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OCEANOLOGICAACTA´VOL.23±N 4 Metamorphosisandestuarinecolonisationinthecommonsole,SoleasoleaimplicationsforrecruitmentregulationRachidAMARA*,FrancËoiseLAGARDERE,YvesDESAUNAY,JocelyneMARCHAND ƒ2000Ifremerditionsscienti®quesetmeÂdicalesElsevierSAS R.AMARAetal.OceanologicaActa23(2000)469±484 peÂriode(avril)oueÂtaleÂed'avrilaÁjuin.DanslegolfedeGascogne,lameÂtamorphosenesemblepaseÃtreunephasecritiqueducycledeviedelasole.Aucontraire,nosobservationsameÁnentaÁlaconsideÂrercommeunmomentde«convergence»ouÁlavariabiliteÂinduitedurantlapeÂriodelarvairetendaÁs'atteÂnuer;ilenreÂsulteprobablementunmeÃmepotentieldesurviepourleslarvesissuesdediffeÂrentescohortesdurantetautermedelameÂtamorphoseetunereÂgulationdunombredepreÂ-recrues.LesjuveÂnilessontconcentreÂsexclusivementdanslesnourriceriescoÃtieÁresetestuariennesbienqued'importantesdensiteÂsetbiomassesdeproiesmeÂiobenthiquessoientdisponiblessurtoutleplateaucontinental.Cependant,danslesnourriceries,caracteÂriseÂespardessurfaceshabitableslimiteÂes,laconcentrationdespreÂdateurspotentiels,lavariabiliteÂdesconditionshydroclimatiques,lesrisquesdemortaliteÂdesjeunessolessontencoremaleÂvalueÂs.ƒ2000Ifremerditionsscienti®quesetmeÂdicalesElsevierSASSoleasoleajuveÂnilephasecritiquecolonisationestuarienne1.INTRODUCTIONThemetamorphosisof®shisaprocesswhichisinitiatedbyontogenetictransformationsandendswhen®shacquiretheformandthebehaviourofjuveniles[68].Theplanktoniclarvalstageslastforaboutonetothreemonthsinthemajorityof¯at®shspecies[15,36,51,60],althoughincertainspeciestheycanlastmuchlonger.Forexample,intheMicrostomuspaci®custheycanlastbe-tweenninemonthsandtwoyears[12].In¯at®sh,metamorphosisischaracterizedbyveryclearmor-phological(e.g.eyemigrationanda90 rotationinposture),anatomicalandphysiologicaltransforma-tionswhichgiverisetonewtypesofbehaviourandinducethetransitionfromapelagictoabenthicMetamorphosisisastagewhichrequiresalotofenergy[7].Inacertainnumberofspeciesitcorre-spondstoaperiodofnutritionalcrisis[43,61],strongmetabolicchangestogetherwiththeslowingdownofmetabolicactivity[68],andare-calibrationofvisioninordertodetectprey[53].Allofthesephenomenacanincreasethevulnerabilityofthelarvae.Inaddi-tion,thetransitiontonewhabitatsexposestheyoung®shtonewformsofcompetitionandpredation[29].Towardtheendofmetamorphosis,youngsolecolo-nizeunstablenurseryecosystemssituatedinbaysandestuaries[48,22].Thisstagemaybecrucialtothesurvivalofthenewsettlersduetothevariablehydro-logicalconditionsinthenurseries,butalsotopreda-tionandcompetitionforspaceandresources[66].Thisiswhyanincreasingnumberofauthorsbelievethattheyearclassstrengthofmany®shspeciesisgenerallydeterminedeitherduringorjustaftermeta-morphosis[8,36,55,69].Inotherwords,thesuccessoftheyearclasscoulddependonthesuccessorfailureduringthisphase.Despitetheseconsider-ations,veryfewstudieshaveassessedinanecologicalcontexttheimportanceoftheprocessesinvolvedinthetransitiontoabenthiclifeforthecontrolandregulationofrecruitment[15,50](controllingfactorsorprocessesarede®nedasthosethatgeneratetheamong-yearvariabilityinyear-classwhereasregulat-ingfactorsorprocessesreducethisamong-yearvari-ability).Thisissurprising,giventheimportanceoftheseprocessesparticularlywhenthetime-spacewin-dowinwhichthelarvaemetamorphoseisrelativelylarge,asisthecaseforsoleintheBayofBiscay[1].Thisreviewisbasedmainlyonresultsthathavealreadybeenpublished.Ourintentionistoclarifytheimportanceoftwoaspectsofthelifecycle,metamor-phosisandnurserycolonisation,indeterminingsolerecruitmentintheBayofBiscay.Theapproachadoptedinthisstudyistoexplainthepotentiallinksbetweenhowtheseeventshappenandtheirimmedi-ateorsubsequentconsequencesonthefateofyoungsole.TheresultspresentedherearebasedonaseriesofsamplingcruisesinthenorthernpartoftheBayofBiscayin1992and1993betweenadepthof100mandthemouthoftheVilaineestuary,andonafollow-upstudyofthisestuaryoverseveralyears).ThesamplingproceduresusedduringthesecruisesaredescribedindetailinAmaraetal.[4],MarchandandMasson[48]andAmaraandBodin[2].Forconvenience,wehaveusedascaleofstages(4and5)andsub-stages(4b,5aand5b)todescribethemainphasesofmetamorphosis[41].Themostobvi-oussignthatmetamorphosishasbegunistheinitia-tionofocularmigration,whichisclassi®edunder R.AMARAetal.OceanologicaActa23(2000)469±484 sub-stage4b.The®nalphaseofmetamorphosistakesplaceatsub-stage5b.Ourobjectivesweretherefore(i)todescribemetamorphictraitsandtoplacethekeystagesofmetamorphosisintheecologicalcontextofthedistributionoflarvaeandtheirprey,(ii)toanalysethenutritionalconditionoflarvaeduringthisphase,and(iii)toexaminetheprocessesinvolvedintheestuarinecolonisation.2.THEONTOGENETICANDECOLOGICAL2.1.SizeandageattheonsetofmetamorphosisThe1992and1993cruisesprovideduswiththepossibilitytostudythemagnitudeoftheseasonalandFigure1.Mapofthestudiedarea,showingtheonshore±offshoretransectsurveyedduringcruisesbyusingthe`ZeÂbulon'andthelocationofthestationsampledforanalysesofthemeiofauna.ThemainsolespawninggroundsareindicatedaccordingtoKoutsikopoulosetal.[38](soleeggdensitiesnumberper100m10;5±10;1±5). R.AMARAetal.OceanologicaActa23(2000)469±484 Figure2.Sizeandage(indays)attheonsetofmetamorphosis(stage4b)ofsolelarvaecaughtin1992.Eachpointonthebivariateplotrepresentsthelengthandageofanindividual(n171).N:numberoflarvae.Sizehistogram(n472);agehis-togram(n185)(modi®edfrom[3]).therelativelyconstantsizeof8.5mm1.3mmandseasonal,yearlyandspatialcomparisonsshowthatthissizedoesnotvarysigni®cantly().Incontrasttothis,therearelargeseasonalandyearlyvariationsintheageatwhichmetamorphosisstarts(e.g.41daysinFebruarycomparedwith25daysinMay1992)().Thisdependsondifferencesinthegrowthrate,whichinturnarecorrelatedwithtemperaturechangesandfoodavailability[3].Itisworthnotingthatin1993therewerenoseasonalvariationsintheageoflarvaeattheonsetofmeta-morphosis().Thisisprobablyduetothefactthatin1993temperatureswererelativelystabledur-ingtheperiodwhenthelarvaewerepresent,com-paredtothesameperiodin1992.AccordingtoFage[24],durationandsizeare``speci®cconstants''thataremodulatedby``thesubtletiesoflife'sphenom-ena''.Sizeattheonsetofmetamorphosisisconsider-ablylessvariablethanagefortheBayofBiscaysole:thecoef®cientofvariationforsizeis0.08,comparedwith0.2forage.SimilarresultswereobtainedwithsolefromthewesternpartoftheChannelandfromthesouthernpartoftheNorthSea(Amara,unpub-lisheddata).Theseresultsareinagreementwiththoseontheageandsizeatmetamorphosisofother¯at®shspeciesrearedinhatcheries[14,36,56].Thisphenomenonhasalsobeendemonstratedwithcoralreef®sh[20,49,65].Themetamorphosisofthesoleseemsthentobeconditionedbytheacquisitionofacompetentsize.Isthisasuf®cientreasontoconcludethatsizeisthedeterminingfactorfortheinitiationofmetamorphosisashasbeensuggestedbyPolicansky[56]forthePaci®cplaicePlatichthysstellatusVictor[65]forthelabridThalassomabifasciatumGenerallyspeaking,achangeinhabitatisoftenmorecloselyrelatedtosizethantoage[27].Furthermore,foragivenspecies,ontogeneticchangesaremorecloselyrelatedtosizethantotheageofthe®sh[16,26].Fishmetamorphosisisacomplexprocessinvolv-ingendocrinalsystemswhosestimulationisunderthecontrolofclimatic(temperature)andnonclimatic(photoperiod)factors[33,68].Theinitiationofmeta-morphosisinthePleuronectidaeisoftenassociatedwithanincreaseinthesecretionofthyroidhormones[35],andthishasalsobeenobservedinthesole[54].LikeChambersandLeggett[14],weviewsizeasacharacterthatdescribesanindividualatmetamor-phosisratherthaninvokingadependencyofmeta-morphosisonthatcharacter.Figure3.Seasonalchangesinthemeanlarvalsize(2standarddeviations)attheonsetofmetamorphosis(nyearlyvariationsinsizeandageattheonsetofmetamorphosis.Thetransectsamplingalsohadtheadvantageofidentifyingpossiblegradientsfromthecoasttotheopensea[3].Theageoflarvaeattheonsetofmetamorphosis,asestimatedfromotolithmicrostructureanalysis,variesbetween20and46days(notincludingtheembryonicperiod)andtheirsize(standardlengthLs)variesbetween6.9and10.4mm().Thereisnosigni®cantcorrelationbetweensizeandageattheonsetofmetamorphosis0.02).Solelarvaebegintometamorphoseat R.AMARAetal.OceanologicaActa23(2000)469±484 Figure4.Sizesofsolelarvaeattheonsetofmetamorphosis(n402)alongthesurveyedonshore±offshoretransect(modi®edfrom[3]).Figure5.Seasonalchangein(a)meanages(2standarddeviations)oflarvaeattheonsetofmetamorphosisin1992and1993and(b)watertemperaturerecordedat4mbelowthesurface.2.2.Modi®cationsinverticalandhorizontalAseriesofsolelarvaesampleswastakenovera28-hourperiodinApril1991froma®xedstationlocatedintheoutermostpartofVilainebay(atadepthof40m),usingalternatelyasupra-benthicsampler,(the`ZeÂbulon'[21])andaplanktonnet.ComparingthecapturesoftheZeÂbulonwiththoseusingplanktonnetscon®rmedthatthebottom R.AMARAetal.OceanologicaActa23(2000)469±484 Figure6.Percentage(combined-24hcatches)ofsolelarvaeofdifferentdevelopmentalstagesintheplanktonandbottomsam-plestakenata®xedstation.inephaseintheirlifecycle,larvalandyoungjuvenilebehaviourisoftensynchronisedwiththetides(selec-tivetidaltransport)[11,58].Comparisonsmadewiththethickbacksole(),aspecieswhichneverleavesthecontinentalshelfandwhoseentirelifecycleiscompletedwithoutiteverenteringthelittoralzone,showthatthecharacteristicsthatdifferentiatethisspeciesfromthesole(appearduringthelatelarvalstages[6].Theseincludeverticaldistribution,theextentofnycthemeralmigra-tionandthepresenceorabsenceofaswimbladder.Theswimbladderofisin¯atedatthebegin-ningofmetamorphosis[9]whereasitisabsentin.Theswimbladderfunctionsduringthebehaviouraldevelopmentoflarvaearepoorlyunder-stood.Inadditiontoitshydrostaticfunction,theswimbladdercouldplayaroleinrecordinghydro-staticpressurevariationslinkedtothetide[30].In-deedthein¯ationofthesole'sswimbladderduringmetamorphosiscoincideswithanincreasedsensitivitytopressurevariationsoftidalamplitude[45].ThissupportsthehypothesisputforwardbyF.LagardeÁre[39]thatmetamorphosinglarvaecouldbetransportedtowardthecoastbytheselectiveuseoftidalcurrents,andinthiswaycolonisethenurseries.Asforhorizontaldistribution,themajorityoflarvaethatbegintometamorphose(stage4b)arefoundonthecontinentalshelfbetween20and90kmoffshore).Nevertheless,afterthisstageveryfewmetamorphosinglarvae(stages5aand5b)arecap-turedaroundthespawningground;mostcapturesaremadenearthestationsthatareclosesttothecoast[4and42].Thisdistributionpatternisalsotrueforotherspeciesof¯at®sh[36].2.3.MeiobenthicresourcesbeyondthecoastalThefactthatthemajorityoflarvaebegintometa-morphoseonthecontinentalshelfimplieseitherthatthereisatransferoflarvaetothecoastduringmetamorphosis,orthatsomelarvaesettleoffshoreorperhapsevennearthespawningground.However,noneofthenewlysettledsolehaveeverbeencap-turedbeyondthecoastalnurseries[4,37],incontrasttotheyoungbenthicstagesoftheotherspeciesof[6].ThisbegsthequestionastowhathappenstosolethatsettleontheFigure7.Percentageofsolelarvaeofdifferentdevelopmentalstagesobtainedfrombottomdaynightsamples.samplerpicksupmainlythelatelarvalstages.Thelatterarepoorlyrepresentedinthewatercolumn,asituationwhichisexactlytheoppositeforthe®rststagesofdevelopment().Thedistributionofcapturesnearthesea-bedshowsthatlarvaearemoreabundantduringtheday().Thiscanbeexplainedbythefactthatasearlyasthe®rstfeedingstages(stage2),solelarvaemigratetowardthesur-faceatnightandareconcentratedinthebottomlayersduringtheday[38].Thisnycthemeralverticallarvalmigrationwasobservedwiththesamespeciesrearedintankexperiments[18].Duringdevelopment,many®shmoveactivelyandpassivelyfromspawningareastocoastalnurseries.InthenorthernBayofBiscay,solespawninggroundsareoffshoreintypicallymarinewaters,whereasnurs-eriesareincoastalandestuarineareas.AccordingtoKoutsikopoulosetal.[38]diffusioncouldberespon-sibleformostofthetransportoflarvaetothecoast.However,recent®eldandexperimentalstudiesindi-catethatverticalmigrationofmetamorphosinglar-vaeandnewlysettledjuvenilesareinvolvedinthemigrationfromoffshorespawningareastocoastalnurseries[17,19,42].Forspeciesthathaveanestuar- R.AMARAetal.OceanologicaActa23(2000)469±484 bottombeforetheycanreachthecoast.Inhistrans-porthypothesis,Hjort[32]suggeststhatmetamor-phosinglarvaethataretransportedtodepthsinappropriateforsettlementarelosttothepopula-tion.AccordingtoGibson[29],theavailabilityoffoodandpredationarethetwomostimportantfac-torswhichdeterminethequalityofthejuvenile¯at®shhabitat.In1993,westudiedthemeiobenthictrophicenviron-mentat®vestationswheresolelarvaewerelikelytosettle,lyingbetweenadepthof100mandthemouthoftheVilaineestuary().Thesestationshaveahighdensityandbiomassofpotentialmeiobenthicpreyforyoungsole.Nearthespawninggroundwherethemajorityoflarvaebegintometamorphose[4],theharpacticoidcopepods,whicharethepreferredpreyofyoungbenthicsole[2,13,48],arevariousandabundant(.Theseresultssuggestthatthefateoflarvaewhichsettlebeforereachingthecoastalnurseriesisprobablynotdeterminedbythequalityandthequantityofbenthicfoodavailableatthesedepths.3.NUTRITIONALCONDITIONOFMETAMORPHOSINGLARVAE3.1.NutritionandfeedingrateThefeedingactivityandverticaldistributionoflarvaeareimportantforourunderstandingofthemecha-nismswhichleadtothecolonisationofcoastalnurs-eries.Forthisreason,wecarriedouttwo24-hoursamplingcyclesin1993intheoutermostpartofVilainebay[42].Ananalysisofthegutcontents(stages4band5a)showthatmetamorphosinglarvaeingestmainlyplanktonicprey(around80%)(mainlycopepods,cladoceransandnauplii)althoughsomeepibenthicprey(polychaetesfragments,harpacticoidcopepods,smallbivalvesandgastropods,andveryfewam-phipods)begantocontributetolarvaldiet.Thequantityoffoodingestedduringeachsamplingcyclewasanalysedintermsofcarbonandnitrogencontent[42].Thequantityofcarbonandnitrogenbeginstodecreaseattheendofthedayandislowestatdawn,afterwhichitstartstoincreaseagain().Thisindicatesthatlarvaeundergoingmetamorphosishavenotmodi®edtheirpreviousfeedinghabits,sincetheycontinuetofeedonplanktonduringthedayanddigesttheirpreyatnight.Inthenurseries,soleattheendofmetamorphosis(stage5b)thatareintheprocessofsettlingonthebottomcontinuetomigrateupthewatercolumnatnight.Atthisstagetheyfeedontheepibenthicmeiofauna(mainlyharpacticoidcopepods)then,withincreasingage,theybegintoconsumetheendobenthicpreythatliveinthetoplayersofthesediment[47,2].Theseresultssuggestthattheverticalmigrationsobservedinlarvaeunder-goingmetamorphosisorinyoungsoleintheestuaryFigure8.Densityofmetamorphosinglarvaealongtheonshore±offshoretransect.stage4b(onsetofmetamorphosis);stage5b. R.AMARAetal.OceanologicaActa23(2000)469±484 Figure9.DensityofmeiofaunaateachstationsampledontheshelfinApril1993(from[2]).isnotrelated,atleastdirectly,totheirfeeding3.2.NutritionalconditionNumerousstudieshaveunderlinedtheimportanceofthemortalitythatoccursduringorjustaftermeta-morphosis[8,36,62]butveryfewhavelookedatthenutritionalstatus(orcondition)oflarvaeduringthisphase[10,50].Thepassagetoanewkindofhabitatexposestheyoung®shtonewsourcesofcompetition(intra-andinter-species)andpredation.Asaresult,theconditionofthe®shatthebeginningofmetamor-phosismaydeterminetheirsurvival.Usingtheratioofthequantityoftriacylglycerol(highenergylipidreserves)tothatofsterol(structurallipids)(TAGST)[28,31],whichisanutritionalconditionindexthatisverysensitivetostarvation,wetestedthehypothesisthatfromametabolicpointofviewmeta-morphosiscorrespondstoacriticalphase.Thechangeintheaveragetriacylglycerolcontentsduringontogenicdevelopment()showsthatlarvaeaccumulatetriacylglycerolandreachmetamor-phosiswithprobablyenoughenergyreservestocover R.AMARAetal.OceanologicaActa23(2000)469±484 theextraenergyrequirementsofthisphase.Ehrlich[23]alsofoundthiswithplaice.Thenutritionalcon-ditionoflarvaeattheonsetofmetamorphosisshowssigni®cantseasonaldifferences(F3,8115.9;0.001),butnoclearpatternemerges(Nevertheless,ineachofthecruisestheaverageTAGSTratiooflarvaeattheonsetofmetamorphosiswasalwaysgreaterthan1,theexperimentalvaluebelowwhichundernutritionismanifestinsolelarvae[28].Thereareyearlydifferencesinthenutritionalcondi-tion:in1993amuchhigherpercentageoflarvae(39%)wereinapoornutritionalcondition(TAG1)comparedwith1992(15%).TheindividualTAGSTvaluesoflarvaeattheonsetofmetamorphosisasafunctionofthedistancefromthecoastwheretheywerecapturedisshownonThereisawidedistributionofvalues,withlargevariationsatasinglestation.However,thenutri-tionalconditionofthelarvaedoesnottendtoim-provealongagradientrunningfromtheopenseatothecoast.Whateverthedistancefromthecoast,themajorityoflarvaehaveasatisfactorynutritionalcondition(TAGThusfromanutritionalpointofviewmetamorphosiscannotbeconsideredtobeacriticalphasefortheBayofBiscaysole.Indeed,thereisnotrophiccrisisduringthisphase:thegutfullnessindexcalculatedduringthetwo24-hourobservationcyclesin1993showthatonly16%and36%ofmetamorphosinglarvaeexaminedhademptyguts[42].Ithasbeenshownthatsolelarvaearehighlyresistanttostarva-tionduringthisdevelopmentalstage[57].Moreover,growthiscontinuousduringthisphase;thetotallength(Lt)oflarvaegrewfrom9mmatstage4b(onsetofmetamorphosis)[3]to10mmwhentheyenteredtheBayofVilaine,mainlyatstage5a,andto12mmwhentheysettledintheestuaryatstage5b(endofmetamorphosis)[46].Triacylglycerolsareusedforenergyrequirementsandarethusadirectmeasureofalarva'spotentialforwithstandingperiodsofstarvation[31].Ifoneacceptsthatthevulnerabilityoflarvaetopredationdependsmainlyontheirnutritionalcondition[25,44],thelipidindexesbasedontriacylglycerolcontentsmaybeconsideredtobeameasureoftheprobabilityofshortandmediumtermsurvival.Basedonthis,ourresultssuggestthatduringanygivenyear,larvaefromdif-ferentcohortsprobablyhavethesamechanceofsurvivalduringorjustaftermetamorphosis.Figure10.BiomassofpotentialsolepreyateachmeiofaunastationinApril1993(from[2]). R.AMARAetal.OceanologicaActa23(2000)469±484 Figure11.Hourlyvariationsinthemeancarbonandnitrogencontent(1standarddeviation)inthegutcontentsofmetamorphosingsolecaughtinlateApril1993,asafunctionofdaytimeillumination(arrowsgivehoursofsunsetandsunrise,respectively)(datafrom[42]).4.COLONISATIONOFCOASTALNURSERIES:THECASEOFTHEVILAINEESTUARYSurveyswerecarriedoutfrom1986to1990[48,47]andin1992[5]intheVilaineestuary.Thesestudiesshowedthatyoungsoleentertheestuaryattheendofmetamorphosis,mainlyatstages5aand5bandasnewlysettledsole.EstuarinecolonizationtakesplacebetweenthebeginningofAprilandthemonthofJune,withanin¯uxtothenurserythatmaybeconcentratedinasingleperiod(April)orbespreadoutfromApriltoJune[48].InApril,colonizationalwaysbeginswithanaccumulationofyoungsoleattheentranceoftheestuary(Forplaice,Hovenkamp[34]showedthattheperiodoflarvalarrivalnearthenurseryareasandsubse-quentimmigrationandsettlementispotentiallycriti-Figure12.Meanandstandarddeviationoftriacylglycerolscon-tents(1standarddeviation)duringsolelarvaontogenesis(n R.AMARAetal.OceanologicaActa23(2000)469±484 Figure13.Seasonalvariationsinthemeantriacylglycerolsratio(1standarddeviation)oflarvaeattheonsetofmetamorpho-sisin1992(ninepenetration.Inthiscase,theyoungsolecanwaitinthebay,whichactsasa`transitzone'.Conversely,whentheriver¯owislow,thewindin¯uenceislessobviousandwhateveritsorientation,marinewatersentertheestuarinearea(mainlybythebottom)favouringestuarinepenetration.Acomparisonoftheverticaldistributionofmetamorphosingsoleandtheirpotentialpredators(e.g.Pleurobrachiapileus(Ctenophora)andAureliaaurita(Cnidaria))atthetimewhentheestuaryisbeingcolonizedshowsthattheriskofmortalityfrompredationislowduetothedifferenceintheirspatialandtemporaldistributions.Moreover,ananalysisofthedigestivecontentsofthepredatorsdidnotprovideanyevidencethatsolehadbeeningested[48].Thefactorswhichdeterminenurserycolonizationarepoorlyunderstood.Theroleofattractants(mainlyglycine-betain)inthesedimentandinfoodhasbeenmentioned[47].Experimentshaveshownthatthebehaviourofmetamorphosinglarvaeandsolejuve-nilesmaybedeterminedbynumerousfactorssuchaslight,gravity,substrate,food,salinity,pressureandcurrents[18].Thecombinedactionofthecurrentsandrheotaxisontheonehandandlightandpressureontheother,probablyinitiatesanactivemigrationcal.IntheBayofVilaine,thetimeofinitiationofsoleestuarinecolonizationcanvaryenormously,de-pendingonthebalancebetweenseawaterandriverwater,whichisregulatedbyacombinationofthedirectionandintensityofthewinds,theriver¯owandthetidalcycle.Acombinationofastrongriver¯owandoffshorewindisunfavourabletotheestuar-Figure14.sterolratiooflarvaeattheonsetofmetamorphosissampledalongtheonshore±offshoretransectin1992 R.AMARAetal.OceanologicaActa23(2000)469±484 Figure15.YearlycomparisonsofthespatialdistributionofjuvenilesoleintheVilaineecosystemfromApriltoJune(modi®edfrom[47]). R.AMARAetal.OceanologicaActa23(2000)469±484 thatallowstheyoungsoletoentertheestuaryandtosettlethere[19].Whatevertheprocessesthatdeterminetheirentryintotheestuary,theestuarinesystemwouldappeartobeanobligatorystepinthelifecycleofthesoleinthestudiedarea.Thismightberelatedtothewealthofpotentialpreyavailablethroughoutthesubmergedandintertidalzoneswhichcoversalargersurfaceinanestuary.Theyoungbenthicstagesfeedthereassoonasthetidalconditionsmakeitaccessible[40]andthehightemperaturesfoundinthiszonearefavourabletogrowth.Fromthecomparisonofthesolewithotherspecieswhoseyoungremaininthebay,suchasthedabLimandalimandaortheso-Buglossidiumluteum,itwouldappearthatthereisatropismtowardslowsalinityzones,imply-ingaspeci®cdegreeofdependencyontheestuary.5.CONCLUSIONInthenorthernpartoftheBayofBiscay,themeta-morphosisofthesoleisaparticularlywelladaptedprocesswhichendsthepelagicdisseminationphaseandoccurswithoutanutritionalcrisisorgrowtharrest.Moreover,someofourobservationssuggestthatthisperiodisoneof`convergence',whenthevariabilityinducedduringthelarvalphasetendstofade.Duringtheperiodjustaftermetamorphosis,whentheriskofpredationdependsonsize[64,67]ornutritionalcondition[44],thefactthatindividualsfromdifferentcohortsareofarelativelysimilarsizeandhavestoredsuf®cientenergysupplies(triacylglyc-erol)meansthattheyallhavethesameprobabilityofsurvivalwhentheyenterthebenthicenvironment.Indeed,metamorphosisseemstocontributetothehorizontaltransferoflarvae,whichfavoursentryintothecoastalzoneandcolonizationoftheestuary.Theriskofhavinganinsuf®cientquantityoffoodduringthisphaseorjustaftersettlementisslight.TheriskofpredationbyCtenophoraandCnidaria,whicharesometimesabundantinthecoastalzone,isinfactlowduringtheperiodwhentheestuaryisbeingcolonised,duetodifferencesinspatialandtemporaldistributionTheseconclusionsruncountertothegenerallyheldideathattheslowdowninfeedingandgrowthduring¯at®shmetamorphosisleadstoahighermortality.Mustweconcludethatintermsofwhatdeterminestherecruitmentofsoles,metamorphosisinitiatestheprocesseswhichdampenvariationsinthenumberofpre-recruitsthatoccupythenursery,resultinginarelativelyinvariablerecruitment[59].Metamorphosisdoesnotactuallyful®lthecriterianormallyat-tributedtoacriticalphase.However,thefateofnewlysettledjuvenilesinthenurseryisprobablyrathermoreuncertain.Thiswouldsuggestthattheyearclassisdeterminedeitherbeforemetamorphosisorduringthejuvenileperiod.AccordingtoMyersandCadigan[52],thisisthecasefordemersal®shpopulationsinwhichthevariabilityinyearclassstrengthhasitsorigininthelarvalphaseorrightatthebeginningofthejuvenileperiod.Themortalitywhichthenoccursduringthejuvenileperiod,pro-vokedbythelimitedspaceinthenurseries,onlyservestoreducethe¯uctuations.ThishasalsobeensuggestedbyRijnsdorpetal.[59]andVanderVeer[63]forNorthSeasoleandplaicerespectively.Thestudyofthecontrolandregulationprocessesthatmaytakeplaceduringthejuvenileperiodwillconstitutethenextstageofthisresearch,andshouldexplaintherelativestabilityofsolerecruitmentintheBayofBiscay.ThisstudywaspartofthePNDR-Soleprogramme.TheauthorsthanknumerouscollaboratorsfromtheIfremerECOHALlabora-tory(C.Koutsikopoulos,D.Dorel,P.Bourriau,P.Beillois,D.GueÂrault,P.Grellier),fromtheCREMAL'Houmeau(R.Galois,L.Joassard,K.Dalet)andtheSciencefacultyoftheBretagneOccidentaleuniversity(P.Bodin)fortheirhelpinthe®eldandthelaboratoryanalyses.Theyalsothanktheteamsoftheoceano-graphicboatsfortheirhelpduringthenumerousexpeditions.[1]AmaraR.,Lasole,Soleasolea(L.),dugolfedeGascogne:meÂtamorphose,transfertdeslarvesverslacoÃteetcolonisationdesnourriceries,theÁseUniv.Paris6,1995,250p.[2]AmaraR.,BodinP.,L'environnementtrophiquemeÂioben-thiqueendehorsdesnourriceriescoÃtieÁresest-ilfavorableaÁl'installationdesjeunessoles?,Oceanol.Acta18(1995)583± 481 R.AMARAetal.OceanologicaActa23(2000)469±484 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