.
DispersalofinvasiveandnativebrineshrimpsArtemia(Anostraca)viawaterbirds
Abstract—NorthAmericanbrine shrimpArtemiafrancis- canahavebeenexportedworldwidesincethe1950sforuse inaquariumtradeandfishfarming.Aquacultureisexpanding alongtheMediterraneancoast,leadingto thereleaseof A. franciscana into native Artemia populations. A.franciscana wasfirstdetectedin1981inPortugalandhassincespreadto saltworksalongtheEastAtlanticflyway usedbyshorebirds. OnceA.franciscanabecomesestablishedinalocality,native Artemiatendtodisappear. Totestwhethermigratoryshore- birdscandisperseinvasiveand nativeArtemiabetweenwet- lands,weextractedArtemiacystsfromfecesand pelletscol- lected at Castro Marim (Portugal) and Cadiz Bay (Spain) duringsouthwardmigration.Wefoundthat largenumbersof viableeggsof A.franciscanaandnativeArtemiapartheno- geneticaweredispersedby RedshankTringatotanus,Black- tailedGodwitLimosalimosa,and othershorebirdsmigrating throughtheIberianPeninsula.Thisisthemostextensivefield demonstration todatethatinvertebrates candispersereadily viagutpassagethroughbirds.
Invasionbynonnativespeciesissecondonlytohabitatloss asathreattoglobalbiodiversity,hasahugeeconomicimpact, andhashaditsgreatestimpactinaquaticecosystems(Ruizet al. 1999;MooneyandCleland2001).Nonnativeaquaticin- vertebrates aretypically moved between continents byman, e.g.,intheballastof shipsorintentionallyforaquacultureor fisheriespurposes(Leppa¨koskietal.2002;Baileyetal.2003). Onceestablished,theyaregenerallyassumedtodisperseusing theirownactivemechanismsviaoceanorrivercurrentsorvia intraregionalboattraffic(Wassonetal.2001).Theroleofmi- gratory birds inspreading exotic invertebrates has notbeen fullyassesseddespitetheimportanceofunderstandingthedis- persalmechanismsofinvasivespeciessothattheirspreadcan bepredicted.Someauthorsreviewingdispersalmechanismsof aquaticinvasiveshavemadenomentionofapotentialrolefor birds(Leppa¨koskietal.2002).
Darwinattributedmuchimportancetotheroleofmigratory waterbirds asdispersers ofinvertebrates (‘‘Thewidedistribu- tionoffresh-waterplantsandoftheloweranimalsI believe mainlydependsonthewidedispersaloftheirseedsandeggs by animals,moreespeciallyby fresh-waterbirds,whichhave greatpowersofflight,andnaturallytravelfromonepieceof watertoanother,’’Darwin1859).Hesuggestedthatshorebirds haveaparticularlyimportantroleandproposedthataliensnails extended theirrangebydispersing onthefeathers orfeetof birds(Darwin1859).Variouslaboratorystudieshave since demonstratedthatpropagulescan survivepassagethroughthe digestivesystem(Figuerolaand Green2002a).However,few studieshavedemonstrated suchdispersalinthefield(Proctor
1964;FiguerolaandGreen2002a).
Owingto similarmorphology,untilthe1980s,allpopu- lationsofbrineshrimpsArtemia(Crustacea,Anostraca)were consideredstrainsofasinglespecies,butsixsexualspecies arenowrecognized,togetherwithaheterogeneousgroupof parthenogenetic populations, under the binomen Artemia
parthenogenetica(Abatzopoulosetal.2002).ThesexualAr- temiafranciscanaiswidespreadintheAmericas.In the Mediterraneanregion,thenativespeciesarethe sexualAr- temiasalina(formerlyArtemiatunisiana)andtheA. par- thenogenetica(mainlydiploidand tetraploidpopulations, Abatzopouloset al.2002).Sincethe1950s,A.franciscana cystshavebeencommerciallyexportedworldwidefromSan FranciscoBayandGreatSaltLake,U.S.A.,foruseinaqua- cultureandintheaquariumandpettrade(Abatzopoulos et al. 2002).In theMediterraneanregion,manyformersalt- worksinwhichsaltproductionhasbecomeunprofitableare beingtransformedintoaquaculturefacilities,leadingto the releaseofA.franciscanaintohatcheriesanditsescapeinto habitatswithnativeArtemiapopulations(Amatetal.2005). Givenitsuseinthepettradeandinmicroscopesets,indis- criminatereleasesintoothersalinewetlandssuitableforAr- temiaarealsopossible.
Between 1993 and 2003, Artemia cysts (resting eggs) fromnumeroussaltworksin theWestMediterraneanwere collected, andtheirspecies composition determined (Amat etal.2005;authors unpubl.). Bythen,A.franciscana was theonlyspeciesrecorded inPortugal, whereitisfoundin areasbothwithandwithoutaquaculture.Itisalsofoundin CadizBay(Spain),twoFrenchsites,andoneinMorocco. A.franciscana wasfirstdetectedin1981inthePortuguese Algarve(Amatetal.2005)andhassincespreadto allthe Iberiansitesconsideredtobemostimportantforshorebirds alongtheEastAtlanticFlyway:Tejo,Aveiro,Faro,andSado inPortugalandCadizBay(BoydandPirot1989;Amatet al.2005).Todate,therehasbeennospreaddetectedtothe manysaltworkseastofGibraltaroutsidetheflyway(Fig.1). AtAveiro,onlyA.parthenogenetica wasrecordedin1985, butby1991,ithadbeenreplacedbyA.franciscana.
Inthisstudy, weassessed theability ofshorebirds (the mostabundant waterbirds incoastal saltworks) todisperse A. franciscana and A. parthenogenetica by sampling two areaswhereA.franciscanahasbeenrecorded:CastroMarim
(Portugal, 37°12’N, 7°26’W) and Cadiz Bay (36°27’N,
6°11’W). BotharesituatedontheAtlanticcoastofthesouth- westernpartoftheIberianPeninsula(Fig.1)andarelisted aswetlandsof internationalimportanceunderthe Ramsar Convention ( Bothsitesholdsaltworksandtensofthousandsof shorebirds duringmigrationperiods(Hortas1997).
Materialsandmethods—Wecollectedfreshfecesandpel- letsfromroostsitesusedbymonospecificflocksinsaltworks atCastroMarimon23July2002andCadizBayfrom22
July2002to3August 2002.Severalshorebirds, including theRedshankTringatotanus,regurgitatepelletsafterdiges- tion.Thedatesofsamplingcoincidedwiththebeginningof the southward(autumn)shorebirdmigration(Hortas1997). Eachsampleoffecesorpelletwascarefullyseparatedfrom thesoil(discardingthatpartincontactwithsoil)andplaced
Fig.1. CastroMarim(leftinsert)andCadizBay(right)onamapoftheIberianPeninsula,showing thecurrentdistributionofA.franciscana(blacksquares)andnativeArtemia(whitedots)inrelationto theEastAtlanticFlyway(shadedafterStroudetal.2004).Hatchedareaswithininsertsrepresentsalt- works.OtherArtemiasiteswithnoinformationonspeciescompositionsince1992arenotshown.
inatube.Giventhenumberofbirdspresentandthefresh- nessof thesamples,weareconfidentthateachsamplewas fromadifferentbird.Thesampleswerestoredat 5°C, and within amonth, Artemia cysts were extracted bywashing them ina0.04-mm sieve and resuspension inhypersaline brineinwhichintactcystsfloat. Thecystswerecounted, washedindistilledwater,andthendriedfor48hat40°C.
Thecystswerethenincubated indiluted, filteredseawater (25gL—1)at26°Candundercontinuousilluminationfor48 h. Hatchednaupliiwerecounted,transferredinto60-cm3 vessels,andculturedin70gL—1filteredbrine(seawaterplus crudeseasalt)onadietofliveDunaliellasalinaandTetra- selmissuecica.Theyweremaintained at24°C,underaera- tionona12:12light:dark(LD)photoperiod. Themedium
Table1.NumberofsampleswithintactArtemiacysts,numberthatproducednaupliuslarvae,andnumberofadultArtemiareared.Not allnaupliihatchedfromcystssurvivedtotheadultstagethatpermittedspeciesidentification,thusthenumbersofsamplescontainingeach taxonmaybeunderestimated.Eachsamplecontainsonlyasmallfractionofthecystsexcretedina24hperiodbyagivenbird.
CadizBay
*DiploidA.parthenogeneticafemales.
†52%weremales
was monitored and renewed every two days. Resulting adultswereidentifiedmorphologically (Amatetal.2005).
Wealsocollectedthousandsof cystsfromsaltpansad- jacenttositeswherewecollectedfeces,determinedhatching success,culturedadults,andidentifiedthemusingthesame methodas usedforcystsextractedfromfeces.Wealsoes- tablishedhatchingsuccessofA.parthenogenetica cystscol- lectedinJanuary2002fromsaltworks atSanlu´cardeBar- rameda(36°50’N,6°20’W),30kmfromCadizBay.
The numbers ofcysts transported and their hatchability werecomparedbetweenbirdspecies,betweenlocalities,and betweenfecesand pelletsusingnonparametricMann–Whit- neyU-tests.Initialattemptstouseparametricstatisticswere abandonedowingtooverdispersion andthehighproportion ofzerosinthedata.
Results—Inbothlocalities,wefoundallshorebirdspecies studied tobetransporting viable Artemia cysts during au- tumnmigration (Tables 1,2).AtCastroMarim,Redshank andBlack-tailedGodwitLimosalimosa,were transporting largenumbersofviableA.franciscanacystsanda small number of A. parthenogenetica. At Cadiz Bay, Redshank andDunlinCalidrisalpinaweretransportingviableA.par- thenogenetica cystsand,occasionally, A.franciscana.
At Castro Marim, Redshank feces held more Artemia
cysts than Redshank pellets (Mann–Whitney U-tests, n=
36,31,U=250,p=0.0001)orgodwitfeces(n=36,30, U=161,p0.0001).Theproportionofcyststhathatched
wasalsohigherforRedshankfecesthanforgodwitfeces(n
=36,27,U=142.5,p0.0001)orRedshank pellets(n
=36,30,U=379.5,p=0.039).Numbersofcystsrecorded atCadizBaywerefewerthanthenumberatCastroMarim forRedshankpellets(n=31,55,U=141.5,p0.0001), buttheproportionofcyststhathatchedwashigheratCadiz Bay(n=30,25,U=101,p0.0001).However,thetotal numberofviablecyststransportedperpelletwasmorethan fivetimeshigher forA.franciscana inCastroMarimthan forA.parthenogenetica inCadizBay.
Amongcystsamplestakendirectlyfromsaltpans,wefound
100%A.franciscanaat bothCastroMarimandCadizBay. HatchingsuccessofA.franciscanaat CastroMarimwas74.1% (n=17,400).HatchingsuccessofA.parthenogeneticaatSan- lu´cardeBarramedawas50.2%(n=15,200).
Discussion—Redshankand godwitswereeffectivedis- persersofA.franciscana. Thousandsofindividualsofboth speciesmigratethrougheachof ourstudysitesandmove thousands of kilometers between breeding and wintering sites(Hortas1997).An estimated15.5millionshorebirds (including440,000Redshank,200,000 Black-tailedGodwit, and2,340,000Dunlin)migratethroughthe EastAtlantic Flyway(Stroudetal.2004),wheremostmajorpassageand winteringsitescontainsaltworks.Bandingdata showsthat somebirdsstopatmorethanonesaltworkcomplexasthey migrate along the Iberian Atlantic coast (details available fromfirstauthor).
Table2.NumberofintactArtemiacystscollected,numberofnaupliihatched,andtheproportionofcyststhathatched.
No.cystspersample
No.naupliipersample*
%cystshatching
No.ofsamples / mean±SE / range / mean±SE / range / mean±SECastroMarim
Redshankfeces / 36 / 65.0±13.1 / 6-379 / 18.0±3.3 / 1–98 / 33.3±2.5
Redshankpellets / 31 / 26.3±6.9 / 0–160 / 7.5±2.7 / 0–62 / 25.8±4.2
Godwitfeces / 30 / 27.8±14.9 / 0–447 / 1.6±0.4 / 0–8 / 12.4±2.7
CadizBay
Redshankpellets / 55 / 1.7±0.3 / 0–13 / 2.5±0.4 / 0–8 / 68.8±5.9
Dunlinfeces / 103 / 0.1±0.04 / 0–2 / 0.1±0.1 / 0–1 / 12.5±12.5
*Forsampleswithatleastonecyst(seeTable1forn).
Thebirdswestudiedincludedamixtureofbirdsthathad just completed orwere just about to commence long-dis- tancemovementsand birdsthat weremakingmovements between feeding androosting spotswithinourstudysites. Theaveragetimespentbyshorebirdsat stopoversitesduring migrationisunknownforourstudysites,makingit impos- sibletoassesswhatproportion ofthecystsextracted from fecesorpelletsweretransportedfromlongdistances.How- ever,the poormatchbetweenthe speciescompositionof Artemiacystsextractedandthosefromadjacentsalt pans showsthatthebirdsweretransportingcystsbetweendiffer- entpartsofwetlandcomplexes.Redshank,godwits,andoth- ershorebirdsregularlymovebetweensaltpansseparatedby
20kmwithinstopoversites(Pottspers.comm.),favoring rapid Artemia dispersal within and between nearby salt- works.Dominanceof A.parthenogeneticain birdsamples fromCadiz(Table1)probablyreflectsfeedinginsaltpans that had been dry since A. franciscana invaded, allowing nativeArtemiato hatchfromcystsin sedimentsuponre- flooding(cystscanremainviablefor decadesin sediments, Abatzopoulos etal.2002). There arehundreds ofpans in CadizBay,anditwasnotpossibletoknowexactlywhere thebirdshadbeenfeedingwhenwecollectedfeces.
Redshank and godwits fly at 56–60 km h—1 (Welham
1994).Inalaboratorystudy,themodalretentiontime(much lessthanthemean)ofviableA.franciscanacystsdefecated byanothershorebird,theKilldeerCharadriusvociferus(size intermediate between redshank andgodwit), wasfound to be90min,andthemaximumwas26h(Proctoretal.1967). Thissuggeststhat,duringmigration,themaximumdispersal distanceofviablecystswouldbeabout1,500km.Studies ofgutpassageof viableA. franciscanacystsin otherbirds suggests that the maximum retention time increases with bodysize,rangingfrom3hinacanarySerinuscanariusto atleast38hinaShelduckTadornatadorna(Proctor1964; MacDonald1980).
Radioandsatellitetrackingshowsthat shorebirdsmove rapidlybetweencoastalwetlands,and distancesbetweenstop- overscanexceed1,000km(Iversonetal.1996).A.francis- canacystsarealsolikelytobetransportedinternallybysome of theother24migratoryshorebirdspeciesusingthe East Atlantic Flyway(Stroudetal.2004),aswellasotherbirds that consumeArtemiaand movefrequentlybetweenwetlands. Artemiacystsare consumedbyGreaterFlamingosPhoeni- copterusruberandShelduckinthewild(MacDonald1980). Viablecystsarealsolikelytobetransportedexternallyonthe feathersandfeetofwaterbirds(FiguerolaandGreen2002b). Wedonotexpectthatsuchdispersalprocessesarerestricted tothesestudysitesortoautumnmigration.Ina studyof Redshank diet at the Odiel marshes in Spain (37°17’N,
6°55’W), cysts were similarly abundant in pellets in both springandautumnmigration(Sa´nchezetal.2005).
Weobservedconsiderablevariationamongwaterbirdspe- ciesandlocalitiesinthenumberof intactArtemiacysts transportedandintheirviability(Tables1,2).Thisvariation islikelytoberelatedtodifferencesbetweenbirdpopulations inhabitatuse,diet,gutmorphology,andretentiontime(Fi- guerolaandGreen2002a).FecesofbothRedshankandgod- witscontainedremainsofadultArtemia,andthesebirdsare likelytoingestcyststhatarestillinsideadultArtemia(some
ofwhichmayhavebeenimmatureandthuslessviable,see BohonakandWhiteman1999)aswellasthoselooseonthe watersurfaceorinsediments.ThegreaterviabilityofRed- shankcystsrecoveredfromfecesratherthanpelletsfurthers long-distancedispersalbecausecystsarelikelytoberetained longerwhenexpelledas fecesthanwhenregurgitated(No- galesetal.2001).Cystsexpelledinpelletsmaybelessvi- ablebecausetheyare groundtogetherwithgritand hard prey items inthegizzard (Sa´nchez etal.2005). Adding gritto cystsfedtoflamingosreducestheirviability aftergutpas- sage(MacDonald1980).
AtCastroMarim,thehatchingsuccessofA. franciscana cyststakenfrombirdsampleswasmuchlowerthanfor cysts collected in adjacent salt pans. Hatching success of cysts from Redshank pellets at Cadiz Bay was higher than for cystsfromtheclosestA.parthenogeneticasitewecouldfind atSanlu´cardeBarrameda.Suchcomparisonsaredifficultto interpretasfloatingcystscollectedattheedgeofsaltpans maynotbe theonesingestedby thebirdsandmayhave differentviabilities.Gutpassagethroughthe GreaterFla- mingoandShelduck hasbeenshownexperimentally tore- ducehatchingsuccessof A. parthenogeneticacysts(Mac- Donald1980).
Althoughtherearefewdataavailableonthetimingofarrival ofA.franciscanaatdifferentlocationsor onthetimingand locationofintroductionsbypeople,thecurrentdistributionof thisexoticintheIberianPeninsulaisconsistentwithexpansion viashorebirds.Of ninesaltworksstudiedon themainEast AtlanticFlywaywestofGibraltarsince1993(Amatetal.2005; authorsunpubl.),A.franciscanaisdominantatsevenofthem (Fig.1).Yetthisspecieshasnotbeendetectedinanyofthe fivesaltworksstudiedtotheeastofGibraltarandofftheflyway (Fisherexacttest,one-tailedp=0.0105).
Oursisthemostextensivefielddemonstrationtodatethat aquatic metazoans can disperse readily via gut passage throughbirds.Recently,ducksand cootswereshownto transportnumerousinvertebrateeggsof unknownviability (Figuerolaetal.2003).Inapreviousfielddemonstrationof internal transport, Proctor (1964) found unknown numbers ofviableCladoceraandOstracodainthreeducks.Thereare increasingnumbersofexoticcrustaceansandbryozoansob- served in aquatic systems (Leppa¨koski et al. 2002), and manyarelikelytohavetheabilitytodisperse asresistant eggsviabirds(FiguerolaandGreen2002a).Theconserva- tionofmigratorywaterbirdsisessentialtomaintainconnec- tivityandindigenousinvertebratebiodiversityintheworld’s wetlands(Amezagaetal.2002).Nevertheless,theircapacity to disperseinvasivespecieswithinandbetweencontinents makes the need to control the importation and release of exoticspeciesatagloballevelallthemoreurgent.
Thereis evidenceof competitiveexclusionof nativeAr- temiabyanexotic species. Thedataavailable suggest that onceA.franciscanaisdetectedamongnativeArtemiainex- isting populations, native Artemia disappear within a few years(Amatetal.2005).A.franciscanaoutcompetesA.par- thenogeneticaandA. salinawithintwoor threegenerations underlaboratoryconditionsusingfew individuals(Abatzo- pouloset al.2002).WeexpectviableA.franciscanapropa- gulestoeventuallyreachallcoastalsaltworksin theMedi- terraneanregionviabirds,buttheremaybeconditionsunder
whichinvasioncanberesisted,similarto thatof otherzoo- plankton communities (Havel andShurin 2004). Preventing theexpansionofaquacultureintoprotectedcoastalareasstill holdingnativeArtemiapopulations (seeAbatzopoulos etal.
2002forinventory)islikelytobethemosteffectivemeasure tofacilitatetheirconservationintheshortterm.
Limnologicaleffectsofbirdsareextremelycomplex(Da- bornetal.1993).Intheirseminalpaperonornitholimnol- ogy, Hurlbert and Chang (1983) showed how waterbirds mayaffectthedynamicsofinvertebratepopulationsand,in- directly, ofentireaquaticecosystems viapredation effects. Wesuggesttheymayalsodosoviadispersaleffects.
AndyJ.Green1
Estacio´nBiolo´gicadeDon˜ana
Avda.Mar´ıaLuisas/n
41013Sevilla,Spain
MartaI.Sa´nchez
Estacio´nBiolo´gicadeDon˜ana
Avda.Mar´ıaLuisas/n
41013Sevilla,Spain;
Departamento deBiolog´ıaAmbientalySaludPu´blica
UniversidaddeHuelva
AvdaFuerzasArmadass/n
21071Huelva,Spain
FranciscoAmat
InstitutodeAcuiculturadeTorredelaSal
12595RiberadeCabanes,Spain
JordiFiguerola
Estacio´nBiolo´gicadeDon˜ana
Avda.Mar´ıaLuisas/n
41013Sevilla,Spain
FranciscoHontoria
InstitutodeAcuiculturadeTorredelaSal
12595RiberadeCabanes,Spain
OlgaRuiz
InstitutodeAcuiculturadeTorredelaSal
12595RiberadeCabanes,Spain
FranciscoHortas
Departamento deBiolog´ıa UniversidaddeCadiz Apartado40
11510PuertoReal,Spain
1 Correspondingauthor()
Acknowledgments
WeareindebtedtoC.deleCourt,N.Grade,andE.Morenofor helpcollectingsamples.CommentsbyP. Jordano,C. Rico,L. San- tamar´ıa,K.Schwenk,andD.M.Wilkinsonhelpedto improvethe manuscript.P. M.Pottsprovidedvaluableinformation.This studyhas beenpartiallyfundedbytheSpanishR+DNationalPlan(projects AGL2001-4582 and BOS2003-02846). M.I.S. wassupported bya grantfromtheMinistryofScienceandTechnology.O.R.was sup- portedbyINCOProjectICA4-CT-2002anda fellowshipfromthe MinistryofEducationandCulture.
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