Apple Scab: Numerical Optimization of a New Thermal Time Scale and Application for Modelling Ascospore Release in Southern France Christophe Roubal, Philippe C

Apple scab: numerical optimization of a new thermal time scale and application for modelling ascospore release in southern France Christophe Roubal, Philippe C. Nicot

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Christophe Roubal, Philippe C. Nicot. Apple scab: numerical optimization of a new thermal time scale and application for modelling ascospore release in southern France. Plant Pathology, Wiley, 2016, 65 (1), pp.79-91. 10.1111/ppa.12398. hal-02631243

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Distributed under a Creative Commons Attribution - NonCommercial| 4.0 International License Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article F-84143Montfavet Cedex, France Cedex, F-84143Montfavet b author:[email protected]*corresponding Venturia inaequalis Venturia Keywords title: Short a C. Roubal Title: Type:Article Original Article This article This protectedis by Allcopyright. rights reserved. 10.1111/ppa.12398 doi: lead to differences betweenversionthis and the Versionof Record. Please cite this article as throughthebeen typesetting,paginationcopyediting, and process, which proofreading may This article hasbeen accepted for publicationand undergone fullpeer review but has not calendar datesingle biofix asandnew a types on thebasis biological of observations. Here, we explored the potential interest of using a date yearly established starting abiofix accumulation from ondegree-day rely models Most releaseby hasbeen toforecasting devoted thus, much effort ascospore and fundamental scab. is of treatments apple Correct timing themanagement spring for of ofAdequate protection treesapple during the Abstract modelling ascosporemodelling release insouthern France Organisation NationaleOrganisation de la Protection des INRA, UR 407Pathologie végétale, F-84140 Montfavet, France

Apple scab: Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 a and P.C. Nicot New prediction models applefor scab

numericalofoptimization anewthermal scale time and applicationfor , degree-day, primary inoculum, predictive model model predictive inoculum, primary , degree-day, Comment citer cedocument: b *, *,

Végétaux (ONPV), Quartier Cantarel, BP70095, primary contamination periodprimary is contamination a cornerstone of timeof scales, with the help of numerical Venturia inaequalis Venturia . Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article if diseaseif development is prevented until the ascospore supply depleted is in summer,early additional numerous duringtreatments thegrowing (Carisse season ondiseased tissue may polycyclic epidemics and inthe produced develop requiring orchard, not early are 1997). If treatments leaves against primary which inoculum c unfolding thefirst protect spring to in early start typically applescab against Treatments those 70%of fungicide treatments and diseases 2009).on Itwas usethatat 75%ofpesticide fungal2007, estimated aims apples controlling France, suggestingSouthern possible the occurre strongly period release reduced thepredictive the conditions of value in model ofthe ascospore the drydaysto during for time scale account inthe inserted rules halting However, rainy influencepositive of days onpseudotheci the totakeintoaccount time scale with "accelerating the rules" improved by adjusting was further the model Thepredictive of value validation. data for of years additional linear response instandard degree-day models.Amodel was constructedthen using 4 accumulati for to temperature rate development of non-li use Provence the established and for wasbiofix biological phenomenon. Anoptimal calendar temperaturethe onof effect scaletime functions, a which requiresmethod thesmallest of number assumptions about the assessed thedaily rateofdevelopment for with field-collectedoptimization data.Using between 2008,we 1996acquired data and This article This protectedis by Allcopyright. rights reserved. large num a control its entails and production inaequalis Venturia Introduction Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 , the , causal of agent scab,apple is ofmajor economic concern for apple Comment citer cedocument:

successful, secondary (consistingis inoculum conidia) of V. inaequalis onsists ascospores mostly of (Stensvand ng thermal time was compared with the usual the was compared with ng time thermal ber fungicidal treatmentsof (Carisse target apple scab (Creemers & Laer, 2006). scab (Creemers &Laer, apple target nce ofstrainsadapted to dry conditions. al maturation prior to al maturationprior ascospore release. near functions relatingnear pseudothecial primary generic inoculum by fitting et al ., 2009). Conversely, et al. et al et ., , Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article triggered bytriggered rain events (Rossi in the releaseof ascospores inthespring, aphenomenon which has to beshownbeen pr pseudothecia the a undergo period, During this isThe known pathogen to overwinter2005). primar have be inoculum conidial overwinteringof complicating suchfactors as co airborne (Stensvandaltogether subsequent fungicide sprays may insome against scab and, bereduced cases, omitted This article This protectedis by Allcopyright. rights reserved. that that the law relating pseudothecial maturation rate to degree-day accumulation was a degree-day base possibletemperatures(among spring. regression ascospores ThisProbit the in scale time consisting ofdegree-day accumulation (base =0°C) thefirst from appearance of data Probit-transformed on thepercentage of to equation regression alinear built byfitting was model NH The worldwide. growers al. developed bymodel" Gadoury and others &MacHardy derived (1982a) from it(Stensvand rate (NH)"New Hampshire to temperature.relating The thepseudothecial maturation scabapple thermal was models, defined time accumulation of asa temperature the function concept isthat kinetics the of biological phe timescalesthermal rather physical timescales than (Lovell maturationthis release of dynamics of and climatic (Holb, factors 2008). Numerous models have been developed topredict the Muchresearch effort has been dedicated to presence ofprimary inoculum,as well theas dy , 2006a; Schwabe Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument: et al. et al. , 2005). This is the general situation in Southern althoughFrance, in situation general the is This 2005). , , 1989; Lagarde, 1988),, 1989;Lagarde, have useful provided tools for apple et al.

, 2000). en reported in other parts of Europe (Holb of Europe other parts in reported en ntamination from neighbouring orchards or neighbouring or orchards ntamination from inoculum. These models have beenbased on nomena are influenced by temperature and in and temperature influenced by are nomena between 0 and 6°C), relied on the assumption mature ascospores plotted against a thermal approach, used to select the most appropriate theappropriate to select approach, most used namics of ascospore release on the basis of ogressive maturation process, results which ogressive maturation predicting the beginning and the end of the of end predictingbeginning the the and ily aspseudothecia onleaf present litter. et al. , 2004). The basis this, 2004). for The et al.et et , Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article rain before the ascospore release period (Stensvand the period ascospore before release rain ascospore release (Rossi an intoaccount taking effect on pseudothecial long maturation of dry during periods al.et first order function. Although time scalesAlthough order time function. first polynomial functions of temperature, rather than degree-daysthe which represent a simple were scales defined achievedpredictions order whenusingas sums second time of pseudothecial maturation release, ascospore the andpredict 1982b) todescribe best predictions. scale Fordeveloped for byJamesin the model example, Sutton(1982a, & explanation could also be that the use of degree-days notdoes constitute an optimal time (XuNH into account model taken by initial the not The such adjustments needfor 2006a). related could factors of to the influence be climate Successful predictionof Successful ascospore releas shapeof specific the curve maturation to fit (Schwabe local data adopted worldwide. thermal scaletime the useofand degree-days atemperatureas function been have largely type of This 1982a). (Gadoury &MacHardy, as commonly"biofix" to referred a date and used for theprediction of ascospore release based on degree-day accumulation, starting at Gaussian AfterProbit reversefunction. sigmoidcurve obtained transformation, a wasthen a This article This protectedis by Allcopyright. rights reserved. response curves that the (1996) Xuby Aspointed out fungi. of tenpathogenic development Notable exceptions include the foundational modelling workof Analytis (1977)onthe pathogenic (Xu,1996; until plant recently Leglerfungi pest development (Damos & Savopoulou-Soultani insect of description including the research, of fields in several modellingfor used routinely , 2005, 2006a,, 2006b). Forexample, predictive haveimprovements been obtained by Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument: et al. , 2000; Stensvand 2000; ,

based on temp non-linear e has sometimese required adjustments the to et al. et al et , 2012), they have rarely been used for usedfor been theyrarely have , 2012), , 2005, 2006a) and of 2005,2006a) of occurrence and , the ., 1995; Rossi et al. et al., , 2012;Battilani et al. 2006b). possible Another , 1989; Stensvand , et al. et erature functions are , 2000;Stensvand , etal. , 2013). etal. , Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article the advantage of combiningsimplicity and pertinence. date, was usedby Beresford inNewZealand Laer, 2006,(Creemers & Eikemo regionalpredictionsfor has often been a topicof discussions controversial between advisers applicationresultsvariable their these somewhat and provided methods all However, 2005). phenologicalthe growth of basis of stages workers were thedate of first detection of ascospores inspore traps or dates selectedon the bytypesofbaskets biofix(Gadoury used different Other 1982a). wire-mesh MacHardy, in & pseudotheci mature ascospores in of observation the first to NH biofix corresponded original In the biofix. model, the of typesusing different linear. than developmentrate the of relate a fungaltemperature of pathogen are to bell-shaped, rather This article This protectedis by Allcopyright. rights reserved. tore scale that function usestime anonlinear episodesduringthe ascospore release period andof the occurrence ofrain before this period. by into account taking improvements effectan onpseudothecialmaturation of long dry growing seasons.A objective thefinal of present study was toexplore possible predictive ascospore release. This model was then valida was th 13-yearperiod, over a acquired data time based onacorpus thermal scale, optimized inaequalis Another method to improve provided thepredictions by NH the model has onrelied The first two objectives of the present study we

Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 to temperature , and (ii) to define a calendar-based biofix. The resulting The biofix. a calendar-based define to (ii) and temperature , to Comment citer cedocument:

et al. et , 2010). An, biofix, alternativetypeof calendar afixed trees the (for bud break) example (Stensvand late the rate of pseudothecial maturation of pseudothecial of maturation rate late the (1999). This calendar-based biofixpresented Thiscalendar-based (1999). ted with independent data of four ted four dataadditional withindependent of en used to construct a predictive model of model a predictive toconstruct en used a collected from storedleaves onthe ground of of biological andon meteorological field re (i) to theevaluate benefit of a thermal et et al. V. V. , Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article January, random samples of approximately 50 leaves were collectedwere and leaves approximately every50 week samplesof random January, perimeter of the area was necessary as a barrier against slugs and snails. Starting in early were Earthworm degradations never litter. degradation possible for regularly examined (GPS 4.883370).French Ministry Agriculture 43.908228, coordinates of The were leaves wire,chicken 5meters froman station belongingagrometeorological network ofthe tothe Nationale de laProtection desVégétaux and arranged onthe ground over a1m² underarea showing spots).Collected scab br leaves were applied that appleand scab had been prev Valley. Each year, one orchard was selected on the basis that treatmentno pesticide hadbeen orchards inthe vicinityorganic located Avignon Rhône (cv of in the from Goldendelicious) in leaves batches 1000scabbed ofapproximately collected autumn were to 2013, From 1996 and maturation ascosporePseudothecial release. Materials and Methods This article This protectedis by Allcopyright. rights reserved. a rainafter event, 10 glass slides were observed under the microscope and the ascospores Ascosporerelease wason batches quantified leaveswire over the (intheand renewed same observation ofmature ascospores wasthenused reference as "biofix" in the modelling work. MacHardy asdescribed & Gadoury bypigmentation ascospores. Ascospore wasas maturity time 100-200) underpresence (magnification andmicroscope for of each the asci examined week and a collected 1-3times samples were pseudothecia.Followingthe detection ofthefirs stereounder aobserved (20-40ma microscope Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument:

sessed on the basis of their morphology and their morphology basisof sessedthe on observed of metaldehyde onthe but application alent alent during theseason (20%-90% leaves of by earthworms or other organisms feeding or organisms other on by earthworms ought back to the station station theOrganisationof tothe ought back a total ofa 50 total pseudothecia crushed were and positions) after after oneeach Within positions) day rain. t (usuallypseudothecia late January), leaf in gnification) todetect the presence of (1982b). Each year,of the Each thedate first (1982b). ofslides glass on placed chicken the Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article averages, each computedwith 72data values. Over1996 from period the to2013, total ofa ground air andrecorded temperature every 20 minutes. The output consisted of daily device (CIMEL Paris, Electronique, France) was collectedData were stationCIMEL theagrometeorological above.from mentioned This 140 Weather data (Gadoury& MacHardy, 1982a). expressed as were the years, numbers different wet them for three successive days. To compare dynamics the of ascospore release over outrain episode followingcarried anartificial andkeeping achievedthe leaves bysprinkling escape detection observationnot of aftertheend period,the was a ascosporefinal count of end (usually rainevents consecutive several pseudothecia, time the whennomoreasco until observations were carried out from the firs were counted on each slide on 7 replicate zones, each 2 mm high22 and long. mm These This article This protectedis by Allcopyright. rights reserved. hypothesis that R( arbitrarily aspecific mathematical function. Instead, we based our on approach the basic pseudothecial daily maturationR andthe average temperature To investigate temperature new functions describing between relationship the the dailyof rate Constructiongenericof a scaletime thermal andselectionof a calendar biofix recordedalso hourly rain intensity with0.2 a mm buckettipping rain gauge. station weather The 3°Cand 20°C.between values the 98%of with May, and 31 September 1 between to 26°C -5°C from daily ranged andthese averages computed were 5173 averages maximum value with increasing value with maximum Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 T Comment citer cedocument: ) is equal to zero to for is equal ) T

andthendecreases to become null when T below aminimumthreshold, it increases to a May). To ensure that further release would release further that Toensure May). a percentage of the total thetotal of yearlya percentage counts spore spores onthe detected glass were for slides t detection of differentiated asci in theof in asci t detection differentiated positioned at a height of 1.50 m above them above heightof1.50 at a positioned T , we chose not to select notto we chose , T is higher than a than higher is Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article March. 1 and September 1 between evaluated, were 10-day interval) biofix(approximately a at using pertinence 19 dates a biofix, of calendar the was optimized function and parameterised same described below. Inthe as time, to explore ABCDtemperature the to 2008, 1996 collected from data experimental of sets Using 11 increasing temperature. a case particular represents of theABCD with function, Interestingly,function maximum. of the degree-day NH its model the for temperature describingfunction the actual complex biological and phenomena toestimate theof value allows ofapproximation the possible asymmetry and“peakness” ofthe unknown R( present inthe function study, with described is four parameters toas "ABCD" referred function, generic 1. This Figure in described as segments linear five of parametersthegeneralnumber shape of such function, describingthreshold. proteiform temperature A a with simple maximum limited This article This protectedis by Allcopyright. rights reserved. correlation rank temperature theparameterisationfunctionsSpearman'soptimize of using usto allowed This prediction of cumulated spore release, is a strictly increasing function of the thermal time. on relied the fact weultimately that Our the sought, method for maturation. function the when tryingthe mostappropriate todefine timethermal scale (as done previously NH the for model[Gadoury &MacHardy, 1982a]), avoid the used to pseof the response underlyingtemperature the wasa function out with me carried temperature Parameterisation of theParameterisation temperature function Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 ρ

a priori Comment citer cedocument: (Sheskin, 2007), which is commonly used to assessthe monotonic which used to commonlyis (Sheskin, 2007), selection of selection of an arbitraryrelating function spore to therelease

rate rate totemperatureresponse for pseudothecial thod doesthat not require prior knowledge of a unimodal curve, consists of a succession of udothecial maturation. was This approach . a =0andalinearincrease rate with The parameterisation of of theThe parameterisation a , b , c and d (Table 1). It (Table T T )

Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article its value is necessarily 1, as the ranks increase together for the thermal time (r thermal the for together ranksincrease the 1,as necessarily is value its temperature function is, for calculating thermal time over all years, the more the ranks r the more the years, over all time thermal for calculating is, function temperature because theoverall ranks donotnecessarily together. increase theThus, pertinent more a defined as: time and for the Y axis (r given data point on the X axis (the thermal time) and on the Y axis (representing the Y axis (representing andonthe time) thermal the (the Xaxis pointon data given cumulated percentageof released ascospores).If the following relationship were evaluated: evaluated: were relationship following the parameters. Torespect of thedefinition the ABCD function, only sets of values respecting of rangeuseful parameterising biological for date, awide of models. Foragivenbiofix the set 40)were tested, -20 and shown 2. in Figure be could Suchapproach usingthe algorithm also of combinations of parametersets values(representing different describesof the dynamics spore cumulated release. points the of which parameters cluster for data atakes value closestother to 1. words, In value of a function,temperature the most pertinent set of relationship betweenrelationship two (Zou variables This article This protectedis by Allcopyright. rights reserved. r where n was the number of data points (days of ascospore release) in the data set, and r set, and thedata release)(days ascospore in of points data numberof the n was where

ar will increase together whenexamining the complete 11-year data set. For a given (abbreviated as r as (abbreviated a , b Selection of a biofix. For each of the 19 biofix dates, large numbers (> numbers large dates, 19 biofix the of each For biofix. of a Selection 100000) of , Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 c and and d values providinghighest the ρ Comment citer cedocument: ts =1-(6 * ) andr ar ). When computing When ). ascospore release Σ (r

thermal time thermal (abbreviated as r as (abbreviated etal. a – r < ρ b for the data of several years, its value is value years, its several data of the for and ascospore release to closestis the ideal andunknown that curve , 2003). In the context of our study, study, of our context In the , 2003). parameters should thus should parameters ρ ρ wasconsidered astheset of optimized b is computed for the data of a single year, ≤ c and ar )² / (n * (n²-1)), (n)² / *(n²-1)), ) were, respectively, the ranks of a of ranks the respectively, ) were, c ρ < nearest 1 to characterizes the d . a , b , c and be that for which for that be d values between values ts ) on the X axis ρ ts thermal thermal was was and ≤ 1, ρ

Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article with a 2 with a day used in function the reference NH model, comparisons were also carried out (Table 1) thedegree- to above. Inaddition described algorithm as using the same and parameterised asshown function inTable1. These twoadditional temperature functions wereoptimized proposedby Analytisdescribe model (1979)to description of curves shapes withdescriptionsuch (Kontodimas comp selected for functions were mathematical ABCDBased ontheshape parameterised of the temperature function, twocontinuous scalesComparisonof thermaltime (Gadoury&model MacHardy, 1982a). R( used to date then biofix was selected The functions. temperature other the using that ABCD to function, was similar onthe based using time date, biofix best thermal the paramete (using function 8000 setsof temperature usin dates, biofix computed the 19 were for parameterisation stepparameterisation described above wa allowed allowed the stability the of December This day to10January). 20 (each from surroundingdates biofix selected the correspondingout andthe was carried described above was not choice biased byanycalculation artefacts.Firstly, parameterisation the step associated thedates tested,mostpertinentcalendaramong weexamined 19 biofix the select the To This article This protectedis by Allcopyright. rights reserved. T ) functions with similar) functions with shapes andto the degree-day used function inthe reference NH Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 nd order polynomial function (Figure 1) as proposed by James & Sutton (1982b) to byas proposed to James&Sutton (1982b) 1) (Figure function orderpolynomial ρ values (Figure 3). Two additional computations were realized to ensure that our that to ensure realized were computations Two additional 3). (Figure values Comment citer cedocument: ρ

values in this period to be verified. Secondly, values the tobeverified. in this period s also carried out and the corresponding the out and s alsocarried compare the ABCD temperature function to other theABCDtemperature to function compare g a modified Gauss function (Table 1) asa g Gaussmodified function (Table a fungal development and the modified the fungal Gaussand development arison, among previously those the usedfor rs for each date). This determined whetherThis determined eachdate). for rs et al. et ρ values were computed for additional , 2004;Jalali et al. et , 2010):the ρ values values Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article Construction and validation of a model ofpredictive Constructionandvalidation for ascospore release the rest of for retained the study. ascospores, halting rules (Stensvand effe slow-down possible accountthe into take To Adaptationof the thermaltime scale to the occurrence ofdry and rainyperiods and under-estimation of observe on thebasiscompared of size residualsthe anddistribution of the and on frequency over- of predictiveits wasvalue compared tothat of the reference NH-based model. The were models 2009,2011,2013 and setsvalidated of 2012and withdata then ABCD-based modelwas The climatic andconditions dynamics ofascospore release ofFrancesouthern (Lagarde, 1988). to adapted reference NH-based model a of that modelwith ABCD-based this of fit the analysis Residual (http://www.curveexpert.net). theparameterise 33 possible functions prop Levenbe with the was carriedout analysis 1996 regression to 2008, setsdata Using from time. 11 of thermal asrelease afunction above, described ABCDfunction on the Based correlation correlation basis Spearman'srank of the on compared were temperature functions these on all based relate average topseudothecial daily The temperature time scales thermal maturation rate. This article This protectedis by Allcopyright. rights reserved. when 7dry days occurred consecutively. insuspending accumulation They consisted the Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 ρ as described above. timescale The as providing described of the highest value Comment citer cedocument: d ascospore release data.

et al. et , 2005) applied, were tothe thermal scales.time rg-Marquardt algorithm (Marquardt, 1963)to (Marquardt, algorithm rg-Marquardt and a Student's Ttest wereused andaStudent's compare to ct of prolonged dry periods on the release of the on dryperiods prolonged of ct osed by the CurveExpert 1.3 software 1.3 CurveExpert by osed the a model was constructed to fit ascosporeconstructed fit was to model a of daily rate of pseudothecial of pseudothecial maturationof daily rate

ρ was was Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article analysis,using datasets 1996 from to 2008. ascosporeofreleasebefore onset estimated the was date its and examined through regression in the context of Southern Forthis, the between the France. relation number ofrainy days development, where development, inaddingconsisted an term" "acceleration adjustment The scale. time ABCD thermal the toadjust used were then line and regression to the of mm) These thebetween optimize 0.2 fit and 3 line. thresholdregression optimized daybe considered as a values for to needed "rainy" was adjusted (among 29threshold the estimated date ofits onset was refined. For this, the minimal of recordedamount rain secondstep,thenumber theIn a relation between rainynumber of days of year a vsrank its for ascospore release. estimated 10% ascospore release dates. Regression analysis was then carried out on the according ranked 10yearstiming of were the ascospore to The (Figure stocktotal 4). observationthe of the first ascosporesmature and in thesuddenresulted ofrelease 41% theof 40 days occurred after rain On thatfirst the year, 2000. in interpolation an accurate allow not this at sets wereused data the 11 Only 10of reached. This date was estimated each year by interpolation linear from observed the data. ascosporewas when release release cumulated date 10%of was ascospore the assessedof as (Stensvand mm considered was0.2 day "rainy" to be a as needed for precedingfirstmonth ascospore the maturity and theminimal rainamount ofrecorded step, the period quantification considered In afirst rainy the of for was defined as the days influence the maturation process (Stensvand (Stensvand process the maturation influence to was reported also theonset release of ascospore occurrence rainyAs of the days before This article This protectedis by Allcopyright. rights reserved. Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument: RD RD represented the number of rainy days and rainy days and numberof the represented

ν * et al. RD stage,thedynamicsof ascospore as did release to the ofpseudothecial rate dailycumulated tothe , 2006b), this phenomenon was investigated of rainy days before ascospore release and ascospore release daysrainy before of et al.et , 2006b). Theonset ν anacceleration Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article Based onthe rABCD function, newa was model constructed to fit ascospore release as a Construction and validation of an ad new predictive modelfor ascospore release. as scale.thermal time was time newpaper This a "rABCD" toconstruct used then thermal to define improved thermalABCD an sensitive" scale, time referred "rain to in therest of this coefficient. The value of This article This protectedis by Allcopyright. rights reserved. comparedon thebasis ofresidual analysis Student'sand a T test. . and its predictive value was tocompared thatof thebasic ABCD-based model. They were 2013 2012and 2009,2011, ofvalidateddata sets with was then rABCD-basedmodel The that with model rABCD-based basicadjusted of thethis model. ABCD-based 1.3 software. Residual andanalysis aStudent's wereT used then test to compare fit the of construction of the basic ABCD-based with proposed functions model by theCurveExpert of time.function regressionThe same method was used describedas above the for ascospore release curve. Theoptimized parameters highest providing the offunctions thermal time scales without any knowledgeabout the specific shapethe of rank correlation of values thebetweenreleasedynamics ascosporewas time andthethermal assessed possible for all usedoptimization above parameterizeto theABCDtimethermal scale. Inthis case,thelink onset the of ascospore release were established, applyingalgorithm thesame of numerical Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 ν and all dates between 9December and 9March. Again,on it relied Spearman's ρ

which allowed the comparison of continuously thecomparison allowed which temperature of increasing Comment citer cedocument: ν , , the and definingtwo dates influencing theperiod thetiming of

justed model for ascospore release release ascospore for model justed ρ value were used used were value Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article January as a biofix (rather than 20Fe (rather than January asabiofix its mature (first referenceand with of observationascospores). choice biofix The of 1 functions temperature NHexcept whichthe model, wastested with both a 1January biofix allthe asbiofix for 1 January study,the of restof wasused date Forthe sharply.decreased missing ascospore missingmaturation for mild years with riskof woulddate a entail later the model at prediction the thatthe fact by starting motivated temperature function. For a biofix on 1 March 1 March on Fora biofix function. temperature changes withcoincided in increases sharp the values of parameter " Compared to the biofix of the NH model (first observation of mature ascospores), whichthe for the (first NHmodel of mature Compared biofix to observationof ascospores), Choice of a biofix taketo into account the widest possible range of climatic variability. the yearly41%ascospore of atthe This rain.first potential year wasretained for modelling, dry the period after first observation of mature long a 40-day with atypical somewhat was (2000) year Another analysis. for further retained considered 2003werenot data 1998and from the counted over a season varied from less than500 to over 48000. Due to thelow spore counts, ascospore releasedatesvaried of ov widely also dates,Februa calendar of 7 range spanning from Over the13years ofobservations, the first mature wereascospores recorded over abroad Observed ascospore release Results This article This protectedis by Allcopyright. rights reserved. similar in lower resulted the ρ value was 0.9229, calendar values of the biofix between 1 September and 20 December 20 December 1 September and between 0.9229, the biofix calendarwas values of value Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 ρ values were observed for biofix datesbetween observed 1January biofix and20February. These valueswere for ρ values of the ABCD thermal time scale (Figure 3). However, higher theABCD scale 3).However, (Figure values or of thermal time Comment citer cedocument:

bruary, which provided a slightly higher slightly higher whichprovideda bruary, er the years. The total numbersof ascospores ascospores, resulted which thein release of ry to 27 March (Table 2). The first and last first and The 2). (Table ry 27March to winters. Furthermore, biological data show biological data Furthermore, winters.

(and later; data not shown), the the shown), datanot later; (and assufficientlywere reliable not and a " of" the ABCD ρ value) was value) ρ value value Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article presented a slightly lower but comparable had shape also similara toof the that established whichfunction byJames& Sutton(1982b), shapes (modified Gauss hadand Analytis) veryall similar ABCD biofix. function and the The a two continuously functions with differentiable similar of date the low whentaking remained model NH Gadoury1982a, processmaturation which can start as early the as weekfirst of December (James &Sutton, avariousprecededobservation stagesby of release is ascospore first ofthe the that This article This protectedis by Allcopyright. rights reserved. with Richard'sobtained law as (defined y= Based on regression analysis, the best fit to the 11 ascospore release datasets (R² = 0.91) were scale Predictive model ascosporefor release, using the parameterised ABCD thermal time δ ABCD temperature function, respectively) with parameters using the time thermal for rate daily andthe accumulation ascosporetotal release percent of 1).The (Table than NH withthe functions model temperature on non-linear 1 January With this higher biofix, scalesComparisonof thermal time 5).(Figure January wasalso bestthe whenusingamodi biofix of1 a Furthermore, of variability5). show ahigh level (Figure not did January presence of ascospores between 1996 and 2008. ascospores of and 2008. presence between 1996 inof 1996) end the (one minor exception nor =1.1586. The predicted ascospore release (Fi release predicted ascospore The =1.1586. Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 et

al. Comment citer cedocument: , 1984). The , 1984).The

ρ ρ values were values were obtained with all thermal timescales based values eleven fordaysand the days before 1 after nine ρ value (Table 1). 1). (Table value α /[1+exp( fied Gaussfunction as a temperature function gure 4) notunderestimatedid the beginning the risk periodrepresented by theobserved the first observation of mature ascospores mature of observation as the first The distribution of residuals of this ABCD- this residuals of of distribution The β - γ *x)]^(1/ α ρ =100, =100, values. These threefunctionsvalues. δ ), where y and x are the are x ), wherey and β =10.3975, =10.3975, ρ γ value of the of value =0.1053 and=0.1053 Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article both theaverage residual values and theaverages of the absolute values of residualsthe were wasalwayssma deviation of the amplitude overall contrast, the residuals for ABCD-based the modelwere notsystematically positive andthe 2013). In 2009 exceptions between and released among 48observations (2 ascospores percentage of the cumulated overestimated regularly model NH-based The 3). (Table thereference2012) for 32.5 (17April 2011) and accurately absolute (Figure with of values residuals 6), maximum highas 64.4(2 April as counts 2009,in 2011, 2012 and2013. Neither model predicted ascosporerelease very ascospore release from 2009 to2013. Predicted The ABCD-based predictive model and the refere Model validation with four independent data sets from 2009 to 2013 significantly higherthan of those theABCD-based model ( wereNH-based of the model theresiduals model. The tothatof referenceNH-based fit its Student comparetest used we a to bell-shaped, being andapproximately modal based model This article This protectedis by Allcopyright. rights reserved. study. conditionsof in ourthe models predictive to improveno the potential had rules halting these thefor than NHthermal timescale, but inboth cases, indicatedthis thatintroduction of the ABCD wasmostsubstantialeffect 4). the The for (Table index rankcorrelation Spearman's during in of values resulted maturation reductionpossible in lower ascospore dry days, accounttimes scales for the to NH thermal reference ABCD and tothe applied Halting rules, Taking intoaccount periodsof drynessduring ascosporethe release period significantly higherthan of those theABCD-based model ( model were of theNH-based residuals model. The ABCD-based the for smaller remarkably Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument:

values were compared to ascosporeobserved nce NH-based model were used to forecast and theABCD-based models,and respectively ller (Table 3). For three of the years, four ofthe three For3). ller (Table P P < 0.01). <0.01). < 0.01). <0.01). Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article pseudothecial development, 2.1 being theoptimized value of the acceleration coefficient ABCD timescale. thermal Itconsisted of adding 2.1x the in development of ascospore dailyrate the for rule" of an"acceleration implementation beyond not (data Taking 3mm shown). this phenomenoninto account led to the 2.5. fitness of The for regressionoptimum decreasedthe mmand lines clearly 1.5 below rain with obtained were relationships pertinent most The mm.of 2.5 threshold a rain 21 Februaryand January to 13 from rainy days with decreasing of occurrence rain. Figure 7 for this shows relationship a recording ofperiod R² = by occurrence0.80) the rainy of eventsin winter. Maturity was increasingly delayed onset of release ascospore 1996 The between and 2008wassignificantly affected ( be events rainy account into Taking This article This protectedis by Allcopyright. rights reserved. construction of the new predictive model for ascospore release. the for used was inturn scale, which time thermal the rainsensitive rABCD to define highest ascospores. optimized provided the These parameters evaluate therelationship between the timethermal the cumulatedpercentageand of released particular case of a rain threshold of 2.5 mm and 2.5 mm and threshold of arain case of particular shows oneexample of such comparisons all for startingpossible and ending the dates with and dates ending of the recording 9 between rain Decemberperiod 9and Figure March. 8 threshold valuesrain of 40values combinationspossible of 28 with of all values optimized the comparison from These dates were 21February. and January and and RD Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 representing the number of days with a rain days with a representing of the number Comment citer cedocument:

fore the ascospore release period period release ascospore the fore thresholds between 1. ν = 2.1. For each pair of dates, the the dates, of pair each For 2.1. = ≥ 2.5 between 13 during mm the period 2.5 RD the to cumulated dailyof rate ρ value (0.945) and were usedwere and (0.945) value ν and all possible startingpossible all and 5 and 3 mm, withan P ρ

< 0.05; values values ν

Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article reference NH-based model ( model NH-based reference ABCD-based model ( the initial those of than smaller significantly were model rABCD-based the of residuals rABCD-based model 3).Basedthe onStude (Table residuals were deviation the smallestfor always absolutevalues of and the the of average of 2009 with values verypredicted closeto observed and ABCD-basedthe model (Figure improvement was model The 6). most substantial for accuracyimproved ascospore the predictions release compared of toboth NH thereference Using datasets from avalidation step,the the 2009 to2013for rABCD-based model than ofsmallerthose the model( ABCD-based initial Based onStudent's Ttest, residualsthe of parameters with with Richard's law obtained bestanalysis, tothe on regression fit Based the Improved prediction of ascospore release,using the rABCDthermal time scale This article This protectedis by Allcopyright. rights reserved. rank correlation index was similarly allthese high whether non-linear for functions, Spearman's of values the Interestingly, 1). (Table scale time thermal degree-day reference the ascosporethan release predicted observed and between with abetter link scales time on 11yearsBased offield non-linear data, funcall concerns thebiofix. ascospore of release of prediction field the improvements for two potential presenthighlighted study The Discussion Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument: P V. inaequalis < 0.001), which in turn were significantly smaller than those of of the thanthose significantly inturnwere smaller which < 0.001), P < 0.001).

. One concerns the thermal time scale and the other the time scale and thermal concernsOne the . this rABCD-based model were significantly were model rABCD-based this α 11ascospore datasetswas release =0.98) (R² =100, =100, values. For all years, the overall amplitude the overall years, all For values. tions thistions tested thermal studyin provided P nt's T tests, the absolute of the absolute values Ttests, nt's < 0.05). 0.05). < β =13.5930, =13.5930, γ =0.1343 and δ =0.5629. Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article temperature during a day may be sufficient to allow ascospore development. This hypothesis development. This sufficient to allow be ascospore duringa daymay temperature slightly This below0°C.daily temperatures optimised R( the Interestingly, thedaily relationship describe the between todata of field direct it make use allowed usto studyis that theused in present method the of temperatures specific constant at development Past studies distribution usually associated with biological phenomena. on smooth a the advantage of as thatare theycontinuouslydifferentiable, present functions system support of decision development further models. Forthepredictive ofwould thedevelopment interest of functions for be linear suggests these that This all non- (1982b). of such James &Sutton conditions equation asthe Gauss Analytis and orderived from functions) experiments in controlledconducted (ABCD, study inthe present data of field optimization through numerical parameterised This article This protectedis by Allcopyright. rights reserved. theremoves it First, the predictions. implementation of field practical several advantages for date of observationfirst of mature ascospores in the spring. simplificationThis presents asthestarting calendar biofix fixed usingthat a is study our of keyresult second The ofdate the thermal time canprovide equivalent prediction capacityor better using than the (usually at constant, well controlledtemperat considerations difficulties highlight possible theapplication data oflaboratory-generated for These under leaf study. the and station litter the weather-recording between microclimate also indifferences could stemfrom this result Alternatively, data. using temperature hourly thestrategyby with Rossi is coherent developed Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument: V. inaequalis T ) functions that we obtainedtookpositive) functions withmean values

have relied on laboratory work to establish daily rates of of rates daily establish to work laboratory on relied have ures) to constructfield prediction tools. suggests that even a even suggests positive few a hoursof that in growth chambers. One significant feature Onein significant growth chambers. et al.et rate of development of and temperature. rate s, preference might be given to those given to might be preference s, (2000) to construct a predictive model predictive construct a (2000)to Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article because resultedit in underestimating theearly rendered inap situation This 2013). Beresford, warm temperatures, winter ascospore occurredrelease earlier than bud break (Alves & SuttonJames (1982a, & Furthermore, recent1982b). workhasshown that ina region with ofwider number pseudothecial maturation phases, including those early evoked phases by itallows models the totakeinto that account possible ofeffects climatic parameters on a those based onphenological the stage of the trees inthe spring (Stensvand France). A of benefit this Southern early biof 1 January largely the anticipates observationfirst of ascosporesmature (by month in 1-1.5 associat imprecision andpossible samples field their regularly uncertainties encountered bylocal services representativeness the concerning of aweek for twice 3-4 in January-February year.weeks each the removes Secondly, it the examine atleast samplesof collect field pseudotheciamicroscope under and ascospores logistical substantial advisorylocal services to determineneed datethe appearanceof mature of inthespring.ascospores saveThus itcan This article This protectedis by Allcopyright. rights reserved. of dormanc the end tothe thus could correspond obtained datesrank correlation coefficient biofix 20 December before 3).Thisfor (Figure little have oneffect pseudothecial maturation, as shown by of thelower Spearman's values the study present to identifyInterestingly, allowed aperiod when temperature appeared to the basisfor leaf emergence on apple trees (Carisse (Gadourymodel NH the days in For a example, temperature of0°C isused as between thephenological stages of theapple tree anddevelopmental stages of pathogen. the predictionmodels.Other was recommended for a of coincidence reported workers have lack Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument: et al

., 1982a), whereas a temperature of 5°C was reported asoftemperature wasreported 5°C whereasa 1982a), ., effort and requirements for qualified labor tolabor qualified for requirements and effort ix incomparison withother methods, including the the basis for the computation ofscab degree- risks of ascospore of release,risks calendarand date a y period of pseudothecia described by before of y period propriate the use of bud break as biofix,a et al. ed with sample ed withsample size. a Thirdly, of biofix , 2007). et al. , 2006a), is Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article and 2013) for whichascosporeand 2013)for release occurred se datathe for all of the four years used for model validation, including two atypical years (2012 sets 11 used model data the for based model, for predictions significantly better provided model withfour evaluation additional data independent ABCD-based to 2013. sets The 2009 from year using 11 predictive model, a of construction of interest The combiningcalendar biofix a and ato temperature response non-linear pseudothecial for (ABCD inmaturation present case)function the with was theconfirmed cultivars. apple and pathogen local Adaptation to might populations beneeded hemisphere. also southern in the in otherregions. Furthermore, adaptation SouthernFrance require andmay in conditions wasbasedlocal climatic on biofix study calendar the present 1January the in optimizeddateof Clearly, for found the 2009). for authors several This article This protectedis by Allcopyright. rights reserved. orchard of the these protection dates, butitwould alsohaveto treatment onall led advicea 6). using resulted in wouldhave model Figure Conversely, the MayABCD-based 2013; 5May 2009;2010; 4,8,April and 27Apriland and20Mayreleases 29April 5 of26 2012; absenceprotection of of theorchards against oneto three infections per year (ascospore would have model incited growersthe tosuspendtoo early treatments andresulted in an ourstudy,validation in basedon such advice of has been years load 90%of ascospore the the four Overall estimated for released. where chemical iscontrol fully successful year after year, if no disease has whenoccurred an treatmentstypicallyby ofadvisorsfor chemical recommendedcessation orchards local is spra interrupt when growers to traditionally tend Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 V. inaequalis V. inaequalis Comment citer cedocument: different calendar biofix dates would obviously be appropriate appropriate dates obviouslywould be biofix calendar different

(James &Sutton, 1982a,1982b)or of ascospore release than the reference NH- yagainst programs apple InProvence,scab. a decision threshold together with the NH a decisionthreshold together with the s of field data from Southern France, and its France, and Southern data from field s of construction. It also provided Italso toconstruction. better fit veral weekslaterveral aperiod than at usual, V. pyrina (Rossi etal. , Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article management. management. For theunnecessary example, of 12 May treatment above mentioned 2009 ascospore releaseperiod,scabthe ofimportancetwo phases for crucial are as those accuramodel consistedgenerally more inbased a release. prior to ascospore Themostuseful improvements of this sensitive""rain rABCD- to takerules" into account the positive influence ofrainy days on pseudothecial maturation major Thethird result of the present study significantthe isthe in improvement thermalobtainedof the time bythe value model, predictive with "accelerating adjusting asdevelopment described byJames&Sutton 1982b). (1982a, timethermal scale takes into account the actual reduction in the daily of rate pseudothecial over-evaluate the toofdaily pseudothecialtends rate maturation. Incontrast, theABCD NH-based model the conditions, accumulationIn such degree-days. of in fast a resulting the release endof period, spring ascospore atthe usually are high inlate temperatures the ABCD-basedof in model theFrance conditions of Southern couldto be due the fact that whic ascosporeagainst the release2009, 12 May of This article This protectedis by Allcopyright. rights reserved. bud breakbefore inalargestudydayperiod i release. winter andadelayof in ascospore end time thermal rABCD ofthe therules" "accelerating of for the establishment basis The strong a for evidence the is study inthis scale overestimation. of risk frequency a reduced but security of level In comparison basicto the ABCD-based model, therABCD-based model carries asimilar NH- ABCD-based and against themodels) ascospore of 2011(Figure release 27 March 6). the both by (prescribed unnecessary treatment an saved have model would rABCD-based the have beenwould not prescribed whenusing th Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument:

nvolving 21 orchards of 11 countries, including11 nvolvingcountries, 21 orchardsof link between the number of rainy the days the of at number between link Such a relation was first described Such relation 30- was the a first for e rABCD-based model (Figure6).Similarly, te prediction of the beginning of the and ending of te prediction h was not justified (Figure Thebenefit6). Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article observed, compared to a maximum of 48443 in 2004), but the first rain triggered release the rain first butthe 48443 in2004), of maximum to a compared observed, captured ascospores was smallestthe inthe15 da observationfollowed matureas the first of the within 2000,for occurred no rain the40daysevent which most illustrative year was that The Southern France. the of of conditions themodels in value the predictive not improve did halting time thermal that with the adjusting present is thestudy of result Anintriguing take possible into to period, of ascosporeaccount the dry effect rules, release the days during particularlydry and windyclimate ofProvence. known, but possiblycould be dueto prlow rainfall original study (0.2 mm; Stensvand thresholdprovided algorithm (2.5 rain by the dailythe optimal However, 21 February. January to 13 from timing, comparable and length present studyyears to11 data of field in Prov (Stensvand France This article This protectedis by Allcopyright. rights reserved. are somehow Provence dryadapted toits windy possible One hypothesis notknown. strainsare could be that of scabresults apple with different reasons ourmarkedly for The data). (unpublished Provence pyrina Venturia described by Eikemo 2000; Stendsvand s progress important in provided introduction surprising whenusing was quite their inourregion improvement because halting rules would have with to provide led an farmers erroneous risk" "low advice. Thisabsence of 41%of 4).Halting the stock total of (Figure Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 ascosporerelease for four data oversets three French regions, including et al. et al. Comment citer cedocument: et al et , 2006a). , Furthermore, 2006a). using forthepear scab modelrules halting , 2006b). , algorithm numerical The applied of optimization inthe . (2011),obtainedwe of substantialimprovement in. the prediction

et al. , 2006b). Specificreasons , are not difference this for cab prediction in various (Rossi countries in cab prediction the thermal during long thethermal time that dry period mm) was substantially higher than that of the higherthan mm) substantially was cospores. On total the year, amount of that ence arainsensitivityestablished period of ence tasets used in this study (total of 610 spores 610 of studyin this tasets (total used climate andtheir pseudothecia are ableto oducing limited wetting of leaf litter in thelitter in leaf wetting of oducing limited V. inaequalis V. prevalentin et al. , Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article contrasted climatic conditions. withregions other temperaturefunction in scales with non-linear based ontimes a models inprogress, usin services. Furtherworkis Southern France.Ithas tested sincebeen 2009 and adopted in 2013 by regional advisory conclusion, thepresented In new model this studymorein providedsignificantly accurate predictions of ascospore release than the reference NHin model conditions the of result the particularfrom behaviour oflocally prevalent strainsof thepathogen. It model. becan speculated that some of the need suchfor adjustments possibly could also climate conditions of type local value ageneral predictive theaim of with the refining of al selectiontypes pressure, of including resistance host and of presence fungicides (deVlas morning dew depositing on the leaf litter. This fungus knownis for its adaptability to various possiblyrain, occasionalmaking absence maturation of even prolonged useof in pursue their This article This protectedis by Allcopyright. rights reserved. Alves Beresford 2013. SAM, RM, Evaluation models of predictingthree for References France)theirPACA, for helpkind withthisstudy. (SRALDRAAF Bernard Rouillé and France) Lyon, (ANSES Remuson Florent France), authors Delphine thank The Blanke (University Avignon, France), of Aude Géa (CIRAME, Acknowledgments ., 2012; Van inaequalis 7. Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 ascospore release SouthernBrazil. in et al et ., 2013). Large effortshave beendedicated toadapt apple scab models to Comment citer cedocument:

g methodologicalapproach, asimilar todevelop New Zealand Plant ProtectionPlant New Zealand

Venturia Venturia 66 , 303- et Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article Analytis S, 1979. Die Transformation von Befallswerten in der quantitativenPhytopathologieder Die in vonBefallswerten 1979. Transformation Analytis S, zwischen Relation die Über Analytis S,1977. biologischer bei undTemperatur Entwicklung This article This protectedis by Allcopyright. rights reserved. Battilani P, Camardo Leggieri M, Rossi V, Giorni P, 2013. AFLA-maize, a P, 2013.BattilaniAFLA-maize,Rossi GiornimechanisticCamardo Leggieri a P, V, M, Carisse O,Jobin T, Bourgeois G, Predic 2007. RM, Beresford 1999.Validation of modelan ascospore apple prediction for blackrelease Eikemo H, Gadoury DM, Spotts RA,H, Villalta Gadoury Spotts DM, Eikemo RA,H, Villalta Gadoury Spotts DM, Eikemo Damos P, Savopoulou-Soultani M, 2012. Temperat Key P, Creemers vanLaer S,the 2006. for strategies dependence reduction of on fungicides Carisse O, Meloche C, Boivin Jobin T,G, 2009. Action thresholds for summer fungicide Gadoury DM, MacHardy 1982a. WE, A model to es II. DasBefallskurven. von Linearisieren II. phytopathogenen Pilzen. Computers andElectronics inAgriculture for model spot ( ofsix models to estimatematuration of ( discharge scab pear ascospore to of seasonal estimate models maturity ascospore of doi:10.1155/2012/123405 requirements. thermal vital and integratedin production. fruit sprays sequential and classification ofapple scab incidence. 229-38. period. scab primary during the accumulation Venturia pirina Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Venturia inaequalis Aspergillus flavus Aspergillus Comment citer cedocument: ). ). IOBC/WPRS Bulletin IOBC/WPRS Phytopathologische Zeitschrift ). ). New ZealandPlant Protection

Phytopathologia Polonica infection and aflatoxin B1 contamination in maize.in B1 contamination aflatoxin and infection Psyche Venturia pyrina.Plant Disease

, vol. 2012, Article ID 123405, ID13 pages,2012. Article 123405, 2012, vol. , 54 Phytopathologische Zeitschrift

O, Creemers P, Stensvand2011.Evaluation P, A, O, Creemers O, Creemers P,Stensv 94 , 41-44. ting leaf emergence degree-day from apple , 38-46. ure-driven models for insect models for ure-driven development Canadian Journal of Plant Science Plant of Canadian Journal timate the maturity of ascospores thetimate maturityof of

90 39

52 , 64-76. , 19-29. Plant Disease , 148-52. and A, 2010.Evaluation and A,

96 , 279-84. , , 156-71. 93 , 490-8.

88 , Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article Holb IJ,Heijne WithagenB, JCM, GállJM, Jeger Analysis MJ, 2005. ofsummer epidemic oftemperature during formation MacHardyGadoury DM, HuC,1984.Effects ascus WE, Gadoury DM, MacHardyPreparation 1982b. WE, a This article This protectedis by Allcopyright. rights reserved. James JR, Sutton TB, 1982b. A model for for SuttonJames1982b. Amodel JR, TB, James TB, JR, 1982a. Sutton Environmental fact removal sprays leaf scabapple final combinedwith against and of first Timing 2008. Holb IJ, Jalali MA, ArbabL, Jalali A,De Tirry P, the Clercq 2010. of development Temperature-dependent Lagarde MP, 1988. Studies on maturation ofmaturation on Studies 1988. MP, Lagarde Eliopoulos DC, Kontodimas Stathas GJ, PA, inaequalis ascospore frequency development of discharge of and onpseudothecial pseudothecia of Venturia inaequalis Hungary. apple different scab at apple of progress inaequalis ascosporeand maturation of 10 afactitious under temperatures. food constant and organic pruninginproduction.and apple criteria. criteria. a linear a of evaluation Pseudococcidae): Coccinellidae)(Coleoptera: preying on development dependent of ladybeetle, two-spotted , paper 124.10.1673/031.010.12401. doi: Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Environmental Entomology Phytopathology . . Plant Disease Phytopathology Comment citer cedocument: Venturia inaequalis . Phytopathology Adalia bipunctata Adalia

68 95 Nephus includens

72 , 223-5.

Venturia inaequalis , 1001-20. , 1081-5.

. 33

Phytopathology 72 , 1-11. , 901-4. Economou LP, 2004.Comparative temperature- Crop Protection predicting of ascosporematuration , on the green peach aphid,peach on the green , Venturia inaequalis Venturia nd various nonlinear models using specific production systems in the Netherlands Netherlands productionand systems the in (Kirsch) and (Kirsch) ors influencing pseudothecial development Planococcus citri Planococcus . Phytopathology nd interpretation ofnd interpretation squash mounts of Journal Science ofInsect (Madison)

72 , 92-5.

27 Nephus bisignatusNephus , 814-22. (Cke. ascospores Wint.) (Risso) (Homoptera:

72 , 1073-80. Myzus persicae (Boheman) Venturia Venturia ,

Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article Rossi V, Salinari Giosue F, V, Rossi S, Pattori E, 2009.Bugiani R, Predicting the dynamics of 2000.newGiosuethe estimating model S,BugianiR, A M, Marinelli I, V,Ponti Rossi least-s 1963. for DW, Analgorithm Marquardt Lovell DJ,Powers SJ,Welham SJ, A Parker ontheSR, perspective 2004. ofmeasurement T, 2012.LeglerCaffi Rossi V, SE, A nonl This article This protectedis by Allcopyright. rights reserved. Eikemo H,StensvandA, Seem GadouryRC,Use of DM, rainfall 2005. a thresholdfrequency 2007.MeasuresSheskin DJ, Association/Correlation. of In. Jones of 1989.Relation to degree-daySchwabe WFS, AL, vanaccumulations E, Blerk Stensvand A, Gadoury DM, Amundsen T, Seem RC, 2006a. An adaptation of the Newof the An2006a. AmundsenT, SeemRC, adaptation Gadoury DM, StensvandA, 96-105. of development ANPP,1093-8. (France), Paris Bordeaux: modelling. to adjust a degree-day model of ascosporematurity degree-day of of a model adjust to 416. Pr Statistical Nonparametric 6. of maturation ascospores of 99 maturation of ascospore weatherto conditions. ascospores of pattern of seasonal air-borne oftheJournal SocietyandIndustrial for Applied Mathematics epidemiology. disease plant in time 89 , 453-61. , 198-202. Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Proceedings of the Second international conference on plant diseases onplant conference international Proceedings Second of the Comment citer cedocument: Erysiphe necator Journal ofPlantPathology Venturia pirina Venturia Venturia inaequalis

ocedures, FourthEdition. ocedures, chasmothecia ongrapevine leaves. Plant Pathology based on environmental factors. on factors. based environmental Venturia inaequalis Venturia quares estimation of nonlinear parameters. estimation of nonlinear quares inear model for temperature-dependent for model inear in South Africa.

53 , 111-8. Venturia inaequalis Venturia , 705–12. Chapman & Hall/CRC, Chapman & 1219- Handbook of Parametric and

11 (Cooke) Wint. in relation in (Cooke) Wint. , 431-41. Phytophylactica Plant Pathology Plant Phytopathology . Plant Disease Plant

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Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article Vlas M de, Jong PF Heijne B, 2012.de, Strategies usingfor protectionplant products against V, Caffier Van AL, Chauveau P, Lasserre-Zuber 1997.DM, release GadouryStensvand AmundsenT,SembL, RC, Ascospore and A, Seem Seem H,Stensvand Eikemo Gadoury RC, A, green 2006b. DM, Climatic priorto conditions This article This protectedis by Allcopyright. rights reserved. Xu XM, Butt DJ, Van DJ, simulating1995. Butt A dynamic Santen G, model Xu XM, apple leaves infection of Xu respons 1996.Onestimating non-linear XM, Zou KH, Tuncali K, Silverman SG, 2003. Correlation and simple linear regression. simple linear Correlation and 2003. Silverman SG, K, KH,Zou Tuncali 29(1) in apple affect ascospore of maturation tip Norway. Hampshire degree-day predictmodel to releaseascospore of apple scab scab ( apple Phytologist a study population: pathogen case inanapplex on locia trait quantitative resistance by host exerted pressures selection Differential temperatures. ofapple infection leaves by ascosporesand conidia of by 84 temperatures. Radiology , 127-31. Venturia inaequalis Venturia Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 , 243-7. , Bulletin OILB/SROP

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44 , 865-76. A, Brunel D, LeCam B, Durel C-E, 2013. e of fungal development under fluctuating fluctuating development under fungal of e Venturia inaequalis Venturia inaequalis Venturia Venturia inaequalis Venturia inaequalis Venturia . Bulletin OILB/SROP Bulletin OILB/SROP Bulletin pathosystem. pathosystem. at low New in

Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article thermal timescales. and dynamics release ascospore thelink between of assessment and maturation pseudothecial 1: functionTable Definition temperature the of This article This protectedis by Allcopyright. rights reserved. x

T scale scale time of thermal Type "ABCD" "ABCD" 1982b) 1982a, & Sutton, (James Sutton James & 1982a) MacHardy, 0) base NH (degree-days - oiidGus R( Gauss Modified 1977) Analytis ( = average daily temperature (expressed in °C); °C); in (expressed daily temperature = average

(Gadoury & Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Analytis, Analytis,

Comment citer cedocument: Equation of the R( the of Equation otherwise otherwise R( R( R( R( + {1if( - c T T T T ) if ( ) if ) = k*( ) = - {(T ) = ) = 0.0031 +0.0546* ) = T T T T > if ) =(1/(1+ >= c T and and T b a - >0 C; 0 otherwise reference reference >0 C;0otherwise

and and )/( a ) b T b * < ( - T c d a - <= a ); 0 otherwise} otherwise} 0 ); T ) if ( ) if ( ) function ) T b c - ) ); 0 otherwise} +{(- ); 0otherwise} d T if ) T )) * exp(-( * )) T > a - 0.00175* T a , > and b s (R)used determining for daily the of rate , a c x or

, T d T < T = parameters of the R( the of parameters = b < - ); 0 otherwise} ); 0 c T c )²/ ² reference ; 0 ; 0 d ²) ²) T + d )/( d value highest the providing rs Paramete 230000 k = d =2.51 59 c = b =0.96 a =5 d =15 10 c = b =-1 a =2.1 d =31 23 c = b =5 a =-4 T x ) equations equations )

1 January Biofix Biofix 1 January 1 January 1 January es ascospor mature on of observati First 1 January st st st st st

coefficient coefficient correlation rank Spearman's 0.924 0.922 0.926 0.911 0.875 0.877 ρ

Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article Year weather recording in Avignon, station France a near ground the on stored and Delicious) Golden (cv orchard organic untreated an in autumn by release Ascospore 2: Table This article This protectedis by Allcopyright. rights reserved. 07 6Fbur 6Mrh7My5875 7357 626 May 7 20May 48443 June 1 6062 <500 610 6March 20March 8June 34519 8April 10439 16February 23May 3March - February 23 2007 May 9 10June March 27 7466 <500 2006 15March June 7 27February 2005 15155 February 27 2004 2April 20February 18May - 2003 7 26March - 19February 2002 2June March 23February 2001 16March 24February 2000 February 27 1999 24February - 1998 2 15February 1997 March 1996 02 2Mrh pi 1My816 2822 17247 11May 25668 31May 7433 19May 9March 15May 1April May 5 15February 15March March 12 3March 2013 9March 12-13 March 2012 16February 2011 7February 2009 2008 Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 mature ascospores ascospores mature first of observation of Date Comment citer cedocument: Venturia inaequalis Venturia ascospore release release ascospore first of Date

(1996 2013)to leaves collected from apple each ascospore release last of Date season season the over counts Cumulated ascospore Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article section. andMethods Materials the in described as scale time thermal rABCD sensitive rain improved the from constructed was model rABCD-based The 1. Table in defined are models ABCD-based and NH-based the of functions release shown in Figure 7 shown Figure in release present study for the prediction of ascospore release by by release ascospore of prediction the for study present Table 3: Validation (with observed data from 2009-2013 seasons) of modelsthe developed in the This article This protectedis by Allcopyright. rights reserved. x rABCD-based model rABCD-based model ABCD-based model model reference NH-based Residuals = difference between observed and predicted values of percent cumulated ascospore ascospore cumulated percent of values predicted and observed between difference = Residuals Model / year year / Model Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 0348 3 1. 251/64/16 6/9 7/9 1/14 11/16 3/ 9 13/14 2/ 9 22.5 6/16 44.32 6 / 9 - 22.71 18.33 / 7 9 -19.5 -14.39 -20.76 3 -10.62 10/16 2013 4.89 3/ 9 29.93 13/14 1.95 7.71 / 2 9 2012 9.85 - 11.05 25.9 1/16 2011 4.67 - 48.1 32.5 - 32.7 2009 -18.00 -24.40 -32.50 9/ 9 15/16 7.90 -2.40 - 2013 5.02 23.70 9/ 9 13/14 2012 16.45 30.30 33.0 64.4 12.10 2011 57.8 60.2 12.70 -32.50 -64.40 2009 -57.80 -60.20 0.50 - - 2013 12.70 - 2012 27.90 16.80 2011 10.50 2009 values absolute of Average Comment citer cedocument: positive Maximum

Residuals negative negative Maximum x

deviation deviation of Amplitude Venturia inaequalis Venturia overestimates overestimates Number of . The temperature temperature The . underestimates underestimates Number of Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article time andthe thermal scales ascospore release of between link dynamics the release period. ascospore the dryness during gained by benefits 4: Assessment of Table possible This article This protectedis by Allcopyright. rights reserved. Type of thermal time scale Type of biofix Type biofix of scale time of thermal Type ABCD-based 0) -base (degree-days NH Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument: aur 0960.721 0.847 0.926 0.875 1 January 1 January mature ascospores ascospores mature observationof First ascospores mature observationof First

Spearman's rank correlation correlation rank Spearman's taking into account taking into the occurrence of ofperiods Temperature only time scale scale time adjustaccount the to into taken factors Climatic 0.923 0.723 0.877 0.843 ρ . was used to quantify wasused the to days days dry + Temperature

This article This protectedis by Allcopyright. rights reserved. Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument:

Version postprint of anew thermaltime scale andapplication formodelling ascospore releaseinsouthern France. Roubal, C.,Nicot,P.C. (Auteurdecorrespondance) (2016).Apple scab:numerical optimization Accepted Article This article This protectedis by Allcopyright. rights reserved. Plant Pathology, 65 (1),79-91. ,DOI :10.1111/ppa.12398 Comment citer cedocument: