# Impact of Agroecological Infrastructures on the Dynamics of Dysaphis plantaginea (Hemiptera: Aphididae) and Its Natural Enemies in Apple Orchards in Northwestern France

Laurence Albert, Pierre Franck, Yann Gilles, Manuel Plantegenest

► To cite this version:

Laurence Albert, Pierre Franck, Yann Gilles, Manuel Plantegenest. Impact of Agroecological Infras- tructures on the Dynamics of Dysaphis plantaginea (Hemiptera: Aphididae) and Its Natural Enemies in Apple Orchards in Northwestern France. Environmental Entomology, 2017, 46 (3), pp.528-537. 10.1093/ee/nvx054 . hal-01517228

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Albert et al.: Agroecological management
in cider apple orchards

Environmental Entomology
Biological control – parasitoids and predators

Laurence ALBERT
Institut Français des Productions Cidricoles
La Rangées Chesnel
61500 SEES
France
Phone: +33 2.33.27.56.70
Fax: +33 2.33.27.49.51
E-mail: [albert5@yahoo.fr](mailto:albert5@yahoo.fr)

Impact of Agroecological Infrastructures on the Dynamics of
*Dysaphis plantaginea Passerini (Hemiptera: Aphididae) and*
its Natural Enemies in Apple Orchards in Northwestern
France

Laurence ALBERT<fnref n="1" />, Pierre FRANCK<fnref n="3" />, Yann GILLES<fnref n="1" />, Manuel PLANTEGENEST<fnref n="2" />

<footnote n="1">¹ Institut Français des Productions Cidricoles, La Rangée Chesnel, 61500 Sées, FRANCE</footnote>

<footnote n="2">² UMR1349 IGEPP, INRA/Agrocampus-Ouest/Université Rennes 1, 65 rue de Saint Brieuc, 35042 Rennes Cedex, FRANCE</footnote>

<footnote n="3">³ INRA Plantes & Systèmes de culture Horticoles, F-84914 AVIGNON Cedex 9, FRANCE</footnote>
# 1 ABSTRACT

# 19 Keywords

Biological control, cider-apple orchard, *Dysaphis plantaginea*, flower strip, hedgerow
30 Agroecology proposes to primarily base agricultural production on the mobilization of natural processes
31 and the improvement of ecosystem services (e.g. pollination, nutrient cycling, biological control of pests)
32 rather than on chemical inputs. In particular, promoting the natural control of pests would lead to
33 insecticide use reduction. The resulting reduction of economic and environmental costs would contribute
34 to increase farmer benefits and the environmental sustainability of agriculture (Tschumi et al. 2015).

35 Various approaches have been proposed to improve pest biological control, including changes in
36 practices (e.g. pesticide use reduction, accurate choice of cultivars) and establishing agroecological
37 infrastructures within or in the vicinity of the crop (Haenke et al. 2009, Miñarro and Prida 2013).

38 Agroecological infrastructures include hedgerows, flower strips, permanent grasslands and woodlands.

39 They may provide pests and natural enemies with various beneficial functions, including suitable
40 microclimatic conditions and refuge during adverse seasons (Landis et al. 2000). Thus, spiders, beetles
41 and syrphids use them as overwintering areas (Collins et al. 2003, Sarthou et al. 2005, Pfiffner et al.

42 2013). Agroecological infrastructures also provide pollen and nectar resources that increase the
43 longevity of parasitoids (Wäckers 2001, Berndt and Wratten 2005) and improve the fecundity of other
44 insects (Schmale et al. 2001, Wäckers 2001, Winkler et al. 2006, Hogg et al. 2011, Laubertie et al. 2012,
45 Rijn et al. 2013). Agroecological infrastructures also provide alternative prey for generalist predators
46 when these resources are not available in the crop (Wyss 1996, Denys and Tscharntke 2002, Lavandero
47 et al. 2005).

48 Northwestern France (i.e. Bretagne, Normandie and Pays de la Loire regions) is the number one cider-
49 apple producing area in Europe. Cider-apple orchard cultivation is thus important in the local economy.

50 The management of apple orchards is based on the intensive use of pesticides to control pests and
51 pathogens (Sauphanor et al. 2009). Currently, farmers are under strong pressure to develop
52 environmentally friendly protection strategies to address the new challenges imposed by society, and
53 environmental laws. Because cider-apples are transformed, their perfect visual aspect is not a
54 prerequisite of their marketability and fewer pesticide treatments are applied in cider-apple orchards
55 than in orchards for fresh fruit production (approximately 15 vs 35 treatments per year). Consequently,
56 cider-apple orchards offer an opportunity to develop and test protection strategies using less pesticide,
57 which could subsequently be generalized.

58 Approximately 60 phytophagous arthropod species are considered to be apple pests (Jenser et al.
59 1999). The rosy apple aphid (RAA) *Dysaphis plantaginea* Passerini (Hemiptera: Aphididae), is among
the most detrimental pests, causing significant economic losses by reducing yield (Blommers et al. 2004). The RAA is problematic not only in organic but also in conventional orchards due to its very low abundance threshold for economic damage, resulting in a low treatment threshold (i.e., as soon as the pest is detected) (Cross et al. 2007). As a consequence, an increase in insecticide resistance has been recorded (Delorme et al. 1998). Many recent studies have suggested that improving biological control efficiency could be an alternative to insecticides use to limit RAA populations (Hemptinne et al. 2003, Dib et al. 2010, Miñarro and Prida 2013). RAA is a host-alternating aphid species. Its primary host is the apple tree *Malus domestica* Borkh. (Rosales: Rosaceae), and its secondary hosts are plantain herbs *Plantago spp*, mainly *P. lanceolata* L. (Lamiales: Plantaginaceae) (Blommers, 1999). At the beginning of spring, eggs laid in autumn hatch on apple trees producing parthenogenically reproducing females (Lathrop 1928, Bonnemaison 1959, Blommers et al. 2004). Migration to a secondary host occurs from mid-June to July in the North of France. The aphids return to apple trees in autumn, where a sexual generation of oviparous females lays fertilized overwintering eggs on the apple trees. The economic losses caused by this leaf-roller aphid, which develops on the lower side of the leaves, are mainly due to the deformations caused to the fruits and growing shoots, decreasing the yield in the year of infestation, as well as in following years (Bonnemaison 1959, De Berardinis et al. 1994, Wilkaniec and Trzcinski, 1997, Blommers et al. 2004).

Several recent studies have focused on the community of natural enemies, which could play a role in the biological control of *D. plantaginea* during spring. In Europe, this community is mostly composed of syrphids, coccinellids, parasitoids (mainly *Ephedrus* sp – Hymenoptera: Braconidae), earwigs, spiders and *Aphidoletes* sp (Diptera: Cecidomyiidae) (Wyss et al. 1999, Miñarro et al. 2005, Dib et al. 2010, Arnaudov et al. 2013). The abundance of these natural enemies in orchards depends on the abundance of RAA prey (Dib et al. 2016) and on the intra-guild predation pressure (Rosenheim et al. 1993, Rosenheim et al. 1995, Korenko and Pekár 2010). Thus, while an increase in natural enemy abundance is expected to result in a decrease in RAA abundance, this trend may reverse when intra-guild predation is important (Snyder and Ives 2001). RAA population dynamics also depend on the presence of ants in the colony, as *D. plantaginea* is commonly attended by ants (Bonnemaison 1959, Starỳ 1970). Interactions between the ants and myrmecophilous aphids are beneficial for both arthropods: ants are supplied with sugar through aphids' honeydew whereas aphids improve their reproductive rate (El-Ziady and Kennedy 1956, Banks and Nixon 1958, Flatt and Weisser 2000) and are protected against natural
enemies (Stadler and Dixon 1999, Yao et al. 2000, Kaneko 2003). Thus, the relationship between ants and *D. plantaginea* enhances the growth of aphid colonies by reducing aphid predation by their natural enemies (Stewart-Jones et al. 2008, Miñarro et al. 2010).

Several recent studies noted the potential of agroecological infrastructures to improve the biological control of *D. plantaginea* by favouring the natural enemy community (Dib et al. 2012, Miñarro and Prida 2013, Pfiffner et al. 2013). Knowledge about the distance at which agroecological infrastructures are operating would help to determine the required density needed to provide an efficient biological control. Indeed, several studies noted that the distance to agroecological infrastructures influenced parasitoids (Corbett and Rosenheim 1996, Lavandero et al. 2005), spiders (Miliczky and Horton 2005) and syrphids (Bowie 1999) abundances. Moreover, the link between the distance to agroecological infrastructures and natural enemy abundance is not systematically linear. For instance, Tylianakis et al. (2004) have shown that the proportion of the aphid *Metopolophium dirhodum* parasitised by *Aphidius rhopalosiphi* decreased exponentially with the distance to flower resources.

The present project aimed to determine the impact of two types of agroecological infrastructures - flower strips and hedgerows - on the abundance of arthropods interacting with *D. plantaginea* (natural enemies and ants) and its consequences on RAA population dynamics. The influence of the distance to these two types of agroecological infrastructures on arthropod dynamics was assessed in 14 cider-apple orchards in northwestern France, which exhibit a range of farming practices (cultivars, insecticide use). For this purpose, the arthropod populations (aphids, their main natural enemies and their mutualistic ants) were monitored in spring during two successive years.

110

111

# Materials and Methods

112

## Monitored Cider-Apple Orchards

Experiments were carried out in the spring and early summer in 2014 and 2015 in cider-apple orchards in seven locations in northwestern France (Fig. 1). The orchards were planted between 2010 and 2012 with three different cider-apple cultivars (three consecutive rows of each cultivar: Douce de l'Aventcov, Dabinett and Judor) grafted onto MM106 rootstock. The three cultivars differed in their vigour and precocity: Douce de l'Aventcov (DDA) was the most vigorous and precocious cultivar, Dabinett (DAB) was the less precocious cultivar and Judor (JUD) was intermediate.

113

114

115

116

117

118
119 In each location, two contiguous orchards were studied that differed in regard to insecticide application and in the agroecological infrastructures established (Table 1). Only five out of the seven locations were monitored in 2014 (Fig. 1).

122
123 Monitored Trees

124 Approximately one-third of the trees were systematically monitored in each orchard (63 to 423 contiguous trees, depending on the considered orchard - Table 1). For each apple tree, the distance to the closest hedgerow (ranging from 5 m to 57 m), the distance to the closest flower strip (ranging from 0 m to 63 m) and the insecticide use were recorded, and the arthropod population dynamics were monitored.

129 The hedgerows were mainly composed of *Carpinus betulus*, *Cornus* sp, *Corylus avellana*, *Viburnum* sp, *Sambucus nigra* and *Quercus pedonculata*. All flower strips, established specifically for the study, included *Centaurea cyanus*, *Silene vulgaris*, *Silene latifolia* alba and *Achillea millefolium*.

132
133 Assessment of Insecticide Toxicity to Beneficial Arthropods

134 Calendars of the insecticide treatments in 2014 and 2015 were collected. The Environmental Impact Quotient (EIQ) was used to estimate the toxicity of each insecticide (https://nysipm.cornell.edu/eiq) to beneficial arthropods. EIQ assigns to each insecticide ingredient a score ranging from 5 to 125 according to its toxicity to beneficial arthropods (Kovach et al. 1992). We calculated the cumulative impact of the insecticides applied during the period of RAA presence in the apple trees (from March to July) in each orchard using the following formula:

140 EIQ<sub>field use rating</sub> = Σ(EIQ<sub>i</sub> * RT<sub>i</sub> * %active ingredient<sub>i</sub>),

141 where EIQ<sub>i</sub> is the EIQ value assigned to the active ingredient contained in the insecticide <i>i</i> relative to beneficial arthropods, RT<sub>i</sub>, the rate of insecticide <i>i</i> use and %active ingredient<sub>i</sub>, the percentage of active ingredient in the insecticide <i>i</i>. The EIQ<sub>field use rating</sub> ranged from 0 to 6.61, depending on the year, the orchard and the cultivar (Table 1). The main active ingredients used against RAA in the cider orchard were flonicamid, acetamiprid and lambda cyhalothrin.

146
147 Monitoring of Arthropod Population Dynamics
148 The monitored trees were visually inspected to record the RAA abundance and the abundance of natural
149 enemies and ants within the RAA colonies. The mean height of the monitored trees was 3.4 m (SD 0.49
150 m). All terminal shoots of each monitored tree were inspected from the lowest branch up to a height of
151 1.7 m for practical reasons. In 2014 and 2015, the trees were monitored every week from mid-April to
152 the end of June and every two weeks from mid-March to mid-April and during July (except in the two
153 orchards (4a and 4b) located at location 4, where the RAA populations were recorded every two weeks
154 from April to July).

155

156

*Dysaphis plantaginea*

157 At each observation date, the total number of RAA individuals was counted on each monitored tree.

158

159

*Natural Enemies and Ants Observed in RAA Colonies*

160 At each observation date, the number and identity of each natural enemy type and the number of ants
161 found within the RAA colonies were recorded and summed for each monitored tree. We also recorded
162 the developmental stage of all of the observed natural enemies, as not all stages are involved in aphid
163 control. In most cases, natural enemy identification was at the family level. Ants were not identified to
164 the species level. However, we observed only *Lasius niger* and *Formica* sp.

165

166

**Data Analysis**

167

*Dysaphis plantaginea*

168 Three variables were considered to characterize the RAA population dynamics on each monitored tree
169 and for each studied year to assess the different ecological processes:

170 (i) The presence/absence variable (PA), indicating the RAA colonization process, was set to 0 when no
171 RAA was observed at any date or to 1 when at least one RAA was observed on the monitored tree

172 (ii) The logarithm of the area under the curve (logAUC) of the tree population abundance, indicating *in situ* RAA population dynamics (survival and reproduction)

174 (iii) The presence duration (PD), in days (last date at which at least 1 aphid was observed minus the
175 first date at which at least 1 aphid was observed), indicating the RAA emigration process

176

177

*Natural Enemies and Ants*
Natural enemy dynamics and ants were only assessed on the monitored trees in which at least one RAA was observed (i.e., a monitored tree where the RAA presence/absence was set to 1). The natural enemy dynamics were characterized using the same variables as for RAA (*PA*, *logAUC* and *PD*) for each considered developmental stage (egg, larva, adult) of each taxon. A global variable (*allNE*) was also created by summing the counts of all observed natural enemies for any stage and taxon. The three dynamics variables were also calculated for *allNE*. The ant dynamics were characterized in the same way as those of RAA and their natural enemies (*PA*, *logAUC* and *PD*).

185

## Statistical Analyses

The main purpose of our study was to assess the influence of agroecological infrastructures on the three above variables characterizing RAA population dynamics. First, Generalized Linear Mixed Models (GLMM) were used to assess the influence of each considered factor (distance to the closest hedgerow, distance to the closest flower strip, *EIQ<sub>field rating use</sub>* and cultivar) on each RAA population dynamics variable (*PA*, *logAUC* and *PD*) as well as its significance. Second, to assess in what extent factor effects could result from variations in natural enemy and ant population dynamics, the same GLMMs were fitted to the population dynamics variables associated to each natural enemy taxon and to ants but including as well the rosy apple aphid abundance (*logAUC*) as a supplementary explanatory variable. This allowed assessing how the dynamics of natural enemies and ants are impacted by agroecological infrastructures and other agricultural variables for a given level of rosy apple aphid abundance. Introducing the *logAUC* of RAA as a fixed factor was equivalent to analysing the influence of the factors under study on the abundance ratio between the natural enemies and aphids or between the ants and aphids. In all models two random factors were added, the orchard location and the studied year. All statistical analyses were carried out with the R 3.1.3 software (R core Team 2015) using the tree as the observation unit.

*PA* were fitted assuming a binomial distribution, *logAUC* were fitted assuming a normal distribution and *PD* were fitted using a Gamma distribution, regardless of the arthropod taxon. The mixed linear models were fitted using the lme4 package, version 1.1-7 (Bates et al. 2015). A significance threshold of p=0.05 was considered.

205

206

207

## Results
208 **Aphid Abundance and its Variation in Space and Time**

209 The mean abundance of RAA observed per tree and per sampling date varied widely, depending on the
210 studied year and studied orchard. For instance, in 2014, the mean number of RAA per tree and per
211 sampling date ranged from 0.8 in orchard 3b to 95.5 in orchard 7a (Table 2 and Appendix B). Globally,
212 the pest abundance was higher in 2015 than in 2014 in all orchards, except in orchards 4a and 4b
213 (Appendix B).

214

215 **Community of Natural Enemies and its Variation in Space and Time**

216 The composition of the natural enemy community remained fairly stable from one year to the next (Table
217 2). The natural enemy community was dominated by Syrphidae (45% and 32% of the natural enemies
218 observed in 2014 and 2015, respectively) and Coccinellidae (22% and 36% of the natural enemies
219 observed in 2014 and 2015, respectively), followed by Forficulidae (18% and 15% of the natural enemies
220 observed in 2014 and 2015, respectively) and Araneae (9% of the natural enemies observed in both
221 years). Few Chrysopidae, Hemiptera and Cantharidae were observed in both years and were not
222 retained for the subsequent detailed statistical analyses (Table 2). Similarly few mummies were
223 observed and the ratio of the mummy number to the RAA number never exceeded 0.2% whatever the
224 considered year and orchard.

225 A large variation in the abundance of RAA, natural enemies and ants was observed among the orchards
226 (Appendix B).

227 The natural enemy community composition varied strongly during the season. The community was
228 dominated by Syrphidae early in the season and then by Coccinellidae and other natural enemies (Fig.
229 2). In both years, the RAA populations peaked between mid-May and the end of May.

230

231 **Influence of Agricultural Practices and Agroecological Infrastructures on the Main**
232 **Observed Arthropod Taxa**

233

234 Table 3 provides a synthetic overview of the results of the GLMMs. Aphids and ants appeared to be
235 more abundant in the vicinity of the hedgerows. On the contrary, hedgerows had in most cases no effect
236 on the natural enemies. They only have a positive effect on the presence duration of Syrphidae larvae
237 and of Syrphidae eggs and a negative effect on the presence duration of Coccinellidae larvae. On the
238 contrary, aphids and ants were less abundant in the vicinity of the flower strips, while all of the natural
239 enemies except the Araneae were positively impacted. All arthropods were generally more abundant on
240 the Douce de l'Aventcov cultivar, followed by Judor, and were generally negatively impacted by the
241 insecticide use (EIQfield use rating). However, the insecticide effect on the Syrphidae and Coccinellidae was
242 ambiguous. Indeed, the Syrphidae eggs (logAUC and PD) and Coccinellidae larvae (PD) were positively
243 impacted by the EIQfield use rating but the Syrphidae larvae (PA) and the Coccinellidae eggs were negatively
244 impacted by the EIQfield use rating (PA) (Appendix A). Finally, all natural enemy and ant abundances were
245 positively impacted by aphid abundance. The results were generally consistent regardless of the
246 variables used to describe the arthropod dynamics (PA, logAUC and PD) or the considered natural
247 enemy stage (egg, larva, adult). Detailed results by stage and variables are provided in Appendix A.

248
249

Discussion

250 Main Findings

251 This study was carried out under field and farming production conditions. Spatio-temporal variations
252 regarding the abundance of aphids and of their natural enemies have long been reported to depend on
253 farming practices (Marliac et al. 2015) and on climatic conditions (Hemptinne et al. 1994, Roy et al.
254 2002). Variations among locations and between years in population dynamics of RAA and their natural
255 enemies are not surprising and were modelled as random factors to focus on the effects of farmer
256 practices (insecticide treatment and cultivar choice) and of agroecological infrastructures (distances to
257 the closest hedgerow and to the closest flower strip). All of these factors had an impact on population
258 dynamics of aphids, of natural enemies and of ants. The tested factors appeared to be widely consistent
259 among all natural enemy groups, suggesting that agricultural practices and agroecological
260 infrastructures either favoured or disfavoured the entire community of natural enemies. While the cultivar
261 and insecticide use intensity had a mostly similar influence on all arthropod abundances, the
262 agroecological infrastructures had opposite effects on aphids and ants on the one hand and on natural
263 enemies on the other hand. This result suggests that agroecological infrastructures actually impacted
264 the level of RAA biological control by its natural enemies.

265 Analyses were carried out using three response variables characterizing arthropod population
266 dynamics: presence probability, logarithm of the area under the curve and presence duration. Our
267 hypothesis was that each variable was related to different ecological processes that could have been
268 differentially influenced by the agricultural practices and agroecological infrastructures. However, in
269 most cases in this study, the three variables were influenced in the same way by the agricultural
practices and agroecological infrastructures, suggesting that environmental and agronomical practices had a similar influence on all of the population dynamics components.

272

## 273 Structuration of the Arthropod Community

Regardless of the year and orchard, Syrphidae and Coccinellidae were consistently the two most abundant groups of natural enemies, with Syrphidae being generally present earlier than Coccinellidae.

These results are consistent with those of previous studies (Miñarro et al. 2005, Dib et al. 2010). However, the synchronization between the RAA and natural enemy dynamics varied between the studied years. The lowest RAA infestation level was observed in 2014, when RAA and natural enemy dynamics appeared to be the most synchronized. Indeed, in 2014, the increase of natural enemy abundance was concomitant to the increase of RAA population whereas in 2015, the natural enemy abundance was at its lowest level when the RAA infestation was highest (Fig. 2).

Hymenoptera parasitoids were very rare in both year and in all orchards. The ratio of the number of mummies to the aphid number was much lower (always less than 0.2% in all years and orchards) than in previous surveys conducted in organic apple orchards (Dib et al. 2010: up to 6.9%; Cruz de Boelpaepe et al. 1987: 3.3%). However, other studies similarly reported the absence or a very low abundance of parasitism in RAA colonies (Miñarro et al. 2005, Brown and Mathews 2007). The low level of parasitism observed in our study could result from the high sensitivity of the hymenoptera parasitoid to insecticides (Theiling and Croft 1988). Another explanation could be an antagonist effect between ants and parasitoids as evidenced in previous studies (Völkl 1992, Stewart-Jones et al. 2008).

As expected, all natural enemies exhibited a positive response to RAA abundance either in their probability of presence (Coccinellidae, Araneae) or in both their probability of presence and abundance (Syrphidae, Forficulidae). This is not surprising, as natural enemies frequently aggregate in places where preys are abundant. In fact, previous studies showed that it is the case for Carabidae and Staphylinidae, (Bryan and Wratten 1984) or for Syrphidae (Tenhumberg and Poehling 1995, Miñarro et al. 2005).

Similarly, the presence probability, logarithm of the area under the curve and presence duration of ants responded positively to RAA abundance, which was expected considering the mutualistic relation between *D. plantaginea* and the two species of ants observed (*Lasius niger* L., *Formica* sp.) (Flatt and Weisser 2000, Stewart-Jones et al. 2008).

299
This dependence of ant and natural enemy abundances on RAA abundance supported our choice to include RAA abundance as a factor in the models (through the *logAUC* of RAA). In this way, we were able to analyse the direct effects of farmer practices and agroecological infrastructures on natural enemies and ants.

304

## 305 Practices and Cultivar Influence

### 306 Impact of Insecticides on RAA and Natural Enemy Population Dynamics

As expected, we observed a decrease in the probability and duration of RAA presence with an increase of the *EIQ<sub>field use rating</sub>*, but the *EIQ<sub>field use rating</sub>* effect on RAA abundance (*logAUC*) was not significant (Table 3 and Appendix A). Such an effect is especially expected in leaf-curling aphids, such as *D. plantaginea*. Indeed, aphids are more vulnerable to insecticides in the first phase of colonization, resulting in a reduction of the colonization success and hence on the presence probability. The aphid vulnerability further decreases while the colony size increases because the rolling-up of leaves provides them with protection against insecticides (Cross et al. 2007). Moreover, the negative effect of insecticides on natural enemies might further reduce aphid biological control. A negative effect of insecticide treatments was observed on the presence probability of *allNE* and on their abundance (*logAUC*). This negative effect was significant on the presence probability of Syrphidae larvae, of Syrphidae eggs and of Coccinellidae eggs, as well as on the Forficulidae abundance and on Araneae presence duration. Insecticide treatments applied early in the season seem to be the most efficient to control the development of *D. plantaginea* colonies. Insecticide applications after the leaf curling, would impact more strongly the natural enemies than aphids. High *EIQ<sub>field use rating</sub>* also reduced ant abundance in RAA-infested trees, suggesting that insecticide treatments also negatively impact the ant population.

322

### 323 Effect of Cultivar on RAA and Natural Enemy Population Dynamics

A strong impact of the cultivar was observed in our study and its effect varied whether we considered the presence probability and the presence duration of RAA and natural enemies or the abundance of RAA and natural enemies (except for the Dabinett cultivar, which always exhibited the lowest presence probability, abundance and presence duration of RAA and natural enemies). Douce de l'Avent<sub>cov</sub> had the highest presence probability and presence duration of RAA and natural enemies (*AllNE*), followed by Judor. For the RAA, this ranking matches cultivars ranked according to precocity. Douce de l'Avent<sub>cov</sub>
was the most precocious cultivar, followed by Judor, with Dabinett being the latest cultivar. Miñarro and Dapena, (2007) still showed that early-leafing apple cultivars were more infested and damaged by RAA than late-leafing ones. We can suppose that the same process operates for natural enemies. However, a different cultivar ranking was obtained when the abundance of RAA and natural enemies was considered, switching between cultivars: Judor had the higher abundance of RAA and of natural enemies (AILNE), followed by Douce de l'Aventcov. This apparent inconsistency could result from an interaction between the colonization rate and treatment frequency. In fact, the most heavily colonized cultivar (Douce de l'Aventcov) was also the earliest one treated with insecticides, resulting in low abundances of both aphids and natural enemies throughout the season.

339

340

## Hedgerows Favour RAA Populations

Unexpectedly, hedgerows appeared to be consistently beneficial to RAA populations. Indeed, hedgerow proximity had a positive impact on all of the RAA population dynamics parameters. This hedgerow effect may result from either direct effects on the RAA population dynamics, from indirect effects through its influence on mutualistic or antagonist arthropods, or both. The vicinity of the hedgerow may influence the flight behaviour of arthropods by modifying the wind speed and turbulences (Pasek 1988), which could result in the accumulation of insects on the leeward side of the hedgerow (Lewis 1965, Grüebler et al. 2008). Such an effect could result in a higher colonization rate by RAA of apple trees situated in the vicinity of hedgerows.

Hedgerows may also indirectly favour aphids by favouring mutualistic ants possibly by providing a suitable nesting habitat. Indeed, the ant presence probability increased with the proximity to the hedgerow in our study. To our knowledge, very few studies have assessed hedgerow influence on ants. Stutz and Entling (2011) found no effect of a woody habitat in the surrounding landscape on ant presence on cherry trees, but Armbrecht and Perfecto (2003) reported a dramatic decrease of twig-nesting ants with an increase in the distance to forest fragments in coffee plantations in Mexico.

Finally, the proximity of hedgerows may modify the arthropods interaction network. For instance, the presence of a hedgerow could reduce RAA biocontrol by increasing the intra-guild predation between natural enemies (Straub et al. 2008) or by diverting natural enemies from pests by offering them alternative prey (Kozar et al. 1994, Koss and Snyder 2005, Symondson et al. 2006). Moreover, as the presence of ants is higher in the hedgerow vicinity, the protection they provide to RAA against their

359
natural enemies could be enhanced. Contrary to previous studies (Altieri and Schmidt 1986, Miñarro and Prida 2013), few hedgerow-distance effects on natural enemy occurrence or abundance in aphid colonies were found in our study. The only significant effects were the decrease of the presence probability and of the presence duration of Coccinellidae larvae and the increase of the presence duration of Syrphidae larvae and Syrphidae eggs in the vicinity of the hedgerow.

## Flower Strips Reduce RAA Populations and Increase Natural Enemy Abundance

Contrary to hedgerows, flower strips had a negative impact on the RAA populations in our study. Indeed, the presence probability, the abundance and the presence duration of RAA all decreased with flower strips proximity. A direct effect of flower strips on aphids was very unlikely. We then assumed that flower strips exerted an indirect effect through their influence on the natural enemies and/or on ants. Indeed, Wyss, (1995) and Wyss et al. (1995) showed that introducing flower strips in apple orchards resulted in an increase in natural enemy abundance (Chrysopidae, Coccinellidae, Araneae). Similarly, in our study, the abundance (logAUC) and presence duration of natural enemies (allNE) increased in proximity to flower strips. More specifically, the presence probability and abundance of Syrphidae (eggs and larvae), presence probability of Coccinellidae (eggs and larvae) and abundance of Forficulidae decreased significantly with the distance to flower strips. This increase of presence and/or of abundance of natural enemies could enhance aphid biological control in the vicinity of flower strips. Hogg et al. (2011) showed that floral resources enhanced aphid suppression by the hoverfly *Eupeodes fumipennis* in a California lettuce field. In addition, the negative influence of flower strips on aphid populations could also be amplified by their negative effect on the ant presence probability. Nagy et al. (2013) showed that applying artificial sugar sources in apple orchards resulted in a reduction of the number of ant-attended *D. plantaginea* colonies and in an increase in natural enemy pressure. Similarly, by providing alternative sugar resources, flower strips could distract ants from aphid attendance. Katayama et al. (2013) showed that extrafloral nectar was more attractive to ants than aphid honeydew. In total, our results suggest that flower strips are beneficial to natural enemies and reduce ant attendance that could account for the observed reduction of *D. plantaginea* infestation in cider-apple trees located in the vicinity of flower strips.

## Conclusion
This study showed an impact of the distance to agroecological infrastructures on *D. plantaginea* dynamics in cider-apple orchards. Hedgerows increased the RAA infestation level. This could result from an indirect effect due to modifications in the RAA interactions network with other arthropods. Indeed, our results showed an increase in the presence of mutualistic ants and a decrease in RAA natural enemy abundance in the vicinity of hedgerow. On the contrary, flower strips appeared unfavourable to *D. plantaginea*. Again it could result from indirect effect due to an increase in natural enemy abundance and a decrease of ant presence in the RAA colony. Additionally, we confirmed a strong influence of cultivars and of insecticide use intensity on *D. plantaginea* dynamics.

## Acknowledgments

We thank A. Taillade and A. Quero for data collection and the farmers who allowed us to access their orchards. We thank Sylvaine Simon for her help in the characterization of agroecological infrastructure.

We thank two anonymous reviewers for their useful comments on a previous version of this manuscript.

The work was supported by ANRT, UNICID, Région Bretagne, Région Normandie and the Ministère de l'Agriculture, de l'agroalimentaire et de la forêt (CASDAR). This project is linked to the PEERLESS project (ANR-12-AGRO-0006) and to the "Verger Cidricole de Demain" CASDAR project.

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TABLE

<table><caption>**Table 1: Main characteristics of the 14 studied cider-apple orchards.** Two contiguous orchards (referred by a or b) have been monitored in each location (referred by number). In each orchard, 3 cider-apple cultivars were planted (DDA = Douce de l'Aventcov cultivar, DAB = Dabinett cultivar and JUD= Judor cultivar). The Environmental Impact Quotient (EIQ) of each insecticide applied during the RAA presence on the apple trees was used to assess the cumulative toxicity of insecticides used in each orchard each year (EIQ<sub>field use rating</sub>). *: only 63 trees monitored in 2014; **:only 425 trees monitored in 2014. NA means Not Applicable.</caption><thead><tr><th>Location</th><th>1</th><th>2</th><th>3</th><th>4</th><th>5</th><th>6</th><th>7</th></tr><tr><th>Orchard</th><th>1a</th><th>1b</th><th>2a</th><th>2b</th><th>3a</th><th>3b</th><th>4a</th><th>4b</th><th>5a</th><th>5b</th><th>6a</th><th>6b</th><th>7a</th><th>7b</th></tr><tr><th>Year of planting</th><th>2010</th><th>2010</th><th>2012</th><th>2012</th><th>2011</th><th>2011</th><th>2012</th><th>2012</th><th>2011</th><th>2011</th><th>2011</th><th>2011</th><th>2010</th><th>2010</th></tr></thead><tbody><tr><td>Density of planting by number of trees/ha (planting distance between rows*planting distance within rows)</td><td>774 (5.5*2.3)</td><td>774 (5.5*2.3)</td><td>495 (6.5*3)</td><td>774 (5.5*2.3)</td><td>774 (5.5*2.3)</td><td>774 (6.5*3)</td><td>495 (5.5*2.3)</td><td>774 (5.3*2)</td><td>1000 (5.3*2)</td><td>1000 (5.3*2)</td><td>774 (5.5*2.3)</td><td>774 (5.5*2.3)</td><td>774 (5.5*2.3)</td><td>774 (5.5*2.3)</td></tr><tr><td>Number of monitored trees</td><td>198</td><td>198</td><td>153</td><td>153</td><td>162</td><td>162</td><td>117*</td><td>117*</td><td>234</td><td>234</td><td>279</td><td>279</td><td>270**</td><td>270**</td></tr><tr><td>EIQ<sub>field use rating</sub> 2014</td><td>DDA</td><td>0.61</td><td>5.58</td><td>0</td><td>1.20</td><td>0.35</td><td>0.35</td><td>0</td><td>0</td><td>NA</td><td>NA</td><td>NA</td><td>NA</td><td>0</td><td>0.29</td></tr><tr><td>in (for each apple cultivar)</td><td>DAB</td><td>0.61</td><td>5.58</td><td>0</td><td>1.20</td><td>0.35</td><td>0.35</td><td>0</td><td>0</td><td>NA</td><td>NA</td><td>NA</td><td>NA</td><td>0</td><td>2.09</td></tr><tr><td>EIQ<sub>field use rating</sub> 2015</td><td>DDA</td><td>0.67</td><td>6.61</td><td>0</td><td>0</td><td>0</td><td>2.80</td><td>0</td><td>1.16</td><td>0.087</td><td>0.33</td><td>0</td><td>6.81</td><td>0</td><td>0.24</td></tr><tr><td>in (for each apple cultivar)</td><td>DAB</td><td>0.67</td><td>6.61</td><td>0</td><td>0</td><td>0</td><td>1.60</td><td>0</td><td>1.16</td><td>0.087</td><td>0.33</td><td>0</td><td>4.67</td><td>0</td><td>0.35</td></tr><tr><td></td><td>JUD</td><td>0.67</td><td>6.61</td><td>0</td><td>0</td><td>0</td><td>2.80</td><td>0</td><td>1.16</td><td>0.087</td><td>0.33</td><td>0</td><td>6.61</td><td>0</td><td>0.35</td></tr></tbody></table>
<table><tbody><tr><td rowspan="2">Mean distance<br>(+SD) of orchard<br>trees to the closest<br>flower strip (in m)<br>(according to the<br>year)</td><td>2014</td><td>0 (0)</td><td>34.5<br>(14.2)</td><td>0<br>(0)</td><td>38.9<br>(11.3)</td><td>1<br>(0)</td><td>43.6<br>(12.0)</td><td>2<br>(0)</td><td>24.9<br>(4.6)</td><td>NA</td><td>NA</td><td>NA</td><td>NA</td><td>1.5<br>(0)</td><td>39.8<br>(13.2)</td></tr><tr><td>2015</td><td>0 (0)</td><td>34.5<br>(14.2)</td><td>0<br>(0)</td><td>38.9<br>(11.3)</td><td>1<br>(0)</td><td>43.6<br>(12.0)</td><td>2<br>(0)</td><td>31.8<br>(8.6)</td><td>10.8<br>(6.2)</td><td>27.0<br>(12.9)</td><td>11.9<br>(6.9)</td><td>36.9<br>(14.8)</td><td>1.5<br>(0)</td><td>33.4<br>(11.9)</td></tr><tr><td rowspan="2">Mean distance<br>(+SD) of orchard<br>trees to the closest<br>hedgerow (in m)<br>(according to the<br>year)</td><td>2014</td><td>16.0<br>(7.2)</td><td>21.3<br>(11.8)</td><td>23.9<br>(12.9)</td><td>20.7<br>(10.4)</td><td>21.3<br>(11.0)</td><td>21.3<br>(11.0)</td><td>15.5<br>(6.0)</td><td>13.8<br>(4.64)</td><td>NA</td><td>NA</td><td>NA</td><td>NA</td><td>21.5<br>(11.3)</td><td>28.1<br>(12.9)</td></tr><tr><td>2015</td><td>16.9<br>(7.2)</td><td>21.3<br>(11.8)</td><td>23.9<br>(12.9)</td><td>20.7<br>(10.4)</td><td>21.3<br>(11.0)</td><td>21.3<br>(11.0)</td><td>20.8<br>(10.4)</td><td>18.3<br>(8.2)</td><td>14.3<br>(6.6)</td><td>15.2<br>(6.5)</td><td>27.6<br>(14.1)</td><td>27.6<br>(14.1)</td><td>23.7<br>(12.7)</td><td>23.7<br>(12.7)</td></tr></tbody></table>
<table><caption>Table 2: Total number of observed arthropods (and range of the mean number for one monitored tree per observation in one studied orchard) by taxonomic group, life stage and year.</caption><thead><tr><th rowspan="2"></th><th rowspan="2">Order</th><th rowspan="2">Family</th><th rowspan="2">Life stage</th><th colspan="2">Year</th><th rowspan="2">Total</th></tr><tr><th>2014</th><th>2015</th></tr></thead><tbody><tr><td></td><td></td><td></td><td></td><td>10</td><td>14</td><td></td></tr><tr><td></td><td></td><td></td><td></td><td>35</td><td>57</td><td></td></tr><tr><td></td><td></td><td></td><td></td><td>(from 5 to 10)</td><td>(from 5 to 11)</td><td>103</td></tr><tr><td rowspan="10">Diptera</td><td rowspan="10">Syrphidae</td><td>Eggs</td><td>1083<br>(from 5.6^-2 to 0.50)</td><td>1122<br>(from 2.9^-2 to 1.7)</td><td>2205</td></tr><tr><td>Larvae</td><td>408<br>(from 1.0^-2 to 0.47)</td><td>429<br>(from 3.0^-2 to 0.51)</td><td>838</td></tr><tr><td>Adults</td><td>9<br>(from 0 to 1.0^-2)</td><td>51<br>(from 0 to 5.3^-2)</td><td>60</td></tr><tr><td>All</td><td>1500<br>(from 6.6^-2 to 0.71)</td><td>1602<br>(from 6.0^-2 to 2.3)</td><td>3103</td></tr><tr><td>Eggs</td><td>533<br>(from 0 to 4.7^-1)</td><td>1325<br>(from 0 to 5.2)</td><td>1858</td></tr><tr><td>Larvae</td><td>141<br>(from 0 to 2.7^-1)</td><td>343<br>(from 0 to 3.8^-1)</td><td>484</td></tr><tr><td>Adults</td><td>65<br>(from 6.3^-3 to 8.8^-2)</td><td>161<br>(from 0 to 3.8^-1)</td><td>226</td></tr><tr><td>All</td><td>739<br>(6.3^-3 to 0.79)</td><td>1829<br>(from 0 to 6.4)</td><td>2568</td></tr><tr><td>Coccinellidae</td><td>Cantharidae</td><td>Adults</td><td>17<br>(from 0 to 1.2^-2)</td><td>68<br>(from 0 to 4.1^-2)</td><td>85</td></tr><tr><td rowspan="3">Coleoptera</td><td rowspan="3">Anthocoridae</td><td>-</td><td>34<br>(from 0 to 4.5^-2)</td><td>92<br>(from 0 to 5.0^-2)</td><td>126</td></tr><tr><td>Miridae</td><td>-</td><td>37<br>(from 0 to 1.2^-2)</td><td>114<br>(from 0 to 1.7^-1)</td><td>153</td></tr><tr><td>Nabidae</td><td>-</td><td>67<br>(from 0 to 2.4^-1)</td><td>0<br>(from 0 to 0)</td><td>67</td></tr></tbody></table>
<table><thead><tr><th rowspan="2"></th><th rowspan="2"></th><th rowspan="2"></th><th colspan="2">Year</th><th rowspan="2">Total</th></tr><tr><th>2014</th><th>2015</th></tr></thead><tbody><tr><td></td><td>Number of studied orchards</td><td></td><td>10</td><td>14</td><td></td></tr><tr><td></td><td>Total number of observations (date*orchard)</td><td></td><td>35<br>(from 5 to 10)</td><td>57<br>(from 5 to 11)</td><td>103</td></tr><tr><td rowspan="5">Neuroptera</td><td rowspan="5">Chrysopidae</td><td>Eggs</td><td>9<br>(from 0 to 1.2^-2)</td><td>0<br>(from 0 to 0)</td><td>9</td></tr><tr><td>Larvae</td><td>0<br>(from 0 to 0)</td><td>2<br>(from 0 to 6.0^-3)</td><td>2</td></tr><tr><td>Adults</td><td>0<br>(from 0 to 0)</td><td>3<br>(from 0 to 2.3^-3)</td><td>3</td></tr><tr><td>All</td><td>9<br>(from 0 to 1.2^-2)</td><td>5<br>(from 0 to 6.0^-3)</td><td>14</td></tr><tr><td>Dermaptera</td><td>Forficulidae</td><td>Juveniles+adults</td><td>582<br>(from 0 to 0.36)</td><td>742<br>(from 2.9^-3 to 0.60)</td><td>1324</td></tr><tr><td rowspan="4">Hymenoptera</td><td rowspan="4"></td><td>Mummies</td><td>33<br>(from 0 to 3.2^-2)</td><td>108<br>(from 0 to 5.4^-2)</td><td>141</td></tr><tr><td>Adults</td><td>12<br>(from 0 to 3.2^-2)</td><td>25<br>(from 0 to 1.9^-2)</td><td>37</td></tr><tr><td>All</td><td>45<br>(from 0 to 6.5^-2)</td><td>133<br>(from 0 to 5.7^-2)</td><td>178</td></tr><tr><td>Araneae</td><td>Juveniles+Adults</td><td>296<br>(from 0 to 0.16)</td><td>440<br>(from 0 to 0.16)</td><td>737</td></tr><tr><td></td><td>AlINE</td><td></td><td>3326<br>(from 0.10 to 1.45)</td><td>5025<br>(from 0.30 to 7.4)</td><td>8355</td></tr><tr><td></td><td>Number of RAA</td><td></td><td>206195<br>(from 0.77 to 95.5)</td><td>554230<br>(from 21.0 to 182.4)</td><td>760425</td></tr><tr><td></td><td>Ratio (natural<br>enemies per RAA)</td><td></td><td>0.016<br>(from 5.0^-4 to 0.18)</td><td>0.009<br>(from 2.4^-3 to 0.21)</td><td>0.0109</td></tr><tr><td></td><td>Ants</td><td></td><td>9279<br>(from 2.4^-2 to 3.8)</td><td>15578<br>(from 4.7^-2 to 7.1)</td><td>24857</td></tr></tbody></table>
<table><caption>**Table 3: Synthetic overview of the Generalized Linear Mixed models results:** "+" (resp. "-" ) indicates that the factor is favourable (resp. unfavourable) to the considered arthropods. For the distance, a "+" (resp. "-" ) indicates that the arthropods are more (resp. less) present in the vicinity of the agroecological infrastructure. For the cultivar factor "*" means that cultivar has a significant effect on the response variable (PA, logAUC or PD) for at least one arthropod stage. 0 indicates that the factor did not significantly influence the variable. NA: not applicable. See Appendix A for detail.</caption><thead><tr><th></th><th>RAA</th><th>ALINE</th><th>Syrphidae</th><th>Coccinellidae</th><th>Forficulidae</th><th>Araneae</th><th>Ants</th></tr></thead><tbody><tr><td>Distance to the<br>closest<br>hedgerow</td><td>+</td><td>0</td><td>+</td><td>-</td><td>0</td><td>0</td><td>+</td></tr><tr><td>Distance to the<br>closest flower<br>strip</td><td>-</td><td>+</td><td>+</td><td>+</td><td>+</td><td>0</td><td>-</td></tr><tr><td>Cultivar<br>(PA/logAUC/PD)</td><td>*/**/*</td><td>*/**/*</td><td>*0/**</td><td>*/*/*</td><td>*0/0</td><td>*0/0</td><td>*0/0</td></tr><tr><td>EIQ<sub>field use rating</sub></td><td>-</td><td>-</td><td>-</td><td>-</td><td>-</td><td>-</td><td>-</td></tr><tr><td>RAA</td><td>NA</td><td>+</td><td>+</td><td>+</td><td>+</td><td>+</td><td>+</td></tr></tbody></table>
FIGURE LEGENDS

**Fig. 1.** Map of the seven studied locations (two orchards per location). Black dots are the locations studied both in 2014 and 2015. Grey dots are the locations studied in 2015.

**Fig. 2.** Mean number (+ SE) of RAA (black dot), of all natural enemies (grey dotted line with circle mark), of Syrphidae (all stages) (grey dotted line with triangle mark) and of Coccinellidae (all stages) (grey dotted line with square mark) per monitored apple tree in aphid colonies in 2014 (A) and 2015 (B).
<figure><img src="image_2.png" /><figcaption>Fig. 1</figcaption></figure>
<figure><img src="image_3.png" /><figcaption>Fig. 2</figcaption></figure>
Supplementary Material

Impact of Agroecological Infrastructures on the Dynamics of
*Dysaphis plantaginea* Passerini (Hemiptera: Aphididae) and
its Natural Enemies in Apple Orchards in Northwestern
France

Laurence ALBERTª, Pierre FRANCKc, Yann GILLESª, Manuel PLANTEGENESTb

Contents

Appendix A: Results of Generalized Linear Models obtained for each arthropod (by taxon and stage) and each variable.

Appendix B: Sum of arthropods observed per orchard each studied year (2014 and 2015) and mean number of arthropods per sampling date per tree infected with rosy apple aphid

<footnote>ª Institut Français des Productions Cidricoles, La Rangée Chesnel, 61500 Sées, FRANCE,
[albert5@yahoo.fr](mailto:albert5@yahoo.fr); [yann.gilles@ifpc.eu](mailto:yann.gilles@ifpc.eu)</footnote>

<footnote><u>UMR1349 IGEPP, INRA/Agrocampus-Ouest/Université Rennes 1, 65 rue de Saint Brieuc, 35042 Rennes Cedex, FRANCE, manuel.plantegenest@agrocampus-ouest.fr</u></footnote>

<footnote><u>INRA</u> Plantes & Systèmes de culture Horticoles, F-84914 AVIGNON Cedex 9, FRANCE,
pierre.franck@avignon.inra.fr</footnote>
<table><caption>Appendix A: Results of Generalized Linear Models obtained for each arthropod (by taxon and stage) and each variable. The first line is the pvalue of the variable, when inferior to 0.05, the second line is the coefficient. NS means no-significant. EIQ means Environmental Impact Quotient. AUC mean Area Under the Curve. DAB means cultivar of Dabinett, DDA means cultivar of Douce de l'Aventcov and JUD means cultivar of Judor.</caption><thead><tr><th rowspan="2"></th><th rowspan="2"></th><th colspan="5">Variables studied</th></tr><tr><th>Log AUC of D. plantaginea</th><th>Distance to the hedgerow</th><th>Distance to the flower strips</th><th>Cultivar</th><th>EIQ<sub>field use rating</sub></th></tr></thead><tbody><tr><td rowspan="3">Dysaphis plantaginea</td><td>Probability of presence (binomial distribution)</td><td>**0.002537<br/>-0.0058</td><td>*** &lt; 2.2e-16<br/>0.0111</td><td>5.348e-12<br/>DAB&lt;JUD&lt;DDA</td><td>*** 7.166e-05<br/>-0.057</td></tr><tr><td>Log(Area Under the Curve) (normal distribution)</td><td>*** 0.0001546<br/>-0.0171</td><td>*0.03814<br/>0.0063</td><td>** 0.003741<br/>DAB&lt;DDA&lt;JUD</td><td>NS 0.7999</td></tr><tr><td>Presence duration (Gamma distribution)</td><td>*** &lt;2.2e-16<br/>-0.0057</td><td>*** 7.867e-16<br/>0.0022</td><td>*** &lt; 2.2e-16<br/>DAB&lt;JUD&lt;DDA</td><td>*** 8.676e-13<br/>-0.019</td></tr><tr><td rowspan="3">Global natural enemies</td><td>Probability of presence (binomial distribution)</td><td>*** &lt; 2.2e-16<br/>0.277</td><td>NS 0.3227</td><td>NS 0.1266</td><td>***1.279e-10<br/>DAB&lt;JUD&lt;DDA</td><td>*** 4.617e-05<br/>-0.091</td></tr><tr><td>Log(Area Under the Curve) (normal distribution)</td><td>*** &lt; 2.2e-16<br/>0.194</td><td>NS 0.4274</td><td>***3.266e-06<br/>-0.0082</td><td>***0.0004949<br/>DAB&lt;DDA&lt;JUD</td><td>0.005526<br/>-0.051</td></tr><tr><td>Presence duration (Gamma distribution)</td><td>*** 2.894e-11<br/>0.0535</td><td>NS 0.1892</td><td>**0.001459<br/>-0.0029</td><td>** 0.003236<br/>DAB&lt;JUD&lt;DDA</td><td>NS 0.2187</td></tr><tr><td rowspan="3">Eggs of Syrphidae</td><td>Probability of presence (binomial distribution)</td><td>*** &lt; 2.2e-16<br/>0.185</td><td>NS 0.7486</td><td>* 0.0366<br/>-0.0048</td><td>*** 2.754e-05<br/>DAB&lt;JUD&lt;DDA</td><td>0.01154<br/>-0.0586</td></tr><tr><td>Log(Area Under the Curve) (normal distribution)</td><td>*** 7.458e-08<br/>0.122</td><td>NS 0.8587</td><td>** 0.001588<br/>-0.00787</td><td>NS 0.1269</td><td>NS 0.1041</td></tr><tr><td>Presence duration (Gamma distribution)</td><td>*** 4.961e-06<br/>0.0422</td><td>*0.04781<br/>-0.0034</td><td>*** 6.688e-05<br/>-0.0044</td><td>NS 0.6885</td><td>*0.03559<br/>0.0225</td></tr><tr><td rowspan="3">Larvae of Syrphidae</td><td>Probability of presence (binomial distribution)</td><td>*** &lt; 2.2e-16<br/>0.286</td><td>NS 0.8352</td><td>** 0.002112<br/>-0.0078</td><td>*** 9.99e-06<br/>DAB&lt;JUD&lt;DDA</td><td>*** 0.0008589<br/>-0.090</td></tr><tr><td>Log(Area Under the Curve) (normal distribution)</td><td>*** 1.125e-07<br/>0.117</td><td>NS 0.8032</td><td>* 0.03901<br/>-0.00452</td><td>NS 0.08464</td><td>NS 0.4199</td></tr><tr><td>Presence duration (Gamma distribution)</td><td>*** 0.0009433<br/>0.0376</td><td>** 0.00516<br/>-0.00536</td><td>NS 0.4155<br/>-0.00091</td><td>* 0.02581<br/>DAB&lt;DDA&lt;JUD</td><td>NS 0.6054</td></tr><tr><td rowspan="3">Eggs of Coccinellidae</td><td>Probability of presence (binomial distribution)</td><td>*** 8.057e-07<br/>0.219</td><td>NS 0.1241</td><td>0.02953<br/>-0.010</td><td>NS 0.2564</td><td>** 0.006066<br/>-0.364</td></tr><tr><td>Log(Area Under the Curve) (normal distribution)</td><td>NS 0.6864</td><td>NS 0.3697</td><td>NS 0.1016</td><td>** 0.002943<br/>JUD&lt;DAB&lt;DDA</td><td>NS 0.8945</td></tr><tr><td>Presence duration (Gamma distribution)</td><td>NS 0.06483</td><td>NS 0.4644</td><td>NS 0.3969</td><td>*0.04445<br/>JUD&lt;DAB&lt;DDA</td><td>NS 0.3095</td></tr><tr><td rowspan="2">Larvae of Coccinellidae</td><td>Probability of presence (binomial distribution)</td><td>*** &lt; 2.2e-16<br/>0.285</td><td>** 0.005793<br/>0.0162</td><td>*** 0.000528<br/>-0.011</td><td>**0.00986<br/>DAB&lt;DDA&lt;JUD</td><td>NS 0.4914</td></tr><tr><td>Log(Area Under the Curve)</td><td>* 0.02581<br/>0.122</td><td>NS 0.75</td><td>NS 0.4144</td><td>NS 0.728</td><td>NS 0.294</td></tr></tbody></table>
<table><thead><tr><th></th><th></th><th></th><th></th><th></th><th></th></tr></thead><tbody><tr><td></td><td>(normal distribution)</td><td></td><td></td><td></td><td></td></tr><tr><td></td><td>Presence duration<br>(Gamma distribution)</td><td>NS 0.1201</td><td>* 0.03643<br>0.0057</td><td>NS 0.7773</td><td>* 0.01121<br>JUD&lt;DAB&lt;DDA</td></tr><tr><td></td><td>Probability of<br>presence<br>(binomial distribution)</td><td>*** 7.437e-15<br>0.246</td><td>NS 0.6654</td><td>NS 0.4651</td><td>* 0.01922<br>JUD&lt;DAB&lt;DDA</td></tr><tr><td rowspan="2">Adults of<br>Coccinellidae</td><td>Log(Area Under the<br>Curve)<br>(normal distribution)</td><td>NS 0.491</td><td>NS 0.1347</td><td>NS 0.895</td><td>NS 0.1843</td></tr><tr><td>Presence duration<br>(Gamma distribution)</td><td>NS 0.8494</td><td>NS 0.5724</td><td>NS 0.6548</td><td>*0.01378<br>JUD&lt;DAB&lt;DDA</td></tr><tr><td></td><td>Probability of<br>presence<br>(binomial distribution)</td><td>*** &lt; 2.2e-16<br>0.223</td><td>NS 0.9295</td><td>NS 0.8388</td><td>*0.01662<br>DAB&lt;DDA&lt;JUD</td></tr><tr><td rowspan="2">Forficulidae<br>(Juveniles and<br>adults)</td><td>Log(Area Under the<br>Curve)<br>(normal distribution)</td><td>** 0.001888<br>0.0892</td><td>NS 0.1346</td><td>0.04627<br>-0.005</td><td>NS 0.05784</td></tr><tr><td>Presence duration<br>(Gamma distribution)</td><td>*0.03107<br>0.0304</td><td>NS 0.2126</td><td>** 0.005847<br>-0.00534</td><td>NS 0.5498</td></tr><tr><td></td><td>Probability of<br>presence<br>(binomial distribution)</td><td>*** 4.533e-12<br>0.146</td><td>NS 0.9254</td><td>NS 0.1275</td><td>*** 1.155e-10<br>DAB&lt;JUD&lt;DDA</td></tr><tr><td rowspan="2">Araneae<br>(Juveniles and<br>adults)</td><td>Log(Area Under the<br>Curve)<br>(normal distribution)</td><td>NS 0.3479</td><td>NS 0.9367</td><td>NS 0.3193</td><td>NS 0.74</td></tr><tr><td>Presence duration<br>(Gamma distribution)</td><td>NS 0.1252</td><td>NS 0.5216</td><td>NS 0.4528</td><td>NS 0.1029</td></tr><tr><td rowspan="3">Ants</td><td>Probability of<br>presence<br>(binomial distribution)</td><td>*** &lt; 2.2e-16<br>0.405</td><td>*** 0.000344<br>-0.0146</td><td>0.008168<br>0.0068</td><td>* 0.01761<br>JUD&lt;DAB&lt;DDA</td></tr><tr><td>Log(Area Under the<br>Curve)<br>(normal distribution)</td><td>*** &lt; 2.2e-16<br>0.509</td><td>NS 0.5379</td><td>NS 0.8873</td><td>NS 0.4117</td></tr><tr><td>Presence duration<br>(Gamma distribution)</td><td>*** &lt; 2.2e-16<br>0.152</td><td>NS 0.1676</td><td>NS 0.8688</td><td>NS 0.6604</td></tr></tbody></table>
<table><caption>Appendix B: Sum of arthropods observed per orchard each studied year (2014 and 2015) and mean number of arthropods per sampling date per tree infected with rosy apple aphid</caption><thead><tr><th rowspan="3">Orchard</th><th rowspan="3">Sampling year</th><th rowspan="3">Sum of monitored tree per year</th><th colspan="4">Diptera</th><th colspan="4">Coleoptera</th><th colspan="2">Dermaptera</th><th colspan="2">Hymenoptera</th><th colspan="2">Araneae</th><th colspan="2">All NE</th><th colspan="2">Ants</th><th rowspan="3">Number of tree with RAA</th><th rowspan="3">Number of RAA per tree infected by RAA</th><th rowspan="3">Ratio NE/RAA</th></tr><tr><th colspan="4">Syrphidae</th><th colspan="4">Coccinellidae</th><th colspan="2">Forficulidae</th><th rowspan="2">Mummies</th><th rowspan="2">adults</th><th rowspan="2">Juvenile +Adults</th><th rowspan="2">-</th><th rowspan="2">-</th><th rowspan="2">-</th><th rowspan="2">-</th></tr><tr><th>Eggs</th><th>Larvae</th><th>Adults</th><th>Total</th><th>Eggs</th><th>Larvae</th><th>Adults</th><th>Total</th><th>Nymph +adults</th></tr></thead><tbody><tr><td rowspan="2">1a</td><td>2014</td><td>1980</td><td>246<br>0.26</td><td>102<br>0.10</td><td>0<br>0</td><td>348<br>0.37</td><td>41<br>0.04</td><td>5<br>5.3^-3</td><td>7<br>7.5^-3</td><td>53<br>0.05</td><td>337<br>0.36</td><td>3<br>3.2^-3</td><td>0<br>0</td><td>105<br>0.11</td><td>850<br>0.91</td><td>3580<br>3.85</td><td>929<br>46,91%</td><td>62291<br>67.05%</td><td rowspan="2">0.01</td></tr><tr><td>2015</td><td>2574</td><td>294<br>0.43</td><td>63<br>0.09</td><td>3<br>4.4^-3</td><td>360<br>0.53</td><td>13<br>0.01</td><td>1<br>1.4^-3</td><td>4<br>5.8^-3</td><td>18<br>0.02</td><td>411<br>0.60</td><td>0<br>0</td><td>0<br>0</td><td>29<br>0.04</td><td>836<br>1.23</td><td>3915<br>5.77</td><td>678<br>26,34%</td><td>123724<br>182.48%</td><td>6.7^-3</td></tr><tr><td rowspan="2">1b</td><td>2014</td><td>1980</td><td>234<br>0.29</td><td>11<br>0.01</td><td>0<br>0</td><td>245<br>0.31</td><td>0<br>0</td><td>0<br>0</td><td>5<br>6.3^-3</td><td>5<br>6.3^-3</td><td>156<br>0.19</td><td>0<br>0</td><td>0<br>0</td><td>19<br>0.02</td><td>425<br>0.54</td><td>2461<br>3.14</td><td>783<br>39,54%</td><td>29953<br>38.25%</td><td rowspan="2">0.01</td></tr><tr><td>2015</td><td>2574</td><td>43<br>0.04</td><td>21<br>0.03</td><td>1<br>1.4^-3</td><td>65<br>0.09</td><td>0<br>0</td><td>2<br>2.1^-3</td><td>8<br>8.4^-3</td><td>10<br>0.01</td><td>211<br>0.22</td><td>0<br>0</td><td>2<br>2.1^-3</td><td>39<br>0.04</td><td>382<br>0.40</td><td>6712<br>7.11</td><td>943<br>36,63%</td><td>158824<br>168.4%</td><td>2.4^-3</td></tr><tr><td rowspan="2">2a</td><td>2014</td><td>1377</td><td>282<br>0.50</td><td>119<br>0.21</td><td>0<br>0</td><td>401<br>0.71</td><td>260<br>0.46</td><td>43<br>0.07</td><td>9<br>0.01</td><td>312<br>0.55</td><td>18<br>0.03</td><td>1<br>1.7^-3</td><td>0<br>0</td><td>46<br>0.08</td><td>821<br>1.45</td><td>342<br>0.60</td><td>564<br>40,95%</td><td>16194<br>28.71%</td><td rowspan="2">0.05</td></tr><tr><td>2015</td><td>1683</td><td>23<br>0.09</td><td>36<br>0.14</td><td>0<br>0</td><td>59<br>0.23</td><td>53<br>0.21</td><td>35<br>0.13</td><td>5<br>0.01</td><td>93<br>0.37</td><td>4<br>0.01</td><td>9<br>0.03</td><td>0<br>0</td><td>12<br>0.04</td><td>212<br>0.84</td><td>12<br>0.04</td><td>251<br>14,91%</td><td>20977<br>83.5%</td><td>0.01</td></tr><tr><td rowspan="2">2b</td><td>2014</td><td>1377</td><td>148<br>0.19</td><td>84<br>0.11</td><td>0<br>0</td><td>232<br>0.31</td><td>32<br>0.04</td><td>15<br>0.02</td><td>5<br>6.7^-3</td><td>52<br>0.06</td><td>8<br>0.01</td><td>2<br>2.6^-3</td><td>0<br>0</td><td>81<br>0.10</td><td>403<br>0.54</td><td>245<br>0.32</td><td>743<br>53,95%</td><td>32682<br>43.98%</td><td rowspan="2">0.01</td></tr><tr><td>2015</td><td>1683</td><td>13<br>0.02</td><td>39<br>0.15</td><td>1<br>3.9^-3</td><td>53<br>0.21</td><td>126<br>0.28</td><td>125<br>0.28</td><td>7<br>0.01</td><td>258<br>0.59</td><td>4<br>9.1^-3</td><td>5<br>0.01</td><td>3<br>6.8^-3</td><td>14<br>0.03</td><td>382<br>0.87</td><td>528<br>1.21</td><td>436<br>25,90%</td><td>57232<br>131.2%</td><td>6.6^-3</td></tr><tr><td rowspan="2">3a</td><td>2014</td><td>810</td><td>19<br>0.06</td><td>3<br>0.01</td><td>0<br>0</td><td>22<br>0.08</td><td>15<br>0.05</td><td>1<br>3.6^-3</td><td>6<br>0.02</td><td>22<br>0.08</td><td>3<br>0.10</td><td>0<br>0</td><td>0<br>0</td><td>0<br>0</td><td>48<br>0.17</td><td>20<br>0.07</td><td>274<br>33,82%</td><td>263<br>0.95%</td><td rowspan="2">0.18</td></tr><tr><td>2015</td><td>972</td><td>235<br>1.79</td><td>67<br>0.51</td><td>7<br>0.05</td><td>309<br>2.35</td><td>221<br>1.68</td><td>51<br>0.38</td><td>37<br>0.28</td><td>309<br>2.35</td><td>24<br>0.18</td><td>0<br>0</td><td>2<br>0.01</td><td>0<br>0</td><td>691<br>5.27</td><td>239<br>1.82</td><td>131<br>13,47%</td><td>22047<br>168.2%</td><td>0.03</td></tr><tr><td rowspan="2">3b</td><td>2014</td><td>810</td><td>16<br>0.05</td><td>3<br>0.01</td><td>0<br>0</td><td>19<br>0.06</td><td>0<br>0</td><td>0<br>0</td><td>5<br>0.01</td><td>5<br>0.01</td><td>5<br>0.01</td><td>0<br>0</td><td>0<br>0</td><td>2<br>7.0^-3</td><td>31<br>0.10</td><td>7<br>0.02</td><td>285<br>35,18%</td><td>222<br>0.77%</td><td rowspan="2">0.13</td></tr><tr><td>2015</td><td>972</td><td>21<br>0.13</td><td>23<br>0.17</td><td>0<br>0</td><td>44<br>0.33</td><td>0<br>0</td><td>0<br>0</td><td>4<br>0.02</td><td>4<br>0.02</td><td>31<br>0.19</td><td>0<br>0</td><td>0<br>0</td><td>3<br>0.01</td><td>89<br>0.55</td><td>57<br>0.35</td><td>161<br>16,56%</td><td>8388<br>52.0%</td><td>0.01</td></tr></tbody></table>
<table><tbody><tr><td rowspan="2">4a</td><td>2014</td><td>378</td><td>6<br>0.07</td><td>9<br>0.11</td><td>0<br>0</td><td>15<br>0.18</td><td>19<br>0.24</td><td>21<br>0.26</td><td>4<br>0.05</td><td>44<br>0.55</td><td>0<br>0</td><td>1<br>0.01</td><td>0<br>0</td><td>13<br>0.16</td><td>92<br>1.16</td><td>80<br>1.01</td><td>79<br>20,89%</td><td>2411<br>30.51</td><td rowspan="2">0.03</td></tr><tr><td>2015</td><td>819</td><td>34<br>0.65</td><td>2<br>0.03</td><td>1<br>0.01</td><td>37<br>0.71</td><td>247<br>4.75</td><td>15<br>0.28</td><td>20<br>0.38</td><td>282<br>5.43</td><td>1<br>0.01</td><td>0<br>0</td><td>1<br>0.01</td><td>1<br>0.01</td><td>354<br>6.80</td><td>0<br>0</td><td>52<br>6.34%</td><td>1629<br>31.3</td></tr><tr><td rowspan="2">4b</td><td>2014</td><td>378</td><td>11<br>0.16</td><td>2<br>0.02</td><td>0<br>0</td><td>13<br>0.19</td><td>32<br>0.47</td><td>16<br>0.23</td><td>6<br>0.088</td><td>54<br>0.79</td><td>7<br>0.10</td><td>0<br>0</td><td>0<br>0</td><td>6<br>0.08</td><td>92<br>1.35</td><td>3<br>0.04</td><td>68<br>17,98%</td><td>1309<br>19.25</td><td rowspan="2">0.07</td></tr><tr><td>2015</td><td>819</td><td>28<br>0.35</td><td>5<br>0.09</td><td>1<br>0.019</td><td>34<br>0.65</td><td>441<br>5.58</td><td>35<br>0.44</td><td>31<br>0.39</td><td>507<br>6.41</td><td>0<br>0</td><td>1<br>0.01</td><td>0<br>0</td><td>1<br>0.01</td><td>587<br>7.43</td><td>2<br>0.02</td><td>79<br>9.64%</td><td>1661<br>21.02</td></tr><tr><td>5a</td><td>2015</td><td>2574</td><td>109<br>0.10</td><td>52<br>0.04</td><td>4<br>3.8^-3</td><td>165<br>0.15</td><td>27<br>0.025</td><td>2<br>1.9^-3</td><td>6<br>5.7^-3</td><td>33<br>0.03</td><td>13<br>0.01</td><td>57<br>0.05</td><td>3<br>2.8^-3</td><td>117<br>0.11</td><td>368<br>0.35</td><td>570<br>0.54</td><td>1044<br>40,55%</td><td>23252<br>22.27</td><td rowspan="2">0.01</td></tr><tr><td>5b</td><td>2015</td><td>2574</td><td>206<br>0.19</td><td>66<br>0.06</td><td>7<br>6.7^-3</td><td>279<br>0.26</td><td>108<br>0.10</td><td>72<br>0.06</td><td>27<br>0.024</td><td>136<br>0.12</td><td>9<br>8.5^-3</td><td>24<br>0.02</td><td>5<br>4.7^-3</td><td>99<br>0.09</td><td>651<br>0.62</td><td>1251<br>1.19</td><td>1048<br>40,71%</td><td>61721<br>58.89</td></tr><tr><td>6a</td><td>2015</td><td>2790</td><td>24<br>0.05</td><td>13<br>0.03</td><td>3<br>6.9^-3</td><td>40<br>0.09</td><td>89<br>0.20</td><td>4<br>9.3^-3</td><td>11<br>0.025</td><td>104<br>0.24</td><td>1<br>2.3^-3</td><td>1<br>2.3^-3</td><td>0<br>0</td><td>70<br>0.16</td><td>245<br>0.57</td><td>641<br>1.49</td><td>429<br>15,37%</td><td>20844<br>48.58</td></tr><tr><td>6b</td><td>2015</td><td>2790</td><td>8<br>0.03</td><td>0<br>0</td><td>6<br>0.01</td><td>14<br>0.03</td><td>0<br>0</td><td>1<br>3.9^-3</td><td>1<br>3.9^-3</td><td>2<br>7.8^-3</td><td>1<br>3.9^-3</td><td>0<br>0</td><td>3<br>0.01</td><td>41<br>0.16</td><td>79<br>0.30</td><td>845<br>3.13</td><td>255<br>9.13%</td><td>16913<br>66.32</td></tr><tr><td rowspan="2">7a</td><td>2014</td><td>1875</td><td>8<br>0.12</td><td>42<br>0.45</td><td>1<br>0.10</td><td>51<br>0.54</td><td>24<br>0.25</td><td>26<br>0.27</td><td>4<br>0.04</td><td>54<br>0.58</td><td>1<br>0.10</td><td>3<br>0.03</td><td>3<br>0.03</td><td>3<br>0.03</td><td>115<br>1.23</td><td>262<br>2.81</td><td>93<br>4,96%</td><td>8889<br>95.5</td><td rowspan="2">0.01</td></tr><tr><td>2015</td><td>2700</td><td>26<br>0.12</td><td>18<br>0.08</td><td>6<br>0.02</td><td>50<br>0.24</td><td>0<br>0</td><td>0<br>0</td><td>0<br>0</td><td>0<br>0</td><td>15<br>0.07</td><td>0<br>0</td><td>3<br>0.01</td><td>7<br>0.03</td><td>76<br>0.36</td><td>187<br>0.90</td><td>207<br>7.66%</td><td>10105<br>48.81</td></tr><tr><td rowspan="2">7b</td><td>2014</td><td>1875</td><td>47<br>0.17</td><td>33<br>0.09</td><td>1<br>2.8^-3</td><td>81<br>0.22</td><td>85<br>0.24</td><td>12<br>0.03</td><td>8<br>0.02</td><td>105<br>0.29</td><td>43<br>0.12</td><td>20<br>0.05</td><td>3<br>8.4^-3</td><td>5<br>0.01</td><td>267<br>0.75</td><td>733<br>2.07</td><td>353<br>18,82%</td><td>17173<br>48.64</td><td rowspan="2">0.01</td></tr><tr><td>2015</td><td>2700</td><td>58<br>0.17</td><td>24<br>0.11</td><td>11<br>0.05</td><td>93<br>0.44</td><td>0<br>0</td><td>0<br>0</td><td>0<br>0</td><td>0<br>0</td><td>17<br>0.05</td><td>11<br>0.03</td><td>3<br>9.1^-3</td><td>7<br>0.02</td><td>122<br>0.37</td><td>619<br>1.88</td><td>329<br>12,18%</td><td>26913<br>81.80</td></tr></tbody></table>