J Appl Ecol. 2018;55:299–310. wileyonlinelibrary.com/journal/jpe | 299

Received:4January2017  |  Accepted:26April2017DOI:10.1111/1365-2664.12929

R E S E A R C H A R T I C L E *

Legacy effects of diversity in space and time driven by winter cover crop biomass and nitrogen concentration

Janna M. Barel1  | Thomas W. Kuyper1 | Wietse de Boer1,2 | Jacob C. Douma3,4 |  Gerlinde B. De Deyn1

1SoilBiologyandBiologicalSoilQuality,WageningenUniversity&Research,Wageningen,TheNetherlands2MicrobialEcology,NetherlandsInstituteforEcology(NIOO-KNAW),Wageningen,TheNetherlands3CentreforCropSystemsAnalysis,WageningenUniversity&Research,Wageningen,TheNetherlands4LaboratoryofEntomology,WageningenUniversity&Research,Wageningen,TheNetherlands

CorrespondenceJanna M. BarelEmail: janna.barel@wur.nl

Funding informationNederlandseOrganisatievoorWetenschappelijkOnderzoekVIDI,Grant/AwardNumber:grantno.864.11.003

HandlingEditor:LeiCheng

*PaperpreviouslypublishedasStandardPaper.

Abstract1. Plantdiversitycanincreasenitrogencyclinganddecreasesoil-bornepests,whichare feedback mechanisms influencing subsequent plant growth. The relativestrength of thesemechanisms is unclear, as is the influence of preceding plantquantityandquality.Here,westudiedhowplantdiversityinspaceandtimeinflu-encessubsequentcropgrowth.

2. During2years,werotatedtwomaincrops (Avena sativa,Cichorium endivia)withfourwintercovercrop(WCC)speciesinmonoculturesandmixtures.Wehypoth-esizedthat,relativetomonocultures,WCCmixturespromoteWCCbiomass(quan-tity)andnitrogenconcentration(quality),soilmineralnitrogen,soilorganicmatter,and reduce plant-feeding nematode abundance. Additionally, we predicted thatprecedingcropsmodifiedWCClegacies.Bystructuralequationmodelling(SEM),wetestedtherelativeimportanceofWCCshootbiomassandnitrogenconcentra-tiononsucceedingcropproductivitydirectlyandindirectlyvianitrogencyclingandroot-feedingnematodeabundance.

3. WCCshootbiomass,soilpropertiesandsucceedingAvenaproductivitywereaf-fectedbyfirst-seasoncropping,whereassubsequentCichoriumonlyrespondedtothe WCC treatments. WCC mixtures’ productivity and nitrogen concentrationshowedover-andunder-yielding,dependingonmixturecomposition.SoilnitrogenandnematodeabundancedidnotdisplayWCCmixtureeffects.SoilorganicmatterwaslowerthanexpectedafterRaphanus sativus + Vicia sativamixture.SubsequentAvenaproductivitydependeduponmixturecomposition,whereasfinalCichorium productivitywasunresponsivetoWCCmixtures.SEMindicatedthatWCClegacyeffects on subsequent Avena (R2=0.52) and Cichorium (R2=0.59) productivitywere driven byWCC biomass and nitrogen concentration, although not by thequantifiedsoilproperties.

4. Synthesis and applications.Throughunderstandingplant–soil feedback, legacyef-fectsofplantspeciesandspeciesmixturescanbeemployedforsustainableman-agement of agro-ecosystems. Biomass and nitrogen concentration of plantsreturned to the soil stimulate subsequent plant productivity.Winter cover cropquantityandqualityarebothmanipulablewithmixtures.Thespecificityofspatial

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,providedtheoriginalworkisproperlycited. ©2017TheAuthors.Journal of Applied EcologypublishedbyJohnWiley&SonsLtdonbehalfofBritishEcologicalSociety

300  |    Journal of Applied Ecology BAREL Et AL.

1  | INTRODUCTION

Studies on plant diversity in space (diversity experiments) and time(plant–soilfeedback,PSF)aremostlyexecutedinnaturalecosystems.Agro-ecology could greatly benefit from this knowledge as an eco-logical basis for sustainable management (Dias, Dukes, & Antunes,2014;Woodetal.,2015).Althoughsoil-mediated influencesofpre-cedingonsucceedingplants isanestablishedphenomenon (Tilman,2001;VanderPutten,Bradford,PernillaBrinkman,vandeVoorde,&Veen,2016),howand towhatextent legacyeffectsofdiversity in-fluence subsequent-plant growth is unresolved. Biodiversity experi-mentsshowedthatnichedifferentiationallowsmixturestobemoreproductivethantheaverageoftheircomponentmonocultures(Loreau& Hector, 2001; Tilman, 2001). Additionally, mixtures promote thebuild-up of soil C- andN-stocks (Cong etal., 2014;DeDeyn etal.,2009),andreducepestpressure(Iversonetal.,2014;Schnitzeretal.,2011),formingpotentialfeed-backstosubsequent-plantgrowth.

Plant–soilfeedbackisthephenomenoninwhichpreceding-plantconditioningof thesoil formsa legacy influencingsubsequent-plantgrowth (Bever, 1994; Ehrenfeld, Ravit, & Elgersma, 2005). Legaciescan be understoodmechanistically through specific feedback path-waysbetweenplantsandsoilpropertiessuchasnutrientcycling,plantmutualists and enemies (Van der Putten etal., 2016;Wardle etal.,2004).Soillegaciesarenotrestrictedtothenextgenerationofplants,but canpersist foroverayear (Bartelt-Ryser,Joshi, Schmid,Brandl,&Balser, 2005;Campiglia,Mancinelli,Di Felice,&Radicetti, 2014).IndirectPSFbetweenplantspeciesseparatedintimefindsitsapplica-tioninagriculture(Bever,Westover,&Antonovics,1997),formingthecornerstoneofcroprotation. Indeed,croprotation is recommendedbecause it disrupts the build-up of specialist herbivores andpatho-gens(Diasetal.,2014;Snappetal.,2005).However,towhatextentpreviousplantgrowthaffectsthefeedbackbetweencurrentandsub-sequentcropshasnotbeenquantified.Yet,suchtestsareneededtodesignoptimalcropsequences.

Croprotationincreasesdiversityintime.Throughincreasedquan-tityandqualityofplantresidues(Diasetal.,2014;Tiemann,Grandy,Atkinson,Marin-Spiotta,&McDaniel,2015),farmerscanemploypos-itivePSFswithoutlosingthesummerseasonbygrowingwintercovercrops(WCCs;Snappetal.,2005).Deepordense-rootingandproduc-tivecovercropscan improvenutrient retention (Thorup-Kristensen,Magid,&Jensen,2003),whereasleguminouscovercropscanfixat-mosphericnitrogen.Althoughgrowingplantsstimulateplant-feedingnematodes,carefulselectionofcovercropspeciescanreducespecificnematodespecies(Fourie,Ahuja,Lammers,&Daneel,2016;Thoden,

Korthals,&Termorshuizen,2011), and reduceyield losses in subse-quentcrops(Singh,Hodda,&Ash,2013).Traditionallybothnutrientcyclingandpathogensuppressionfeedbackpathwayshavebeenstud-iedinisolation.MechanisticunderpinningofhowthesePSFpathwaysactinconcertcanimprovecroprotationguidelines.

Includingcovercropmixtures into rotationscombinesbeneficialspatial and temporal diversity effects. Finney andKaye (2017) con-firmedthediversity-ecosystemfunctioningrelationshipinagriculture.Next-crop productivity is positively correlatedwith cover crop bio-massandnitrogenconcentration(Finney,White,&Kaye,2016).Plant-feedingnematodedensitiesdecreasedwithincreasingplantdiversityinnaturalgrasslands(Cortoisetal.,inpress).Moreover,mixingcovercropscouldsuppressnematodenumbersashostplantsarehardertofind(Iversonetal.,2014;Mitchell,Tilman,&Groth,2002).Howcovercropmixture legaciesactonnitrogencyclingandpestmanagementsimultaneously,however,remainsunaddressed.

Understanding legacies of plant diversity in space and time isessential for successful application of WCC mixtures. We, there-fore, studied soil-mediated legacies ofWCCmixtures compared tomonoculturesonsucceeding-cropproductivity.Wetested(1)ifWCCmixturesincreaseWCCproductivityandnitrogenconcentration,soilorganicmatter(SOM)content,soilmineralnitrogenandsubsequent-plantproductivity,andifplant-feedingnematodeabundancedifferen-tiallyincreasesunderWCCmonocultureandmixturesincomparisontowinterfallow.Forthelatter,wepredictedneutraltonegativemix-tureeffectsonplant-feedingnematodeabundance.Additionally,wetested(2)fordifferentialinfluenceoftwopreviousmaincrops(Avena sativa and Cichorium endivia)ontheseWCClegacies.Lastly,throughstructural equation modelling (SEM) we quantified (3) the relativeimportance ofWCC quantity and quality on next-crop productivitythrough mediation of soil properties. In this 2-year field study,wedemonstratethatWCCbiomassandshootnitrogenconcentrationin-creasesubsequent-cropproductivityandthatthesepropertiescanbepromotedbymixingfunctionallycomplementaryplantspecies,with-out trading-off with increased root-feeding nematode abundance.ThismakesWCCmixtures,apromisingavenueforsustainableagro-ecosystemmanagement.

2  | MATERIALS AND METHODS

2.1 | Study site and experimental design

LegacyeffectsofWCCmixturesandmonoculturesandthepreviousmain-crophistoryontheproductivityofA. sativa L. and C. endivia L.

andtemporaldiversityeffectswarrantsconsiderationofplantspecieschoiceinmixturesandrotationsforoptimalemploymentofbeneficiallegacyeffects.

K E Y W O R D S

agriculture,agroecology,croprotation,plantdiversity,plantproductivity,plant-feedingnematodes,plant–soilfeedback,soilmineralnitrogen,soilorganicmatter,wintercovercrops

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(henceforthgenericnamesareused)weretestedinafactorialrotationexperimentconsistingofthreephases(Figure1).Theexperimentwascarriedoutonsandysoil(91%sand,pH5.8,1.31gtotalN/kg,284mgtotal P/kg ofwhich 7.2mg plant-available P/kg, and93.8mgK/kg;Nergena,Wageningen,TheNetherlands,51°59′41.9″N,5°39′17.5″E).

Insummer2014,Avena and Cichorium were grown as preceding main crops (S′14) followedby autumn cultivation ofWCCs (W′14):four monocultures (Lolium perenne L., Trifolium repens L., Raphanus sativus L., and Vicia sativaL.), twomixtures[Lolium+Trifolium (hence-forthL+T);Raphanus+Vicia(R+V)]andfallowascontrol.Lastly,Avena and Cichoriumwerecultivatedassubsequentmaincrops(S′15).Therotationtreatmentswerereplicatedfivetimesfollowingarandomized

blockdesignof120plotsof3×3m(Figure1c).Eachplotconsistedoftwoexperimentalunits(1.5×3m).Monoculturesandfallowwereappliedonfull3×3mplots(oneoftwoexperimentalunitswasran-domlyselectedforsampling).Mixturesweregrownononeoftheex-perimental units (1.5×3m) per plot. Plotswere separatedby grassstrips(Phleum pratenseL.,1.5mwidth).

2.2 | Plant and soil treatments

Allplantmaterialwasobtained fromcommercial suppliers inTheNetherlandsandchemicallyuntreated.Avena(var.Dominik),Phleum (var.Grindstad),Lolium(var.Mathilda)andVicia(var.Ebena)seeds

F IGURE  1 Experimentalset-up.(a)Timelinefieldexperimentinthreephases:summer2014(S′14),winter2014/2015(W′14),summer2015(S′15),indicatingwhenmeasurementsweretaken.(b)Rotationdesign(n=5):Phaceliawasgrowninsummer2013(S′13)priortocultivatingmain crops Avena sativa(Avsa)andCichorium endivia(Cien),followedbywintercovercropmonoculturesLolium perenne(Lope),Trifolium repens(Trre),Raphanus sativus(Rasa),Vicia sativa(Visa)andmixturesLolium+Trifolium(L+T)andRaphanus+Vicia(R+V),withfallowascontrol.Subsequently,Avena and Cichoriumweregrown.(c)AerialphotographduringS′15,showing60Avena(dark)and60Cichorium(light)plotsoftwoexperimentalunits(1.5×3m)infiverandomisedblocks(byJ.Suomalainen).*Mixturesgrownononeexperimentalunit[Colourfigurecanbeviewedatwileyonlinelibrary.com]

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302  |    Journal of Applied Ecology BAREL Et AL.

werepurchasedfromAgrifirm(Apeldoorn,NL).OrganicallyrearedCichorium seedlings were obtained from Jongerius (Houten, NL).Trifolium (var. Alice) was provided by Barenbrug (Nijmegen, NL),and Raphanus (var. Terranova) by Joorden’s Zaadhandel (Kessel,NL).

To homogenize the field cultivation history prior to the ex-periment,Phacelia tanacetifoliaBenth.(var.Angelia)(June–August2013)wasgrown,mownandresiduesleftonthefield(Figure1b).InMarch 2014, the fieldwas ploughed (25cm depth).All plotswere fertilized in both spring2014and2015, following generalpractice.AttheendofMarch2014allplotsreceived:82kgN/ha, 249kgK/ha, 168kgS/ha, 84kgCa/ha. In early May another28kgN/haand4.2kgCa/hawasgiven.InMarch2015,41kgN/ha, 203kgK/ha, 137kgS/ha, 6.4kgCa/hawere applied, and addi-tionally 14kgN/ha and 3kgCa/ha inMay. In 2015, theN fer-tilizationwashalvedcompared to2014to facilitateobservationofWCCeffectsonnitrogencyclingwithoutpotentialoverrulingeffectsofhighlevelsoffertilizerapplication.NoPwasaddedtothesoilasthiswasamplyavailable.

2.2.1 | Main crop cultivation (S′14 and S′15)

Avena and Cichoriumcultivationwassimilarin2014and2015.InendMarch,Avenawassown(193.5kg/ha;12.5cmrowspacing,3–5cmdepth). In earlyMay, all plotswere treatedwith herbicide to sup-press dicotweeds (Damine 500 2L/ha,mcpa 500 1L/ha, Starane2001L/ha),and4-week-oldCichorium seedlingswereplanted (in-terplant distance 30×30cm). Thereafter, allCichorium plotsweremanuallyweeded.Allplotswereirrigatedaccordingtogeneralagri-culturalpractice.Cichoriumwasgrownuntilmid-JulyandAvena was harvestedinlate-July.Shootswereharvestedandstubbleleftonthefield.

2.2.2 | Winter cover crop cultivation (W′14)

AllplotswerehoedpriortoWCCssowingon25August(12.5cmrowspacing,2–3cmdepth,Lolium25kg/ha,Trifolium10kg/ha,Raphanus 30kg/ha,Vicia125kg/ha).Mixtureswerecomposedof50/50pro-portions of the monoculture seeding densities. Mid-September,plotsweremanuallyweededandadditionally10kg/haTrifolium was hand-sowntoensureestablishment(5kg/haforL+T).Weedingwasrepeated early October. WCCs were mown mid-February and theresidueincorporatedintothesoilbymilling(10cmdepth),twicewitha1-weekinterval.

2.3 | Measurements

2.3.1 | Winter cover crop biomass and nitrogen concentration

Winter cover crop shoot and root biomass were determined mid-December2014,attimeoffirstfrost.Shootswerecut(25×25cm)inthecentreofeachexperimentalunit.Rootbiomasswasdetermined

fromsoilcores(8cmdiameter,0–30cmdepth)takenfromthecentreof each sampling square. Rootswere gently rinsedwith tapwater.Samples were dried at 70°C for 72hr and weighed. Shoots weregroundwithaRetschMM2000ballgrinder(RetschBeneluxVERDERNV,Aartselaar, Belgium).N concentration of shoots fromblocks 1,3and5wasmeasuredwithaCHNanalyser (LECOCorporation,StJoseph,MI,USA).

2.3.2 | Plant- feeding nematodes

Nematode samples were taken mid-December 2014. Per plot, 12cores (6 per experimental unit) were taken with an auger (2.5cmdiameter,20cmdepth)andmixed.Sampleswerestoredat4°Cuntilprocessingwithin2weeks.Nematodeswereextracted from100gfresh soil following Oostenbrink (1960). The elutriator suspensionwas washed over four stacked sieves (mesh 45μm), then pouredoverdoublecottonfiltersonacoarsesieveonashallowtraywith90mltapwater.After24hr,thefiltratewascollectedandfilledupto100ml.Totalnumberofnematodeswascountedina9mlsubsam-plefromthe100mlsuspension.Next,nematodesuspensionswereconcentrated into2ml and subsequently fixedby adding4-mlhotand4-mlcoldformalin(concentrationof4%).Nematodeswereiden-tified microscopically by applying 0.15ml formalin suspension onmicroscopeslides.Ineachsample,150individualswereassignedtofeedinggroups(Yeates,Bongers,DeGoede,Freckman,&Georgieva,1993).

2.3.3 | Soil organic matter and mineral nitrogen

Soil abioticpropertieswerequantifiedon7April2015.Mixedsoilsampleswerecollectedperexperimentalunit,bytakingthreecores(diameter2.5cm,depth0–30cm). Sampleswere stored1weekat4°Cand sievedover2mm.SOMcontentwasdetermined as loss-on-ignition(550°Cfor4hr).PotentialsoilnitrogenpoolwasdefinedastotalmineralN(NO3

−andNH4+)afterincubation(3weeks,20°C,

60%waterholdingcapacity)(seeAppendixS1).MineralNwasmeas-ured on dried soil (40°C), using KCl extraction (Keeney &Nelson,1982).

2.3.4 | Productivity of main crops in 2015

Cichoriumwasharvestedon6July.Averagedryweightperplantwasdeterminedbyharvestingthreeplantsperexperimentalunit.Samplesweretakenequallyspaced,omittingtheouterrows.Plantswerecutatsoilsurfaceandstoredat4°Cuntilprocessingwithin4days.Avena washarvestedon24July,bycutting25×25cmarea(containingtworows)6cmabovesoilsurfaceinthecentreoftheexperimentalunit.Samplesweredriedat70°C.

2.4 | Data analysis

StatisticalanalyseswereperformedwithRstatisticalsoftwareversion3.2.1(RCoreTeam2015)usingthebelow-mentionedpackages.

     |  303Journal of Applied EcologyBAREL Et AL.

2.4.1 | Winter cover crop performance

Differences between WCC treatments effects on crop biomass(quantity)andnitrogenconcentration(quality)weretestedusinglin-earmixedeffectsmodels(nlmepackage;Pinheiro,Bates,DebRoy,&Sarkar,2016),withcroppinghistoryasacovariate.Formodelselec-tionandoptimizationwefollowedtheprotocoloutlinedinZuur,Ieno,Walker,Saveliev,andSmith(2010).Inbrief,fullmodelsincludedWCCtreatments (W′14),previouscroppinghistory (S′14)and their inter-action (W′14×S′14)withblockasa randomfactor.Toaccount forheteroscedasticity,weselectedvariancestructuresbestcapturingthedifferenceinvariancebetweenthestrata.Modelswerefurtheropti-mizedbybackwardsremovalofnon-significantinteractionsandmaineffects.Thegoodness-of-fitofthesimplifiedmodelandtheoriginalmodelwerecompared through the likelihood-ratio test.Parametersof the finalmodelswere estimatedwith restrictedmaximum likeli-hood. Normality and homogeneity of residual variances of eachmodel were verified with resp. Kolmogorov–Smirnov and Levene’stest.Differencesbetweentreatmentswereevaluatedpost-hocwithTukey’stest.

2.4.2 | Soil properties

Wetestedwhether soilpropertiesof theWCCtreatmentsdifferedfromfallowbyalinearmixedmodelwithfallowasbaselineandblockasrandomfactor.

WequantifiedtheWCCeffectonsoilpropertiesbyexpressingtheresponse of the soil parameters (Y) per treatment (i) relative to thefallow (f)accordingtoEquation1(Brinkman,VanderPutten,Bakker,&Verhoeven,2010).Treatment-controlcomparisonsweremadepair-wise,withinthesamepreviouscroppinghistory(j)andblock(b).

Next, the relativeWCC effect on soil parameters and previouscropping effect thereuponwere testedwith a linear mixed effectsmodel as described above.

2.4.3 | PSF effects

SubsequentAvena and CichoriumproductivityonformerWCCplotswascomparedtotheproductivityonformerfallowplots.Inaddition,thefeedback-effectsofWCContheproductivityofbothmaincropsandtheinfluenceofpreviouscroppingthereuponwasquantifiedwithEquation1andtestedwithalinearmixedeffectsmodel.

2.4.4 | Mixture effects

WCCmixtureseffectsweretestedseparatelyforWCCbiomassandnitrogenconcentration,aswellasforsoilproperties(SOM,potentialNpool,nematodeabundance)andproductivityofsubsequentAvena and Cichorium. Per response variable, the expected value (YE) was

calculatedastheaverageoftheobservedcomponentmonoculturesvalues.Themixtureeffectwasquantifiedasthenaturallogarithmoftheratiooftheobservedresponsetothemixturetreatment(YO)andtheexpectedvalue(YE)(Equation2)withinblock(b).

Mixtureeffectswereconsideredsignificantiftheydeviatefromzerobasedona two-sidedStudent’s t-test (α=0.05).Positivemixtureef-fectsonproductivitywereconsideredasoveryielding.Mixtureswouldoveryieldtransgressivelywhenproductivityexceededthemostproduc-tivecomponentmonoculture(Schmid,Hector,Saha,&Loreau,2008).

2.4.5 | Testing relative importance of PSF pathways

TheextenttowhichthelegaciesofWCCmixturesweremediatedbysoil properties and affect biomass production of subsequent plantswas evaluated by SEM, using packages Lavaan (Rosseel, 2012) andMVN(Korkmaz,Goksuluk,&Zararsiz,2014).

Thedegreeofmodelfitgiventhedatawastestedinamultigroupmodel grouped per subsequent main crop (Avena or Cichorium), inwhichweconstrainedthepathsbetweenWCCshootbiomassandni-trogenconcentration,andsoilpropertiesSOM,potentialsoilnitrogenpoolandplant-feedingnematodeabundance,aswellasthepathwaybetweenSOMandpotentialNpooltobeequalacrossbothgroups(seeAppendixS2).Dataonfallowwereexcluded.Thedegreeoffitwasmeasuredwithmaximumlikelihoodchi-squarestatistics(multivariatenormaldistributionofendogenousvariableswasverified).Weverifiedthemodel outcomewithmethods for small sample size byBollen–StinebootstrappingandMonteCarloχ2simulations(Shipley,2016).

3  | RESULTS

3.1 | Winter cover crop performance

Winter cover crop shoot biomass varied byWCC treatment (W′14:F5,104=82.78, p<.001), previous main crop (S′14: F1,104=10.37,p=.0017) and displayed an interaction effect (S′14×W′14:F5,104=2.35,p=.0457).TheWCCtreatmentsthatincludedRaphanus were threefold more productive than Lolium and Trifolium monocul-turesandmixture (Figure2a).Loliumwasmoreproductiveon formerCichoriumplotsthanonformerAvenaplots.OtherWCCspecieswereunaffectedbypreviouscropping.TheLolium+Trifolium(L+T)mixturewasasproductiveasexpectedbasedonmonoculturebiomass(Figure2a),whereastheRaphanus+Vicia(R+V)mixtureoveryieldedonbothformerAvena (t9=3.18,p=.011)andCichorium soil (t9=5.29,p<.001).

StandingrootbiomassdifferedsignificantlybetweenWCCtreat-ments(W′14:F5,110=57.35,p<.001,Figure2b),whilepreviousmaincrop effect on root biomass was non-significant. Treatments withLolium and Raphanus had thehighest rootbiomass,whereas the le-gume treatments, specifically Vicia monoculture, had low root bio-mass.The L+Tmixture had a significantly larger root biomass than

(1)relativeWCCi,j,b=

(

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304  |    Journal of Applied Ecology BAREL Et AL.

expected(t19=2.30,p=.033),whereasR+Vmixturerootbiomassdidnotsignificantlydeviatefromtheexpectation(Figure2b).

Shoot nitrogen concentration differed between WCC treatments(F5,63=95.98,p<.0001,Figure2c)andwasunaffectedbypreviousmaincrop.Nitrogenconcentration in legumeshootswastwiceashighas inLolium and Raphanus.TheL+Tmixtureshoweda lowershoot nitrogenconcentration thanexpected (t10=−3.58,p=.005,Figure2c),whereasthenitrogenconcentrationofR+Vmixturedidnotdifferfromexpectation.

3.2 | Legacy effects on soil properties

Most WCC treatments left SOM content unaltered comparedto fallow, except for a reduction by former Lolium monocultures(t129=−3.38,p=.0009,Table1).Mixtureseffects variedwith com-position;SOMlevelsinformerL+Tplotswereasexpected,butSOMinR+Vplotswaslowerthanexpected(t19=−2.50,p=.022,Table1).The relative effect sizes ofWCCs on SOMwere small but signifi-cantly different between WCC treatments (F5,109=2.83, p=.019,Figure3a)andloweronplotswithlegaciesofAvenathanofCichorium (F1,109=6.95,p =.01,Figure3b).

ThepotentialsoilnitrogenpoolwasincreasedbyallWCCtreatmentsexceptLoliummonoculture(Table1),withhighestvaluesinRaphanus and R+Vplots.WCCmixtureeffectswerenon-significant.RelativeWCCeffectsonthepotentialNpoolweredifferentbetweenWCCtreatments(W′14:F5,109=3.33,p=.008,Figure3c),andmorepositiveonformerCichorium plotsthanonAvenaplots(S′14:F1,109=6.38,p =.013,Figure3d).

The abundance of plant-feeding nematodes showed large differ-ences betweenWCC treatments (F5,109=9.03, p<.0001, Figure3e).Compared to fallow, plant-feeding nematode abundances were al-mostdoubled inplotswithViciaandR+V.Raphanusalsosignificantlyincreased nematode abundances. Nomixture effectswere observed(Table1, Figure3e). Previous cropping history influenced the rela-tiveWCC effect significantly (F1,109=6.38,P=.013),with nematodeabundance being higher on formerCichorium plots thanAvena plots(Figure3f).

3.3 | Legacy effects on subsequent- crop growth

Relativetofallow,WCCtreatmentsresultedincontrastingfeedbackeffectsonbothAvena (F5,49=15.68,p <.001,Figure4a)andCichorium biomass (F5,50=3.90, p=.005, Figure4c).Mixtures ofWCCs influ-enced AvenaproductivitydifferentlythanCichorium(Table1).Avena productivityonformerL+Tplotswaslowerthanexpected(t9=−2.63,p=.027),whileR+Vmixtures led tohigherAvenabiomass thanex-pected (t9=2.59, p=.029). WCC mixtures effects on Cichorium productivity were non-significant. More specifically, Avena grown on former Trifolium (t59=4.04, p<.001, Table1), Vicia (t59=4.15,p<.001)andR+V(t59=4.20,p <.001)plotsresultedinhigherAvena biomasscomparedtothefallowtreatment,whereasLolium reduced it(t59=−2.37,p=.02).Overall,CichoriumbiomassincreasedbymostWCCtreatments(exceptLolium)comparedtofallow.

PreviousmaincropsinfluencedtheWCClegacyeffectsonAvena (F1,49=43.58, p<.001, Figure4b), with more positive feedback onformer CichoriumthanonformerAvenaplots,whereastheidentityoftheprecedingmaincropdidnotinfluencetheWCCfeedbackeffectson succeeding Cichorium.

3.4 | Relative strength of PSF pathways

Our SEMmodel including both indirect and direct effects ofWCCabove-ground biomass (quantity) and nitrogen concentration (qual-ity) on subsequent-plant productivitywas consistentwith our data

F IGURE  2 Wintercovercrop(WCC)biomassofshoot(a),root(b)andshootnitrogenconcentration(c).ForabbreviationsseeFigure1.Shootbiomass(a)isspecifiedperpreviousmaincropAvena(Avsa′14)or Cichorium(Cien′14).Dashedlinesspecifyexpectedmixtureresponsebasedoncomponentmonocultureperformance.*Specifiesasignificantdeviationfromexpectedresponsebasedonatwo-sidedt-test(p<.05),***p<.001,ns(p>.05).For(a)n=10,(b)n=20,(c)n=12exceptLope(n=11).Errorbars±1SE,lettersindicatesignificantdifferencesbasedonTukeyposthoctest.Note:Shootbiomass(a)ofLolium differed per precedingmaincrop,asindicatedbydifferentletters

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a

cd

abb

*

ns

(c)

     |  305Journal of Applied EcologyBAREL Et AL.

(χ2=13.01,df =14,p=.526,Figure5).BiomassofsucceedingAvena and Cichorium was positively related toWCC quantity and quality.Avenabiomasswasmorestronglyinfluencedbyqualitythanquantity,whileforCichoriumproductivityquantitywasastrongerdriverthanquality(Figure5).Moreover,CichoriumbiomasswasmostinfluencedbySOM,whereasthiswasnotasignificantfactorforAvena.

WintercovercropbiomasspositivelyaffectedthepotentialNpoolandplant-feedingnematodeabundance.However,biomassdidnotin-fluenceSOMcontent.NeitherdidWCCshootnitrogenconcentrationinfluence the potentialNpool, nor nematode abundance. SOMdid

positivelyinfluencethepotentialNpool.AlthoughtherewasastrongpositiveeffectofWCCbiomassandNconcentrationonthebiomassofbothmaincrops, theseeffectsdidnotoperatevia thequantifiedsoilparameters.

4  | DISCUSSION

Significanceoftemporalandspatialdiversityinagro-ecologicalmanage-ment is increasingly recognizedbyscientistsandpolicymakers (FAO

TABLE  1 Meansandstandarderrorofsoilpropertiesandproductivityofsucceedingplantsperwintercovercroptreatment(W′14)andpreviouscroppinghistory(S′14):soilorganicmatter(SOM),potentialsoilnitrogenpoolandplant-feedingnematodesabundancepersoildryweight(dw),anddrybiomass(Bm)ofAvena(Avsa′15)andCichorium(Cien′15).ForabbreviationseeFig1.Significantdifferences(two-sidedt-testp<.05)betweenexpectedandobservedmixtureresponsesareunderlinedandthedirectionindicated[(+)positive,(−)negative].Boldvaluesindicateasignificantdifference(p<.05)ofW′14treatmentsrelativetofallowinalinearmixedmodel

SOM (%)Potential N pool (mg/kg dw)

Nematodes (#100 per g dw) Bm Avsa′15 (g/m2)

Bm Cien′15 (g per plant)

W′14

Fallow 4.75(0.06) 20.58(0.93) 707(63) 999.66(26.59) 34.37(1.23)

Lope 4.53 (0.06) 21.54(1.00) 822(69) 836.53 (43.29) 33.86(0.90)

Trre 4.79(0.06) 26.79 (1.46) 620(72) 1,295.74 (44.17) 41.03 (0.90)

L+T 4.65(0.05) 25.04 (1.50) 788(47) 836.42(53.98)(−) 38.99 (1.01)

Rasa 4.82(0.06) 29.77 (1.19) 992 (91) 941.94(85.32) 43.22 (0.91)

Visa 4.75(0.07) 24.69 (1.24) 1,385 (132) 1,292.18 (44.83) 40.55 (0.68)

R+V 4.65(0.06)(−) 28.69 (1.22) 1,295 (123) 1,477.39 (75.94) (+) 41.32 (1.13)

S′14

Avsa14 4.73(0.03) 25.34(0.73) 1,059(63) 1,016.89(42.98) 39.53(0.62)

Cien14 4.68(0.04) 25.26(0.77) 830(47) 1,177.35(36.20) 38.57(0.66)

F IGURE  3 Theeffectofwintercovercrops(WCCs)relativetofallowonfoursoilproperties:soilorganicmattercontent(SOM,aandb),potentialmineralnitrogen(soilN,candd),abundanceofplant-feedingnematodes(Nem,eandf)specifiedperWCCtreatment(leftpanels)andaggregatedperpreviouscroppinghistory(rightpanels).PositiveeffectsindicatevaluesinWCCtreatmentsarehigherthaninfallow.For(a),(c)and(e)n=20,for(b),(d)and(f)n=60.ForabbreviationsseelegendFig1.Errorbars±1SE.Lettersindicatesignificantdifferences(p <.05),basedonTukeyposthoctest.y-axesarescaleddifferently

Winter cover crop legacy

Rela

tive

effe

ct

o

n SO

M

–0.06–0.04–0.02

0.000.020.04

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Previous cropping history

–0.06–0.04–0.02

0.000.020.04

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b

(b)

Rela

tive

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(f)

306  |    Journal of Applied Ecology BAREL Et AL.

2017;Finney&Kaye,2017).Includingcovercropsandtheirmixturesinrotationispromoted(Dijksma,2014;FAO2017),althoughthescien-tificbasistodecidewhichcropstoincludeislaggingbehind(Diasetal.,2014).We discuss our results in the light of biodiversity-ecosystemfunctioning(BEF)theorytoassessWCCdiversityeffectsinspace,andplacetheroleofcropdiversityintimeinthecontextofindirectPSF.

4.1 | Winter cover crop performance

WehypothesizedourWCCmixturestooveryield.Indeed,wefoundpositivemixture effects for shootbiomassofRaphanus+Vicia (R+V)and root biomass of Lolium+Trifolium (L+T). Legumes fix nitrogen,improving nitrogen availability to neighbouring plants (Thorup-Kristensen etal., 2003). Nyfeler etal. (2009) demonstrated above-ground overyielding in grass-clovermixtures.However,we did notobserveabove-groundoveryieldingofourL+Tmixture.Interspecificcompetition is a possible explanation as Trifolium is cold sensitive(Brandsæter, Heggen, Riley, Stubhaug, & Henriksen, 2008) leadingtoreducedcompetitiveabilitywhengrownwithLolium in latesum-mer/autumn(Nesheim&Boller,1991).LoliumdominationisreflectedintheoveryieldingofL+Trootbiomass,whichwassimilartoLolium rootbiomass.Incontrast,R+Vmixtureshowedabove-groundovery-ieldingaswasalsoobservedbyMöllerandReents(2009),indicating decreasedcompetitionforNinthemixture.

WeexpectedincreasedlevelsofmixtureshootNduetocomple-mentaritybylegumes.TheneutralmixtureeffectonR+VshootNsug-gestsimprovednitrogen-useefficiencyratherthanaqualityincrease.Incontrast,thenitrogenconcentrationinL+Tshootsshowedanega-tivemixtureeffect,probablybecausethespecieswiththelowestni-trogenconcentrationwasmostabundant(ownobservations).

Ideally,WCCmixturesincreasenitrogeninputintothesoilthroughincreased biomass and/or plant nitrogen content. Positive mixtureeffects (overyielding)aredesirablemixtureproperties (Schmidetal.,2008). Since the choiceof species in amixture is key to itsperfor-mance, studying the behaviour of species inmixtures underwinter

growing conditions is needed to validate BEF principles in utilizingWCCmixtures.

4.2 | Winter cover crop legacy effects on soil properties

Aspredicted,mostWCCsincreasedthepotentialsoilNpoolrelativetowinterfallow.However,thehypothesizedmixtureeffectswerenotobserved.PreviousfieldexperimentsshowedthatWCCspeciesdif-ferinproductivityandNconcentrationandconsequentlyintheirni-trogensupplytofollowingcrops(Campigliaetal.,2014;Finneyetal.,2016).ThepotentialNpoolinourSEMwas,indeed,drivenbyWCCshoot biomass. However, the proposed causal pathway betweenWCCshootNconcentrationandpotentialNpoolwasnon-significant,indicating that theNpools are steeredbyplantproductivity ratherthanplant quality.Orwin etal. (2010) found that highly productiveplantsoftenproduceeasilydecomposablelittercomparedtolesspro-ductiveplants,makingitlikelythathighlyproductiveWCCspromotesoilnitrogenthroughhighinputsofeasilymineralizableplantresidues.

Increasedplantdiversity inboth timeand space increasesSOM(i.e.Diasetal.,2014;Tiemannetal.,2015).Here,theobservedrela-tiveeffectsofWCCtreatmentsweresmalland,exceptforareductionby Lolium,didnotdifferfromfallow.Moreover,thecausalpathwaybe-tweenWCCshootbiomassandSOMinourSEMwasnon-significant.TheL+TmixturedidnotinfluenceSOMdifferentlythanitsmonocul-tures,whereastheR+Vtreatmentdisplayedanegativemixtureeffect.Build-upofSOMrequirescarbon inputsexceeding itsturnover.TheincorporationofresiduesintotheSOMpooltakestime,whereasthereis a continuous break-down of old SOM. The presence of growingplantsandtheadditionoffreshorganicmattercouldprimethebreak-downofoldSOM(Kuzyakov,2010),andtheeffect-sizecandependontheresidingorganicmatterquality(Saar,Semchenko,Barel,&DeDeyn,2016).UnderstandingcarbonandnutrientdynamicsofWCCresidues inrotationthroughdecompositionstudieswouldbecrucialforavailableNsynchronizationwithcroprequirements.

F IGURE  4 Plant-soilfeedbackeffectsonsubsequentAvena(aandb)and Cichorium(candd)perwintercovercroptreatment(leftpanels)andpreviouscroppinghistory(rightpanels).Positivevaluesindicatesubsequent-cropbiomassonformerwintercovercropplotsishigherthanonformerfallowplots.ForspeciesabbreviationsseelegendFig1.Errorbars±1SE.For(aandc)n = 10; (b and d)n=30.Lettersindicatesignificantdifferences (p<.05),basedonTukeyposthoctest

Winter cover crop treatmentsPS

F on

Ave

na

–0.4

–0.2

0.0

0.2

0.4

0.6

b

a

bab

a

a(a)

Previous cropping history

Lope Trre L+T Rasa Visa R+V

PSF

on C

ichor

ium

–0.2

0.0

0.2

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0.6

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aa a

(c)

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     |  307Journal of Applied EcologyBAREL Et AL.

Plant-feeding nematode abundanceswere expected to increaseinWCCplots compared to fallow.Raphanus, Vicia andR+Vmixtureincreased nematode abundances in comparison to fallow.Our SEMestimatedthatWCCshootbiomassstimulatednematodeabundances,whereasWCCshootNdidnot.Increasedplantproductivitycouldleadto increased feedingarea forherbivorousnematodes (Thodenetal.,2011).Also,increaseinbottom-upresourcequantity(Chenetal.,2016)orquality(Cortoisetal.,inpress)canstimulatenematodeherbivory.

Additionally,mixtureswereexpected todilute theabundanceofnematodehostplants,resultinginneutraltonegativemixtureeffects.OurincreasedrootproductivityofL+Tmixtureshadneutraleffectson

nematodeabundances.TheseresultsareinlinewithCortoisetal.(inpress)whoshowadecreaseinplant-feedingnematodedensityperunitofrootbiomassinplantspeciesrichcommunities.Although,plantpro-ductivity generally stimulates nematode abundance, diversifying thebiomasscompositionisapotentialbio-controlfornematodeincreases.

4.3 | WCC legacy effect on Avena and Cichorium

ThelegacyeffectsofWCCsonsubsequentAvena and Cichorium rep-resentindirect(orinterspecific)feedbackeffects(Beveretal.,1997).AllWCCtreatmentsexceptLoliummonoculturepromotedCichorium

F IGURE  5 Multigroupstructuralequationmodelexplainingsoil-mediatedeffectsofwintercovercropsonproductivityofAvena(a,n=36)andCichorium(b,n=35)(ML)χ2=13.01,df=14,p=.526.Biomassquantity(LnwintercovercropBm)andquality(wintercovercropN)weretestedtoinfluencesubsequent-plantproductivity(Avena or CichoriumBm)directlyorindirectlyviasoilorganicmatter(SOM),potentialnitrogenavailability(potNpool)andplant-feedingnematodeabundance(Nem).Blacklinesaresignificant:*p<.05,**p<.01,***p<.001,greylinesarenon-significant.Numbersneararrowsarestandardisedpathcoefficients.Encirclednumbersarestandardizedresidualvariances.R2 is given foreachendogenousvariable

Ln winter cover crop Bm(g/m2)

Winter cover crop N (g/kg)

Ln Nem (# 100 per g dw)R2 = 0.148

SOM %R2 = 0.000

pot N pool (mg/kg) R2 = 0.187

Avena Bm (g/m2)R2 = 0.519

0.31**

0.00ns

–0.05ns

0.03ns

0.58 ***

0.48***

0.970 0.744 0.963

0.490

0.07ns

–0.02ns

0.39***

0.28*

0.13ns

(a)

Ln winter cover crop Bm(g/m2)

Winter cover crop N (g/kg)

Ln Nem (# 100 per g dw)R2 = 0.189

pot N pool (mg/kg)R2 = 0.164

Cichorium Bm (g per plant) R2 = 0.587

0.31**

0.49***

– 0.15ns

0.19ns

0.33**

0.42**

SOM % R2 = 0.000

0.973 0.875 0.719

0.416

(b)

0.07ns

–0.02ns

0.39***

0.28*

0.13ns

308  |    Journal of Applied Ecology BAREL Et AL.

productivity, while Avena productivity increased only after legumetreatments(Trifolium,ViciaandR+V).PrecedingLolium reduced Avena productivity.WeexpectedthatWCCmixturesgeneratenon-additiveeffects onAvena and Cichorium productivity via changes inmineralN availability and plant-feeding nematode abundances. We foundsignificantmixtureeffectsonAvenabiomassinthatL+Tsuppressed,andR+VpromotedAvenabiomassbeyondtheexpectation.Cichorium biomassdidnotshowWCCmixtureeffects.

Avena and Cichorium display differential feedback responses be-causeofspecies identityandassociatedmanagement.Plantsexhibitdifferentfeedbackeffectsdependingontheirfunctionaltraits(Cortois,Schröder-Georgi,Weigelt,vanderPutten,&deDeyn,2016;Kulmatiski,Beard,Stevens,&Cobbold,2008).OurcropslikelyprofiteddifferentlyfromWCCs,sinceAvena and Cichoriumhavedifferentgrowingseasons.ThedifferentialresponsesareexemplifiedinourSEMbyvaryingrela-tivepathwaystrengths.AvenabiomasswasmostinfluencedbyWCCshootN,whereasCichoriumbiomasswasprincipallydrivenbySOM,representingtheimportanceofsoilstructurerelatedprocesses(Carter,2002).Theseresultsemphasizethespecificityofplantsrespondingtotheirenvironmentandtheneedtotailorcropmanagement.

OurSEMsupports the findingsofFinneyetal. (2016) thatbothWCC biomass quantity and quality promote subsequent-crop pro-ductivity,indicatingtherelevanceofnutrient-cyclingforpositivePSFeffects.DespitethesignificantpathwaysfromWCCbiomasstosoilni-trogenandplant-feedingnematodeabundance,thosesoilpropertiesdidnotcapturethehypothesizedPSFmechanisms.Tobuildasoundscientific foundationof crop rotation principles, the components ofsoil-mediatedWCClegaciesthatpromotesubsequentgrowthofspe-cificcropsareyettobeidentified.Takingthegrowthrequirementsofsubsequentcropsasstartingpoint,futurestudiesshouldmakeeffortstodisentanglenutrientcyclingprocessesfromdirectbioticinfluences(pathogens,mutualists,decomposers)thatunderlietheWCCbiomassquantityandqualitypathways.

4.4 | Legacy effects of previous main cropping

DespitetheincreasingPSFliterature,moststudiesarelimitedtoleg-acyeffectsofprecedingplantstodirectlysucceedingplantswhereinpersistence of plant legacies remains unclear (Kardol, De Deyn,Laliberté,Mariotte,&Hawkes,2013).ThepositiveindirectfeedbackeffectsonsubsequentAvena growing on former Cichoriumplotsillus-tratethatpreceding-croplegaciescanpersistforatleast1year,whichagreeswithotherstudies(Bartelt-Ryseretal.,2005;Campigliaetal.,2014).Previousstudiesshowreducedplant-productivityonsoilspre-viouslyoccupiedbyclosely relatedspecies (Kulmatiskietal.,2008).Particularlygrassesshowstrongnegativefeedbackeffectsonsoilcon-ditionedby(near-)congenericspecies(Cortoisetal.,2016;Kulmatiskietal., 2008). Indeed, Lolium shoot biomass was lower on previousAvena thanCichoriumplots.LoliumsignificantlyreducedsubsequentAvenaproductivity.Theseobservationsstrengthenthegeneralrota-tion recommendations of avoiding successive cultivation of closelyrelatedcrops.Therefore,persistenceoflegaciesshouldbeconsideredwhenemployinglegacyeffectsforsustainablemanagement.

4.5 | Synthesis

Disentangling the relative strength of PSF mechanisms is vital formanagement of (agro-) ecosystems (Dias etal., 2014; Kardol etal.,2013; Van der Putten etal., 2016). Here, we showed that plantdiversity effects can influence subsequent-plant growth in agro-ecosystems.Theeffectsofplant–soil interactionsarespeciescom-binationspecificandwarrantconsiderationofpreviousplantgrowth.Bothbiomassquantityandqualityarekeydriversofsoillegaciesonsubsequent-plantproductivity,andresearchshouldundertakeeffortstodisentanglenutrientcyclingprocessesfromdirectbioticinfluences.Understandingtheseunderlyingpathwaysisessentialtosustainablymanageecosystemfunctioningthroughspatialandtemporaldynam-icsofplantmixtureeffects.Well-chosenWCCspeciesmixturesareapromisingagriculturalpracticetopromotebiologicalandchemicalsoilquality.

ACKNOWLEDGEMENTS

We thank G. Korthals for advice; J. Paul, D. Piwcewicz, I. GarcíaGonzález,H.MartensandUnifarmforpracticalassistance;JoordensZaadhandelandBarenbrugforprovisionofseeds;andJ.Suomalainenfortheaerialphotograph.Wearegratefulfortheconstructivecom-mentsof three anonymous reviewers.Thisworkwas supportedbyNWO-ALWVIDItoG.B.D.D.(grantno.864.11.003).

AUTHORS’ CONTRIBUTIONS

J.M.B.,T.W.K.,W.B.andG.B.D.D.conceivedtheideasanddesignedthe experiment. J.M.B. and G.B.D.D. executed the experiment andcollectedthedata,whichwasanalysedbyJ.M.B.,andB.D.J.M.B.andG.B.D.D. led thewriting of themanuscript. All authors contributedcriticallytodraftsandapprovedthefinalmanuscriptforpublication.

DATA ACCESSIBILITY

Data supporting the results of this manuscript are archived inDryadDigitalRepository:https://doi.org/10.5061/dryad.sp21b(Barel Kuyper,deBoer,Douma,&DeDeyn,2017).

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How to cite this article:BarelJM,KuyperTW,deBoerW,DoumaJC,DeDeynGB.Legacyeffectsofdiversityinspaceandtimedrivenbywintercovercropbiomassandnitrogenconcentration.J Appl Ecol. 2018;55:299–310. https://doi.org/10.1111/1365-2664.12929