DOI10.1007/s10750-010-0370-0
PRIMARY RESEARCH PAPER
Recoveryofzooplankton diversity inarestored Mediterraneantemporarymarsh inDon˜ana National Park (SWSpain)
AnnaBadosa• Dagmar Frisch •
ArantzaArechederra• LauraSerrano•
AndyJ.Green
Received:16November2009/Revised:24June2010/Accepted:30June2010/Publishedonline:8August2010
Abstract Over30yearsafterdrainageforagricul- ture,a2700hatemporarymarshlandwasrecently restoredinDon˜anaNationalPark.Wedescribethe recoveryofzooplankton communities (copepods, cladoceransandrotifers)in47newtemporary ponds excavatedaspartoftherestorationprojectduring the first twohydroperiods(April2006and2007),and compare themtothoseofeightreferencesitesinthe surroundingmarshland. Majorchangesinthespecies composition andabundanceoccurredinnewponds between years.Whilerotifersandcyclopoidcope- podsdominatedintermsofnumberofindividualsin
2006,calanoidcopepods andcladoceranswerethe mostabundant groups in2007.Rotifer species richnesswassignificantly lowerin2007,butthere wasanincreaseinSimpsonandb-diversityin2007 owing largelytoadramaticdeclineintheabundance ofHexarthracf.fennica(rare inreferencesites) from
93%ofallrotiferindividualsinnew pondsin2006to
Handlingeditor:K.E.Havens
A.Badosa() D.Frisch A.Arechederra A.J.Green DepartmentofWetlandEcology,Don˜anaBiological Station(EBD-CSIC),C/Ame´ricoVespucios/n,Isladela Cartuja,41092Sevilla,Spain
e-mail:;
L.Serrano
DepartmentofPlantBiologyandEcology,University ofSevilla,P.O.Box1095,41080Sevilla,Spain
only32%in2007.Incontrast,speciesrichness of copepods andcladoceranswassignificantlyhigherin newpondsin2007,buttherewerenochanges in Simpsondiversity. b-Diversityofcladoceranswas alsosignificantlyhigher in2007.In2006, thespecies richness ofcladoceraandcopepods wassignificantly lowerinnewpondsthaninreferencesites,butby
2007 there were no differences in richness or Simpsondiversity.Overall,7copepod,13cladoceran and26rotifertaxawererecorded innewponds, including80%oftaxarecorded inreferencesites. Theseresultsindicatethatzooplankton communities canberapidlyrestoredinMediterraneantemporary wetlands,atleastwhenlargesourcepopulationsin the surrounding area reduce dispersal limitation. Theyalsoillustratetheimportance ofcomparing differentmetricsofrichnessanddiversityinstudies ofzooplanktonrestoration.
Keywords Wetlandrestoration
Mediterraneantemporaryponds Zooplankton Speciesrichness a-andb-diversity Colonization
Introduction
In recent decades, freshwaterbiodiversityhas declinedfasterthanterrestrial ormarinebiodiversity, andincreasing demandsonfreshwater resources, climatechangeandtheimpactofalienspecieswill
leadtoacontinuinglossofbiodiversity inthefuture (Jenkins,2003;Garc´ıa-Berthouet al., 2007;Moss etal.,2009).Restoration ofdegradedwetlandsor creationofnewonesarenowcommon measuresfor conservationofaquatic biodiversity(Cookeet al.,
2005;Williamsetal.,2008).
Zooplankton communitiescanprovideanexcel- lentmodelforassessingthesuccessofrestorationand increasingourunderstanding ofrestorationand community ecology(Dodson &Lillie,2001;De Meesteretal.,2005).Todate,studiesofrestoration ofzooplankton communitieshaveconcentrated mainlyonlakecommunities innorthern-temperate regions.Forexample,inlakesdegraded byeutrophi- cationandfish introductions,reductionofnutrient loadingandcontroloffishstockscanleadtorecovery ofmanycladocerantaxapresentbeforedegradation within3years(Louetteetal.,2008),whichinturn canfacilitatetop-down control ofphytoplankton abundance andrestoration ofclearwater states that favourhighbiodiversityingeneral(Jeppesenetal.,
2007).Dodsonetal.(2007) foundnewlakesin Wisconsin (averageageof14years)tohavesimilar zooplankton speciesrichnessthanmucholderlakes, although itisunclearhowlongittooktoreachsuch levelsofrichness. InCanadian mountain lakes, zooplankton communities took about 19 years to recoverfullyafterremovalofintroducedsportsfish (Donaldetal.,2001).Zooplankton recoveryafter restorationofacidifiedlakescanbehighlysuccessful, atleastforsometaxa(Yanetal.,2004, Gray& Arnott,2009).Afteranexperimentalacidification of an 18ha lake during 6 years, the zooplankton communityreturnedtoreferencelevelsafteranother
6years(Frostetal.,2006).Factorsdeterminingthe recoveryspeedofindividualtaxaincludethelength ofthedegradationperiodpriortorestoration,andthe life-historyofthe zooplankter(Knapp& Sarnelle,
2008).Incaseswheredispersal limitationprevents recolonizationbynaturalmeans,sometaxahavebeen successfullyreintroduced(KohoutFott,2006).
Wetlandlosshasbeenparticularlyintenseinthe
Mediterraneanregion(Greenetal.,2002;DeStefano,
2004),and Mediterraneanenvironmentsareapriority for biodiversity conservation at a global scale (Brooksetal.,2006).TemporarypondsinMediter- raneanregionsarebiodiversity hotspotshighly threatened by habitat degradation (Grillas et al.,
2004;Oertlietal.,2009)andareamongthemost
protectedEuropeanaquaticenvironments (EUHabitat Directive92/43/EEC). Thetemporarypondsand marshes in Don˜ana National Park in South-West Spain(Serranoetal.,2006)areparticularlyfamous andareprotected as aUNESCOWorldHeritageSite, owing largelytotheirgreatinternationalimportance for waterbirds (Rendo´n et al., 2008). Studies of zooplanktonsince1980havefocusedmainly on dune pondsoutsidethemainmarshland, whichhostan endemicrotiferspecies(Fahdetal.,2000, 2009). After minewaste contaminatedtheareasurrounding theNational Parkin1998(Taggartetal.,2006),a major restoration project was launched to restore someareasoftemporarymarshpreviously trans- formedforagriculture(Enggass,1968;Garc´ıa-Novo
Mar´ın,2006).
Inthisstudy,wedescribethezooplankton com- munitiesthathavedevelopedinthelargestrestora- tion area in Don˜ana, including the copepods, cladoceransandrotifers.Asrecommendedforstudies ofrestorationofzooplanktoncommunities(Gray& Arnott,2009),giventheabsenceof historicaldatafor ourstudyareawecombinedtemporalsamplingand theuseofreferencesitestoassessthesuccess of recovery.Furthermore, unlikemostrestorationstud- ies(DodsonLillie,2001;GrayArnott,2009),we didnotfocusexclusivelyonspeciesrichness,but usedandcompared variousmetricsofdiversityand richnessasdistinctindicatorsofrecovery.
Materialsandmethods
Studysite
The main study area was the Caracoles estate (Fig.1), a former seasonally inundated marshland areaof2700hathatwasisolatedfromsurrounding marshes(alsoknownasthe‘‘marismasdelGuadal- quivir’’)andturnedinto arablefarmlandinthe 1960s. ItislocatedonthenorthernedgeofDon˜anaNational Park(Fig.1)andsituatedintheGuadalquivirestuary at1–2ma.s.l.,butfreefromdirecttidalinfluence. During the ‘‘Don˜ana 2005’’ restoration plan, the estatewasincorporated intotheNationalPark,the surroundingdykesandagriculturaldrainagesystem wereremovedandasetof96experimentaltemporary pondswere createdbetweensummer2004and spring
2005(Santamar´ıaetal.,2006;FrischGreen,2007).
Fig.1 Mapofthestudy area.Thesubsetofnew pondsincludedinthe presentstudyisinblack. Notetheoldstreambed (Can˜oTravieso,dotted line),whoseconnectionto
naturalmarshestothesouth wasrestoredatthesame timeasthenewpondswere excavated
Alltheponds havethesameellipticalshape butwith threedifferentsizes(surfaceareaof0.18,0.74and
2.95ha),andanexcavateddepthof30or60cm. Ponds are distributed in two major blocks of 44 ponds,plus8relativelyisolated ponds distributed throughout theestate(Fig.1).Themainblockswere situatedinrelativelylow-lying areasthatwere regularlyinundated priortotheagriculturaltransfor- mation(Santamar´ıa etal.,2006).Thepondsare primarily filled by precipitation and local surface run-off fromwithintheestate,withvariationin microtopography causingdifferencesindepthand hydroperiod.Duringthisstudy,somepondstempo- rarilyoverflowedandconnectedtofloodedgrassland areasduringandaftermajorrainfallevents.During the summer, all new ponds and reference sites (seebelow)dryoutcompletely,asdoesalmostall thenaturalmarshsystemwithintheNationalPark (seeSerranoet al.,2006;Espinar& Serrano,2009for details).Duringthewettestperiods,movementwithin theCaracoles estateandtherestofthemarshesis impossiblebyvehicle,makingresearchdifficult.
Don˜anahasaMediterraneanclimatewithAtlantic influence, withdry,hotsummersandshort,mild winters.Rainfallisvariableandconcentrated mainly betweentheendofSeptember andthebeginning of April, withhightemperaturescausing rapidevapora- tioninthesummermonths(EspinarSerrano, 2009 andreferencestherein).Theautumn–winterfollow- ingpondconstructionwasexceptionally dry,with
only 167mm of rainfall from September2004to
March2005(comparedtoameanof455mmfor
1979–2009,datafromPalaciodeDon˜ana),andonly puddleswereformedinthebedofafewoftheponds foramaximumof20days(FrischGreen,2007). Thus,thebasinsofthenewpondswerecompletely inundatedfor thefirsttimeinJanuary2006following heavy rainfall (136mm in January, followed by
150mmfromFebruarytoApril).Hydroperiodlength varied,withsomepondsbeginningtodryout inearly MayandotherspersistinguntillateJune2006.The nexthydroperiodstartedmuchearlierinlateOctober
2006 owingtoabove-average precipitationbetween SeptemberandDecember 2006(445 mm,compared to149mmforthesamemonthsin2005).Thefirst pondsdriedoutinearlyMayandsomepersisteduntil July 2007. Water temperatures became high from Mayonwardsandalreadyreachedmaximaofover
35°CinthefirstweekofMay.
Zooplanktoneggbankswerealmostindetectable inthenewponds aftertheirexcavationandprior to first hydroperiod. Only two rotifer individuals hatchedfromatotalof72sedimentsamples(Frisch
Green,2007).Justbeforetherestorationproject, theeggbankinanoldstreambed thatcrossesthe estateneartheponds(Fig.1)waslowindiversity andabundance, despitebeingtheonlypartofthe estatethatstillfloodedinwinterduringtheagricul- turalphase(Frisch etal.,2009). Cattlewereelimi- natedfromtheestatebeforethenewpondsfilledwith
water, butharesandfallowdeerwerepresent throughoutthestudyandactedaspotentialagents ofzooplankton dispersal,togetherwithwaterbirds (Frischetal.,2007;Rendo´netal.,2008).
Sampling
Asubsetof47 new pondsrepresentative ofallponds, intermsofsize,depthandconnectivity wasselected for sampling, including ponds from both major blocks as well as isolated ponds (Fig.1). Nearby naturalandsemi-natural temporarywaterbodies presentaroundtheCaracoles estatewereselectedas referencesites tobesampledsimultaneously(Fig.1). Theseincludedeight siteswhich were apotential sourceofcolonistsforthenewpondsandvariedin hydrogeomorphology(e.g.ditches,anoldstreambed, smallmarshdepressions andshallowponds), and aquatic communities(e.g.presenceorabsenceoffish, extentofaquaticvegetation).
Inthispaperwepresentdatafromtwosampling campaignsthatwerecarriedoutfrom17–26April
2006and16–24April2007tocomparethezooplank-
toncommunitypresentduringthefirst twohydrope- riodsatastandardtimeofyear.Aprilwasselectedasan optimalmonthforlong-term monitoring,because accesstotheareaiscomplicatedduringearlier,wetter months, andbecause thepondsandreferencesites begin todryoutcompletelyfromMayonwards. Samplingwascarriedoutbetween10:00and18:00h, avoidingperiodsofhighwindsorrainfall.
Ineachnewpond andreferencesite,zooplankton wassampledbyfilteringatotalof20Lofwater througha64lmmesh-sizenet,andpreservedin70% ethanol. The smallest rotifers are likely to have passedthroughthismesh.Fortysubsamples(each
500ml)werecombinedtoovercometheexpected patchydistributionofzooplankton. Thewaterwas collected with a 500ml plastic jar while walking alongatransectfromtheshoretothecentreofthe pond.Everysubsamplewastakeninfrontortothe side of the personsampling,takingcare to avoid areaswheresedimenthadbeendisturbed.Toavoid spreadingzooplanktonbetweenponds,thesampling equipmentwasthoroughlyrinsedwithtapwaterand
70%ethanolinbetweenconsecutiveponds. In addition,bootswerecovered withplasticbagswhich werereplacedforeachpondtoavoidsedimentand propaguletransferfromonepondtoanother.
Allzooplankton individuals (includingrotifers, copepodsandcladocerans)werecounted,andiden- tified tospecieslevel(wheneverpossible),using Utermo¨hl chambersundera Zeissinvertedmicro- scope,mainlyatmagnificationsfrom509to4009. Fortheobservationofsomemorphological details, involving individualdissection, alightmicroscope withmagnifications from4009to10009wasused. Taxa were identified according to Dussart (1967,
1969)andEinsle(1993)forcopepods, toAlonso (1996) forcladocerans,andtoKoste(1978)for rotifers. Bdelloid rotifersandjuvenilestagesof copepodsandsomecladocerans couldnotbeiden- tified tospecieslevel.Sampleswithlessthan400 individualswerecountedwithoutsubsampling. At higher densities, subsamples representing at least
1/16thof thetotalsample,andcontainingatleast200 individualsofthemostfrequent taxon, werecounted. Thecompletesamplewasthenscreened microscop- icallytofindandidentifyraretaxa.
Depth(takenastheaveragefromfive points), temperature,pHandelectricalconductivity were measuredinsitu (Table1).Environmentalconditions weresimilarbetweenyearsforbothnewpondsand referencesites(Table1),theonlyexceptionbeing thatpHwashigher inthenewponds in2007 (Wilcoxonpairedtest,P\0.001).In2007,chloro- phyll-a(mean±SE=3.84±0.67lgl-1 fornew ponds,9.60±4.84forreferencesites),totalphos- phorus(59.81±5.15lgl-1for newponds,132.23±
29.04forreferencesites),andturbidity(17.60±3.12
NTUfor newponds, 63.78±41.08for reference sites) were also measured. pH was negatively correlated withchlorophyll-aconcentration(Pearson’sR=0.353, P=0.012).
Nofish werepresentinthenewpondsduringthe study,butbothfishandcattlewerepresentin someof thereferencesitesoutsidetheCaracolesestate(Fig.1). Innewponds,there wasa notableincreasefrom2006 to2007intheproportion ofthebottomcoveredwith submergedvegetation,especiallycharophytes,Ruppia drepanensisandRanunculus peltatus.Unlikenew ponds,referencesiteshademergentvegetation(e.g. ScirpusmaritimusandJuncussubulatus).
Zooplanktondiversityandcommunitysimilarity
a-Diversitywasquantified bytwomeasures:local speciesrichnessasthenumberofallidentifiedtaxa
Table1 Mean,standarderror(inparentheses)andrangeforenvironmentalvariablesrecorded inthenewpondsandreferencesites
April2006 / April2007Mean(SE) / Range / Mean(SE) / Range
Newponds / N=47 / N=47
Temperature(°C) / 20.31(0.36) / 16–27.30 / 21.02(0.41) / 16.80–28.30
pH / 8.50(0.07) / 7.09–9.21 / 9.05(0.05) / 8.50–10.18
Electricalconductivity(mScm-1) / 6.88(0.50) / 2.03–17.04 / 6.94(0.33) / 2.64–15.22
Watercolumndepth(cm) / 19.06(1.44) / 5.00–49.40 / 21.32(1.42) / 6.80–48.40
Referencesites / N=8 / N=6
Temperature(°C) / 21.96(0.98) / 19.8–27.8 / 22.18(1.63) / 16.30–25.70
pH / 8.62(0.13) / 7.96–8.96 / 8.99(0.26) / 8.16–9.65
ElectricalConductivity(mScm-1) / 4.55(0.52) / 2.16–6.64 / 5.37(0.74) / 4.09–9.00
Watercolumndepth(cm) / 12.92(2.75) / 4.4–29.6 / 18.80(3.21) / 10.02–33.40
SignificantdifferencesbetweenyearswereonlyfoundforthemeanpHvalueinthenewponds(Wilcoxonpairedtest,P\0.001)
perpondandyear,andtheSimpson index,which takesintoaccounttherelativeabundances ofthe identifiedtaxa. Allthesemeasureswerecomputedfor eachnewpond andreferencesiteforthewhole zooplankton community,aswellasforrotifer, cladoceranandcopepod assemblagesseparately. Between-yeardifferencesfor measuresin a given newpondweretestedwithnon-parametricWilcoxon matched-pairedtests.Differencesbetweennewponds andthe reference sitesweretestedforbothyears usingnon-parametricMann–Whitneytests.
b-Diversityasameasureofcommunitydifferen- tiationamongsites canbeestimatedby averagingthe dissimilarity values among sites (Legendre et al.,
2005).Dissimilaritiesamongpondswereestimated
usingthecomplement-to-oneoftheabundance-based Chao–Sørensen similarityindex(computedusing EstimateS v.8.0software,Colwell,2005).Thisindex isrecommended forassessingcompositionalsimilar- itybetweensamplesthatdifferinsizeandarelikely tocontainnumerous rarespecies(Chaoetal.,2005). Foragiven year,theb-diversitywasestimatedby averagingthedissimilarity valuesobtainedfrom pairwisecomparisons amongponds.Itwasalso estimatedforrotifer,cladoceranandcopepod assem- blages.Between-year differencesofthefrequency distributionsofpairwisecomparisonsofb-diversity weretestedwithWilcoxon matched-pairedtests(i.e. comparingthevaluesforagivenpondin2006and
2007).
Aredundancy analysis(RDA)wascarriedoutto examine community composition patterns in new
pondsandtheirrelations withtheenvironmental variables measured(LepsˇSˇmilauer,2003).Priorto analysis,waterdepth,conductivityandtemperature
werelog(x?1)transformed.Theyearofsampling (2006or2007)was added also asapredictorvariable intheRDA(nominalvariable).Abundances of juvenilestagesofcopepods andcladoceranswere includedtoperformthisanalysis.Theabundancedata matrixwassubjectedtotheHellinger transformation followingLegendreGallagher(2001).
Differences betweenyearsinthefrequency of occurrence (i.e.number ofponds whereagiventaxa wasfound),andinthefrequency ofdominance(i.e. number ofpondswhereagiventaxon wasthesingle mostabundant taxon)weretestedbymeansofFisher exacttests.
Results
Changesindiversityandabundance betweenyearsinnewponds
Inthenewponds,therewasasignificantdecreaseinthe totalabundanceofzooplanktonfrom2006to2007 (means of709and 164individualsperlitre,respec- tively,Wilcoxonpairedtests,P\0.001).Thisreflects adrasticreductioninthemeanabundance ofrotifers (from459to22individualsperlitre,P\0.001)as wellasasignificantreduction inthemeanabundance ofcopepods(from240to117individualsperlitre, P=0.044,Fig.2).Incontrast,theabsoluteabundance
Fig.2 Barplotsshowingthemeantotalabundance(no.of individuals perlitre)ofthecopepod,cladoceranandrotifer assemblagesrecordedinnewpondsforbothyears.Errorbars show95%confidence intervals
ofcladoceransincreasedfromameanof10individuals perlitrein2006to24in2007(P=0.002).Intermsof relativeabundance, bothcladoceransandcopepods increasedin2007attheexpenseofrotifers(Wilcoxon paired tests, P\0.001). The mean percentage of rotifersdropped from65%in2006to14%in2007, whereas forcopepodsandcladoceransitincreased from34to 72andfrom2to 15,respectively.
a-Diversitymeasured aslocalspecies richness (richnessperpond)ofthezooplanktoncommunity didnotdiffersignificantlybetween2006and2007 (Table2).Incontrast,a-diversitymeasuredbythe Simpsonindexwassignificantlyhigherin2007.When analyzingcopepods, cladoceransandrotiferssepa- rately,thespeciesrichness foreachgroupdiffered significantly between years (Table2). While the localrichnessincreasedin2007forcopepodsand
Table 2 Mean,standarderrorandrangeforlocalspecies richnessandSimpsondiversityindexinnewponds(N=47) and the reference sites (only those sampled in both years,
N=6) for the whole zooplankton community, and for copepods,cladoceransandrotifersseparately
Simpsondiversity
Simpsondiversity
DifferenceswereanalyzedwithWilcoxonpairedtests
cladocerans,itdecreased forrotifers. Between-year differences intheSimpsonindexwasfoundonlyfor rotifers,withasignificantincreasein2007(Table2). Whencomparingthefrequencydistributions ofpair- wisecomparisonsofb-diversitybetween2006and
2007 (Fig.3), significant differences were found (Wilcoxon paired tests, P\0.001), indicating a greateramong-ponddifferentiationor higherb-diver- sityin2007forthewholezooplanktoncommunity,and alsoseparatelyforcladoceranandrotiferassemblages. Theb-diversityofthecopepod assemblageswasalso higherin2007,butnotsignificantly so(Wilcoxon pairedtest,P=0.067).
Changesintaxonomiccompositioninnewponds
Upto37.9% ofthetotalvariationofthespeciesdata wasexplainedbythepredictor variables.Thefirst RDAaxisaloneaccountedfor31.3%ofthevariability whereasthesecondoneonlyaccountedfor4.1%.The effectofthetwofirstaxeswassignificant(P=0.002 with499permutations) buttheeffectofthethird canonicalaxiswasnot(P=0.268).ThefirstRDA axiswashighlyrelatedtotheyearofsampling(r=-
0.870).pHwasthesecond variablemostrelatedwith thisaxis (r=-0.490).Conductivityandwaterdepth werethevariablesmostrelatedwiththesecondaxis (r=0.565andr=-0.449, respectively).Theyear ofsamplingwasclearlythemostimportantvariablein explainingthevariationobserved inthespeciesdata sincecommunities frombothyearswereperfectly separatedalongthisaxiswithpositivesscoresforthe
2006communitiesandnegativescoresforthoseof
2007(Fig.4).Thisindicatesthatzooplanktoncom- position differedgreatlybetweenyears,withmajor differences inthemostabundantspecies.Therotifer Hexarthracf.fennicawashighlyabundantin2006, whereas calanoidnauplii,adultsofthecalanoid Neolovenula alluaudiandthecladoceranMoina brachiatawerehighlyabundant in2007.When removing theeffectoftheyearofsamplingasa predictorinasecond RDA(results notshown), the environmentalvariablesonlyexplained6.9%ofthe speciesvariation,although theireffectwasalso significant(P=0.002with499permutations),and conductivityandwaterdepthwerethemoreimportant variables.Highabundances oftherotiferBrachionus plicatiliswererelated to higherconductivity,whereas
highabundancesofcalanoidcopepodidswererelated togreaterdepth(Fig.4).
In2006,juvenilecyclopoid stages(naupliiand copepodids)andadultsofthecyclopoidMetacyclops minutus werethemostabundantcopepodsinnew ponds,representing 94%ofcopepods(Table3).The most abundant cladocerans were Moina brachiata followed byCeriodaphniaquadrangula,together constituting 92%ofcladocerans.Themostabundant rotifers were Hexarthracf. fennica, followed by B. plicatilis, together representing 98% of rotifers (Table3). In terms of frequency of occurrence, juvenilecyclopoidstages,M.minutus, M.brachiata andH.cf.fennicawerethemostwidespreadtaxain
2006,eachonebeingpresentinat least98%ofponds (Table3).Ofthesetaxa,M.minutus andM.brachi- atadid notdominatethecommunityinanypond (i.e. theywereneverthemostabundant taxoninagiven pond), in contrastto cyclopoidnauplii and H.cf. fennicawhichweredominant in13and30ofthe47 ponds,respectively(Table3).Thehighabundanceof thesefewtaxainalargenumber ofpondsexplained theverylowdissimilarityindices foundin2006fora largenumberofthepairwisecomparisons(Fig.3). Overall,60%ofthetaxarecordedin2006occurredin lessthan20%ofthenewponds.
In2007,calanoidjuvenilestages werethemost abundantcopepods. Togetherwithadultsofthe calanoid Neolovenula alluaudi, they represented
55%ofcopepodindividuals.Thisspeciesincreased itspresencefrom4%ofnewpondsin 2006to85%in
2007(Fisherexact,P\0.001).Amongstcladocer-
ans,the mostabundantspecieswereM.brachiata andDaphnia magna,togetherrepresenting93%of individuals.Compared to2006,theformertaxon increased markedlyinthefrequency ofdominance, andthelatterinfrequencyofoccurrence(Table3). N.alluaudi,M.brachiataandD.magnasignificantly increasedtheirabsoluteabundancein2007(Wilco- xon paired tests, P\0.05). The most abundant rotifers were Keratella tropica and Hexarthracf. fennica,togetherrepresenting 65%ofindividuals, althoughLecanelunahadthehighestfrequency of occurrence.However, Hexarthraunderwentmajor declinesinabundance(P\0.0001)and frequencyof occurrence(P\0.001).It wasthe mostabundant zooplankter in30pondsin2006,butinnonein2007 (P\0.001). In 2007, L. luna increased its total
bFig.3 For2006and2007(leftandrightplots,respectively): frequencydistributionsofpairwisecomparisons(N=1081)of b-diversity(measuredascomplement-to-one oftheChao– Sørensen similarityindex)inthenewpondsforthewhole zooplankton community andthecopepods,cladoceransand rotifersseparately
abundance(P\0.001)anditsfrequencyofoccur- rence(P\0.05).ThecyclopoidAcanthocyclopscf. robustuswasnotrecordedin2006,butwaspresentin
23% of pondsin 2007 (P\0.001). Also striking were significant reductions in absolute abundance (P\0.001)andfrequencyofoccurrence(P\0.001) oftherotifersB.plicatilisandB.quadridentatus,and ofthecopepodMixodiaptomusincrassatus in2007 (Table3).In2007, 63% ofthetaxarecordedstillhad afrequencyofoccurrencebelow20%.
Zooplanktoncommunitiesinnewandreference sites
Innewponds,atotalof46taxawererecordedin
2006and2007combined:7copepods, 13cladocer- ansand26rotifers. Fromeachgroup, 5,9and14 species, respectively,werecommontobothyears. Totalspeciesrichnessforcopepods(6)andcladoc- erans(11)wasthesameforbothyears.Fortherotifer assemblage,speciesrichnessincreasedfrom19in
2006to21in2007.Therefore, totalspecies richness in new ponds was 36 in 2006 and 38 in 2007 (Table3). Despite the small number of reference sites,thetotalspeciesrichnessrecorded inthemwas similarwithatotalof44taxa:9copepods, 14 cladoceransand21rotifers.Fromeachgroup,5,6 and7species,respectively, werecommontoboth years.Totalcumulativespeciesrichness wasalso similarbetween 2006and2007with32and30taxa, respectively (Table3). Eighty percent of 44 taxa foundinreferencesiteswerealsorecorded innew ponds,only3copepods, 2cladoceransand4rotifers beingabsent.Ontheotherhand,1copepod, 1 cladoceranand6rotifertaxafoundinnewponds werenotfoundinreferencesites(Table3).
Forthereferencesites, therewerenosignificant differencesbetween2006and2007inlocalspecies richness andSimpsondiversityofthewholezoo- planktoncommunityor ofthecopepod,cladoceranor rotiferassemblages(Table2).Similarly,nosignifi- cantchanges intheabsoluteabundance ofzooplank- tonwererecorded(Wilcoxonpairedtests,P[0.05).
Whencomparing newpondswithreferencesites, significant differencesinlocalspeciesrichnesswere recordedin2006,withlocalspeciesrichnessbeing lowerinnewpondsforthewholecommunity,and alsoforcopepods andcladocerans(Mann–Whitney test,P\0.05,Fig.5).Forrotifersin2006,andall comparisons in2007,therewerenosignificant differences between the new ponds and reference sites(Fig.5).NosignificantdifferencesinSimpson diversityindexwerefoundbetweennewpondsand referencessitesineitheryear(Mann–Whitneytest, P\0.05).
Discussion
Toourknowledge, thisisoneofthemostextensive studiestodateofzooplankton inrestoredMediterra- nean wetlands. The present study confirms the success of the Don˜ana restoration project and its newponds,whichhaverapidlyacquired diverse zooplankton communitieswithsimilaritiestothose foundin the natural wetlandsusedasa reference sites.Themuchsmallernumberofreferencesites thannewpondsgaveusreduced statisticalpower for comparisonswithnewpondsandtodetectchanges between yearsinthereferencesites.However, we wererestrictedbythelimitednumberofisolated and accessiblewaterbodies intheareasurroundingthe Caracolesestatesuitableasreferencesites(Fig.1).
Snapshotsamplings oftenfailtodetectasub- stantial fraction of the annual species pool (e.g. Arnottetal.,1998;Fahdetal.,2007).Ideallysamples shouldbetakenmorethanonemonthayear, but comparison atseveralpointsintheannualcycleis difficultintemporarypondswithvariablehydrope- riods. Thetimingandextentofinundation is extremelyvariableinDon˜anainresponsetorainfall fluctuations (Kloskowskietal.,2009),leadingto majorannualvariationinhydroperiodanddepthin thenewponds.The30yearmeanforprecipitation between September and March inclusive at the PalaciodeDon˜anais440mm,andwestudiedone year that was slightly below average (402mm in
2006)withalatestarttothehydroperiod,andone thatwaswellaboveaverage(599mmin2007).
Arangeofmetricsindicatedtherecovery of zooplankton communities over time in the new ponds,althoughthe resultsvariedwiththe metric
Fig.4 RDAordination triplotsummarizingthe differencesbetweenyears andtheeffectsof explanatoryvariableson zooplanktoncommunities. Speciescodesforthe displayedspecies(only thosewith17%oftheir variationexplained)are: Aloazo:Alonaazorica; Alorec:Alonarectangula; Braplic:Brachionus plicatilis;Braqua: Brachionusquadridentatus; Cal_nau:calanoidanauplii; Cal_cop:calanoida copepodids;Hexar_sp: Hexarthrasp.;Leclun: Lecaneluna;Moibra:
Moinabrachiata; Neoall:
Neolovenulaalluaudi
used.Most studiesofrestorationofzooplanktonhave focusedonlyonspeciesrichness(GrayArnott,
2009),buttheinclusionofdiversitymetrics,asinthe presentstudy, cangivedifferent andcomplementary results.Thisisillustratedbyrotifers innewponds, whichhadlowerrichnessperpondin the second year,buthigherSimpsonandbetadiversity. In additiontothisrecovery ofrotiferdiversity, thetotal number ofrotifertaxafoundinallnewponds combinedincreasedinthesecondyear.
Changesbetweenyearsinnumberofindividualsof eachgroup,and numberofpondsdominatedby each, indicatedthatrotifersandcopepodscolonizedthenew pondsfasterthancladocerans(seealsoFrischGreen,
2007). Thecolonizationratesofthese threegroups in ournewpondswillbecompared inmoredetail elsewhere (Frischetal.,inpreparation).Cladocerans alsotook themosttimetocolonizemuch smaller experimentalpondsinVirginia(JenkinsBuikema,
1998)andhaveoftenbeentheslowestgrouptorecover inacidifiedlakesafterpHhasbeenrestored(Yanetal.,
2004,GrayArnott,2009,butseeKnappSarnelle,
2008).
Highercommunity differentiation orb-diversity wasrecordedinnewpondsinthesecondyear.The
lower b-diversityfoundin2006 mayhavebeen facilitatedbyalackofenvironmentalheterogeneity whenthenewlyexcavated pondswerefirstfilled,and bytheweakness oflocalregulatoryprocesses(e.g. competitionorpredation)inthefirst stagesof communityassembly. Onlyafewspecieswere successfulinestablishingwidespread, largeand dominantpopulationsin2006,constitutinga‘‘core- assemblage’’ commontomostoftheponds.The cyclopoidcopepodMetacyclopsminutus,therotifer Hexarthra cf.fennicaandthecladoceranMoina brachiata were prominent pioneers, and only the latterapproached similarlevelsofabundancein referencesitesandincreased inabundancein2007 (Table3). M.minutusis abletorecolonizetemporary pondswithinhoursofinundation fromdiapausing stagesinthesediment, anditwasdominant in ephemeralrainpoolsformedinthenewpondsin2005 (Frisch& Green,2007).Owingtoitsgreatabundance in2006,thestriking declineintheHexarthrapop- ulationsobservedin2007hadamajorinfluenceon thediversity patternsofthewholezooplankton community.
Inwell-establishedzooplanktoncommunities,var- iationinpredationintensityandhabitatdiversityhave
Table3 Listoftaxafoundinnewponds(N=47)andreferencesites(N=8in2006,N=6in2007) NewpondsReferencesites
April2006April2007April2006April2007
ODTotalabund. ODTotalabund. O D Totalabund. O D Totalabund.
COPEPODS1128155081453226
Juvenilestages
Cyclopoidanauplii / 47 / 13 / 10233 / 33 / 14 / 2252 / 8 / 2 / 652 / 3 / 0 / 101Cyclopoidacopepodids / 47 / 1 / 264 / 34 / 0 / 80 / 8 / 0 / 93 / 5 / 0 / 9
Calanoidanauplii / 38 / 1 / 275 / 45 / 10 / 1954 / 7 / 0 / 58 / 5 / 2 / 70
Calanoidacopepodids / 33 / 0 / 247 / 36 / 5 / 501 / 7 / 0 / 154 / 5 / 0 / 15
Harpacticoidacopepodids / 4 / 0 / 4 / – / – / – / – / – / – / – / – / –
Acanthocyclopscf.robustus / – / – / – / 11 / 0 / 1 / 1 / 0 / 0.05 / 3 / 0 / 3
Metacyclopsminutus / 46 / 0 / 148 / 32 / 0 / 35 / 8 / 0 / 62 / 2 / 0 / 0.10
Metacyclopsplanus / 1 / 0 / 0.05 / 14 / 0 / 4 / 2 / 0 / 0.35 / 4 / 0 / 1
Arctodiaptomuswierzejski / 31 / 0 / 77 / 25 / 0 / 87 / 6 / 1 / 348 / 1 / 0 / 1
Copidodiaptomusnumidicus / – / – / – / – / – / – / 1 / 0 / 0.05 / – / – / –
Mixodiaptomusincrassatus / 22 / 0 / 26 / 5 / 0 / 1 / 5 / 0 / 8 / – / – / –
Neolovenulaalluaudi / 2 / 0 / 1 / 40 / 3 / 594 / 3 / 0 / 76 / 5 / 1 / 26
Nitocralacustris / – / – / – / – / – / – / – / – / – / 1 / 0 / 0.15
Harpacticoidaundet. / 5 / 0 / 6 / – / – / – / – / – / – / – / – / –
Harpacticoidaundet.2 / – / – / – / – / – / – / 1 / 0 / 0.20 / – / – / –
CLADOCERANS4891143176160
Daphniajuveniles / 5 / 0 / 1 / 8 / 0 / 2 / – / – / – / 1 / 0 / 3Alonaazorica / 2 / 0 / 0.20 / 21 / 0 / 18 / 1 / 0 / 1 / 2 / 0 / 1
Alonarectangula / 20 / 0 / 3 / 30 / 0 / 38 / 6 / 0 / 8 / 3 / 0 / 4
Bosminalongirostris / – / – / – / – / – / – / 2 / 0 / 0.20 / – / – / –
Ceriodaphniaquadrangula / 12 / 0 / 122 / 10 / 0 / 8 / 6 / 0 / 43 / – / – / –
Daphniaatkinsoni / 2 / 0 / 0.10 / – / – / – / – / – / – / – / – / –
Daphniamagna / 14 / 0 / 5 / 30 / 2 / 175 / 6 / 1 / 360 / 3 / 1 / 30
Daphniacf.similis / 1 / 0 / 0.05 / – / – / – / – / – / – / 2 / 0 / 11
Dunhevediacrassa / 1 / 0 / 0.05 / 3 / 0 / 1 / – / – / – / 2 / 0 / 1
Macrothrixhirsuticornis / 11 / 0 / 31 / 7 / 0 / 7 / 2 / 0 / 11 / 2 / 0 / 0.30
Megafanestraaurita / – / – / – / – / – / – / – / – / – / 1 / 0 / 0.25
Moinabrachiata / 47 / 0 / 328 / 36 / 12 / 887 / 7 / 4 / 1337 / 4 / 0 / 5
Oxyurellatenuicaudis / – / – / – / 1 / 0 / 0.05 / – / – / – / 1 / 0 / 0.05
Pleuroxusletourneuxi / 1 / 0 / 0.05 / 4 / 0 / 2 / 2 / 0 / 0.25 / – / – / –
Scapholeberisramneri / 1 / 0 / 0.05 / 1 / 0 / 0.05 / – / – / – / 1 / 0 / 2
Simocephalusexspinosus / – / – / – / 5 / 0 / 4 / 1 / 0 / 0.10 / 3 / 0 / 2
ROTIFERS215581041872463
Ascomorphasp. / – / – / – / 1 / 0 / 0.15 / – / – / – / – / – / –
Aplanchnasp. / – / – / – / 2 / 0 / 0.40 / – / – / – / – / – / –
Belloidea / – / – / – / 1 / 0 / 0.05 / – / – / – / 2 / 0 / 42
Brachionusangularis / – / – / – / – / – / – / 2 / 0 / 100 / – / – / –
Brachionusplicatilis / 20 / 2 / 1277 / 2 / 0 / 4 / 1 / 0 / 1 / 1 / 1 / 254
Brachionusquadridentatus / 30 / 0 / 169 / 14 / 0 / 9 / 6 / 0 / 5 / 3 / 0 / 1
Brachionusurceolaris / 1 / 0 / 0.05 / – / – / – / 2 / 0 / 2 / – / – / –
Table3continued
NewpondsReferencesites
April2006April2007April2006April2007
O / D / Totalabund. / O / D / Totalabund. / O / D / Totalabund. / O / D / Totalabund.Brachionusvariabilis / 8 / 0 / 6 / 8 / 0 / 64 / 4 / 0 / 376 / 3 / 0 / 6
Cephalodellagibba / 12 / 0 / 9 / 10 / 0 / 3 / 3 / 0 / 0.50 / 2 / 0 / 2
Cephalodellasp. / 1 / 0 / 3 / 5 / 0 / 3 / – / – / – / – / – / –
Colurellasp. / – / – / – / 2 / 0 / 0.10 / – / – / – / 1 / 0 / 0.20
Colurellauncinata / – / – / – / 2 / 0 / 0.10 / – / – / – / – / – / –
Filinalongiseta / – / – / – / – / – / – / 1 / 0 / 330 / – / – / –
Gastropushyptopus / 1 / 0 / 0.05 / 2 / 0 / 2 / 2 / 0 / 1 / – / – / –
Epiphanessp. / – / – / – / – / – / – / 1 / 0 / 2 / – / – / –
Euchlanissp. / 4 / 0 / 2 / – / – / – / – / – / – / – / – / –
Hexarthracf.fennica / 46 / 30 / 19972 / 15 / 0 / 336 / 3 / 0 / 10 / – / – / –
Keratellaquadrata / 1 / 0 / 8 / 1 / 0 / 0.20 / 2 / 0 / 1 / – / – / –
Keratellatropica / 9 / 0 / 12 / 3 / 0 / 342 / 1 / 0 / 2 / – / – / –
Lecanebulla / – / – / – / 1 / 0 / 0.05 / – / – / – / – / – / –
Lecaneluna / 20 / 0 / 33 / 31 / 0 / 203 / 3 / 0 / 46 / 6 / 1 / 138
Lecanelunaris / – / – / – / 3 / 0 / 0.50 / – / – / – / 1 / 0 / 0.10
Lecanesp. / 18 / 0 / 9 / – / – / – / 1 / 0 / 0.05 / 1 / 0 / 10
Lepadellapatella / 1 / 0 / 0.05 / 1 / 0 / 0.05 / – / – / – / – / – / –
Notholcaacuminata / 2 / 0 / 0.10 / – / – / – / – / – / – / – / – / –
Polyarthra sp. / – / – / – / – / – / – / – / – / – / 1 / 0 / 6
Proalessp.1 / 2 / 0 / 0.10 / 10 / 0 / 5 / 1 / 0 / 0.15 / 1 / 0 / 0.25
Proalessp.2 / 4 / 0 / 55 / 7 / 1 / 68 / – / – / – / 2 / 0 / 1
Testudinellapatina / 9 / 0 / 2 / 9 / 0 / 3 / – / – / – / 1 / 0 / 3
Trichocercasp. / 2 / 0 / 0.50 / – / – / – / – / – / – / – / – / –
Foreachtaxonthefrequencyofoccurrence(O,numberofpondswhereagiventaxawasfound),anddominance(D,numberofponds whereagiventaxawasmoreabundantthananyother),andthetotalabundance(sumofnumberofindividuals/l forallponds)are listed
beenshowntoproducestrongdifferences in communitycomposition, eveninthepresenceof hydrologicalconnections(Cottenieetal.,2001).New Caracolespondswerealreadyvariablein their habitat characteristicsby2007(Table1).Diversificationof aquaticvegetationandassociatedmacroinvertebrate communitiesislikelytoincreasethisvariationinthe future.Predationandcompetitionarelikelytohave importanteffectsonthezooplankton community composition innewponds.Itispossiblethatcom- petition with species that established populations early on delayed colonization by other species presentinnearbysourcepopulations, justasacid- tolerantspeciesestablishedinacidifiedlakesdelay therecoveryofacid-sensitivespeciesafterrestoration
ofnormalpH(Binks etal.,2005;Frostetal.,2006). However, littleisknownabouttheinteractions between thespeciesrecordedinthisstudy.Although fish wereabsentinnewponds,macroinvertebrate predators such as Coleoptera and Hemiptera may havebeenimportant, althoughtheyhavenotbeen studiedin detail to date (butseeRodriguez-Perez etal.,2009fordetailsofCorixidae).Hexarthraspp. populations canbepartlycontrolledbypredationby otherzooplankters (HerzigKoste,1989;Stark- weather, 2005),andtheinitialboominabundanceof Hexarthrain 2006mayhavebeenassociatedwiththe lowinitialabundance andlaterarrivalofcladocerans andcalanoids.AlthoughDaphniaareknowntohave anegativeeffectonrotifers,atleastinlakesystems
Fig.5 Foreachyearand classofwaterbodies:mean valuesofrichnessforthe wholezooplankton community(square)andthe copepod(rhombus), cladoceran(circle)and rotifer(triangle) assemblages,separately. Errorbarsshow95% confidenceintervals.Values sharingthesame letterwere significantlydifferent.No significantdifferenceswere foundin2007betweennew pondsandreferencesites
(Fussmann, 1996),wefoundnocorrelationbetween ponds intheabundance ofDaphniaandofrotifers (resultsnotshown).
Thehighercoverofmacrophytesinnewponds in2007islikelytohavehadanimportantinfluence onthezooplankton communities,andmayhave enhancedtherelativeabundanceof large-bodied(e.g. Daphnia),andalsovegetation-associated(e.g.Alona) cladoceransatthecostofrotifers andcyclopoids. Zooplanktonspeciesrichnessisgenerallypositively relatedtothecoverofsubmergedvegetation(Romo etal.,2004;Declercketal.,2005).Cladoceransare associated withclear,macrophytedominatedshallow ponds,whereasrotifersandcopepodsoftendominate inturbid,plant-freewaters(Burks etal.,2006and referencestherein).Thehigher pHin2007isalso likelytobeduetogreatermacrophytebiomassthat year(CarpenterLodge,1986).
Thetaxonrichness ofrotifersandcopepodsis negativelycorrelatedwithtotalphosphorusinlakes insouthernSpain(Declerck etal.,2005),and phosphorusavailabilitycaninfluence zooplankton biomass(Conde-Porcuna etal.,2002).However, indirecteffectsowingtotheinfluence ofphosphorus concentrationonsubmergedmacrophytesmayhave moreconsequences forzooplankton diversity(Decl- erck et al., 2007). Although reference sites were
generallymoreeutrophic thannewCaracolesponds, thiswasnotassociated withashifttowards higher abundanceofrotifersandcyclopoid copepodsand lowerabundance oflargecladocerans inthemore eutrophic andturbidsites(i.e.inreferencesites),as mightbeexpectedwhencomparing pondsofsimilar age(Cottenieetal.,2001).
In Don˜ana as a whole, 41 copepod taxa, 48 cladoceransand80rotifershavebeenrecordedto date(Arechederraetal.,2006;Fahdetal.,2009),and only25%ofthesetaxawererecorded inthenew ponds. Asimilarpercentagewasfound forthe referencesites.Allthetaxarecorded inthisstudy werealreadycitedintheseearlierstudies.Thevast majorityofcopepodand cladocerantaxafoundinthe newpondsinhabitawiderangeof temporaryhabitats in Don˜ana, but tend to be more frequent in the marshlandthaninduneponds(Fahdetal.,2009).The relativelyhighsalinityinourstudyareaislikelyto limitthenumberofzooplankton speciesableto colonize(Schelletal.,2001;Frischetal.,2006).
Despitethelowdensityofanyremainingeggbank afterpondexcavation,dispersal limitationisunlikely to have been a major factor for the new Don˜ana ponds,owingtotheirproximitytoalargesurface areaofnaturalwetlands. Winddispersalfromnearby sourcesislikelyto havebeenespeciallyimportantfor
smallerpropagules suchasrotifereggs(Vanschoen- winkeletal.,2008). Waterbirdsarelikelytohave beenimportantvectors, especially forcladocerans (Frisch etal.,2007,Brochetetal.,2010),and40bird specieswererecorded inthenewpondsduringthe studyperiod(A.J.Greenunpublished data).Within themajorblocks ofnewponds(Fig.1),hydrological connectionsatpeakflooding arelikelytohave facilitatedthearrivalofnewspecies tosomeponds, although othersinthesameblocks remained unconnected.
After the firstyear, no subsequentincreasesin localspeciesrichness orbetadiversity weredetected forcladocerans innewpondswithapermanent hydroperiodinBelgium(Louetteetal.,2008).This contrasts withourownresults,butthismaybe explainedbythefactthatourfirst samplingwas carriedout4monthsafternewpondswerefirstfilled, whereasthe‘‘first year’’intheBelgianstudy includingsamples upto15monthsafterpondfilling. Indeed, astrongincreaseincladoceranspecies richnesswasrecordedbetweenmonths4and14in theBelgianponds. Anaverageof4.2cladoceran speciescolonizedwithin15months(LouetteDe Meester,2005).
Thesefindings areconsistentwithourownin suggestingthatrestorationofzooplankton communi- tiescanbeachievedinponds inashorttimeperiod, wellbelowthe10–20yearsgenerallyconsideredas necessaryin lakes(Donaldetal.,2001,Dodsonetal.,
2007).Thisislikelytobelargelyaconsequenceof thedifferenceinvolumeoftheseecosystems, result- ingintimelagsandalleeeffects thatcaninhibitthe recoveryofzooplanktoninlakes(KnappSarnelle,
2008).InWisconsinwetlandsvaryinginsizefrom
0.4 to 4.5ha (i.e. similar to our new ponds of
0.2–2.9ha),agriculturaluseloweredthenumberof speciesof crustaceanzooplanktonpresent(Dodson& Lillie,2001),but6years afterrestorationtheir zooplankton communities closely resembled those ofreferencesites.
Ourstudyillustratesthevalueofzooplanktonas indicatorsofsuccessful restorationofaquaticcom- munitiesinMediterraneanwetlands,andunderlines thevalueofwetlandrestorationtomitigateforhabitat lossintheMediterranean region.Moreresearchis required infuturetoestablishthelong-termchanges inzooplankton inthenewpondsandhowthey respond to future development of vegetation and
changesinnutrientloading,salinity,etc.,aswellasto theannual variationinprecipitationand expected climatechange(Mossetal.,2009).
Acknowledgements WethankRaquelOrtells,SarahRousseaux, Ernesto Garc´ıaandPieterVanormelingenforassistance withfield sampling, andIsabelCarribero fortechnicalassistance in laboratory analyses.FernandoPaciospreparedthemapofthe studyarea.Financialsupport forthisresearchwasprovided by theConsejer´ıadeInnovacio´n,CienciayEmpresa,Juntade Andaluc´ıa(P06-RNM-02431),theSpanishMinisteriodeMedio AmbienteDon˜ana 2005restorationproject anda European ScienceFoundationEurocoresproject(BIOPOOL).
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