(Tunisia) Using Living Foraminifera Assemblages and a Multiproxy Approach

24 Pages·2015·4.03 MB·English

RESEARCHARTICLE
Environmental Quality Assessment of Bizerte
Lagoon (Tunisia) Using Living Foraminifera
Assemblages and a Multiproxy Approach
MariaVirgíniaAlvesMartins1,2,3*,NoureddineZaaboub4,LotfiAleya5,FabrizioFrontalini6,
EgbertoPereira1,PauloMiranda3,MiguelMane1,FernandoRocha3,LazaroLaut7,MoniaEl
Bour4
1 UniversidadedoEstadodoRiodeJaneiro—UERJ,FaculdadedeGeologia,Av.SãoFranciscoXavier,
524,Maracanã.20550–013RiodeJaneiro,RJ,Brasil,2 UniversidadedoEstadodoAmazonas–UEA,Av.
DjalmaBatista,3578,Flores,CEP69050–010,Manaus,Brasil,3 UniversidadedeAveiro,Dpto.
Geociências,CampusdeSantiago,3810–193,Aveiro,Portugal,4 InstitutNationaldesScienceset
TechnologiesdelaMer,1934–2025Salammbô,Tunisia,5 UniversitédeBourgogneFranche-Comté,
LaboratoiredeChrono-Environnement,UMRCNRS6249,PlaceLeclerc,F-25030BesançonCedex,
France,6 UniversitàdegliStudidiUrbino"CarloBo",DipartimentodiScienzedellaTerra,dellaVitae
dell'Ambiente,CampusScientificoEnricoMattei,LocalitàCrocicchia,61029Urbino,Italy,7 Laboratóriode
Micropaleontologia–LabMicro,UniversidadeFederaldoEstadodoRiodeJaneiro–UNIRIO,Av.Pasteur,296
—Urca—Cep22290–240,RiodeJaneiro,Brazil
*[email protected]
OPENACCESS
Citation:AlvesMartinsMV,ZaaboubN,AleyaL,
FrontaliniF,PereiraE,MirandaP,etal.(2015) Abstract
EnvironmentalQualityAssessmentofBizerteLagoon
(Tunisia)UsingLivingForaminiferaAssemblagesand
ThisstudyinvestigatedtheenvironmentalqualityoftheBizerteLagoon(Tunisia)through
aMultiproxyApproach.PLoSONE10(9):e0137250.
doi:10.1371/journal.pone.0137250 anintegratedapproachthatcombinedenvironmental,biogeochemical,andlivingbenthic
foraminiferalanalyses.Specifically,weanalyzedthephysicochemicalparametersofthe
Editor:LipingZhu,InstituteofTibetanPlateau
Research,CHINA waterandsediment.Thetextural,mineralogical,andgeochemicalcharacteristicsofthe
sediment,includingtotalorganiccarbon,totalnitrogen,simultaneouslyextractedmetals
Received:April13,2015
(SEM),acidvolatilesulfides(AVS),chlorophylla,CaCO ,andchangesinbacterialpopula-
3
Accepted:August13,2015
tionsandcarbonisotopesweremeasured.TheSEM/AVSvaluesindicatedthepresenceof
Published:September15,2015
relativelyhighconcentrationsoftoxicmetalsinonlysomeareas.Foraminiferalassem-
Copyright:©2015AlvesMartinsetal.Thisisan blagesweredominatedbyspeciessuchasA.parkinsoniana(20–91%),Bolivinastriatula
openaccessarticledistributedunderthetermsofthe (<40%),Hopkinsinaatlantica(<17%),andBolivinaordinaria(<15%)thatcannotbeconsid-
CreativeCommonsAttributionLicense,whichpermits
eredtypicalofimpactedcoastallagoonsbothinMediterraneanandnortheastAtlantic
unrestricteduse,distribution,andreproductioninany
medium,providedtheoriginalauthorandsourceare regions.TheresultsofthisworksuggestthatBizerteLagoonisauniquesetting.This
credited. lagoonispopulatedbytypicalmarinespeciesthatinvadedthisecosystem,attractednot
DataAvailabilityStatement:Allrelevantdataare onlybytheprevailingfavorableenvironmentalconditionsbutalsobytheabundanceand
withinthepaperanditsSupportingInformationfiles. qualityoffood.Theresultsindicatethatthemetalpollutionfoundinsomeareashaveaneg-
Funding:Thisworkwaspartiallysupportedbythe ativeimpactontheassemblagesofforaminifera.Atpresent,however,thisnegativeimpact
projectsBilateralofCooperationTunisianPortuguese isnothighlyalarming.
48/TP/09andPEst-OE/CTE/UI4035/2014andbythe
fellowshipfromthePROTECProgramof
UniversidadedoEstadodoRiodeJaneiro—UERJ
andUniversidadedoAmazonas–UEA.
CompetingInterests:Theauthorshavedeclared
thatnocompetinginterestsexist.
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EnvironmentalQualityAssessmentofBizerteLagoon
Introduction
TheEuropeanWaterFrameworkDirective(WFD,Directive2000/60/EC)establishesthatthe
ecologicalstatusofwaterbodiesisassessedintermsofthequalityoftheirbiological,physico-
chemical,andhydro-morphologicalelements.Suchcriteriaarewelldefinedforcoastalwaters,
whiletheyarestillunderdiscussionfortransitionalwaters,suchascoastallagoons.Coastal
lagoonsandestuaries,whichgenerallysupporthighlevelsofbiologicalproductivity,represent
acontinuumbetweencontinentalandmarineaquaticecosystems,andtheyarecommonly
characterizedbyashallowwaterdepth,strongfluctuationsofphysicochemicalparameters,
andmarkedgradients,suchasinsalinity[1],organicmatterquantityandquality,oxygenavail-
ability,andtheoccurrenceofpollutants[2].
Lagoonsaresubjectedtosignificantenvironmentalchangesduetobothnaturalandanthro-
pogenicinfluences.Theseinfluencesincludeengineeringconstructionsthataltertheirnatural
circulationpatterns,theextractionordepositionofmineralogicalmaterials,theexploitationof
biologicalproducts,andwaterandsedimentpollutionthatarethemaincausesofenvironmen-
taldegradation[2],[3],[4].Differentproxies,suchasbiogeochemicalindicators[2],[5],[6],
[7],[8],havebeenusedtoassessthewaterandsedimentqualityofcoastallagoonsandtoeval-
uatetheirenvironmentalvulnerability.
Amongthese,benthicforaminiferaareonethelargestappliedandmosteffectivebioindica-
torsofenvironmentalqualityand,thereforetheyhavebeenusedtobetterunderstandchanges
inthephysicochemicalparametersofmarineandtransitionalenvironments[7],[9],[10],[11].
Benthicforaminiferaoccurinmanyenvironments,includingtransitionalsettingssuchassalt-
marshes,riverestuaries,coastallagoonsandbaysaswellasoceanicbasins[12].Theirdistribu-
tioniscontrolledbymanyfactors,suchastemperature,salinity,oxygen,andsedimentgrain
sizeorsubstratetype[13],andchangesinthetypesandamountsoffood[12],[14],[15],[16].
Somespeciescolonizeoxicsediment-waterinterfaces,whileotherstolerateoxygendeficiency
andepisodicanoxicconditions[17],[18].Benthicforaminiferalassemblagesareprevalently
influencedbysedimentcharacteristicsbuttheyarealsoaffectedbysedimentpollution[2],[8],
[19],[20],[21],[22],[23].
Otherelements,suchasmineralogical,physicochemical,geochemicalandbiologicalprox-
ies,shouldbeconsideredandintegratedtoassesslagoonalecologicalquality[2],[23],asalso
suggestedbytheWFD.Amongthese,theavailableconcentrationsofheavymetalsshouldbe
analyzedinsedimentsand/orwaterstoinvestigatetheextentoftheimpactofanthropogenic
activities,aswellastoevaluatetheirhazardlevel.Sedimentsgenerallyretainpollutantslonger
thanwater,whichis,inlargepart,renewedbytidesincoastalsystems[24],[25],[26],[27].Rel-
ativelyhighavailableconcentrationsofheavymetalsadsorbedtosedimentsmaybetoxicto
benthicorganisms[24],[25],[26].Moreover,pollutantsdepositedinsedimentscanberesus-
pendedintothewatercolumnandaffectbenthicandplanktonichabitats[28],[29].Mostof
theworkbasedonforaminiferalresponsestometalpollutionisbasedontotalmetalconcentra-
tionsinthesediments,yetverylittleisknownabouttheresponsesoflivingbenthicforaminif-
eratorelativelyhighconcentrationsofavailablemetalsinsediments,whoselevelsareof
concernforbiota[2],[30].
ThisworkaimstostudythelivingbenthicforaminiferalassemblagesoftheBizerteLagoon,
aswellasthepossiblefactorsdrivingtheirdistribution.Thisstudyisthefirsttoevaluatethe
sustainabilityandthesedimentqualityofBizerteLagoonusingbiogeochemicalproxies,includ-
inglivingbenthicforaminifera,bacteriaaswellasthefirsttopredicthowcoastalecosystems
arerespondingtothecombinedeffectsofeutrophicationandpollutionpressure.Inthebroader
contextofthestudyofcoastallagoonsandothertransitionalenvironments,thisworkadvances
ourknowledgebecauseitshowsthat:theanalysisofsedimentqualitybasedonlyonpollutant
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EnvironmentalQualityAssessmentofBizerteLagoon
assessmentcanresultinaninconclusiveknowledgeaboutthenegativeimpactofcontaminants
onlivingorganisms.
StudyArea
TheBizerteLagoonisaMediterraneantransitionalecosystemlocatedinnorthTunisia(lati-
tude:37°8’–37°14’N,longitude9°46’–9°56’E),withanextensionofover150km2(themaxi-
mumwidthis11kmandthemaximumlengthis13km)andanaveragedepthof7m(Fig1).
Fig1.a)StudyareaintheBizerteLagoon(adaptedfromOTC,1992,MapofBizerteLagoonofficedelatopographieetdelacartographiede
Tunisie).Thestudiedstationsarelabeledwithnumbers.Themaintownsandstreamsareindicated.b)Photoofthesurfacewatercolumnshowing
thecnidarianbloom.c)Photoshowingsuspendedstructuresusedinmollusksculture.
doi:10.1371/journal.pone.0137250.g001
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EnvironmentalQualityAssessmentofBizerteLagoon
ItconnectswiththeMediterraneanSeathroughastraightchannelthatisabout6kmlong,300
mwide,and12mdeep(Fig1).BizerteLagoonissetinabasementofante-Neogenerocks[31]
thatwaserodedandexperiencedseveralsedimentaryphasesduringtheMiocene[32].Itcom-
municatesinthesouthwithIchkeulLakeviatheTinjastream.Theprincipalstreams,which
arenon-permanentwatercourses,whoseflowsdependonrainfallthatfeedsthelagoonwith
freshwaterareTinjaChannelandRharek,BenHassine,andGuennichestreams(Fig1).
Theregionischaracterizedbyasub-humidclimatewith600to800mmofannualrainfall
[33].Therainyperiodcoincideswiththewinter,fromNovembertoApril,withmaximumpre-
cipitationinFebruary(219.5mm).Summerandtherestoftheyeararedry,withoutanyfreshwa-
terinputfromneighboringstreams[34],andstrongerseawaterinfluence[35].Theseasonal
gradientofwatersalinityintheBizerteLagoonisrelativelylarge,ranging,onaverage,from20in
winterto40insummer[36]whenthewatercolumnwarmingcanproducestratification[35].
Thislagoonhasbeenexploitedforfishingactivitiesforseveralcenturiesandformusselfarming
since1964.ThemusselMytilusgalloprovincialis,theEuropeanflatoysterOstreaedulis,andthe
JapaneseoysterCrassostreagigashavebeenintensivelyculturedinthislagoonfordecades,and
naturalbedsfortheEuropeanclamTapes(Ruditapes)decussatusarestillpresentinthelagoon.
About163,000inhabitants(2004census)livearoundthelagoon,ofwhicharemainlycon-
centrated((cid:1)70%)inthetownofBizerte[36].Theotherimportanturbancentersborderingthe
lagoonareMenzelBourguiba,MenzelAbderrahman,andMenzelJemil(Fig1).Themost
importantindustrialactivitiesarelocatedinthevicinityofBizerte(cementfactoryandmetals
treatment),MenzelJemil(dyeworksandmetallurgy),andMenzelBourguiba(withanaval
port,ElFouledhsteelworks,amilitaryarsenal,andmetallurgy)[34].Someotherindustries,
suchasanironandsteelplant,acementfactory,andarefinery,areestablishedoutsideofthese
towns[37].
Humanpopulationgrowtharoundthelagooncausedanincreaseinthedischargeofwaste-
waterintothelagoon[38].Recently,twomainwastewatertreatment(ofMenzelBourguiba
andBizerte)stationshavebeeninstalledaroundthelagoon.Sincethecommissioningofsewage
fromtheBizerte(October1997)andMenzelBourguiba(January1998)stations,wastewater
dischargeintothelagoonhasalmosthalted.Furthermore,thislagoonhasalsobeensubjectto
intensivemaritimetrafficandindirectlytoseveralpollutantscomingfromoilandsteelfacto-
ries.TheconstructionofdamsonIchkeulLake,whichsuppliesthelagoonwithfreshwater,has
stronglyaffecteditsnaturalequilibrium[37],asitcausedadroppedofwaterinputfrom165to
only20millionm3peryear[39].AnyhumaninterventionintheMediterraneanSea,Ichkeul
Lake,andthecatchmentarea,particularlyintheMenzelBourguibaindustrialzone(construc-
tionofdams,break-waves,andindustrialwaste)mightalterthedistributionofthebiogeo-
chemicalpropertiesofthissensitiveecosystemand,consequently,modifyitsenvironmental
quality[40].
MaterialsandMethods
Tenstationsweresampledinthelagoonon22March2013(Fig1A).Thesamplingtookplace
duringajellyfishbloomevent(Fig1B).Threesuccessfulreplicatesweretakenfromeachsta-
tionbetweenadepthof7and12musingabox-corer,asweresplitsofthefirstsurfacecentime-
terofeachstation.Thesampleswereanalyzedforlivingbenthicforaminifera,bacterial,and
pigmentcontents,andseveralabioticsedimentaryvariables,includinggrainsize,carbonates,
acidvolatilesulfides(AVS),simultaneouslysequentialextractedmetals(SEM),totalorganic
carbon(TOC)andtotalnitrogencontent(TN),mineralogy,andmagneticsusceptibilityaswell
δ13Cdata.Physicochemicalparameters,suchastemperature,salinity/conductivity,andoxygen
contentinwater,andpH,Eh,andoxygencontentinsediments,weremeasuredwitha
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multiparametricprobeateachstation.Duringthefieldwork,sedimentsforthebenthicforami-
niferalanalysisweretreatedwithasolutionofRoseBengal(2gofRoseBengalin1,000mlof
alcohol)todifferentiateliving(Bengalrose-stained)fromdeadspecimens[11].Thesediments
forgeochemicalanalysiswereheldinpolyethyleneflasksandkeptatapproximately-4°Cprior
toanalysis.
Textural,mineralogical,andmagneticsusceptibilityanalyses
Alasermicrogranulometer(MastersizerSinstrument,MalvernInstruments,Malvern,UK)
wasusedtodeterminethesedimentaryparticlesizes(intherangefrom0.05–2,000μm)ofthe
sedimentsineachsampleaftertheremovaloforganicmatter(withhydrogenperoxide)and
carbonates(withhydrochloricacid70%).Themineralogicalcompositionofthesedimentswas
analyzedinthe<63μmand<2μm(clay)fractionsbyX-raydiffraction(XRD)techniques,
accordingtothemethodologyadoptedbyMartinsetal.[41].Magneticsusceptibilityofthe
sedimentswasmeasuredinthetotalsedimentwithaportableKT-9DigitalMagneticSuscepti-
bilityMeterbytaking10successivereadingspersampleandusingthemeanvaluestoobtaina
reliableresult.
Chemicalanalyses
Theevaluationofcalciumcarbonate(CaCO )contentinthesedimentswasbasedonthevolu-
3
metricanalysisofcarbondioxide(CO ),whichisliberatedduringtreatmentwitha4Nhydro-
2
chloricacid(HCl)solution.TheTOCandTNcontentswereanalyzedusingaPerkinElmer
(Waltham,MA,USA)PE2400CHNsystem.
Themethodforchlorophylla(Chla)andphaeopigmentextractionwasquitesimilarto
thatappliedinawatersample,exceptthatitwasnecessarytosuspendthefractionofsediment
directlyinacetone90%,andthentoallowtheextractiontoproceedfor12hat-20°C,followed
byspin-dryingandspectrometrymeasurements[42].
TheSEMandAVSanalysesofsedimentsweremadeusingacoldacidpurge-and-traptech-
nique[43],[44]andusingthemethodologydescribedbyOueslatietal.[45].Theavailablecon-
centrationsofCr,Ni,Zn,Pb,Cu,Fe,Mn,andCo,aswellasthetotalconcentrationsofreactive
metals(SSEM)wereevaluated.Itispossibletopredicttheheavy-metalbioavailabilityandthe
toxicityofthesedimentaccordingtotherelationshipSSEM/AVS(referredasSEM/AVS).
Undersuboxictoanoxicconditions,ifSEM/AVS<1,Metal-A(AvailableConcentrationsor
ReactiveMetals)concentrationsarecontrolledbysolubility(Ksp)oftheirsulfidesandthere
areweakmetalconcentrationsdissolvedandbioavailableinpore-water.Onthecontrary,if
SEM/AVS>1,metalconcentrationsbecomehigh,toxicandbioavailableinpore-water.Itis
inferredthatnopotentiallymetalbioavailabilityexistsforbenthicorganismswhenSEM/
AVS<1[46],[47],[48],[49],[50].
Bacterialanalysis
Fortotalcoliform(TC),fecalenterococci(FE),totalmesophiliccounts(TMC),sulfate-reduc-
ing(SR)bacteriaandVibrionaceae(Vb)enumerationinthesediment,10gofsamplewassus-
pendedinphysiologicalwatercontaining3%NaCl(w/v).Allcountingmethodswerebasedon
cultivationbyastandardplatecountingagarprocedure[51].Marineagar(Difco,BectonDick-
inson,FranklinLakes,NJ,USA)wasusedtocountthetotalnumberofmesophilicbacteria,
andtheincubationtemperaturewasmaintainedat32°Cformesophilicpopulationcounting
andallplateswereincubatedfor72hbeforecounting.ForTCenumeration,ten-folddilutions
(100μL)ofthesedimentsamplessuspensionwerespreadonthesurfaceofDesoxycholateLac-
toseagarplates.Countswereperformedafterincubationfor48hat37°C.AnaerobicSR
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bacteriawereidentifiedonthebasisoftheirselectivegrowthinThioSulfateNeomycin(TSN)
agarmedium(BioMérieux,Marcyl'Etoile,France)underananaerobicatmosphereenrichedto
5%CO ,accordingtothemethodofLarpentandGourgand[52].Theestimationwasrealized
2
afterincubationfor72h.ForVibrionaceaecounting,theselectiveThiosulfate-Citrate-Bile-
Sodiumagar(TCBS,Bio-Rad,Hercules,CA,USA)wasused,andthetotalVBwerecounted
afterincubationfor72hat25°C[53].
Foraminiferalassemblagesanalysis
Onsplitsofthe>63μmsedimentfraction,atleast300livingspecimenswerepicked,counted,
andidentified.Therelativeabundanceofeachspecieswasdeterminedtocharacterizetheliving
assemblages.Foraminiferaldensity(FD)andShannonindex(H’)[54]wereanalyzedaccording
totheprocedureadoptedbyMartinsetal.[2].Thebenthicforaminiferaldiversityalsowas
assessedthroughthespeciesrichness(S)andH’.Thespeciesequitabilitywasevaluatedthrough
theequationJ=H’/lnS.
Carbonisotopes
About20specimensofalivingAmmoniaparkinsonianawerecollectedfromthesedimentfraction
300–350μmforcarbonisotopicanalysisontheirtests.Thistaxonwasselectedsinceitspresentin
allthestudiedstations.Thesedimentfraction300–350μmwasusedtoavoidontogeneticvaria-
tionsduetobiologicalvitaleffects[55].The"KielIVCarbonateDevise"equipmentand"DeltaV
Plus—IsotopeRatioMS"analyzer(ThermoScientific)wereusedforthisanalysis.Theobtained
resultsarecomparedwithastandardcarbonate,thePeeDeeBelemnite(PDB).Datafromcarbon
isotopesareshownbytheδparameterdefinedby:δ(‰)=[R —R /R )×1000.In
sample standard standard
which,RvaluescorrespondtoC /C .Theaccuracyoftheanalysisis0.030‰.
13 12
Dataanalysis
Selectedlogarithmicallytransformedvariables[log(x+1)]weresubmittedtoanR-modeand
Q-modeclusterAnalysis(CA)andprincipalcomponentsanalysis(PCA).Theseanalysiswere
conductedinStatistica7.0software.TheR-modeCAwasbasedonthe“weightedpair-group
average”algorithmforagglomeration,andthe1-Pearsonrcorrelation,asadistancemeasure
andtheQ-modeCAwasbasedontheWard’smethodandEuclideandistance.
Thepercentageofbenthicforaminiferalspeciesandsometaxa/groupsthatreachedarela-
tiveabundance(cid:3)2%inatleastonestationandanoccurrenceinatleastthreestationswere
usedintheseanalyses.Abioticvariableswereselectedaccordingtotheirrelevancetotheaimof
thisworkand,patternofvariabilityinthestudyarea.
ThestationLB1,locatedinthechannelconnectingthelagoonwiththeseawasnotconsid-
eredinbothanalyses,becauseithadthelowestFD,diversityindexesandJandwascharacter-
izedbyanassemblagelargelydominatedbyonespecies(A.parkinsoniana,reaching91%)and
itwasthereforeconsideredasanoutlier.
Results
AbioticVariables
Thesamplelocations,theabioticvariables,andthemainbioticvariablesanalyzedinthiswork
arepresentedinS1Appendix.Thewatertemperaturevariedbetween14.7and15.8°C,salinity
from28to33.3,pHrangedfrom7.7to8.2(Fig2A)andEhvaluesfrom-57.2to-30.0mVmea-
suredinthesedimentsubsurface(Fig2B).TheDOinthewatercolumn(0.09–0.18mg/l)was
lowerthaninthesurfacesedimentpore-water(0.16–0.55mg/l;Fig2C).Thegraycolorof
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Fig2.Distributionmapsof:a)pH;b)redoxpotential(Eh)(mV);c)dissolvedoxygen(DO)contentin
surfacesediments(mg/l);d)sedimentmeangrainsize(SMGS;μm);e)phyllosilicates(%);f)ferrous
berthierine(f.;%);g)kaolinite(%);h)magneticsusceptibility(SIunities).
doi:10.1371/journal.pone.0137250.g002
sedimentsseveralmillimetersbelowthesurfaceindicatedreducingconditionsagreeingwith
thenegativeEhvalues.RelativelylowvaluesofEhandDOvalueswerealsofoundintheinner
partofthelagoon.
Inthestudiedsites,thesedimentmeangrainsize(SMGS)variedbetween6.6–23.3μm
(Table1),includingmostlyafinegraymuddyfraction(<63μm;76–100%).Thesandfraction
(>63μm)wascomposedmostlyofshelldebris,whichresultedinthetexturalcharacteristicsof
thesediments(bimodaltopolymodal,poorlytoverypoorlysortedsediments).Thecoarsest
sedimentsampleswerefoundinthenorthernareaneartheconnectionwiththeMediterranean
Seaandatsiteslocatednearthestreams’mouths(Fig2D).
Sedimentsweremostlycomposedofphyllosilicates(15–62%;mean42%:Fig2E),calcite
(13–40%;mean26%),quartz(9–60%;mean18%),pyrite(0.2–15%;mean3%),andanatase
(<10%;mean3%),alongwithminorproportionsofK-feldspars(1–5%),plagioclase(<4%),
anhydrite(<5%),ferrousberthierine(<4%:Fig2F),dolomite(<2%),siderite(<2%),magne-
tite/maghemite(<1%),andhematite(<0.5%)(S1Appendix).Theassemblageofclayminerals
wasmainlyrepresentedbykaolinite(62–87%;mean74%;Fig2G),illite(2–35%;mean21%),
chlorite(<21%;mean4%),andsmectite(<2%).Sedimentsweremoreenriched,forinstance,
inphyllosilicatesattheinnerstationsofthesouthern-westernsideofthelagoon(Fig2E),cal-
citenearthelagoonentranceandatstationsoftheeasternsideofthelagoon,pyriteatsome
stationsinthecenterofthelagoon,ferrousberthierineinthesouthernpartofthelagoon(Fig
2F)andkaoliniteatsomestationsoftheexternalsectorandcentralpartofthelagoon(Fig2G).
Thevaluesofthesediments’magneticsusceptibilitieswerenegativeatallthesitesranging
from-0.29to-0.13SIunities(Fig2H).Thehighestvalueswererecordedinthenorthernand
southernsidesofthelagoon.
TheCaCO ,TOC,TN,andtheC/Nratiorangedfrom12–28%(mean20%),2.5–5.9%
3
(mean4.2%),0.6–2.3%(mean1.1%),and1.5–6.9(mean4.3),respectively(Table1).The
Table1. Selectedsedimentologicaldata.
Stations SMGS CaCO TOC TN C/N Chla δ13C AVS SEM/AVS
3
LB-1 20 21 5.93 1.25 4.74 196.7 -1.78 212.23 0.52
LB-2 23.3 16 4.02 0.92 4.37 91.4 -1.17 617.28 0.16
LB-4 9.3 28 5.87 1.26 4.66 127.4 -2.32 242.33 0.37
LB-5 6.6 23 4.87 0.78 6.24 699 -2.21 181.32 0.54
LB-6 7.8 20 3.93 0.57 6.89 155.1 -2.4 65.96 2.6
LB-7 18.1 18 3.57 0.78 4.58 92.3 -1.64 0.0
LB-8 6.6 12 2.54 0.88 2.89 244.7 -1.51 212.4 0.42
LB-9 7.9 18 3.29 2.25 1.46 69.3 -2.52 35.56 3.56
LB-10 7.7 21 4.02 1.09 3.69 241.9 -1.77 193.67 0.59
LB-11 9.7 19 3.77 1.05 3.59 122.8 -2.36 695.19 0.16
Max. 23.3 28 5.9 2.3 6.9 699 -1.2 695 4
Min. 6.6 12 2.5 0.6 1.5 69.3 -2.5 0.0 0.2
Med. 11.7 19.6 4.2 1.1 4.3 204.1 -2 245.6 1
SMGS–sedimentmeangrainsize(μm);CaCO (%);TOC(%),TN—totalnitrogen(%);C/Nratio;Chlorophylla(Chla;mg/m3);δ13C(‰;VPDB);
3
AVS(μgg-1);SEM/AVSratio.
doi:10.1371/journal.pone.0137250.t001
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highestvaluesofTOC(Fig3A)andCaCO (Fig3B)werefoundinthenorthernandeastern
3
areaoftheBizerteLagoon.TheAVSvaluesandSSEMvariedbetween0and695μgg-1and
80and172μgg-1,respectively(Table1).AVSwerefoundatallthestations(exceptLB7).
TheAVSvalueswerehigherinthenorthernandcentralareasoftheBizerteLagoon(Fig
3C).Therangesofavailableconcentrationsofreactivemetalswere:Fe,78–168μgg-1;Mn,
0.9–2.22μgg-1;Zn,0.67–1.45μgg-1;Cr,0.09–0.24μgg-1;Ni,0.05–0.12μgg-1;Pb,0.04–
0.11μgg-1;Cu,0.06–0.1μgg-1;andCo,0.002–0.031μgg-1(S1Appendix).Mostofthe
accumulatedreactivemetals(SSEM)werehigherinsitesLB-1,LB-6andLB-9withconcen-
trationsof110.1μgg-1,171.7μgg-1and126.7μgg-1,respectively.Ontheotherhand,SEM/
AVS>1valueswerefoundatsitesLB-6andLB-9(Table1).Inthiscase,thetracemetal
concentrationsinpore-waterresultedhighneartheTinjaChannelandtheRharekStream
(Fig3D).
Chlorophyllacontentsvariedfrom69–699mgm-3(mean204mgm-3;Table1).Pheophy-
tinconcentrationwasbelowthedetectionlimit.Thehighestconcentrationsofchlorophylla
werefoundinfrontofGuennicheStream,inthechannelconnectingthelagoonwiththeMedi-
terraneanSeaandneartheMenzelBourguibatown(Fig4A).TheA.parkinsonianaδ13Cvalues
oscillatedbetween-1.2and-2.5‰(mean-2.0‰;Table1).Thehighestδ13Cvalueswere
recordedinthenorthernareaofthelagoonwhereasthelowestvaluesweremostlyfoundinsta-
tionslocatednearthestreamsoutflowandinthecentralpartofthelagoon(Fig4B).
BioticVariables
Bacterialcounts(Table2)revealedthattheTCvariedfrom3–40(NPP/100mg:“Nombrele
PlusProbable”or“MostProbableNumber”per100mg),FErangedfrom3–1,000(NPP/100
mg),andTMC,whichincludesallbacteriagrowingattemperaturesrangingbetween15°Cand
45°C,wasthemostrepresentedgroup,rangingfrom8x102to9x103(colony-formingunitsper
gram,CFUg-1).SRbacteriawerepresentinallsamples,indicatingtheoccurrenceofanoxic
conditionsforalmostallstations.TheabundanceofTCwashigherintheinnerpartofthe
lagoon,infrontofthemainstreams,indicatingexogenousdischarges(LB5,LB6,LB7,LB8,
andLB9)(Fig5A);FEreachedlocallyhighvalues(Fig5B),andTMCincreasedinstationsin
boththeouterandinnerlagoonalzones(Fig5C).TCabundancewerehigherthanFEvalues,
indicatingananthropogenicdischargeatsomestations.
TheFDrangedfrom~557–14,862n°g-1(Table2),andwasparticularlyhighatsomesta-
tionsinthenorthernandcentralpartsofthelagoon(Fig6A).Atotalof87speciesofliving
benthicforaminiferawereidentified(S2Appendix).Speciesrichnessvariedbetween17and46,
theH’indexrangedfrom0.5to2.9(Fig6B),andJfrom0.2to0.7(Table2).Thelowestvalues
ofthesevariableswerefoundatthestation(LB1)locatedinthechannelthatconnectsthe
lagoonwiththesea.
TheforaminiferalassemblageoftheBizerteLagoonwasmainlyrepresentedbyA.parkin-
soniana(20–91%:dominantatallthesites),Bolivinastriatula(upto33%),Hopkinsinaatlan-
tica(upto17%),andBolivinaordinaria(upto15%).Assemblagesalsoincludedspeciessuch
asElphidiumgunteri(<5%),Bolivinacompacta(<4%),Quinqueloculinaseminula(0.5–4%),
Bolivinapseudoplicata(<4%),Triloculinarotunda(<4%),Buliminaaculeata(<4%),aswellas
thoseofminorrelativeabundance(<3%),forinstance,Ammoniatepida,Ammoniabeccarii,
Bolivinadilatata,Bolivinaspathulata,Bolivinasubaenariensis,Buliminaelongata/B.gibba,
Buliminamarginata,Fursenkoinasquamosa,Nonionellaatlantica,Nonionellairidea,Spirolo-
culinaexcavata,andTriloculinatrigonula.Ammoniaparkinsoniana(Fig6C),H.atlantica
(Fig6D),andElphidiumspp.reachedtheirhighestrelativeabundancesintheouterpartofthe
lagoon.Bolivinastriatulawasmostlyrepresentedintheinnerpartofthelagoon(Fig6E),and
PLOSONE|DOI:10.1371/journal.pone.0137250 September15,2015 9/24
EnvironmentalQualityAssessmentofBizerteLagoon
Fig3.Distributionmapsof:a)totalorganiccarbon(TOC;%);b)calciumcarbonatecontent(CaCO ;%);c)acidvolatilesulfidesconcentrations
3
(AVS;μg/g);d)simultaneousextractedmetalsandAVSratio(SEM/AVS).
doi:10.1371/journal.pone.0137250.g003
PLOSONE|DOI:10.1371/journal.pone.0137250 September15,2015 10/24