Agricultural wetland restorations on the USA Atlantic Coastal Plain achieve diverse native wetland plant communities but differ from natural wetlands
Metthea Yepsen
a,*, Andrew H. Baldwin
a, Dennis F. Whigham
b, Eliza McFarland
b, Marina LaForgia
b, Megan Lang
caUniversityofMaryland,DepartmentofEnvironmentalScienceandTechnology,1423AnimalScienceBuilding,CollegePark,MD20740,UnitedStates
bSmithsonianEnvironmentalResearchCenter,647ConteesWharfRoad,Edgewater,MD21037,UnitedStates
cUSDAForestService,NorthernResearchStation,10300BaltimoreAvenue,Building007,Room104BARC-West,Beltsville,MD20705,UnitedStates
ARTICLE INFO
Articlehistory:
Received6October2013
Receivedinrevisedform10July2014 Accepted11July2014
Availableonlinexxx
Keywords:
Agriculture AtlanticCoastalPlain Floristicquality Restoration Vegetation Wetland
ABSTRACT
Wetlandrestorationisgloballyimportantforoffsettingeffectsofwetlandlossanddegradationbutisnot consistentlysuccessful.Vegetationstudiesprovideinsightintotheeffectivenessofrestoringwetland ecosystem functions.Wecomparedplant communitycomposition in47non-tidal wetlandsunder differentmanagement(natural,restored,andformerwetlandsthathadbeenconvertedtocropland)in the Atlantic Coastal Plain of the USA. As expected, drained cropland sites were dominated by conventionaluplandrowcrops,hadlowspeciesrichnessandevenness,andwerehighlydisturbed.Plant communitiesinrestoredsitesweremorelikenaturalsitesbasedonthepercentageofspeciesthatwere nativeandhydrophytic,plantcommunityevenness,andfloristicquality.However,naturalsiteswere forested,whilerestoredanddrainedcroplandsiteswereprimarilyherbaceous.Restoredsitescontinued tobeimpactedbyanthropogenicdisturbancecomparedtonaturalsites.Ourfindingsdemonstratethat restoredwetlandsinagriculturalsettingscandevelopdiversenativewetlandplantcommunitieswithina decadebuttheyremainverydifferentfromnaturalwetlands,raisingquestionsaboutrestorationgoals, ecosystem service tradeoffs, and ourabilitytorestore wetlands toecological conditions found in referencesites.
ã2014PublishedbyElsevierB.V.
1.Introduction
Thewetlandsoftheworldprovidemoreecosystemservicesper areathananyotherhabitattype(Costanzaetal.,1997;Doddsetal., 2008). They store and clean water, sequester carbon, provide habitatfor diverse and often rare plants and animals, and are popularrecreationspots(Doddsetal.,2008;Heftingetal.,2013;
Hubbard and Linder 1986; Millennium Ecosystem Assessment 2005;Ullah andFaulkner2005).Thelossof ecosystemservices whenwetlandsaredegradedorconvertedtootherlandusetypes iswelldocumented,asareglobalratesofwetlandlossthatrange from30to90%byregion(Dahletal.,1990,2011;Junketal.,2012;
ZedlerandKercher,2005).
Inordertoslowandreversetherateofwetlandlossandbenefit fromtheservicestheyprovide,theUnitedStatesofAmerica(USA) and manyothernationshaveimplementedprogramstoprotect andrestorewetlands.TheUSADepartmentofAgriculture(USDA), for example, provides financial and technical assistance to landowners to help protect, restore, and enhance wetlands, primarilythroughtwovoluntaryinitiatives:theWetlandReserve Program (WRP) and the Conservation Reserve Program (CRP)–Wetland Initiative. Stated objectives of WRP and CRP-Wetlands Initiative include protecting wetlands; providing habitatfor migratorybirdsandotherwetland-dependent fauna and flora; protecting and improving water quality by trapping sediment and removing nutrients; attenuating floodwater;
recharging ground water; protecting and improving aesthetics of open spaces; and contributing to education and scientific knowledge. According to the technical guidelines for wetland restorationundertheseprograms,ecosystemservicesareprovided byreturningthe“soil,hydrology,vegetationandhabitatconditions of thewetlandthat previouslyexistedonthesitetotheextent
* Correspondingauthor.Presentaddress:TheNatureConservancy,2350Route 47,Delmont,NJ08314,UnitedStates.Tel.:+16104016166.
E-mailaddress:[email protected](M.Yepsen).
http://dx.doi.org/10.1016/j.agee.2014.07.007 0167-8809/ã2014PublishedbyElsevierB.V.
ContentslistsavailableatScienceDirect
Agriculture, Ecosystems and Environment
j o u r n a l h o m e p a g e : w w w . e l s e vi e r . c o m / l o c a t e/ a g e e
practicable”. These conditions may be determined by historic documentationorthroughtheuseofareferencesite(USDANRCS Manual Title440 WetlandReserve Program, 2010; USDA NRCS PracticeStandardCode657,2010).
Conceptually, restoration is the process of returning an ecosystemtoapre-anthropogenic-disturbancestate.Inpractice, specific featuresor services are targeted for restorationrather than attempting a complete ecosystem restoration. Wetland restorationisacomplicatedprocess,inpart,becausewetlandsare regionallydistinctandthe actionsrequired torestore them to thefunctionalequivalencyofnaturalwetlandshavebeenshown tobedifficulttoprescribebroadly(ZedlerandCallaway,1999).In manycases,restorationeffortshavefailedtoreturnthebiological andbiochemicalfeaturestolevelsfoundinnaturalwetlandseven aftermanydecades(Benayasetal.,2009;Moreno-Mateosetal., 2012).Restoredwetlandsalsotendtodifferphysicallyfromtheir original condition. In the USA, for example, most non-tidal wetlandrestorationshaveresultedintheformationofpondswith afringeofemergentmarsh,regardlessofwhattypeofwetland theywerehistorically.Asaresult,fewrestoredwetlandsmatch reference conditions (Cole and Shafer 2002; De Steven et al., 2010;Kentulaetal.,1992).
In a typicalyear,allof theapproximately$500million WRP budgetandmorethan11%ofthe$1.8billionCRPbudgetarespent onwetland restorations (American Planning Association, 2010;
personal communication, Alexander Barbarika, Farm Service Agency). The return on these investments can be difficult to determineduetothecomplexityandcostofmeasuringecosystem functions. The USDA’s Natural Resources Conservation Service (NRCS) has implemented a national project to assess the effectiveness of conservation practices and programs through theConservationEffects Assessment Project(CEAP).It is under CEAPthattheresearchinthispaperwasconducted.
Due to the difficulty and expense of measuring multiple ecosystemfunctionsasmetricsofrestorationsuccess,rapidfield assessmentmethodshavebeendevelopedtofacilitatequantifica- tionofbiologicalindicatorsofecosystemintegrity(Fennessyetal., 1998,2004;LopezandFennessy,2002).KarrandDudley(1981) definedecosystemintegrityas“thecapabilityofsupportingand maintaining a balanced, integrated, adaptive community of organismshaving speciescomposition, diversity,and functional organizationcomparabletothatofnaturalhabitatsoftheregion”. Rapidfieldassessmentsare usedtodescribe overallecosystem condition,suggest probable causes of poorconditions, identify humanactivitiesthatcontributetodegradation,monitorwetland restoration trajectories, and set and assess measurable goals (CronkandFennessy,2001;Galatowitschetal.,1999).
Plants are one of the easiest and most frequently used indicators for assessing the progress of a wetland restoration (MitschandWilson,1996).Theyareadaptedtonaturalvariations inconditionsandcanreflectcurrentaswellashistoricconditions (Bedford1999; Cronkand Fennessy,2001; Wilcoxetal., 2002).
Plant communities also respond to human disturbance in predictableways.Forexample,theproportionofweedyspecies tendsto increase with human disturbanceand, given extreme disturbance,plantstendtodecreaseinsizeofindividuals,cover, andlifespan(Karr,1993).Advantagesofusingplantsasbiological indicatorsinclude:theyarepresentinmostwetlandecosystems;
theyare relativelyeasy toidentify;sampling methodsare well established; and theirrelative immobilitycreates a direct link betweenonsiteenvironmentalconditions andplantcommunity characteristics(CronkandFennessy,2001).Becauseofthesetraits, plant communities provide a good way to compare wetland conditionsunderdifferenttypesofmanagement.
We compared plant communities in two hydrogeomorphic wetland classes (depression and flat wetlands; Brinson,1993;
Brooks et al., 2011) under different management practices on the Atlantic Coastal Plain of the USA. Our goals were to (1) compare plant communities in restored wetlands and natural wetlands as well as in drained croplands that were previously wetlands, and (2) determine the degree to which eachofthehabitattypeswereimpactedbyhumandisturbance.
Specifically, we used plant speciescomposition and indicesof diversity, floristic quality, and anthropogenic disturbance to compare management practices. We expected to find differ- encesin plant communities between the habitattypes dueto their land usehistoryandbecause the group of restoredsites thatwerechosenwereonly3–11yearsinage.Eventhoughthe restored sites were relatively young, we sought to test the hypothesis that restored ecosystems are on a trajectory to having high ecosystem integrity, based upon the presence of seedlings andsaplings of speciesfound in natural sites.
2.Methods 2.1.Studysites
Forty-seven sites were selected for comparison in the USA Atlantic Coastal Plain regions of Delaware, Maryland, Virginia, andNorthCarolina (Fig.1).Thesites consistedof 14“natural” wetlands,16“drainedcropland”sites,and17“restored”wetland sites. Natural anddrainedcroplandsites were identifiedusing aerial photography and digital elevation models. They were selectedtoserveasreferencesandcontrolsforrestoredsitesby minimizing natural differences (i.e., geomorphology, soil, and geographicproximity) and maximizingland usehistory differ- ences.Naturalsiteswererelativelyundisturbedshallowwetlands characterized as either depressions or flats as described by Brinson’shydrogeomorphicclasses (1993).Theyranged insize from approximately 0.04 to 4.01ha (mean=1.58, SD=1.6;
estimatescalculatedviaremotemappingof7outof14natural sites;calculationsweredifficultduetocanopycoverandinsome cases flat terrain).Depressions andflatsare seasonallyflooded andonly occasionallyconnected toother wetlandsvia surface water.Thedrainedcroplandswereoncenaturaldepressionorflat wetlands, but had been drained hundreds of years prior to restoration for agricultural use. The restored wetlands were drainedcroplandsthathadbeenrestoredtodepressionwetlands.
Theyrangedinagefrom3to11yearssincerestorationandinsize from 0.12 to 1.13ha (mean=0.53, SD=0.38). As part of the restorationprocess,hydrology wasrestored eitherbyplugging ditches or by excavating and compacting cropland to create shallow perched water table depressions often with water retention berms. Hummocks or islands were installed in the depressions of most restored sites in order to create within- wetland microtopographicdiversity.Someof therestoredsites hadbeenplantedwithtreesandmostwereplantedwithupland grassesonbermsandinbufferareas.
2.2.Plantcommunitysurvey
Plantcommunitysurveyswereconductedonceineachofthe47 sitesfromlate Junethrough September2011at thepeak ofthe growing seasontominimize differences due to timeof year.Theareas sampledinnaturalandrestoredwetlandswerewithinthewetland boundaryasroughlydelineatedbytheplantcommunityshiftfrom wetlandtouplandplants.Ponded areas(i.e.,standing water)without vegetationwerenotsampled.Drainedcroplandsitesweresampled withinapproximately25mofthecenterofthewettestdrainedarea.
Given adequatearea, three 10m10mquadrats (adapted from Peetetal.,1998)wererandomlyselectedperplantcommunityat each site.Plantcommunities withineach wetland werevisually
determined based on the relative cover of dominant species (e.g., Phragmites australis would visibly dominate one plant community and Xanthium strumarium another). Where space allowed, quadrat locations were selected using a randomly generatedcompasspointandnumberofpacesfromthecenterof theplantcommunity.Ifspacewaslimited,quadratswereplacedso thattheywerecompletelycontainedwithintheplantcommunity, whichsometimesmeantchangingtheshapeofthe100m2sampling quadrat(Peetetal.,1998).Whenspacewasverylimited,quadrats wereplacedsoasnottobeoverlapping,whichsometimesresulted infewerthanthreequadratsperplantcommunity.Wesampledall plantcommunitieswithineachwetlandboundary andsurveyedthe siteoutsideofthequadratstocapturespeciesthathadnotbeen sampledin thequadrats.Inordertoensureadequate sampling, quantitativecoverdataforalldominantplantsand90%ormoreof thespeciesineachsitewerecapturedinthequadrats,thelatter basedon thesurveys ofspecies that wereat each sitebut not encounteredintheplots.
Eachspecieswithina100m2quadratwasassignedapercent coverclass(trace,0–1,1–2,2–5,5–10,10–25,25–50,50–75,75–95, or>95;classmidpointswereusedin dataanalysis) (Peetetal., 1998).Coverwasusedratherthannumberofindividualsbecauseit wasmoreequitablewhencomparingtreeandherbspecies.Any plantsthatcouldnotbeidentifiedtospecieslevelinthefieldwere collected, pressed, dried, and later keyedout using Brown and Brown(1972,1984);GleasonandCronquest(1991);Radfordetal.
(1968). Plant nomenclature is according to the USDA Plants Database (USDA NRCS, 2012). Approximately 23% of plant observationscouldnot beidentifiedtospeciesdue toa lackof flowering or fruiting material and were not included in calcu- lationsthatrequiredspecieslevelidentification.
2.3.Commonanddominantspecies
Common plant species weredefined as those that occurred withinquadratsat 40%ormoreof natural,restored, ordrained Fig.1.Mapofstudysites.MapofstudysitesbycountyinDelaware,Virginia,Maryland,andNorthCarolinaontheeasterncoastoftheUnitedStatesofAmerica.
croplandsites.Dominantplantspecieswithineachsitetypewere defined asthosethathad coverof20%orhigherinthesitesin whichthey werefound.Percentcoverof aspecies and percent coverofwoodyandherbaceousspeciesateachsitewerecalculated as the average of the species’ cover across all quadrats at the site,with0%coverassignedinquadratswherethespecieswere notfound.
2.4.Indices
Natural,restored,anddrainedcroplandswerecomparedusing 9vegetationindicescommonlyusedtodeterminedifferencesin wetland condition. The indices (described in Table 1) were calculated from the quadrat cover data and the presence of speciesfoundinsideandoutsidethequadrats.Themeanofeach indexwasaveragedforeachtypeofsite.
2.5.Statisticalanalysis
Statistical comparisons of natural, restored, and drained cropland sites were made using analysis of variance (ANOVA) performed using the MIXED procedure in SAS version 9.2 (SASInstitute, Cary,NC).Significancewasassignedforp<0.05.
Arithmetic mean and standard error were calculated using MEANSprocedureinSAS.Regressionswerecalculatedusingthe REGprocedureinSASand SigmaPlot(SystatSoftware,SanJose, CA)comparing(1)theAnthropogenicActivityIndex(AAI)tothe Floristic Quality Assessment Index (FQAI), (2) AAI to Floristic Assessment Quotient for Wetlands (FAQWet) scores, and(3)timesincerestorationtopercentcoverbywoodyspecies inrestoredsitestodetermineifsuccessionwas takingplace in restoredsites.
Variationinplantcommunitiesbetweensitesandtheirrelation to metrics of diversity, quality, and disturbance were also examined using non-metric multidimensional scaling (NMS) analysis. Sørenson distance measures were used and Beal’s smoothingwasappliedtovegetationdatatoachieveafinalstress
valuenear10(McCuneand Grace,2002).Significantdifference betweenwetlandtypeswastestedusingmulti-responsepermu- tation procedures (MRPP). Both NMS and MRPP analyses were conductedusingPC-ORDv.6(MjMSoftware,Gleneden,OR).Joint plotswerepreparedtovisualizesitescoresrelativetovectorsof plantcommunityanddisturbancemetrics.
3.Results
3.1.Plantcommunitycomposition
Atotalof204specieswereobservedacrossthethreesitetypes with71speciesfoundinnaturalsites,134inrestoredsites,and34 in drained cropland sites. Four species (Hypericum mutilum, Phytolacca americana, Diospyros virginiana, and Liquidambar styraciflua)werefoundatallthreetypes ofsites.Therewas no overlapindominantspeciesbetweensitetypesandlittleoverlap in commonspecies (Fig.2).Woodyspecies accountedfor more than 70% of the cover in the natural sites, typically from L. styraciflua, Acer rubrum, and Nyssa biflora (Fig. 2A). These specieswerealsofoundinamajorityofnaturalsitesandshadedan understoryshrubandsmalltreestratum,whichcontainedspecies such as Clethra alnifolia, Smilax species, Eubotrys racemosa, Magnoliavirginiana,andvariousVacciniumspecies.
Bycontrast,only10%ofcoverinrestoredsiteswasfromwoody species and there was more variation in plant community composition between sites. While woody species such as L. styraciflua and A. rubrumwere found in 30–50% of restored sites, they averaged <1% cover. Echinochloa crus-galli, X. strumarium, Scirpus purshianus, P. australis, and Mollugo verticillatawerefrequentlyfoundinrestoredstiesandtendedto haverelativelyhighcover(Fig.2B).Only7herbaceousspecieswere foundinbothrestoredandnaturalsites.Ofthosesevenspecies, only Scirpus cyperinus and Woodwardia virginica werefoundin more than one site of each type. Drained cropland sites were dominatedbyconventionalrowcropsofZeamays,Glycinemax, Gossypiumhirsutum,orSorghumbicolor(Fig.2C).
Table1
Summaryofvegetationanddisturbanceindicesused.
Index Description
Shannon–Weinerevennessindex TheShannon–Weinerevennessindexwascalculatedforeachsitebasedonthespeciesrichnessandcoverofthespeciesfound inquadrats.Itisusedasanindexthatcombinesdiversityandevenness.Itiscalculatedas[sum(ACln(TC)]/ln(SR);whereACis theaveragecoverofeachspeciesfoundinquadratsatthesitewith0%coverassignedinquadratswherethespecieswasnot found;TCisthesumofallACvaluesfoundpersite;andSisnumberofspeciesfoundinquadratsatthesite(Gurevichetal., 2006).
Speciesrichness Thetotalnumberofspeciesfoundineachsite.
Wetnesscoefficient(WC) Valueassignedtoplantspeciesbetween5(alwaysoccursinnon-wetlanduplandareas)and+5(alwaysoccursinwetlands).
BasedonregionalU.S.FishandWildlifeServiceWetlandIndicatorStatus(Ervinetal.2006;LichvarandKartesz,2009).
Coefficientofconservatism(CC) Valueassignedtoplantspeciesbetween0(non-nativeorweedyspeciesthattoleratedisturbanceandarefoundinwidevariety ofconditions)and10(nativespeciesthatareonlyfoundinspecificundisturbedconditions)(ChamberlainandIngram,2012).
Proportionofwoodyspecies Thepercentofspeciesfoundineachsitecharacterizedaswoody(asopposedtobeinganherborvine)(USDAPlantsDatabase).
Proportionofnativespecies Thepercentofplantsidentifiedtospeciesfoundineachsitethatwerenative(USDAPlantsDatabase).
FloristicQualityAssessmentIndex (FQAI)
Sitewideindexbasedonnativespeciesrichnessandcoefficientsofconservatism.Alowscoreindicateslownativespecies richnessand/orspeciesthattolerateawiderangeofconditionsanddisturbance.Ahighscoreindicateshighnativespecies richnessandplantsthatareonlyfoundunderspecificconditionsanddonottoleratedisturbance.CalculatedasFQAI=R/p
N;
whereRisthesumofthecoefficientsofconservatismforallspeciesfoundatasiteandNisthenumberofnativeplants identifiedtospeciesineachsite(developedfromAndreasetal.,1995;Ervinetal.,2006;LopezandFennessy,2002).
FloristicAssessmentQuotientfor Wetlands(FAQWet)
Sitewideindexbasedonspeciesrichness,speciesnativeness,andwhetherthespeciesaremorecommonlyfoundinwetlandor uplandareas.Alowscoreindicateslownativespeciesrichnessand/ornon-wetlandspecies.Ahighscoreindicateshighnative speciesrichnessandplantsthatarealmostalwaysfoundinwetlands.FAQWethastheadvantageofusingwetnesscoefficients, whichhavebeendevelopedforallregionsoftheUSA,ratherthancoefficientsofconservatism,whichhavenot.Theotherway thatFQAIandFAQWetdifferisthattheFAQWetequationplacesaheavierweightonnon-nativeplantspecies.Bothindicesare influencedbyspeciesrichness.TheFAQWetscoreforeachsitewascalculatedasFAQWet=(SumWC)/(p
S)(N/S);whereWCis thewetnesscoefficientvalueassignedtoeachspecies,Sisthespeciesrichnesspersite,andNisthenumberofnativespeciesat eachsite(Ervinetal.,2006;Hermanetal.,1997;Reed,1988).
AnthropogenicActivityIndex(AAI) AAIisanindexforqualitativelyassessinghumandisturbancebasedonobservationsduringsitevisits.TheAAIrateswetlands onascaleof0–3forfiveconditions:landuseintensityina500mbuffer;intactnessandeffectivenessofa50mbuffer;
hydrologicalteration;habitatalteration;andhabitatqualityandmicrohabitatheterogeneity(Ervinetal.,2006).
3.2.Indexvariationbetweensitetypes
Formostindices,restoredsitesweremoresimilartonatural sitescomparedtodrainedcroplands(Fig.3).Naturalandrestored sites had similar proportions of native species and evenness (Fig.3CandD).Naturalsites,however,hadasignificantlyhigher proportion of woody species, higher FQAI scores, and lower anthropogenic disturbance (Fig. 3B, G, and I). Restored sites,
comparedtonaturalsites,hadsignificantlyhigherspeciesrichness andtheplantspeciesweremorewetlandspecific(Fig.3AandE).
There was a stronger negativecorrelation betweenAAI and FQAI than AAI and FAQWet scores, but both were significant (R2=0.65 and 0.30, respectively, p<0.001; Fig. 4A and B). The correlationbetweenpercentcoverbywoodyspeciesandnumber of years since restoration in restored sites was not significant (R2=0.24,p=0.17;Fig.5).
0 10 20 30 40
*Diospyros virginiana
*Vacc* Morella ceriferainium fuscatum *Pinus taeda
*Partheno*Vacc*Toxicoden*Liquida*Smil WoodWood*Eubociss*Magno*Smilinium corymbo*Que*Vitis rotundax glau*Clethra alnifolimbawardia areous quwardia virginicatrys*Nyssax rotunddron*Acer rubrumrcus phelllia virginianr styraciflua*Ilex opa racemosainqueca Walter rada bifloraifoliicanfoliifolilata sumos caa a saaa
Symbols: Relative frequency (%)
0 20 40 60 80 100
A
Restored
0 10 20 30 40
Species
ApocynuJunEleom cannabcus secunducharis ovainumtas Polygonum cespitosum Polygonu*LiquidaAmbrosia artemisiiEchinoXanBoehSolanuPhragmites auScirpum hydropMollugo veTyphaScirpuLudwigia pathium strumariummbameria cylindJunchloam carolinen*Acer rubrums cype anr styracifluas pucus effBiden crus-gallipegustifolirticillrshiauroidestralilustrisrinus sp.ususfoliricaatases sassai
0 20 40 60 80 100
Natural
B
Drained
Bars: Cover (%)
0 20 40 60 80 100
Morus rubra Sorghum bicolor EchinoAmaranGoss IpomoeaIpoLudwigia paypium hirsutumchloamoeathus spino crus-gall lacuno purpulustrissusreasai CommAmaranPhytolacc XanSolanuChenopod IpoPortulaca oleracea Mollugo vethium strumariummoeaelinathum carolinenSida Glycs retroflexusa american commun hedeZeaium albu spinorticilline maysracea maxsa atais sema
0 20 40 60 80 100
C
Fig.2. Commonandfrequentspecies.Averagecoverandfrequencyofthemostcommonplantspeciesfoundin(A)natural,(B)restored,and(C)drainedcroplanddepressional wetlandsintheUSmid-AtlanticCoastalPlain.Theplantspecieslistedarethe20mostfrequentspecieswiththehighestaveragepercentcoverinthesitesinwhichtheywere found.Plottedcovervaluesaremean+1SE.*woodyspecies.Dotsrepresentfrequencyandbarsrepresentaveragepercentcover.
3.3.Community–indexrelationships
The NMSordination indicatedthatplantcommunities in the threetypesofsitesweresignificantlyseparatedfromeachother (MRPPA-statistic=0.35,p<0.0001;Fig.6).Axes1and2cumula- tivelyexplained 87.6% of the variation in species composition.
Positionandlengthofdisturbanceandcommunitymetricvectors indicatethatthenaturalsitestendedtobeundisturbed(lowAAI) anddominatedbywoodyspeciesandnativeplantcommunitiesof highfloristicquality(highFQAIandcoefficientsofconservatism).
Drainedcropland sites were, in contrast, highly disturbed and dominated by non-native, herbaceous, and low-floristic-quality communities(i.e.,cropmonocultures). Restoredsitestended to havemorediverseplantcommunitiesthannaturalsitesandwere clearlydominated bywetland plantspecies. Therestoredsites, however,hadlowerfloristicqualityindexvaluesandhadalower proportionofnativespeciescomparedtonaturalsites.
4.Discussion
4.1.Speciesrichnessandevenness
Despite thepresence of a larger number of non-native and opportunistic species, restored sites had the highest species richness and evenness that matched natural sites, a finding consistentwithstudiesofrecentlyrestoredfreshwaterwetlands
(Balcombeetal.,2005;Fickenand Menges2013;Gutrichet al., 2009;Matthewsetal.,2009).Higherspeciesrichnessmaybedue tothemixofnewhydrophyticspeciesandtheexistingseedbankof weedyspeciesthatwerepresentduringtheperiodoftimethatthe sites were farmed. Although matching the species richness of referencesitesis acommonmanagement goal,species identity must be considered to determine whether richness indicates ecological health or degradation. Species richness may be increased by the presence of weedy and invasive species, by removingnutrientlimitationsthroughtheadditionofpollution,or bycreatingmoremico-habitatswhereuplandspeciescancolonize (Ehrenfeld,2000;EhrenfeldandSchneider,1993).
4.2.Floristicquality
Floristicquality indicesincorporate plant speciesidentity as wellasrichness,allowingfor meaningfulcomparisonsbetween sites (Lopez and Fennessy, 2002). Although we recognize that coefficients of conservatism have not been developed for all regionsoftheUSAandarenotusedinothercountries,ourfindings suggestthattheFQAIindexispreferabletotheFAQWetindexfor comparingfloristicqualitybetweenrestoredandnaturaldepres- sions.ThisisbecauseFAQWetscoresarebasedonnativespecies richnessandspeciestoleranceforwetlandconditions.Likespecies richness,ahigherFAQWetscoremayindicateamorediverseand nativewetlandplantcommunityoritmayindicatehighlyaltered B
Woody species (%)
0 20 40 60 A 80
Species richness per site
0 5 10 15 20 25
30 C
Shannon Evenness Index
0.0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
D
Native species (%)
0 20 40 60 80 100 120
E
Site type
Wetness Coefficient
-3 -2 -1 0 1
2 F
Coefficient of Conservatism
0 1 2 3 4 5 a
b
c
a
b c
a a
b
a a
b
b a
c
a b
c
G
Natural Restored
Drained
FQAI
0 2 4 6 8 10 12 14 16
18 a
b
c
H
Natural Restored
Drained
FAQWet
-2 0 2 4 6 8
a a
b
I
Natural Restored
Drained
Anthropogenic Activity Index
0 2 4 6 8 10 12 14 16
c b
a
Fig.3. Indices.Plantcommunitymetricsfornatural,restored,anddrainedcropland(“Drained”)depressionalwetlandsoftheUSmid-AtlanticCoastalPlain.Plottedvaluesare mean+1SE;meanswithdifferentlettersrepresentstatisticallysignificantdifferences(Tukey,p<0.05).(A)Speciesrichnesspersite(numberofspecies)(F2,44=38.7, p<0.0001);(B)percentofspeciesthatwerewoody(F2,44=183.8,p<0.0001);(C)Shannonindexofspeciesevenness(F2,44=77.15,p<0.0001);(D)percentofspeciesthat werenativetotheUSA(F2,44=35.66,p<0.0001);(E)wetnesscoefficient(rangesfrom5forspeciesthatarealwaysfoundinwetlandsto5forspeciesthatareonlyfoundin wetlands;F2,44=35.66,p<0.0001);(F)coefficientofconservatism(rangesfrom0to10,with10assignedtospeciesleasttolerantofdisturbedconditions;F2,44=97.50, p<0.0001);(G)FloristicQualityAssessmentIndex(FQAI) (F2,44=115.99,p<0.0001;(H)FloristicAssessmentQuotientforWetlands Index(FAQWet) (F2,44=24.65, p<0.0001);(I)AnthropogenicActivityIndex(F2,44=137.46,p<0.0001).
hydrology,wheretherestoredwetlandiswetterthannaturalsites duetoanthropogenicmanipulation(Ervinetal.,2006),acondition weobservedinourstudysites.
AnotherpotentialproblemwithFAQWetisthatifitwasagood indicatorofecosystem integrity,wewouldexpecta correlation betweentheindexscoresandthelevelofhumandisturbanceata siteasindicatedbyAAI.SimilartoTietjenand Ervin(2007),we found that FAQWet was not significantly correlated with AAI, indicating that FAQWet is not a good indicator of ecosystem integrity.Bycontrast,FQAIhasbeenfoundbyourstudyandothers tobestronglycorrelatedwithanthropogenicdisturbancessuchas agricultural land use, fragmented vegetation buffers, altered hydrology, and long distances between wetlands (Lopez and Fennessy, 2002). This is likely because the coefficients of conservatismusedinFQAIarebasedonhowspecificthespecies’ habitatrequirementsareanditstoleranceofdisturbancerather thanwhetherornotthespeciesiswetlandspecificasisthecasefor FAQWet. Thus, FQAI may inherently be a better measure of ecosystemintegrity.
4.3.Anthropogenicdisturbance
Restoredwetlandscontinuetohavemoresignsofhistoricand ongoinganthropogenicdisturbancethannaturalsitesasevidenced byhigherAAIscores.Historicimpactsincludelargeareasofopen waterthatresultedfromrestorationmethodsandproximitytoroads andagriculturalfields.Ongoingdisturbancesobservedatrestored sitesincludedactivemowingandinsomecasesdigging.Ecosystem integrityisthoughttobeinverselyrelatedtohumandisturbance because disturbances can upset ecosystem balance bychanging Fig.4. Disturbanceandfloristicquality.Relationshipbetween(A)FloristicQuality
AssessmentIndex(FQAI)andAnthropogenicActivityIndex(AAI)scoresassignedto eachsite(p<0.001,R2=0.65)and(B)FloristicAssessmentQuotientforWetlands (FAQWet)andtheAAI(p<0.001,R2=0.30).
Fig.5.Restorationageandsuccession.Relationshipbetweenthenumberofyears sincerestorationandthepercentcoverofwoodyspeciesinrestoredsites.
Fig.6.Non-metricmultidimensionalscaling.Resultsofnon-metricmultidimen- sionalscaling(NMS)ordinationofplantcommunitiesofnatural,restored,and drainedcroplandwetlandsites.Plantcommunitiesofthethreesitetypesdiffered significantly(MRPP,A=0.35,p<0.0001).Thedirectionandlengthofvectorsreflect therelationship ofplantcommunitiestocommunityanddisturbancemetrics (AAI=AnthropogenicActivityIndex;CC=coefficientofconservatism;evenness= Shannonindexofspeciesevenness;FAQI=FloristicQualityAssessmentIndex;
FAQWet=FloristicAssessmentQuotientforWetlands;herbaceous=absolutecover of herbaceous plant (%); native=proportion ofspecies that were native (%);
RichPlot=numberofspeciesper100m2plot;RichSite=numberofspeciesinthe entire wetlandsite; WetCoeff=wetnesscoefficient; woody=absolutecover of woodyplants(%).
nutrientcycling,photosynthesis,hydrology,competition,predation, andmore(DeLeoandLevin,1997;LopezandFennessy,2002).
4.4.Differencesinplantcommunitycomposition
Given enough time, the structure and function of restored wetlands shouldbecome more like natural sites, although this processmaytake100years ormore(MitschandWilson,1996;
Moreno-MateosandComin,2010).Therestoredwetlandssampled inthisstudywerecomparativelyyoung(i.e.,sampled3–11years postrestoration),butweanticipatedthattheoldestwouldhave increasedcoveranddensitybythewoodyspeciesfoundinnearby referencesites.Thisassumptionwasbasedonastudyofrestored wetlands that were similar to ours as well as predictions of successionbasedonthe growthrates of commonwetlandtree species(DeStevenetal.,2006,2010;USDAPlantsDatabase).De Stevenetal. foundthat thecoverof woodyspeciesin restored wetlandsaveraged40%after5yearsandthatrestoredsiteshad 53% of species in common with forested reference sites. In addition,thecommontreespeciesfoundinthenaturalsiteswe sampledcangrow0.6mormoreperyear(USDAPlantsDatabase 2014).Incontrast,wefoundthatrestoredsiteshadveryfewofthe woody species found in natural sites and that there was no correlationbetweenthetimesincerestorationandpercentcover of woody species. Several explanations could account for the differencesbetweenourpredictionsandourfindings.
Sincefewoftherestoredsiteswereplantedwithwoodyspecies andthemajorityofthetreesthatwereplantedwerenotthesame speciesfoundin thenatural sites(e.g.,Platanusoccidentalisand Taxodiumdistichumwerenotfoundinnaturalsites),seedbanks andseeddispersalremainasthemajorsourcesofpropagulesin restoredwetlands. However, the seed banks of farm fields are dominatedbyherbaceousspeciesandtendnottocontainwoody species(DeStevenetal.,2006;Middleton,2003).Evenifviable seedsofnativespecieswerepresentintheseedbankatthetime thesiteswererestored,manyofthemwouldhavebeenremoved duringrestoration,asacommonpracticeistoremovetopsoilto create a depressions and use the excavated material to create berms,thus,reducingthepotentialimportanceoftheseedbankin restoringnativespeciesdiversity.
Because restored wetlands in agricultural areas are often surroundedbyfarmfieldsratherthanforestedwetlands,dispersal limitationofthepropagulesofwoodyspeciesmayexplaintheir lowerabundanceinrestoredwetlands(HeraultandThoen,2009;
Kettenring and Galatowitsch, 2011; Middleton, 1999, 2003).
Depressionsandflatsareespecially isolatedbecausetheyrarely receiveoverlandflowofwaterfromotherwetlands,whichleaves wind transport as the major remaining source of woody propagules. Dispersal of seeds from woody species declines exponentially from forest edges into clearings (Greene and Johnson,1996).Clewell and Lea (1990) suggestedthat wetland restorationsiteswithintwotreeheightsofaforestcomposedof maturetreeswouldhavethemostsuccessfulnaturalregeneration of early colonizers like L. styraciflua and A. rubrum. Thus, the availabilityof propagules in the restoredsites we studied was potentiallylimited by prior land use, restoration methods, and isolationfrompropagulesources.Thissuggeststhatmore-active managementandplantingmayberequiredforplantcommunities inrestoredwetlandstomorecloselyresemblenaturalwetlands.
Hydrologicdifferencesbetweenrestoredandnaturalsitesmay beanotherexplanationfordifferencesinplantcommunities.Long- termchangesinthelandscape,likeditchingandover-extractionof groundwater,maypreventtherestorationofhydrologytopre- disturbanceconditions(Zhengetal., 1988).Asdescribedabove,itis commontoremovetopsoilduringrestorationandcompactsubsoil withequipmentinordertoensurethatthedepressionsholdwater.
Thispracticecreatespondedconditionsandlikelyalterssurface– groundwaterconnectivity,leadingtolongerand deeperhydro- periods. Field observations support this hypothesis, as many restoredsiteshadpondedwaterinthesummerwhenallbutthe largestnaturalsitesweredry.
Hydroperiodplaysan importantrole in determiningspecies composition.Herbaceouswetlandspeciesareonlyabundantinthe naturaldepressionwetlandsinourstudyareawhentheyarelarge enoughtohaveadeepercentralzonewherewaterdepthspreclude the establishment of woody species (Tyndall et al., 1990;
Verhoevenetal.,1994).Forestedwetlands existonlywherethe hydroperiodislonganddeepenoughtoexcludeuplandspecies, butnotsowetastokilltrees(Lugo,1990).Inonestudy,higher cover by woody plant species was correlated with shorter hydroperiods 5 years post-restoration (De Steven et al., 2010).
Thus,restoredsitesmayhavelackedwoodyspeciesforavarietyof reasons(i.e., seedavailability, longerhydroperiods withdeeper water).Ifthisisthesituation,wewouldexpectthatwoodyspecies wouldfirstcolonizerestoredwetlandsneartheupland–wetland boundarywherefloodingdepthislessandsoilsaremorelikelyto beexposedduringdryperiods.Thissituationhasoccurredina separatesetofrestoredwetlandsintheAtlanticCoastalPlainthat were initially sampled in the mid-1990s and again in 2011 (D. Whigham and L. McFarland, personal observation, and unpublisheddata).
Onefinalexplanationastowhyrestoredsitesremainedlargely dominated by herbaceous species is continued anthropogenic disturbance. Many sites were regularly mowed and some had evidence of recent disturbance by heavy machinery. Regular mowingandsoildisturbanceareeffectivemethodsforpreventing theestablishmentofwoodyspecies.
4.5.Restorationandmanagementgoals
Mostoftherestoredwetlandssampledwererestoredunder eitherWetlandReserveProgram(WRP)orConservationReserve Program(CRP), both of which usetheUSDA Natural Resources Conservation Service (NRCS) Practice Standard Code 657. The practice standard defines wetland restoration as the return of vegetation, soils, and hydrology to pre-human disturbance conditions to the extent possible so as to “restore wetland function, value, habitat,and diversity”. NRCSPractice Standard Code657allowsfornomorethan30%oftherestoredwetlandarea tobeaplantcommunitydifferentfromwhatwouldhaveexisted pre-disturbance,butnotimeframeisgivenastowhenthisshould bereached.Noneoftherestoredsitessampledforthisstudymet thedesiredcondition.However,thereissomeambiguitytothese guidelinesbecauseanherbaceouswetlandcommunityisconsid- eredtobeanacceptableprecursortoaforestedwetlandandcanbe maintainedasaherbaceouscommunityforCRPrestorations,but notunderWRP(personalcommunication,SteveStrano,NRCS).Itis possiblethattheseallowancesaremadeinpartduetolandowner preference,sincetheWRPandCRParevoluntaryandwilltailor implementation to meet landowner expectations within USDA guidelines.Forafewreasons,landownersmaynotbeinterestedin having a forested wetland on their property: (1) it may be consideredlessaestheticallypleasingandblocktheview(Clewell andLea,1990)and(2)forestedwetlandhabitatmaynotattract waterfowlforhuntingorbirdwatchingaswellasanopenpond withherb-dominated edges.Thus, it is likely that some of the restored sites were never designed to transition into forested wetlandsthataresimilartothenaturalwetlands.Forthisreason,it maybebeneficialtore-examinethedefinitionandgoalsofUSDA wetland restorations to ensure that restoration techniques are tailored to unambiguous, measurable, and realistic restoration goalsthathaveastatedtimeframeforbeingreached.
Althoughrestoredsitesmaynotprovidethesamefunctionsas naturalsitesduetotheirstructuraldifferences,theyarestilllikely toprovidemanyoftheservicesassociatedwithwetlandsandmeet broadCRPand WRPgoals.Asemergentwetlands dominatedby herbs,grasses,andsedges,themajorityofrestoredsitesprovide foodandhabitatformigratorybirdsandwaterfowl,albeitdifferent speciesthanaforestedwetland.Therestoredsitesalsosupport diversenativewetlandplantcommunities.Thehydrogeomorphic status(i.e.,depressional class)of therestoredsitesalsoassures improvedwaterqualityviasedimentationanddenitrification,but restoredsitesarelesslikelytorechargegroundwaterduetotheir perched water tables (Ator et al., 2013; Bruland et al., 2003;
Tanner et al.,2005).The depressionalwetlands, throughwater storage and reduction of flow velocity, would also reduce downstream flooding. Due to their proximity to houses and agriculturalfields, restoredsites mayeven providemoreof the servicesvaluedbylandownersthandonaturalsites.
5.Conclusions
RestoreddepressionalwetlandsinagriculturalareasoftheUSA AtlanticCoastalPlainhavedevelopeddiversenativewetlandplant communities that are likely to provide many of the broad functional benefits targeted by the federal programs that supportedtheirimplementation.However,wehypothesizedthat restoredsites,especiallythosethathadbeenrestoredforadecade, wouldshowsignsofwoodyspeciesestablishment,demonstrating thattheirplantcommunitieswereonatrajectorytowardthatof naturalsites.Thishypothesiswasnotsupported;after3–11years, thetreeandshrubspeciesthatoccurredinnaturalwetlandswere notrepresentedinrestoredwetlands.Thus,withoutachangein management,itisunlikelythatplantcommunitiesofrestoredsites willconvergetobesimilartonaturalwetlands.Ambiguityinthe goals and guidelines in the federal restoration documentation makeitdifficulttodeterminewhetherornottheseprojectswere intendedtoreturntopre-anthropogenicdisturbanceconditions.
Itis importanttorecognize thatalthough theserestorations provideimportantecosystemservices,wetlandsofdifferenttypes inherently provide different services. We need to consider the landscape scale effect of this shift from forested wetland to croplandtoherbaceouswetlandsonresultantservicesandthen clearlydefineourrestorationgoals andobjectives basedonthe needsofa givenarea.Thelackof establishedgoals andsuccess criteriaisawell-documentedprobleminwetlandrestoration.In ordertodemonstratethatenvironmentalrestorationisareliable tool,itisimperativethatoutcomesmatchstatedgoals.Thegoals and objectives of a wetland restoration must be site specific, measurable,andhaveastatedtimeframeforwhenthegoalsare expectedto beachieved. Thesegoals and objectives should be documented and used toinform the entire restorationprocess fromselectingrestorationmethodstoprojectevaluation.
Acknowledgements
This project was funded by the USDA’s Natural Resources ConservationService(NRCS) aspartof theConservationEffects Assessment Project (CEAP). Thank you to the landowners for participatinginthestudyandtoStephanieYarwoodforhelpwith multivariateanalyses.
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