Aikawá, Hideki

Strüssmann, Carlos A.

Takashima, Fumio

Tsuzuki, Mônica Y.

Brazilian Journal of Oceanography

English

Mônica Y. Tsuzuki

Hideki Aikawá

Carlos A. Strüssmann

Fumio Takashima

Crossref

Revista Brasileira de Oceanografia

Physiological responses to salinity increases in the freshwater silversides Odontesthes bonariensis and O. hatcheri (Pisces, Atherinidae)

Cadernos Espinosanos (E-Journal)

NoteRev.bras.oceanogr.,48(1):81-85,2000Physiological responses to salinity increases in the freshwatersilversides Odontesthesbonariensisand O.hatcheri(Pisces, Atherinidae)MônicaY. Tsuzuki\ HidekiAikawa2;CarlosA. Strüssmann1& FumioTakashima1lTokyoUniversityofFisheries,DepartmentofAquaticBiosciences'(4-5-7Konan,Minato-ku,Tokyo108-8477,Japan)e-mail:monica_tsuzuki@hotmail.com2InlandWaterExperimentalStation,KanagawaPrefectureFisheriesResearchCenter(Ooshima3657,Sagamihara-shi,Kanagawa-ken229-1135,Japan). Descriptors:Salinitytolerance,Cortisol,Osmoregulation,Stress,Pejerrey,Atherinidae.. Descritores:Tolerânciasalinidade,Cortisol,Osmoregulação,Estresse,Peixe-rei,Atherinidae.IntroductionMembersofthefamilyAtherinidaedisplayvariousdegreesof salinitytoleranceandasa resulttheyhaveradiatedintoawiderangeofenvironments(Hubbset ai., 1971;Bamber& Henderson,1988;Middaughet aI., 1990).The pejerreyor silverside,Odontesthesbonariensis(Valenciennes,1835),is animportantcommercialspeciesnativeto temperateand sub-tropicalinlandwatersof SouthAmerica.Pejerreyhasbeenintroducedintosevera1countries,includingJapan,asagamefishor asacandidatefortteshwateraquaculture(Bonetto& Castello,1985).The congenerico. hatcheri(formerlyPatagoninahatcheri;Dyer,1993),ttomffeshwatersofPatagonia,Argentina,isalsoapotentialspeciesforcu1tivationitemperateareas(Strüssmannetai.,1997).Although these speciesare commonlypropagatedin ffeshwater,preliminaryevidencegatheredin seedproductioncentersandcommercialfish farmsin Japansuggeststhatmoderatesalinitiesallowbetterperformance,in particulartheattaÍnmentof stab1esurvivalrates under stressconditions(Murayamaetai., 1977;Umezawa& Nomura,1984;Strüssmannet ai., 1996;Tsuzukiet ai., 2000b).Studieswithlarvaeandjuvenilesofbothspeciesalsoshowedbestsurvivalandgrowthratesatintermediatesalinities,althoughthe optimumsalinityfor eachspeciesvariedconsiderably(Tsuzuki,1999;Tsuzukietai.,2000a).Thepresentstudyhadthedualpurposeofcomparingthesalinitytoleranceof sub-adultsof O.bonariensisand O. hatcheri, and obtainingpreliminaryinformationontheirosmoregulatoryandcompensatorystressresponsesunderdifferentNaClconcentrations.Sodiumchlorideinsteadof seawaterwasusedinthisstudybecausethesearethesaltsmostcommonlyemployedto raise salinity duringhusbandrypracticesofthesespecies.Thus,therewasalso an interestin the elucidationof the relationbetweenNaClandimprovedperformance.Thestudyconsistedof the ana1ysisof survivaland bloodparameters(Na+ andcr ion levels,osmolality,hematocritandcortisol)in fishgraduallyor direct1yexposedtosa1initiesbetweenOand3.0%NaCl.MateriaisandmethodsThe experimentwas conductedwithhatchery-rearedsub-adults of Odontesthesbonariensis(meanbodyweightof 24.1g andtotallengthof 16.1em)ando. hatcheri(27.8g and18.1cm) at the Inland Water ExperimentalStation,KanagawaPrefectureFisheriesResearchCenter,Japan.Fishraisedin ffeshwaterweretransferredto200-litertanksandallowedto acclimateto thetanksin runningwater(O % NaCl) for 10 daysbeforeexperimentationata densityof 150fish/m3.Duringthisperiod,fishwerenotdisturbedexceptforfeeding,whichconsistedof theadministrationf commercialpellets(EX ayu#3;NihonNousanKougyouLtd.)twicedailytosatiation.No foodwasdistributed24hprior to and during the experimentalperiod.Temperaturewaskeptat19::I:1°candaerationwasprovidedtomaintaindissolvedoxygenearsaturationlevels.Naturalphotoperiodconditionswereusedinthe experiment.No mortalityoccurredduringtheacclimationperiod.In ordertomeasuretheosmoticandnormalcompensatorystressresponses,salinityin the test82 Rev.bras.oceanogr.,48(1),2000tankswasabruptlychangedtoO,0.5,1.0,2.0and3.0% NaCl,orgraduallyincreasedto 1.0,2.0and3.0%NaCl (increasesof 0.5% NaClperday),byadditionof a concentratedstocksolutionof NaCl. ThestocksolutionWa~preparedby dissolutionof commercial~rad\';NaClsaltin fTeshwater.Salinitywasmeasuredw\thapopticalrefTactometer(Atago)to thenearest0.1%.BIQodsampleswerecollectedfTom4-5fishfTomeachsalinitygroupimmediatelybefore,andat3, 9, 24and168h afierthesalinityincrease(ortheattainmentof the fmal salinitylevelsin gradualIyacclimatedgroups).For thi~purpose,fish werequicklyanesthetized(0.5mUI- 2ftphenoxyethanol),the size of the fish w'!arecorded,andbloodwasdrawnfTomcaudalvesseh!into lithium-heparinizedsyringes.Hematocritwasftl~{lSUfedimmediatelywithanautocritcentrifuge(ClayAdamsLtd.;11,500rpm,10minutes).Plasmawass@paratedfTomthewholebloodbycentrifugationat3,000rpmfor 10min,andstoredat - 85°C untUanal)'$is.The foUQwinganalysisweremade:plasmacortisol,with the1125radioimmunoassaycortisolkit (SPAC-SCortisolKit,Japan),osmolality,witha vaporpressureosmomet@r(WescorInc.), cr and Na+,with an ion meter(ShimadzuCIM-I04A). Becausep@jerreyof thesizeemployedin thisstudyhavelittleblood(only0.3-0.4ml can be takenfTom one individual),ít wasnecessaryto pool the bloodfrom alI fish in eachsamplingto obtainsufficÜmtvolumefor analysis.Duetothislimitation,individualvariationscouldnotbeassessed.However,becausesampleswerepooled,eachvaluesupposedlyapprQ"imatesthetruemennQf4-5 individuaIs.Survivalrateswere.calculatedITomthenumberof survivingfi!?llbetwee.neachsamplingperiod.Resultsand discussion.Thegradualacclbnationto salinityin dailyincrementsof 0.5%NaCl did.noteffectanychangesin theresultsof survival,osmoreg\llatoryandstressresponsesin comparisontothecorrespondinggroupssubjectedto directtransf~r,For thh3reason,dataforgradualIyacclimatedgroupsarenotpresentedin thefigures.NomortalityoccurredatsalinitiesbetweenOand2.0%NaCl forbothspecie!';(resultsnotshown).ln contrast,mortalityrates'reached100% within3hin o. hatcheriandwithin24h in o. bonariensisafiertransferto3.0% NaCl.Thus,theupperlimitforthesurvivalof sub-adultsof thesespedesfallsbetween2.0and3.0%NaCl.AlthQughthepresentstudydealtwith differentconcentrationsof NaCl insteadofseawater,theresultssuggesta toleranceto a widerangeofsalinities.Thismightindicatethatsub-adultsof both speciesare also euryhaline,as has beenobservedwith eggs,larvaeandjuveniles(Tsuzuki,1999;TsuzukietaI.,2000a),ConspicuouschangesinplasmaNa+,cr andosmolalityoccurredonlyat2.0and3.0% NaCl inbothspecies,wherealI threeparametersincreased,andatO% NaCl in o. bonariensis,wherecr levelsweresomewhatlowerthanatothersalinities(Fig.1).Decreasesandincreasesin plasmacr alsooccurredduringrecoveryafierstressat O and3.0% NaCl,respectively,in sub-adultsof stripedbassMoronesaxatilis (Cech et aI., 1996). Higher plasmaosmolality,Na+ or cr withincreasingwatersalinity\.Vasalsoobservedin otherspecieswhenindividuaIswere exposedto differentdilutionsof seawater(Morgan& lwama,1991;AltinoketaI.,1998;VoncketaI., 1998).In ourstudy,Odontesthesbonariensisseemedto osmoregulatemoreefficient1ythan o.hatcheriat2.0% NaCl astotalosmolality,Na+andcr returnedto basallevelswithin 1 weekin theformerbutnotinthelatterspecies.Hematocritvaluesvariedwidely,particularlyin o. hatcheri,precludingan accuratecomparisonbetweensalinitiesand species.However,valuesseemedto be lower in o. bonariensisthanin o.hateheriandtovarygrosslyin inverseproportiontosalinityin bothspecies(Fig. 1).The lowestvalueswereobtainedin animaIsat3.0% NaCljustbefore100 % mortality.A similartrendof decreasedhematocritvalue witb increasingsalinity wasobserved in chinook salmon Oneorhynchustshawytscha:fTy(Morgan& Iwama,1991)andinsturgeonAcipenseroxyrinehusde sotoi(Altinoketai.,1998)whenanimaIsweretransferredfTomdilutedto fullftstrengthseawater,On the otherhand,theoppositephenomenonoccurredin rainbowtroutO.mykiss(Morgan& lwama,op.eit.).Morgan& lwama(1991)attributedtbesevariableresponsesto species-specificdifferencesin red bloodcell andplasmavolumechanges.PlasmaCQrtisQlalso variedmarkedlybutvaluesweresomewhatlowerandmorestableat2.0and1,0% NaCl in O. bonariensisando. hateheri,respectively,comparedto othersalinities(Fig. 1).LQwel,'cortisolevelsmightsuggesteithera naturalpreferencefor these particularsalinity levels,resultingin decreasedcortisolsecretion,or anincreasinthemetaboliclearancerateofcortisol,asobservedbyNichols& Weisbart(1985)afieI,'transferof AtlanticsalmonSalmosalar to seawater.It isinterestingtonotethatanimaIskeptatO% salinity,originallyconsideredthenaturalconditionfor bothspecies,didnotpresentthelowestcortisolevels.Infact,thelowestlevelsfoundforbothspeciesatO%salinityintbisandsubsequentstudies(Tsuzuki,1999Tsuzukieta!.2000b)are7-to 10-foldhigherthanthebasal levei!!reportedfor stenohalinefteshwaterspeciesuchascarpCyprinuscarpio(AboHegab&Hanke,1984)andgoldfishCarassiusauratus(Barton& Iwama,1991).Incomparisontoeuryhalinespeciesrearedin freshwater,therestinglevelsforpejerreyTSUZUKI etai.:Physiologicalresponsesof atherinidfishtosalinity300===-250$200E-150"cu? 10050240_200M 160;S 120Õ 8040~550E 500rnO 450E;:400~ 350~ 300() 25090-~ 75~ 60CJO~ 45E~ 3015100-:ê 80O)2; 60~ 40to 20()OO. bonariensis16816883O. lzatclzeri30025020015010050240200160120804055050045040035030025090756045301510080604020O3 24 168o 9168o 3168olime (h)~ 0% NaCI [!iJ 0.5% NaCI A 1.0% NaCI V 2.0 % NaCI ~ 3.0 % NaCIFig. 1.PlasmaNa+,cr andosmolality,hematocritandplasmacortisolin sub-adultsof Odontesthesbonariensisando. hatcheriduringexposuretosalinitiesofO-3.0%NaCl.CortisolvaluesforO. bonariensisat3h for0.5and1.0% NaCI couldnotbeincluded ueto problemsduringanalysis.84 Rev.bras.oceanogr.,48(1),2000were 10- to 20-fo1dhigherthanthosefor ti1apiaOreochromismossambicus(Assem& Hanke,1981;AboHegab& Hanke,1984),and4- to5-foldhigherthanthosefor the stripedbassMoronesaxati/is(Barton& Iwama,1991;Cechet aI., 1996).Theformerisafreshwaterspecieswhereasthelatteris anestuarinespecies.The physio10gica1ndeco10gica1significanceof theseleve1sof cortiso1forpejerreyisstill unknown.However,since cortisolincreasesduringstressandsinceitpromoteswaterinfluxacrossthegillswithsubsequentlossofelectro1ytes(e.g.Cr)in tresh water (Mazeaud& Mazeaud, 1981;Wedemeyeret aI., 1990),highcortisolevelscouldprecipitateandJor potentiate osmoregu1atorydysfunctionat O % salinity.Likewise,treshwatermadedifficu1ttomaintainstableion levelsduringorafterstressin browntroutSalmotrutta(NikinrnaaetaI., 1983),walleyeStizostedionvitreum(Barton&Zitzow, 1995)and stripedbassMoronesaxatilis(Cechet.aI.,1996). .Theresu1tsofcortisolandcr ionobtainedinthe presentstudycouldbe an indicationthatO.bonariensisando. hatcheriarenottrulyadaptedtoO% salinity.Thishypothesis supportedbyevidencethat the familyAtherinidae,which is consideredprimari1ya marinecoastalgroup,only recent1yinvaded treshwaterenvironrnents(Bamber &Henderson,1988).In fact,many species of thegenusOdontesthesthatare regardedas treshwaterspeciescan be foundin brackishwaterssuchasin estuaries and lagoons (Martty, 1992),suggestingthatthetransition of thesespeciestotreshwaterenvironrnentsis still notcomp1eted.Onthe otherhand,theseobservationsare consistentwith the 1ackof differencesin salinityto1erancebetweensub-adultstransferredgraduallyor abrupt1yto different sa1initiesin this study,as well as inlarvaeandjuvenilesasreportedby Tsuzuki(1999)and Tsuzukiet aI. (2000a).Thislackof differenceseemsto becoherentwith a naturalability ofthese speciesto cope with short-term,abruptvariations in salinitythat can be expectedinestuarineenvironrnents(Bamber& Henderson,1988).The abovefindingssuggesthatthe sub-adu1tsof both species respond similarly atintermediatesa1initiesbutnotatextremeones.Thus,Odontesthesbonariensisseemsto toleratehighsalinitiesbetterthano. hatcheri,whereasthereverseoccursin low sa1inities.The resultsalso raiseaquestionon theadequacyof treshwater,especiallyduringsituationsof stress,for therearingof bothspeciesandpointto a possibleeffectof salinityonplasmacortisol1eve1s.Ongoingresearchshouldhe1pclarifYthepointsraisedinthisstudyandelucidatethephysiologicalroles of salts in the promotionofsurvivaland in the reductionof stress-inducedosmoticandionicimbalances.AcknowledgementsWe thankthe staffof the InlandWaterFisheries Experimental Station, KanagawaPrefectureFisheriesResearchCenter,for supportand for providingthe materiaIsand accesstofacilitiesfor this study.We a1sothankDr. JiroKoyamaandDr. MasashiMaitafor assistancewithion andcortiso1measurements.We appreciatedthetechnicalhelp of Chiho Shirakusaand MasamiHashimoto.Duringthis researchthe seniorauthorwassupportedby allowancestromtheMinistryofEducation,Science,Sportsand Cultureof Japan(Monbusho)andFapesp(Fundaçãode AmparoàPesquisadoEstadodeSãoPaulo).ReferencesAbo Hegab,S. A. & Hanke, W. 1984.Thesignificanceofcortiso1forosmoregu1ationin carp(Cyprinuscarpio) and tilapia (Sarotherodonmossambicus).Gen. Comp. Endocrinol.,54(3):409-417.Altinok,1.;Galli, S. M. & Chapman,F. A. 1998.Ionic and osmoticregulationcapabilitiesofjuvenileGulf of Mexico sturgeon,Acipenseroxyrinchusde sotoi.Comp.Biochem.Physiol.,120A(4):609-616.Assem,H. & Hanke,W. 1981.Cortiso1andosmoticadjustmentoftheeuryha1inete1eost,Sarotherodonmossambicus.Gen. Comp. Endocrinol.,43(3):370-380.Bamber,R. N. & Henderson,P. A. 1988.Pre-adaptiveplasticityin atherinidsandtheestuarineseatofteleostevolution.J FishBiol.,33:17-23.Barton,B. A. & Iwama,G. K. 1991.Physiologicalchangesin fish tromstressin aquacu1turewithemphasison the responseand effects ofcorticosteroids.Annu.Rev.FishDis.,1:3-26.Barton,B. A. & Zitzow,R. E. 1995.Physiologicalresponsesof juvenilewalleyestohand1ingstresswithrecoveryin sa1inewater.Prog.Fish-Cult.,57:267-276.Bonetto,A. A. & Castello,H. B. 1985.Pescaypisciculturaen aguascontinentalesde AmericaLatina.Washington,OEA. 118p.CechJr., J. J.; Bartho10w,S. D.; Young,P. S. &Hopkins,T. E. 1996.Stripedbassexerciseandhandling stress in treshwater:physiologicalresponsesto recoveryenvironrnent.Trans.Am.Fish.Soe.,125(2):308-320.TSUZUKI etai.:Physiologiealresponsesof atherinidfishtosalinity 85Dyer, B. S. 1993. A phy10geneticstudy ofatheriniformfisheswitha systematicrevisionoftheSouthAmericansi1versides(Atherinomorpha,Atherinopsinae,Sorgentinini).Tesededoutorado.UniversityofMichigan.596p.Hubbs,C.; Sharp,H. B. & Schneider,1. F. 1971.Deve10pmenta1r tesof Menidia audenswithnoteson saltto1erance.Trans.Am. Fish. Soc.,100(4):603-610.Martty,H. 1992.ManualdeIpejerrey(nomenclatura-reproducción-pesca).BuenosAires, A1batroz.159p.Mazeaud,M. M. & Mazeaud,F. 1981.Adrenergicresponsestostressinfish.10:Pickering,A D.,ed.Stressandfish.London,AcademiePress.p.49-75.Middaugh,D. P.; Hemmer,M. J.; Shenker,1.M. &Takita,T. 1990.Laboratorycultureofjacksmelt,Atherinopsis californiensis, and topsmelt,Atherinopsisaffinis(Pisces:Atherinidae),withadescriptionof larvae.Calif.Fish Game,76(1):4-13.Morgan,1. D. & Iwama,G. K 1991.Effectsofsalinityongrowth,metabolism,andionregulationin juvenile rainbow and steelheadtrout(Oncorhynchusmyskiss)andfalI chinooksalmon(Oncorhynchust hawytscha).Cano1.Fish.Aquat.Sei.,48:2083-2094.Murayama,T.; Nishihara,A T.; Ishizaki,H. &Oyama,S. 1977.Highdensityrearingof pejerreyO. bonariensisin brackishwater.Rep.KanagawaPref.Freshwat.FishProp.Exper.Station,13:22-26.Nichols, D. J. & Weisbart,M. 1985.Cortisoldynamicsduringseawateradaptationof Atlanticsalmon,Salmosalar.Am. 1.Phys.,248(6):R651-R659.Nikinrnaa,M.; Soivio,A; Nakari,T. & Lindgren,S.1983.Hauling stressin brown trout (Salmotrutta):physio10gica1responsesto transportinfreshwateror saltwater,andrecoveryin naturalbrackishwater.Aquacu1ture,34(1-2):93-99.Strüssmann,c. A; Moriyama,S.; Hanke,E. F.;Ca1sinaCota, 1. C. & Takashima,F. 1996.Evidenceof thermolabi1es x determinationipejerrey.1.FishBiol.,48(4):643-651.Strüssmann,c. A; Akaba,T.; Ijima,K; Yamaguchi,K.; Yoshizaki, G. & Takashima,F. 1997.Spontaneoushybridizationin thelaboratoryandgeneticmarkersfor theidentificationof hybridsbetweentwo atherinidspecies,Odontesthesbonariensis(Valenciennes1835)andPatagoninahatcheri (Eigenmann1909). Aquac. Res.,28(4):291-300.Tsuzuki,M. Y. 1999.Effectsof salinityonviability,physiologyandstressinducedresponsesin th~pejerreyOdontesthesbonariensisando. hatcheri.Tesededoutorado.Tokyo,TokyoUniversity()fFisheries.85p.Tsuzuki,M. Y.; Aikawa,H.; Strüssmann,C. A &Takashima,F. 2000a.Comparativesurvivalaridgrowthof embryos,larvae,and juvenilesOfpejerreyOdontesthesbonariensisandO. hatcheriat different salinities. 1. Appl. IchthYol.,16(3):126-130.Tsuzuki,M. Y. Ogawa,K; Strüssmann,C. A.; Maita,M. & Takashima,F. 2000b. Physiologicalresponsesduringstressandsubsequentrecoveryat different salinities in adult pejerreyOdontesthesbonariensis.Aquaculture(inpress).Umezawa,K & Nomura,H. 1984.TransportationfpejerreyOdontesthesbonariensis.Rep. SaitamaPref.Freshwat.FishProp.Exper.Station,43:82-86.Vonck,A P.M. A; Bonga,S.E. W.& Flik,G. 1998.Sodiumand calciumbalancein mozambiquetilapia, Oreochromismossambicus,raised atdifferentsa1inities.Comp. Biochem.Physiol.,1I9A(2):441-449.Wedemeyer,G. A; Barton,B. A & McLeay,D. 1.1990.Stressandacclimation.10:Schreck,C. B. &Moy1e,P. B., eds.Methodsfor fish bio10gy.Bethesda,AmericanFisheriesSociety. p. 451-489.(Manuscriptreceived29July 1999;revised24April2000;accepted29 June2000)

Directory of Open Access Journals

http://www.scielo.br/pdf/rboce/v48n1/07.pdf

Physiological responses to salinity increases in the freshwater silversides Odontesthes bonariensis and O. hatcheri (Pisces, Atherinidae)

Abstract

Similar works

Full text

Available Versions

Crossref

Cadernos Espinosanos (E-Journal)

Directory of Open Access Journals