoetal., 2010).AtBenicarló,therewasagreatdifferenceofvaluesbetween impactedandcontrolstationduetoanincreasedabundanceofthe polychaeteOphryotrocha,especiallyin2007and2008.Moreover, polychaetefamiliesnotconsideredopportunisticforthecalcula- tionofBO2AorBPOFAindices,suchastheParaonidae,werehighly abundantattheimpactedsites.However,overthewholearea,the polychaeteassemblagewasusuallydominated byopportunistic speciesatsitesclosertodischarges.

IntheCanarianArchipelago,attheBarrancoHondofishcages, highBPAvalueswereobservedattheimpactedstationsinApril 2007duetothegreaterabundancesoftheopportunisticspionid Prionospiosteeenstrupii.AttheCalerosite,theBPOFAandBPApeaks inJune2005wereduetotheincreaseoftheopportunisticspionid Pseudopolydoracf.paucibranchiata.BO2Ashowedminimumvalues in2004mainlyduetotheincreaseofamphipods,e.g.Pariambustyp- icusandMegamphopuscornutus.Incontrast,maximumvalueswere reportedinJune2005,whenamphipodsshowedtheirminimum abundances,associatedwiththepresenceoftheopportunisticspi- onidPseudopolydoracf.paucibranchiata.

ThethreeindicescandeservetoassesstheEcoQSoftheimpact stationssincethereisanotableincreaseofworsestatusbetween impactandcontrolstationsinthedifferentstudiedsites,i.e.the threeindicesshowedthatingeneral,controlstationshadhigher ecologicalqualitystatuscomparedwithimpactedstations.(Fig.3).

Amongthem,BPAgivesamoresevereclassificationthanthetwo otherindices.Infact,thisindexshowedlowagreementwiththe others while BO2A and BPOFA assigned similarEcoQS in most oftheareas.However,thisapparentstricterclassificationofBPA could be an underestimation of EcoQS, since both control and impactstationswererankedin lowercategoriesin someareas.

The use of BPA would be determined by the lack of sensitive speciesamongpolychaetesthatinhabitthestudiedarea.Ingeneral, therearetwomainsourcesofstressincoastalandmarineenvi- ronments:naturalphysical−chemicalstress(e.g.estuarineareas, stronghydrodynamics onmobile sediments preventingspecies recruitment,acidification, sea warming,hipoxia...)and human pressures(e.g.dredgingandsedimentdeposition,organicmatter accumulation...).High valuesofthepolychaete/amphipodratio couldoccurintheabsenceofamphipodsduetoanaturaldisturb- ance.Withoutamphipods,oranexplanationfortheirabsence,(e.g.

veryhighorganicmattercontents,anoxiccrisis,recentoilspill...), itisdifficulttoaccuratelyassessthequalitystatusofasiteandinfer onprobablecausesproducingthehighratiovalues.

Since the proposeduse of the polychaetes/amphipodsratio (Gomez-GesteiraandDauvin,2000),itsrevisedversionwiththe creationofBOPA(DauvinandRuellet,2007),anditstransforma- tionintoBO2A(DauvinandRuellet,2009),theseindiceshadbeen effectivelyappliedinmanylocationsundervariousenvironmen- talconditionsandwithanthropogenicperturbationsofdifferent intensities.

The polychaetes/amphipods ratio has proven successful at several geographic locations in detecting the effect of differ- entanthropogenic pressures on benthicmacrofauna. This ratio hasprovenespeciallyeffectivetodetectbenthicdisturbancesin responsetohumanpressuresresultingfromoilspillsoroffshore oilandgasproduction(e.g.GomezandDauvin,2000;Nikitikand Robinson,2003;DauvinandRuellet,2007;AndradeandRenaud, 2011;Joydasetal.,2011,2012;Sukumaranetal.,2013;Seoetal., 2014; Spagnoloet al., 2014), organic enrichment in sediments duetosewagedischarge(de-la-Ossa-Carreteroetal.,2009,2012b;

VazirizadehandArebi,2011;Subidaetal.,2012;Pinedoetal.,2012;

Serranoetal.,2014),fishfarms(Keeleyetal.,2012;Jahanietal., 2012;Karakassisetal.,2013;Zhangetal.,2013;Rieraandde-la- Ossa-Carretero,2013;Aguado-Giménezetal.,2015),organicand heavymetalcontaminationanddiversehumanactivities(Dauvin etal.,2007,2009,2012;MunariandMistri,2007;Pranovietal., 2007; Blanchet et al., 2008; Bakalem et al., 2009; Dauvin and Ruellet,2009;Grimesetal.,2010;Pelin,2011;Wetzeletal.,2012;

CaglarandAlbayrak,2012;SaddikandZourarah,2013;Tauppand Wetzel,2013), mosaic of habitats (Bouchetand Sauriau, 2008;

MunariandMistri,2008; Lavesqueet al.,2009;Doetal.,2011, 2012;Culhane,2012),eutrophication(Aflietal.,2008;Zhangetal., 2012,2013;Nebraetal.,2014)orinareasaffectedbyharbourcon- struction(Ingoleetal.,2009;Rieraandde-la-Ossa-Carretero,2013), butwasnotefficienttodetectnaturallong-termchangesofben- thiccommunitiesafteraseverewinter(KrönckeandReiss,2010).

BOPA/BO2Awasamongthefivemostusedindicesinareviewof35 benthicqualityassessmentindicesemployedindifferentcountries toassesstheimpactof15differenthumanpressures(Borjaetal., 2015).Moreover,inmostofthesestudies,BOPAandBO2Awere comparedwithotherindices,mainlyBENTIX,AMBIandM-AMBI (see alsoBoon et al., 2011; Culhane, 2012; Nebra et al., 2014;

Reizopoulouetal.,2014).Itappearedthat,inmostcases,theBOPA andBO2AindicestendedtooverestimatetheEcologicalStatusof thestations(e.g.Caglarand Albayrak,2012;Reizopoulou etal., 2014;Aguado-Giménezetal.,2015),butthecomparisonsshowed inmostofthecitedstudiesdidnottakeintoaccounttherevised thresholdsproposedbyde-la-Ossa-CarreteroandDauvin(2010), includingrecentpublications(Nebraetal.,2014;Aguado-Giménez etal.,2015).Inaddition,Keeleyetal.(2012)pointedoutthatthe EcologicalStatusclassificationwasunderestimatedbyBOPAwhen thespeciesrichnessandabundancesofmacro-invertebrateswere verylow,thoughtheuseofBOPAwasnotrecommendedforabun- dance<20ind.However,manyusersofBOPA/BO2Adidnotapply thisthreshold. OtherslikeNebra et al.(2014)continuedtouse BOPAintheupperpartofthetransitionestuarinesystem,whilethe BO2A,whichincludedtheoligochaeta,wasrecommendedinsuch lowsalinityzoneofestuaries.Nevertheless,insomecases,suchas theoffshoreplatformsintheAdriaticSea,theBOPAindexseemed toyieldabetterassessment ofstressedsituationsthanAMBIor M-AMBI(Spagnoloetal.,2014).Inthesameway,asregardsthe dumpingofdredgedmaterialintheElbeEstuary,theBO2Aindex showedabetterecologicalstatusthantheotherindicessuchas AMBIandM-AMBI(TauppandWetzel,2013).Ithadbeenexten- sivelynotedthatBOPA(andBO2A)indiceswereeasiertoapplythan otherindicesbecausetherequiredleveloftaxonomicknowledge wasreduced;itwasonlynecessarytoidentifyamphipods,along withareducedlistofopportunisticpolychaetes,anddistinguished thegenusJassafromtheotheramphipods(Jahanietal.,2012).

The Taxonomic Sufficiency principle has often been pre- sentedasarelativelysimple,usefulandpotentiallycost-effective complement to other more demanding assessment techniques (Włodarska-Kowalczuk and K ˛edra, 2007; Andradeand Renaud, 2011). For the Adriatic Coastal Transitional Ecosystems (CTEs), MunariandMistri (2010)pointedout that,inspiteof anAMBI check-listcontainingthebenthictaxaatthespecieslevel,theTS

principlewasalreadyincludedintheAZTIlist.Moreover,Munari andMistri(2010)indicatedthatagenusorfamilylevelofidentifica- tionforthebenthiccompartmentofItalianCTEsmightbesufficient forassessingthestatusofwatermasses.

MistriandMunari(2008)proposedaBenthicIndexbasedon TaxonomicSufficiency(BITS),specificallyforcoastallagoonsinthe MediterraneanSea,whichconsideredthreefamilycategories:1) sensitivefamilies;2)tolerantfamilies,and3)opportunisticfami- lies.Intheirappendix,theyproposedassigningecologicalgroups forBITScomparedwithBENTIXandAMBIreferring tothesame genus.

Apartfromconsideringtheuniqueresponseofafamilytostress, incompliancewiththeTSconcept,twootherproblemswereraised bythefaunallistdrawnupbyMistriandMunari(2008):i)notall invertebratefamiliesfoundin Europeancoastalandtransitional waterbodieswereincluded,andii)itwaslinkedtotheAZTIlist, which showedmajortemporal modifications over time (http://

ambi.azti.es/).Forexample,whenthelistwasrevisedinJuly2006, thenewlistincludedsignificantmodifications,whichresultedin movingLagiskorenifromgroups1to4.Nevertheless,Lagiskoreni, likePectinariidae,remainedclassifiedasasensitivespeciesinthe 2008BITSlistof MistriandMunari(2008).Therefore, the2008 BITSlistshouldbeupdatedbeforeusingBITSand extendingits applicationtootherwaterbodies.

Andradeand Renaud (2011) suggested using a simple ratio betweenpolychaetesandamphipodsasapotentiallycost-effective complement to othermore demanding technique for assessing soft-bottomcommunities. This approach reinforced theidea of makingacontradistinctionbetweenallpolychaetesastolerantor opportunisticspeciesandallamphipodsassensitivespecies.

Recently,Aguado-Giménez etal.(2015)proposeda BOPA-FF includingtheopportunisticpolychaetefamiliesconsideredinthe BOPA/BO2A indices, i.e. Capitellidae, Cirratulidae; Dorvilleidae, Pectinariidae,andSpionidae,plusalsoothertolerantpolychaete familiestothefishfarminginfluence,i.e.Glyceridae,Nereididae, andOweniidae,butexcludingCirratulidae,whichweremostlyclas- sifiedasopportunisticpolychaetefamily.

However,afurtherquestionarose:whatwasthelimitofaccept- able TS allowing an accurate assessment of the quality of the benthicenvironmentbasedonmacroinfauna?

Firstofall,therewasacontrastbetweenAndradeandRenaud’s proposition(2011)assumingauniqueresponseofamphipodsto pollution andtheevidence fora gradientin theirsensitivityto pollution(de-la-Ossa-Carreteroetal.,2012a).Infact,thepresence ofamphipodsthatwereconsideredasstress-tolerantorganisms couldproducediscrepanciesbetweenthecalculatedindicesand otherbioticindicatorsthattakeintoaccountthedifferencesintol- erancelevelamongamphipodspecies(Pinedoetal.,2012,2014).

Therewasalsoadebateamongbenthiccommunityexperts.Some authorsconsideredthattherewasauniqueandhomogeneousgeo- graphicalresponseofmacrobenthicspeciestoincreasedorganic matter,andageneraleffectofstressandpollutiononthebiogeo- graphicaldistributionofaspecies(i.e.agivenspecieswasincluded inasingleecologicalgroup)(Borjaetal.,2000,2011).Otherssug- gestedthatitispossibletoobservedifferentresponsesofspeciesto organicmatter,stressandpollutionaccordingtolocalandregional particularities(Grémareetal.,2009;Zettleretal.,2013).Thiscould correspondtotheexistenceofdistinctadaptedpopulationsthatcan responddifferentlytopollutionand,therefore,andbeclassifiedin severalecologicalgroupsinfunctiontotheirsensitivity(Grémare etal.,2009;Zettleretal.,2013).Speciessensitivities,tolerances andpreferencescouldchangealongenvironmentalgradientsand betweendifferentbiogeographiczones(Leonardssonetal.,2015).

Hence,therewasaneedtoadjustindicatorspecieslistsasafunction ofareasshowingmarkedenvironmentalgradients(Zettleretal., 2013;Leonardssonetal.,2015).Inaddition,there wasadegree

ofsubjectivityinallspeciesclassifications(Dauvinetal.,2010).

Furthermore,thesimplification ofthe taxonomyprior toindex calculationasproposedinthispresentstudyreducedtheriskof attributingawrongEcologicalQualityStatusduetothedifficul- tiesofidentifyingcertainpolychaetegeneraandfamilies(Dauvin, 2005).Moreover,Spilmont (2013)underlined thatcurrent ben- thicindicatorsbasedonspeciescompositionsufferedfromsevere drawbacksandtheirpracticalitymighthavereachedadeadend.He suggesteddevelopingfunctionalindicators,whichcouldbemore relevanttodetectperturbationsofbenthiccommunities.

Finally,asamajorresultofthisstudy,theverystrongcorrelation betweenBO2AandBPOFAindicatedthatthelossofinformation wasverylowwhenpolychaeteswereidentifiedonlyatfamilylevel andall amphipodswereconsideredasa singlesensitivegroup.

Acriticismof indicesthat employtaxonomicsufficiencyis that groupingoforganismsintaxabelongingtoasinglehighertaxo- nomicleveloccursirrespectiveoftheirecologicalrelevanceand maythereforeleadtounnecessarylossoftaxonomicdetailsand reducetheabilitytoinferaboutecologicalprocessesunderlying theobservedpatterns(Bevilacquaetal.,2015).Ithasbeensug- gested thateffective ecologicalqualityindicators needtoshow gooddiscriminatorypoweracrossafullspectrumof,e.g.benthic enrichmentconditions,andunderarangeofregionalenvironmen- talconditionsbut theserequirementsarenot alwaysmeteven bymoredevelopedindices(Keeleyetal.,2012).Asolutionmight betodevelopbiotic indices calibratedforparticular geographi- calareascombinedwithmultivariatestatistics(Aguado-Giménez etal.,2015)whichmayincreasemonitoringprogramcosts.

Inthispaper,ithasbeenshownthatthesimpleindicesevaluated caneffectivelyidentifytheeffectsofdiverseanthropogenicimpacts acrossa largegeographicalscalebycomparingimpactedversus controlareasateachsite.Thecostsofidentification,knowledgesta- tusandavailableexpertiseshouldbeevaluatedwhenchoosingan index.Therefore,toassessanthropogenicimpactsinbenthiccom- munitiesinareaswithweakavailablelevelofknowledge,itmight besuitabletouseinafirststepalowdegreeoftaxonomicexpertise withlimitedfundinginvolvingastep-wisebottom-upapproach.In thisway,lowerdegreesofTS(BPAindex)couldprovideageneral ideaofthebenthiccommunityassemblagesunderthecondition thatcomparisonscouldbemadewithreferencestations.However, theBenthicPolychaeteOpportunisticFamiliesAmphipods(BPOFA) indexcouldbeacceptedasasurrogateoftheBO2Aindexrepresent- ingasimpleeffectivebenthicindicatorforassessingtheecological statusofcoastalwatermasses.

Acknowledgements

TheauthorsthankJoséLuisGomez-GesteirafromtheCentro Tecnológico del Mar–Fundación CETMAR, Eduardo Cabello, s/n, 36208Vigo,Spain–fortheGaliciasamplesandM.S.N.Carpenter forcorrectingtheEnglishgrammar,syntaxandstyle.H.Andrade receivedfinancialsupportfromtheNorwegianResearchCouncil;

throughtheECOBARproject(BenthicIndicatorsforMonitoringthe EcosystemoftheBarentsSea,#190247/S40toP.Renaud)andEni Norge,withintheArcticSeasBiodiversity(ASBD)project;WP4.5 Analyses of offshorebenthic biodiversity. Y.Del-Pilar-Ruso and J.A.de-la-Ossa-Carreterogratefullyacknowledgethestaffofthe Department ofMarine Sciences and Applied Biologyof Univer- sityofAlicantefortheirhelpandCONSOMARS.AandEntitatde Sanejamentd’Aigüesforthefinancialcontribution.RodrigoRiera isgratefultotheremainingstaffofCIMASLfor invaluablehelp duringfieldsurveysandtaxonomicidentificationofmacrofauna samples.ThanksalsotoDr.AngelBorja(AZTITecnalia)forprovid- ingaccesstotheExcelsoftwaresheetusedtocomputetheKappa analysisresults

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