in plant-herbivore systems in an urban landscape? Do levees support diversity and affect spatial turnover ofcommunities Ecological Engineering

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Ecological Engineering

j o u r n a l h o m e p 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 e n g

Research Paper

Do levees support diversity and affect spatial turnover of

communities in plant-herbivore systems in an urban landscape?

Dawid Moro ´n

^a,∗

, Łukasz Przybyłowicz

^a

, Marcin Nobis

^b

, Agnieszka Nobis

^b

, Ewelina Klichowska

^b

, Magdalena Lenda

^c

, Piotr Skórka

^c

, Piotr Tryjanowski

^d

aInstituteofSystematicsandEvolutionofAnimals,PolishAcademyofSciences,Sławkowska17,31-016Kraków,Poland

bInstituteofBotany,JagiellonianUniversity,Kopernika27,31-501Kraków,Poland

cInstituteofNatureConservation,PolishAcademyofSciences,Mickiewicza33,31-120Kraków,Poland

dInstituteofZoology,PoznanUniversityofLifeSciences,WojskaPolskiego71C,60-625,Pozna´n,Poland

a r t i c l e i n f o

Articlehistory:

Received21January2016

Receivedinrevisedform12April2017 Accepted27April2017

Keywords:

City Corridor Dispersion Pollinator Trophiclevel

a b s t r a c t

Valuablehabitatsinvariousspatialconfigurationsareessentialformaintainingbiodiversityacrosshighly fragmentedurbanlandscapes.Inalarge-scalestudy,weexploredthevalueofhuman-madestructures –riverlevees–asvaluablehabitatsthatsupportlargepopulationsofplantsandbutterfliesandaffects thespatialturnoverofspecieswithinanurbanlandscape.Themostsignificantenvironmentalvariables affectingplantandbutterflypopulationsonleveeswerealsoexamined.Therichnessofnativeplant specieswasabout25%greateronleveetransectsthanoncontrolgrasslandtransects.However,therich- nessandabundanceofbutterfliesonleveeswerethesameasongrasslandsites.Amongenvironmental factors,urbanareacovernegativelyaffectedtherichnessofnativeplantspecies.Shrubcoverdecreases therichnessandabundanceofbutterflyspecies.Inaddition,highmowingintensityhadanegativeinflu- enceonabundance.Communitydissimilarityofplantsonleveeswasaffectedbyspatialvariables.Our studyisthefirsttohighlightleveesassignificanthabitatsforplantandherbivorousinsectpersistence, andtheirpotentialfunctionforplantdispersal.

1. Introduction

Increasing urbanisation is one of the main factors nega- tivelyaffectingplant-herbivoresystemsworldwide(Harrisonand Winfree,2015;McKinney,2006;Paliketal.,2005).Urbanareasare characterisedbyintensivemanagement,withdiminishingsemi- naturalhabitatpatchesseparatedfromeachotherbyamatrixof developedfeatures(McKinney,2008).Thus,conservationstrate- gieswhichcounteracturbanisationshouldtakeintoaccountthe preservationofvaluablehabitats,aswellasspatiallyaffectedpro- cessessuchas species dispersion.Accordingly, interventions in urbanlandscapes,i.e.creatinggreen areas,havebeenproposed inthehopethatsuchspaces mayserve asvaluable habitatsfor livingcreatures(HunterandHunter,2008).Afurtherpotentialben-

∗ Correspondingauthor.

E-mailaddresses:dawidmoron@poczta.onet.pl(D.Moro ´n),

lukasz@isez.pan.krakow.pl(Ł.Przybyłowicz),m.nobis@uj.edu.pl(M.Nobis), agnieszka.nobis@uj.edu.pl(A.Nobis),ewelina.klichowska@uj.edu.pl (E.Klichowska),lenda.m@vp.pl(M.Lenda),skorasp@poczta.onet.pl(P.Skórka), piotr.tryjanowski@gmail.com(P.Tryjanowski).

eﬁtofgreen areasisthat theymaysustainspatially dependent processes(HaddadandTewksbury,2005),especiallyinthehighly modiﬁedurbanlandscape.However,conservationofspeciesdiver- sityandsustainingspatialprocessesfacesmanypracticalhurdles.

Forexample,landscapemanagementinacityiscostly(Commission forArchitectureandtheBuiltEnvironment,2006),whileitseffec- tivenessdependsontheecologicalgroupororderoforganisms beingtargeted(Jaroˇsíketal.,2011)andtypeofmatrixorlandscape structure(SogaandKoike,2013).Asupplementarysolutionisto discoverandutilisethepotentialadvantagesofexistinghuman- madehabitatsandstructuresenrichingbiodiversityandenabling essentialspatialconnections betweenpopulations(Lenda etal., 2012;Schrieveretal.,2009;Toniettoetal.,2011).Forexample,lin- earelementsofthelandscape,frequentlyrelatedtohumanactivity, mightoffersigniﬁcantconservationbeneﬁts(Buenoetal.,1995;

Moro ´netal.,2014).Thus,environmentsresultingfromthedevel- opmentofcivilisationmightpartlyreducetheadverseeffectsof urbanisation.

Humans traditionally settled along rivers, which led to the developmentoftownsandcitiesinsuchplaces(Kostof,1992).In developedcountries, leveesarebuilttoprotecturbanisedareas againstﬂoods,especiallysinceciteswereusuallylocatedonriver http://dx.doi.org/10.1016/j.ecoleng.2017.04.052

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banks.Forexample,theoveralllengthofleveesinFrance,Poland or the USA amounts to 10 000km, 8 500km and 40 000km, respectively (Dupray et al., 2010; McCully, 2007; Ministerstwo

´Srodowiska,2010).Thisshowsthatleveesarefrequentelements oftheurbanscenery.Theseandotherelongatedstructuresmight besignificantreproductivehabitatsanddispersalroutesformany organisms(Fukamachietal.,2005;Martinetal.,1991).Despitethe ubiquityofleveesinthelandscapesofmanyEuropeanandAmer- icancities,theirbenefitsforthedynamicsofanurbanecosystem havenotbeenstudiedtodate.Wethereforeperformedalarge-scale studytoexplorethevalueofthishabitatinplant-herbivoresystems,i.e.nativeplants(hereafterplants)andbutterfliesinanurban landscape.To thisend, we investigated therichness andabun- danceofplantandbutterflyspecies,andtherelationshipsbetween thesegroups’ dissimilaritiesand geographic distances. In refer- encetobiodiversityandthespatialprocessesatlevees,westudied speciesrichness,andabundanceanddissimilarityintypicalplant andbutterflyhabitatsinurbanlandscapesconsistingofextensively managedorrecentlyabandonedgrasslands(Skórkaetal.,2007).

We anticipatedthat,ifleveesare valuablehabitats,theywould supportarichnessandabundanceofplantandbutterﬂyspecies relativelyequivalenttoorevenhigherthanoncontrolgrasslands.

Next,wedeterminedsiteaswellaslandscapevariablesimpacting therichnessandabundanceofbutterfliesandtherichnessofplants onlevees,inordertoformulateproposalsessentialforimproving themanagementofthishabitat.Weexpectedalsothat,ifdispersal- dependentprocessesdonotdriveplantandbutterflycommunities, thestudysitesshouldexhibitaspatiallyrandompatternofdissim- ilarity.However,iftheplantsandbutterfliesdisperseusinglevees, thisshouldbereflectedinlessdissimilarspeciescompositionat adjacentsites.

2. Materialsandmethods 2.1. Studyarea

Theinvestigationwasperformedalong aleveesysteminthe agglomerationofKraków,southernPoland(Fig.1).Residentialpop- ulationdensityatthestudyarea(basedontheprincipalunitof administrativedivision)was1558perkm²,whereasforPoland itis123perkm².Alltheleveesarewell-settledand werecon- structedmorethan20years ago.Weselected30leveesand20 grasslandsinsuchawayastoensureanaveragedistancebetween all sites of each type as similaras possible (Fig.1).The mean distancebetweenallpairsofselectedleveeswas7.0km(range:

0.7–20.4km)andthemeandistancebetweenallpairsofgrasslands was6.9m(0.6–20.6km;Wilcoxontest,W=42066,p=0.722).The leveesclosesttoeachotherwereseparatedbyameandistanceof 1.1±0.7km(0.7–3.8km),andthegrasslandsclosesttoeachother wereseparatedbyadistanceof1.3±0.6km(0.6–2.4km;Wilcoxon test,W=379,p=0.120).Wechosegrasslandsincloseproximityto alevee,withthemediandistancetothenearestleveeat1.1km (range:0.6–2.7km),inordertoensurethatlocalenvironmental conditionssuchasbedrock,microclimateandlandscapewereas similaraspossibletothelevees.Grasslandsweresituatedclose towatercoursestominimisethepotentiallyconfoundingeffectof waterbodypresencenearlevees.Theleveesandgrasslandsareboth maintainedwithlow-intensitymanagement,withmowingtaking placeatmostonceperyear.

2.2. Plantandbutterﬂysurveys

Thenumberofplantspecieswasnotedintworectangularplots of12m² (3×4m)situated ateach site,withashortaxisorien- tatedalongthenearestwatercourse(AppendixAinSupplementary

Table1

Variablesmeasuredonlevees.Mean±standarddeviation(SD)withminimumand maximumvaluesareshown.

Independentvariables Mean±SD(min.–max.)

arablelandcover(%) 2.41±4.02(0.00–13.91) humansettlementcover(%) 25.30±22.94(0.00–81.00)

leveecover(%) 4.13±2.07(0.30–9.67)

indexofmowingfrequency 0.08±0.07(0.00–0.20) speciesrichnessofnon-nativeplants

(no.species)

4.03±2.22(0.00–10.00) angleofslopes(degree) 25.68±4.20(16.50–38.17) lengthofslopes(m) 7.22±2.26(3.58–13.17)

shrubcover(%) 11.17±27.03(0.00–100.00)

waterreservoircover(%) 11.70±9.54(0.00–34.38) woodlandcover(%) 9.92±7.34(0.00–25.34)

material).Forlevees,asingleplotwasestablishedinthemiddleof theinneraswellastheoutersides.Therewasadistanceof100m betweentwoplotsbothatleveeandgrasslandsites.Plantswere notedonthreeoccasions,inthemiddleofMay,attheendofJune andinAugust.

Atransectof200mwasusedateachsiteforbutterﬂysurveys (PollardandYates,1993).Transectsatleveesandgrasslandswere situatedalongthenearestwatercourse.Forlevees,halfofatransect spannedtheinnersideoftheleveeandthesecondhalfwasplacedat theouterside(AppendixAinSupplementarymaterial).Butterﬂies werecountedoneachtransectinMay,attheturnofJuneandJuly andinAugust.Transectswerevisitedinrandomorderatdifferent timesofdayandduringwarmandcalmweather.

2.3. Environmentalvariablesmeasuredforlevees

Environmentalvariableslikelytoaffectnativeplantsandbut- terﬂiesweredeterminedforlevees.Thosevariableswerearable landcover,humansettlementcover,leveecover,indexofmowing frequency,speciesrichnessofnon-nativeplants,angleofslopes, lengthofslopes,shrubcover,waterreservoircoverandwoodland cover(Table1).Shrubcoverwasmeasuredaspercentage(0–100%) ofleveearea.Arableland,humansettlement,levee,waterreservoir andwoodlandcoversweremeasuredaspercentages(0–100%)ina bufferof200maroundthetransects(AppendixAinSupplementary material).Variableswithinbuffersweremeasuredintheﬁeldby GPS,anddigitalisedusingtheQGISprogramme.Angle(degree)and length(m)weremeasuredatbothendsandinthemiddleoftran- sectsandthenthemeanwascalculated.Invasiveplantspecieswere countedonthesameplotsthatweresurveyedfornativeplants.

Duringeachtransectsurvey,mowingfrequencywasnotedandthe indexintroducedbyValtonenetal.(2006)wasused.Theindex talliestheoverallimpactof mowingonplantsduringthestudy duration.Foreachsurveyamowingintensityvalue(0=nomow- ing,1/2=partialmowing,1=totalmowing)wasassignedandthe valuewasdecreasedtothelowerlevel,respectivelyfrom1to1/2 andfrom1/2to0,sevenweeksaftermowing,asaresultofveg- etationrecoveryaftermowing.Thesumofthevaluesfromeach surveywasusedforfurtheranalysis.

2.4. Analysis

Model selection procedure based on information theory (BurnhamandAnderson,2002)wasusedtoidentifyenvironmen- talvariablesassociatedwiththerichnessandabundanceofspecies onlevees.Foridentiﬁcationofthemostparsimoniousmodelsfrom eachvariableset,theAkaikeinformation criterioncorrectedfor smallsamplesize(AICc)wasused.Next,allmodelswereranked accordingtotheirAICcvalues,andweusedthosewiththelowest AICccombinedwithrelatedweightvaluesasthebestforexplaining the data. Models with AICc lower than two were acknowl-

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Fig.1.MapindicatingthelocationsofthestudysitesintheKrakówregion,south-easternPoland.

edgedasequallygood(BurnhamandAnderson,2002).Estimation of functionslopes of parameters of concernwasperformed by modelaveraging(BurnhamandAnderson,2002).Lastly,themodel weightswereappliedtodeterminetherelativeimportanceofeach independentvariableoverthefullsetofmodelsassessedbysum- mingweightvaluesofallmodelsetsthatincludedtheindependent variableofconcern(BurnhamandAnderson,2002).Thefunction slopes(betas)wereconsideredassigniﬁcantiftheir95% conﬁ- denceintervalsdidnotoverlapwithzero.Forthemodelselection procedure,dependentvariablesweresquare-roottransformedin ordertolineariserelationships,tonormalisedistributions,andto lowertheimpactofoutliers(Quinnand Keough,2002).Toper- mitdetection ofstraightforward relationshipsof function slops betweenindependentvariables,theywerestandardised(meanof zeroandastandarddeviationofone;QuinnandKeough,2002).

Spatialautocorrelationinthenumberofspecies(plantsandbut- terﬂies)andindividuals(butterﬂies)werecheckedbycalculating Moran’sstatisticsoncorrelograms(LegendreandLegendre1998).

However,therewasnoevidenceforstatisticallysignificantauto- correlation,andthereforeweusedtraditionalstatistics.Statistical modelswerebuiltindependentlyforplantsandbutterflies(mod- elstested:plants–511;butterflies–2047).Modelselectionand averagingbasedontheAICcwereperformedusingSAM4.0soft- ware(Rangelet al.,2010).TheWilcoxon ranksumtestin R(R DevelopmentCoreTeam,2016)wasappliedtocomparethenum- berofplantspeciesandbutterflyspecies,aswellasabundances betweenleveesandcontrolgrasslands.

WeusedtheJaccarddissimilarityindextoascertainspatially affectedspeciesturnover.Thisindextakesintoaccountthespecies thataredifferentbetweenapairofsites,andisdeﬁnedasthepro- portionoftheoverallpullofspeciespresentateachsite.Theindex rangesfrom0foridenticalpullofspeciesatsitesto1fornocommon speciesbetweensites.TheJaccardindexaccountsfordissimilarity derivedfromturnover(speciesreplacement)aswellasfromnest- edness(eliminationofspecies;Baselga2012).WeusedtheJaccard dissimilaritycomponentbasedsolelyonspeciesturnover(Baselga etal.,2013).Thisdissimilarityindexwascomputedforeachpairof sitesforplantsandbutterﬂies.

WegeneratedthespatialvariablesusingMoran’sEigenvectors Maps(MEM)fromthesitecoordinates(Borcardetal.,2011).Each spatialvariable generated representsa differentspatial pattern

thatmightexplaincommunitydissimilarity.WeusedalltheMEM eigenvectorswithpositiveeigenvaluesaspotentialspatialpredic- tors(Borcardetal.,2011).Eigenvectorswithpositiveeigenvalues correspondtopositivespatial correlation(Borcardet al.,2011).

MEMeigenvectorswithhighassociatedeigenvalues,e.g.MEM1, aresaidtorepresentbroad-scalepatterns,whereastheMEMeigen- vectorswithlowerassociatedeigenvalues,e.g.MEM7,represent finerspatialscales(Borcardetal.,2011).Next,weselectedthebest MEMeigenvectorsexplaining community dissimilaritiesby for- wardselection.TheselectedMEMeigenvectorswereusedasspatial explanatoryvariables.Then,withthehelpofpartialRedundancy Analysis,weevaluatedthecontributionofselectedMEMeigenvec- torstothedissimilarityofplantsandbuttireflies.Weaccounted herefor thevariance explained exclusively byspatial variables (afterremovingthecofoundingeffectoftheenvironmentalvari- ables).Allspatialanalysiswasperformedseparatelyforbutterflies andplantsatleveesandgrasslands.Allstatisticalanalysisofdis- similaritywasperformedusingtheadespatial(Drayetal.,2016), betapart(Baselga,2012)andvegan(Oskanenetal.,2013)packages inR(RDevelopmentCoreTeam,2016).

3. Results

3.1. Comparisonofleveesandgrasslands

A total of 179 plant species and 40 butterﬂy species were recordedonlevees,comparedto148plantspeciesand39butter- ﬂyspeciesoncontrolgrasslands(AppendixAinSupplementary material). The richness of native plant species was about 25%

greateronleveetransectsthangrasslandtransects(28.9vs.21.2 species; W=135.5, p=0.001), whereas the richness of invasive speciesdidnotdifferbetweenhabitats(4.0vs.3.3species;W=238, p=0.218).Differencesbetweenleveesandgrasslandsfortherich- nessandabundanceofbutterﬂyspecieswerenotsigniﬁcant(9.8vs.

10.2species;W=258,p=0.408;31.7vs.27.2individuals;W=244, 0.271).Altogether,74plants(outof222)andeightbutterflies(out of47)wereuniquetolevees.Atotalof43plantandsevenbutterfly specieswereuniquetograsslands(AppendixAinSupplementary material).However,thesedifferenceswerenotsignificant(plants:

Fexact,p=1.000;butterﬂies:Fexact,p=0.570).Therewere105 speciesofplantsand32speciesofbutterﬂiesthatwerepresenton

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bothleveesandgrasslands(AppendixAinSupplementarymate- rial).

3.2. Leveecharacteristicsaffectingspeciesrichnessand abundance

ModelselectionbasedonAkaike’scriterionidentifiedthreebest modelsandexplainedabout36%ofvariationinnativeplantspecies richnessonlevees(Table2).Amongthevariablesweexamined, onlyhumansettlementcoverwasdisplayedinallthebestmod- els(Table2;AppendixAinSupplementarymaterial).Thespecies richnessofplantswasalsoaffectedbyarablelandandleveecover (Tables2and3).AccordingtoAkaike’scriterion,ninebestmodels explainedabout56%ofthevariationinspeciesrichness ofbut- terflies(Table2).Ofthevariables,shrubcover wasdisplayedin allthebestmodels(Table2;AppendixAinSupplementarymate- rial).Theabundanceofbutterflieswasalsoaffectedbyarableland cover,humansettlementcover,indexofmowingfrequency,angle ofslopes,lengthofslopes,andwoodlandcover(Table3).Model selection accordingto Akaike’s criterion showedsix best mod- elsexplainingabout50%ofthevariationinbutterflyabundance (Table2).Amongthevariables,themowingindexwasdisplayedin allselectedmodels(Table2).Theabundanceofbutterflieswasalso vulnerabletohumansettlementcover,speciesrichnessofnative plants,angleofslopes,lengthofslopes,andshrubcover(Table3).

3.3. Plantandbutterﬂydissimilarityandspatialprocesses

Community dissimilarityof plants and butterﬂies on levees andcontrolgrasslandsdisplayeddifferencesconnectedwithspa- tial variables. Plant dissimilarity on levees was inﬂuenced by MEM1, MEM3, MEM4 and MEM5 eigenvectors: the closer the sites,themoresimilartheircommunitycomposition(F4,15=1.16;

R²_adj=0.08;p=0.021).Incontrast,dissimilaritywasnotadjusted withspatialvariablesforplantspeciesongrasslands.Spatialvari- ableswerenotaffectedforbutterﬂiesonleveesorgrasslands.

4. Discussion

Despitetheubiquityofleveesandtheirpotentialroleasurban matrixhabitatsforthedispersionoforganisms,theyhavenever beenstudiedinthecontextofplant-herbivoresystems.Ourresults indicatethatriverleveesareimportanthabitatsforplantandbut- terflypopulationsandthattheycanspatiallymodifydissimilarityof communities.Thepotentialroleofleveesasvaluablehabitatsmay bedue totheadvantageousconditionsandresourcestheyoffer formanyspecies,forexample,bycreatingastrongenvironmental gradient,e.g.inmoisture(Moro ńetal.,2014).Also,leveescrossthe natural-urbangradientandthusmayensureconnectivitybetween populationsfromdifferentlandscapes(Moro ńetal.,2014).How- ever,ouranalysisindicatedassociationsbetweenspatialvariables andcommunitycompositiononlyforplantsacrosslevees.Thus, leveesmayhavelimitedvalueforbutterflypopulationconnectivity inurbansettings.Thismayresultfromthepossibilitythatleveesare verygoodhabitatsforthestudiedorganisms.Itwasdemonstrated thatpoor-qualityhabitatsarethemosteffectivedispersalroutes becauseorganismsarenotwillingtoreproducethere(Haddadand Tewksbury,2005).

4.1. Leveesvs.grasslands

Leveesarelinearhabitatsthatexhibitdrier,warmerconditions attheirupperportionswhereastheirlowersegmentsarecolder andwetter,creatingastrongenvironmentalgradient.Moreover, ﬂoodsandregulardisturbanceatthetimeofrepairsoftenaddto

theconsiderablehabitatmosaic(Fiesetal.,2016).Thus,leveescon- tainvaluablehabitatsformanyspeciesinplant-herbivoresystems, particularlyinanthropogeniclandscapes.Theresultsshowthatlev- eesaresignificanthabitatsforplantsandbutterfliesinanurban landscape. Themean numberof plantspecies wassignificantly highercomparedtocontrolgrasslands,andthemeannumberof butterflyspeciesandindividualsdidnotdifferbetweenleveesand grasslands.Thisindicatesthattherichnessofplantspeciesisnot necessarilyagoodindicatorofbutterflyrichnessbetweenlevees andgrasslands(Kremen,1992).

4.2. Leveecharacteristicsaffectingplantsandbutterﬂies

Theenvironmentalattributesofleveessigniﬁcantlyaffectedthe richnessofplantspecies.Thefactorsexplainedabout36%ofvaria- tioninplantcompositiononlevees.Themostimportantfactorfor therichnessofplantspeciesonleveeswashumansettlementcover.

Manystudiesabouttheresponseofplantcommunitiestourban- isation have foundthat richness increases withonly moderate urbanisation,decreasingwhenintensityisloworhigh(McKinney, 2008).However,weonlyfoundastronglinear,negativerelation- shipbetweenplantrichnessandhumansettlementcover.Despite this,ourresultsareinlinewithmanystudiesshowingtheneg- ativeimpactofhumansettlementsonplants(McKinney,2008).

Urbanisationnegativelyaffectsplantpopulationsbecauseitcauses asigniﬁcantincreaseindisturbance,structuralsimpliﬁcationofthe remainingvegetation,andincreasedpollution(McKinney,2008).

These factorscombine todecrease habitatareaand quality for plants.Moreover,theeffectsofthesefactorsseemtoboosttheir magnitudealongwithurbanisationlevel(McKinney,2008).

The environmental attributes of levees also significantly affectedtherichnessandabundanceofbutterflyspecies.Thefac- torsexplainedabout56%ofvariationinbutterflyspeciesand50%

ofvariation inabundanceonlevees.Themostimportantfactor shapingthediversityofbutterflies,andotherpollinatorspecies, isforagingrequirements(Pottsetal.,2005).Nativeplantspecies atleveesdidnotinfluencetherichnessofbutterfliesinourstudy area.Thismaybetheconsequenceofmobilespecies,suchassome butterflies,usingresourcesoverabroaderarea,notonlyatthescale ofalevee,notablyinintensivelymodifiedlandscapes(Ekroosand Kuussaari,2011).Shrubsnegativelyimpactbutterflyspeciesand theirabundance.Densestandsofshrubscouldlowertheappropri- atenessofleveesforpioneerorspecialistbutterflyspeciesby,for example,alteringthecompositionoffoodplants.Thepresenceof shrubsmightalsocausegreaterpredationratebybirdsofwoodlots thathuntbutterflies(LendaandSkórka,2010).Finally,mowingfre- quencyseemstobeafactorthatnegativelyimpactstheabundance ofbutterfliesonlevees.Thisfindingisinlinewithearlierstud- iesonotherlinearhabitats,indicatingthedirectnegativeimpactof mowingonfoodresourcesandmodificationofvegetationstructure (Skórkaetal.,2013;Valtonenetal.,2006).

4.3. Effectsofleveesonspeciesturnover

Distance decay of turnover for plants and invertebrates has alreadybeendemonstrated(NekolaandWhite,1999;Rouquette et al.,2013).However,nostudieshave examinedplantspecies turnoverinplant-herbivoresystemalongleveesinahighlyaltered urbanlandscape. It is known that,in a patchy urbanarea, lin- earhabitatsfacilitatemovementsofplantsandanimalsbetween sites(BeierandNoss,2008).However,theconservationvalueof corridors has also been questioned (Good, 1998). Because evi- dencefromriversasdispersalroutesforterrestrialorganismsis limited(Rouquetteetal.,2013), therole ofleveesinenhancing thedispersalofspecieswasalsobarelyknown(FreyandConve, 2006).Ourresultsshowthatleveesaffectedspatiallyturnoverfor

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Table2

Bestmodelscharacterizingplantorbutterflyspeciesrichnessandabundancebyvariablesonriverlevees.Foreachmodelthenumberofpredictors(k),varianceexplained bythemodel(r²),theAkaikeinformationcriterionscore(AICc),thedifferencebetweenthegivenmodelandthemostparsimoniousmodel()andAkaikeweight(w)are listed.Explanationsofvariablecodes:arablelandcover–arable,humansettlementcover–human,leveecover–levee,indexofmowing–mowing,speciesrichnessof nativeplants–native,speciesrichnessofnon-nativeplants–non-native,angleofslopes–angle,lengthofslopes–length,shrubcover–shrub,waterreservoircover– water,woodlandcover–wood.(↑)–positivestatisticallysignificantrelationship;(↓)–negativestatisticallysignificantrelationship.

No. Model k r² AICc w

Plantspeciesrichness

1 human(↓) 1 0.35 202.43 0.00 0.119

2 human(↓)+levee(↑) 2 0.37 204.26 1.83 0.048

3 arable(↑)+human(↓) 2 0.36 204.34 1.911 0.046

Butterﬂyspeciesrichness

1 angle(↑)+length(↑)+mowing(↓)+shrub(↓) 4 0.62 147.35 0.00 0.032

2 angle(↑)+arable(↓)+length(↑)+mowing(↓)+shrub(↓) 5 0.65 148.22 0.97 0.020

3 angle(↑)+length(↑)+shrub(↓) 3 0.57 148.41 1.16 0.018

4 shrub(↓)+wood(↑) 2 0.52 148.63 1.38 0.016

5 angle(↑)+human(↓)+shrub(↓) 3 0.56 148.67 1.42 0.016

6 angle(↑)+human(↓)+shrub(↓)+wood(↑) 4 0.60 148.99 1.74 0.013

7 human(↓)+shrub(↓) 2 0.51 149.03 1.78 0.013

8 shrub(↓) 1 0.46 149.09 1.84 0.013

9 angle(↑)+human(↓)+shrub(↓) 3 0.56 149.15 1.90 0.012

Butterﬂyabundance

1 length(↑)+mowing(↓)+shrub(↓) 3 0.46 237.00 0.00 0.039

2 human(↓)+mowing(↓)+shrub(↓) 3 0.46 237.19 0.19 0.035

3 mowing(↓)+shrub(↓) 2 0.39 237.83 0.82 0.026

4 mowing(↓)+native(↑) 3 0.44 238.13 1.12 0.022

5 angle(↑)+length(↑)+mowing(↓)+shrub(↓) 4 0.49 238.30 1.30 0.020

6 length(↑)+mowing(↓)+shrub(↓)+water(↓) 4 0.48 238.94 1.94 0.015

Table3

Estimatesofthefunctionslopesofvariablespresentinthemostparsimoniousmodelscharacterizingplantandbutterﬂyspeciesrichnessandabundancebyvariableson riverlevees.Standarderrors(SE)and95%conﬁdencelimits(CL)arealsopresented.NameofvariablesasinTable2.

Variable Importance Estimate SE Lower95%LC Upper95%CL

Plantspeciesrichness

human 0.961 −4.425 1.308 -6.988 -1.863

arable 0.277 1.326 0.383 0.576 2.076

levee 0.268 1.259 0.159 0.543 1.974

Butterﬂyspeciesrichness

shrub 0.996 −2.212 0.563 −3.317 −1.108

angle 0.557 0.960 0.300 0.373 1.548

length 0.438 1.008 0.293 0.433 1.583

wood 0.432 0.809 0.225 0.368 1.251

mowing 0.388 −0.745 0.202 −1.141 −0.348

human 0.360 −0.822 0.217 −1.248 −0.396

arable 0.279 −0.572 0.149 −0.846 −0.280

Butterﬂyabundance

shrub 0.801 −5.923 1.987 −9.818 −2.028

mowing 0.722 −4.911 1.652 −8.149 −1.674

human 0.425 −4.290 1.198 −6.639 −1.941

length 0.385 3.924 1.156 1.658 6.190

native 0.287 2.955 0.778 1.431 4.479

angle 0.278 2.561 0.690 1.209 3.914

plantspecies, suggestingthatplantscanuseleveesasdispersal pathways.Thelackofpatternsforbutterﬂiesindicatesthatthese speciesdonotuseleveesasdispersalroutes.Oneofthepossible explanationsofwhyplantspeciesusedleveestodisperseisthat seed-disseminatinganimalsmovealonglinearhabitats,especially acrossanurbanlandscape(Vittozand Engler,2007).Moreover, highlymobilespeciessuchasbirdsormammalsmaytransport seeds(epizo-andendo-zoochory)overgreatdistancesalonglinear habitatsoredges(VittozandEngler,2007).Similarly,windswhich arecommonly recorded along rivers,includingurbanised areas (Woodetal.,2013),couldpropagatewinddispersedseeds.Noneof thespeciesgroupsshowedspatialpatternsoncontrolgrasslands.

5. Conclusions

Weshowedthatdevelopmentofinfrastructuresuchaslevees alongriversmaybebeneﬁcialtobiodiversityinurbanareasbythe

creationofsemi-naturalhabitats.Thus,possiblepositiveimpactsof human-mediatedinterventioninthelandscapeshouldbecarefully identifiedand exploitedfortheconservationof plant-herbivore systems(Tryjanowskietal.,2013),especiallyinareaswherethere arenootheroptionsfornatureconservation.Leveesmanagedin suchasmannerastopreventhabitatdegradationbysubstantial shrubcover wouldbenefitopenhabitatspecies suchas butterflies.Furthermore,mowingbothslopesofaleveeatdifferenttimes mighthaveapositiveeffectonpollinatorconservation.Mowing shouldbeperformedaftertheflightseason,intemperateweather andnotearlierthanthemiddleofSeptember(Skórkaetal.,2013).

Shrubsareremovedduringregularmaintenance,apositiveside effectofwhichisthatleveesremainfavourablehabitatsformany open-habitatspecies(S ´ykoraetal.,2009).Surprisingly,leveefea- turessuchasangleandslopelengthdidnotaffectmostplantand butterﬂyspecies.Thus,theresultsshowthatleveesofvarioussizes andshapesarepossiblycomparableforthesustainabilityofplant-

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herbivoresystems.Finally,thedevelopmentofhumansettlements incloseproximitytoleveesshouldbelimited,inordertomaintain highplantdiversity.Thiswouldalsoreducethenegativeeconomic impactofﬂoodsthatregularlyoccurinthestudyarea.

Althoughthemeannumber ofinvasiveplantspecies onlev- eeswasmarginallyhigherthanonreferencegrasslands,therewas nonegativeeffectonnativeplants andbutterflies.Theabsence ofanegativeimpactappearstocontradictearlierarticlesdemon- stratingthatinvasiveplantshaveasignificant,negativeimpacton pollinators(Moro ńetal.,2009).However,invasiveplantsonlevees rarelyformdensemono-specificpatches.Whenthedensityofthe invasivespeciesislow,itmaybenefitbutterfliesbyaddingagreater varietyoffoodsaccessiblethroughouttheseason,butiftheden- sityofinvasivespeciesincreases,nativeplantsbecomeeliminated andasaresultbutterflypopulationsmightdecline(Moro ńetal., 2009).Thelackofimpactofinvasivespeciessuggestsnocurrent needforthedifficultandexpensiveeliminationofinvasiveplants fromlevees.Ontheotherhand,theinvasivespeciesthatoccuron leveesmayentersurroundinghabitats(Hongetal.,2015)andhave amorenegativeeffectonplant-herbivoresystems(Moro ńetal., 2009).

Acknowledgments

WethankBartosz Czaderforassistancein theﬁeld. Wealso thank Maciej Pabijan for comments onan earlyversion of the manuscript.Thisstudywasﬁnancedby PolishNationalScience Centreviaapost-doctoralinternship(DEC-2013/08/S/NZ8/00758).

AppendixA. Supplementarydata

Supplementarydataassociatedwiththisarticlecanbefound,in theonlineversion,athttp://dx.doi.org/10.1016/j.ecoleng.2017.04.

052.

References

Baselga,A.,Orme,D.,Villeger,S.,DeBortoli,J.,2013.PackageBetapart.

Baselga,A.,2012.Therelationshipbetweenspeciesreplacement,dissimilarity derivedfromnestedness,andnestedness.Glob.Ecol.Biogeogr.21,1223–1232, http://dx.doi.org/10.1111/j.1466-8238.2011.00756.x.

Beier,P.,Noss,R.F.,2008.Dohabitatcorridorsprovideconnectivity?Conserv.Biol.

12,1241–1252,http://dx.doi.org/10.1111/j.1523-1739.1998.98036.x.

Borcard,D.,Gillet,F.,Legendre,P.,2011.NumericalEcologywithR.Springer,New York,http://dx.doi.org/10.1007/978-1-4419-7976-6.

Bueno,J.A.,Tsihrintzis,V.A.,Alvarez,L.,1995.SouthFloridagreenways:a conceptualframeworkfortheecologicalreconnectivityoftheregion.Landsc.

UrbanPlan.33,247–266,http://dx.doi.org/10.1016/0169-2046(94)02021-7.

Burnham,K.,Anderson,D.,2002.ModelSelectionandMulti-ModelInference:A PracticalInformation-TheoreticApproach,2nded.Springer-Verlag,NewYork.

CommissionforArchitectureandtheBuiltEnvironment,2006.PayingforParks EightModelsforFundingUrbanGreenSpaces.CommissionforArchitecture andtheBuiltEnvironment,London,UKhttp://www.cabe.org.uk/AssetLibrary/

8899.pdf.

Dray,S.,Blanchet,G.,Borcard,D.,Guenard,G.,Thibaut,J.,Larocque,G.,Legendre,P., Madi,N.,Wagner,H.H.,2016.PackageAdespatial.

Dupray,S.,Tourment,R.,Pohl,R.,Schelfhout,H.,Gamst,K.,Williamson,T.,Sharp, M.,2010.InternationalLeveeHandbook–ScopingReport.

Ekroos,J.,Kuussaari,M.,2011.Landscapecontextaffectstherelationshipbetween localandlandscapespeciesrichnessofbutterﬂiesinsemi-naturalhabitats.

Ecography(Cop.)34,1–7,http://dx.doi.org/10.1111/j.1600-0587.2011.07005.x.

Fies,R.,Rabl,D.,Schulze,C.H.,Fiedler,K.,2016.Summerfloodsshapemeadow butterflycommunitiesinafloodplainnaturereserveinCentralEurope.J.

InsectConserv.20,433–445,http://dx.doi.org/10.1007/s10841-016-9876-8.

Frey,S.N.,Conve,M.R.,2006.Habitatusebymeso-predatorsinacorridor environment.J.Wildl.Manage.70,1111–1118,http://dx.doi.org/10.2193/

0022-541X(2006)70[1111:HUBMIA]2.0.CO;2.

Fukamachi,K.,Oku,H.,Miyake,A.,2005.Therelationshipsbetweenthestructure ofpaddyleveesandtheplantspeciesdiversityinculturallandscapesonthe westsideofLakeBiwa,Shiga.Japan.Landsc.Ecol.Eng.1,191–199,http://dx.

doi.org/10.1007/s11355-005-0019-8.

Good,J.,1998.Thepotentialroleofecologicalcorridorsforhabitatconservationin Ireland:areview.IrishWildl.Manuals,1–72.

Haddad,N.M.,Tewksbury,J.J.,2005.Low-qualityhabitatcorridorsasmovement conduitsfortwobutterﬂyspecies.Ecology15,250–257,http://dx.doi.org/10.

1016/j.tree.2011.08.009.

Harrison,T.,Winfree,R.,2015.Urbandriversofplant-pollinatorinteractions.

Funct.Ecol.29,879–888,http://dx.doi.org/10.1111/1365-2435.12486.

Hong,S.,Do,Y.,Kim,J.Y.,Kim,D.-K.,Joo,G.-J.,2015.Distribution,spreadand habitatpreferencesofnutria(Myocastorcoypus)invadingthelowerNakdong River,SouthKorea.Biol.Invasions17,1485–1496,http://dx.doi.org/10.1007/

s10530-014-0809-8.

Hunter,M.R.,Hunter,M.D.,2008.Designingforconservationofinsectsinthebuilt environment.InsectConserv.Divers.32,189–196,http://dx.doi.org/10.1111/j.

Jaroˇsík,V.,Konviˇcka,M.,Pyˇsek,P.,Kadlec,T.,Beneˇs,J.,2011.Conservationina city:dothesameprinciplesapplytodifferenttaxa?Biol.Conserv.144, 490–499,http://dx.doi.org/10.1016/j.biocon.2010.10.002.

Kostof,S.,1992.TheCityAssembled:theElementsofUrbanfromThroughHistory.

Thames&HudsonLtd.,London.

Kremen,C.,1992.Assessingtheindicatorpropertiesofspeciesassemblagesfor naturalareasmonitoring.Ecol.Appl.2,203–217.

Legendre,P.,Legendre,L.,1998.NumericalEcology,2nded.Elservier.

Lenda,M.,Skórka,P.,2010.Patchoccupancy,numberofindividualsandpopulation densityoftheMarbledWhiteinachangingagriculturallandscape.ActaOecol.

36,497–506,http://dx.doi.org/10.1016/j.actao.2010.07.002.

Lenda,M.,Skórka,P.,Moro ´n,D.,Rosin,Z.M.,Tryjanowski,P.,2012.Theimportance ofthegravelexcavationindustryfortheconservationofgrasslandbutterﬂies.

Biol.Conserv.148,180–190,http://dx.doi.org/10.1016/j.biocon.2012.01.014.

Martin,R.P.,Hamilton,R.B.,McKenzie,P.M.,Chabreck,R.H.,Dell,D.A.,1991.

Habitatusebysmallmammalsincoastalmarshesofsouthwesternlouisana.

Estuaries14,107–110.

McCully,P.,2007.BeforetheDeluge:CopingwithFloodsinaChangingClimate.

McKinney,M.L.,2006.Urbanizationasamajorcauseofbiotichomogenization.

Biol.Conserv.127,247–260,http://dx.doi.org/10.1016/j.biocon.2005.09.005.

McKinney,M.L.,2008.Effectsofurbanizationonspeciesrichness:areviewof plantsandanimals.UrbanEcosyst.11,161–176,http://dx.doi.org/10.1007/

s11252-007-0045-4.

Ministerstwo ´Srodowiska,2010.Diagnozaaktualnegostanugospodarkiwodnej.

Moro ´n,D.,Lenda,M.,Skórka,P.,Szentgyörgyi,H.,Settele,J.,Woyciechowski,M., 2009.Wildpollinatorcommunitiesarenegativelyaffectedbyinvasionofalien goldenrodsingrasslandlandscapes.Biol.Conserv.142,1322–1332,http://dx.

doi.org/10.1016/j.biocon.2008.12.036.

Moro ´n,D.,Skórka,P.,Lenda,M.,Ro ˙zej-Pabijan,E.,Wantuch,M.,Kajzer-Bonk,J., Celary,W.,Mielczarek,L.E.,Tryjanowski,P.,2014.Railwayembankmentsas newhabitatforpollinatorsinanagriculturallandscape.PLoSOne9,e101297, http://dx.doi.org/10.1371/journal.pone.0101297.

Nekola,J.,White,P.,1999.Thedistancedecayofsimilarityinbiogeographyand ecology.J.Biogeogr.26,867–878.

Oskanen,J.,Blanchet,F.G.,Kindt,R.,Legendre,P.,Minchin,P.R.,O’Hara,R.B., Simpson,G.L.,Solymos,P.,Stevens,M.H.H.,Wagner,H.,2013.Vegan:

communityecologypackage.In:RPackageVersion2.,pp.0–10.

Palik,E.P.,Przybyłowicz,Ł.,Kosior,A.,Król,W.,Solarz,W.,Witkowski,Z.,2005.

Changesinthespeciescompositionanddistributionofbutterﬂies

(Rhopalocera)inCracow(Poland)sincethemid-19thcentury.Fragm.Faun.48, 181–215.

Pollard,E.,Yates,T.J.,1993.MonitoringButterﬂiesforEcologyandConservation.

Chapman&Hall,London,UK.

Potts,S.G.,Vulliamy,B.,Roberts,S.,O’Toole,C.,Dafni,A.,Ne’eman,G.,Willmer,P., 2005.Roleofnestingresourcesinorganisingdiversebeecommunitiesina Mediterraneanlandscape.Ecol.Entomol.30,78–85,http://dx.doi.org/10.1111/

j.0307-6946.2005.00662.x.

Quinn,G.P.,Keough,M.J.,2002.ExperimentalDesignandDataAnalysisfor Biologist.CambridgeUniversityPress,UK.

RDevelopmentCoreTeam,2016.R:ALanguageandEnvironmentforStatistical Computing.RFoundationforStatisticalComputing,Vienna,Austria.

Rangel,T.F.,Diniz-Filho,J.A.F.,Bini,L.M.,2010.SAM:acomprehensiveapplication forSpatialAnalysisinMacroecology.Ecography(Cop.)33,46–50,http://dx.doi.

org/10.1111/j.1600-0587.2009.06299.x.

Rouquette,J.R.,Dallimer,M.,Armsworth,P.R.,Gaston,K.J.,Maltby,L.,Warren,P.H., 2013.Speciesturnoverandgeographicdistanceinanurbanrivernetwork.

Divers.Distrib.19,1429–1439,http://dx.doi.org/10.1111/ddi.12120.

S ´ykora,K.V.,Stuiver,H.J.,deRonde,I.,deNijs,L.J.,2009.Fourteenyearsof restorationandextensiveyearroundgrazingwithfreeforaginghorsesand cattleanditseffectparticularlyondryspeciesrichriverineleveegrasslands.

Phytocoenologia39,265–286,http://dx.doi.org/10.1127/0340-269X/2009/

0039-0265.

Schriever,T.A.,Ramspott,J.,Crother,B.I.,Fontenot,C.L.,2009.Effectsofhurricanes Ivan,Katrina,andRitaonasoutheasternLouisianaherpetofauna.Wetlands29, 112–122,http://dx.doi.org/10.1672/07-82.1.

Skórka,P.,Settele,J.,Woyciechowski,M.,2007.Effectsofmanagementcessation ongrasslandbutterﬂiesinsouthernPoland.Agric.Ecosyst.Environ.121, 319–324,http://dx.doi.org/10.1016/j.agee.2006.11.001.

Skórka,P.,Lenda,M.,Moro ´n,D.,Kalarus,K.,Tryjanowski,P.,2013.Factorsaffecting roadmortalityandthesuitabilityofroadvergesforbutterﬂies.Biol.Conserv.

159,148–157,http://dx.doi.org/10.1016/j.biocon.2012.12.028.

Soga,M.,Koike,S.,2013.Mappingthepotentialextinctiondebtofbutterﬂiesina moderncity:implicationsforconservationprioritiesinurbanlandscapes.

Anim.Conserv.16,1–11,http://dx.doi.org/10.1111/j.1469-1795.2012.00572.x.

(7)

Tonietto,R.,Fant,J.,Ascher,J.,Ellis,K.,Larkin,D.,2011.Acomparisonofbee communitiesofChicagogreenroofs,parksandprairies.Landsc.UrbanPlan.

103,102–108,http://dx.doi.org/10.1016/j.landurbplan.2011.07.004.

Tryjanowski,P.,Sparks,T.H.,Ku ´zniak,S.,Czechowski,P.,Jerzak,L.,2013.Bird migrationadvancesmorestronglyinurbanenvironments.PLoSOne8,e63482, http://dx.doi.org/10.1371/journal.pone.0063482.

Valtonen,A.,Saarinen,K.,Jantunen,J.,2006.Effectofdifferentmowingregimeson butterﬂiesanddiurnalmothsonroadverges.Anim.Biodivers.Conserv.29, 133–148.

Vittoz,P.,Engler,R.,2007.Seeddispersaldistances:atypologybasedondispersal modesandplanttraits.Bot.Helv.117,109–124,http://dx.doi.org/10.1007/

s00035-007-0797-8.

Wood,C.R.,Pauscher,L.,Ward,H.C.,Kotthaus,S.,Barlow,J.F.,Gouvea,M.,Lane,S.E., Grimmond,C.S.B.,2013.Windobservationsaboveanurbanriverusinganew lidartechnique,scintillometryandanemometry.Sci.TotalEnviron.442, 527–533,http://dx.doi.org/10.1016/j.scitotenv.2012.10.061.