Applied Soil Ecology

(1)

ContentslistsavailableatScienceDirect

Applied

Soil

Ecology

j ou rn a l h o m e pa ge : w w w . e l s e v i e r . c o m / l o c a t e / a p s o i l

Effect

of

banana

crop

mixtures

on

the

plant-feeding

nematode

community

Patrick

Quénéhervé

a

, Virginie

Barrière

b

, Frédéric

Salmon

c

, Florianne

Houdin

c

,

Raphael

Achard

b

,

Jean-Claude

Gertrude

b

,

Serge

Marie-Luce

a

,

Christian

Chabrier

b

,

Pierre-Franc¸

ois

Duyck

b

,

Philippe

Tixier

b,∗ a_IRD,_Unité_Mixte_de_Recherche₁₈₆_Résistance_des_Plantes_aux_{Bioagresseurs}_{(IRD-CIRAD-UM2),}_Pôle_de_Recherche_{Agroenvironnementale}_de_la_Martinique,_BP_214,₉₇₂₃₂_Le LamentinCedex2,Martinique,France

b_CIRAD,_Unité_Propre_de_Recherche_Système_Bananes_et_Ananas,_Pôle_de_Recherche_{Agroenvironnementale}_de_la_Martinique,_BP_214,₉₇₂₃₂_Le_Lamentin_Cedex_2,_Martinique,_France c_CIRAD,_Unité_Propre_de_Recherche_{Amélioration}_génétique_d’espèces_à_{multiplication}_{végétative,}_Pôle_de_Recherche_{Agroenvironnementale}_de_la_Martinique,_BP_214,₉₇₂₃₂_Le LamentinCedex2,Martinique,France

a

r

t

i

c

l

e

i

n

f

o

Articlehistory:

Received19May2011

Receivedinrevisedform5July2011 Accepted7July2011 Keywords: Communitystructure Cropmixture Nematode Musa Martinique Radopholussimilis

a

b

s

t

r

a

c

t

Varietalmixtureisaculturaltechniqueinwhichthegeneticandfunctionaldiversitiesofvarietiesare usedtomanagepestsanddiseases.Thisstrategyiscommonlyusedongrasscropssuchasrice,barley, maize,andwheattomitigatesomewindborneandsoilbornepathogens.Theeffectsofvarietalmixtures onthenumberandcommunitystructureofpests,includingplant-feedingnematodes(PFNs),however, haverarelybeenstudied.InexperimentsconductedinMartinique,weevaluatedtheeffectofvarietal mixturesofbananasonPFNcommunities.Agrowthchamberexperimentwasusedtomeasurethe susceptibilityofthreebananacultivarsdessertbananacv.902(MusaAAA,Cavendishsubgroup);anew synthetichybridcv.FB924(MusaAAA);andaplantaincv.Creoleblanche(MusaAAB,FrenchHorn)tothe twomajorPFNs.ThemultiplicationratesofRadopholussimilisandPratylenchuscoffeaeweresubstantially differentonthethreevarieties;forexample,themultiplicationratewasupto10timesgreateronplantain cv.Creoleblanchethanonhybridcv.FB924.Inafieldexperiment,weplantedthethreevarietiesinpairs thatincludedallsixpossiblecombinations.BananavarietalmixturessignificantlyaffectedbothPFN densitiesandcommunitycomposition.Differencesincommunitycompositionamongthepairsinvolved ashiftingequilibriumamongnematodespeciesandaninterspecificcompetitionforfoodresources. TherelativeabundanceofthespiralnematodeHelicotylenchusmulticinctusincreasedwhilethatofthe burrowingnematodeR.similis,whichisthemostdamagingspeciesonbananas,decreased.Theuseofa varietalmixtureinwhichonevarietysupportsalowPFNmultiplicationrateappearstohavepractical relevance,especiallyinsystemsbasedonverysusceptiblecultivarssuchasplantains.Theuseofvarietal mixturesshouldnotcreatemanagementproblems,especiallyforplantationsthatproducebananasfor localmarkets.

1. Introduction

Geneticuniformityofmonoculturesiswellknownto predis-posecropstooutbreaksofplantdiseasesandpests(Meungetal., 2003).Because theintroductionof plantdiversityincreasesthe numberofindividualfunctionaltraitsandpotentialecosystem ser-vices(Hajjaretal.,2008;Malezieuxetal.,2009),anagroecological strategy for diseasecontrol is togrowa mixture of plants dif-feringintheirsusceptibilitytopathogens(SmithsonandLenné, 1996;Wolfe, 1985).Thisstrategy,which hasmainlybeenused tocontrol fungaldiseases ongraincrops, is promisingbecause varietiesarewellselectedtowardcomplementaryfunctionaltraits

∗Correspondingauthor.Tel.:+596596423017;fax:+596596423001.

E-mailaddress:[email protected](P.Tixier).

(Mundt,2002).Effectivediseasemanagementbasedonplant diver-sityrequiresthatthemixedplantshavecomplementarylevelsof resistance/susceptibility.Varietalmixtures canreducepathogen selectivepressureproviding hoststhatdifferin theirsensitivity andcomprisevariablesourcesresistance.Varietalmixtureshave beenusedtosuppressriceblast(Wolfe,2000),powderymildewof barleyandwheat,andrustonbarley,wheat,maize,andcommon bean(SmithsonandLenné,1996).

Theeffectofvarietalmixtureshavebeenrarelystudiedonpests, includingplant-feedingnematode(PFN),forwhichonlyonestudy investigatethiseffectonsugarcane(Cadetetal.,2007).Nematodes areoneofthemostdamagingpestsofbananasandplantains,which are mostly cultivated in intensive monocultures (Quénéhervé, 2009).BecausecommunitiesofPFNsinbananaagroecosystemsare structuredbyhostplants(Duycketal.,2009;Quénéhervéetal., 2006b),amixtureofbananacultivarscouldalterthestructureof

(2)

thenematodecommunity,andnotonlyactasadilutionprocessof thepestasfordiseases.

In banana plantations, two species of PFNs are particularly prevalentanddamaging:theburrowingnematodeRadopholus sim-ilisCobbandthelesionnematodePratylenchuscoffeaeZimmerman (Gowenetal.,2005).Botharemigratoryendoparasitesthatfeed insidetherootcells;theycausenecrosisandlesionswhichmay attractotheropportunistic pathogens,reducerootbiomass,and eventuallycausetheplantstotoppleover.Whiletheburrowing nematodeismostlyfoundincommercialplantationsofCavendish varieties,thelesionnematodeP.coffeaeismostlyassociatedwith plantains(Quénéhervéetal.,2009b)orincroppingsystemsbased oncroprotationwithsugarcane(Tixieretal.,2006).Otherharmful PFNsinbananaplantationsincludethespiralnematode Helicoty-lenchus multicinctusCobb, theroot-knot nematode Meloidogyne

spp.,andthereniformnematodeRotylenchulusreniformisLinford andOliveira.BananasinfectedwithPFNarelessabletotakeup waterandnutrients,resultinginstunting,delayedmaturation,and reducedbunchsize.Thedamagecanvaryfromaslight lengthen-ingofthevegetativeperiodtotheultimatesymptomofattackby lesionnematodes,whichisthetopplingoverofbananaplants.The effectofacommunity ofPFNoncropdamagesdepends onthe geographicallocation(Quénéhervé,2009).

Aswiththedamagecausedbyanyotherpestorparasite,damage causedbyPFNsdependsonenvironmentalconditions, suscepti-bilityofthehost,andpathogenicityofthenematodeconsidered. Inthelast50years,nematologistshavecollectedsubstantialdata concerningthesefactors,and theyhave alsostudiedarange of nematodemanagementpracticesonbananas.Several complemen-taryapproachesarenowusedtoreducebothnematodedamage and nematicideapplications in commercialbananaplantations. Theseincludetheplantingofcleanseedmaterialcombinedwith croprotationor fallowing;theplantingofcovercrops; andthe useofresistantvarieties(ChabrierandQueneherve,2003). Nev-ertheless,PFNsremainamajorpestproblemforthecultivationof bananasworldwide(Quénéhervé,2009).Thesepestsarean impor-tantcauseinthelimitationoftheproduction,bothinexportand local market systems, which represent 16 and 90 million tons offruitsperyear,respectively.Inexportsystems,thecontrolof PFNsrelymainlyonpesticidesandrotations,whileinsmallholder systemsthecontrolisbasedonre-plantationofolderandmost damagedﬁelds.Varietalmixturesrepresentapromisingwayto controlPFNsinbothexportandsmallholdersystems.The organi-zationofsmallholdersystemsmakestheuseofvarietalmixturesa relevantoptionbecauseinthesesystems,ﬁeldsusuallyencompass manycultivarsofbanana.

Inthisstudy,weevaluatedhowthePFNcommunityisaltered byvarietalmixturesinbananaplantations.First,wecharacterized undercontrolledconditionsthemultiplicationratesofthe burrow-ingnematodeR.similisandthelesionnematodeP.coffeaeonthree varietiesofbanana.Inaﬁeldexperiment,wethenmeasuredthe effectofassociatingtwovarietiesofbananaonthePFNcommunity. Wemeasuredthenematodedensitiesandnematodecomposition forallthepossiblepairsofthreevarietiesofbanana.Finally,we dis-cusstheapplicabilityofusingamixtureofvarietiesforcultivation ofbananasforthelocalmarketandforexport.

2. Materialsandmethods

2.1. Plantmaterials

Weselectedthreecultivarsofbananathataregeneticallydistant fromeach other: thehybrid cv.FB924 (MusaAAA,a new syn-thetichybridfromCIRAD,Centredecoopérationinternationaleen rechercheagronomiquepourleDéveloppement;A)waschosenfor

itsresistancetonematodes(Quénéhervéetal.,2009a).The plan-taincv.Creoleblanche(MusaAAB,FrenchHorn;B),andthedessert bananacv.902(MusaAAA,Cavendishsubgroup;C)werechosen becausetheyarethemostprevalentplantainsanddessertbananas cultivatedintheFrenchWestIndies.

2.2. Growthchamberexperiment

The screenings were conducted with an experiments in a growthchamberwithcontrolledconditions.Thecomplete screen-ingmethodhasbeendescribed(Quénéhervéetal.,2006a),andall cultivarswereseparatelychallengedwiththeburrowingnematode

R.similisandthelesionnematodeP.coffeae.Theplantmaterialwas propagatedonMurashigeandSkoog(MS)medium,maintainedin thedarkina cooledincubatorat22±0.5◦Candregeneratedas neededintesttubesonmodiﬁedMSmediumincludingactive char-coalinacultureincubatorat25±0.5◦Cwithcontinuouslightfor 6–8weeks.PlantletswerethentransferredtoPVCculturetubes (4.5cmindiameter;17.5cminlength),placedinagrowth cham-ber(24–28±1◦C,with14hoflight).Theculturetubeswereﬁlled withsteam-sterilizedAndosol(1hat100◦C;pH6.2,organic mat-tercontent7.3%,CEC10.3mequiv./100gsoil).Plantswerewatered everythreedayswithanutrientsolution(Mairol®_14:12:15₊ oligo-elements,GmbH&Co,Germany).Inadditiontothreecultivarsand twonematodes,theexperimentsalsoincludedthreeculturetimes (plantsweredestructivelysampled30,45,and60daysafterthey wereinoculatedwithnematodes).The18treatmentcombinations (3cultivars,2nematodespecies,and3culturetimes)were repli-cated5times.Bothnematodespecieswereoriginallyisolatedfrom bananaplantsinMartinique.R.similiswasmaintainedonthe sus-ceptiblebananacv.GrandeNaine(MusaAAA,Cavendishsubgroup), whileP.coffeae wasmaintainedonthesusceptible plantain cv. Popoulou(MusaAAB).Nematodeswereextractedfromtheroots inamistchamber(Seinhorst,1950)overa48-hperiodtoprepare theinoculum,whichconsistedof400femalesperplantforR.similis

orP.coffeae.Ateachmeasure,30,45,and60daysafterinoculation withthenematodes,theentirerootsystemwascarefullycollected andweighedseparatelybeforenematodeswereextracted.Allthe rootswereplacedinamistchamberfora2-weekperiodof extrac-tion(Seinhorst,1950).Nematodeswerecountedina5-mlaliquotof ahomogenizedsuspensionwithastereomicroscopeandexpressed asnumberofnematodespergramoffreshroots.Themultiplication ratewascalculatedastheratiooftheﬁnalnematodepopulation dividedbytheinoculum.

2.3. Fieldexperiment

TheexperimentwassetupinOctober2008inanarea previ-ouslyoccupiedbya6-year-olddessert bananaplantationatthe RivièreLézarderesearchstationinthecentreofMartinique;the bananaplantshadbeenremoved,andweedsinvadedthearea.The soilwasanitisolderivedfromvolcanicash(andesiticbasalt)with 73%clay.Thistypeofsoilismostlyfoundinthelowlandsincentral Martinique.Theexperimentaldesignwasarandomized complete-blockwith16replicatesorblocks.Allblocks(235.2m2_per_block) consistedofsixpairsofbananaplants(AA,BB,CC,AB,BC,andAC). Apairofbananaconsistof twoplantsseparated by80cm, this limiteddistancebetweenplantsfacilitatetheirbiological interac-tions.Pairswereplanted6-mapartfromotherpairstoavoidroot interferencebetweentwodistinctpairs.Irrigationandfertilization wereconductedaccordingtostandardrecommendationsindessert bananaplantations(Lassoudière, 2007).Allbananaandplantain materialsforplantingoriginatedfrommicropropagation,andthey werethereforefreeofnematodesbeforeplanting.

Before the bananas were planted, theabundance of PFN in thesoilwasassessedateachlocationwherebananapairswere

(3)

Table1

Abundanceofnematodes(mean±SE)andrelativeabundanceintheﬁeldexperimentmeasuredbeforeplanting(October2008)in96soilsamples.

Variable Radopholussimilis Helicotylenchusmulticinctus Rotylenchulusreniformis Hoplolaimusseinhorsti

Nematodeabundance(numberper250cm3_of_soil) ₈_±₂ ₂₉_±₆ ₃₆₀₅_±₂₈₇ ₁₁_±₃

Relativeabundance(%) 0.20% 0.80% 98.70% 0.30%

planted.Nematodeswereextractedfrom96soilsamples(sixper block) by elutriation (Seinhorst, 1962).The PFN community in theexperimentalplotcomprised theﬁvemostcommonspecies inthebanana–nematodecomplex(Table1).Reniformnematodes

R.reniformis weremostabundantand represented98.7%ofthe PFNs.Other,lessabundantspeciesincludedspiralnematodesH. multicinctus(0.8%),lancenematodesHoplolaimusseinhorsti(0.3%), burrowingnematodesR.similis(0.2%),andafewbarelydetectable

P.coffeae.ThisPFNspeciﬁccompositionisusuallyfoundinbanana monoculture.ForeachspeciesofPFN,wecalculatedtheirrelative abundancethatisforagivenspeciesitsproportionamongthetotal PFNpopulation.

ThebananaswereplantedinOctober2008,andbananaroots werecollectedbetweenbananapairsinFebruary,June,and Novem-ber2009andinJuly2010.Thebananarootsamples(about500g freshmasspersample)werewashed,sliced,andhomogenizedin thelaboratory. Asubsampleof50gwasplacedinamist cham-ber,andnematodeswerecollectedfor2weeks(Seinhorst,1950). Nematodeswereidentiﬁedtospecies,counted,andexpressedas thenumberofnematodespergramoffreshroots.

2.4. Statisticalanalysis

For thegrowth chamber experiment, multiplication rates of nematodeswereanalysedusingageneralizedlinearmodel(GLM) withPoissonerrorasafunctionofnematodespecies,culturetime, bananacultivar,andinteractionsamongthesefactors.Forthefield experiment,densitiesofthedifferentnematodespecieswere anal-ysedbyaGLMwithPoissonerrorasafunctionoftime,nematode species,initialabundanceofnematodesinsoil,andgenotypesof bananapairs.Weusedstandardmodelsimplificationprocedures toeliminatenon-significanttermsofthemodel.Thesignificanceof eachtermwasassessedthroughthechangeindeviancebetween modelswithandwithoutthatterm.Overdispersionwasaccounted forusingQuasi-PoissoninsteadofPoissonmodelsinR(O’Haraand Kotze,2010).Westartedfromthemostcomplexmodel (includ-ingallinteractionsandquadratictermsforcontinuousvariables) andkepteliminatinghigherordertermsaslongastheyremained insignificant(Crawley,1993).Allmodelswerefitted usingR(R DevelopmentCoreTeam,2009).

3. Results

3.1. R.similisandP.coffeaemultiplicationratesinthegrowth chamberexperiment

Multiplicationratesofthenematodespeciesdifferedamongthe threebananacultivars(Dev=7111.9;df=2,96;P<0.001).The multiplicationrateonplantaincv.Creoleblanchewassigniﬁcantly affectedbynematodespecies(Dev=1141.4;df=1,32;P<0.001), culturetime(Dev=5365.5;df=2,30;P<0.001),andthe interac-tionbetweenthesetwofactors(Dev=228.8;df=2,28;P<0.001). Inotherwords,nematodemultiplicationsofR.similisandP.coffeae

differedovertimeforthiscultivar.Theplantaincv.Creoleblanche wassigniﬁcantlymore susceptibletonematodes thantheother varieties(Fig.1).Sixtydaysafterinoculation,themultiplicationrate was644forP.coffeaeand187forR.similis,andtheplantaincv. Cre-oleblanchewastheonlycultivarexhibitingahighermultiplication rateforP.coffeaethanR.similis(Table2).

Fig.1.Nematodedensities(individualspergramoffreshroot,mean±SE)ofR. similis(A)andP.coffeaeat30,45,and60daysafterinoculationforthreebanana cultivarsinthegrowthchamberexperiment.

Onthedessertbananacv.902,onlyculturetime(Dev=968.41; df=2, 30; P<0.001) and thenematode species (Dev=124.81; df=1,32;P<0.001)affectedtheﬁnalnumbersofnematodes.The susceptibilityofthedessertbananacv.902wasintermediatefor Table2

Freshrootweight(FRW)andmultiplicationrates(MR)ofR.similisandP.coffeaeat 30,45,and60daysafterinoculation(DAI)forthreebananacultivarsinthegrowth chamberexperiment.

DAI Radopholussimilis Pratylenchuscoffeae

30 45 60 30 45 60 FRW(g) A 10.7 15.4 14.9 11.3 13.6 14.1 B 9.9 11.9 14.5 8.3 11.8 12.9 C 8.2 9.7 11.7 7.7 9.3 11.0 MR A 1.3 5.6 17.8 2.8 8.7 14.0 B 11.8 94.5 187.2 11.1 132.1 643.6 C 2.2 42.1 113.8 6.7 18.7 60.9

WithAtheHybridcv.FB924,BthePlantaincv.Creoleblanche,andCtheDessert bananacv.902.

(4)

Table3

Nematodedensities(mean±SE)andrelativeabundancesintheﬁeldexperimentmeasured6monthsafterplanting(February2009)in96samples.

Variable Radopholussimilis Helicotylenchusmulticinctus Meloidogynespp. Rotylenchulusreniformis Hoplolaimusseinhorsti

Nematodedensity(numberspergramofroot) 21±5 55±13 11±3 5±1 0.3±0.08

Relativeabundance(%) 22.8% 59.4% 11.8% 5.7% 0.3%

bothnematodespecies.Themultiplicationratewas61forP. cof-feaeand114forR.similis(10.5and1.6timesless,respectively,than thoseonplantaincv.Creoleblanche).

On the hybrid cv. FB924, only culture time signiﬁcantly inﬂuencednematode multiplication(Dev=124.517; df=2,30; P<0.001).Ofthethreecultivars,thehybridcv.FB924wastheleast susceptibletobothnematodespecies.Attheendoftheexperiment, therewere550P.coffeaepergramoffreshroots,correspondingto amultiplicationrateof14,aratethatwas45timeslowerthanthat withtheplantaincv.Creoleblanche.

3.2. PFNcommunitycompositionandpopulationdynamicsin bananarootsintheﬁeldexperiment

Sixmonthsafterplanting(February2009),sixspeciesofPFN weredetectedinroot samplesofall pairsof banana.ThePFNs detectedintherootsincludedfourspeciesidentiﬁedinsoil sam-plesatplanting(R.reniformis,H.multicinctus,H.seinhorsti,R.similis) andonespecies,Meloidogynespp.,thatwasnotdetectedinthesoil (Table3).NoP.coffeaewasdetectedattheﬁrstsamplingbutafew individualsweredetectedinsubsequentsamples(datanotshown). ThecommunitywasdominatedbyH.multicinctusand R.similis

(59.4%and22.8%,respectively).BetweenFebruary2009andJuly 2010,PFNdensitiesincreasedsharply,andthisincreasewas signif-icantlyassociatedwithtimeafterplantingandnematodespecies (Table4).Thepercentageoftheﬁeldcommunityrepresentedby

H.multicinctusincreasedfrom58%inFebruary2009to83%inJuly 2010,whilethatrepresentedbyR.similisdecreasedfrom22to13% forthesamesampletimes.ThedensitiesofcombinedPFNincreased withtimefrom92pergramrootattheﬁrstsamplingto648per gramrootattheﬁnalsampling.

3.3. Factorsaffectingthenematodecommunityintheﬁeld experiment:bananagenotypecombinationsandtime

Thegenotypesofbananashada majorimpactonthe densi-tiesofnematodes(Table4).Thecomparisonofallpossiblepairs ofbananavarietiesonR.similisandH.multicinctus,whicharethe twoofthemostdamagingtoroots,showsthatnumbersofthese nematodeswereincreasedbygenotypeBbutdecreasedby geno-typeA(Fig.2).PFNdensitieswerehighestwiththeBBpair(plantain

Fig.2. Densities(mean±standarderrors)ofR.similisandH.multicinctusinroot samplesfrompairedplantingsasaffectedbysamplingtimeandgenotypesofthe pairs.Speciesrefertonematodespecies,genotypepairreferstoAA,BB,CC,AB,AC, andBC(withAthehybridcv.FB924,Btheplantaincv.Creoleblanche,andCthe dessertbananacv.902).

cv.Creoleblanche);almost2yearsafterplanting,PFNinfestations ontheBBpairhadincreasedto1081nematodespergramoffresh roots.WhengenotypeB(plantaincv.Creoleblanche)was associ-atedwithgenotypeA(hybridcv.FB924)orC(dessertbananacv. Table4

ResultsoftheanalysisofdevianceonnematodedensitiesinrootsintheﬁeldexperimentusingaGLMwithQuasiPoissonerror.

Sourceofdeviance df Residualdf Deviance Residualdeviance P-value

Sample 1 2302 592760 108 ns

Species 5 2297 286918 305841 <0.0001

Genotypepair 5 2292 272877 14041 <0.0001

Time 1 2291 230565 42312 <0.0001

Abundanceinsoil 1 2290 230110 455 ns

Species×Genotypepair 25 2265 225417 4693 ns

Species×Time 5 2260 220001 5416 <0.0001

Species×Abundanceinsoil 4 2256 212604 7397 <0.0001

Species×Genotypepair×Time 30 2226 210029 2575 ns

Species×Time×Abundanceinsoil 5 2221 205942 4087 <0.0001

df:degreeoffreedom.

Speciesreferstonematodespecies,GenotypepairreferstoAA,BB,CC,AB,AC,andBC(withAthehybridcv.FB924,Btheplantaincv.Creoleblanche,andCthedessertbanana cv.902).

Timereferstotimeofsampling.

(5)

902),thedensitiesofPFNwerelower(760and589nematodesper gramoffreshrootforABandCB,respectively)thaninthepurestand pairs(BB).ThecompositionofthecommunitywassimilarforBB andCBpairsandshowedlessR.similisinfestationforAB combina-tions(11%oppositeto16%forBBcombination).Incontrast,theAA pairsupportedthelowestdensitiesofR.similisandofallPFNs.

4. Discussion

Thegrowthchamberexperimentshowedthat,ofthethree vari-eties tested,the plantain cv.Creole blanche is by farthemost susceptibletonematodes.ThehighmultiplicationrateforP. cof-feaeonthisvarietyis consistentwiththeworkofSpeijeretal. (2001)andconﬁrmsthatmonocultureofthisplantaincultivar(like monocultureofmany otherplantain cultivars)shouldleadtoa fastincreaseofthemostdamagingPFNspeciesandtothe over-allunsustainabilityofthecroppingsystem(Coyneetal.,2005).The dessertbananacv.902showedanintermediatelevelof susceptibil-ityforbothinoculatednematodespecies,andthehybridcv.FB924 showedthelowestlevelofsusceptibility.Theseresultsconﬁrmthat thetestedvarietieshaveawiderangeofmultiplicationratesforat leasttwodamagingPFNspecies(Quénéhervéetal.,2009a,b).

Atplantingin theﬁeldexperiment, thesoil nematode com-munitywasdominatedbythereniformnematode,R.reniformis, whichwaspresentinlargenumbersinallsamples.Other nema-todespecies,includingR.similis,H.multicinctus,H.seinhorsti,and

P.coffeae,werepresentbutwithirregularandsparsedistributions. Thisdiverse PFN community is typicalof bananamonoculture, i.e.when bananafieldsarereplanted shortlyafter theprevious bananacropshavebeendestroyed.In ourcase, theexperiment wasstartedjustafterweedsinvadedthisoldbananaplantation. WeedsaffectthestructureofthePFNcommunity (Duycketal., 2009;Quénéhervéetal.,2006a).Thesixpairsofgenotypesshowed markedlydifferentPFNcommunitiesandPFNdensitiesattheend of the field experiment. The pairing of the plantain cv. Creole blanchewithitself(BB)supportedthehighestnumbersofPFNs, andthenexthighestnumbersweresupportedbythepairingof plantainandthehybridcv.FB924(AB).Incontrast,thepairingof Cavendishandhybridcv.FB924(AC)supportedthelowest PFN densities.Comparisonofthesepairsindicatesthatthegenotype oftheplantaincv.Creoleblancheisnotonlythemostsusceptible butisalsothelargestreservoirofPFNs.Thepairingofthehybrid cv.FB924withitself(AA)supportedthelowestproportionsand densitiesofR.similisthroughouttheexperiment.Twoyearsafter planting,AAandBBexhibitedthelowestandhighestPFN densi-ties,respectively.Allotherpairinghadintermediatenumbersof PFN.Wecanconcludethatthedepressiveeffectduetothemost resistantvarietyofthepairismoderated.However,thepairingof themostsusceptiblevarietywithoneoftheothertwovarieties (pairABorBC)appearstobesufficienttodecreasethePFN den-sitiestoa levelsimilartotheonesobserved forpairCC,which supportedanintermediatedensitiesofPFNs.PFNshavedifferent levelsofpathogenicityandaffectdifferentlythegrowthofbananas. AlthoughH.multicinctuswasdominatingthecommunity,itisnot themostdamagingonbanana(effectonbunchweight)asshownby Moensetal.(2006).

IncontrasttoCadetetal.(2007),weshowaneffectofcrop mix-turenotonlyonthePFN densitiesbut alsoonPFN community structure. In our study, the changes in community composi-tionamongthegenotypecombinationsmainlyinvolveabalance betweennematodespeciesandinterspeciﬁccompetitionforfood resources.Theuseofmixturescausedtherelativeabundanceof

H. multicinctus to increase while that of R. similis to decrease slightly, which wasconsistent withresults, obtainedwithnew bananahybridsbyTixieretal.(2008).Thiscanbeexplainedbythe

differencesinthePFNmultiplicationratessupportedbythetested genotypes.Thebananarootdynamicscanalsoaltertheratioof

H.multicinctus toR. similis. Indeed,the proportionof old roots increasedinolderbananaplants,whichareapotentialresourcefor

H.multicinctusbutnotforR.similis,whichpreferyoungerbanana roots(Quénéhervé,1990).Thisdifferenceinresourcepreference probablycontributedtothesuccessionthatweobservedinthePFN community.

Fromapracticalpointofview,theintroductionofhybridFB924 inaformermonoculturecomposedofplantainorCavendishwould bebeneficialforPFNcontrol.Inaddition,thishybridisalso resis-tanttoblackSigatokadisease,e.g.,theblackSigatokacausedbythe fungusMycosphaerellafijiensis(Abadieetal.,2009).Conversely,the introductionofdessertbananaorplantainintoacroppingsystem solelybasedonhybridcv.FB924wouldtendtodilutetheexisting resistanceandthereforeincreasetheglobalinfestationof nema-todes.Themainreasonforthelimiteduseofvarietalmixturesis thatmodernagriculturegenerallyrequiresuniformityincultural practicesandharvest.Inthecaseofbanana,however, monocul-tivarplantationsalready containunsynchronizedpopulationsof bananaplants(Tixieretal.,2004),leadingtoheterogeneous cul-turalpracticesafteronlytwocroppingcycles.Insuchconditions, itseemspossiblethatfarmerswouldbeabletomanagea com-plexplantpopulationthatincludesmorethanonecultivar.Because harvestofbananaisalwaysmanual,itappearsreasonableto orga-nizeseparateharvestsfortwoormorecultivars,whichallowthe targeting of different marketswith fruits harvested within the sameplot,e.g.,localmarketandexport.Suchinnovativesystems are alsoimportant to addressenvironmental and health issues (pesticideresidues)thatareparticularlyimportantwhenbanana plantpopulationisunsynchronized,ascommonlyfoundin small-holderplots(Tixieretal.,2007).Forsmallholders,theuseofcrop mixturesprovidesaninterestingperspective,especiallywhenno rotation,fallows,orchemicaltreatmentsarepossible. Neverthe-less, for being efficient, crop mixture systems need to include atleasthighlytolerantcultivaragainstthetargetedpest.These systemsmayhelp togrowthemostfavouritecultivarsin miti-gatedlevelsofpests.Inproductionareaswhereotherdiseasesare hamperingtheproduction ofbanana, theuseofa varietal mix-ture(includingtolerantvarieties)maylimittheriskofemergence ofpesticide-resistantstrains.Suchstrategiesshouldbemanaged fromthefieldscaletothelandscapescale,asisthecasewithrice (Wolfe,2000).

By altering the composition of the PFN community so that thereisareduceddensityofthemostdamagingspecies,varietal mixtures combiningseveralresistances couldbea useful strat-egyforimprovedmanagementofPFNsonbananas.Thisstrategy appearstobeparticularlyappropriatewithextremely suscepti-blecultivarsofsuchplantains.Insuchsystems,specialattention hastobepaidinthechoiceofvarietiesintheplantmixturein ordernotonlytointroducegeneticdiversitybutalsotoincrease thefunctional diversitywithrespecttopestresistance(Mundt, 2002).Attentionshouldalsobepaidtothespatio-temporal pat-tern ofPFNs, especially onthe capacity of varietal mixtures to suppressnematodedissemination.Recognizingtheeffectof vari-etalmixturesonmultiplepestsanddiseasesisalsoakeytothe designofinnovativeandefﬁcientcroppingsystemsbasedoncrop mixtures.

Acknowledgments

ThisworkwassupportedbyCIRADandIRDfunds,bytheSYBAN projectfromtheFrenchMinistryof Ecology,Sustainable Devel-opment(grantCV070000779),andbythe“sustainablecropping systemsdesign”projectfromE.U.ERDF(grantPRESAGE30411).

(6)

References

Abadie,C.,Chilin-Charles,Y.,Huat,J.,Salmon,F.,Pignolet,L.,Carlier,J.,Lescot,T.,Côte, F.,Jenny,C.,2009.Newapproachestoselectcultivarsofbananawithdurable resistancetoMycosphaerellaleafspotdiseases.ActaHorticulture828,171–178. Cadet,P.,Berry,S.D.,Leslie,G.W.,Spaull,V.W.,2007.Managementofnematodes andastalkborerbyincreasingwithin-ﬁeldsugarcanecultivardiversity.Plant Pathology56,526–535.

Chabrier,C.,Queneherve,P.,2003.Controloftheburrowingnematode(Radopholus similisCobb)onbanana:impactofthebananaﬁelddestructionmethodonthe efﬁciencyofthefollowingfallow.CropProtection22,121–127.

Coyne,D.L.,Rotimi,O.,Speijer,P.,DeSchutter,B.,Dubois,T.,Auwerkerken,A., Tenk-ouano,A.,DeWaele,D.,2005.Effectsofnematodeinfectionandmulchingonthe yieldofplantain(Musaspp.,AAB-group)ratooncropsandplantationlongevity insoutheasternNigeria.Nematology7,531–541.

Crawley,M.J.,1993.GLIMforEcologists.BlackwellScientiﬁcPublications,Oxford. Duyck,P.F.,Pavoine,S.,Tixier,P.,Chabrier,C.,Quénéhervé,P.,2009.Hostrangeasan

axisofnichepartitioningintheplant-feedingnematodecommunityofbanana agroecosystems.SoilBiology&Biochemistry41,1139–1145.

Gowen,S.R.,Quénéhervé,P.,Fogain,R.,2005.Nematodesofbananaandplantain. In:Luc,M.,Sikora,R.,Bridge,J.(Eds.),PlantParasiticNematodesinSubtropical andTropicalAgriculture.,2nded.CABI,London,UK,pp.611–643.

Hajjar,R.,Jarvis,D.I.,Gemmill-Herren,B.,2008.Theutilityofcropgeneticdiversity inmaintainingecosystemservices.AgricultureEcosystems&Environment123, 261–270.

Lassoudière,A.,2007.Lebananieretsaculture.Quae.

Malezieux,E.,Crozat,Y.,Dupraz,C.,Laurans,M.,Makowski,D.,Ozier-Lafontaine,H., Rapidel,B.,deTourdonnet,S.,Valantin-Morison,M.,2009.Mixingplantspecies incroppingsystems:concepts,toolsandmodels.Areview.Agronomyfor Sus-tainableDevelopment29,43–62.

Meung,H.,Zhu,Y.Y.,Revilla-Molina,I.,Fan,J.X.,Chen,H.R.,Pangga,I.,Cruz,C.V., Mew,T.W.,2003.Usinggeneticdiversitytoachievesustainablericedisease management.PlantDisease87,1156–1169.

Moens,T.,Araya,M.,Swennen,R.,Waele,D.,2006.Reproductionandpathogenicity ofHelicotylenchusmulticinctus,MeloidogyneincognitaandPratylenchuscoffeae, andtheirinteractionwith RadopholussimilisonMusa. Nematology8,45– 58.

Mundt,C.C.,2002.Useofmultilinecultivarsandcultivarmixturesfordisease man-agement.AnnualReviewofPhytopathology40,381.

O’Hara,R.B.,Kotze,D.J.,2010.Donotlog-transformcountdata.MethodsinEcology andEvolution1,118–122.

Quénéhervé,P.,1990.Spatialarrangementofnemadesaroundthebananaplant intheIvory-Coastrelatedcommentsontheinteractionamongconcomitant phytophagousnematodes.ActaOecologica– InternationalJournalofEcology 11,875–886.

Quénéhervé,P.,2009.Integratedmanagementofbanananematodes.In:Ciancio,A., Mukerji,K.G.(Eds.),IntegratedManagementinFruitCropsandForest Nema-todes.Springer,Netherlands,pp.3–61.

Quénéhervé,P.,Chabrier,C.,Auwerkerken,A.,Topart,P.,Martiny,B.,Marie-Luce, S.,2006a.Statusofweedsasreservoirsofplantparasiticnematodesinbanana ﬁeldsinMartinique.CropProtection25,860–867.

Quénéhervé,P.,Marie-Luce, S.B.B.,Grosdemange,F.,2006b.Une techniquede criblagevariétalprécocedesbananierscontrelesnématodesphytoparasites. Nematology8,147–152.

Quénéhervé,P.,Salmon,F.,Topart,P., Horry,J.P.,2009a. Nematoderesistance inbananas:screeningresultsonsomenewMycosphaerellaresistantbanana hybrids.Euphytica165,137–143.

Quénéhervé,P.,Valette,C.,Topart,P.,duMontcel,H.T.,Salmon,F.,2009b.Nematode resistanceinbananas:screeningresultsonsomewildandcultivatedaccessions ofMusaspp.Euphytica165,123–136.

RDevelopmentCoreTeam,2009.R:ALanguageandEnvironmentforStatistical Computing.RFoundationforStatisticalComputing,Vienna,Austria. Seinhorst,J.W.,1950.Debetekenisvandetoestandvandegrondvoorhet

optre-denvanaantastingdoorhetstengelaaltje(Ditylenchusdipsaci(Khün)Filipjev). TijdschriftoverPlantenziekten56,289–348.

Seinhorst,J.W.,1962.Modiﬁcationsoftheelutriationmethodforextracting nema-todesfromsoil.Nematologica8,117–128.

Smithson,J.B.,Lenné,J.M.,1996.Varietalmixtures:aviablestrategyforsustainable productivityinsubsistenceagriculture.AnnalsofAppliedBiology128,127–158. Speijer,P.R.,Rotimi,M.O.,DeWaele,D.,2001.Plant parasiticnematodes asso-ciatedwithplantain(Musaspp.,AAB-group)insouthernNigeriaandtheir relative importance compared to other biotic constraints. Nematology 3, 423–436.

Tixier,P.,Chabrier,C.,Malézieux,E.,2007.Pesticideresiduesinheterogeneousplant populations,amodel-basedapproachappliedtonematicidesinbanana(Musa

spp.).JournalofAgriculturalandFoodChemistry55,2504–2508.

Tixier,P.,Malezieux,E.,Dorel,M.,2004.SIMBA-POP:acohortpopulationmodel forlong-termsimulationofbananacropharvest.EcologicalModelling180, 407–417.

Tixier,P.,Risède,J.M.,Dorel,M.,Malézieux,E.,2006.Modellingpopulationdynamics ofbananaplant-parasiticnematodes:acontributiontothedesignofsustainable croppingsystems.EcologicalModelling198,321–331.

Tixier,P.,Salmon,F.,Chabrier,C.,Quénéhervé,P.,2008.Modellingpest dynam-ics of new crop cultivars: the FB920 banana with the Helicotylenchus multicinctus–RadopholussimilisnematodecomplexinMartinique.Crop Protec-tion27,1427–1431.

Wolfe,M.S.,1985.Thecurrentstatusandprospectsofmultilinecultivarsand varietymixturesfordiseaseresistance.AnnualReviewofPhytopathology23, 251–273.

ScienceDirect

w w w . e l s e v i e r . c o m / l o c a t e / a p s o i l