.

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±SE
CastroMarim
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.

References

ABATZOPOULOS,T.J.,J.A.BEARDMORE,J.S.CLEGG, AND P.SOR- GELOOS[EDS.].2002.Artemia:Basicandappliedbiology.Klu- werAcademic.

AMAT, F.,F.HONTORIA,O.RUIZ, A.J.GREEN, M.I.SA´NCHEZ, J.

FIGUEROLA,AND F.HORTAS. 2005.TheAmericanbrineshrimp ArtemiafranciscanaasanexoticinvasivespeciesintheWest- ernMediterranean.Biol.Invasions7:37–47.

AMEZAGA,J.M.,L.SANTAMAR´ıA,AND A.J.GREEN. 2002.Biotic wetlandconnectivity—supporting anewapproachforwetland managementpolicy.ActaOecol.23:213–222.

BAILEY, S.A.,I.C.DUGGAN, AND C.D.A.VAN OVERDIJK.2003.

Viabilityofinvertebratediapausingeggscollectedfromresid- ualballastsediment.Limnol.Oceanogr.48:1701–1710.

BOHONAK, A.J.,AND H.H.WHITEMAN.1999.Dispersalof thefairy shrimpBranchinectacoloradensis(Anostraca):Effectsof hy- droperiodandsalamanders.Limnol.Oceanogr.44:487–493.

BOYD, H.,AND J.Y.PIROT. 1989.Flywaysandreservenetworks forwaterbirds.InternationalWaterfowland WetlandsResearch Bureau.

DABORN, G. R.,AND OTHERS. 1993.An ecologicalcascadeeffect: Migratorybirdsaffectstabilityofintertidalsediments.Limnol. Oceanogr.38:225–231.

DARWIN,C. 1859.Onthe originofspeciesbymeansof natural selection.JohnMurray.

FIGUEROLA,J.,AND A.J.GREEN.2002a.Dispersalof aquaticor- ganismsbywaterbirds:A reviewofpastresearchand priorities forfuturestudies.FreshwaterBiol.47:483–494.

,AND .2002b.Howfrequentisexternaltransportof seedsandinvertebrateeggsbywaterbirds?AstudyinDon˜ana, SWSpain.Arch.Hydrobiol.155:557–565.

, ,GREEN, AND L.SANTAMARIA.2003.Passivein- ternaltransportofaquaticorganismsbywaterfowlinDon˜ana, south-westSpain.GlobalEcol.Biogeogr.12:427–436.

HAVEL, J.E.,AND J.B.SHURIN. 2004.Mechanisms, effects,and scalesofdispersalinfreshwaterzooplankton.Limnol.Ocean- ogr.49:1229–1238.

HORTAS, F.1997.Migrationofshorebirdsinsouth-westIberia,mi- gration routefortheWestMediterranean andAfrica,p.77–

116.InA. Barbosa[ed.],TheShorebirdsof Spain.Direccio´nGeneraldeConservacio´ndelaNaturaleza,MinisteriodeMe- dioAmbiente.[InSpanish]

HURLBERT, S.H.,AND C.C.Y.CHANG.1983.Ornitholimnology: EffectsofgrazingbytheAndeanflamingo (Phoenicoparrus andinus).Proc.Natl.Acad.Sci.USA80:4766–4769.

IVERSON,G.C.,S.E.WARNOCK,R.W.BUTLER, M.A.BISHOP, AND N.WARNOCK. 1996.Springmigrationof westernsand- pipersalongthePacificCoastofNorthAmerica:Atelemetry study.Condor98:10–21.

LEPPA¨ KOSKI, E., S. GOLLASCH, AND S. OLENIN. 2002. Invasive aquaticspeciesofEurope—distribution, impactsandmanage- ment.Kluwer.

MACDONALD,G.H.1980.TheuseofArtemiacystsasfoodbythe flamingo(Phoenicopterusruberroseus)andtheshelduck(Ta- dornatadorna),p. 97–104.InG.Persoone,P. Sorgeloos,O. Roels,andE. Jaspers[eds.],ThebrineshrimpArtemia.Ecol- ogy,culturing,useinaquaculture,V.3.UniversaPress.

NOGALES,M.,F.M.MEDINA,V.QUILIS,AND M. GONZLEZ-RO- DR´ıGUEZ.2001.Ecologicalandbiogeographicalimplicationsof Yellow-LeggedGulls(LaruscachinnansPallas)as seeddis- persersofRubiafruticosaAit.(Rubiaceae)in theCanaryIs- lands.J.Biogeogr.28:1137–1145.

MOONEY, H.A.,AND E.E.CLELAND.2001.Theevolutionaryim- pactofinvasivespecies.Proc.Natl.Acad.Sci.USA98:5446–

5451.

PROCTOR,V.W.1964.Viabilityofcrustaceaneggsrecoveredfrom ducks.Ecology45:656–658.

,C.R.MALONE, AND V.L.DEVLAMING.1967.Dispersalof aquatic organisms: Viability ofdisseminules recovered from theintestinaltractofcaptiveKilldeer.Ecology48:672–676.

RUIZ, G.M., P.FOFONOFF,A.H.HINES, AND E.D.GROSHOLZ.

1999.Non-indigenousspeciesasstressorsinestuarineandma- rinecommunities:Assessinginvasionimpactsandinteractions. Limnol.Oceanogr.44:950–972.

SA´NCHEZ, M.I.,A.J.GREEN, AND E.M.CASTELLANOS.Inpress.

SeasonalvariationinthedietoftheRedshankTringatotanus intheOdielMarshes,south-westSpain:Acomparisonoffae- calandpelletanalysis.BirdStudy.

STROUD, D.A.,AND OTHERS. 2004.Statusofmigratorywaderpop- ulationsinAfricaandWesternEurasiain the1990s.Interna- tionalWaderStudies15:1–259.

WASSON, K.,C.J.ZABIN, L.BEDINGER,M.C.DIAZ, AND J.S.

PEARSE.2001.Biologicalinvasionsof estuarieswithoutinter- nationalshipping:Theimportanceof intraregionaltransport. Biol.Cons.102:143–153.

WELHAM, C.V.J.1994.Flightspeedsofmigratingbirds:Atestof maximumrangespeedpredictionsfromthree aerodynamic equations.Behav.Ecol.5:1–8.