Primary scab control using a 'during-infection' spray ... · Primary scab control using a “during-infection” spray timing and the effect on fruit quality and yield in organic

BASE Biotechnol. Agron. Soc. Environ.201014(3),423-439

Primaryscabcontrolusinga“during-infection”spraytimingandtheeffectonfruitqualityandyieldinorganicappleproductionLaurentJamar,MarcCavelier,MarcLateurCentrewallondeRecherchesagronomiques.DépartementSciencesduVivant.RuedeLiroux,4.B-5030Gembloux(Belgique).E-mail:[email protected]

Reçule10septembre2009,acceptéle2février2010.

Organic appleproduction inEuropedepends to agreat extenton theuseof copper fungicides for scabcontrol (Venturia inaequalis).Theobjectiveofthis6-yearstudy(2003-2008)conductedinBelgiumwastodeterminemeasuresforreducingthe use of copper fungicides in organic apple production.The effectiveness of a “during-infection” spray strategy usingwettablesulphur(withorwithoutcopper),limesulphur,potassiumbicarbonate,siliconandfivenaturalplantextracts(orangepeel,soapbark,teaseed,quinoaseedandgrapefruitseed)forcontrollingprimaryscabwasinvestigatedinasplit-plotfieldexperiment. Four apple cultivars that express a gradient of partial scab resistancewere included: a high scab-susceptiblecultivar (cv. ‘Pinova’), amedium scab-susceptible cultivar (cv. ‘Pirouette’) and two old cultivars expressing low to verylowscabsusceptibility(cvs.‘ReinetteHernaut’and‘ReinettedesCapucins’).Apartfromthesecultivars,fourmonogenicVfscab-resistantcultivars(cvs.‘Initial’,‘Topaz’,‘Zvatava’and‘JN20/33/58’)werealsoincludedintheexperimentalorchard.Inordertoreducetheamountoffungiciderequired,twostrategieswereused:aspecificspraytiminginvolvingsprayingduringtheinfectionprocesses,beforefungalpenetration,determinedbytheRIMprosoftwarewarningsystem,andatunnelsprayermachineforoptimaltreatmentapplications.Dependingontheyear,atotalof8-12applicationsweremadeannually.Underfieldconditions thatwerehighlyconducivedisease, lowratesofelementalsulphur(≤40kg.ha-1peryear)combinedwithlowratesofcopper(≤2.1kg.ha-1peryear)providedthebestscabcontrolandreducedscabseverityontheleavesandfruitsby85-100%,dependingontheyearandcultivar,comparedwiththeuntreatedcontrol.Inmostcases,thelimesulphurspraytreatment,whichusedmoreelementalsulphurbutdidnotusecopper,providedasimilarlevelofscabcontroltothecombinedwettablesulphurandcopperspraytreatment.Sulphur,potassiumbicarbonateandallplantextractssignificantlyreducedscabseverityonleavesandfruits.Ingeneral,thetreatmentsincreasedtheyieldofthehighandmediumscab-susceptiblecultivarsaswellasthatofthelowandverylowscab-susceptiblecultivars.Undertheseexperimentalconditions,noneofthetreatmentscausedphytotoxicity,increasedfruitrussetorledtoundesirablesoilandfruitresiduesatharvest.Thepotentialandlimitationsof“during-infection”sprayingasaprotectionstrategyagainstapplescabinorganicfarmingarediscussed.Keywords. Copper, disease management, lime sulphur, plant extract, potassium bicarbonate, scab resistance, Venturia inaequalis.

Protection contre la tavelure ciblée sur les infections primaires et effets sur la qualité des fruits et les rendements en production biologique de pomme.Laproductioneuropéennedepommesenagriculturebiologiquedépendfortementdesfongicidesàbasedecuivrepourlaprotectioncontrelatavelure(Venturia inaequalis).L’objectifdecetteétuded’uneduréedesixannées,menéede2003à2008,étaitderechercherlesmoyenspourréduirel’usagedefongicidesàbasedecuivreenproductionbiologiquedepommes.UnvergerexpérimentalimplantéenBelgique,selonundispositifexpérimentalensplit-plot,aétémisenplaceafind’étudierl’efficacitéd’unestratégiedepulvérisation«durant-infection»comparantlesapplicationsdesoufre(avecousanscuivre),debouilliesulfocalcique,debicarbonatedepotassium,d’unextraitdesiliceetdecinqextraitsnaturelsdeplante(pelured’orange,boisdePanama,grainesdethéoudequinoaetpépinsdepamplemousse)pourlaluttecontrelesinfectionsprimairesdetavelure.Leseffetsdestraitementsontétéétudiéssurunesériedequatrevariétés(cvs)depommesprésentantungradientdeniveauxderésistancepartielleàlatavelure:unevariététrèssensible(cv.‘Pinova’),unemoyennementsensible(cv.‘Pirouette’)etdeuxanciennesvariétéspeuàtrèspeusensibles(cvs.‘ReinetteHernaut’et‘ReinettedesCapucins’).Parailleurs,unesériedequatrevariétésrésistantespossédantlegèneVfontégalementétéintégréesdansleverger(cvs.‘Initial’,‘Topaz’,‘Zvatava’et‘JN20/33/58’).Danslebutderéduiredefaçonoptimalelesquantitésdefongicidesàappliquer,lesstratégiessuivantesontétéexpérimentées:unpositionnementdestraitementsimpliquantdespulvérisations

424 Biotechnol. Agron. Soc. Environ. 201014(3),423-439 JamarL.,CavelierM.&LateurM.

1. IntroductIon

Apple scab caused by Venturia inaequalis [Cooke]Winter is amajor disease in apple production in theworld’s temperate zones (MacHardy, 1996). Mostcommercial apple cultivars are very susceptible toscab,andincommercialappleorchardsveryfrequentfungicideapplications(15-22annually)areneededtocontrolapplescab,dependingonweatherconditions,diseasepressureandcultivarsusceptibility(Holbetal.,2005b). Environmental considerations are becomingincreasinglyimportantandinteresthasthereforeturnedfromconventionalorintegratedproductiontoorganicappleproduction,wheremanagementpracticesdifferfromthoseinconventionalandintegratedproduction.In addition, consumers increasingly demand applesfree of any synthetic chemical residues. In organicapplegrowingcontexts,onlyafewapprovedchemicalcompounds are available for disease control, basedmainlyonsulphurandcopper(Holb,2008).Prolongeduseofcopper-basedcompoundscouldresultincopperlevels exceeding the international official limit of36 mg.kg-1 soil in European orchards (Holb, 2008);these levels have been shown to induce a negativeimpact on soil ecology and earthworm populations(vanRhee,1976;Paolettietal.,1998).Consequently,someEuropeancountries, includingTheNetherlandsand Scandinavian countries, have banned copper-basedproductsandothershave restrictedcopperuse(EC,2008).

The known remaining chemical option for applescabcontrolinorganicfarmingistheuseofelementalsulphurandlimesulphurproducts(Holbetal.,2003).Sulphur compounds are often less effective thancopper-basedcompounds,especially incoldweather,andapplescabcontrolneedslargeamountsofsulphurcompoundstocompensateforcopper.Severalstudieshave shown that the repeated application of largeamounts of sulphur compounds has ecotoxicological

andphytotoxicside-effects(Mills,1947;Kreiteretal.,1998;Holbetal.,2003;Palmeretal.,2003).

Organicgrowers often adopt a preventive controlstrategythatrequiresmoretreatmentsandnonusefultreatments. Early warning systems based on diseaseforecastingmodelsthatgivetimelyinformationaboutapplescabinfectionperiodshavethepotentialtolimittheuseoffungicides(MacHardy,1996;Trapmanetal.,1997;Hindorfetal.,2000;Jamaretal.,2008b).Mills(1944)reportedthatelementalsulphurisfullyeffectiveasarainapplicationonlyuptothetimewheninfectionoccurs. In a 2-year study, a “during-infection” spraystrategyinvolvingsprayingduringtheinfectionprocesswasdevelopedtoreducetheamountoffungicidesusedfor scab control in an organic apple orchard, usingcompoundswithpoorcurativeproperties(Jamaretal.,2008b;2010b).

An after-infection programme can significantlyreducefungicideapplicationsforscabcontrol(Funtetal.,1990;Holbetal.,2003).However,thistechnology,including the after-infection spray approach, has notbeen widely adopted by organic growers, probablybecause of the lack of compounds with curativeproperties and an accurate local warning system,including weather forecast management. Mostsulphur compounds have poor curative properties;theexceptionislimesulphur,whichmighthavegoodcurative properties against apple scab (Mills, 1944;Holbetal.,2003;Montagetal.,2005).AlthoughtheuseoflimesulphurispermittedunderEUregulationsfororganicproduction(EC,2008), it iscurrentlynotallowedinBelgium.

As an alternative to using copper compounds,severalnaturalsubstanceshavethepotentialtobeusedas fungicides that have a low eco-toxicologic profile(no adverse effects on the environment or humanhealth known) and are acceptable and economicallyfeasible in organic farming. Bicarbonates are one of

pendant lesprocessusd’infection,déterminéeà l’aidedusystèmed’avertissementdu logicielRIMproetunpulvérisateurtunnelpourl’applicationdestraitements.Suivantlesannées,untotalannuelde8à12applicationsontétéréalisées.Dansdesconditionsextérieurestrèsfavorablesaudéveloppementdetavelure,chaqueannée,defaiblesquantitésdesoufreélémentaire(<40kg.ha-1paran)combinéeàdefaiblesquantitésdecuivre(<2,1kg.ha-1paran)ontdonnélameilleureprotectioncontrelatavelure.Encomparaisondutémoinnontraité,cestraitementsontpermisderéduirelasévéritédetaveluresurlesfruitsde85%à100%selonlesvariétésetlesannées.Danslaplupartdescas,leschémadetraitementàbasedebouilliesulfocalcique,excluanttoutusageducuivre,adonnéquasilesmêmesrésultatsqueleschémacombinantlesoufremouillableetlecuivre.Lesoufre,lebicarbonatedepotassiumettouslesextraitsdeplanteontréduitsignificativementlasévéritédetaveluresurlesfeuillesetlesfruits.Touslestraitementsontaugmentélerendementenpommeaussibiensurlesvariétéstrèssensiblesetmodérémentsensiblesquesurlesvariétéstrèspeusensiblesàlatavelure.Danslesconditionsexpérimentalesdéfinies,aucundestraitementsappliquésn’aprovoquédelaphytotoxicité,nin’aaugmentélarugositésurfruitetfinalement,aucunrésiduindésirablen’aétédétectésur les fruitsà la récolteetdans lesol.Lepotentielet les limitesde lapulvérisation«durant-infection»,commemoyendeprotectioncontrelataveluredupommierenculturebiologique,sontdiscutées.Mots-clés. Cuivre, gestion des maladies, bouillie sulfocalcique, extrait de plante, bicarbonate de potassium, résistancevariétale,Venturia inaequalis.

Alowinputstrategyforscabcontrolinorganicappleproduction 425

severalcontroloptionsnowattractingattention.Theyhavebeenusedagainstseveralplantpathogens(Horstetal.,1992;Beresfordetal.,1996;Schulzeetal.,2003;Ilhanetal.,2006;Jamaretal.,2007a;2007b).Variousnaturalplantextractscontainingtriterpenoidsaponins,polyphenolsandspecificflavonoidshavebeenreportedto possess antifungal properties (Köhl et al., 2007;Bahraminejad et al., 2008; Bengstsson et al., 2009).Naturalsubstanceshavealsobeenreportedaselicitorsof resistance (Lateur, 2002) and specific mineralsubstanceshavebeenreportedtobeprotectiveagentsagainst several fungal pathogens in horticulture, e.g.silicon-basedproducts(Belangeretal.,1995;Köhletal.,2007).

Expanding thecultivationof lowscab-susceptibleorscab-resistantcultivarscarryingtheVfgenewouldbe another way of significantly reducing the use offungicidesforscabcontrol(Ellisetal.,1998;MacHardyetal.,2001).However,newscabraces,virulenttotheVf gene, have appeared in most European countries(Gessleretal.,2006),andthesemonogenicresistancecultivars therefore need to be carefully integratedinto anti-breakdown strategies. Apple cultivars withpolygenic resistance, deficient in most commercialcultivars, andnewcultivars that combinemonogenicand polygenic resistances are therefore of increasinginterestforbreedersandgrowers(Lateuretal.,1999;Gessleretal.,2006).

Although several field studies have evaluated thescabsusceptibilityofapplecultivarsunderunsprayedorchard conditions (Lateur et al., 1999), little infor-mationisavailableonthelong-termreactionofapplecultivars to scab under a clearly defined sprayingstrategyinorganicorchardsinvolvingvariousfungicidetreatmentsandtheirimpactonfruityieldandquality.

The aims of this 6-year studywere to contributetothereductionofcopperinorganicappleproductionbyinitiallyevaluatingtherelativeeffectivenessoffiveinorganicfungicides(sulphur,limesulphur,potassiumbicarbonates,siliconandcopper)andfivenaturalplantextracts(orangepeel,soapbark,teaseed,quinoaseedandgrapefruitseed)inprimaryscabcontrol,andthenevaluating over the long-term the effectiveness ofthe “during-infection” spray strategy using reducedamounts of fungicides. Effectiveness against scab,phytotoxicityandeffectsonyieldandfruitqualitywerestudied for high, medium and low scab-susceptiblecultivarsinamodernappleorchardsystem.

2. MaterIals and Methods

2.1. orchard design and equipment

The study was conducted over a period of 6 years,from2003to2008,intwoexperimentalappleorchards

planted in 2002 at Gembloux, Belgium. The firstorchard was composed of one high scab-susceptiblecultivar (‘Pinova’), one medium scab-susceptiblecultivar (‘Pirouette’), one low scab-susceptiblecultivar (‘ReinetteHernaut’) andonevery low scab-susceptible cultivar (‘Reinette desCapucins’) (Jamaret al., 2008b).The secondorchardwas composedoffourVfscab-resistantcultivars(cvs.‘Initial’,‘Topaz’,‘Zvatava’and‘JN20/33/58’).The treesweregraftedon dwarfing rootstocks (interstem of cv. ‘GoldenDelicious’)andplantedinasinglerowsystem(3.5x1.5m).A split-plot design based on six randomizedblockswith six replicateswas used in each orchard.Each block comprised six rows (plots) of 24 dwarftrees.Theplotsconsistedof24treesoffourcultivars.Thecultivarswererandomizedtosubplotswithintheplotsin4mono-cultivargroupsof6trees.Treedensitywas1,900treesperhainblocksor1,500treesperhainorchards,including20%ofecologicalzones.

The trees were grown according to the organicproduction standards (EC, 2008). The orchard soilwasaheavyloamcontaining1.2%Canditreceivedcattle compost twice and then in most years about1,000 kg.ha-1 of organic fertilizers (5% N) and2,000 kg.ha-1 of hydrated lime for pH enhancement(table 1). Any significant soil nutrient limitationwas registered.Treemaintenance training included acentrifugal training system (Simonet al., 2006).Thetreesreachedanaverageheightof3.25min2005.Forweedcontrolunder the tree rows,amechaniccover-cropmachinewasusedsuccessfullyfourtimesayear.Thegrassinthealleysbetweenthetreerowswaskeptshortbymowingregularly.LeafanalysisrevealedB,ZnandMndeficiency.Thereforefourcorrectingfoliartreatments were applied during the growing seasonfrom2004to2008.

From 15 March to harvest time in each year,potentialinfectionperiods,basedontheMillscriteria,were recorded in the field using aMETY computer-based weather recorder (Bodata Co. Ltd, Dordrecht,TheNetherlands)connectedtoaRIMproscabwarningsystem (Trapman et al., 1997) from 15 March toharvest time each year. The scab warning systemcalculated the infection periods based on hourlyrecordedmeteorologicaldata,themodifiedMillstable(MacHardyetal.,1989),thesimulationofascosporesrelease and the effect of previously used sprays. Inaddition, the local climate forecasts were registeredevery6hoursusingtheRIMprosoftwareforinfectionriskextrapolations.

2.2. treatments

Each year, the experiment was conducted on1,440 trees and involved 10 experimental spraytreatments each year. Each treatmentwas applied to


144trees(36treespercultivar).Thetreatmentswererandomizedinplotswithineachofthe12blocks.Eachtreatmentcombinationwasappliedonceineachblock.The experimental orchard could be considered ashomogeneousat thebeginningof theexperiment.Toprevent spray-drift and to reduce pesticide dispersal,the treatments were applied using a tunnel sprayer(Munckhof,5961CVHorst,TheNetherlands).Inordertocompletethevarioustreatmentsinasinglerun,thesprayerwasfittedwithsixindividualtanks.

The applied products and active ingredientsapplicationratearedescribedinthetable 2.

In thefirstorchard, the six spray treatmentswere(table 3):– untreatedcontrol(UC1);– potassiumbicarbonate-basedcompounds(AR1);– depending on the year, sulphur from wettable sulphur,silicon,delayedlimesulphur,soapbark,tea seedorquinoaseed(SF1);– dependingontheyear,productsusedinIntegrated Fruit Production (IFP), sulphur, grapefruit seed or coppercombinedwithorangepeel(RE1);

– sulphurfromlimesulphur(LS1);– sulphur from wettable sulphur combined with copperfromthehydroxideform(CS1).

In the second orchard, there were four spraytreatments(table 3):– untreatedcontrol(UC2);– sulphurfromwettablesulphur(SF2);– depending on the year, products used in IFP, a combinationofcopperandwettablesulphur(RE2);– othercombinationsofcopperandwettablesulphur (CS2).

Eachspraytreatmentwasmaintainedonthesameplotsfrom2003to2008.

Alltreatmentswereappliedatalowsprayrateof300l.ha-1.Eachyear,thetreatmentswereappliedduringthepotentialprimaryinfectionperiodidentifiedbytheRIMpro scab warning system. The treatments wereappliedduringtheinfectionprocess,afterascosporesinoculationandbeforehyphapenetration(Figure 1).Inpractice,thetreatmenttimings,definedasthenumber

table 2. Treatmentsandactiveingredientsapplicationrates—Traitements et taux d’application des substances actives.

code trademark (Manufacturer) active ingredient a.i. (%) a.i. application rate (%)a

arm Armicarb®100(HelenaChem.Co.,US) Potassiumbicarbonate(85%) 1.6(0.8)bcit Citripur(Pro-vera,Be) Grapefruitseedextract(33%) 0.15(0.15)cop KocideWG(GriffinEurope,Be) Copper(hydroxyde)(40%) 0.16(0.04)lms PolisolfuriodiCalcio(Polisenio,It) Elementalsulphur(23%) 1.6(0.8)myc Myco-Sin(AndermattBiocontrol,Ch) ClayandEquisetum arvense(100%) 1.0(1.0)pbi Potassiumbicarbonate(Sigma-Al.,Be) Potassiumbicarbonate(99%) 1.6(0.8)prv Prev-B2(Vivagro,Fr) Orangepeelextract(100%) 0.5(0.5)qui QLAGRI35(DesertKingInternat.,US) Soapbarktree,Quillaja saponaria(100%)1.0(1.0)sil Potassiumsilicate(Sigma-Aldrich,Be) Potassiumsilicate(34%) 0.1(0.1)sul Thiovitjet(SyngentaAgro,Fr.) Elementalsulphur(80%) 1.6(0.8)tea Teawet-TQ-Liquid(Nor-Natur,Dk) Teaandquinoaseedextract(100%) 1.0(1.0)aAlltreatmentswereappliedatalowsprayrate(300l.ha-1)—Tous les traitements ont été appliqués avec un faible volume d’eau (300 l.ha-1);bApplicationrateapartfromflowering(valuesinbracketsareapplicationrateduringflowering)—Taux d’application en dehors de la période de floraison (les valeurs entre parenthèses indiquent le taux d’application pendant la période de floraison).

table 1. Organicfertilizersandamendmentsappliedintheexperimentalorchard—Fertilisants organiques et amendements appliqués dans le verger expérimental.

compound 2002 2003 2004 2005 2006 2007 2008 MeanCompost0.5%N(t.ha-1) 30.0 - - 25.0 - - - 7.9Lin-waste5/2/2(t.ha-1) 0.5 1.0 1.0 1.0 0.8 1.0 0.7Patentkali(t.ha-1) 2.0 - 0.3 - - - - 0.3Naturalphosphate50%(t.ha-1) 1.0 - 0.3 - - - - 0.2Hydratedlime50%(t.ha-1) 2.0 1.0 2.0 2.0 2.0 2.0 2.0 1.8Nitrogenunit(u.N.ha-1)a 57.5 67.5 72.5 62.5 50.0 63.8 45.0 59.8Cab - - 4.0 4.0 4.0 4.0 4.0 2.8B,Mn,Znb - - 4.0 4.0 4.0 4.0 4.0 2.8aEstimationofnitrogenavailabilityforthecompostused:30%year1,20%year2,15%year3andforthelin-wasteused:50%year1and50%year2—Estimation de la disponibilité de l’azote fourni par le compost : 30 % l’année 1, 20 % l’année 2, 15 % l’année 3 et par le tourteau de lin : 50 % l’année 1 et 50 % l’année 2;bNumberoffoliartreatments—Nombre de traitements foliaires.


ofhoursmultipliedbythemeantemperatureindegreesCelsius(degree-hours,DH)betweentheonsetofrain(associatedwithinfection)andthetimeofapplication,werealwaysbetween50and300DH.Therefore, thetreatmentswereappliedjustbeforeoratthebeginningof the infection riskperiodsdetectedby theRIMproscabwarningsystem.Toanticipateinfectionperiods,theextrapolationsystemofRIMpro,using theshort-term weather forecasts, was used. In some cases,the treatments were applied even when RIMpro didnot indicate a primary infection risk on those days;potential infectionswerethenbasedonrevisedMillscriteria. A delayed spray treatment, consisting ofspraying12-24hafterthe“during-infection”spraying,wasalsoimplementedin2006withlimesulphur(lmsdelayed).

Between2004and2008,twoadditionaltreatmentswereapplied in twosecondary infection riskperiods

in the summer. All the treatments included twopost-harvest applications of 0.2% copper (from thehydroxide form) from 2002 to 2006, mainly forEuropeancanker(Nectria galligena)control.Limitedinsectcontrolwasuniformlyappliedforalltreatmentsand followed standard European organic guidelines(EC,2008).

The Polisolfurio di Calcio contained 23% ofelementalsulphur,whichwasconsideredastheactiveingredient content in this study. Armicarb®100 isa new formulation registered by the EnvironmentalProtectionAgency(EPA)andcanbeused inorganicfarming systems in the USA. Armicarb, Citripur,Prev-B2, Teawet TQ Liquid andQLAGRI 35werechosen for this study for their effectiveness undergreenhouse conditions and their adapted formulationfor foliar applications (Jamar, 2007; Jamar et al.,2007b).

table 3.Spraytreatmentsappliedfrom2003to2008inthetwoexperimentalorchards—Schémas de traitement appliqués de 2003 à 2008 dans les deux vergers expérimentaux.

orchard 1 2003 2004 2005 2006 2007 2008UC1(UntreatedControl) - - - - - copAR1 pbi−myca pbi arm arm arm cop−armSF1 sul sil sil lmsdelayed qui cop−teaRE1 ipm ipm sul sul cit cop−prvLS1 lms−sul lms−sul lms lms lms lmsCS1 cop−sul cop−sul cop−sul cop+−sul cop+−sul cop+−sulNumberoftreatmentsb 3+3+6 3+2+5 4+1+3 4+1+5 0+0+8 3+1+5

orchard 2 2003 2004 2005 2006 2007 2008UC2(UntreatedControl) - - - - - -SF2 sul sul sul sul sul sulRE2 ipm ipm cop+−sul cop+−sul cop++−sul cop++−sulCS2 cop−sul cop−sul cop−sul cop−sul cop+−sul cop+−sulNumberoftreatmentsb 3+3+5 3+2+4 4+1+3 4+1+5 0+0+8 3+1+5

Orchard1—verger 1: cvs. ‘Pinova’, ‘Pirouette’, ‘ReinetteHernaut’, ‘ReinettedesCapucins’;Orchard2—verger 2: cvs.‘Initial’,‘Topaz’,‘Zvatava’,‘JN20/33/58’;afortreatmentsexplanations,seetable 2 — pour l'explication des traitements, voir le tableau 2; the ‘ipm’ (Integrated ProductionManagement) includes dodine, captane, kresoxymméthyl, dithianon,pyriméthanilanddifénoconazoleatrecommendeddoses — l’« ipm » (système de production intégrée) implique l’usage de la dodine, du captane, du kresoxym méthyl, du dithianon, du pyriméthanil et du difénoconazole, aux doses recommandées;cop:includestreatmentsonlybeforeflowering — implique des traitements seulement avant la floraison;cop+:includesadditional0.04% copper treatments from flowering — implique des traitements supplémentaires de cuivre à 0,04 % à partir de la floraison;cop++:includesadditionaltreatmentsat0.04%copperfromfloweringtofruit-tipping-overstageandat0.08%copperfromfruit-tipping-overstage — implique des traitements supplémentaires de cuivre à 0,04 % pendant la floraison jusqu’au stade de basculement des fruits et à 0,08 % par la suite. Prv, tea: include treatments only afterflowering, and all othersinclude treatmentsbeforeandafterflowering — impliquent des traitements seulement après la floraison et tous les autres impliquent des traitements avant, pendant et après la floraison.In‘cop−sul’,‘cop+−sul’and‘cop++−sul’treatments,‘sul’wasassociatedwith‘cop’ifthetemperatureroseabove10°C —Dans les traitements ‘cop−sul’, ‘cop+−sul’ and ‘cop++−sul’, ‘sul’ a été associé avec le ‘cop’ si la température était supérieure à 10 °C;bnumberoftreatmentsappliedduringtheprimaryscabinfectionseasons,fromMarchtoJune(first,secondandthirdvalue=before,duringandafterflowering,respectively).From2004to2008,allspraytreatmentsincludedtwoadditionalsummerapplicationsof2%sulphur(forscabcontrol)andfrom2002to2006twoadditionalpost-harvestapplicationsof0.2%copper(forEuropeancankerNectria galligenacontrol)—Nombre de traitements appliqués pendant la période d’infection primaire, du mois de mars au mois de juin (première, deuxième et troisième valeur = avant, pendant et après la floraison, respectivement). De 2004 à 2008, tous les schémas de traitements impliquent deux applications supplémentaires d’été à 2 % de soufre (pour lutter contre la tavelure) et de 2002 à 2006, deux applications supplémentaires après la récolte à 0,2 % de cuivre (pour lutter contre le chancre Nectriagalligena).


A recovery system that included a continuousrecycling process in the tunnel sprayer led to savinganaverageof30%oftheappliedspraymixtureswhenspraying under moderate wind speed (≤ 15 km.h-1)in a 6-year-old apple orchard (Jamar et al., 2010c).The amountof active ingredients appliedper ha andperyearthereforeneedalsotoincludea30%productsaving.

2.3. scab incidence and severity assessment

Eachyear,diseaseassessmentsontheleavesandfruitsweremade.For leaf severity assessments, 10 shootspertreewererecordedabout60daysafterflowering.Observationsweremadeon10olderleavespershoot.A1-9globalscab intensityscalewasusedwhereby:1=noscablesions;2=≤1%infectedleaveswithatleastonelesion;3=≤5%infectedleaveswithatleastone lesion; 4 = 5-50% infected leaves with at leastone lesion; 5=≥ 50% leaveswith lesions andwith≤5%leafareaspotted;6=5-25%leafareaspotted;7=25-50% leaf area spotted; 8=50-75% leaf areaspotted;and9=maximuminfection,leavesblackwithscab(Lateuretal.,2002).

Diseaseassessmentonfruitwasmadeonharvestedfruitsfrom15to31Octobereachyear.Thepercentage

of diseased fruit was assessed for the whole yieldcollectedperplot.Fruitincidence(FI)wascalculatedas the proportion of infected fruitswith at least onescab lesion.Scabseverityon fruitswasassessed forthewholeyieldfromeachplotbasedonascaleof1to6followingthestandarddiagrammethodreportedbyCroxall et al. (1952)whereby: 1 = no scab; 2 =0-1%;3=1-5%;4=5-20%;5=20-50%;6=≥50%fruitsurfacecoveredbyscab.Fruitseverity(FS)wasdefined as the mean proportion of the fruit surfacecovered by scab, and it was calculated using thefollowingequation:

wheren1ton6representthenumberoffruitsineachcategory;ntrepresentsthetotalnumberoffruits;andthecoefficients0,0.5,2.5,12.5,35and75representthe median of the lower and upper boundaries ofclasses1to6,respectively.

2.4. Yield, fruit number and size, and phytotoxicity

The fruits were harvested from 1 September to 15October, depending on cultivar maturity. When allfruits per plot were collected, yieldwas determined

Figure 1. Schematic illustration of the “during-infection” spray timing [treatment applied 0-320degree-hours (DH) afterthewettingstart]inrelationtoleafwetnessduration,infectionrisksaccordingtoMillscriteria,fungus(Venturiainaequalis)activity and the approximateRIMpro infection starting-point—Représentation schématique de la stratégie de traitement « durant-infection » [traitements appliqués de 0 à 320 degrés-heures (DH) après le début de la pluie] en relation avec la durée d’humectation du feuillage, les risques d’infections selon les critères de Mills, l’activité du champignon (Venturiainaequalis) et le point de départ approximatif du signal RIMpro.

n1x0+n2x0.5+n3x2.5+n4x12.5+n5x35+n6x75nt nt nt nt nt ntFS=

Preventive treatment Curative treatment

During-infectiontreatment

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Incubation period14 to 21 days

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Infection or germination period

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0 125 175 250 320 DH

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pen

etra

tion

and

sym

pto

ms

rate

s


according to the weight of all harvested fruits andwasclassifiedintofoursizecategories(<65;65-75;75-85and>85mm).Thenumberofharvestedfruitsassociatedwithyieldwasassessedforeachplot.Nohandorchemical thinninghadbeendoneduring thegrowingseasonsforanyofthecultivars.

Fruitrussetwasassessedonthewholeyield,afterharvest,accordingtoEPPO/OEPPstandardsbasedonascaleof1to4whereby:1=norusset;2=<10%;3=10-30%;4=30-100%russetonthefruitsurfacearea.Thefruitrussetseverityindex(FR)wascalculatedasdescribedby Jamaret al., 2008b.Leafphytotoxicityobservationsweremadeonfivespur-leafclusterspertreeinJune.Leafphytotoxicitywasassessedona0-5scale,asdescribedbyHolbetal.(2003)andfollowingEPPO/OEPPstandards.

2.5. copper residues in soil and fruits

Sincesoilmicrobialactivityandearthwormabundanceare particularly sensitive to copper, chemical soilparameters and soil copper content (EDTA andammoniumacetate extractionmethod), in particular,were assessed every 2 years in the experimentalorchards,inuntreatedcontrol(UC)plotsaswellasincopper-treated (CS) plots.Each assessment includedfivereplicatespertreatment.

In 2006, on fruits of the cultivars ‘Pinova’ and‘Topaz’, fungicide residueswereassessedon treatedfruits(CS)incomparisonwithuntreatedfruits(UC).Analyses were made using an overall fruit or peelmineralanalysisatharvestandincluded10-fruitsub-samples replicated six times for each treatment andcultivar.

2.6. data analysis

Yearfactorswereanalyzedseparatelyforeachvariable.Thepercentagedataweretransformedinarcsinebeforeperformingananalysisofvariance.Notransformationwas carried out for other measures. The data wereanalyzed using SAS software version 9.1 (SASInstitute,Cary,NorthCarolina,USA)andtheStudent-Newman-Keuls multiple range test was applied todeterminewhetherthedifferencesbetweentreatmentswere significant. All the statistical evaluations wereconductedatasignificancelevelofP=0.05.

3. results

3.1. apple scab assessments

From2003to2008,theRIMproscabwarningsystemidentifiedamaximumof10potentialinfectionperiodsper year in Gembloux, with 0-2 infection periods

occurringduringthefloweringperiod.Between2003and 2008, the number of primary infection periodsper year, based on the revised Mills criteria, wereclassifiedassevere in3-5 instances,moderate in2-6instancesand low in2-5 instances.Therewasheavydisease pressure in the primary infection seasons,especiallyin2005,2006and2008,asrevealedbythehighscabinfectionratesrecordedintheuntreatedcv.‘Pinova’plots (Figure 2). In2007 theprimaryapplescab infectionswereparticularly lowdue toawarm,dryspring.

Based on apple scab symptoms present in theuntreated plots in the orchard (Figure 2), aswell asapplescabsymptomspresent inotherlocaluntreatedorchardsincludingcvs.‘Gala’and‘GoldenDelicious’(Lefrancq et al., 2009), the following susceptibilityratingsforthecultivarscanbeproposed:hightoveryhigh scab-susceptible cultivars for cvs. ‘Pinova’,‘Initial’, ‘Zvatava’ and ‘JN20/33/58’;medium scab-susceptiblecultivars forcvs. ‘Pirouette’and ‘Topaz’;and low scab-susceptible cultivars for cvs. ‘ReinetteHernaut’and‘ReinettedesCapucins’.Veryfewscabinfections were recorded on the untreated Vf scab-resistantcultivarsupto2007,exceptforthecv.‘Initial’,butin2008thescabinfectionswereverysevereonalltheVf scab-resistant cultivars, indicating that theVfscabgeneprotectionhadbeencompletelybrokendownby new virulent races except for cv. ‘Topaz’, whichstill expressed good residual resistance after the Vfgenebreakdown(Figure 2).Underourconditions,thetreatmentsdidnotcompletelypreventthepropagationof these new virulent scab races between 2006 and2008(Figures 3and6).

A total of 8-12 treatmentswere applied annually,dependingontheyear.Ineachyear,allthetreatmentssignificantly reduced apple scab compared with theuntreated control for the high scab-susceptible cvs.‘Pinova’ and ‘Initial’. In eachyear, for cvs. ‘Pinova’and ‘Initial’, the combined copper and wettablesulphur treatments CS1, CS2 and RE2 gave thebest apple scab controlonboth the leaves and fruits(Figures 3 and4). For theCS spray treatments, theamountofelementalsulphurandcopperusedannuallywerelessthan40and2.1kg.ha-1,respectively.Inboth2003and2004,CS1wasaseffectiveastheIFPcontrolmanagement(RE1).Between2003and2007,withthetreatmentsCS1, thescabseverityonthefruitsof thescab-susceptiblecv. ‘Pinova’wasreducedbyat least97%comparedwithwatercontrolandby85%in2008(Figure 4).Oncv.‘Pinova’,inboth2005and2006,thelimesulphurtreatments(LS1)resultedinsignificantlylower scab damage on both the leaves and fruitscompared with wettable sulphur treatments (RE1),although the same amount of elemental sulphurwasapplied. In2006, thedelayed lime sulphur treatment(SF1),was less effective than the “during-infection”


limesulphur treatment (LS1),although the timingoftheapplicationsdifferedbynomorethan0-144DH.Inmostcases,forthehighandmediumscab-susceptiblecultivars the lime sulphur treatment LS1 resulted inalmostthesamelevelofscabcontrolasthatachievedby thecombinedcopperand sulphur treatmentsCS1(Figure 4).

Each year the potassium bicarbonate treatments(AR1)significantly reducedapplescabseverityon theleavesandfruitscomparedwithwatercontrol(Figures 3and 4). In most cases, AR1 was as effective as thewettablesulphurtreatment(RE1)usedin2005and2006,using the same amount of active ingredients for bothtreatments. In 2005, the potassium silicate treatments

Figure 2.Evolutionof overall scab severity on leaves (1-9 scale: 1= no scab, 9=maximum scab infection) assessed inuntreatedcontrolplots60daysafterflowering,foreachcultivarfrom2003to2008—évolution de la sévérité globale de la tavelure sur les feuilles (échelle de 1 à 9 : 1 = pas de symptôme de tavelure, 9 = infection maximum de tavelure) évaluée sur les parcelles « Témoin non traité », 60 jours après la floraison pour chaque variété de 2003 à 2008.

Errorbarsdenotestandarderrorofthemean(n=6)—Les barres d’erreur représentent l’erreur standard de la moyenne (n = 6).

Figure 3.Effectsofspraytreatmentsonoverallscabseverityonleaves(1-9scale)assessed60daysafterfloweringfrom2003to2008forcvs.‘Pinova’and‘Initial’,themostsusceptiblecultivarsineachorchard—Effets des schémas de traitement sur la sévérité globale de la tavelure (échelle de 1 à 9) évalués 60 jours après la floraison de 2003 à 2008 sur les variétés ‘Pinova’ et ‘Initial’, les plus sensibles de chaque verger.

Fortreatmentsexplanations,seep426andtable 3—Pour l’explication des traitements, voir p 426 ettableau 3;Errorbarsdenotestandarderrorofthemean(n=6)—Les barres d’erreur représentent l’erreur standard de la moyenne (n = 6).

2003 2004 2005 2006 2007 2008 2003 2004 2005 2006 2007 2008

1

2

3

4

5

6

7

8

9

1

2

3

4

5

6

7

8

9Reinette des Capucins

Reinette Hernaut

Pirouette

Pinova

Topaz (Vf)

JN 20/33/58 (Vf)

Zvatava (Vf)

Initial (Vf)

Sca

b s

ever

ity o

n le

aves

Sca

b s

ever

ity o

n le

aves

YearYear

1

2

3

4

5

6

7

8

9

Sca

b s

ever

ity o

n le

aves

1

2

3

4

5

6

7

8

9

Sca

b s

ever

ity o

n le

aves

2003 2004 2005 2006 2007 2008 2003 2004 2005 2006 2007 2008Year Year

cv. ‘Initial’ cv. ‘Pinova’

UC1

SF1

LS1

AR1

RE1

CS1

UC2

RE2CS2

SF2


(SF1)at0.1%,usingthe“during-infection”strategy,didnotreducescabseverityonleaves,butdidreduceitveryslightlyonfruits.

In 2007 theQuillaja saponaria extract treatments(SF1)and thegrapefruit seedextract treatments (RE1)significantlyreducedthescabseverityonleaves,buttheweatherconditionswerenotconducivetothedevelopmentofscabepidemicsthatyear(Figure 3).In2008,boththeTeawetTQLiquid(SF1)andPrev-B2(RE1)treatmentsused during and after flowering significantly reducedscabincidenceandseverityonfruits,confirmingearliergreenhouseexperiments(Jamar,2007).

Scab control was more effective on the mediumscab-susceptible cv. ‘Pirouette’ than on the high scab-susceptiblecv.‘Pinova’(Figure 4).

3.2. Yield, fruit number and size

Inmost cases, comparedwith the untreated control,alltreatmentssignificantlyincreasedoverallyieldpertree(Figure 5).Ingeneral,thelimesulphurtreatments(LS1) did not affect mean yields per ha comparedwithwettable sulphur treatments (CS1). InCSplots,thecvs.‘Initial’,‘Topaz’and‘Pinova’werethemoreproductivecultivars,withanaveragemeanyieldperyear of 16.8, 16.7 and15.9kgper tree, respectively(Figure 6). For cv. ‘Pinova’, with a very high scabrate, theyieldvaluesonCS1plotswere2.6,4.6and2.0timeshigherthanintheuntreatedcontrolplotsin2005,2006and2008, respectively.For cv. ‘ReinettedesCapucins’,withavery lowscab rate, treatments

Figure 4. Effectsofspraytreatmentsonscabincidence(left)andseverity(right)ofthefruitatharvestfrom2003to2008forcvs.‘Pirouette’(mediumscab-susceptible)and‘Pinova’(highscab-susceptible)—Effets des schémas de traitement sur l’incidence et sur la sévérité de la tavelure sur les fruits récoltés, des variétés ‘Pirouette’ (modérément sensible) et ‘Pinova’ (très sensible) de 2003 à 2008.

Fruitincidence:proportionoftotalharvestedfruitswithatleastonespot—Incidence sur les fruits : la proportion des fruits récoltés avec au moins une tache;Fruitseverity:meanscabbedareaormeanproportionoffruitsurfacecoveredbyscab—Sévérité sur les fruits : surface moyenne tachée de tavelure ou proportion moyenne de la surface des fruits couverte de tavelure; Fortreatmentsexplanations,seep426andtable 3—Pour l’explication des traitements, voir p 426 et tableau 3;Errorbarsdenotestandarderrorofthemean(n=6)—Les barres d’erreur représentent l’erreur standard de la moyenne (n = 6).

Sca

b in

cid

ence

on

frui

ts (%

)

2003 2004 2005 2006 2007 2008

Year

0

20

40

60

80

100

UC1

SF1

LS1

AR1

RE1

CS1

cv. ‘Pirouette’

Sca

b s

ever

ity o

n fr

uits

(%)

2003 2004 2005 2006 2007 2008Year

0

4

8

12

16

20

cv. ‘Pirouette’ 24S

cab

inci

den

ce o

n fr

uis

(%)

2003 2004 2005 2006 2007 2008

Year

0

20

40

60

80

100 cv. ‘Pinova’

Sca

b s

ever

ity o

n fr

uis

(%)

2003 2004 2005 2006 2007 2008

Year

0

4

8

12

16

24 cv. ‘Pinova’

20

UC1

SF1

LS1

AR1

RE1

CS1


also increased yield compared with the untreatedcontrolUC1 in those yearswith high scabpressure(2005, 2006 and 2008). This is due largely to theeffectsonfruitnumberpertreeratherthanonmeanfruitweight (table 4 andFigure 7). Inmost cases,comparedwith the untreated control, all treatmentssignificantly increased the number of fruits per tree(Figure 7).

In most cases, compared with the untreatedcontrol, the CS treatments significantly reducedthe proportion of fruits smaller than 65mm on thehigh scab-susceptible cultivars (table 4). The CS1treatmentsignificantlyincreasedthemeancumulatedyieldofhighscab-susceptiblecultivars(cvs.‘Pinova’and ‘Initial’) in comparison with the untreatedcontrol, although on the low scab-susceptiblecultivars (cv. ‘Reinette des Capucins’) significantdifferencesbetweentreatedanduntreatedplotswerealsoregistered(table 4andFigure 6).

Noneof the treatmentsadverselyaffected leavesin either year (no phytotoxicity, leaf size reductionor necrotic damage).All the scores rangedbetween0 and 0.3 on the 0-5 scale used (data not shown).Noneofthetreatmentsadverselyaffectedfruitrussetcompared with the untreated control in any year,exceptforRE2ineither2007or2008.Forexample,in 2007, the average fruit russet incidence (with>2%russet)was16.2%fortheRE2spraytreatmentcompared with 1.2% for the CS2 spray treatment(datanotshown).

3.3. copper residues in soil and fruits

Copper residues on the standard and peel fruits atharvestweresignificantforcv.‘Pinova’inCS1plots,treatedwithcopperafterflowering(Figure 8).Forcv.‘Topaz’, no significant difference in copper residuesbetweentheUC2untreatedcontrolandCS2treatmentswasregistered.Standardandpeelfruitanalysisdidnotshowanysulphurresidueatharvestforcvs.‘Pinova’and‘Topaz’.Sulphurandcopperresiduesonthefruitsatharvestfromcombinedcopperandsulphurtreatments(CS1) were always far below the maximal residuelevel(LMR)permittedinapplebyECregulations(5and50mg.kg-1forcopperandsulphur,respectively).

Soilcoppercontentintheexperimentalorchardwaskept below 26.8mg.kg-1.Any significant differencesin copper soil content between CS and UC plotswereregisteredin2008,attheendoftheexperiment(table 5).

4. dIscussIon

The results presented in this study show that the“during-infection” spray strategy offers valuableadvantages for effective apple scab control with areducedamountoffungicideusesuchassulphur,limesulphur, copper, potassium bicarbonate and variousplantextractsonhighscab-susceptiblecultivars,underconditions conducive to scab infections. The most

Figure 5. Effectsofspraytreatmentsonoverallyieldforcv.‘Pinova’(highscab-susceptible)andcv.‘ReinettedesCapucins’(lowscab-susceptible)from2003to2008.—Effets des schémas de traitement sur les rendements globaux pour la variété ‘Pinova’ (très sensible à la tavelure) et la variété ‘Reinette des Capucins’ (très faiblement sensible à la tavelure) de 2003 à 2008.

Fortreatmentsexplanations,seep426andtable 3—Pour l’explication des traitements, voir p 426 et tableau 3; Treedensitywas1,900treesperhainblocksor1,500treesperhaintheoverallorchards,including20%ofecologicalzones—La densité de plantation était de 1 900 arbres par ha dans les blocs expérimentaux ou, si l’on considère les 20 % de zone de compensation écologique, 1 500 arbres par ha dans l’ensemble des vergers; Errorbarsdenotestandarderrorofthemean(n=6)—Les barres d’erreur représentent l’erreur standard de la moyenne (n = 6).

2003 2004 2005 2006 2007 2008Year

0

10

20

30

40 UC1

SF1

LS1CS1

RE1

AR1

cv. ‘Pinova’

Yie

ld (k

g p

er t

ree)

2003 2004 2005 2006 2007 2008Year

0

10

20

30

40 cv. ‘Reinette des Capucins’

Yie

ld (k

g p

er t

ree)

UC1

SF1

LS1CS1

RE1

AR1


Figure 6. Overallyieldatharvestinrelationtooverallscabseverityonleavesassessed60daysafterflowering(1-9scale),subjectedtoCSspraytreatmentscomparedwiththeUCuntreatedcontrolsfrom2002to2008—Poids total de fruits récoltés en relation avec la sévérité globale de la tavelure sur les feuilles (échelle de 1 à 9) évaluée 60 jours après la floraison, obtenu avec le schéma de traitement « CS » et le schéma témoin non traité « UC » de 2002 à 2008. Treedensitywas1,900treesperhainblocksor1,500treesperhainorchards,including20%ofecologicalzones—La densité de plantation était de 1 900 arbres par ha dans les blocs expérimentaux ou, si l’on considère les 20 % de zone de compensation écologique, 1 500 arbres par ha dans l’ensemble des vergers;Errorbarsdenotestandarderrorofthemean(n=6)—Les barres d’erreur représentent l’erreur standard de la moyenne (n = 6).

Yie

ld (k

g p

er t

ree)

Yie

ld (k

g p

er t

ree)

Yie

ld (k

g p

er t

ree)

Yie

ld (k

g p

er t

ree)

Yie

ld (k

g p

er t

ree)

Yie

ld (k

g p

er t

ree)

30

30

30 30

30

30

20

20

20 20

20

20

40

40

40 40

40

40

10

10

10 10

10

10

0

0

0 0

0

02003

2003

2003 2003

2003

20032004

2004

2004 2004

2004

20042005

2005

2005 2005

2005

20052006

2006

2006 2006

2006

20062007

2007

2007 2007

2007

20072008

2008

2008 2008

2008

20082002

2002

2002 2002

2002

2002

cv. ‘Pinova’

cv. ‘Pirouette’

cv. ‘Reinette Hernaut’ cv. ‘Zvatava’ (Vf)

cv. ‘JN 20/33/58’ (Vf)

cv. ‘Initial’ (Vf)Yield UC1 Yield UC2Yield CS1 Yield CS2Scab sev. CS1 Scab sev. CS2Scab sev. UC1 Scab sev. UC2

9

9

9 9

9

98

8

8 8

8

8

7

7

7 7

7

7

6

6

6 6

6

6

5

5

5 5

5

5

4

4

4 4

4

4

3

3

3 3

3

3

2

2

2 2

2

21

1

1 1

1

1

Sca

b s

ever

ityS

cab

sev

erity

Sca

b s

ever

ity

Sca

b s

ever

ityS

cab

sev

erity

Yie

ld (k

g p

er t

ree)

Yie

ld (k

g p

er t

ree)

30 30

20 20

40 40

10 10

0 02003 20032004 20042005 20052006 20062007 20072008 20082002 2002

cv. ‘Reinette des Capucins’ cv. ‘Topaz’ (Vf)9 98 87 76 65 54 4

3 3

2 21 1

Sca

b s

ever

ity

Sca

b s

ever

ityS

cab

sev

erity

Year Year


efficientspraytreatmentsusedforapplescabcontrolin this experiment (CS1 and CS2) never exceeded40kgofelementalsulphurand2.1kgofcopperperhaperyear,appliedinamaximumof12treatmentsperseason.Theseamountsoffungicidesarelessthan50%belowtheamountsusuallyusedtocontrolapplescabinorganicproductionunderhumidclimateconditions

(Ellis et al., 1998;Holb et al., 2003; Palmer et al.,2003;Holbetal.,2005b).Upto110kg.ha-1peryearofelementalsulphurcombinedwith8kg.ha-1peryearofcopperwereusedforscabcontrolinorganicappleproductioninTheNetherlands(Holbetal.,2001).Inaddition,theresultsofthisstudyshowedthat:– dilutedcopperisveryeffectiveundercoldweather conditions during early primary scab infection periods;– thelimesulphurtreatmentcanbeaseffectiveasthe combinedwettablesulphurandcoppertreatment;– the lime sulphur is more effective than wettable sulphur used alone, confirming the results of previous studies (Mills, 1947; Ellis et al., 1998; Holbetal.,2003).

A previous study (Jamar et al., 2010c) showedthatthespraydepositsateachsamplingpointofthetree canopy produced by the tunnel sprayer werenotsignificantlydifferentfromthestandardsprayer.Consequently, the performances obtained in thepresent study cannot be attributed to the specificcharacteristicsofthetunnelsprayer.

Thetreatmentswereappliedshortlyafterrainfallassociated with primary scab infections, during theinfectionprocess,sometimesondryingleaves.Atthis

table 4.Effectsofspraytreatmentsagainstscabonthemeancumulatedyieldandthemeanproportionoffruitsatasizeofbelow65mm,from2003to2008—Effets des schémas de traitement de protection contre la tavelure sur les rendements cumulés moyens et sur la proportion moyenne de fruits avec un calibre inférieur à 65 mm, de 2003 à 2008.

cultivar spray Mean cumulated Proportion of fruits < 65 mm (%)b

treatmenta yield (kgpertree) 2003 2004 2005 2006 2007 2008Pinova UC1 56.1 12.2 22.1 15.3 68.6 42.8 44.6 CS1 111.1*c 5.5* 3.0* 6.0* 26.6* 27.0* 27.8*Pirouette UC1 62.3 5.2 13.3 9.1 10.7 14.6 9.0 CS1 83.4* 3.0 11.0 2.0* 2.7* 12.5 4.0*Reinettedes UC1 63.7 4.3 13.8 8.0 8.0 2.3 4.8Capucins CS1 88.2* 3.0 7.0 6.3 5.8 2.8 5.2ReinetteHernaut UC1 49.0 3.1 1.5 2.0 2.0 0.0 2.3 CS1 56.6 4.0 1.0 3.1 0.0 0.0 1.0Initial(Vf) UC2 95.8 5.6 12.2 6.5 2.5 12.0 11.5 CS2 117.9* 4.0 6.0* 1.0* 4.0 5.8* 2.5*Topaz(Vf) UC2 98.3 5.2 15.6 6.0 10.9 42.2 40.3 CS2 116.7* 3.0 7.0 2.4 7.8 29.2* 19.0*JN20/33/58(Vf) UC2 49.3 1.8 16.4 6.5 9.9 7.0 7.1 CS2 56.5 0.0 7.2 7.0 7.1 14.0 5.3*Zvatava(Vf) UC2 55.9 2.9 18.7 9.1 30.2 61.8 46.2 CS2 77.8* 1.0 8.8 8.0 23.0* 31.6* 44.8aFortreatmentsexplanations,seep426andtable 3—Pour l’explication des traitements, voir p 426 ettableau 3.bNohandorchemicalthinninghadbeendoneduringthegrowingseasonforanyofthecultivars—Aucun éclaircissage manuel ou chimique n’a été effectué durant la saison de croissance pour aucune variété;cvaluefollowedby‘*’aresignificantlydifferentfromthecorrespondinguntreatedcontrolvalue(UC1orUC2)accordingtheStudent-Newman-Keulstests(P≤0.05)—Les valeurs suivies de ‘*’ sont significativement différentes des valeurs correspondantes « témoin non traité » (UC1 ou UC2) au sens de Student-Newman-Keuls (P ≤ 0,05).

table 5. Copper content (mg.kg-1)a of organic orchardsoils atGembloux from 2002 to 2008—Teneur en cuivre (mg.kg-1)a du sol du verger biologique à Gembloux de 2002 à 2008.

spray treatmentsb 2002 2004 2006 2008UC1+UC2 - - - 14.8cCS1+CS2 18.5 22.3 26.8 15.5aEDTAandammoniumacetateextractionmethod—EDTA et méthode d’extraction de l’acétate d’ammonium;bFortreatmentsexplanations,seep426andtable 3—Pour l’explication des traitements, voir p 426 et tableau 3;cvaluesarethemeansoffivereplicates,andvaluesfollowedbythesameletterarenotsignificantlydifferentaccordingtheStudent-Newman-Keulstests(P≤0.05)—les valeurs sont des moyennes de cinq répétitions et les valeurs suivies par les mêmes lettres ne sont pas significativement différentes au sens de Student-Newman-Keuls (P ≤ 0,05).


Figure 7. Meannumberoffruitspertreeforeachspraytreatmentfrom2003to2008—Nombre moyen de fruits par arbre pour chaque schéma de traitement de 2003 à 2008.

Fortreatmentsexplanations,seep426andtable 3—Pour l’explication des traitements, voir p 426 et tableau 3;Errorbarsdenotestandarderrorofthemean(n=6)—Les barres d’erreur représentent l’erreur standard de la moyenne (n = 6).

Figure 8. EffectsoftheCScomparedwithUCspraytreatmentsonthecopperandsulphurfruit(standard)andpeelcontentsatharvestin2006.Meandryweightcontentwas14.5%(±0.5)and20.6%(±0.7)forfruitsandpeels,respectively—Comparaison de l’effet du schéma de traitement « CS » avec l’effet du schéma témoin non traité « UC » sur la teneur en cuivre et soufre dans les fruits (Standard) et dans les pelures des fruits (Peel) à la récolte en 2006. Le poids sec moyen était de 14,5 % (± 0,5) et 20,6 %(± 0,7) pour, respectivement, les fruits et les pelures.

Fortreatmentsexplanations,seep426andtable 3—Pour l’explication des traitements, voir p 426 et tableau 3;Errorbarsdenotestandarderrorofthemean(n=6)—Les barres d’erreur représentent l’erreur standard de la moyenne (n = 6);Inthe‘UC−CS’pairs,meanvalueswithdifferentlettersaresignificantlydifferentaccordingtheStudent-Newman-Keulstests(P≤0.05)—Au sein des paires « UC−CS », les valeurs moyennes suivies par des lettres différentes sont significativement différentes au sens de Student-Newman-Keuls (P ≤ 0,05).

mg.

100

g-1 fr

esh

tissu

e

mg.

100

g-1 fr

esh

tissu

e

Topaz Topaz

Standard StandardStandard StandardPeel PeelPeel Peel

Pinova Pinova

12

10

8

6

4

2

0

Sulphur content Copper contentUC UCCS

CS

a a

a

a

a

a a

a aa

ab

ba

a

a

0.10

0.08

0.06

0.04

0.02

0.00

Frui

t nu

mb

er p

er t

ree

Frui

t nu

mb

er p

er t

ree

300 300

250 250

200 200

150 150

0 0

100 100

50 50

cv. ‘Pinova’ cv. ‘Initial’

UC1 UC2

SF1 RE2

LS1

AR1 SF2

RE1 CS2

CS1

2003 20032004 20042005 20052007 20072006 20062008 2008

Frui

t nu

mb

er p

er t

ree

Frui

t nu

mb

er p

er t

ree

300 300

2003 20032004 20042005 20052007 20072006 20062008 2008

250 250

200 200

150 150

0 0

100 100

50 50

cv. ‘Reinette des Capucins’ cv. ‘Topaz’

Year Year

UC1

SF1

LS1

AR1

RE1

CS1

UC2

RE2SF2

CS2


stage,ascosporeshadbeendischarged,susceptibleyoungtissueswerepresent,andtheminimumtemperatureandleaf-wetness conditions for infection according to therevisedMillscriteriacouldbeachieved,butpenetrationof thecuticlehadnotyetoccurred(Figure 1).Below250DHafterrainfall,fewascoporesreachthestadiumofpenetration,andarelevantportionwillonlyreachthisstageafter300DH(Smerekaetal.,1987;MacHardy,1996).Spraysbelow300DHcanbeconsideredtobeappliedduringtheinfectionprocess(beforeinfection),ongerminatingsporespossiblyalreadywithappressoriabut not yet with the primary stroma that allow thefungustobeprotectedbytheplantcuticle.Thepoorerresultregisteredwiththedelayedspraytreatment(SF1in2006)showedthatthetimingoftreatmentsmustbeclosetotheonsetofinfection,evenwithlimesulphur.

The “during-infection” spray strategy has severalimportant advantages compared with the preventive(beforerainfall)spraystrategy;theseinclude:– reducedwashingeffectfromtherain;– greater treatment effectiveness on germinating spores;– avoidance of unnecessary treatments (Funt et al., 1990;Holbetal.,2003;Jamaretal.,2009);– in hot seasons, applying treatments during less sunnyperiods.

However, there are potential problems with thisstrategy,suchas:– the need to be able to adapt the spray timing to withinafewhoursoftheonsetofrain;– the risk of delaying spraying during an extended rainyperiod;– theriskofsprayingduringwindyweather;– theriskofcausingsoildamageunderwetconditions.

Alowdiseaselevelatanygivenpointintimeduringthe growing season is neededwhen themanagementaim isnotonly toprevent infectionson the fruitsbutalsotokeepinoculumpressureatalowlevel(Holbetal.,2005b).Fromthetimetheorchardwasplanted,until2008,anincreasingimpactofthediseasewasobserved,exceptin2007whichwascharacterizedbyparticularlypoor weather conditions for scab. This suggests thatsome untreated and poorly treated plots led to heavydiseasepressureduringthefollowingprimaryinfectionseason. Inorder to limit the influenceof thepreviousyear,severalsanitationpracticessuchasautumnleaf-shredding and leaf-buryingwere carried out betweentwogrowingseasons(Holb,2006),butthesespracticesdid not suppress the scab inoculum sufficiently. Inaddition, the riskof early scabepidemics initiatedbyover-winteredconidiaishighinorganicorchards(Holbet al., 2005a) and this could explain the relativelylow effectiveness of wettable sulphur and potassiumbicarbonate used alone, since the primary 2006 scab

season. This suggests that the results recorded wereprobably influenced by treatments applied in thepreviousyear and shows theusefulness of presentingresults covering a 6-consecutive-year study. As onlytwo summer sprays were applied, some of the scabdamage observed on the harvested fruits might havearisenfromsecondaryscabinfection,especiallyinplotswhere primary scab control was partial (MacHardy,1996;Holbetal.,2005b).

WithregardtoVfscab-resistantcultivars,mainlyinuntreatedcontrolplots,significantandincreasingscabdamagewasrecordedonleavesandfruitsofcv.‘Initial’from2003to2008,asaresultoftheappearanceofnewscabracesvirulent to theVfgenesince theplantationyear. The scab-inoculum pressure therefore increasedfromyeartoyearintheseorchards,whichcouldexplainthe poorer treatment effectiveness at the end of theexperiment,in2008.

The efficiency of bicarbonate salts in controllingapple scab, as reported here and in previous studies(Schulze et al., 2003; Ilhan et al., 2006; Jamar et al.,2007a; 2007b; 2008b), suggests that this compoundcould be introduced in apple disease management,although our results indicated that applications ofArmicarb alone throughout the growing season werenot effective enough against scab and that it neededto be supplemented by other active compounds. Thefact that thebicarbonatesaltsareubiquitous innatureand commonly present in human food, means thatthis simple compound is very appropriate for organicproduction systems. However, potassium bicarbonateactsasacontactfungicideandisnotlikelytobesystemicorcurative.Greenhouseexperimentshaveshown thatArmicarb is effective in controlling apple scab, but along-lasting effect cannot be expected (Jamar et al.,2007b).Bicarbonatesareunstablecompoundsthatarehighlywater-solubleandeasilywashedofftheleavesbyasmallamountofprecipitation.Therefore,theyrequirefrequentandwell-targetedsprayapplications.Activitybelow10°Cisaprerequisiteifcopperistobereplacedand, so far, nodata are availableon theeffectivenessof potassium bicarbonate under low temperatureconditions.

Yucca schidigeraextractwasalsoeffectiveagainstapplescabundergreenhouseconditions(Jamar,2007),butwedecidednottoexperimentwithitbecauseofitsverypoorsustainableprofileasitisbasedonharvestingwildplantsthatgrowindesertareaswithlittlevegetationandverylittlerainfall.

Inour experimental conditions, siliconhad averypoor effect on apple scab. However, Belanger et al.(1995) reported that there iscumulativeevidence thatincreased silicon absorption offers protection againstvarious fungal diseases. This suggests an eventualinadequate timing strategy for thiskindofproduct inourexperiments.


Although some authors have reportedpoorer leafappearancewithsulphurandcoppertreatments(Holbetal.,2003;Palmeretal.,2003),theamountofactivesubstancesusedinourstudytocontrolapplescabdidnot induce any phytotoxic effects, plant damage oryield reduction. However, the treatment frequenciesand fungicide doses in our experiment were verylimited,particularlyduringthefloweringperiod.

Forthelowscab-susceptiblecultivarcv.‘Reinettedes Capucins’, sprays based on sulphur and copper(CS1) led to a significant increase in the yield pertree, especially in the yearswith high scab pressure(2005, 2006 and 2008). These results contrast withearlier studies showing that sulphur applicationsreducedyieldandfruitnumbers(Mills,1947;Holbetal., 2003;Palmeret al., 2003).Suchpositiveeffectsonyieldcannotbeexplainedbythecontrolofapplescaborotherapplediseasessuchaspowderymildew(Podosphaera leucotricha), because all years theinfectionlevelsinuntreatedplotswereverylow,evenat a later stage.There are twopossible explanationsforthis:– triggering defence responses and resistance mechanismsburnupenergyinplantswhichisnot necessarytouseintreatedplants(Doehlmannetal., 2008);– the application of elemental sulphur to crops is increasingly advocated as a way of overcoming deficiencyinthiskeynutrient,andsulphurdeficiency hasrecentlybecomeawidespreadnutrientdisorder in crops, largely due to the reduced rate of fossil fuelburning(Schnug,1998;Williamsetal.,2004). Achemicalanalysisoftheleavesfromcv.‘Reinette desCapucins’,collectedon25June2006andwashed withacidsolutions,showedthattheleafdryextracts from the SF1, LS1, RE1 and CS1 treatments contained 0.38%of sulphur,whereas the leaf dry extractsfromtheAR1andUC1controltreatments contained0.30%ofsulphur(P<0.001).

Sulphur compounds can have harmful effects onusefulphytoseiids(Kreiteretal.,1998).However,theabsenceofthephytophagousmitessuchasPanonychus ulmi and Aculus schlechtendali in the orchard from2003to2008mightbeassociatedwith theveryhighdensity of the predator Typhlodromus pyri observedthroughout the orchard in spite of various sulphurtreatments (Jamar et al., 2008b). Some studies havereported predator mite populations with an acquiredresistancetosulphur(Markoyiannaki-Printziouietal.,2000)andbicarbonatesalts(Beresfordetal.,1996).

Earthworms are particularly sensitive to copperand zinc (Paoletti et al., 1998). Soil copper contentin the experimental orchard was kept below26.8mg.kg-1,whichisfarbelowtheestimatedharmfullevel forearthworms. Itwas shown that copperdoes

not have a negative impact on soil ecology or onearthwormpopulations at up to 36mg.kg-1 soil (e.g.van Rhee, 1976; Holb, 2008; Paoletti et al., 1998).VanRhee(1976)foundthatearthwormswerealmostcompletelyeradicatedwhenthecopperconcentrationwasmore than80mg.kg-1 soil.Organicmanagementsignificantly increases soil microbial activity andearthwormabundanceinorchards(Jamaretal.,2008a;2010a),although:– soil tillageoperations forweedcontrolcan reduce earthwormabundance(Paolettietal.,1998);– thepresenceofcopperon leavescould reduce the earthwormconsumption rates (Deptaetal.,1999). Several authors have found that microbial and earthworm communities play an important role in leaf litter decomposition corresponding to a reductionintheamountofscabascosporicinoculum inappleorchards(MacHardy,1996;Paolettietal., 1998).

5. conclusIon

Thislong-termstudyclearlyshowsthat:– the“during-infection”spraystrategyusingreduced amounts of wettable sulphur and copper are very effectiveagainstprimaryscabinfections;– the use of lime sulphur significantly reduces or suppresses the copper used in a spray treatment basedona“during-infection”spraystrategy;– the amount of copper for scab control could be reduced for medium and low scab-susceptible cultivars compared with high scab-susceptible cultivars;– potassium bicarbonate significantly reduces apple scabandis,insomecases,aseffectiveaswettable sulphur;– natural plant extracts (from orange peel, soapbark tree, tea seed, quinoa seed and grapefruit seed) significantlyreduceapplescab;– sulphur-basedtreatmentsincreaseyieldevenwitha lowscab-susceptiblecultivar;– the fungicide doses and frequencies used in this study are not phytotoxic, do not adversely affect yieldanddonotleaveundesirableresiduesonfruits andsoils.

The studyhas shown that somenewcompounds,especially potassium bicarbonate and five newplant extracts, have an effect onVenturia inaequalisinfections, and therefore have the potential, incombinationwithothercompounds,toreducecoppertreatmentsduringboththeprimaryandsecondaryscabseasons. Control did not, however, always reach theleveldesiredbycommercialfruitgrowers,andseveralpractical issues need to be addressed before these


materialscanbeconsideredasausefulalternative tocopper.

AslimesulphurisnotallowedinBelgium,copperisstillneededforapplescabcontrolinappleorganicproduction in the country. Currently, lime sulphurappearstobethesoleremainingoptionforreplacingcopperwhentemperaturesarebelow10°Cinorganicfarming, and therefore scabmanagement inBelgiumwould be compromised if there were new Europeanor national regulations restricting or banning the useof copper-based compounds. Our 6-year study hasdemonstrated the potential of controlling apple scabwithreducedandnon-damagingamountsofinorganicfungicides,usingclearlydefinedtimingoftreatmentsandaspraymachine.

acknowledgements

This research is funded by the Ministry of the WalloonRegionalGovernment,GeneralDepartmentofAgriculture,Research Direction, project RW D31-1144. The authorswould like to thankDrR.Oger (CRA-W,Gembloux) forhisvaluablehelp in the statistical analysis, IrP.Creemers(PCF-KOG,StTruiden)forstimulatingdiscussionsduringthis study andB. Pahaut for his excellent co-operation inthisresearch.

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