Assessing the ecological integrity of endorheic wetlands, with focus on Mediterranean temporary ponds

(1)

EcologicalIndicators54(2015)1–11

ContentslistsavailableatScienceDirect

Ecological Indicators

jou rn al h om ep a g e :w w w . e l s e v i e r . c o m / l o c a t e / e c o l i n d

Review

Assessing the ecological integrity of endorheic wetlands, with focus on Mediterranean temporary ponds

Maarten Van den Broeck

^a,c,∗

, Aline Waterkeyn

^a,b

, Laila Rhazi

^c

, Patrick Grillas

^b

, Luc Brendonck

^a

aLaboratoryofAquaticEcology,EvolutionandConservation,UniversityofLeuven,CharlesDeberiotstraat32,Leuven3000,Belgium

bTourduValatResearchCentreforMediterraneanWetlands,LeSambuc,Arles13200,France

cLaboratoiredeBotanique,MycologieetEnvironnement,UniversitéMohammedV,FacultédesSciencesdeRabat,4AvenueIbnBattouta,RabatBP1014, RP,Morocco

a r t i c l e i n f o

Articlehistory:

Received2October2014

Receivedinrevisedform6February2015 Accepted10February2015

Keywords:

Biologicalindicators Temporarywetlands Ecologicalassessment WFD

a b s t r a c t

EUcountriesarerequiredtoperformanassessmentofallfreshwaterhabitatslargerthan50haby2015 tomeettherequirementssetbytheWaterFrameworkDirective(2000).Toachievethis,anarrayof indicatorsandmultimetricindiceshasbeendevelopedtomonitorEuropeanwaters.Ingeneral,these indicatorsaredevelopedforlargewaterbodies,whiletheyarestilllargelylackingforsmallerwetlands.

Thisisincontrastwiththeconservationvalue,valuableecosystemservicesandtheoftenuniquebio- diversityofthesesystems,andthefactthatlikelarge(>50ha)wetlandstheyarealsocoveredbythe RamsarConvention.In(semi)aridregions,suchastheMediterraneanbasin,smallwaterbodiesareoften ofatemporarynature,areabundantandprovideanimportantsourceofwaterforthelocalpeople,their livestockandagriculture.Thequantityandqualityoftemporarywetlandsare,however,decreasingatan alarmingrateworldwide.Althoughsomemonitoringtechniqueswererecentlyproposed,thereisstill anurgentneedforaconsistentpolicyandauserfriendlysetofmonitoringtoolsfortemporarywetlands thatcanbeappliedindifferentregions.Inthefollowingreview,wepresentawholerangeofindicators usedtomonitordifferenttypesoffreshwaterhabitats,anddiscusshowsomeofthesemethodscould beappliedtotemporarywetlands.Finally,weformulatesomerecommendationsfortemporarywetland monitoringandconservation.

Contents

1. Introduction... 2

2. Overviewofsuitableindicators... 3

2.1. Abioticindicators... 3

2.2. Bioticindicators... 3

2.2.1. Vertebrates... 3

2.2.2. Macroinvertebrates... 3

2.2.3. Zooplankton... 6

2.2.4. Macrophytes... 6

2.2.5. Phytoplankton... 7

2.2.6. Multimetricindices(MMI)... 7

2.2.7. Modelingapproaches... 7

3. Discussion... 7

3.1. Temporalandspatialregionalvariabilityintemporaryponds... 7

∗Correspondingauthorat:KULeuven,DepartmentofBiology,CharlesDeberiotstraat32,Box2439,3000Leuven,Belgium.Tel.:+3216373750.

E-mailaddress:Maarten.VandenBroeck@bio.kuleuven.be(M.VandenBroeck).

(2)

2 M.VandenBroecketal./EcologicalIndicators54(2015)1–11

3.2. Monitoringguidelinesfortemporarywetlands... 8

3.2.1. Dryphase... 8

3.2.2. Aquaticphase... 8

3.3. Concludingremarks... 9

Acknowledgments... 9

References... 9

1. Introduction

Wetlandsareoneofthemostbiologicallydiverseecosystemson earth(MitschandGosselink,2007).Theyusuallyhouseadiverse faunaandflora,includingmanyrareandthreatenedspecies(Keddy, 2010).Wetlandsalsoperformmanyimportantecosystemservices, includingwaterstorage,carbonsequestration,floodreduction,sed- imenttrappingandreducing theeffectsofpesticides andother typesofpollutionthroughfiltration(Costanzaetal.,1997;Joyce, 2012).Althoughwetlandsonlycover6%ofthetotallandsurface (NaimanandDécamps,1997),thevalueoftheseareasisestimated torangebetween49billionto3.4trillioneurosperyear,measured asthebudgetneedediftheseservicesweretobereplaced(Schuyt andBrander,2004).AccordingtotheRamsarConvention(Ramsar, 2013),wetlandsincludemarshes,peatlandandfens,ditches,lakes, ponds,lagoons,floodplains,estuariesand coastalzones(includ- ingcoralreefs)notdeeperthansixmeters(atlowtideincaseof tidalsystems).Theyarecharacterizedby:(i)awatersaturatedsoil, (ii)adifferentsoilcompositioncomparedtothesurroundingnon- wetlandareasand(iii)specificallyadaptedvegetationthattolerates highwaterlevelseitherpermanentlyortemporarily,dependingon thetypeofwetland(Maltbyetal.,2009).

Ingeneral,highpressureduetohumanpopulationgrowthoften resultsinthedisappearanceofnaturallandscapecomponents,such asnaturalwaterbodiesandriparianzones.Globally,awetlandloss of50%inthelast centuryiscommonlyreported(Finlaysonand D’cruz,2005), and differentmodelspredicta lossrangingfrom 11%to62%by2080forcoastalwetlands alone(Nicholls,2004).

Togetherwithintensiﬁedagriculture,anthropogenicpressurehas also led to diffuse pollution and eutrophication in freshwater ecosystems(Arheimeretal.,2005).Thislossanddegradationof wetlandsingeneralandtheirecosystemservicesisfurtheraccel- eratedbyclimatechangeandintroductions ofinvasive species.

Despite theurgent need of protection of wetlands, monitoring andconservationareoftenhamperedbysometimesinconsistent andcontradictoryinternationalagreementsandnationalpolicies (Turner et al., 2010), which makes their ecological assessment difﬁculttoachieve. Even thoughthe socio-economicvalue and ecologicalimportanceof wetlandsystemshaswidely (butonly recently)beenaccepted,particularlyinthesubtropics,norecovery hasyetbeenobserved(Prigentetal.,2012).

TheWaterFrameworkDirective(WFD)(Directive2000/60/EC) commitsEuropeanUnionmemberstatestoachievegoodqualita- tiveandquantitativestatusofall(groundandsurface)waterbodies by2015accordingtoasetofstandardcriteria.Inordertoassess thecurrentstatus ofEuropeansurfacewaters andmonitorany changesaftermanagementpracticesareimplemented,awidearray ofindicatorsweredeveloped,notonlybasedonstandardchemi- calparameters,butalsoonbiologicalcharacteristics,focusingon macrophytes,ﬁsh,phytoplanktonandbenthicmacroinvertebrates (Soliminietal.,2009).Manyindicatorshavebeendevelopedfor differenttypesofaquaticecosystemsrangingfromsmallstreams tolargelakesasreviewedinBirdandDay(2010)andBirketal.

(2012).However,theWFDmonitoringprogramsdonotincorpo- rateassessment techniquesfor temporarywetlands. Infact,the WFDcurrentlyexcludesmosttemporarysystems,sincemanyof themaresmallerthanthestatedsizethresholdof50ha.Onthe otherhand,theNatura2000NetworkandtheRamsarConvention

dohaveaspecialresolutionontemporarywetlands(Ruiz(2008) andRamsarResolutionVIII.33,respectively)thatsuggeststheneed formonitoringprogramsbasedonbiologicalindicatorstoprotect andmanagetemporarywetlands.

In arid and semi-arid regions, temporary waters are often very abundant and are an important water source (Brendonck andWilliams,2000;Williams,2006;Bouahimetal.,2011).They areusuallydefinedaswetlandsthatoccurinendorheic depres- sions,characterizedbyalternatingdryandwetphases,wherethe wetphase is sufficientlylongtoestablish thespecificsoil con- ditionsand floral and faunal communities of ephemeral ponds (Williams,2006).Theyoftenhousediverseplantandanimalcom- munities (Williams, 1997; Blaustein and Schwartz, 2001) and contributetremendouslytoregional(gamma)biodiversity(Gibbs, 2000;Nicoletetal.,2004;Williamsetal.,2004),sometimeseven morethanlargewaterbodies(Biggsetal.,2014).Theyoffer(temporary)housingtobothgeneral(opportunistic)speciesaswellas tounique(temporarypondspecific)speciesthatareadaptedto livingunder time stressand extremeenvironmentalconditions (Grillasetal.,2004).Unfortunately,temporarywetlandsareoften neglectedanddisappearatanalarmingrate,withpercentageloss duringthelastcenturyrangingfrom60%to97%indifferentparts oftheworld(BrendonckandWilliams,2000;Nicoletetal.,2004;

Rhazietal.,2012).Duetotheirsmallsizeandshallowness,these habitatsarepoorlybufferedandeasilydestructedordegradedby humanactivities,suchasurbanization,agricultureandpollution (Rhazietal.,2012).Additionally,climatechangeisexpectedtohave amuchgreaterimpactonthesesmallwatervolumescomparedto largerlakes(Parmesan,2006).Therefore,vigilantmonitoringand conservationofthesesystemsiscrucial.Ontheotherhand,climate changecouldalsoincreasethenumberofhabitatsbytransforming currentlyperennialsystemsintotemporaryones.

Mediterraneantemporarypondsareapeculiartypeoftempo- rarywetlands,whichmainlyoccuraroundtheMediterraneanbasin insouthernEuropeandNorth-Africa,butalsoinotherregionsexpe- riencingaMediterraneanclimate(i.e.mildandrainywinters,hot anddrysummers),suchasthesouthwesterncoastalregionofSouth Africa, South-WestAustralia, California and Chile(Grillas etal., 2010).TheMediterranean temporaryponds insouthern Europe areincludedas aEU PriorityHabitat undertheauspicesofthe HabitatsDirective(Naturacode3170,92/43/CEE,21May1992).

Thesepondsharborseveralrareorthreatenedspeciesofplants, amphibiansandinvertebrateslistedoninternationalconventions (HabitatsDirective,theBernConventionandtheIUCNRedList) (Grillasetal.,2004).TheRamsarConventionisalsoimplemented intheMediterraneanWetlandsStrategy,aimedat“stoppingand reversingthelossanddegradationofMediterraneanwetlandsas acontributiontotheconservationofbiodiversityandtosustain- abledevelopmentintheregion”(Ramsar,2013).However,lackof politicalrecognitionofsmallwaterbodiesasanentityandvitalpart ofthewaterenvironmentremainsunacceptablyhighthroughout Europe(Oertlietal.,2005b).Currently,effortsaremadetoempha- sizetheneedtoprotectandincludesmall(temporary)watersinthe WFD,suchasthe“workshopontheprotectionandmanagementof smallwaterbodies”whichtookplaceinNovember2013andwas organizedbytheEuropeanEnvironmentalBureau,inco-operation withtheEuropeanCommission,theLithuanianPresidencyandthe FreshwaterHabitatsTrust(Biggsetal.,2014).

(3)

M.VandenBroecketal./EcologicalIndicators54(2015)1–11 3

In this paper, we do not aim at presenting an exhaustive overviewofallexistingindicatorsforwetlandsthatarecurrently usedoravailable.Instead,weaimtocriticallyreview examples ofdifferentindicatorsthatweredevelopedtoassesstheecolog- icalqualityofendorheicwetlands ingeneralandevaluatetheir usefulness for temporary wetlands more specifically. Although theseindicatorscannotsimplybeextended,webelievethatthey are a good starting point. Using thorough ecological research, theyshouldthenbemodifiedandcalibratedtoberepresentative for temporaryaquaticsystems. We also reviewnovel indicator approachesbasedspecificallyontheecologyoftemporarywet- lands.

2. Overviewofsuitableindicators

Niemi and Mcdonald (2004) deﬁne ecological indicators as componentsof structural,compositional, and landscape related processesthatareusedtoquantifyhumanimpactonecosystems.

Theseindicatorsmaybeofachemical,physicalorbiologicalnature.

Sinceecologicalindicatorsareessentialcomponentsofthewetland ecosystem,understandingtheroletheyplayintheecosystemis vital(Innisetal.,2000).Bycorrelatinggroupsofbioticvariables, suchasspecies richnessand lifehistorytraits,withabioticfac- tors,suchashydrology,oxygenconcentration,salinity,nutrient andpollutantlevels,theindicatorvalueofsuchbioticfactorscanbe assessed.Traditionally,onlyabioticindicatorssuchaswaterchem- istrywereusedtoassessanthropogenicdisturbance.Lateron,biotic indicatorswerepreferredsincetheyintegrateoverallwaterand habitatqualityandthereforedocumenthowepisodicandcumu- lativedisturbancesimpacttheecologicalintegrityofanecosystem (Burtonetal.,1999).Nowadays,modernstatisticalapproachesare usedtoconstructindicatorsfordifferenttypesofhabitats.Such a statistical approach is based oncalculating distance matrices (e.g.Bray–Curtisdistances,Euclidiandistances)from(a)bioticvari- ablesbetweensamplingsites.Then,byusingManteltests(Mantel, 1967)orothermatrixcorrelationtests,communityconcordance canbeassessedbetweenthesematrices,asdescribedbyforexam- plePadialetal.(2012),toprovideinformationonhowcommunities arecorrelatedwiththemeasuredenvironmentalvariables.

Morethan75studieswerereviewedtoselectindicatorsofvar- iousfreshwaterhabitats.Table1summarizesdifferentindicator groups,includingsomespeciﬁcexamples,theiradvantages and disadvantages,andindicatesforwhichtypeofhabitatandanthro- pogenicdisturbance/pressuretheywereoriginallydeveloped.

2.1. Abioticindicators

Abioticindicatorsarespecificsoilorwaterconditionsthatcan beusedtoquantifythelevelofanthropogenicdisturbanceimpact- ingthewetlandecosystem.Theycanbedividedintophysicaland chemicalindicators.Mostphysicalindicators(e.g.soilgranulom- etry,%of organicmatterandsediment redox potential)canbe impactedbylanduseandchangesinthehydrologyofthesystem suchasdrainage.Hydrologicalchangeshaveanimpactonthedura- tionofflooding,maximumdepthandnumberoffloodingevents peryearoftemporarywetlands.Chemicalindicators(e.g.pH,con- centrationsofions,dissolvedgases,pollutantsandnutrients)are potentiallyusefulfordetectingandquantifyingthelevelofenvi- ronmentalstressimpactingtheecosystem(Feldetal.,2009).For example,measuringthenutrientconcentrations(e.g.totalnitrogen (tN),totalphosphorus(tP),ammonium(NH₄⁺),orthophosphates (PO43−)andnitrates/nitrites(NOx−))inthesoilorwatercolumn cangiveanindicationofthelevelofeutrophication,whilethecon- centrationofionsmayreflectsecondarysalinizationandpHvalues giveanideaofthelevelofacidification.Specificallyforwetlands

andshallowlakeswithﬂuctuatingwaterlevels,thecorrectproduc- tivityassessmentisimportantfordistinguishingbetweennatural andanthropogeniceutrophication(Elkiathietal.,2013).Forexam- ple,Golterman(2004)describedaccurateP-fractionationmethods tomeasuretheP-bindingcapacityofwetlandsedimentsasanesti- mationofeutrophication(asthisrepresentstheP-bioavailability forprimaryproducers).Toassessthedegreeoforganicpollution, chemicalandbiologicaloxygendemand(CODandBOD)testscan beusedsincetheyareanindirectmeasureoftheamountoforganic componentsthatcanbebrokendown(i.e.oxidized,biologicallyor chemically)byaerobicorganismsinthewatercolumn(Kadlecand Wallace,2008).

2.2. Bioticindicators

Biotic indicators or bio-indicators can involve single indicator species or entire assemblages/communities whose pres- ence/absence, abundance or diversity patterns can provide information about ecological changes and health of a system (AngermeierandDavideanu,2004;CousinsandLindborg,2004).

Animalindicatorsforaquaticsystemsmainlyfocusonmacroin- vertebrates,since theyarewellstudiedandhave a widespread distribution (Resh, 2008). Many bio-indicators are also based on macrophytes and phytoplankton (Resh, 2008; Bornette and Puijalon,2011).Below,weevaluatethesuitabilityofdifferentani- malandplantgroupsthatarepresentintemporarypondsasbiotic indicatorsForeachgroup,thisassessmentisfollowedbyapresen- tationofsomespeciﬁcexamples(seealsoTable1),makinguseof speciescomposition,communitystructureanddiversityofassem- blages/communities,oronfunctionaltraitsofselectedspecies.

2.2.1. Vertebrates

Althoughfisharethemostcommonvertebrategroupusedas biotic indicators in aquatic environments (e.g. indices of biotic integrity,physiological/behavioraltraits,etc.(AdamusandBrandt, 1990)),theyarelackingin mosttemporarywatersandwillnot furtherbediscussed.Similarformammals,althoughrelativelysim- plytoidentify,theirpresenceishighlyvariableandisaffectedby migration(CroonquistandBrooks,1991).Foramphibians,arela- tivelyeasywayofquantifyingtheirabundances(especiallyAnura) hasbeendevelopedviatheircallintensity,asusedintheWiscon- sinIndex(WI)(Balcombeetal.,2005;Paloskietal.,2014).Although itisnotalwayspossibletoquantifyexactnumbersofindividuals, thismethodischeap,relativelyfastandnon-invasive.Rarestud- ieswithwaterfowlhaveshownsomepotentialfortheiruseasa bioindicator,withcontrastingbirdcommunitiesinpristinehabi- tatscomparedtoheavilyimpactedhabitats,bothonalocaland regionalscale(AmatandGreen,2010).Birdspeciescomposition anddiversityingeneralcanthereforemainlyactasanindicatorof landusealteration,habitatfragmentation,andotherhumaninflu- ences.Whilewaterfowlcaneasilybeidentified,haveahighsocietal valueandawell-knownlifehistory,theyarehighlymobileandare oftenmoreaffectedbyhabitatcharacteristics(e.g.watersurface, vegetation)andseasonthanbywaterquality.

2.2.2. Macroinvertebrates

Macroinvertebratesarethemostcommonlyusedorganismsas aquaticbioindicatorsbecauseoftheirwell-knownlifehistoryand ecology(RosenbergandResh,1993;Innisetal.,2000).Abundance andcompositionofmacroinvertebrateshavebeenusedvariablyto developsometimescountryspeciﬁcbiotic indices.Invertebrates areusually highlyadaptedtoa particularenvironment, making themsusceptibletostressorssuchaslackofoxygenorhighsalinity (Keddy,2010),andarethereforeintegratedintheWFD(ascompo- sitionandabundanceofbenthicinvertebrates).Oertlietal.(2005a) developedarelativelycost-efﬁcientmethodforassessingthestatus

(4)

4M.VandenBroecketal./EcologicalIndicators54(2015)1–11

Table1

Overviewofindicatorsusedforsurfacewatermonitoring,withemphasisonlenticwetlandsystems.Thedifferentindicatorgroupsarepresentedwithsomespeciﬁcexamples,alsomentioningtheirindicatorvalueforthewetland typeforwhichtheyweredeveloped,theiradvantagesanddisadvantagesandtherespectivereference(s).Bioticintegrity:deﬁnesthegeneralstateoftheecosystemfunctioning.

Indicatorgroup Indicator Indicativeof Wetlandtype Advantages Disadvantages References

Abioticindicators Concentrationsof nutrientsandions

-Eutrophication -Salinization -Acidiﬁcation

Allwetlands Easytomeasure Snapshotofcurrentstate Yangetal.(2008)

COD/BOD Organicpollution Allwetlands CODfasterthanBOD CODnodifferentiation

betweenbiological active/inactivesubstances

KadlecandWallace(2008)

Sediment P-bindingcapacity

Eutrophication Allwetlands Highsensitivityandaccuracy towardsotherP-fractionation methods

Golterman(2004)

Vertebrates WisconsinIndex (WI),frogcall intensity

Bioticintegrity Allwetlands -Cheapandrelativelyfast Non-invasive

-OnlyforAnura -Notalwayspossibleto estimateabsolutenumbers

Paloskietal.(2014)

Diversityof waterfowl

-Landcoveralteration -Habitatfragmentation

Allwetlands -Highsocietalvalue -Well-knownlifehistoryand identiﬁcation

-Moreaffectedbysiteand seasonthanbywaterquality -Mobilityandmigrations

BeckandHatch(2009)

Macroinvertebrates PLOCH -Eutrophication -Organicpollution

Ponds Relativelyeconomical Oertlietal.(2005a)

Diversityofhigher taxaofColeoptera

Bioticintegrity Mediterranean

ponds

-Fast

-Nodetailedidentiﬁcation needed

Sánchez-Fernándezetal.

(2006)

MIdiversity -Humandisturbance -Phosphorousconcentration -Pesticides

-Eutrophication

Mediterranean ponds

Lessdetailedidentiﬁcation required(genuslevel)

Interannualvariationnot considered

Trigaletal.(2007,2009)

Coleoptera diversity

-Magnesiumconcentration -Conductivity

-Turbidity

Temporary wetlands

-Cheap Limitedperiodperyearwhere

samplingcanoccur

Gutiérrez-Estradaand Bilton(2010)

Zooplankton ACCO(aspartof QAELS)

-Nutrientinput -Salinity -Organicpollution

Mediterranean wetlands

-Occuringreatnumbers -Easilycaptured -Highsensitivitytowards disturbances

-Knowninteractionswith macrophytesand phytoplankton-Limited mobility

-Lowperceivedsocietalvalue -Seasonal/dailyfluctuations -Difficultidentification

Boixetal.(2005)

-Hatchingofeggs -Diversityof unhatchedeggs

Physicalandchemical disturbances

Temporaryand permanent wetlands

-Easyandcostefﬁcient sampling,possibleduring wholeyear

-Deeperlayerswitheggs availabletoreﬂectpast changes

Difﬁcultieswithdetermining diversityofeggs

(hatching/identiﬁcation)

AngelerandGarcía(2005), Vandekerkhoveetal.

(2005)

Macrophytes WMI Eutrophication

Organicpollution

Lakes -Immobile

-Wellknownidentiﬁcation andlifehistory

-Susceptibletostress

-Sometimeslongrecovery timeafterdisturbance -Variablesuccessionpatterns

BornetteandPuijalon (2011),Croftand Chow-Fraser(2007)

Multispectral remotesensing

Physicalandchemical disturbances

Allwetlands Largeareasatonce Reﬂectionsfromdifferent vegetationspeciesaredifﬁcult todistinguish

Adametal.(2010)

(5)

M.VandenBroecketal./EcologicalIndicators54(2015)1–115 Table1(Continued)

Indicatorgroup Indicator Indicativeof Wetlandtype Advantages Disadvantages References

Phytoplankton DIWC -Pesticides

-Sedimentation -Habitatalteration

-Marshes -Estuaries

-Longhistoryofuse -Cosmopolitandistribution -Lowsamplingeffort

Lowperceivedsocialvalue Resh(2008)

Multimetric indices(MMI)

TrophicStateIndex (TSI)

Eutrophication Lakes -Relativelyeasytomeasure

-Canbeappliedforwhole rangeofstandingwaters

Snapshotofcurrentstate Carlson(1977)

QAELS -Nutrientinput

-Salinity -Organicpollution

Mediterranean wetlands

SeeACCO SeeACCO Boixetal.(2005)

WZI BioticIntegrity Lakes -Occuringreatnumbers

-Easilycaptured -Highsensitivitytowards disturbances

-Knowninteractionswith macrophytesand phytoplankton-Limited mobility

-Lowperceivedsocietalvalue -Seasonal/dailyfluctuations -Difficultidentification

LougheedandChow-Fraser (2002)

MMIformacroin- vertebrates

Eutrophication Arableditches -Lifehistoriesandecology oftenwellunderstood -Oftenspecializedand sensitivetowardsdisturbances -Widespreadandabundant -Limitedmobility

-Lowperceivedsocietalvalue -Communitiesmaybe predatedselectivelybybirdsor ﬁsh

Verdonschotetal.(2012)

PSYM Bioticintegrity Pondsand

canals

-Rapidassessment -Nodetailedidentiﬁcation neededformacroinvertebrates

OnlydevelopedforUK Biggsetal.(2000)

LEMN Eutrophication Shallowcoastal

lagoons

-Changesinstructural hydrologicpatternsareoften theunderlyingcausefor changesinbiological correlations

-Sometimeslong-termdata available

Extensivemeasurements required

Souchuetal.(2000), Brehmeretal.(2011)

Predictivemodeling RIVPACS Bioticintegrity (UK)rivers -O/Eratiosareeasyto interpret

-Standardizedstatistical modeling

-SometimesnoReference conditionsleft

-Hastobedevelopedforeach region

Wrightetal.(1998)

(6)

ofSwissponds,calledPLOCH(‘Plans(PL)d’eau(O)suisses(CH)’).

Thequalitystatusisallocatedbasedonthepresence/absenceof aquaticGastropodaand Coleopteraand theabundanceofadult Odonata(inadditiontoquadratbasedpresence/absenceofmacro- phytes,andabundanceofadultAmphibia).Thenumberofgenera orevenfamiliesofaquaticColeoptera(whichsparestheeffortof detailedspeciesidentiﬁcations)wereshowntobeusefulforfast, cost-efﬁcientmonitoringoftheoverallqualityofSouthernSpan- ishlenticfreshwaterecosystems(Sánchez-Fernándezetal.,2006).

TheuseofmacroinvertebratesasbioindicatorsforSpanishwet- landsand Mediterraneanponds ingeneralhasbeen studiedas well.Trigaletal.(2007),forexample,foundthat thepondcon- ditionindex (toassess humaninduceddisturbance) alongwith pesticidesandphosphorousconcentration,werethebestpredic- torsofmacroinvertebratecommunities.Inafollow-upstudy,an indexwascreatedforthesamepondsusing differentmacroin- vertebratediversitycharacteristicsthatchangedwithincreasing levelsofeutrophication(Trigaletal.,2009).Also,fortemporary pondsGutiérrez-EstradaandBilton(2010)showedthatthediver- sityofColeopterawashighlycorrelatedwithdepth,conductivity, turbidityandmagnesiumconcentration.Anotherexampleisthe RICindex(‘richnessofinsectsandcrustaceans),developedbyBoix etal.(2005).Thismeasurementof taxonrichnessis thesumof thenumberofcrustacean,adultColeopteraandHeteropteragen- era,plusthenumberofimmatureinsectsandispartoftheQAELS index(Catalanfor‘waterqualityoflenticshallowenvironments’).

2.2.3. Zooplankton

Althoughtheyare notincludedin theWFD, thereare many characteristicsofzooplankton(microcrustaceans)thatmakethem usefulasbioindicatorsespeciallyinlenticwaterbodies(Lougheed andChow-Fraser,2002;Boixetal.,2005):(i)theyoccuringreat numbersandareeasilycaptured,(ii)theircommunitystructure variesaccordingtotrophicstatedifferencesandrespondsquickly tochangesintheenvironment,(iii)trophicinteractionsbetween microcrustaceansandphytoplanktonaswellasmacrophytesare wellknownand(iv)theyhaveahightaxonomicresolutionallowing verydetailedecologicalassessments.Incaseofproblemstoiden- tifyallgroupsdowntospecieslevel,evenamixed-taxonresolution canbeappliedtoobtainacceptableresultsinamorecost-efﬁcient way.ThisisillustratedbytheACCOindex,aspartoftheQAELS- indexforMediterraneanwetlands(Boixetal.,2005).Thisindex isbasedontherelativeabundanceofzooplanktongroups(ACCO:

AbundanceofCladocera,CopepodaandOstracoda),andassesses thetaxonsensitivitytowaterquality.Nevertheless,zooplanktonas anindicatorgrouprequireshighdeterminationskillsandusually hasalowperceivedsocietalvalue.Moreover,seasonalorevendaily ﬂuctuationscanoccurmakingthetimingofsamplingtheactive communitiesanimportantfactor.

Tosurviveperiodicunsuitableconditions(suchasdrought,pre- dation,lowtemperaturesoroxygenlevels),zooplanktonspecies producerestingeggsthataccumulateasrestingeggbanksinthe soiland from which theyrecolonize thehabitat when suitable conditionsrestore(BrendonckandDeMeester,2003;Angelerand García,2005).TheconceptualstudybyAngelerandGarcía(2005) suggeststhattheprocessofhatchingfromtheeggbankscanbe disturbedbybothphysicalandchemicalstressorsandmaythere- forebeusedasanindicatorforanthropogenicstress.Thisallows monitoringtheecologicalintegrityofsystemswhenitisdifﬁcult tosampletheactivecommunities.Itcanalsobeusedtocomple- mentthesnapshotsamplingofactivecommunitiesastheeggbank integratestemporalvariationincommunitydynamics.Sediment samplingcaneasily bedoneyear-round, even whenponds are dry.Deepersedimentlayerscanevenbesampled(usingasedi- mentcore)toreconstructpastchangesonthebasisofbiological remainsand liferestingeggsarchivedin thesediment(Cousyn

etal.,2001;WhitmoreandRiedinger-Whitmore,2014).Astudy byVandekerkhoveetal.(2004)showedthatitispossibletoesti- matethebiodiversityofcladoceransinshallowlakesbydirectly identifyingtheephippialeggsusingmorphologicalcharacteristics.

Asaresult,onlyasinglesamplingeffortisrequiredandsediment samplescanbeprocessedquicklyaftercollection.Identiﬁcationof restingstagesisnotyetstudieddowntospecieslevelinalltaxa,so adequatedeterminationkeysarerequired(Vandekerkhoveetal., 2004).

2.2.4. Macrophytes

Mostexamplesofstudiesinwhichplantcommunitiesareused toassess ecologicalquality ofa habitatconcern terrestrialsys- tems(Bobbinketal.,2010).However,macrophytesalsohavean importantindicatorvalue inaquaticenvironments due totheir well-knownlifehistoriesandsuccessionpattern,susceptibilityto stress,immobilityandtherelativeeaseofidentiﬁcation(Bornette andPuijalon,2011).Aquaticplantsresponddirectly(throughcom- petitionforlightandnutrients)orindirectly(throughfoodweb interactions)tochangesinwaterquality.Especiallyeutrophica- tionisamajorstressorforaquaticbiodiversity,andparticularly formacrophytes,asshownbyRossetetal.(2014).Bornetteand Puijalon(2011)reviewedthedifferentresponsestoabioticfactors ofaquaticplantsinfreshwaterhabitats.Thisreviewshowsthat functionaltraits,dispersalanddynamicsofaquaticplantcommu- nitiesarenotonlyimpactedbyeutrophication,butalsobyother environmentalparameters,includinglight,temperature,substrate characteristicsandwatermovements.Astudyof110boreallakes ofFinland(Alahuhtaet al.,2013)shows that submergedplants aremoredependentonwatertransparency,nutrientconcentration andcarboninthewaterthantheemergentvegetation.Incontrast, emergingmacrophytesareonlyinﬂuencedbythelowavailabil- ityoflightintheearlystageofdevelopmentandcanusecarbon dioxidefromtheair.Theseemergingplantscanalsoobtainnutri- entsfrom thesediment andare thereforeless related towater quality. Macrophyte community composition and abundanceis alsopartoftheindicatorsintegratedintheWFD(Dudleyetal., 2013).It is alsogenerallyaccepted thatthere isa positive cor- relationbetweenthediversityandcomplexityofvegetationand diversityofvegetationdependentanimaltaxa(Nicoletetal.,2004).

CroftandChow-Fraser(2007)developedaWetlandMacrophyte Index(WMI)fortheGreatLakestoinfertheecologicalcondition ofthewetlandsbasedonpresence/absenceofemergentandsub- mergedmacrophytespecies.Amacrophyte-basednutrientindex forSwisspondswasdevelopedbySagerandLachavanne(2010), wherebytheecologicalresponsetototalphosphorouswasmea- suredusingindicatorvaluesandspeciescover.Alsointemporary pondsin southwestPortugal, effortshavebeenmade todistin- guishdifferentpondtypesbasedonpresence/absenceofselected indicatorplantspecies,whichhelpsdecisionmakersinapracti- calwaywithassessingtemporarypondstatus(Pinto-Cruzetal., 2011).Similarly,intemporarypondsonbothsidesoftheStraitof Gibraltar(IberianPeninsulaandMorocco),theplantcommunity structureisrelatedtonutrientloading,temperatureandprecipi- tation(Lumbrerasetal.,2012).Lastly,therichnessandabundance ofrareandtemporarypondspeciﬁcspeciesareagoodindicator ofchemicalandphysicaldisturbancesintemporaryponds(Rhazi etal.,2001b;Bouahimetal.,2014).Rareandtemporarypondspe- ciﬁcspeciesarenottolerantofdisturbances,impactingnegatively theirrichnessandabundance.

Submerged and emergent macrophytes in wetlands can be mappedbyremotesensingtechnology(Adametal.,2010;Dekker andHestir,2012).Basedontheirspectralsignature,macrophyte cover(bothsubmergedandemergentvegetation)andwaterqual- ity variables such as chlorophyll a, cyano-phycocyanin levels (reﬂectingthepresenceof algalblooms)and suspendedmatter

(7)

canbeestimated.Althoughfreeandmultispectralimageryfrom Landsatarefrequentlyusedforlargewaterbodies,duetoitscoarse (30m)resolution,itis notsuitableforsmallsystems(DeRoeck et al.,2008).However, highmultispectral imagery (e.g.Ikonos, Worldview-2andRapidEye),isnowcommerciallyavailable(spa- tialresolution2–5m)andcanbeusedforthispurpose(Dekkerand Hestir,2012).

2.2.5. Phytoplankton

Phytoplankton (such as diatoms and cyanobacteria) have a longhistoryasecologicalindicators,beingcharacterizedbyacos- mopolitandistribution,shortgenerationtimeandlowsampling effort(Resh,2008).Theyarethereforealsoincludedasanindi- catorgroupintheWFD,wherethequalityscoreisbasedonthe composition,abundanceandbiomassofphytoplankton.Thecom- positionandtotalbiomassofalgalspeciesinaquaticsystemsserves indeedasanimportantmetricfororganicpollutionandnutrient loading,suchasnitrogenandphosphorus(Brucetetal.,2013).Dif- ferentanalyticalmethodsexist,suchastheinsitumeasurement ofphycocyanin(characteristicpigmentofcyanobacteria),analyz- ingthemorphologicalvariabilityofphytoplanktontoassessthe trophicstateoflakes(Naselli-Flores,2013)orthemoreuniversal assessmentofchlorophylla,asageneralindicatorofphytoplankton biomass(Paerletal.,2003;Boyeretal.,2009).Particularlydiatoms areoftenusedforbiomonitoring,forexampleintheDiatomIndex ofWetlandCondition(DIWC),whichwasdevelopedformarshes inFlorida,withepiphyticdiatomdensityasthemostresponsive factortoarangeofanthropogenicdisturbances(pesticides,sedi- mentationandhabitatalteration)(LaneandBrown(2007).Aswith macroinvertebrates,identiﬁcationuntilgenuslevel,oreventaxa basedapproachessuchasfunctionalgroups,canalsoactasasurro- gateforphytoplanktonrichnessandcommunitystructure(Gallego etal.,2012).Forareviewonusingphytoplankton(amongothers)as abioindicatorinEuropeanlakes,seeBrucetetal.(2013),wherethey showedthatassessmentmethodsbasedonphytoplanktonhadthe highestnumberofcorrelationsbetweenanthropogenicstressand impactontheirenvironment.

2.2.6. Multimetricindices(MMI)

Properassessmentofsurfacewaterhealthconditionsingeneral andofwetlandsmoreparticularrequiresthesimultaneousassess- mentofitsphysical,chemical,and biologicalcomponents(Sims etal.,2013).Theintegrationofmultiplespeciesgroupstogether withphysicaland/orchemicalparametersinmultimetricindices (MMI)isthereforepreferredoversinglecomponentindicators.The trophicstateindex(TSI)forlakes,developed byCarlson(1977), isbasedonSecchidisktransparency,chlorophyllandtotalphos- phorus.Whileabioticvariablesarerelativelyeasytomeasure,they havelimitedvaluewhennotcomplementedwithbiologicalassess- mentssincetheyonlyrepresent(spatial/temporal)snapshotsof thecurrentstateofawetland.Therefore,mostmultimetricindices implementbioticvariablesaswell.TheQAELSindex,developed byBoix et al.(2005) for assessingthe water qualityof temporary and permanentfreshwater and thalassohaline wetlands, is agoodexampleoftheintegrationofdifferentfaunalgroupsand waterparameterstoassessecologicalintegrity.Thisindexisbased ontherelativeabundanceofeachmicrocrustaceantaxon(ACCO) andisimprovedbyaddingthetaxonomicrichnessofinsectsand crustaceans(RIC).LougheedandChow-Fraser(2002)developeda similarWetlandZooplanktonIndex(WZI)fortheLaurentianGreat LakesBasin,basedonwaterquality(totalphosphorus,totalnitrogen,totalsuspendedmatter,chlorophylla,temperature,dissolved oxygen,pHandconductivity)andzooplanktonassociationswith aquaticvegetation.AnotherexampleistheMMIbyVerdonschot etal.(2012)toassesstheeutrophicationstatusofarableditches, whichincludesthenumberofTrichopteraandGastropodafamilies,

totalfreshwatertaxaandpredatortaxaandthenutrientloading.

ThePredictiveSYstemforMultimetrics(PSYM)method,similarto thePLOCHmethod,wasdevelopedfor(permanent)pondsinthe UK,tocompareaparticularsitetootherpondsonecologicalquality (Biggsetal.,2000).Here,thecombinationofseveralmacroinverte- brateandmacrophytemetrics,includingthenumberofOdonata, MegalopteraandColeopterafamilies,thenumberofuncommon plantspeciesandthetrophicrankingscores(i.e.eutrophication measure)foraquaticandemergentplants,areusedtoassessthe generalqualityassessmentoflenticsystems.TheLagoonEutroph- icationMonitoringNetwork(LEMN)method,developedbySouchu et al.(2000)for shallowlagoonsin Southern France,integrates informationonwaterquality(temperature,salinity,turbidity,con- centrationsofdissolvedoxygen,nutrientschlorophylla,tPandtN), soilquality(organicmattercontent,totalphosphorus,totalnitrogen, granulometry, reduction potential), phytoplankton (abun- danceofcells <and>2␮m),acrophytesandmacroinvertebrates (speciescomposition,speciesrichness,speciﬁcbiomassdensity), togiveanindicationoftheeutrophicationstatusofthelagoons.

2.2.7. Modelingapproaches

Anotherwaytoestimatebiologicalqualityoffreshwaterhabi- tats is via predictive modeling approaches. An example is the RIVPACS(RiverInVertebratePredictionandClassiﬁcationSystem) method,originallydevelopedforrivers,whichallowspredicting macroinvertebratecommunitiesofahabitatbasedonmeasured environmental variables (Wrightet al., 1998).A series of pris- tineUKriversiteswerecarefullyselectedasreferencehabitats.

Foreachsite,macroinvertebratedataandphysicochemicalcharac- teristics(geographicaldata,historicaldata,substratecomposition analkalinity)werecollected,sometimesduringmultiplesampling campaignsovertheyear,afterwhichriverswereclassiﬁedinriver sitegroups.Modelingallowsthentorelatethecommunitydata withthephysicochemicaldata.Whenaphysicochemicalsampleis takenfroma(new)siteofinterest,theexpectedmacroinvertebrate faunacanbepredictedaccordingtothereferencesite.TheWFD deﬁnesthisexpectedfaunaasthe‘biologicalreferencecondition’.

Ifthenamacroinvertebratesampleistakenfromthisnewsite,the observedmacroinvertebratecommunitycanbecomparedwiththe expectedreferencecommunity.Theecologicalqualityofthesiteis thenassessedbytheobserved/expected(O/E)ratio.Theadvantage ofthismethod(atleastforUKrivers)isthattheO/Eratiocaneasily beconvertedtoEcologicalQualityRatios(EQRs),whichareusedby theWFD.Inaddition,O/Eratioscanbeinterpretedmoreintuitively andhaveabiologicalexplanation(CaoandHawkins,2004).

3. Discussion

Wehavegivenabroadoverviewofdifferentindicatortypesand indicesthat arecurrentlyusedtoassesstheecologicalintegrity of (mostly permanent)surface waters. We will now discuss to what extentwe expectsomeofthesemethodstobeusefulfor themonitoringoftemporarywetlands,onceadaptedtothispar- ticularecosystem.First,wefocusonthemostimportantecological characteristicsoftemporarywetlands,andwewillthenusethisas abasistoevaluateandrecommendpotentiallyusefulmonitoring approaches.Wewillalsosuggestspeciﬁcsamplingguidelinesto acquiretheneededbiologicalinformationinastandardisedway.

3.1. Temporalandspatialregionalvariabilityintemporaryponds

Temporarypondsare oftencharacterizedby theirsmallsize (generally not larger than 5ha)and shallowdepth (oftenonly a few decimeters deep). Such small water volumes are prone to strong diurnal and seasonal ﬂuctuations in abiotic parame- terssuchaspH,oxygen,nutrients,temperatureandconductivity

(8)

(Grillas et al.,2004; Williams, 2006). Waterlevelsalso tendto vary strongly betweenand within years depending onclimate conditions(Vanschoenwinkeletal.,2009;Waterkeynetal.,2009;

Sahuquilloetal.,2012).Thisimpliesthatsnapshotmeasurements of water quality parameters only provide information on the currentstateofthewetland,neglectingsometimesprominenttem- poralfluctuations.Thetimingofthesemeasurements(timeofday, season,year)isthereforecriticallyimportantfortheoutcomeof theassessment. The seasonal fluctuations in abiotic conditions alsoresult in a strong turnover of the animal and plant communities,withclearsuccessionalphases,eachrepresentedby a characteristicgroupoforganisms(Wigginsetal.,1980;Rhazietal., 2001b;Gascónetal.,2005;Jocquéetal.,2007;Waterkeynetal., 2009;Vanschoenwinkel et al., 2010).The community assembly processstronglydependsonthehydroperiod(lengthofinunda- tion)ofthewetlandssinceitrepresentsthetimewindowduring whichorganismsmusthatch/germinate/colonize,growandrepro- duce (Brooks, 2000; Serrano and Fahd,2005;Vanschoenwinkel etal.,2009).Alsointer-annualdifferencesinenvironmentalcondi- tionscanleadtodifferentcommunitiesinsubsequentinundations (Rhazietal.,2009;Waterkeynetal.,2009).Thetimingofsamp- lingthereforegreatlydetermineswhichtaxawillbeencountered (i.e.highbeta-diversityin time).Additionally,pondswithinone singleregion are often characterized by different communities andenvironmentalcharacteristicsandcontributethereforetohigh beta-diversityinspace(Williamsetal.,2004;Angeleretal.,2008), whichmakesitdifficulttofindgeneralindicatorspecies.Therefore, conservingandmonitoringnetworksoftemporarypondsinstead offocussingonsinglepondswassuggestedtobemoreaccurateand efficient(Gómez-Rodríguezetal.,2009;Rhazietal.,2012;Rosset etal.,2014).

3.2. Monitoringguidelinesfortemporarywetlands

Asfishesaregenerallylackingfromtemporarywetlands,with theexceptionofkillifishandlungfishinsome(sub)tropicalregions, indicesbasedonthisfaunalgrouparenotusefulandwillnotbe furtherdiscussed.Bioticindicessuchasthewaterfowlindexand thefrogcallintensityindexarealsolessusefulforassessingthe bioticintegrityoftemporarysystemssincethepresenceofthese faunalgroupsisoftenlimitedintime.Nonetheless,sincetempo- rarypondsareoftenusedasbreedingspotsforamphibians(Sala etal.,2008;Gómez-Rodríguezetal.,2009),thequantificationoflar- vaeduringspringtimecouldbeintegratedinamultimetricindex, especiallysinceamphibianlarvaeareverysensitivetopollution (Bakeretal.,2013).Withthedevelopmentofmulti-spectralremote sensingtechniques(Adametal.,2010;DekkerandHestir,2012), largewetlandareascanbeassessedatonceandfollowed-uponthe longterm.However,sincemosttemporarywetlandsaresmallsized waterbodies,evenonlyquantificationofthesehabitatsremains difficult(DeRoecketal.,2008).Incontrasttotheassessmentofthe ecologicalstatusofshallowpermanentlakesthatcanbedoneby visitingthelakeonlyoncetohaveanoverviewofthecatchment, measurepHand turbidity,and documentthegeneral structure ofmacrophytecommunities(Mossetal.,2003),temporaryponds aresuchfluctuating,highlydynamic systemsthat welladapted samplingprotocolsare required that incorporatethis temporal variability(Brocketal.,2003).Therefore,weproposestandardized guidelinesthatcanbeusedforsamplingpondswithaperiodically dryphase,takingintoconsiderationthisseasonality.

3.2.1. Dryphase

Duringthedryphaseofatemporarypond,thesedimentiseasy tosample.Bycollectingaspatiallyintegratedsampleoftheupper 3cmofthesediment(i.e.‘theactiveeggbank’;BrendonckandDe Meester,2003),andhatchingitinthelaboratoryundercontrolled

climateconditions,‘hidden’pondbiodiversitycanbeassessed(and restored)evenwhenthepondisnotinundated(Brendonckand Williams,2000;AngelerandGarcía,2005;Vandekerkhoveetal., 2005).However,sinceaproportionofeggsmayremainunhatched afteronelaboratoryinundation,‘sugarﬂoatation’canbeusedto isolatetheremainingeggs(Onbé,1978;Marcus,1990).Thisfrac- tioncanthenbefurtheridentiﬁedunderamicroscopebasedonegg morphology(Vandekerkhoveetal.,2005;Brendoncketal.,2008).

Similarly,thisalsoappliestoannualtemporarypondplants,which produceseedsthatbuilduptheseedbankintheupperlayersofthe sediment(Rhazietal.,2001a).Theisolationofseedsisbasedonthe methodbyMalone(1967),andidentiﬁcationcanbeperformedby comparingseedmorphology.

Duetopartialhatchingateachoccasioncombinedwithdisturb- anceofthesurfacesediment,eggsintherestingeggbankoften originatefromdifferentgenerations(BrendonckandDeMeester, 2003).Assuch,so-called‘mixed’eggbanksmaynotalwaysprovide informationonrecentchangesintheecologicalqualityofwetlands.

Insystemswhereconditionsaretemporarilyunfavorableforcer- tainspeciesthatdosurviveasrestingpropagulesinthesediment, assessingthe‘hiddenbiodiversity’maythereforeresultinadif- ferentecologicalstatusthaniftheassessmentwasonlybasedon theactivecommunities(Vandekerkhoveetal.,2005).Thisaspectis oftenneglectedinexistingindicesforpermanentwaters,butcan beimplementedinindicesfortemporarywaterstocreateamore integratedlongtermviewofthewetlandcondition.

Thesediment itself canalsobeused formeasuringsoil abioticindicators,suchasgranulometry,chemicalcharacteristics(pH, totalNandP)anddryorganicmattercontent,asdescribedinthe LEMNmethodbySouchuetal.(2000).Thesevariablesarelesssen- sitivetoﬂuctuationsinthewatercolumnandmeasurementscan evenbedoneduringthedryseasonwhenthesedimentisexposed.

Someanthropogenicimpactsthatarepossiblyinvisibleduringthe wetseason,suchas theamountof landﬁllor patternsofcattle useintensity(tramplingandgrazing),mayalsobeeasiertoassess duringthedryseason.

3.2.2. Aquaticphase

Thesedimenthasastrongimpactontherecyclingofdissolved minerals(Golterman,2004).Intemporaryponds,thiseffectiseven stronger since the dissolvedminerals are recycled throughthe sediment each time theydryout. Therefore, trophic thresholds developedfordeepstratiﬁedlakescannotbeusedforassessingthe ecologicalqualityoftemporaryponds,implyingthenecessityfor anewmethodofeutrophicationassessment(Elkiathietal.,2013).

Assuch,basedontheequilibriummodelofGolterman(2004),the ratiobetweentheamountoftotalphosphorusandtheparticulate Ppoolscouldactasanindicatorforeutrophicationinthesetempo- raryhabitats.PreliminaryanalysesbasedonSpanishandMoroccan wetlanddataappeartoconﬁrmthis(Serrano,unpublisheddataand VandenBroecketal.,unpublisheddata).

Samplingoftheactivecommunities(zooplankton,phytoplankton,macroinvertebrates,macrophytesandamphibians)shouldbe accomplishedtoprovideadditional informationonspecies that permanentlyinhabitthepond butthatdidnothatchinthelab fromtheeggorseedbank.Suchsamplingisevidentlyalsoneeded tocollecttheactivedispersersthatusuallyleavethepondbefore itdries.Duetothehighanimalandplantspeciesturnover,multi- plesamplingcampaignsduringthewetseasonarepreferred(Boix etal.,2005; Bovenand Brendonck,2009).Samplingonemonth afterinundationandonemonthbeforedryingout,completedwith asamplingcampaignhalf-waythroughtheinundation,givesin mostcasesanintegratedviewofthecommunitystructure.Anaddi- tionalﬂoralsurveycanbeperformedafterdryingout,toassessthe communitystructureofthelatesuccessionalplantsaswell.

(9)

Thehighsensitivitytowarddisturbancesand knownecology of zooplankton, macroinvertebratesand macrophytesallowthe integrationofthesediversegroupsinbioticindicesfortemporary waters.TheintegrativeQAELSindexdevelopedbyBoixetal.(2005) offersinterestingperspectives.First,thisindexisbasedonmulti- plesamplingperiodswhicharenecessarytogenerateanintegrated overviewoftheturnoverofspeciesandﬂuctuatingdynamics.Sec- ond,itintegratesbothzooplanktonandmacroinvertebratesinto onesingleindex.Althoughzooplanktonisaveryimportantpartof theecologicalintegrityofwetlands(Mossetal.,2003),theWFD currentlylackstheincorporationofazooplanktoncomponent.The useofmacro-invertebratesin(multi-metric)indices,however,is alreadywidelyusedinpermanentsystems(CriadoandAlaez,1995;

Verdonschotetal.,2012),andrecentlyalsointemporaryponds (Gutiérrez-EstradaandBilton,2010).Sinceithasbeenshownfor somegroups(e.g.Coleoptera)thatconsideringonlyhighertaxo- nomiclevelsalreadyallowsthemonitoringofwaterbodies(Criado andAlaez,1995;Oertlietal.,2005a;Gutiérrez-EstradaandBilton, 2010),detailedspeciesidentifications,whichareoftendifficultand time-consuming,maynot alwaysbenecessary. Nevertheless,if detailedspeciesidentificationsarerequired,weconsiderDNAbar- codingasapotentialtool toovercomeidentificationdifficulties, suchasshownforexamplebyHajibabaeietal.(2011)forbenthic freshwatermacroinvertebrates.Indicesbasedonmacrophytesare alsohighlyrelevantsincetemporarypondsoftenhousecharac- teristichighlyspecializedspecies(Bouahimetal.,2014)thatplay importantrolesintemporarywetlandecosystems(Bornetteand Puijalon,2011).

Predictivemodelingapproaches offeradditionaltoolsforthe bioassessment of temporary waters, not only using macroinvertebrates,but also other taxonomicgroups that show strong associationswiththeirenvironment.Althoughtemporaryponds showstrongspatialandtemporalvariation,multiplesamplingof activefaunaland ﬂoralcommunities, incombination withana- lyzingtherestingcommunitiesandtheenvironmentalvariables, shouldindicatewhichsitesaremorepristineandcanbeusedas referencesitesinthearea.Temporarypondsofinterestcanthen beassessedusingtheO/Eratio,cfr.Wrightetal.(2000).However, currentlytoolittledataisavailabletovalidatethismethod.

Lastly,formonitoringtemporaryponds,wespecificallypromote theuseoflargebranchiopods(Anostraca,Notostraca,Laevicaudata, SpinicaudataandCyclestherida).Theseverycharacteristictempo- rarywetlandspeciesareconsideredtobetheflagshipspeciesof thesehabitats(Colburn,2004).Theyhaveaworldwidedistribution (Brendoncketal.,2008),theirecologyiswellstudiedandtheypro- ducerestingeggbankswhichcaneasilybesampledandhatched inthelaboratory(BrendonckandWilliams,2000).Mostofthem alsohave aspeciesspecificeggmorphology(Brendonckand De Meester,2003)makingthemeasilyidentifiableafterisolation.Dif- ferentstudiesindicatethatlargebranchiopodsareverysensitive towardstressors,suchassalinity(Waterkeynetal.,2010),hydro- logicalchanges(Pyke,2005;Tuytensetal.,2014),pollution(Hamer andBrendonck,1997)andhabitatmodification(Vanschoenwinkel etal.,2013).

3.3. Concludingremarks

Althoughtemporarywetlandsareamainwatersourcein(semi) aridregionsandoftenhouseauniquediversity,ofﬁcialmonitor- ingprogramsliketheWFDcurrentlydonotcoverthishabitattype.

Despitethebroadrangeofdifferenttypesofexistingindicatorsand indicesforlakesandwetlands,manylimitationsstillexistfortheir generalapplication(Innisetal.,2000).Onesuchconstraintisthe lackoftaxonomicallyskilledspecialistswhocaneasilyidentifytax- onomicgroupsdowntothedesiredlevel.Combinedwithfurther neededresearchontheauto-ecologyofparticulartaxa,thisshould

leadtothedevelopmentofmorereliableindicatorsthatcanbeused by wetland managers. These limitations and recommendations alsoapplyforthecurrentsetofmonitoringtoolsfortemporary wetlands that weregenerallyonly developedand appliedfor a particularregion.Theserestrictionscanleadtothefurtherdegra- dationoftemporarypondsworldwide,especiallyincombination withthevariousandofteninconsistentinternationalagreements andnationalpolicies.Basedonexistingtoolsforassessingdiffer- enttypesofwaterbodies,wehavemadesomerecommendations forstandardizedmonitoringofthislargelyignoredbutecologically andsocio-economicallyimportanthabitattype.Wehaveespecially highlightedtheuseoflargebranchiopods,mixedrestingeggand seedbanksand sedimentqualitytoassess thequalitystatusof temporaryponds.Asbothrestingegg andseedbanksand sed- imentintegratetemporal variationinwaterandhabitatquality, theycouldtosomeextentreplacelaborintensivefrequentsnap- shotsamplingoftheactivecommunities.Whenthesemethodsare furtherinvestigated,theycanbevalidatedforalargesetoftempo- rarypondtypesfromdifferentregions,followedbytherealization ofuserfriendlyprotocolsandtrainingsessions,especiallyforland ownersandconservationists.

Acknowledgments

MaartenVandenBroeckisaresearchfellowfundedbyaVLIR- UOS (VLADOC) grant. This project hasbeen achieved with the ﬁnancial support of a VLIR-UOS SI project(No. ZEIN2011Z092/

2011-101).

References

Adam,E.,Mutanga,O.,Rugege,D.,2010.Multispectralandhyperspectralremote sensingforidentiﬁcationandmappingofwetlandvegetation:areview.Wet- landsEcol.Manage.18,281–296.

Adamus,P.R.,Brandt,K.H.,1990.ImpactsonqualityofinlandwetlandsoftheUnited States:asurveyofindicators,techniques,andapplicationsofcommunity-level biomonitoringdata.In:EPAReport600/3-90/073.

Alahuhta,J.,Kanninen,A.,Hellsten,S.,Vuori,K.-M.,Kuoppala,M.,Hämäläinen,H., 2013.Variableresponseoffunctionalmacrophytegroupstolakecharacteristics, landuse,andspace:implicationsforbioassessment.Hydrobiologia737,1–14.

Amat,J.,Green,A.,2010.Waterbirdsasbioindicatorsofenvironmentalconditions.

In:Hurford,C.,Schneider,M.,Cowx,I.(Eds.),ConservationMonitoringInFresh- waterHabitats,vol.5.Springer,Netherlands,pp.45–52.

Angeler,D.G.,García,G.,2005.Usingemergencefromsoilpropagulebanksasindi- catorsofecologicalintegrityinwetlands:advantagesandlimitations.J.North Am.Benthol.Soc.24,740–752.

Angeler,D.G.,Viedma,O.,Cirujano,S.,Alvarez-Cobelas,M.,Sánchez-Carrillo,S.,2008.

Microinvertebrateandplantbetadiversityindrysoilsofasemiaridagricultural wetlandcomplex.Mar.FreshwaterRes.59,418–428.

Angermeier,P.L.,Davideanu,G.,2004.Usingﬁshcommunitiestoassessstreamsin Romania:initialdevelopmentofanindexofbioticintegrity.Hydrobiologia511, 65–78.

Arheimer,B.,Löwgren,M.,Pers,B.C.,Rosberg,J.,2005.Integratedcatchmentmod- elingfornutrientreduction:scenariosshowingimpacts,potentialandcostof measures.AMBIO34,513–520(AJournaloftheHumanEnvironment).

Baker,N.J.,Bancroft,B.A.,Garcia,T.S.,2013.Ameta-analysisoftheeffectsofpesti- cidesandfertilizersonsurvivalandgrowthofamphibians.Sci.TotalEnviron.

449,150–156.

Balcombe,C.K.,Anderson,J.T.,Fortney,R.H.,Kordek,W.S.,2005.Wildlifeuseof mitigationandreferencewetlandsinWestVirginia.Ecol.Eng.25,85–99.

Beck,M.W.,Hatch,L.K.,2009.Areviewofresearchonthedevelopmentoflakeindices ofbioticintegrity.Environ.Rev.17,21–44.

Biggs,J.,Nicolet,P.,Mlinaric,M.,Lalanne,T.,2014.ReportoftheWorkshoponthe ProtectionandManagementofSmallWaterBodies.EuropeanEnvironmental Bureau(EEB).

Biggs,J.,Williams,P.,Whitﬁeld,M.,Fox,G.,Nicolet,P.,2000.Biologicaltechniquesof stillwaterqualityassessment.Phase3.Methoddevelopment.In:Environment AgencyR&DTechnicalReportE110.EnvironmentAgency,Bristol.

Bird,M.,Day,J.,2010.AquaticinvertebratesasindicatorsofhumanimpactsinSouth Africanwetlands.In:WetlandHealthandImportanceResearchProgramme (WRCProjectNo.K5/1584).

Birk,S.,Bonne,W.,Borja,A.,Brucet,S.,Courrat,A.,Poikane,S.,Solimini,A.,Van DeBund,W.,Zampoukas,N.,Hering,D.,2012.Threehundredwaystoassess Europe’ssurfacewaters:analmostcompleteoverviewofbiologicalmethodsto implementthewaterframeworkdirective.Ecol.Indic.18,31–41.

Blaustein,L.,Schwartz,S.S.,2001.Whystudyecologyintemporarypools?Isr.J.Zool.

47,303–312.