Effects of Greater flamingo Phoenicopterus ruber on macrophytes, chironimds and turbidity in natural marshes in Doñana, SW Spain.
Rodríguez-Pérez,H., GreenA.J., andFiguerola,J.
Dept.of AppliedBiology,EstaciónBiológicadeDoñanaCSIC. Avd. MaríaLuisas/n,41013, Sevilla,Spain.
Authors Version. Publishedin:
Fundamental and Applied Limnology -Archiv für Hydrobiologie(2007) 172:167-
175.
Abstract
Toppredatorsandnutrientinputsareimportantfactorsdeterminingthestructureof freshwateraquaticsystems.Greaterflamingos(Phoenicopterus ruber) has beenshown to destroysubmergedmacrophytesandmaypromoteaswitchfromclearwatertoturbid waterinthetemporarymarshesof DoñanaNationalPark. Weexcludedflamingosfrom twenty4x4 mplotsdistributedbetweentwo lucios(shallowseasonallakes)withinthe marshesfromFebruarytoJuly2004. InJuly,we measuredtotalsuspended solids
(TSS), macrophytebiomassandabundanceandsizeof chironomidlarvaeinthetwenty exclosuresandinthetwentyadjacentcontrolplots.TSS was lowerandmacrophyte biomasswashigherinexclosures,butnotsignificantlyso. Flamingoswerefound to causeasignificantreductioninchironomidabundanceandanincreaseintheproportion of largerlarvae.Theeffectof exclusionwas greaterwherethedensityof flamingoswas highest.Comparisonwiththeresultsfrompreviousexperimentssuggest thattheimpact of flamingosarecontextdependentandlargelyinfluencedby birddensityand/orfactors relatedto macrophyteproductivity.Waterlevelswereespeciallyhighin2004 owing to heavyrains,andflamingosmayhavestrongereffectsinyearsof lowerrainfall.
Keywords: Flamingos, macrophytes, turbidity, nutrients, chironomids, sediment resuspension.
Introduction
Submergedvegetationhas amajorfunctionalroleinshallowwetlands,becauseit providesrefugefor invertebrates,changesthenutrientdynamicsof thesystem,prevents resuspension of thesediments(JEPPESENetal.1998, SCHEFFER1998). Itistherefore importanttoidentifythefactorsthataffectthepresenceandabundanceof submerged vegetation.Theroleofherbivorouswaterbirdssuch as swans, geeseandcootshas been studiedextensively,andisanimportantfactorintherestorationof shallowlakes(VAN DONKetal.1994, VANDONKOTTE1996, SONDERGAARDetal.1996). Itiswidely assumedthatthedisturbanceof sedimentsby benthivorousfishescaninhibitthe
colonizationof submergedplantsandenhancesedimentresuspension (SCHEFFERetal.
1993, SCHEFFER1998). However, thepotentialeffectsof benthivorousbirds on submergedplantshavelargelybeenignored.
Phoenicopteridaefamilyincludesthreegenus, andfivespecies,two speciesof genus Phoenicopterus (P. ruber andP. chilensis), othertwo speciesof genus Phoenicoparrus (P. andinus andP. jamesi), andonesinglespeciesof thegenus Phoeniconaias (P. minor). Thethreespeciesof thelasttwo genus haveinthebeakvery finestructures(lamella),who haveevolvedfor averyspecialiseddietbasedon algae (Jenkins 1957, Vareschi1978, HurlbertandChang1983), neverthelessPhoenicopterus specieshaveabroaderdietandless finelamellafor filtration(Jenkins 1957). All
speciesarecolonialbirds, andcanreachtolargepopulationsinthewetlandwherethey occur,duetotheirgregariousbehaviour,theirfeedinghabitsandtheirlargesizes,their presencemayprovokeecologicalshiftsinthewetlandswheretheyoccur.Greater Flamingo(Phoenicopterus ruber) has adistributionwithinOld Worldtropicalto Mediterraneanareas.Theyinhabitmainlyinshallowsalineor alkalinewaterbodies, frequentlyincoastalandestuarinezones,formingflocksof tenstohundreds animals. Theyaremainlybottomfeedersandexhibitdifferentfeedingbehaviours(including wading,tramplingthesediment,movementswiththebeakon themudsurface,etc)to catchsmallinvertebrates(insects,crustaceans,molluscsandannelids),algaeandplant material(seeds andplantfragments)(Crampetal.1982, Johnson 1997).
Ithas previouslybeensuggestedthatGreaterflamingos(Phoenicopterus ruber) havenegativeeffectson submergedplantsandon herbivorousbirds inthemarshesof DoñanaNationalPark inSpain(DUARTEetal.1990, GRILLASetal.1993;MONTES& BERNUÉS1991) andintheCamargueinFrance(GALLET1950). MONTESBERNUÉS (1991) comparedareasintheDoñanamarsheswithandwithoutconcentrationsof flamingos,andfound theirpresencetobeassociatedwithadecreasein macrophyte biomassandanincreaseinturbidityandinphytoplanktonabundance(as measuredby chlorophylla).However, manyfactorsarelikelytoaffectboththepresenceof macrophytesandflamingos,butno experimentalstudyhas beendoneinnatural marshes up tonow. Greaterflamingosproducecratersof ca.1 mdiameterduringtheir tramplingfeedingbehaviour,andareoneof themostabundantwaterbirdsin Mediterraneanwetlands,withanincreasingpopulationsize(WETLANDS INTERNATIONAL2006;RODRÍGUEZ-PÉREZGREEN2006). Theycausedamagetorice crops inFranceandSpain(TOURENQetal.2001) andhavebeenshown tochange sedimentpropertiesandtodecreasetheabundanceof benthicinvertebratesinNamibia (GLASSOMBRANCH1997a,1997b). Theirfootstepshavebeenshown to mobilize sedimentsandnutrients(COMÍNetal.1997). However, manyfactorsarelikelytoaffect boththepresenceof macrophytesandflamingos,butno experimentalstudyhas been doneinnaturalmarshesup tonow.
In thisstudywe conductedanexclosureexperimenttotestthehypothesisthat flamingosincreaseturbidityinthewatercolumnandreducethebiomassof submerged
macrophytesandtheabundanceof benthicinvertebratesintemporarymarshesof DoñanaNationalPark. Wecarriedouttheexperimentfor 6 monthsduringasingle hydrologicalcycle,intwo areaswithinthemarshes.
Study site
Our studywas carriedoutin2004 attwo “lucios”(ElLoboandMarilópez)located withinthe26,000 haof naturalmarshesinDoñanaNationalPark (Fig.1, CASTROVIEJO
1993). Thisparkisalsoprotectedas aBiosphereReserve,UNESCO WorldHeritage site,RamsarsiteandanEU SpeciallyProtectedArea.“Lucio”isthelocalnamefor
shallow,seasonallakescreatedindepressionswithinthemarshthatremainflooded
untilthemarshdriesup. At theheightof thewetseason inwinterandearlyspring, luciosaresurrounded by andinterconnectedviashallowerareasof marshthatdry out sooner (ESPINARetal.2002). Themarshisfedby freshwater(rainfallandrunoff) and isolatedfromtidalinfluenceof theGuadalquivirestuary.Theconcentrationof salts dependson thefrequencyandthedurationof flooding(SERRANOetal.2006). While dryingduringthehotanddry summer,themarshlandchangesfromoligohalineto mesohaline(Table1), withawidespatialvariationdependingon distancefrom freshwatersources, depth,etc(CASTROVIEJO 1993). Theaveragenumberof waterbirds winteringintheNationalPark andits surroundings is morethan250,000 birds, and morethan20,000 flamingoswinterinthearea(AGUILERAetal.2006). In verywet years,up to16,000 pairsbreedin theNationalPark marshes(MARTÍDELMORAL
2002;JOHNSONARENGO2005), althoughmanyclutchesarelostduetopredationand changingwaterlevel.
The‘Lucios’ElLoboandMarilópezarelocatedinthenorthernpartof the DoñanaNationalPark (Fig.1).Theyhaveasurfaceareaofca. 120 and300 ha respectively,andaresurrounded by saltmarshvegetationdominatedby perennial Arthrocnemum macrostachyum . Themaximumdepthfor both‘lucios’isca. 1 meter, andfluctuatesstronglywithrainfallandwind direction.Theemergentvegetationis dominatedby scatteredpatchesofScirpus litoralis. During our studythedominant submergedmacrophyteswereRuppia drepanensis, Ranunculus peltatus, Callithriche truncata andcharophytes.Fish speciespresentinbothlucioswereCiprinus carpio, Gambusia holbrooki, Fundulus heteroclitus, Anguilla anguilla andAtherina boyeri.
Materials and methods
ExperimentalplotswereestablishedfromFebruary2004, (priortotheemergencefrom thesedimentof submergedmacrophytesstemsinearlyspring, GRILLASetal.1993),to July2004, thuscoveringmostof thefloodingcycle(fromNovember2003 toJulyin
2004). Two paralleltransectsof 300-400 metresinlengthwereestablishedineachof theluciodelLobo(Lobofromhereon)andtheluciodeMarilópez(Marilópezfrom hereon,Fig.1). Theminimumdistancebetweenthetwo transectswithineachLucio was 90 metres.Fivepairsof flamingoexclosuresandcontrolplotswereestablished
alongeachtransect,makingatotalof20 exclosuresand20 plots.Eachexclosureandits controlwerepositionedon opposingsides of thetransectline,andseparatedby 20 m. Thedistancebetweenpairsof plotswas50-80 m(seeFig.1 for details).Thepositionof eachplotwas pinpointedviaGPS.
Bothexclosuresandcontrolswere4 x 4 msquares delimitedby four ironpoles pushed verticallyintothemudineachcorner.Exclosureswerecreatedby extendinga wirearoundthepolesataheightofca. 70 cmabovethebottom,copyingadesignused successfullyinnearbyfish ponds (RODRÍGUEZ-PÉREZGREEN2006). Thisdesigntakes advantageof themuchgreaterheightof flamingos,andtheheightof thewirewas
selectedaftertrialsconfirmingthatotherwaterbirdspass comfortablyunderneaththe wireandfreelyentertheexclosures(RODRÍGUEZ-PÉREZGREEN2006).
Our plotswerevisitedeachmonth,andphysico-chemicalmeasurementswere taken.Thewaterdepthwas measured(alwaysatthesamecornerof eachplot),turbidity was measuredwithan8cmSecchidiskandtemperature,conductivityandsalinitywere measuredwithaWTWmultiprobe340-idevice.During visits,we alsotookspot measurementsof turbidity(using aHannaHI 93703 probeinFormazineTurbidityUnits (FTU) equaltoNephelometricTurbidityUnits)fromdifferentareasof eachluciothat wereoccupiedby flamingoconcentrationsatthattime,andfromotherpointswithout birds. Wecountedtheflamingospresentineachluciowithbinocularsandrecorded
theirbehaviour(roostingor feeding).
On our finalvisiton 7-8 Julyas thefloodingcyclewas approachingitsend,we tooksamplesof macrophytes,chironomidsandtotalsuspended solids(TSS) fromeach plot.TSS was measuredwithagravimetricmethod(AMERICANPUBLICHEALTH ASSOCIATION1999). One litreof waterwas carefullytakenon arrival,beingcarefulto collectitfromoutsidethesedimentcloudcausedby our steps, thatcouldinfluencethe measurement.Eachsamplewas laterresuspendedinthelab,thenaknown volumeof samplewasfilteredthrougha WhatmanGF/C filterwhichhadpreviouslybeendried andweighed.Eachsaturatedfilterwasthendriedfor 48 h at70º C,keptinadesiccator untiltheenvironmentaltemperaturewas reached,andthenweighedwithaprecision balance(tothenearest0.0001 g).
Wetookfour samplesof macrophytesperexclosurewithaPVCpipesection (0.125 m2cross-sectionalarea)thatwas pushed intothesediments.Allwaterwas extractedwithabowl, andthenall macrophytestemsandleaveswerecutatthebase
andremoved.Toreduceedgeeffects,thepipewas inserted1 mintowardsthecentreof theplotfromthemiddleof eachsideof thesquare.At thelab,sampleswererinsedwith tapwatertocleanthemfrommudandinvertebrates,anddriedat70ºC for 48 h priorto weighting.
Benthoswas sampledby takingfour coresamplesof theupper5 cmlayerof sedimentswitha5.5 cmdiametercorerfromeachplottoavoidedgeeffects,benthos samplesweretakenfromcloseto macrophytesamples,butfromundisturbedareas.At thelab,sampleswerestoredinarefrigeratoruntiltheycouldbefilteredthrougha0.5 mmsieve.Basedon previousexperiencefromexclosureexperimentsdoneinthe adjacentareaVetalaPalma(Rodríguez-Pérez2006), andtherelativeabundanceof chironomidslarvaeinbenthossamples(chironomidswere>80%of benthicinvertebrate retainedby a500 micronssieve),onlychironomidlarvaewereretrievedandpreservedin formalin.Werestrictedtheanalysistothisgroup duetoits majorabundancein macrobenthosinwetlandsanditsroleasverycommonfood itemfor flamingosand other waterbirds(DELHOYOetal.1992, JOHNSON1997). Chironomidlarvaewere identifiedtotribelevel.Thelengthof theselarvaewas latermeasuredunderabinocular microscopetothenearest0.01 micronswiththeaidof adigitalimagesystem.Prior to statisticalanalysis,thedatafromthefour sampleswithineachplotwerepooled,since theywerenotstrictlyindependent.
Toestimatewaterbirdabundance,we used theresultsof theaerialmonthly census of waterbirdscarriedoutin DoñanaNationalPark anditssurroundings. We reporttotalnumberscountedfor thewholecensus of theparkandadjacentareas (includingtheVetala Palmafish ponds, seediscussionandFig1 for thegeographical positionof VetalaPalma).
Statistical analysis
Weused generalizedmixedlinearmodels(GLMs,MCCULLAGHNELDER1989) to analysetheeffectof Treatment(flamingoexclosureandcontrol),Site(Loboand Marilópez)andwaterdepth.TreatmentandSitewereincludedas fixedfactors,and Depthas acontinuousvariable.TheTransect(two persite)andExclosure/ControlPair (nestedwithinTransect)wereincludedas randomfactorsintheanalysis,using GLIMMIX procedure(SASINSTITUTE2005). WeinitiallyincludedTreatmentx Site interactionsbutexcludedthemfromthefinalmodelwhen theywerenotsignificant (p>0.05).Whenpost-hoc analysisof least-squaredmeanswasperformed,the
significancelevel(α=0.05)was adjustedwithFalseDiscoveryRate(FDR) techniques
for repeated-tests(GARCIA2003, GARCIA2004).
For TSS andmacrophytebiomass,we selectedthoseerrordistributionsandlink functionsthatpreventedheteroscedasticity,anddeviationfrommodelassumptions.
TSS was analysedwithalognormalerrordistributionandanidentitylinkfunction. Macrophytebiomasswaslog10transformedandmodelledwithanidentitylinkfunction andnormalerrordistribution.For chironomidcounts,we used anegativebinomialerror distributionandaloglinkfunction(GRAY2005).
A modelwithabinomialerrordistributionandalogitlinkfunctionwas used to analyzethesizedistributionof chironomidlarvae.Thedependentvariablewas the proportionof chironomidlarvaethatweresmalleror equaltothemediansizeobserved (6.475 mm)incontrolplots.Thenumeratorof thebinomiallydistributeddependent variablewas thenumberof larvae≤ 6.475 mm,andthedenominatorwas thetotal numberof larvae(seeCRAWLEY1993).
Graphs of TSS, macrophytebiomassandchironomidabundancewereproduced usinggeometricmeanstobetterrepresenttheskewed datadistributions.Thesewere calculatedby log10+1transformationof theraw data,calculationof thearithmeticmean andSE,followedby back-transformation.
Results
During thecourseof theexperiment,asteadyincreaseinevaporationtogetherwitha lackof waterinputproducedagradualdeclineindepth(Table1), followedby desiccationby theendof July.Sharp risesintemperature,salinityandconductivity occurredovertime,andthelucioschangedfromoligohalinetomesohaline(Table1).
MarilópezheldmoreflamingosthroughoutthestudythanLobo,andhada higher densityof flamingosfromFebruarytoJuneinclusive(Fig.2). Thenumbersof flamingosusingbothluciosincreasedtowardstheendof theexperimentas shallower areasof marshinDoñanadriedout,andasthetotalnumbersof flamingosinDoñana increased(Fig.2). Throughoutthestudy,flamingoswereobservedusingtheareas where our transectswereplaced.However,untilJune, mostof theflamingoswere roostinginflocks(probablyfeedingatnightintheLucioor inothersurrounding areas, e.g.ricefields),whereasfromJune onwards theyspreadoutmoreacross theluciosand increasedfeedingactivity.Turbiditywas visiblyincreasedattheareaswhereflamingos werefeeding.Thus, on 18 June turbidityspotmeasurementsinareasof Lobonot disturbedby flamingoswere20.5 and36.7FTU, whereasinareasdisturbedby flamingostheywere105 and172 FTU. Similarmeasurementsfor Marilópezwere18.4 and26.4 for areaswithoutflamingos,and87 and121 FTU inareaswithactive flamingos.Thelowestturbidityvalues(2.2 FTU inLoboand2.3 inMarilópez)were recordedinMay, when thedensestmatsof macrophytesoccurred.
TSS inJulywas notsignificantlydifferentbetweenTreatments(controlor exclosures),Sites(lucios)or Depth(Table2). However, TSS tendedtobehigherin Marilópezandinflamingoexclosures(Fig.3A).
At thetimeof sampling,Ruppia drepanensis was theonlysubmerged macrophyte stillinflower,theotherspecies(seestudysitesection)havingendedtheir reproductivecyclealready.R. drepanensis representedthegreatmajorityofthebiomass of submergedmacrophytessampled.Macrophytebiomassdidnotdiffersignificantly betweenTreatmentsor withDepth(Fig.3B),buttherewas ahighlysignificanteffectof Site,withmorebiomassinMarilópez(Table2).
BothtribesChironominiandTanytarsiniwererepresentedamongstchironomid larvae.Densityof larvaewas higherinMarilópez(Table3, Fig.3C). Theeffectof Treatmentvariedbetweenlucios,as shown by ahighlysignificantTreatmentx Site interaction(Table3). Post-hoc testsshowed larvalabundancetobesignificantlyhigher inexclosuresthancontrolsfor Marilópez,withno Treatmenteffectfor Lobo(control vs. exclosure:Marilópezt27=2.43,p=0.03;Lobot27=0.42,p=0.2;Fig.3C).
In aGLM of larvalsize,Treatmenthadasignificanteffectintheabsenceof a siteeffect(Table3). Thetreatmentx siteinteractionwas notsignificant(p =0.9).A higherproportionof largelarvaewerefound incontrolsthaninexclosures.Whereas
58% of larvaeinexclosureswereless than6475 μminlength,thiswas truefor only
50% of thoseincontrols(Fig4). Depthdidnothaveasignificanteffectinanyof the analyses.
Discussion
Our exclosureexperimentdidnotprovidesupportfor previoussuggestionsthatgreater flamingosreducebiomassof submergedmacrophytesandincreaseturbidityinthe naturalmarshesof DoñanaNationalPark (MONTESBERNUÉS1991, DUARTEetal.
1990;GRILLASetal.1993). Theseresultsaresurprising, giventhatdirectobservation shows thatfeedingflamingosdo damagemacrophytesandcreatecloudsof suspended sedimentsintheprecisepointswheretheyarestanding,as indicatedby our spotturbiditymeasurements.However, our resultsindicatethattheseeffectswerenotdetectableata broaderscaleacross alucioafterfivemonthsof exclusionandcontrastwithresultsof a previousexperimentinanearbyarea.A significanteffectof flamingoson Ruppia maritima has alreadybeenrecordedinextensivefish ponds inVetalaPalma,anarea adjacenttoDoñanaNationalPark (Fig1 andRODRÍGUEZ-PÉREZGREEN
2006). Sincemostof theseponds werecreatedin1993, thedensityof flamingosinthe NationalPark has decreased,andVetalaPalmahas becomethepreferredareafor flamingos(AGUILERAetal.2004), whicharethedominantwaterbirdspeciestherein termsof biomass(RODRÍGUEZ-PÉREZGREEN2006). Additionally,fish ponds present
ahighersalinityandturbidity,whichincreasesthestress on Ruppia andmayincreaseits susceptibilitytootherstressors such as waterbirds.
Therewas no evidenceofdifferencesbetweencontrolsandexclosuresinthe possibleeffectson waterflow or sedimentation.Furthermore,samplesweretaken separatelyofthepolessituatedateachcorner,toreduceanypossiblestrangeeffect causesby themon thevariablemeasured.
Our studyyear(2004) was averywetyearwithaparticularlyhighextensionand biomassof submergedmacrophytesacross thetemporarymarshesoftheNationalPark, andthisfactmighthaveinfluencedtheoutcomeby minimizingthepossibleeffectof flamingos.Our resultsshow thatastrongereffectof flamingoson chironomid
abundancewas observedatthesite(Marilópez)withahigherdensityof flamingos.
Such densityeffectsarealsotobeexpectedfor macrophyteimpacts,andwe observeda trendfor lowerTSS inexclosuresinMarilópez(Fig.3).
In additiontodifferencesinthedensityof flamingos,otherfactorscanexplain the differentresultsfor elLobo,MarilopezandVetalaPalma(seeRODRÍGUEZ-PÉREZGREEN2006). First,owing topoor visibilitywe wereunabletoquantifymacrophyte coverinanon-destructivemannerduringthecourseof our study,anditispossiblethat significanteffectsmayhaveoccurredearlier(e.g.biomassmayhavebeenfasterto
reacha peakinexclosures).Second,giventhereducedsizeofexclosures,Flamingos feedingclosetoour exclosuresarelikelytohaveincreasedturbiditywithinthem,andit ispossiblewe would havehadsignificantresultswithlargerexclosures.
Wefound flamingostohaveasignificanteffecton benthicchironomidlarvae, reducingtheirdensity(inMarilópez)andchangingtheirsizedistribution.Greater flamingosconsumechironomidlarvae(Johnson1997), andwe havealsofound themto reducethedensityof benthicchironomidsandpolychaetesintheVetalaPalmafish ponds (RODRÍGUEZ-PÉREZ2006). Exclosureexperimentshavealsoshown Greater flamingostohavestrong effectson benthicinvertebratepolychaetedominated communityincoastaltidallagoonsinNamibia(GLASSOMBRANCH1997 a,1997b). Theseauthorsshowed how theexclusionof flamingosincreasedtheabundanceof three polychaetespeciesup tothreetimesinsideexclosurescomparedtocontrolplots, furthermoreflamingosactivityhadconsequenceson sedimentphysico-chemical properties.Additionally,exclosureexperimentsshowed Andeanflamingostohave
majoreffectson benthicprimaryproducers,faunaandflora,andfound significant reductionscausedby flamingos(HURLBERTCHANG1983).
Theexclusionof vertebratepredatorsoftenleadstoindirecteffectson thesize distributionofbenthicinvertebrates,mediatedviacompetitionor interactionswith invertebratepredatorsthemselvesreleasedfrompredationpressure (SIHetal.1985, THRUSH1999). Itispossiblethatthedensityof predatoryinvertebrates,suchas beetles or dragonflylarvae,increasedinflamingoexclosuresleadingtoareductionin chironomidsize.However, such predatoryinvertebratesmaynotbeselectivepredators amongstthesizerangeof chironomidlarvaewe recorded(WELLBORN etal.1996).
Theexclosureeffectswe observedonchironomidsareclearlyattributableto flamingos.Theonlyotherbirds intheareawithsufficientheighttobeexcludedwere smallnumbersof Glossy Ibis (Plegadis flacinelus), butnonewas seennearexclosures andthisspeciespreys mostlyon beetlesandOdonatalarvae(MACÍASetal.2004). Fishes couldenterinsidecontrolsandexclosures,so differencesfound couldnotbe attributabletofishes. Exclosuredesignwas highlyefficienttoexcludeflamingos, allowingothervertebratesdwellingattheluciostoenterbothinsideexclosuresand controlplots.
Althoughwe onlyfound chironomidabundancetobehigherinexclosuresinMarilópez, whereflamingodensitywas higher,thisdoes notnecessarilyindicatethatflamingos were notconsumingchironomidsinLoboaswell,butsuggestedthatthereduced
densityof birds precludedthedetectionof significanteffects.Wealsofound chironomid larvaetobelargerincontrols.If flamingosselectedlargechironomid larvae, we would expecttheoppositeeffect,i.e.larvaetobesmallerincontrols(see SÁNCHEZGREEN2006 for such aresultfor waders). As flamingoshavefinelamellae capableof filteringplankton,itseemspossibleour resultwas duetothemselecting
smalllarvae.Anotherpossibleexplanationfor our sizeeffectisthatanincreaseinlarval densityinexclosuresledtoareducedsizetoinhibitionofgrowthratesbycompetition (ARMITAGEetal.1995). However, thiscouldnotexplainwhy we recordedan
interactionbetweensiteandtreatment.Thirdexplanationcouldbeadifferencebetween
treatmentsintherelativeabundanceof differentchironomidspeciesof differentsize (seeFUENTESetal.,2005). Itisnoteworthythat,althoughcontrolshadahigher proportionof larvaewithlength>6475μm,themaximumlengthwas recordedin exclosures(Fig.4).
Conservationmanagementhas ledtoamarkedincreaseinthesizeof theGreater
flamingopopulationinDoñanaandacross theMediterraneanregionsince1970, making thisoneof themostabundantbreedingwaterbirdsintermsof biomass(JOHNSON1997, WETLANDSINTERNATIONAL2006, AGUILERAetal.2006). Althoughtherewas a
decreaseinthenumbersof flamingosusingthenaturalmarshesof Doñanafollowingthe creationof fish ponds, numberstherehavebegantorecoverinrecentyears(AGUILERAetal.2006. As thewholeSpanishpopulationcontinuestoincrease,numbersinthe NationalPark arealsolikelytocontinueincreasing.Thus,thechanceof
flamingosreachingsufficientdensitiestohaveanimportantimpacton macrophytesand benthosmayincreaseinthefuture,especiallyinyearsof low rainfallwhen flamingos aremoreconcentratedinavailablehabitatthanin2004.
In conclusion,greaterflamingoshaveapronouncedeffecton thebenthic invertebratesintemporarymarshes,as has previouslybeenobservedinmorepermanent habitats.Althoughtheyreducethecoverofsubmergedvegetationinbrackishfish
ponds, thishas yettobedemonstratedconclusivelyfor naturalmarshes.Our study suggest thattheimpactof flamingoson wetlandcommunitiesishighlycontext dependent,andboththedensityof flamingosandenvironmentalfactorsrelatedto macrophytegrowth (inundation,salinity,etc.)arelikelytobeimportant.More research isrequiredtounderstandthenatureof spatialandtemporalvariationintherelationship betweenflamingosandsubmergedvegetation.
Acknowledgements
HéctorRodríguezPérezhadaPhD grantfromtheCSIC-I3P programmefundedby the EuropeanUnion SocialFund. Aerialcountdatawereprovidedby theEquipode SeguimientodeProcesos Naturalesof DoñanaBiologicalStation.An earlierversionof thismanuscriptwas improvedwiththecommentsof two anonymousreferees.
Literaturecited:
AGUILERA,E.,GREEN,A.J.,RENDÓN,M.A.ALMARAZ,P. (2006):Análisisdelos patronesespacialesy temporalesdelaspoblacionesdeavesacuáticas invernantesenDoñana.-Informefinal.OrganismoAutónomodeParques Nacionales.MinisteriodeMedioAmbiente,Sevilla.
AMERICANPUBLICHEALTHASSOCIATION.(1999):Standardmethodsfor the examinationof waterwastewater.-Washigton.
ARMITAGE,P.,CRANSTON,P.S.PINDER,L.C.V. (Eds) (1995):TheChironomidae:the biologyandecologyof non-bitingmidges.-ChapmanandHall,London.
CASTROVIEJO,J. (1993):MapadelParqueNacionaldeDoñana;Memoria.-Consejo
SuperiordeInvestigacionesCientíficas,Sevilla.
CRAWLEY,M.J. (1993):GLIM for ecologist.-BlackwellScience.
COMÍN,F.A.,HERRERA-SILVEIRA,J.A.MARTÍN,M. (1997):Flamingofootsteps enhancenutrientsreleasefromthesedimenttothewatercolumn.In Limnology andwaterfowls.Monitoring,modellingandmanagement.-Proceedingsofa Symposiumon LimnologyandWaterfowl.WetlandsInternationalPublications
43:211-227.
DELHOYO,J.,ELLIOT,A.SARGATAL,J.(Eds.)(1992):Handbookofthebirdsofthe world.- LynxEditions,Barcelona.
DUARTE,C.M.,MONTES,C.,AGUSTÍ,S.,MARTINO,P.,BERNUÉS,M.KALFF,JC. (1990):Biomasade macrófitosacuáticosenla marismadelParqueNacionalde Doñana(SW España);Importanciay factoresambientalesquecontrolansu distribución.-Limnética6:1-12.
ESPINAR,J.L.,GARCÍAL.V.,MURILLO,P.G.TOJA,J. (2002):Submergedmacrophyte zonationinaMediterraneansaltmarsh:afacilitationeffectfromestablished helophytes?.-Journalof VegetationScience13(6): 831-840.
FUENTES,C.,GREEN,A.J.,ORR,J.OLAFSSON,J.S. (2005). Seasonalvariationin speciescompositionandlarvalsizeofbenthicchironomidcommunityin southernAlicante,Spain.-Wetlands25: 289-296.
GALLET,E.(1950):Theflamingosof theCamargue.-Blackwell,Oxford.
GARCIA,L.V. (2003):Controllingthefalsediscoveryrateinecologicalresearch.- TrendsinEcologyEvolution18:553-554.
GARCIA,L.V. (2004):EscapingtheBonferroniironclawinecologicalstudies.-Oikos
105: 657-663.
GLASSOM,D.BRANCH,G.M. (1997a):Impactof predationby greaterflamingos Phoenicopterus ruber on themacrofaunaof two southernAfricanlagoons.- MarineEcologyProgress Series149: 1-12.
GLASSOM,D.BRANCH,G.M. (1997b):Impactof predationby greaterflamingos Phoenicopterus ruber on themeiofauna,microflora,andsedimentpropertiesof two southernAfricanlagoons.-MarineEcologyProgress Series150: 1-10.
GRAY,B.R.(2005):Selectinga distributionalassumptionfor modellingrelative densitiesof benthicmacroinvertebrates.-EcologicalModelling185: 1-12.
GRILLAS,P.,GARCIA-MURILLO,P.,GEERTZ-HANSEN,O.,MARBÁ,N.,MONTES,C., DUARTE,C.M.,TANHAM,L.GROSSMAN,A. (1993). Submergedmacrophyte seedbankinaMediterraneantemporarymarsh:abundanceandrelationshipwith establishedvegetation.-Oecologia94: 1-6.
HURLBERT,S.H.CHANG,C.C.Y. (1983):Ornitholimnology- Effectsof Grazingby theAndeanFlamingo(Phoenicoparrus-Andinus).-Proceedingsof theNational Academyof Sciencesof theUnitedStatesof America-BiologicalSciences80:
4766-4769.
JEPPENSEN,E.,SONDERGAARD,M.,SONDERGAARD,M.CHRISTOFFERSEN,K.E. (Eds) (1998):Thestructuringroleof submergedmacrophytesinlakes.-Spring-Verlag, New York.
JOHNSON,A.R. (1997):Long-termstudiesandconservationof GreaterFlamingosinthe
CamargueandMediterranean.-ColonialWaterbirds20:306-315.
JOHNSON,A.R.ARENGO,F. (2005):Flamingospecialistgroup Newsletternº12.- WetlandsInternational.
MACÍAS,M.,GREEN,A.J.SÁNCHEZ,M.I. (2004):Thedietof Glossy IbisPlegadis falcinellus inDoñana,southwest Spain.-Waterbirds27: 234-239.
MARTÍ,R.DELMORAL,J.C. (2002):LainvernadadeavesacuáticasenEspaña.- DirecciónGeneraldelaConservacióndelaNaturaleza-SEO/Birdlife. OrganismoAutónomadeParques Naturales.MinisteriodeMedioAmbiente. Madrid.
MCCULLAGH,P.NELDER,J.A. (1989):Generalizedlinearmodels.-Chapmanand
Hall.
MONTES,C.BERNUÉS,M. (1991):IncidenciadelFlamencoRosa (Phoenicopterus ruber roseus) enelfuncionamientodela marismadelParqueNacionalde
Doñana(SW España).-In:PINTOS,M.R.,PRIETO,S.,REDÓN,M.JOHNSSON, A. (Eds.):Reunióntécnicasobre lasituacióny problemáticadelflamencorosa (Phoenicopterus ruber roseus) enelMediterráneoOccidentaly África Noroccidental'.-AgenciadeMedioAmbientedelaJuntade Andalucía,Sevilla, pp.105-110.
RODRÍGUEZ-PÉREZ,H.GREEN,A.J. (2006):Waterbirdimpactson widgeongrass RuppiamaritimeinaMediterraneanwetland:comparingbirdgroups and seasonaleffects.-Oikos112: 525-534.
SÁNCHEZ,M.I.,GREEN,A.J.ALEJANDRE,R.(2006):Shorebirdpredationaffects density,biomassandsizedistributionof benthicchironomidsinsaltspans:an exclosureexperiment.-Journalof theNorth AmericanBenthologicalSociety25:
9-18.
SASINSTITUTEINC.(2005):SAS GLIMMIX.
SCHEFFER,M.,HOSPER,S.H.,MEIJER,M.L.,MOSS,B.JEPPESEN,E.(1993): Alternativeequilibriainshallowlakes.-TrendsinEcologyandEvolution8:
275-279.
SCHEFFER,M. (1998):Ecologyof shallowlakes.-Kluwer AcademicPublisher, Dordrecht.
SERRANO,L.,REINA,M.,MARTIN,G.,REYES,I.,ARECHENDERRA,A.,LEÓN,D.TOJA, J. (2006):Theaquaticsystemsof Doñana(SWSpain):watershedsandfrontiers.- Limnetica25(1-2): 11-32.
SIH,A.,CROWLEY,P.,MCPEEK,M.,PETRANKA,J.STROHMEIER,K. (1985):Predation, competitionandpreycommunities:areviewof fieldexperiments.-Annual Reviewof EcologyandSystematics16:269-311.
SONDERGAAR,M.,LAURIDSEN,T.,JEPPESEN,E.VINDBAEKMADSEN,T.(1996):The impactof grazingwaterfowlon submergedmacrophytes:In situexperimentsin ashalloweutrophiclake.-AquaticBotany53: 73-84.
THRUSH,S.E.(1999):Complexroleof predatorsinstructuringsoft-sediment macrobenthiccommunities:Implicationsof changesinspatialscalefor experimentalstudies.-AustralianJournalfo Ecology24: 344-354.
TOURENQ,C.,AULAGNIER,S.,DURIEUX,L.,LEK,S.,MESLÉARD,F.,JOHNSON,A.& MARTIN,J.L. (2001):Identifyingricefieldsatrisk fromdamageby greater flamingo.-Journalof AppliedEcology38:170-179.
VANDONK,E.,DE DECKERE,E.,KLEINBRETELER,J.G.P.MEULEMANS,J.T. (1994).
Herbivoryby waterfowlandfish on macrophytesinabiomanipulatedlake: effectson long-termrecovery.-VerhandlungenInternationalevereinigungfür teoretischeund andwebantelimnologie25:2139-2143.
VANDONK,E.,OTTE,A. (1996):Effectsof grazingby fish andwaterfowlon the biomassandspeciescompositionof submergedmacrophyes.-Hydrobiologia
340:285-290.
WELLBORN,G.A.,SKELLY,D.K.,WERNER,E.E.(1996):Mechanismscreating communitystructureacross afreshwaterhabitatgradient.-AnnualReviewof EcologyandSystematics27:337-363.
WETLANDSINTERNATIONAL.(2006):Waterbirdpopulationestimates.-Wetlands
International.
Table1.- Physicalandchemicalfeaturesof MarilópezandElLobolucioson sampling datesin2004. ‘Bottom’indicatesthattheSecchidiskwas visibleatthebottom, indicatinghighvisibility.
Marilópez
4thFebruary 10thMarch 23thApril 11thMay 18thJune7thJuly
TemperatureºC181826192830
Salinity%0.70.40.70.92.96.6
ConductivitymS/cm1.761.211.672.125.311.38
DepthMin-Max cm46-5163-6952-5750-5325-308-16
SecchiMin-Maxcm14-1924-5122-Bottom Bottom5-172-Bottom
ElLobo
4thFebruary 10thMarch 21thApril 12thMay18thJune8thJuly
TemperatureºC181820222735
Salinity%0.70.40.813.26.8
ConductivitymS/cm1.721.151.892.285.9810.93
DepthMin-Max cm46-5161-6947-5345-5025-2912-18
SecchiMin-Maxcm16-2114-2630-Bottom Bottom 12-Bottom 9-Bottom
Table2.- Summaryof generalizedlinearmodelstestingthemainfactorsSite(two levels)andTreatment(two levels)on totalsuspended solids(TSS, g/l)andmacrophyte dry biomass(g/m2,log10transformed).Theinteractionwas notsignificant(p>0.05)and
was removedfromtheanalysis.Transectandflamingoexclosure/controlpairwere
includedas randomfactorsusingtheGLIMMIX procedure,withidentitylinkfunction andlognormalerrordistributionfor TSS,andnormalerrordistributionfor macrophyte biomass.Marilópezandexclosureswerealiased.Seemethodsfor details.
TotalsuspendedsolidsMacrophytebiomass
Estimate SE dfN dfDF p Estimate SE dfN dfDF p Intercept 4.18 0.21 -1.03 0.07
Site128 4.20 0.05128 35.59 <0.0001
ElLobo-0.510.25-0.40.07
Treatment128 1.64 0.21280.230.6
Control0.320.25-0.040.03
Table3.- Summaryof generalizedlinearmodelstestingthemainfactorsSite(two levels) andTreatment(two levels)on chironomidlarvaeabundanceandchironomidsize. Whentheinteractionwas notsignificant(p>0.05)itwas removedfromtheanalysis. Transectandflamingoexclosure/controlpairwereincludedas randomfactorsusingthe GLIMMIXprocedure,withloglinkfunctionandnegativebinomialerrordistributionfor chironomidabundance,andlogitlinkandbinomialerrordistributionfor chironomidsize. Marilópezandexclosureswerealiased.Seemethodsfor details.
ChironomidabundanceChironomidssize
Estimate SE dfN dfD F P Estimate SE dfN dfD F P
Intercept / 3.7 / 0.3 / 0.39 / 0.17Site / 1 / 27 / 9.23 / 0.005 / 1 / 24 / 0.02 / 0.9
ElLobo / -1.68 / 0.4 / 0.03 / 0.2
Treatment / 1 / 27 / 0.50 / 0.5 / 1 / 24 / 4.44 / 0.05
Control / -0.99 / 0.4 / -0.36 / 0.17
Sitex Treatment / 1 / 27 / 7.14 / 0.01 / n.s.
ElLobox
Control1.570.59
Fig1.- Map of thestudyareashowing thelocationwithinSpain.A schematicdrawing shows aclose-upofeonetransectwithfivepairsof controlplotsandflamingo exclosures.Thelargeimageisaclipof LandsatTM imagecomposedwiththebands 5,
4, and3 (RBG) for theareaof studyat13thof June 2004, showing floodedareasof the
marshindarkgrey.Two straightparallelwhitelinesineachlucioindicatetheposition of thefour transects.
Fig2.- Monthlyaerialcountsof flamingosatMarilópez(lightgreybars), ElLobo
(blackbars), andtotalnumberof flamingos(straightline)countedfor thewholeDoñana areaduringtheaerialcensus for theperiodfromJanuarytoJuly2004. Thelefty axis shows thescalefor luciocountsandrighty axisfor thewholeof Doñana.Maximum floodedareaof Lobo120 Ha andmaximumfloodedareaMarilopez300 Ha.
**
n.s.
Fig3.- Geometricmeanandback-transformedSEof TSS, macrophytebiomassand chironomidcountsfor bothtreatmentsinthetwo luciosinJuly2004.
Fig4.- Sizefrequencydistributionofchironomidstakenfromcontrolsandexclosures, combiningdatafor bothlucios.Theintervalsfor lengthinthex axisareof 0.5 mm.N referstothetotalnumberof chironomidsrecordedineachtreatment.Thedashedline shows themedianvalueof 6475μm.