TheAmericanbrineshrimpasanexoticinvasivespeciesinthewestern
Mediterranean
FranciscoAmat1,*,FranciscoHontoria1,OlgaRuiz1,AndyJ.Green2,MartaI. Sanchez2,JordiFiguerola2FranciscoHortas3
1Instituto deAcuiculturadeTorredelaSal(CSIC),12595RiberadeCabanes(Castello´n),Spain;
2Estacio´nBiolo´gicadeDon˜ana(CSIC),Avda.Marı´aLuisas/n,Pabello´ndelPeru´,41013Sevilla,Spain;
3GrupodeConservacio´ndeHumedalesCosteros,Departamento deBiologı´a,FacultaddeCienciasdelMary
Ambientales,Apartado40,11510PuertoReal(Ca´diz),Spain;*Authorforcorrespondence(e-mail: amat@
iats.csic.es;fax:+34-964-319509)
Keywords:Artemia,aquaculture,salterns,westernMediterranean
Abstract
ThehypersalineenvironmentsandsalternspresentinthewesternMediterranean region(includingItaly, southernFrance,theIberianPeninsulaandMorocco)containautochthonousformsofthebrineshrimp Artemia, withparthenogeneticdiploidandtetraploidstrainscoexistingwiththebisexualspeciesA.sal- ina. Introduced populationsoftheAmericanbrineshrimpA.franciscana havealsobeenrecordedin theseMediterraneanenvironmentssincethe 1980s.Basedonbrineshrimpcystsamplescollectedinthese countriesfrom1980until2002,wewereabletoestablishthe presentdistributionofautochthonousbrine shrimpsand ofA.franciscana, whichisshowntobeanexpandinginvasivespecies.Theresultsobtained showthatA.franciscana isnowthedominantArtemia speciesinPortuguesesalterns,alongtheFrench MediterraneancoastandinCadizbay(Spain).Co-occurrenceofautochthonous(parthenogenetic)and AmericanbrineshrimppopulationswasobservedinMorocco(MarChica)andFrance(AiguesMortes), whereasA.franciscana wasnotfoundinItaliancystsamples.TheresultssuggesttheseexoticA.francis- canapopulationsoriginateasintentionalornon-intentionalinoculationsthroughaquacultural(hatchery effluents)orpetmarketactivities,andsuggestthatthenativespeciescanberapidlyreplacedbytheexo- ticspecies.
Introduction
ThebrineshrimpArtemia (Branchiopoda,Anos- traca)isperhapsthe mostconspicuousinhabitant of hypersaline lakesandlagoonsandsolarsal- ternponds,coastalandinland,overtheworld, wheresimpletrophicstructuresandlowspecies diversityarepresent(LenzandBrowne1991).
ThegenusArtemiacomprisesagroupofbisex- ualandparthenogenetic species,whichprobably divergedfiveto sixmillionyearsago froman ancestralformliving intheMediterraneanarea (Abreu-GroboisandBeardmore1982;Badaracco
et al. 1987). The stringof shallowbrinylakes intowhichtheMediterraneanseahadconverted (Hsuetal.1977)createdopportunitiesforcoloni- zation,extinctionandrecolonizationcycleswith differentdegreesofreproductive isolation,while the appearanceof a parthenogeneticmodeof reproduction,togetherwithpolyploidy,mayhave facilitateddispersion.Thus, the Mediterranean hasbeenproposedasthecentreofradiationfor Artemia, basedon changesinreproduction modes,bisexualityand parthenogenesison the onehand,togetherwithdiploidyandpolyploidy onthe other(Gajardoetal.2002).
On the basis of criteria from morphometry andlaboratoryreproductiveisolation,andsubse- quentlythroughkaryology,allozymedivergence andnewmolecular(DNA)markers,sevenbisex- ualspecies andtwoorthreeparthenogenetic formsarecurrentlyrecognized inthegenusAr- temia.They alllookrathersimilarinbodyshape, butshowmorphologicaltraitsthatenablemor- phometricdifferentiation whentheyarecultured understandardlaboratoryconditions(Hontoria andAmat1992a,b).
ThebisexualA.persimilis(PiccinelliandPros- docimi1968)(ArgentinaandChile)andA.fran- ciscana(Kellogg1906)(North,CentralandSouth America)areendemicto theNewWorld.The bisexualA. salina Leach 1819 (Mediterranean area and Africa), A. urmiana (Gunther 1890) fromIran,A.sinica(Cai1989)fromP.R. China, andA.tibetiana (Abatzopoulosetal.1998,2002) fromTibet, withArtemia sp.fromKazakhstan (PillaandBeardmore1994)areendemicto the OldWorld. Recently,the AmericanspeciesA. franciscana hasbeenintroduced intheOld World,especiallyintheFarEastandintheMed- iterraneanarea,asexplainedinthisstudy.
The parthenogenetic forms, withdifferent degreesofploidy,arepresentintheOldWorld, i.e.EurasiaandAfrica,andwereintroducedin Australia.Althoughtheseformsarelistedtaxo- nomicallywiththe binomenArtemia partheno- genetica, thewidediversity foundamong differentasexual populations,especially interms of ploidy,suggeststhat theirgroupingundera singlespeciesmaybemisleading (Browneetal.
1991; Gajardo etal. 2002). The distribution of Artemia populationsinthewesternOldWorld, includingItaly,southofFranceandtheIberian Peninsula(SpainandPortugal),togetherwiththe northofAfrica,isespeciallyinterestingowingto thepresenceanddistributionof theMediterra- neanbisexualA.salina and,atleast,twodiffer- entparthenogeneticforms,diploidandtetraploid (Artom1906;Stella1933;Gilchrist1960;Stefani
1960;Amat1983a,b;Vieira andAmat1985; Vanhaeckeetal.1987;Amatetal.1995;Tryan- taphyllidisetal.1997a,b).
Thisregionalsoshows theunfortunateevent ofthepresenceoftheAmericanspeciesArtemia franciscana (Narciso1989;Hontoriaetal.1987; Amatetal.1995).Thispaperaimstoreviewthe currentdistributionofA.franciscana populations
in the westernMediterraneanregionandtheir likelyorigins.Wealsocomparethebiometryof bothintroducedandautochthonouspopulations, andconsidertheimpactoftheexoticspecieson the nativeones.
Materials andmethods
Thisresearch wascarriedoutusingalargecol- lectionof Artemia cystsamplesintheInstituto deAcuiculturadeTorredelaSal(CSIC), sup- portedbythesamplesavailablefromtheArtemia ReferenceCenter(UniversityofGhent,Belgium), and a databaseof morphometriccharacteriza- tionsof adultspecimens fromdifferentArtemia populationsand species.This databaseuseda
‘morphometricstandard’describingthepopula- tionsobtainedafterhatchingthesecystsinthe laboratoryandtheircultureunderstandardcon- ditions(Hontoria andAmat1992a).
The cystcollectioncontainedabout 130 cyst samplesfromWesternEurope(Spain,Portugal andItaly)collectedsince1980.During2001and
2002, newcystsamples weretakenfromthe southwest of Spain andPortugal(by the authors),andthesoutheastofFrance(provided byDrThomasLenormand,UniversitedeMont- pellier,France),theEuropeanregionswherethe invasive presenceof A. franciscana wasfirst reported (Narciso 1989; Thiery and Robert
1992).WealsoanalysedcystsofasexualArtemia thatweextractedfromthepelletsofRedshank Tringa totanus that werecollectedfrom Cadiz BayinJulyandAugust2002(A.J. Green,M.I. Sanchez,F. Amat, J. Figuerola, F. Hontoria, O.Ruiz,F.Hortas,unpublishedmanuscript).
CystsfromItaly(DrGraziellaMura,Univer- sityofRome)andfromPortugal(DrMªElena Vilela,InstitutodeInvestigacaodasPescasedo Mar, Lisbon) were preservedin plastic bags undervacuum.Other cystssampleswerepro- cessedaccordingto standardized methods (VanhaeckeandSorgeloos1980) andstoredat
4°Cinsealedplasticbags.
Biometryofadults
Thenaupliiobtainedbycysthatchingweremade togrowupin5lplasticcontainers,with70gl)1 filteredbrine(seawaterpluscrudeseasalt),and
putonamixeddietofDunaliellasalinaandTe- traselmis suecica. The temperature wasmain- tainedat 24±1°C, undermildaerationat a
12D:12Lphotoperiod.Themediumwas moni- toredandrenewedevery2days.Once50% of thefemalesattainedfullovisacdevelopmentand the first ovoviviparousoffspringwasobserved, randomsamplesof 30 females(parthenogenetic andbisexual strains)and30males(bisexual strains)wereremovedfromtheculture,anaesthe- tizedand measuredundera dissectingmicro- scope.The followingmorphologicalparameters werequantifiedin eachspecimen:total length, abdominallength,widthofthirdabdominalseg- ment,widthoftheovisacinfemalesandwidth ofthegenitalsegmentinmales,lengthoffurca, numberofsetaeinsertedoneachbranchofthe furca,widthofhead,maximaldiameteranddis- tancebetween compoundeyes,lengthof first antennaandtheratioofabdominallength·100/ totallength.Thebiometricalanalysis ofthese datawasperformedviamultivariatediscriminant analysis(HontoriaandAmat 1992a) usingthe statistical package SPSS for Windowsversion
11.0(SPSSInc.,Chicago,Illinois,USA),andthe resultswereintegrated inthemorphologicaldata basedevelopedattheInstitutode Acuiculturade TorredelaSal(Amat etal.1995).
Biometryofcysts
Whencystsfromoldormishandledsamplesdid nothatch,itwasimpossibletoobtainlivingnau- plii;therefore,togrowuplaboratorypopulations toadulthood.Inthiscase,thepopulationspecific adscriptionwasobtainedthroughthebiometric studyofcysts,whichprovidesafittingalternative forthispurpose(VanhaeckeandSorgeloos1980; Hontoria1990).
Samples providing sufficient quantities of cystsallowed cystdiameteranalysiswithan electronicCoulterCounter® counter-sizer(Van- haecke and Sorgeloos 1980; Hontoria 1990). The other cyst samples were previously hydrated with 20gl)1 filtered seawater, at
28°C with continuousilluminationand aera- tion, and measuredundera dissectingmicro- scopetothenearestlm.Cystswere hatched understandardconditions:35gl)1 filteredsea water, at 28°C, with continuousillumination andaeration.
Severalcystsamplesdidnot hatchafter the firstattempt,andaccordingto the amountof cystsavailable,theyweresubmittedto twoor threehydrationanddehydration(24hovendessi- cation under39°C) cycles,and/or to a H2O2 treatment,processes that terminatediapauseof Artemia cysts(Lavens andSorgeloos1987; VanStappenetal.1998),beforeafinalattemptto hatchtheminordertoobtainlivingnauplii.
Results
Biometryofcystsandadults
Theinformation obtainedfromcystsamples fromPortugalisshowninTable1. Onlythose samplescollectedsince1990hatched.Laboratory populations showedtheexclusivepresenceofA. franciscana, basedonthemorphometricstudyof adultspecimens (Figure1). However,theinfor- mationfromcystbiometryallowsinferringthe presenceof A. franciscana intheAlgarvefrom thebeginning ofthe1980s.IntheSadoestuary area,thesituation issimilar, butOlhosand CachopossalternsmaystillhaveheldA.parthe- nogeneticapopulationsinthe1980saccordingto the cyst diameter that exceeded 260lm (Hontoria1990).IntheTejoestuary,itispossible to inferthepresenceof A. franciscana inAlco- cheteandBoavistasalterns inthe1980s,but autochthonousparthenogenetic(diploidandtetra- ploid)populations(cystdiameterbetween 260 and280lm)weredominant atthattime.Finally, intheEsmolassalterns,fromthedistrictofAve- iro,thepresenceofA.parthenogenetica wasstated byVieira(1990), butsamplescollectedin1991 showedtheexclusivepresenceofA.franciscana.
MorerecentcystsamplesfromHuelvaandCa- diz provincesinSpain,fromMarChica(Nador, Morocco)and fromtheSouthofFrancehatched successfully.Thepopulationsobtainedfromthese cystsverifiedthepresenceoftheautochthonous bisexual(A.salina)andtheparthenogeneticdip- loidandtetraploidstrains,togetherwiththeexo- tic A. franciscana (Table2). The Westernmost Spanishpopulations(OdielinHuelvaandN.S. delRocıoinSanlucardeBarrameda, Cadiz) showed theexclusive presenceofautochthonous populations(A.salina and/orA.parthenogeneti- ca) in variable ratios, whereasthe Moroccan
Table1. ArtemiacystsamplesavailablefromPortugal,meandiameterofcystsandtaxonomicalidentification.
Locality / Samplingdate / Cystdiameter(lm) / ObservationsMicro / C.C. / C.C.(*)
AlgarveProvince
SanFranciscosalterns / 1980–1981 / 243 / 236 / 238 / NH
MarinaBiassalterns / 1987 / 246 / 248 / – / NH
Olhaosalterns / 1985 / 247 / – / 259 / NH
Tavirasalterns / 1985 / 240 / – / – / NH
Olhaosalterns / 2002 / 253 / – / – / A.franciscana
Faro.Ludosalterns / 2002 / 245 / – / – / A.franciscana
CastroMarimsalterns / 2002 / 250 / – / – / A.franciscana
SadoEstuary
Batalhasalterns / 1986 / 236 / – / – / NH
Sadosalterns / 1987 / 248 / – / – / NH
Olhossalterns / 1986 / 262 / – / – / NH
Cachopossalterns / 1987 / 276 / – / – / NH
RioFriosalterns / 1993 / 228 / – / – / A.franciscana
Bonfimsalterns / 1996 / 224 / – / – / A.franciscana
TejoEstuary
Alcochetesalterns / 1988 / 259 / 256 / 266 / NH
Boavista salterns / 1987 / 258 / 260 / – / NH
MarinaNovasalterns / 1987 / 264 / 273 / – / NH
MarinaVelhasalterns / 1987 / – / 276 / – / NH
Providenciasalterns / 1987 / – / 276 / – / NH
AveiroDistrict
Esmolassalterns / 1985 / 266(**) / – / 263 / A.parthenog.(d)
Esmolassalterns / 1991 / 249 / – / – / A.franciscana
Esmolassalterns / 1993 / 248 / – / – / A.franciscana
Micro.: cystdiametermeasuredwithmicrometereyepiece.C.C.: cystdiametermeasuredwithCoulterCounter.C.C.(*): idem
(Hontoria1990);(**) Vieira1990;NH=Nohatchingcysts.(d):Artemiaparthenogeneticadiploid.
population showedamixtureoftheautochtho- nousdiploidparthenogenetic andtheAmerican species.However,thesalternslocatedinCadiz bayshowedtheexclusivepresenceofA.francis- cana. Frenchsamplescorresponded mostlytoA. franciscana populations,verifiedthroughspeci- mensobtainedundercultureor throughthose providedaspreservedsamples.InAiguesMortes, lowproportionsoftheautochthonouspartheno- geneticpopulation wererecorded.
Cystsamples availablefromItalyandthe informationobtainedfrom themare shownin Table3.Someofthesesamples,collectedbefore
1987,did nothatch.Laboratorypopulations obtainedfromviablecystsshowedthepresence oftheautochthonouspopulations,i.e.,thebisex- ualA. salina andboth parthenogeneticstrains, diploid andtetraploid.Accordingto data reportedpreviouslybyHontoria(1990),thecysts from the Comacchiosalternscorrespondto a parthenogenetictetraploidstrainbecauseoftheir
bigsize,while theSiciliansamplefromIsola Longa (Trapani) resembles the sizeof cysts obtainedforA.salina populationsfromTarqui- niaandSardiniansalterns.
Themultivariate procedureproduces12discri- minantfunctionsfor each analysis(malesand females).In the case of the females,the first
11functionssignificantly(P£0.01) accountfor theincreaseofvarianceexplainedwhentheyare included inthemodel.For males,theanalysis needsonlythefirsteightdiscriminantfunctions to completelyseparatethepopulationsstudied. Thesefunctionssignificantly(P£0.01) account for thevarianceexplained. However, inboth cases,the four firstdiscriminant functions account for the larger part of the variation (90.5%intheanalysispertainingtofemalesand
93.2%inthatforthemales).
Figures1and2summarizethecentroids(mean
pointsforeachpopulation)forthefirsttwodis-
criminantfunctionsobtained, for femalesand
FEMALES
4
2
0
-2
-4
-6-4-202468
Firstdiscriminantfunction
Figure1. Groupcentroidsofthe populationsstudiedforthefirsttwodiscriminantfunctionsresultingfromthediscriminantanaly- sisonfemalemorphometricvariables.
Table2. Artemiapopulationsobtainedinthe laboratoryfrom cystsamplescollectedinsouthwesternSpain, northofMoroccoand southeasternFrance,andtheirrelativespecificcomposition wheredifferentspeciesorstrainsappeared.
LocalitySamplingdateSpecificcomposition
Spain
HuelvaProvince
EsterosOdielsaltern06.2002A.parthenog.(d):97%A.parthenog.(t):3%
CadizProvince
N.S.delRocıosaltern / 01.2002 / A.parthenog.(d):98% / A.salina(bisex.)2%ElEstanquillosaltern / 01.2002 / A.franciscana
ElPilarsaltern / 06.2002 / A.franciscana
SanPascualsaltern / 02.2003 / A.franciscana
LaDoloressaltern / 02.2003 / A.franciscana
Morocco
LagunaMarChicasaltern / 06.2000 / A.parthenog.(d):80% / A.franciscana:20%
France
Sete-Listelsaltern / 05.2002 / A.franciscana
AiguesMortessaltern / 06.2002 / A.parthenog.(d):2% / A.franciscana:98%
Fossaltern / 05.2002 / A.franciscana(p.s.)
Pesquierssaltern / 05.2002 / A.franciscana(p.s.)
Hyeresaltern / 05.2002 / A.franciscana(p.s.)
ThauCastelansaltern / 05.2002 / A.franciscana(p.s.)
A.parthenog.(d):Artemiaparthenogenetica (diploid);(t):tetraploid;(p.s.):alcoholpreservedoriginalspecimens.
Locality / Samplingdate / Cystdiameter / ObservationsVenetoprovince
Comacchiosalterns / 1985 / 278 / NH
Apuliaprovince
MargheritadiSavoiasalterns / 1988 / 258 / A.parthenogenetica (d):67%
MargheritadiSavoiasalterns / 1988 / 267 / A.parthenogenetica (t):33%
A.parthenogenetica (d):22%
A.parthenogenetica (t):78%
Lacioprovince
Tarquiniasalterns / 2002 / 243 / A.salina
Siciliaprovince
IsolaLongasalterns / 1985 / 245 / NH
Sardiniaprovince
Cagliarisalterns / 1988 / 254 / A.salina
Carlofortesalterns / 1987 / 251 / NH
Carlofortesalterns / 1988 / 256 / A.salina
A.parthenogenetica (d)1%
SanAntiocosalterns / ? / 255 / A.salina
ARC579
SantaGillasalterns / 1994 / 253 / A.salina
Meandiameterofcysts(lm)measuredwithamicrometereyepiece.Relative specificcomposition wheredifferentspeciesorstrains appeared.(d):Artemiaparthenogenetica diploid,(t):tetraploid.
NH:Nohatchingcysts.ARC579:ArtemiaReferenceCentercystbanksample.
males,respectively.Thepopulationsanalysedcan besplitintothreedifferentgroupswhenfemales (Figure1) are considered and two different groups formales.Twoofthethreegroups obtainedforfemalesareshowntobe quitehomo- geneous,andtheseinclude13A.franciscana and
9A. salina populations.Thethirdgroup,more complexandlesshomogeneous,includesdiploid andtetraploidparthenogeneticpopulations.
When malesare considered(Figure2), only two groupsareobservedowingtotheabsenceof malesfor parthenogenetic populations.The groupconcerning A. salina maleslooksmore homogeneous, whereastheothergroup,dealing withA. franciscana males,showsa clear split betweenagroupofmales morphologically simi- lar to those originallyfrom Great Salt Lake (Utah, USA), whereastheothersaresimilarto SanFranciscoBay(California,USA)ones,sug- gestingthepossibilitythatthedifferentAmerican brineshrimppopulations introducedintheWes- ternMediterraneanlocalitiesoriginatefromcysts importedfrom both parts of the USA. These dataalsosupporttheviewof PillaandBeard- more(1994) on thegreaterusefulnessof male traitsinthistypeofmorphologicalanalysis.
Discussion
ThefirstrecordeddeliberateintroductionsofAr- temia franciscana were thosecarriedoutona PacificIsland andinBrazilinthe1970s (VanStappen2002).According toourresults obtainedthroughthescreening of oldand updatedbrineshrimpcystsamplescollectedin salternsfromvariouswestern Mediterranean countries,includingtheAtlanticshoresalternsin PortugalandsouthwestSpain,thepresenceofA. franciscana asanexoticinvasivespeciesiscon- firmedinPortugal,Spain,France,aswellasin the northofMorocco.
The presenceof A. franciscana inthesouth- west ofPortugalappearstodatefromtheearly
1980s as suggested by previousinformation (Hontoriaetal.1987).TheAmerican brine shrimppopulations probablythenspread(or wasintroduced)totheNorth,invadinghypersa- lineenvironments incentralPortugal,i.e.,Sado andTejo estuaries duringthecourseof this decade,reachingthesalternsintheAveirodis- trictattheend of1980sorearly 1990sand outcompeting autochthonousArtemia popula- tions.
MALES
4
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Firstdiscriminantfunction
Figure2. Groupcentroidsofthe populationsstudiedforthefirsttwodiscriminantfunctionsresultingfromthediscriminantanaly- sisonmalemorphometricvariables.
Thesalternsinthesouthwestof Spain,espe- ciallyintheprovincesofCadizandHuelva,have beenthesubjectoffieldstudiesoverseveraldec- ades.They providea well-documented caseof coexistenceofparthenogenetic(diploidandtetra- ploid)strainsandthe amphygonic A. salina (Amat 1983a; Amat et al. 1995). However,in most ofthe140oldsalternsexploitedaroundthe CadizBay(PuertoReal,SanFernando,Chiclana andCadiz),saltextractingactivityceasedatthe beginning ofthe1980s(Amat1983b),theirland usechangingtoaquaculturalprojects.Thisfact presumably provokednon-intentionalinocula- tionsofA.franciscana throughhatchery efflu- ents,whileafewofthembecamethesourceof brineshrimpproductsforaquaristsandpetmar- ketsafterintentionalinoculations(J.A.Calderon, pers.comm.).
Thesameaquaculturalsourcefortheintroduc- tionof Americanbrineshrimpinthesouthof SpainandPortugalispresumablyresponsiblefor
its presencein the French Mediterranean(see below),wherean unusualsexualpopulationof Artemia waspreviously recordedbyThieryand Robert(1992).Acloseinspectionoftheirpaper showsthattheyhadfoundanintroducedpopula- tionofA.franciscana, although theyfailedto namethe species.
Italiansamplesstudiedfromeightlocalitiesdo notshowthepresenceofA.franciscana. Inthese Italian salterns,onlytheautochthonousstrains werefound.ThissupportstheresultsofNascetti etal.(2003)intheirstudyofthegeneticstructure ofItalianArtemia frombrackish andhypersaline waters.
AccordingtoEhrlich(1984),Lodge(1993)and McMahon(2002),successfulinvasivespeciesusu- ally displaydifferentdegreesof the following attributes:(1)abundanceintheiroriginalrange orlargenativerange,(2)polyphagous oreury- trophic(i.e.widefeedingniche),(3)muchgenetic variability or phenotypic plasticity, (4) short
generationtimes,(5) fertilizedfemalesable to colonizealone(i.e. singleparentreproduction), (6)vegetativereproduction, (7)largerthanmost relatedspecies,(8)highdispersalrate,(9)associ- atedwithhumanactivities(humancommensal- ism)and(10)abletofunctioninawiderangeof physicalconditions.
Infact,thebiologicalattributesofspeciesare nottheonlyreasonof successfulintroductions. AccordingtoWilliams(1996)andBlackburnand Duncan(2001), thematchbetweentheclimatic orenvironmental conditionsinaspeciesnatural rangeandtheclimateinthelocationoftheintro- ductioncouldalsobeanimportantfactor.
Therearemanyexamplesofinvadingaquatic speciesshowingmostofthecitedtraits,butnot allthesetraitscanplayadefinitiveroleindeter- miningthesuccessofinvasions,theshiftsinthe structureofinvadedcommunities overtime,and theprobability ofextinctionofautochthonous species.HowwellArtemiacomplieswithmostof thesetraitsthoughttocharacterizeinvasive spe- ciesisaddressedbelow.
Ithasbeenarguedthatthereislittleevidence suggestingthatphysiological capacitytotolerate andfunctioninawiderangeofphysicalcondi- tionsisaprerequisite tosuccessful invasionsof aquatichabitats(McMahon2002).Inthegenus Artemia, althoughtheinformationonthetoler- anceof itsdifferentspeciesto a widerangeof physicalconditionsis not complete,it is com- monly acceptedthatitsadaptationtothesevere habitatsofhypersaline ecosystems,anditswide distributioninall continentsexceptAntarctica, meanthatthespeciesandpopulationscanwith- standthewidestsalinityandtemperatureranges amongaquaticorganisms,livinginsalinitiesat orbelowseawaterconcentration(35gl)1), upto saturationlevel(300gl)1).
It is possibleto assimilatethe filterfeeding mechanismof Artemiatoa polyphagousregime equivalentto eurytrophy,providedthat thefil- teredparticlesdonotexceedarangeofcritical sizes,i.e., between6.8 and 27.5lm (Gelabert
2001).
Thesympatryofsexualandasexualautochtho-
nousArtemia speciesrecordedin severalsites,
e.g. Spanish Mediterranean coastal salterns
(Browne and McDonald 1982; Amat 1983a;
Browneetal. 1988), or lakeUrmia(Iran) and
peripheralhypersalinelagoons (N. Agh, pers.
comm.) has previously motivatedlaboratory studiesof theinteractionbetween sexualand asexualpopulations.These competitionstudies canshed lightonlifehistorytraitsthatmay explainthesuccessofA.franciscana asaninva- der.
Competitionexperimentsbetweenbisexualand asexualArtemia populationsfromseverallocali- ties of the Old World havebeen carriedout inthelaboratory(Browne 1980;Browne and Halanych 1989),withA.franciscana usually incorporatedas a modelspeciessinceit isthe bestknownand studiedtaxon(Lenzand Browne
1991).Intheseexperiments,A.franciscana popu- lations outcompetedparthenogenetic (diploid) populationsin91%ofthescorabletrials.How- ever, whentheseA.parthenogenetica populations competed againsttheco-occurringOldWorld andMediterraneansexualpopulationsA.salina, bisexualswereeliminated in 98% of thetrials. Thus, the competitiveabilitiesof the Artemia populationsunderthe experimentalconditions testedareA. franciscana A. parthenogenetica
A.salina. However,salinity,temperature and otherenvironmentalgradientsarelikelytoinflu- encethe relativeperformanceofeachspecies.
Manyinvasive aquaticspecieswithsignificant ecologicalimpactsarecharacterizedbyadapta- tionssupporting rapidpopulationgrowth, includingrapidindividualgrowth,earlymaturity, short generationtimes,highfecunditiesandsmall egg–offspring size.Thesearetraitscharacteristic ofspeciesadaptedtounstablehabitats,withfre- quentpopulationdensityreductions or disap- pearanceassociatedwithunpredictablenatural environmental events(BrowneandWanigasekera
2001).Artemia andespecially A.franciscana can
beconsideredtoexhibitthesetraits,A. francis-
cana beinga moreextremer-strategist(Lodge
1993;Williamson1996)comparedtothespecies
itoutcompetes.
Awidevarietyoffactorssuchasenvironmen-
tal cues,life-historytraits, heterozygosity levels
andgeneticvariabilitymaycontributeindeter-
miningthecompetitive abilitiesof theArtemia
populations.Thesevariablescannot be pooled
togetherinexperimental designs,butthepartial
informationavailablefromstudiesofeachfactor
andtheevidencefromstudiesinthefieldwhere
competition occurs suggest the possibility of
competitive exclusion of native Artemia by
A. franciscana in 10–100 generations (Miller
1967), althoughaccordingto LenzandBrowne
(1991)itmaybeattainableintwoorthreegener-
ations.
Most Artemia speciesreproduceprimarilyby
ovoviviparityunder favourable environmental
factors,especiallywhenthereisnofoodlimita-
tion, but they switchto oviparity(producing
cyststhatcanundergoprolongeddiapauseand
cryptobiotic periods)whenunfavourableenviron-
mentalfactorsthreatentheovoviviparousrepro-
ductionand the populationpersistence.These
cystsarethebestwaytoensuretheappearance
of a newpopulationunderrenewed favourable
conditionspromotingcysthydrationandhatch-
ing,i.e.therenewalofthepopulationinthefol-
lowingseason.Thesecystsarealsothebestway
toensureasuccessfuldispersionofArtemiapop-
ulations.Thesecystsarethoughttobebroadly
dispersedby windtransportationamongshort
distances,orbybirdsforlongerdistances(Figue-
rolaandGreen2002;Greenetal.2002).
Lastbutnottheleast,thepresenceofA.fran-
ciscanafromtheNewWorldintheWesternEur-
opeandMediterraneanshoresisunquestionably
associatedwithahumanactivity,withtheaqua-
cultureofmarine speciesofcommercialinterest.
Withtheunavoidable development ofhatcheries
toobtainpostlarvaeandfingerlingsforaquacul-
ture,theuseof Artemianaupliiasadietforlar-
valculturebecamewidespread.Dormantcystsof
Artemia canbestoredforlongperiodsincans
andthenusedasanoff-the-shelffoodrequiring
only24h of incubationto obtain livenauplii
(Lavens and Sorgeloos2000). From the early
1950s,commercialsourcesofcysts initiallyorigi-
natedfromthecoastalsalternsintheSanFran-
ciscoBay,California,USA,andtheinlandGreat
SaltLake,Utah,USA.Thesecystswereprimar-
ilymarketedfortheaquariumpettrade,andin
the mid-1970s, the demand increased from
emergingaquacultureoperations,currently
attainingrequirementsofabout2000metrictons
ofcystsannually.
Shrimpculture,basedonPenaeids,startedto
develop rapidly in the Mediterranean area
(mainlyinItalyandFrance)inthelatteryearsof
the 1970 decade(Lumare 1990). Experimental
productionsof Penaeus japonicus in thesouth-
westof Spain (Cadiz)startedin 1982, andin
1986, about 20 millionpostlarvaewerereared
(Rodriguez 1986).Shrimpculturewaslargely replacedbymarinefinfish(seabass,seabream) cultureintheearly1980s,whenmanyoldsea- sidesalternsthathadbeentraditionallyexploited intheareaofCadizbayswitched theiractivity tointensive fishculture.By1998,900haofold salternpondshad beenconvertedto intensive fishculture(Espinosaetal.1999).
In southwesternPortugal(Algarveprovince), oldsalternswereconvertedto prawnandfish culturein1985–1986(Gouveia1994),butAmeri- canbrineshrimpmayhavebeenintroducedear- lier for the aquariumpet trade (M.N. Vieira, pers.comm.).
Intheearly1970s,therewere important advancesinseabassintensiveculturesinpilot plantssettled intheareaofSete(Languedoc, France)nearcoastallagoonsandmarine salt exploitations (Barnabe1974a,b). Duringthis decade,severalfish farms developed in the lagoons and brackish environments along the Languedocshore:Salses-Leucate,Thau.,etc.
These aquaculture developmentshave been closelylinkedto thesuccessinshrimpandfish hatcheryproductions,wherelarviculturerelied onthesupplyoflivefoodorganismsinsufficient quantity.To date,theselivingpreysarerotifers (Brachionusplicatilis)obtainedthrough season- roundmassiveculture,andArtemia naupliifrom themassivehatchingof cystspurchasedinthe internationalmarketfrom sourcesin America, especiallyfrom GreatSaltLake,Utah.
Ourresultssuggestthatthenativepopulations ofArtemiaintheMediterraneanregionareunder severethreatfromcompetitionwith theexpand- ingA.franciscana. Inanattempttopreventor slowdown furtherspreadofthisexoticspecies, wesuggestthataquacultureactivitiesshouldbe subjecttotighterregulation.Wherepossible,the useof cystsfromnativespecies shouldbe encouraged.
Acknowledgements
ThisstudyhasbeenfundedbytheSpanishGov- ernmentRDNationalPlanundertheprojects AGL 2001-1968, INCO Project ICA4-CT-2002-
10020 and AGL 2001-4582 E. Olga Ruiz has beensupportedbyafellowshipoftheFPU Pro- grammefromtheSpanishMinistryofEducation
andCulture.Wewouldliketo thankClaudine delaCourtandNunoGradefor theirhelpin collectingcystsamples.Themanuscriptincorpo- ratedthesuggestions ofananonymousreviewer whichhelpedimproveit.
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