Apple pest and pathogen reduction in landscapes with large patch size and small area of orchards: a national-scale analysis

Context : The composition and con�guration of habitats in agricultural landscapes may determine crop damage resulting from pests or pathogens either by directly affecting their population dynamics or through indirect effects on their natural enemies. Objectives The aim of this study was to assess the impact of landscape composition and con�guration on the occurrence and damage caused by the codling moth and apple scab in apple orchards. Methods Using monitoring data at the French national scale, we examined how the proportion of landscape area grown with orchards the mean patch area of orchards the share of organic orchards and the proportion of woodlands and grasslands affected the occurrence and damage of these two pests from 2015 to 2019 in approximately sixty apple orchards each year.


Introduction
Understanding how environmental conditions affect pest populations in agricultural landscapes is the cornerstone of agroecological crop protection limiting the use of pesticides.While several environmental factors operating at multiple scales affect pest population dynamics landscape structure and weather conditions are among the important factors (Courson et al. 2022; Zhang et al. 2018).Several aspects of landscape structure belonging to the composition or con guration of agricultural landscapes can directly and indirectly impact the abundance of insect pests and pathogens in crops (Delaune et al. 2021;Martin et al. 2019;Plantegenest et al. 2007;Rusch et al. 2016).First increasing host crop area can directly enhance the population of pests or pathogens by providing them with more resources and breeding habitats or facilitating dispersal (Landis et al. 2000;Plantegenest et al. 2007;Ratnadass et al. 2012;Tscharntke and Brandl 2004).This facilitation can result from both the quantity of host crops and the increase in the size of the crop patches creating more homogeneous landscapes with a high degree of crop connectivity (Martin et al. 2019).In addition, farming practices within crop mosaics affect pest and pathogen habitat quality (Marrec et al. 2022;Rusch et al. 2010;Vasseur et al. 2013).Organic farming for instance has been shown to host more biodiversity including pests and natural enemies in many crops (Muneret et al. 2018a; Samnegård et al. 2019).At the landscape scale organic crops could thus act as reservoirs of both pests and their natural enemies making the outcome of an increasing share of organic crops di cult to predict.Then, homogeneous landscapes with a low proportion of fragmented seminatural habitats tend to allow for greater and earlier immigration of insect pests due to reduced topdown control delivered by natural enemies (Gagic et al. 2021;Tscharntke and Brandl 2004).Indeed, seminatural habitats such as grasslands or forests provide resources breeding sites and refuges for a large diversity of natural enemies of pests (Landis et al. 2000).Decreasing their proportion or connectivity at the landscape scale can thus reduce pest control services ( Veres et al. 2013).Moreover, seminatural habitats may act as a barrier to pathogens or pests with passive dispersal thus reducing pest or disease outbreaks (Plantegenest et al. 2007; Ratnadass et al. 2012).Despite decades of research, the relative effects of these different aspects of landscape structure on pest or pathogen infestation levels in crops remain poorly understood as they are rarely jointly analysed.
The explicit consideration of weather conditions is rare in studies of the effect of landscape structure on pests (but see Courson et  and can interfere with landscape effects (Karp et al. 2018).For example, increased air humidity and precipitation can promote disease infestations by supporting pathogen dispersal and spore germination (Combina et al. 2005).In addition, increased temperature can promote insect pest infestations by increasing their development rate and possibly the number of generations of multivoltine species (Deutsch et al. 2018;Gilbert and Raworth 1996).The few studies that have investigated the combined effects of landscape structure and weather conditions on pests (Courson et al. 2022;Gutiérrez Illán et al. 2020) con rmed that both aspects can affect pest dynamics and more studies integrating these two dimensions are needed to better manage pests.
Apple orchards are the dominant orchards in metropolitan France (46% of orchards in area 2020, Agreste 2021).Apples are one of the most treated crops with a treatment frequency index (TFI) of up to 35 in 2017 compared to 7 on wheat or 18 on potato that same year (Agreste 2020).Most treatments target two main pests: the apple scab pathogen and the codling moth insect pest.Apple scab is caused by the fungus Venturia inaequalis (Cooke) G. Wint which is speci c to apple trees (Bowen et al. 2011).It is the most economically damaging disease in apple (MacHardy et al. 2001).Decision support tools predicting the risk of apple scab infection are mainly based on weather variables such as temperature humidity and rainfall (Rossi et al. 2001).The effect of landscape structure on apple scab infestations remains poorly documented although spores may disperse among distant elds (Aylor 1999).
The codling moth Cydia pomonella L. (Lepidoptera: Tortricidae) is the most damaging insect pest of pome fruits including apples and pears in many temperate regions.Free neonate larvae penetrate into fruits causing damage.At the end of their development, the larvae leave the fruit and depending on temperature and photoperiod conditions either pupate to produce the next generation or enter diapause (Riedl and Croft 1978).Adults emerge in spring from overwintering larvae.Models predicting codling moth phenology are mainly based on temperature (Boivin et al. 2005;Riedl et al. 1976;Welch et al. 1978) with a minimum temperature required for codling moth development of approximately 10°C (Gharehkhani 2010; Saethre and Hofsvang 2002).In addition, as for apple scab weather conditions can impact codling moth population dynamics.In general rainfall is unfavourable (Zhao et al. 2015) because it increases larval mortality (Hagley 1972) and decreases oviposition (Hagley 1976).The landscape proportion of host crops was shown to affect codling moth abundance but with opposite directions of effect for intensive apple orchards (Ricci et al. 2009) and extensive cider orchards (Martínez-Sastre et al. 2021).
The predation of sentinel codling moth eggs and larval parasitism were lower in apple orchards surrounded by a large area of conventional orchards (Maalouly et al. 2013;Monteiro et al. 2013).In addition, seminatural habitats tend to increase codling moth predation by natural enemies (Heath and Long 2019).
Using national-scale data, we aimed to assess the impact of landscape structure on the infestation levels of apple orchards by the apple scab and the codling moth and associated fruit damage while controlling for weather conditions.We rst hypothesised that increased overall orchard area orchard patch size or orchard organic farming in the landscape would promote apple scab and codling moth infestations due to a large amount of crop resources.In addition, we expected that increasing the amount of seminatural habitats would reduce the abundance of apple scab and codling moths due to the barrier effect of woodlands or hedgerows and the bene cial effects of seminatural habitats on pests' natural enemies.

Data collection
Pest data were retrieved from the Epiphyt database an epidemiological surveillance database held by the French Ministry of Agriculture.Apple scab and codling moths were monitored from 2015 to 2019 according to standardised protocols based on observations of pests or damage to different plant organs from one to several times each year (Table S1).Data are available at the plot level.The observation plots are not precisely located but their municipality is known.For each of the two main pests i.e. apple scab and the codling moth data are available from two observation protocols each corresponding to a different period of the pest's life cycle.Plots were distributed all over France except for the plots monitored for adult codling moths which were located only in western France (Fig. 1).

Apple scab records
The rst two variables that we retrieved from the database are the presence/absence of shoot damage in the plot and the date of rst occurrence of shoot damage expressed as the number of days from the 1st of January.The data came from a single protocol based on the visual evaluation (presence or absence of damage) of 500 shoots per orchard at each observation date from April to June.On average 113 ± 34 (standard deviation, SD) plots were monitored each year in a total of 169 municipalities.The date of rst occurrence was only recorded when damage was present which was the case for 40 ± 15 (SD) plots each year on average (Table 1).These two variables are associated with early pest abundance.The third retrieved variable was the presence/absence of fruit damage in the plot in June.These data were based on the visual assessment (presence or absence of damage) of 500 fruits (20 fruits per tree on 25 trees) in June (end of primary infection).On average 77 ± 20 (SD) plots were monitored each year in a total of 150 municipalities (Table 1).

Codling moth records
The rst retrieved variable was the date of rst adult moth occurrence expressed as the number of days from the 1st of January each year.These data came from adult codling moth trapping using pheromones from April to October in a total of 60 municipalities.The date of rst occurrence was only recorded for plots in which codling moth adults were captured i.e. on average 32 ± 10 (SD) plots per year (Table 1).
The second retrieved variable was the presence/absence of fruit damage by codling moth larvae in June when rst-generation larvae were fully developed.These data came from the visual inspection of 500 fruits per orchard (20 fruits per tree on 25 trees).Data were available for a total of 151 municipalities.On average 80 ± 18 (SD) plots were monitored per year (Table 1).

Weather data
To describe the weather context of each plot each year we used the interpolated meteorological dataset of Météo-France (Safran).This dataset contains estimated weather information for France based on 8 km x 8 km grid cells.Many weather variables are available among which we retrieved daily relative humidity rainfall and temperature (average and minimum values).For each year from 2015 to 2019 to associate the pest data with weather variables the centroid of the municipality in which each Epiphyt plot was located was associated with the corresponding grid cell.
Weather variables used in statistical models seeking to explain pest occurrence were selected based on their expected effect on the pest life cycle.For both pests the following variables were thus selected: proportion of days with rainfall average relative humidity and average temperature.For data on pest or damage occurrence these weather variables were calculated every year starting from the rst day when the average temperature was 10°C until the last day of the last month of the corresponding protocol.For data on the day of rst occurrence the weather variables were calculated from the rst day with a mean temperature of 10°C to the day of occurrence.Temperature and rainfall were slightly correlated (R = 0.54, Figure S1).
Depending on the year the proportion of rainy days varied from 0.44 to 0.60 with an average humidity from 70.4-79% and an average temperature from 8.9°C to 13.1°C in municipalities where apple scab was observed (supplementary material, Table S2).The proportion of rainy days varied from 0.40 to 0.63 with an average humidity from 67.8-80.9% and an average temperature from 8.4°C to 13.4°C in municipalities in which codling moths were observed (Table S2).

Landscape context
The landscape was characterised at the municipality level.These administrative areas covered 2776 ± 3242 ha on average (mean ± SD).Maps were created by combining; (i) the French parcel identi cation system (RPG a geographic database for registering farmers' parcels under the Common Agricultural Policy) which provided information on the type of crop or grassland (temporary or permanent) in each parcel from 2015 to 2019; and (ii) BD TOPO® (v2 2017 IGN, Institut géographique national) which provided information on woodland orchards and vineyards.Land cover information from these two landscape databases was combined with a priority on the RPG which is lled in every year (R package alm, Allart et al. 2021).Then the proportion of area covered with orchards woodland and grassland as well as orchard fragmentation (i.e.here average area of an orchard patch) were calculated within each municipality (Table S2).Note that information was not available about the crops grown in orchards.However, data for districts (French "département" administrative entity grouping several municipalities) in which the monitored plots were located indicate that apple orchards were generally the majority representing (mean ± SD) 44 ± 11% of orchards (Figure S2).
To determine the area of orchards under organic management in each municipality we used the 2015-2019 data provided by the French Agency for the Development and Promotion of Organic Agriculture (https://www.agencebio.org/).When fewer than three farms were organic in a municipality only the number of farms and not area was available because of statistical secrecy.There were organic orchards in 26-70% of the municipalities with study plots depending on the year and retrieved pest variable (Table S3).Municipalities with only one or two organic farms represented 35-74% of the municipalities with organic orchards depending on the year and retrieved variable (Table S3).We extrapolated the area of orchards under organic management for these municipalities.For this purpose, we used data available at the district level.For each year we estimated the area of organic orchard per farm by dividing the area of organic orchards in each district by the number of organic farms in that district.We then used this area to estimate the area of organic orchards at the municipality level taking into account the number (1 or 2) of organic farms (see also Etienne et al. 2023).The results of this procedure which was evaluated on municipalities with more than three organic farms showed that on average the estimated areas under organic farming were aligned with the actual areas.However, there was some variation in the results among municipalities (Figure S3).
For the municipalities in which apple scab was monitored the proportion of area grown with orchards was low with mean values of 3.2-7.8%(mean orchard area of 1.7 to 2.4 hectares) depending on the year.
Over the course of the study the proportion of organic orchards increased from 10.9-34.4% of the orchard area.The proportion of grassland ranged from 9.6-16.5% and the proportion of woodland ranged from 17.0-26.6%.In the municipalities where the codling moth was monitored the proportion of area grown with orchards was also low with mean values of 2.2-8.1% (mean orchard area of 1.8 to 3.1 hectares).Over the course of the study the proportion of organic orchards increased from 6.1-33.8% of the orchard area.The proportion of grassland ranged from 6.3-17.2%and the proportion of woodland ranged from 20.4-36.1%.For each year and protocol some landscape variables were signi cantly correlated although with low R values (|R| < 0.2, Figure S2).The proportion of area grown with orchards in particular was not signi cantly correlated with the mean orchard patch area (R = -0.04)indicating that different proportions of area grown with orchards did not correspond to particular spatial distributions of orchards (i.e.orchards clustered in large patches or distributed in numerous isolated patches).

Statistical analyses
Statistical analyses were conducted using Rstudio software (R version 3.6.1,R Core Team 2022).A generalised linear mixed model with a binomial distribution was used to analyse the variation in the probability of pest or damage occurrence while a linear mixed model was used to analyse the logtransformed date of rst pest occurrence.The xed independent variables in the models described the landscape and weather contexts and a random 'municipality' effect was included to account for the fact that there were multiple plots within the same municipality.The xed landscape variables included the proportion of area grown with orchards the proportion of orchard area with organic management the proportion of area with grassland and the proportion of area with woodland as well as the average size of an orchard patch in the municipality.The weather variables included the proportion of days with rainfall the average humidity and the average temperature over the period of observation for each speci c pest and observation protocol.Variance in ation factors (VIFs) were calculated for all models.The proportion of days with rainfall and humidity were found to be collinear (VIF > 2); thus only the proportion of days with rainfall was retained in the nal models.The number of records per plot was included as a xed variable in all models to account for variability due to this factor.The number of records per plot did not signi cantly affect the dependent variables with the exception of apple scab occurrence on shoots where an increase in the number of records on the plot signi cantly increased the probability of apple scab occurrence.Model residuals were inspected for dispersion using a quantile-quantile (QQ) plot of standardised residuals as well as for uniformity and outliers using a plot of residual versus predicted values.Associated statistical tests were performed with the DHARMa R package ( ) and no spatial autocorrelation was detected.Moreover, standardised residuals were plotted against the region in which the municipality was located to detect potential unaccounted-for temporal or spatial effects.

Results
The occurrence of scab on shoots was on average higher than that on fruits but occurrence frequencies were highly variable between and within years (as shown by a large standard deviation).The lowest scab occurrence was in 2019 (25% on shoots and 17% on fruits) and the highest occurrence was in 2015 on shoots (up to 60%) and 2018 on fruits (up to 39%) (Table 2).The day of rst apple scab occurrence on shoots did not vary much between years (between the 138th and 142nd day on average) except for the year 2016 when it was approximately ten days later.The day of rst moth occurrence was more variable than the day of rst apple scab occurrence ranging from Day 140 in 2016 and 2017 to Day 155 in 2019.
The occurrence of codling moth damage reached 43% in 2017 and was between 18% and 29% in the other years.increased with the proportion of area grown with orchards (Fig. 2).The probability of scab occurrence on shoots increased from 0.30 to 0.83 when the proportion of area grown with orchards increased from almost 0-30% (Fig. 3).Landscape effects were more often signi cant on codling moths than on apple scab (Fig. 2).The rst codling moth occurrence was earlier in landscapes supporting a higher proportion of area grown with orchards.This effect reached 25 days when the orchard proportion increased from almost 0-40% (Fig. 3).In addition, an increased size of orchard patches from less than 1 ha to 14 ha decreased the probability of damage to apples from 0.30 to 0.02 (Fig. 3).
Weather conditions did not affect apple scab or codling moth occurrences but affected their phenology.Earlier apple scab occurrence and later occurrence of adult moths were related to a yearly increase in both the proportion of days with rainfall and the average temperature (Fig. 2).

Discussion
Inconsistent effects of landscape structure on pest infestations have been previously reported possibly due to covariables not being taken into account or variability in climatic conditions (Chaplin-Kramer et al. 2011; Karp et al. 2018).Here we investigated how several aspects of landscape structure related to host crop and seminatural habitats surrounding orchard plots affected the two main apple pests at the French national level while taking into account weather effects.Our results clearly con rmed that weather conditions prominently affect both pests.Among landscape variables only orchard-related metrics signi cantly affected pest infestations.Apple scab occurrence on shoots increased and the rst codling moth adults occurred earlier in orchard plots located in landscapes with a large proportion of area grown with orchards.Furthermore, the occurrence of codling moth damage to fruits decreased in landscapes with large orchard patches.Unexpectedly we found no effects of seminatural habitats on pest or damage occurrence.
We expected positive effects of the proportion of landscape area grown with orchards on infestation levels of both pests.Our results partially con rmed this hypothesis: the rst occurrence of codling moths was earlier and the probability of apple scab occurrence on shoots was higher with an increasing proportion of landscape area grown with orchards.These two signi cant relationships are consistent with the extension of the resource concentration hypothesis to the landscape scale which states that landscapes with large areas of host crops promote agricultural pest loads by increasing their amount of resources and reducing their dispersal costs (O'Rourke and Petersen 2017).They are also consistent with studies that point to the importance of host crop area in explaining pest densities both in annual

2009
).The two variables that responded to orchard area indicate that landscape-scale orchard area affects early pest populations while variables corresponding to later observations such as codling moth and apple scab damage on fruits were not signi cantly affected.Such timing suggests that landscapescale orchard area promotes early eld colonisation.This interpretation is in line with the fact that longdistance dispersal of apple scab spores and its consequences for in-eld contamination by spores emitted by distant elds were formerly demonstrated by modelling studies (Aylor 1999).Similarly, adult codling moths emerge in spring from overwintering larvae and at least part of the population is able to y long distances (Schumacher et al. 1997); thus earlier adult occurrence in traps may also re ect a larger landscape level abundance.
Relationships between host crop area and pest abundance are complex and may show opposite trends For apple orchards in particular opposite effects of host crop area on pests may come from differences in landscape-level pesticide intensity.Large areas of intensively treated host crops tend to reduce pest populations (Ricci et al. 2009) whereas an opposite effect is observed when host crops are extensive (Martínez-Sastre et al. 2021).We investigated this question by considering the share of organic orchards.We found no effect of this variable contrary to our initial hypothesis.This absence of effect is consistent with former results obtained at a smaller spatial scale (Ricci et al. 2009) and concur with results on grapevines (Muneret et al. 2018b) and arable crops (Gosme et al. 2012).Farmers manage pests with a diversity of practices in organic apple orchards (Marliac et al. 2016).For the most part organic orchards are grown with apple cultivars that are resistant or tolerant to apple scab (Holb 2007).In addition, effective treatments against codling moths based on granuloviruses are available and in some regions are complemented by netting systems to protect apple orchards against the codling moth especially in areas where codling moth populations have become resistant to the granulovirus (Marliac et al. 2016).It is therefore possible that although pest damage is generally greater in organic orchards (Samnegård et al. 2019;Simon et al. 2017) organic orchards are not a source of codling moth or apple scab for other orchards.This result should however be taken with caution given that the share of organic orchards in municipalities was approximated based on higher level administrative information for part of the data (see material and methods).Furthermore, we could explore only a restricted range of variation for this variable because most orchards were conventional in the study landscapes.
Our study supports the idea that both landscape composition and its con guration affect pest infestations as we found a lower occurrence of fruit damage caused by codling moths in orchards located in landscapes with large orchard patch areas.Two ecological mechanisms possibly explain the negative trends between crop patch area and pest abundance.The rst stems from dispersal limitation.
Based on a simulation study Edwards et al. (2018) found that grouping elds of annual crops could limit the abundance of dispersal-limited pests because pests cannot build-up populations in the most central elds.Dispersal limitation however is unlikely to affect codling moths that can y over long distances (Schumacher et al. 1997).Furthermore, codling moths overwinter on apple tree trunks or in orchard soil and do not need to colonise orchards every year.The second mechanism is dilution.Negative trends between pest population and crop patch area can be observed when a constant number of pests is distributed over a range of crop areas and the pest becomes locally less abundant as the crop area increases (Zaller et al. 2008a, b).Dilution is expected for actively dispersing specialised pests.Dilution may be responsible for the pattern observed in fruit damage: mated codling moth females can y over long distances (Schumacher et al. 1997) and although females tend to cluster their eggs on nearby trees they may also disperse them among distant trees within orchard patches (Franck et al. 2011;Margaritopoulos et al. 2012) possibly to avoid within-fruit larval competition that is detrimental to larvae (Ferro and Harwood 1973;Jackson 1982).Lastly it is possible that fruit damage was affected by early insecticide treatments that speci cally target neonate larvae.The observed trend could then have resulted from less e cient pest management in isolated orchards either because they are less central to the farm or because pests do not suffer from insecticides sprayed in neighbouring orchards (Ricci et al. 2009).
The absence of effects of seminatural elements whatever the pest was unexpected given our hypotheses but such cases are also often reported in global syntheses (Chaplin-Kramer et al. 2011; Karp et al. 2018;Martin et al. 2019;Rosenheim et al. 2022;Veres et al. 2013).One explanation is that seminatural habitats might also act as reservoirs of pests (Tscharntke et al. 2016).This is unlikely here given the host speci city of the codling moth and apple scab.Another explanation is related to the absence of natural enemies or the limited resources for natural enemies in seminatural habitats (Tscharntke et al. 2016).Such an explanation is likely for apple scab for which to our knowledge no natural enemy has yet been reported.However, it is less likely for the codling moth since the presence of seminatural elements has been shown to increase predation of codling moths in orchards (Heath and Long 2019) the abundance of a predatory spider (Lefebvre et al. 2016) and possibly promote its primary parasitoids (Maalouly et al. 2013).However, the scale of the effect of seminatural habitats considered by these studies was smaller than in the present study and it is possible that small-scale analyses are necessary to detect the effects of seminatural habitats on pest populations (Begg et al. 2017).
Considering data at the national level made it possible to explore a large gradient of weather conditions and landscapes.However, because this dataset was not originally compiled for scienti c purposes there were a few limitations.First we had to strongly simplify the dataset (e.g.modelling the probability of occurrence rather than abundance of pests) to account for differences in data monitoring along years or regions.This likely reduced the ability of our analysis to detect landscape effects but increased its robustness.Second landscape characteristics may covary with weather conditions.To address this possible bias, we included weather variables in the models.These variables as expected impacted pests particularly their date of rst occurrence but none was found to strongly covary with landscape variables (Figure S1 and low model variance in ation factors) indicating that we were able to disentangle weather and landscape effects.Last we could have overlooked some regional features that impacted pest populations (e.g.different farm structures or apple cultivars).However residual variations in our models were homogeneous among the French regions suggesting that this was not the case except for the date of rst scab occurrence for which we found no landscape effect (Figure S4).Despite these limitations we acknowledge that such large datasets initially built for advising farmers also contain precious information that nicely complete more classic information provided by empirical studies usually performed in landscape ecology (e.g.several elds surveyed along landscape gradients).Analysing such datasets makes it possible to explore the variability of landscape-scale effects in multiple climatic contexts and appears to be a step forwards in the direction of building predictive models to anticipate pest outbreaks.

Conclusion
Our results indicate that the main driver of pest dynamics in apple orchards was the spatial distribution of orchards themselves rather than the quantity of seminatural elements.In particular we found indications that the area grown with orchards affected early in-eld colonisation.This calls for the territorial management of orchards to limit pest pressure and pesticide use in apple orchards.The management choices however should be adapted to the local context focusing on the most problematic pests as our results indicate that pests do not all respond similarly to the orchard spatial distribution.In the context of a necessary reduction in the use of pesticides our study further indicates no speci c impact of an increase in the area under organic agriculture but it should be noted that the explored range of area grown organic remained low.

Declarations
Competing interests: the authors that they have no known competing nancial interests or personal relationships that could have appeared to in uence the work reported in this paper.

Figure 1 Locations
Figure 1

Figure 2 Estimates
Figure 2

Table 1
Structure of the data retrieved from the Epiphyt database: number of plots and corresponding municipalities (between parentheses) each year.
Grau et al. 2015)over, ROC curve analyses(Hoo et al. 2017)were performed on binomial models to assess the t of the models with data (PRROC package,Grau et al. 2015).The areas under the ROC curve (AUC) indicated good model ts with values ranging between 0.92 and 0.94 for binomial models.Graphs for signi cant effects and partial residuals were obtained with the effects(Fox etal.2016) visreg (Breheny et al. 2020) and ggplot2 (Wickham et al. 2016) R packages.Spatial autocorrelation was explored on residuals for each year using variograms (variog function geoR package, Diggle and Ribeiro 2007

Table 2
Occurrence (mean ± standard deviation) and date of rst occurrence (in number of days from 1st January) according to the pest per plot each year.
Landscape effects on scab infestation were generally not signi cant.Only scab occurrence on shoots