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

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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, Entomological Society of America, 2017, 46 (3), pp.528-537. ￿10.1093/ee/nvx054￿. ￿hal-01517228￿

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Distributed under a Creative Commons Attribution - ShareAlike| 4.0 International License Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin Albert et al.: Agroecological management Laurence ALBERT ALBERT Laurence management Agroecological al.: et Albert 2 1 3 FRANCE Cedex, Rennes Laurence ALBERTLaurence France Northwestern in Orchards Apple in Enemies Natural its plantagineaDysaphis Impact of Agroecological Infrastructures on the Dynamics of E-mail: [email protected] [email protected] E-mail: La Rangées Chesnel Chesnel La Rangées 2.33.27.56.70 +33 Phone: Cidricoles Productions des Français Institut control Biological Entomology Environmental orchards apple in cider M14 IEP IR/goapsOetUiest Rne 1 6 re e an Biu, 3504 Brieuc, Saint de rue 65 1, Rennes INRA/Agrocampus-Ouest/Université IGEPP, UMR1349 Institut Français des Productions Cidricoles, La Rangée Chesnel, 61500 Sées, FRANCE FRANCE Sées, 61500 Chesnel, La Rangée Cidricoles, Productions des Français Institut INRA Plantes & Systèmes de culture Horticoles, F-84914 AVIGNON Cedex 9, FRANCE 9, FRANCE Cedex AVIGNON F-84914 Horticoles, de culture Systèmes & Plantes INRA Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological

– 1 parasitoids and predators Fax: +33 2.33.27.49.51 2.33.27.49.51 +33 Fax: predators and parasitoids , Pierre FRANCK , Pierre Comment citer cedocument: 3 Passerini (Hemiptera: Aphididae) and (Hemiptera: Passerini , Yann GILLESYann ,

1 , Manuel PLANTEGENESTManuel , France France SEES 61500 2

2 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 11 11 10 10 12 12 14 14 13 13 15 15 16 16 19 19 18 17 21 21 20 24 24 25 25 29 29 28 23 23 26 26 27 27 22 22 9 9 8 8 7 7 6 6 5 5 4 4 3 3 2 2 1 Apple orchard production is facing new environmental and societal challenges, resul challenges, societal and environmental new facing is production orchard Apple (2014 and 2015), we monitored the population dynamics of of dynamics population the monitored we 2015), and (2014 in apple orchards in Europe, which causes important economic production losses. losses. production economic important causes which Europe, in orchards apple in and mutualistic ants in commercial production cider-apple orchards. The influe The orchards. cider-apple production commercial in ants mutualistic and were assessed. Our results suggest that flower strips favour an increase in natura in increase an favour strips flower that suggest results Our assessed. were control of pests. In this study, we focused on on focused we study, this In pests. of control vicinity of or within orchards could increase natural enemy presence and thus and presence enemy natural increase could orchards within or of vicinity cultivar, insecticide use and distance to agroecological infrastructures (hedgerows and and (hedgerows infrastructures agroecological to distance and use insecticide cultivar, reproduction reproduction habitats to many arthropods. Consequently, setting-up agroecological in the vicinity of the orchards and could thus play an important role in ye. goclgcl nrsrcue pa a iprat oe n rvdn setr f shelter, providing in role important an play infrastructures Agroecological types. developing new agronomic strategies, which could be subsequently extended to to extended subsequently be could which strategies, agronomic new developing of fruits is not a marketability imperative, offers good to opportunities study of offers fruits is a imperative, not marketability the biological control of of control the biological in strong pressure to reduce pesticide use. Cider-apple production, for which the perfect v perfect the which for production, Cider-apple use. pesticide reduce to pressure strong in ABSTRACT Biological control, cider-apple orchard, cider-apple control, Biological Keywords n h scn hl o te 20 the of half second the In resulted resulted in agricultural landscape simplification (Robinson and Sutherland 2002, produced numerous negative side effects on biodiversity (Krebs et alet (Krebs biodiversity on effects side negative numerous produced practices are strongly required. required. arestrongly practices giutrl ehnzto ad h ue f ytei psiie ad fertiliz and pesticides synthetic of use the and mechanization agricultural 2004, Simon et alet Simon 2004, urn arclua prdg ad h dvlpet f oe niomnal friendly environmentally more of development the and paradigm agricultural current agricultural yields in developed countries. This yield increase was achieved achieved was increase yield This countries. developed in yields agricultural Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological

. 2007) and the quality of soil and water (Moss 2008). Consequently, a chang a Consequently, 2008). (Moss water and soil of quality the and 2007) Dysaphis plantagineaDysaphis Comment citer cedocument: th century, the green revolution allowed an unprecedented increase in in increase unprecedented an allowed revolution green the century, Dysaphis plantaginea Dysaphis

. . Dysaphis plantaginea Dysaphis Dysaphis plantaginea Dysaphis , flower strip, hedgerow hedgerow strip, flower , (Passerini), one of the major pests major the of one (Passerini), the the production system by improving . 1999), human health (Lee et al et (Lee health human 1999), production systems that are systems production ers. The green revolution revolution green The ers. by the generalization of of generalization the by nces of the cider-apple cider-apple the of nces improve the biological biological the improve Benton Benton et al , its natural enemies enemies natural its , infrastructures infrastructures in the all apple-production apple-production all l enemy abundance abundance enemy l o rsucs or resources ood During two years two During ting, in particular, particular, in ting, flower strips) strips) flower agricultural agricultural isual aspect aspect isual . 2003) and e in the the in e 2 .

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 31 31 30 30 50 50 36 36 32 32 52 52 49 49 38 38 35 35 54 54 57 57 56 51 51 33 33 37 37 58 58 48 48 34 34 53 53 55 55 39 39 46 46 47 47 59 59 45 45 40 40 41 41 43 43 44 44 42 42 Agroecology proposes Agroecology proposes to primarily base agricultural on production the of mobilization prxmtl 6 pyohgu atrpd pce ae osdrd o e pl pss (J pests apple be to considered are species arthropod phytophagous 60 Approximately Agroecological infrastructures include hedgerows, flower strips, permanent grassl permanent strips, flower hedgerows, include infrastructures Agroecological rather than on chemical inputs. In particular, promoting the natural control of pests pests of control natural the promoting particular, In inputs. chemical on than rather and and the improvement of ecosystem services (e.g. pollination, nutrient cycl ahgn (apao e al et (Sauphanor pathogens nrsrcue wti o i te iiiy f h co (ane t al et (Haenke crop the of vicinity the in or within infrastructures insecticide insecticide use reduction. The resulting reduction of economic and envir

niomna lw. eas cdrape ae rnfre, hi pret v perfect their transformed, are cider-apples Because laws. environmental The management of apple orchards is based on the intensive use of pesticides to pesticides of use intensive the on based is orchards apple of management The hy a poie et ad aua eeis ih aiu bnfca functions beneficial various with enemies natural and pests provide may They practices (e.g. pesticide use reduction, accurate choice of cultivars) and establis and cultivars) of choice accurate reduction, use pesticide (e.g. practices than in orchards for fresh fruit production (approximately 15 15 (approximately production fruit fresh for orchards in than which could subsequently be generalized. generalized. be subsequently which could environmentally friendly protection strategies to address the new challenges impo challenges new the address to strategies protection friendly environmentally to increase farmer benefits and the environmental sustainability of agriculture (T agriculture of sustainability environmental and the benefits farmer to increase 1999). The rosy apple aphid (RAA) (RAA) aphid apple rosy The 1999). apple producing area in Europe. Cider-apple orchard cultivation is thus important i is thus important cultivation orchard Europe. Cider-apple in area apple producing Various approaches have been proposed to improve pest biological control, including including control, biological pest improve to proposed been have approaches Various prerequisite of their marketability and fewer pesticide treatments are applied applied are treatments pesticide fewer and marketability their of prerequisite cider-apple orchards offer an opportunity to develop and test protection strategies usi strategies protection test and develop to an opportunity offer orchards cider-apple microclimatic microclimatic conditions and refuge during (Landis adverse et seasons al. 200 et al Northwestern France (i.e. Bretagne, Normandie and Pays de la Loire regions) is the number one cide number is the regions) Loire dePays la and Normandie Bretagne, (i.e. France Northwestern when these resources are not available in the crop (Wyss 1996, Denys and Tsc and syrphids use them as overwintering areas (Collins et alet (Collins areas overwintering as them use syrphids and 2013). Agroecological infrastructures also provide pollen and nectar resources resources nectar and pollen provide also infrastructures Agroecological 2013). insects insects (Schmale et al Rijn et alet Rijn longevity of parasitoids (Wäckers 2001, Berndt and Wratten 2005) and improve the improve and 2005) Wratten and Berndt 2001, (Wäckers parasitoids of longevity Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological . 2005). 2005). . 2013). Agroecological infrastructures also provide alternative prey for generalist preda generalist for prey alternative provide also infrastructures Agroecological 2013). . 2001, 2001, Wäckers Winkler et al Comment citer cedocument: . 2009). Currently, farmers are under strong pressure to develop develop to pressure strong under are farmers Currently, 2009). Dysaphis plantaginea Dysaphis

. 2006, Hogg et al Passerini (Hemiptera: Aphididae), is among among is Aphididae), (Hemiptera: Passerini vs . 2003, Sarthou et alet Sarthou 2003, 35 treatments per year). Consequently, Consequently, year). per treatments 35 . 2009, Miñarro and Prida 2013). 2013). Prida and Miñarro 2009, onmental onmental costs would contribute ing, ing, biological control of pests) . 2011, Laubertie et al 0). 0). Thus, spiders, beetles harntke harntke 2002, Lavandero in cider-apple orchards orchards cider-apple in sa apc i nt a not is aspect isual schumi et alschumi ands and woodlands. woodlands. ands and . n the local economy. economy. local n the 2005, Pfiffner 2005, sed by society, and and society, by sed hing agroecological agroecological hing , including suitable suitable including , natural processes fecundity of other other of fecundity that increase the the increase that control pests and and pests control ng less pesticide, pesticide, less ng would lead to to lead would ne e al et enser changes in in changes . 2015). 2015). . 2012,

et alet tors tors r- 3 . .

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 60 60 62 62 63 63 66 66 61 61 67 67 68 68 65 65 64 64 69 69 71 71 70 70 76 76 75 72 72 74 74 77 77 73 73 78 78 80 80 79 79 81 81 86 86 85 85 82 82 84 84 87 87 88 88 83 83 89 89 Arnaudov Arnaudov et al h ms dtietl et, asn sgiiat cnmc oss y reduci by losses economic significant causing pests, detrimental most the 2004). The RAA is problematic not only in organic but also in conventional in also but organic in only not problematic is RAA The 2004). pest pest is et al(Cross detected) recorded (Delorme et alet (Delorme recorded apple tree tree apple abundance threshold for economic damage, resulting in a low treatment threshold (i.e., as (i.e., threshold treatment low a in resulting damage, economic for threshold abundance Plantago spp Plantago of spring, eggs laid in autumn hatch on apple trees producing parthenogenically r parthenogenically producing trees apple on hatch autumn in laid eggs spring, of Dib et al efficiency could be an alternative to insecticides use to limit RAA pop RAA limit to use insecticides to alternative an be could efficiency (Lathrop 1928, Bonnemaison 1959, Blommers et alet Blommers 1959, Bonnemaison 1928, (Lathrop generation of oviparous females lays fertilized overwintering eggs on the a the on eggs overwintering fertilized lays females oviparous of generation mid-June to July in the North of France. The aphids return to apple trees in aut in trees apple to return aphids The France. of North the in July to mid-June Several recent studies have focused on the community of natural enemies, which which enemies, natural of community the on focused have studies recent Several 2004). et al. Blommers 1997, Trzcinski, losses caused by this leaf-roller aphid, which develops on the lower si lower the on develops which aphid, leaf-roller this by caused losses infestation, as well as in following years (Bonnemaison 1959, De Berardinis et al et Berardinis De 1959, (Bonnemaison years following in as well as infestation, the biological control of of control biological the o h dfrain cue t te ris n goig hos dcesn te il i t in yield the decreasing shoots, growing and fruits the to caused deformations the to syrphids, coccinellids, parasitoids (mainly (mainly parasitoids coccinellids, syrphids, and f A pe (i e al et (Dib prey RAA of Interactions between the ants and myrmecophilous aphids are beneficial for both arthrop both for beneficial are aphids myrmecophilous and ants the between Interactions the colony, as as colony, the Rosenheim Rosenheim et al is important (Snyder and Ives 2001). RAA population dynamics also depend on the presenc the on also depend dynamics population RAA 2001). Ives and (Snyder is important supplied supplied with sugar through aphids’ honeydew whereas aphids improve their reproducti and Kennedy 1956, Banks and Nixon 1958, Flatt and Weisser 2000) and are protected are and 2000) Weisser and Flatt 1958, Nixon and Banks 1956, Kennedy and is expected to result in a decrease in RAA abundance, this trend may re Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Aphidoletes . 2010, Miñarro and Prida 2013). RAA is a host-alternating aphid species. Its Malus domesticaMalus , mainly , . 2013). The abundance of these natural enemies in orchards depends on the abundance . sp (Diptera: Cecidomyiidae) (Wyss et al et (Wyss Cecidomyiidae) (Diptera: sp . plantagineaD. 1995, Korenko and Pekár 2010). Thus, while an increase in natural enemy abundanc P. lanceolata P. D. plantagineaD. . . 1998). Many recent studies have suggested that improving biological control control biological improving that suggested have studies recent Many 1998). 06 ad n h itagid rdto pesr (oehi e al et (Rosenheim pressure predation intra-guild the on and 2016) Comment citer cedocument: Borkh. (Rosales: Rosaceae), and its secondary hosts are plantain herbs herbs plantain are hosts secondary its and Rosaceae), (Rosales: Borkh. . As 2007). a an in increase consequence, resistance has insecticide been s omny tedd y ns Bneasn 99 Star 1959, (Bonnemaison ants by attended commonly is L. (Lamiales: Plantaginaceae) (Blommers, 1999). At the beginning beginning the At 1999). (Blommers, Plantaginaceae) (Lamiales: L. during spring. In Europe, this community is mostly composed of of mostly composed is community this Europe, In spring. during

Ephedrus . sp sp 2004). Migration to a secondary host occurs from from occurs host secondary a to Migration 2004). – Hymenoptera: Braconidae), earwigs, spiders spiders earwigs, Braconidae), Hymenoptera: . 1999, Miñarro et al et Miñarro 1999, ulations (Hemptinne et alet (Hemptinne ulations de of the leaves, are mainly due due mainly are leaves, the of de verse verse when predation intra-guild orchards due to its very low low very its to due orchards g il (lmes t al et (Blommers yield ng pple trees. The economic economic The trees. pple . 2005, Dib et al et Dib 2005, . umn, where a sexual sexual a where umn, 1994, Wilkaniec and Wilkaniec 1994, eproducing females females eproducing could play a role in role a play could primary host is the ve ve rate against natural natural against ods: ants are ants ods: soon as the as soon he year of of year he e of ants in antsin of e (El-Ziady (El-Ziady ỳ 1970). 1970). . . . 1993, 1993, 2003, 2003, 2010, 2010, e e 4 . Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 100 100 102 102 101 103 103 115 115 104 104 116 116 118 118 117 105 105 114 114 113 106 106 107 107 112 112 111 110 109 108 90 90 91 91 96 96 92 92 95 95 97 97 99 99 93 93 94 94 98 98 enemies (Stadler and Dixon 1999, Yao et alet Yao 1999, Dixon and (Stadler enemies and enemies (Stewart-Jones et alet (Stewart-Jones enemies Indeed, several studies noted that the distance to agroecological infrastructures i infrastructures agroecological to distance the that noted studies several Indeed, shown that the proportion of the aphid aphid the of proportion the that shown The The present project aimed to determine the impact of two types of agroecological infras resources. flower to distance the with exponentially decreased Several recent studies noted the potential of agroecological infrastructures to infrastructures agroecological of potential the noted studies recent Several operating would operating help the needed to required density determine anto provide efficien strips strips and hedgerows - on the abundance of arthropods interacting with (Corbett (Corbett and Rosenheim 1996, Lavandero et al aiet n Jdr gatd no M0 rosok Te he clias ifrd n hi vigo their in differed cultivars three The rootstock. MM106 onto grafted Judor) and Dabinett and natural enemy abundance is not systematically linear. For instance, Tyliana instance, For linear. systematically not is abundance enemy natural and and ants) and its consequences on RAA population dynamics. The influence influence The dynamics. population RAA on consequences its and ants) and control of control of precocity: Douce de l’Avent de Douce precocity: 2013, Pfiffner et alet Pfiffner 2013, was the less precocious cultivar and Judor (JUD) was intermediate. intermediate. was (JUD) Judor and cultivar precocious less thewas w tps f goclgcl nrsrcue o atrpd yais a asse i assessed was dynamics arthropod on infrastructures agroecological of types two (Bowie 1999) abundances. Moreover, the link between the distance to agroecological to distance the between link the Moreover, abundances. 1999) (Bowie with three different cider-apple cultivars (three conse (three cultivars cider-apple different three with 2012 and 2010 between planted were orchards 1). The (Fig. France northwestern in locations in seven orchards in northwestern France, which exhibit a range of farming practices (cultivars, insecticide use insecticide (cultivars, practices farming of a range exhibit which France, northwestern in orchards For this purpose, the arthropod populations (aphids, their main natural enemies and the and enemies natural main their (aphids, populations arthropod the purpose, this For Experiments were carried out in the spring and early summer in in cider in out and were the 2015 and 2014 early summer spring carried Experiments years. successive two during spring in were monitored ants) Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological D. plantagineaD. Monitored Cider-Apple Orchards Orchards Cider-Apple Monitored D. plantaginea D. plantaginea . enhances the growth of aphid colonies by reducing aphid predation by their natur their by predation aphid reducing by colonies aphid of growth the enhances 2013). Knowledge about the distance at which agroecological infrastructures are infrastructures agroecological which at distance the about Knowledge 2013). by favouring by natural enemy communitythe Comment citer cedocument: cov . 2008, Miñarro et alet Miñarro 2008, (DDA) was the most vigorous and precocious cultivar, Dabinett (DAB) (DAB) Dabinett cultivar, precocious and vigorous most the was (DDA)

Metopolophium dirhodum Metopolophium Materials and Methods and Materials . 2000, Kaneko 2003). Thus, the relationship between ants ants between relationship the Thus, 2003). Kaneko 2000, . 2005), spiders (Miliczky and Horton 2005) and syrphids . 2010). 2010). cutive rows of each cultivar: Douce de l’Aventde Douce cultivar: each of rows cutive parasitised by parasitised

(Dib et (Dib al

D. D. plantaginea . 2012, and 2012, Miñarro Prida of the distance to these these to distance the of improve the biological biological the improve Aphidius rhopalosiphi Aphidius kis et alet kis nfluenced parasitoids parasitoids nfluenced t biological t control. biological (natural enemies n 14 cider-apple cider-apple 14 n tructures tructures - flower -apple orchards -apple infrastructures infrastructures . (2004) have have (2004) ir mutualistic mutualistic ir ur and and ur cov al ). ). 5 , ,

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 134 134 129 129 133 133 132 131 130 130 128 128 127 119 119 126 126 123 123 122 121 120 124 124 143 143 125 125 135 135 147 147 146 145 144 142 142 136 136 141 141 137 137 140 140 139 139 138 prxmtl oetid f h tes ee ytmtcly oioe i ec orc each in monitored systematically were trees the of one-third Approximately Quotient (EIQ) was used to estimate the toxicity of each insecticide (https://n insecticide each of toxicity the estimate to used was (EIQ) Quotient abcs nigra Sambucus Calendars of the insecticide treatments in 2014 and 2015 were collected. The En The collected. were 2015 and 2014 in treatments insecticide the of Calendars included included The The hedgerows were mainly composed of monitored. and in the agroecological infrastructures established (Table 1). Only five of out m o 3 ) n te netcd ue ee eodd ad h atrpd ouain dynami population arthropod the and recorded, were use insecticide the and m) 63 to m 0 1). (Fig. 2014 in monitored contiguous trees, depending on the considered orchard - Table 1). For each apple tree, the d the tree, apple each For 1). Table - orchard considered the on depending trees, contiguous In each location, two contiguous orchards were studied that differed in regard to insecticide insecticide to regard in differed that werestudied orchards contiguous two location, each In orchard and the cultivar (Table 1). The main active ingredients used against RAA i RAA against used ingredients active main The 1). (Table cultivar the and orchard the closest hedgerow (ranging from 5 m to 57 m), the distance to the closest flo closest the to distance the m), 57 to m 5 from (ranging hedgerow closest the beneficial beneficial arthropods. EIQ assigns to each insecticide ingredient a score rangi cyhalothrin. lambda and acetamiprid flonicamid, were ingredient in the insecticide insecticide the in ingredient to its toxicity to beneficial arthropods (Kovach et al et (Kovach arthropods beneficial to toxicity its to beneficial arthropods, arthropods, beneficial insecticides applied during the period of RAA presence in the apple trees (f trees apple the in presence RAA of period the during applied insecticides where ܧܫܳ formula: following the using orchard Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological ௙௜௘௟ௗ௨௦௘௥௔௧௜௡௚ Monitoring of Arthropod Population Dynamics Dynamics ArthropodPopulation of Monitoring EIQ Assessment of Insecticide Toxicity to Beneficial Arthropods Arthropods Beneficial to Toxicity Insecticide of Assessment Monitored Trees Trees Monitored Centaurea cyanusCentaurea i is the EIQ value assigned to the active ingredient contained in the insectic the in contained ingredient active the to assigned value EIQ the is and and  ൌ σ ሺܧܫܳ RT uru pedonculata Quercus i , the rate of insecticide insecticide of rate the , Comment citer cedocument: ௜ כܴܶ , Silene vulgarisSilene i . The The . ௜ ݐ݊݁݅݀݁ݎΨܽܿݐ݅ݒ݁݅݊݃כ EIQ

field Carpinus Carpinus betulus

use ratinguse , . All flower strips, established specifically for the study, study, the for specifically established strips, flower All . Silene latifolia albalatifolia Silene i ranged from 0 to 6.61, depending on the year, the the year, the on depending 6.61, to 0 from ranged use and use . 1992). We calculated the cumulative impact of the of impact cumulative the calculated We 1992). ௜ ሻ , %active ingredient %active , Cornus and and sp, Achillea millefoliumAchillea Corylus Corylus avellana rom March to July) in each each in July) to March rom ng ng from 5 to 125 according the seven locations were i the percentage of active active of percentage the ysipm.cornell.edu/eiq) to to ysipm.cornell.edu/eiq) wer strip (ranging from from (ranging strip wer vironmental Impact Impact vironmental n the cider orchard orchard cider the n hard (63 to 423 423 to (63 hard ide ide . . , , Viburnum i application application relative to to relative istance to to istance cs were were cs sp, 6 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 149 149 161 161 150 150 162 162 151 151 163 163 148 148 160 160 155 155 154 153 152 152 169 169 168 167 166 165 164 156 156 171 171 170 159 159 158 157 173 173 172 177 177 176 175 174 At each observation date, the total number of RAA individuals was counted on each monitored tre monitored each on was counted individuals RAA of number total the date, observation At each At each observation date, the number and identity of each natural enemy type type enemy natural each of identity and number the date, observation each At m). All terminal shoots of each monitored tree were inspected from the lowest branch up branch lowest the from inspected were tree monitored each of shoots terminal All m). the developmental stage of all of the observed natural enemies, as not all stages all not as enemies, natural observed the of all of stage developmental the 1.7 m for practical reasons. In 2014 and 2015, the trees were monitored every week fr week every monitored were trees the 2015, and 2014 In reasons. practical for m 1.7 control. In most cases, natural enemy identification was at the family level. An level. family the at was identification enemy natural cases, most In control. The The monitored trees were visually inspected to record the RAA abundance and th the end of June and every two weeks from mid-March to mid-April and du and mid-April to mid-March from weeks two every and June of end the the species level. However, we observed only only weobserved However, level. the species enemies enemies and ants within the RAA The colonies. mean height of the wasmonitored trees found within the RAA colonies were recorded and summed for each monitored tree. We We tree. monitored each for summed and recorded were colonies RAA the within found April to July). from orchards orchards ( (i) The presence/absence variable variable ( (i) The presence/absence processes: ecological the different assess year to studied each and for tree monitored each on dynamics population RAA the characterize to considered were variables Three (ii) The logarithm of the area under the curve ( curve the under area the of logarithm The (ii) tree monitored the on observed was RAA one at least when 1 or to date any at was observed RAA

(iii) The presence duration ( duration presence The (iii) situ process emigration RAA the indicating observed), was aphid 1 least at datewhich at first RAA population dynamics (survival and reproduction) reproduction) and (survival dynamics population RAA Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Data Analysis Analysis Data 4a Dysaphis plantagineaDysaphis Natural Enemies and Ants Ants and Enemies Natural Dysaphis plantagineaDysaphis Natural Enemies and Ants Observed in RAA Colonies Colonies RAA in Observed Ants and Enemies Natural and 4b ) located located at ) location Comment citer cedocument: PD) ,

in days (last date at which at least 1 aphid was observed minus the minus observed was aphid 1 least at which at date (last days in

PA ), indicating the RAA colonization process, was was to set process, 0 when RAA indicating no ), the colonization

4 , where the RAA populations were recorded every two weeks every were two recorded where populations , RAA the Lasius nigerLasius logAUC ) of the tree population abundance, indicating indicating abundance, population tree the of ) and and Formica sp. sp. ring July (except in the two two the in (except July ring ts were not identified to to identified not were ts and the number of ants of number the and e abundance of natural are involved in aphid aphid in involved are 3.4 m (SD 0.49 om mid-April to to mid-April om to a height of of height a to also recorded recorded also e. e. in 7 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 181 181 183 183 182 178 178 186 186 185 184 196 196 179 179 180 180 201 201 187 187 197 197 188 188 198 198 195 195 189 189 200 200 199 207 207 206 205 204 203 202 202 194 194 191 191 190 190 192 192 193 193 created by summing the counts of all observed natural enemies for any stage and stage any for enemies natural observed all of counts the summing by created Natural Natural enemy dynamics and ants were only assessed on the monitored trees in way as those of RAA and their natural enemies ( enemies natural their and RAA of those as way for calculated also were variables dynamics was was observed (i.e., a monitored tree where the RAA presence/absence was set to 1). The n The The main purpose of our study was to assess the influence of agroecological i of RAA as a fixed factor was equivalent to analysing the influence of the fac the of influence the analysing to equivalent was factor fixed a as RAA of yais ee hrceie uig h sm vrals s o RA ( RAA for as variables same the using characterized were dynamics considered developmental stage (egg, larva, adult) of each taxon. A global variable ( variable global A taxon. each of adult) larva, (egg, stage developmental considered PD bv vrals hrceiig A pplto dnmc. is, Generaliz First, dynamics. population RAA characterizing variables above abundance abundance ratio between the natural enemies and aphids or between the ants and (GLMM) (GLMM) were used to assess the influence of each considered factor (distance to the c two random factors were added, the orchard location and the studied year. All statistical analyses w year. analyses All statistical studied the and location the were orchard added, factors two random and and other agricultural variables for a given level of rosy apple aphid distance to the closest flower strip, strip, flower closest the to distance PA unit. observation the as tree the using 2015) Team core (R software 3.1.3 with R the out carried considered. was were were fitted using the lme4 package, version 1.1-7 et (Bates al assessing assessing how the dynamics of natural enemies and ants are impacted by agro could result from variations in natural enemy and ant population dynamics, the variable variable ( to the population dynamics variables associated to each natural enemy taxon and to ants to and taxon enemy natural each to associated variables dynamics population the to as as well the rosy apple aphid abundance ( were fitted assuming a binomial distribution, distribution, a binomial fittedwere assuming were fitted using a Gamma distribution, regardless of the arthropod taxon. The mixed l of mixed thetaxon. arthropod The distribution, regardless a were using fitted Gamma Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological PA Statistical Analyses Analyses Statistical , logAUC and Comment citer cedocument: PD ) ) as well as its significance. Second, to assess in what extent factor effects EIQ

logAUC il rtn use rating field allNE Results ) ) as a supplementary explanatory variable. This allowed logAUC PA . The ant dynamics were characterized in the same same the in characterized were dynamics ant The . ,

and cultivar) on each RAA population dynamics dynamics population RAA each on cultivar) and logAUC were fitted assuming a normal distribution and distribution and a normal fitted were assuming and and . 2015). A significance threshold of p=0.05 PD abundance. Introducing abundance. the ). ). PA , , logAUC nfrastructures nfrastructures on the three ed Linear Mixed Models Models Mixed Linear ed same GLMMs were fitted ecological ecological infrastructures tors under study on the the on study under tors which at least one RAA In aphids. all models and and taxon. The three three The taxon. losest losest hedgerow, allNE PD inear models inear atural atural enemy but including including but ) was also was ) ) for each each for ) logAUC ere ere 8

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 222 222 224 224 223 226 226 225 221 221 227 227 233 233 232 231 230 229 228 220 220 237 237 234 234 238 238 218 218 235 235 219 219 236 236 216 216 208 208 217 217 209 209 210 210 215 215 214 213 212 211 211 A large variation in the abundance of RAA, natural enemies and ants was observe observed and the ratio of the mummy number to the RAA number never exceeded exceeded never number RAA the to number mummy the of ratio the and observed considered year and orchard. yearorchard. and considered The natural enemy community composition varied strongly during the season. The The season. the during strongly varied composition community enemy natural The B). (Appendix eand o te usqet eald ttsia aaye (al 2. Simi 2). (Table analyses statistical detailed subsequent the for retained dominated by Syrphidae early in the season and then by Coccinellidae and other other and by Coccinellidae then and season in the early Syrphidae by dominated Table 3 provides a synthetic overview of the results of the GLMMs. Aphids and a and Aphids GLMMs. the of results the of overview synthetic a provides 3 Table Arthropod Taxa Observed May. of end the and mid-May between peaked populations RAA years, the In2). both er) Fw hyoia, eitr ad ataia wr osre i bt yas n wr n were and years both in observed were Cantharidae and Hemiptera Chrysopidae, Few years). contrary, aphids and ants were less abundant in the vicinity of the flower str flower the of vicinity the in abundant less were ants and aphids contrary, more more abundant in the vicinity of the hedgerows. On the contrary, hedgerows had in observed observed in 2014 and 2015, respectively), followed by Forficulidae (18% and 15% on the natural enemies. They only have a positive effect on the presence durati presence the on effect positive a have only They enemies. natural the on observed in 2014 and 2015, respectively) and Araneae (9% of the natural ene natural the of (9% Araneae and respectively) 2015, and 2014 in observed and of Syrphidae eggs and a negative effect on the presence duration of Coccinel of duration presence the on effect negative a and eggs Syrphidae of and 2). The natural enemy community was dominated by Syrphidae (45% and 32% of the of 32% and (45% Syrphidae by dominated was community enemy natural The 2). The The mean abundance of RAA observed per tree and per sampling date varied widely,

bevd n 04ad 05 epciey ad ocnlia (2 ad3% f the of 36% and (22% Coccinellidae and respectively) 2015, and 2014 in observed studied year and studied orchard. For instance, in 2014, the mean number of R of number mean the 2014, in instance, For orchard. studied and year studied sampling date ranged from 0.8 in orchard orchard in 0.8 from ranged date sampling The The composition of the natural enemy community remained fairly stable fro B). (Appendix the pest abundance was higher in 2015 than in 2014 in all orchards, except in orchar in except orchards, all in 2014 in than 2015 in higher was abundance pest the Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological nlec o Arclua Patcs n Areooia Ifatutrs n h M the on Infrastructures Agroecological and Practices Agricultural of Influence Aphid Abundance and its Variation in Space and Time and Time Space in Variation its Abundance and Aphid Community of Natural Enemies and its Variation in Space and Time and Time Space in Variation its and Enemies Natural of Community Comment citer cedocument:

3b to 95.5 in orchard orchard in 95.5 to 7a (Table 2 and Appendix B). Globally, Globally, B). Appendix and 2 (Table m m one year to the next (Table ips, while all of the natural natural the of all while ips, larly few mummies were were mummies few larly on of Syrphidae larvae larvae Syrphidae of on mies observed in both both in observed mies of of the natural enemies d among the orchards natural enemies (Fig. (Fig. enemies natural AA per tree and per and tree per AA most most cases no effect lidae larvae. On the the On larvae. lidae nts appeared to be be to appeared nts 0.2% whatever the the whatever 0.2% depending depending on the natural enemies enemies natural natural enemies enemies natural community was was community ds ds 4a and ain 4b ot 9

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 260 260 261 261 262 262 259 259 264 264 263 265 265 258 258 266 266 256 256 267 267 257 257 268 268 254 254 244 244 269 269 255 255 243 243 245 245 246 246 241 241 240 240 239 239 253 253 250 250 249 248 247 242 242 251 251 252 252 nlss ee are ot sn tre epne aibe caatrzn atrpd popul arthropod characterizing variables response three using out carried were Analyses n isciie s itniy a a oty iia ifune n l atrpd ab arthropod all on influence similar mostly a had intensity use insecticide and agroecological infrastructures had opposite effects on aphids and ants on the one ha one the on ants and aphids on effects opposite had infrastructures agroecological enemies on the other hand. This result suggests that agroecological infrastruc agroecological that suggests result This hand. other the on enemies infrastructures infrastructures either favoured or disfavoured the entire community of natural en the level of RAA biological control by its natural enemies. enemies. its natural bycontrol biological RAA of level the yais peec poaiiy lgrtm f h ae udr h cre n peec d presence and curve the under area the of logarithm probability, presence dynamics: mn al aua eey rus sgetn ta arclua patcs n agroecol and practices agricultural that suggesting groups, enemy natural all among hypothesis was that each variable was related to different ecological processes th processes ecological different to related was variable each that was hypothesis the closest hedgerow and to the closest flower strip). All of these factors these of All strip). flower closest the to and hedgerow closest the ifrnily nlecd y h arclua patcs n areooia i agroecological and practices agricultural the by influenced differentially dynamics dynamics of aphids, of natural enemies and of ants. The tested factors appear ot ae i ti suy te he vrals ee nlecd n h sm wy by way same the in influenced were variables three the study, this in cases most nme ae o srrsn ad ee oeld s adm atr t ou o te fet o effects the on focus to factors random as modelled were and surprising not are enemies oiiey matd y pi audne Te eut wr gnrly consis generally were results The abundance. aphid by impacted positively practices (insecticide treatment and cultivar choice) and of agroecological agroecological of and choice) cultivar and treatment (insecticide practices impacted by the the by impacted enemies enemies except the Araneae were positively impacted. All arthropods were generally aibe ue t ecie h atrpd yais ( dynamics arthropod the describe to used variables enemy stage (egg, larva, adult). Detailed results by stage and variables are provided i provided are variables and stage by results Detailed adult). larva, (egg, enemy stage ambiguous. ambiguous. Indeed, the Syrphidae eggs ( insecticide insecticide use ( h Due e l’Avent de Douce the 2002). Variations among locations and between years in population dynamics o dynamics population in years between and locations among Variations 2002). This study was carried out under field and farming production conditions. Spati conditions. production farming and field under out carried was study This . impacted impacted by the regarding the abundance of aphids and of their natural enemies have long been reported to depend o to depend reported been long have enemies natural their of and aphids of abundance the regarding farming practices (Marliac et al et (Marliac practices farming Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Main Findings Findings Main EIQ EIQ EIQ field use rating field field use rating field use ratinguse field cov cultivar, followed by Judor, and were generally negatively impacted by the the by impacted negatively generally were and Judor, by followed cultivar, Comment citer cedocument: ). ). However, the insecticide effect on the Syrphidae was and Coccinellidae but the Syrphidae larvae ( ( PA . 2015) and on climatic conditions (Hemptinne et al et (Hemptinne conditions climatic on and 2015) ) (Appendix A). Finally, all natural enemy and ant abundances were were abundances ant and enemy natural all Finally, A). (Appendix )

logAUC Discussion Discussion and PD PA PA ) ) and Coccinellidae larvae ( , ) ) and the Coccinellidae eggs were negatively logAUC and and PD had an impact on population population on impact an had infrastructures (distances to to (distances infrastructures nfrastructures. However, in in However, nfrastructures. ) or the considered natural natural considered the or ) ed to be widely consistent emies. emies. While the cultivar tures actually impacted impacted actually tures f RAA and their natural natural their and RAA f et eades f the of regardless tent o-temporal variations variations o-temporal at could have been been have could at PD more more abundant on . nd and on natural natural on and nd 1994, Roy et alet Roy 1994, n Appendix A. A. Appendix n ) ) were positively the agricultural agricultural the undances, the the undances, uration. Our Our uration. farmer f ogical ogical ation ation 10 n n .

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 281 281 282 282 279 279 275 275 276 276 283 283 280 280 277 277 299 299 294 294 295 295 284 284 278 278 274 274 296 296 298 298 293 293 297 297 290 290 285 285 288 288 273 273 272 271 270 291 291 286 286 292 292 289 289 287 287 s xetd al aua eeis xiie a oiie epne o A abundanc RAA to response positive a exhibited enemies natural all expected, As Hymenoptera parasitoids were very rare in both year and in all orchards. The ratio of of ratio The orchards. all in and year both in rare very were parasitoids Hymenoptera mummies to the aphid number was much lower (always less than 0.2% in all years all in 0.2% than less (always lower much was number aphid the to mummies abundance was concomitant to the increase of RAA population whereas in 2015, the natural the 2015, in whereas population RAA of increase the to concomitant was abundance hs rsls r cnitn wt toe f rvos tde (iar e al et (Miñarro studies previous of those with consistent are results These oee, h snhoiain ewe te A ad aua eey yais varied dynamics enemy natural and RAA the between synchronization the However, in previous surveys conducted in organic apple orchards ( abundance was at its lowest level when the RAA infestation was highest (Fig. 2). (Fig. highest was infestation when RAA the level lowest was its at abundance studied years. The lowest RAA infestation level was observed in 2014, when RAA when 2014, in observed was level infestation RAA lowest The years. studied al Similarly, the presence probability, logarithm of the area under the curve and presence durat presence and of the area the curve under logarithm probability, presence the Similarly, et alet dynamics appeared to be the most synchronized. Indeed, in 2014, the increase of natural natural of increase the 2014, in Indeed, synchronized. most the be to appeared dynamics abundant abundant groups of enemies, natural with Syrphidae being generally present earlier responded positively to RAA abundance, which was expected considering the the considering expected was which abundance, RAA to positively responded Weisser 2000, Stewart-Jones et al 2000, Stewart-Jones Weisser Staphylinidae, (Bryan and Wratten 1984) or for Syrphidae (Tenhumberg and Poehling 1995, Miñarr 1995, and Poehling Syrphidae (Tenhumberg or for 1984) Wratten and (Bryan Staphylinidae, practices and agroecological infrastructures, suggesting that environmental and agronomical agronomical and environmental that suggesting infrastructures, agroecological and practices between probability of presence (Coccinellidae, Araneae) or in both their probability of both of or in their Araneae) probability of probability presence (Coccinellidae, parasitism inparasitism RAA(Miñarro et colonies al parasitoids as evidenced in previous studies (Völkl 1992, Stewart-Jones et al Stewart-Jones 1992, (Völkl studies previous in evidenced as parasitoids eades f h ya ad rhr, ypia ad ocnlia wr consi were Coccinellidae and Syrphidae orchard, and year the of Regardless components. dynamics the population of all on influence a similar had Srhde Friuia) Ti i nt upiig a ntrl nme freque enemies natural as surprising, not is This Forficulidae). (Syrphidae, observed observed in our study could result from the high sensitivity of the hy hr pes r audn. n at peiu suis hwd ht t s h cs fr Car for case the is it that showed studies previous fact, In abundant. are preys where (Theiling and Croft 1988). Another explanation could be an antagonist effect effect antagonist an be could explanation Another 1988). Croft and (Theiling . 2005). 2005). Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological . 1987: 3.3%). However, other studies similarly reported the absence or a very a or absence the reported similarly studies other However, 3.3%). 1987: Structuration of the Arthropod Community Community Arthropod the of Structuration D. plantaginea plantaginea D. and the two species of ants observed ( observed ants of species two the and Comment citer cedocument: . 2008). 2008).

. Brown2005, and The lowMathews 2007). level of parasitism Dib et et al Lasius niger Lasius . 2010: up to 6.9%; Cruz de Boelpaepe menoptera parasitoid to menoptera insecticides L., L., . . presence abundance and presence 2008). 2008). ty grgt i places in aggregate ntly 05 Db t al et Dib 2005, Formica stently the two most most two the stently

and orchards) than than orchards) and and natural enemy enemy natural and mutualistic relation relation mutualistic than than Coccinellidae. between ants and and ants between low abundance of abundance low e either in their their in either e sp.) (Flatt and and (Flatt sp.) the number of number the between the the between abidae and and abidae ion of ants of ion practices practices . enemy 2010). 2010). enemy enemy o

11 et et Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 309 309 306 306 305 304 303 302 310 310 308 308 307 307 311 311 301 301 312 312 300 300 313 313 314 314 319 319 318 318 329 329 327 327 315 315 320 320 328 328 316 316 326 326 323 323 322 321 317 317 324 324 325 325 As As expected, we observed a decrease in the probability and duration of RAA pres A strong impact of the cultivar was observed in our study and its effect varied whet varied effect its and study our in observed was cultivar the of impact strong A ned ahd ae oe unrbe o netcds n h frt hs o coloniz of phase first the in insecticides to vulnerable more are aphids Indeed, ants. and enemies reduction of the colonization success and hence on the presence probability. The aphi The probability. presence the on hence and success colonization the of reduction 3 and Appendix A). Such an effect is especially expected in leaf-curli of of the further decreases while the colony size increases because the rolling-up of of rolling-up the because increases size colony the while decreases further be o nls te iet fet o fre patcs n areooia infrastruc agroecological and practices farmer of effects direct the analyse to able rtcin gis isciie (rs e al et (Cross insecticides against protection include RAA abundance as a factor in the models (through the the (through models the in factor a as abundance RAA include natural natural enemies might further reduce aphid biological control. A negative effect ins of was observed on the presence probability of of probability presence the on observed was more more strongly the natural enemies than aphids. High development of of development This dependence of ant and natural enemy abundances on RAA abundance supported our our supported abundance RAA on abundances enemy natural and ant of dependence This the highest presence probability and presence duration of RAA and natural enemies ( enemies natural and RAA of duration presence and probability presence highest the fet a sgiiat n h peec poaiiy f ypia lra, of larvae, Syrphidae of probability presence the on significant was effect infested trees, suggesting that insecticide treatments also negatively impact the ant thepopulation ant impact also negatively treatments insecticide that suggesting trees, infested by Judor. Fo ocnlia eg, s el s n h Friuia audne n o Aaee presen Araneae on and abundance Forficulidae the on as well as eggs, Coccinellidae probability, abundance and presence duration of RAA and natural enemies). Douce de l’ de Douce enemies). natural and RAA of duration presence and abundance probability,

netcd tetet apid al i te esn em o e h ms efcet t efficient most the be to seem season the in early applied treatments Insecticide the presence probability and the presence duration of RAA and natural enemies or the a the or enemies natural and RAA of duration presence the and probability presence the RAA and natural enemies (except for the Dabinett cultivar, which always exhibited the lowest p the lowest which always exhibited the (exceptDabinett cultivar, for enemies RAA natural and Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological EIQ Impact of Insecticides on RAA and Natural Enemy Population Dynamics Dynamics Population Enemy Natural and RAA on of Insecticides Impact Influence and Cultivar Practices Effect of Cultivar on RAA and Natural Enemy Population Dynamics Dynamics Population Enemy Natural and RAA on of Cultivar Effect field r r the RAA, this ranking matches cultivars ranked according to precocity. Dou

use rating D. plantaginea plantaginea D. , , but the Comment citer cedocument: EIQ field colonies. Insecticide applications after the leaf curling, would impact impact would curling, leaf the after applications Insecticide colonies.

use use rating

effect on RAA abundance ( . 07. oevr te eaie fet f netcds on insecticides of effect negative the Moreover, 2007). allNE EIQ and on their abundance ( abundance their on and field

use use rating logAUC also reduced ant abundance in RAA- ng ng aphids, such as logAUC of RAA). In this way, we were were we way, this In RAA). of ) ) was not significant (Table leaves provides them with with them provides leaves Syrphidae eggs and of of and eggs Syrphidae logAUC ence ence with an increase ation, resulting in a a in resulting ation, ecticide ecticide treatments her we considered considered we her tures on natural natural on tures AllNE ). This negative negative This ). D. plantaginea ce ce de l’Avent d vulnerability vulnerability d o control the the control o Avent bundance of of bundance ce duration. duration. ce ), followed followed ), choice to to choice . . resence resence cov had had 12 cov . .

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 352 352 353 353 342 342 354 354 351 351 336 336 348 348 343 343 355 355 340 340 339 338 337 349 349 344 344 356 356 341 341 333 333 358 358 350 350 345 345 335 335 347 347 334 334 359 359 357 357 346 346 332 332 330 330 331 331 presence on cherry trees, but Armbrecht and Perfecto (2003) reported a dramatic decrease of decrease dramatic a reported (2003) Perfecto and Armbrecht but trees, cherry on presence nesting ants with an increase in the distance to forest fragments in coffee plantations in Mexico. Mexico. in plantations in coffee fragments to forest distance in the increase with an ants nesting may result from either direct effects on the RAA population dynamic population RAA the on effects direct either from result may Finally, the proximity of hedgerows may modify the arthropods interaction n interaction arthropods the modify may hedgerows of proximity the Finally, tt ad nln (01 fud o fet f woy aia i te surrounding the in habitat woody a of effect no found (2011) Entling and Stutz utvr Due e l’Avent de (Douce cultivar Hedgerows may also indirectly favour aphids by favouring mutualistic ants ants mutualistic favouring by aphids favour indirectly also may Hedgerows influence on mutualistic or antagonist arthropods, or both. The vicinity of the hedge the of vicinity The both. or arthropods, antagonist or mutualistic on influence presence of a hedgerow could reduce RAA biocontrol by increasing the intra-gui the increasing by biocontrol RAA reduce could hedgerow a of presence Unexpectedly, Unexpectedly, hedgerows appeared to be consistently beneficial to RAA populations season. the throughout enemies natural and aphids both of abundances utbe etn hbtt Ide, h at rsne rbblt icesd ih h proximi the with increased probability presence ant the Indeed, habitat. nesting suitable h lgtbhvoro rhoosb oiyn h idsedadtruecs ( turbulences and speed wind the modifying by arthropods of behaviour flight the aua eeis Sru e al et (Straub enemies natural proximity proximity had a positive impact on all of the RAA population dynamics considered, switching between cultivars: Judor had the higher abundance of RAA and and RAA of abundance higher the had Judor cultivars: between switching considered, presence of ants is higher in the hedgerow vicinity, the protection they provide to to provide they protection the vicinity, hedgerow the in higher is ants of presence hedgerow hedgerow in our study. To our knowledge, very studies have few assessed could result in the accumulation of insects on the leeward side of the hedgerow ( hedgerow the of side leeward the on insects of accumulation the in result could interaction between the colonization rate and treatment frequency. In fact, the most he most the fact, In frequency. treatment and rate colonization the between interaction the vicinity of hedgerows. hedgerows. of vicinity the nme ( enemies alternative prey (Kozar et alet (Kozar prey alternative et alet dfeet utvr akn ws band hn h audne f A ad aua en natural and RAA of abundance the when obtained was ranking cultivar different a was was the cultivar, withby followed precocious latest Judor, most being the Dabinett cul Dapena, (2007) Dapena, still (2007) that wereapple cultivars showed early-leafing infested more and dam than late-leafing ones. We can operates process for enem natural the ones. suppose than that same late-leafing We Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological . 2008). Such an effect could result in a higher colonization rate by RAA of RAA by rate colonization higher a in result could effect an Such 2008). Hedgerows Favour RAA Populations Populations RAAFavour Hedgerows AllNE ), followed by Douce de l’Avent de Douce by followed ), Comment citer cedocument:

cov . 1994, Koss and Snyder 2005, Symondson et alet Symondson 2005, Snyder and Koss 1994, ) was also the earliest one treated with insecticides, resulting in low low in resulting insecticides, with treated one earliest the also was ) . 2008) or by diverting natural enemies from pests by offering them them offering by pests from enemies natural diverting by or 2008)

cov Ti aprn icnitny ol eutfo an from result could inconsistency apparent This . parameters. This hedgerow effect s, from indirect effects through its its through effects indirect from s, hedgerow hedgerow influence on ants. . etwork. For instance, the the instance, For etwork. 2006). Moreover, as the as Moreover, 2006). possibly by providing a a providing by possibly apple trees situated in in situated trees apple Lewis 1965, Grüebler Grüebler 1965, Lewis ld predation between between predation ld Pasek 1988), which 1988), Pasek landscape on ant ant on landscape . Indeed, hedgerow row may influence influence may row RAA against their their against RAA tivar. Miñarro and and Miñarro tivar. avily colonized colonized avily ies. However, aged by RAA me was emies of natural natural of ty to the the to ty

twig- 13 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 380 380 381 381 383 383 382 382 384 384 379 379 389 389 388 387 386 385 377 377 378 378 376 376 373 373 372 372 374 374 360 360 367 367 375 375 361 361 371 371 368 368 362 362 369 369 366 366 365 364 363 370 370 applying artificial sugar sources in in apple a sources reduction orchards sugar applying resulted artificial D. plantaginea that extrafloral nectar was more attractive to ants than aphid honeydew. In total, our resul sugar sugar resources, flower strips could distract ants aphid from attendance. Kata flower strips are beneficial to natural enemies and reduce ant attendance that could acc could that attendance ant reduce and enemies natural to beneficial are strips flower mlfe b ter eaie fet n h at rsne rbblt. ay t al et Nagy probability. presence ant the on effect negative their by amplified strips. of reduction observed that floral resources enhanced aphid suppression by the hoverfly hoverfly the by suppression aphid enhanced resources floral that lettuce field. In addition, the negative influence of flower strips on aphid populations populations aphid on strips flower of influence negative the addition, In field. lettuce enemies enemies could enhance aphid biological control in the vicinity of f flower flower strips. More specifically, the presence probability and abundance of Syrphid natural enemies could be enhanced. Contrary to previous studies (Altieri and Sc and (Altieri studies previous to Contrary enhanced. be could enemies natural the abundance ( abundance the rsne rbblt o Ccielde eg ad ave ad bnac o Forficuli of abundance and larvae) and (eggs Coccinellidae of probability presence and Prida 2013), few hedgerow-distance effects on natural enemy occurrence or or occurrence enemy natural on effects hedgerow-distance few 2013), Prida and the presence probability, the abundance and the presence duration of RAA all decrea all RAA of duration presence the and abundance the probability, presence the significantly with the distance with significantly theto distance flower This increase of strips. and/or presence oois ee on i or td. h ol sgiiat fet wr te decre the were effects significant only The study. our in found were colonies an increase in natural enemy abundance Coccinellidae, (Chrysopidae, Araneae). Si strips strips proximity. A direct effect of flower strips on aphids was very unli probability and of the presence duration of Coccinellidae larvae and the increase of of increase the and larvae Coccinellidae of duration presence the of and probability strips exerted an indirect effect through their influence on the natural enemies and/or and/or enemies natural the on influence their through effect indirect an exerted strips Contrary to hedgerows, flower strips had a negative impact on the RAA populations hedgerow. the of vicinity in the eggs Syrphidae and larvae Syrphidae of duration Wyss, alet (1995) Wyss, and Wyss Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Flower Strips Reduce RAA Populations and Increase Natural Enemy Abundance Abundance Enemy Natural Increase and Populations RAA Strips Reduce Flower colonies and in an increase in natural enemy pressure. Similarly, by providi logAUC . plantagineaD. ) and presence duration of natural enemies ( enemies natural of duration presence and ) Comment citer cedocument: . (1995) showed that introducing flower strips in apple orchards resulted in resulted in orchards strips flower apple introducing that showed (1995) infestation in cider-apple trees located in the vicinity of flower flower of vicinity the in located trees cider-apple in infestation

Conclusion lower lower strips. Hogg et al Eupeodes fumipennis Eupeodes kely. kely. thenWe assumed that flower allNE of the number of ant-attended of ant-attended number of the ) increased in proximity to to proximity in increased ) yama yama et al of abundance abundance of natural of . (2013) showed that that showed (2013) ase of the presence presence the of ase ae ae (eggs larvae), and in our study. Indeed, hmidt 1986, Miñarro Miñarro 1986, hmidt abundance in aphid aphid in abundance milarly, milarly, in our study, on ants. Indeed, Indeed, ants. on . . dae decreased decreased dae sed with flower flower with sed (2013) showed (2011) showed in a California California a in ts ts suggest that could also be be also could the presence presence the ng alternative ount for the for ount 14 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin 404 404 400 400 395 395 412 412 408 408 407 406 405 415 415 401 401 396 396 416 416 417 417 413 413 409 409 403 403 402 393 393 399 399 398 397 410 410 411 411 394 394 414 414 392 392 390 390 391 391 plantaginea project (ANR-12-AGRO- project orchards. We thank Sylvaine for her orchards. Simon help of in characterization agro the We enemy abundance and a decrease of ant presence in the RAA colony. Additionall colony. RAA the in presence ant of decrease a and abundance enemy within within a forest fragment and neighboring coffee plantations of contrasting habitat quali lir, . . ad . . cmd. 1986 Schmidt. L. L. and A., M. Altieri, We We thank two anonymous reviewers for their useful on comments a previous version strong influence of cultivars and of insecticide use intensity on intensity use insecticide of and cultivars of influence strong Scientific Symposium Symposium Scientific Ecosyst. Environ., 97(1): 107 97(1): Environ., Ecosyst. interface interface of abandoned, organic and commercial apple orchards and adjacent woodl l’Agriculture, de l’agroalimentaire et de la forêt (CASDAR). (CASDAR). forêt la de et l’agroalimentaire de l’Agriculture, The work andwas Normandie de Ministère ANRT, by UNICID, Région Bretagne, the supported Région aua eey bnac i te iiiy f egrw O te otay foe s flower contrary, the On hedgerow. of vicinity the in abundance enemy natural We thank A. Taillade and A. Quero for data collection and the farmers who allo who farmers the and collection data for Quero A. and Taillade A. thank We Ecosyst. Environ., 16(1): 29 16(1): Environ., Ecosyst. Armbrecht, I., and I. Perfecto. 2003 Perfecto. I. and I., Armbrecht, unfavourable to to unfavourable Arnaudov, Arnaudov, V., S. Raikov, R. Davidova, and H. Hristov. 2013 Indeed, our results showed an increase in the presence of mutualistic ants and a de a and ants mutualistic of presence the in increase an showed results our Indeed, hs td soe a ipc o te itne o goclgcl nrsrcue on infrastructures agroecological to distance the of impact an showed study This yaisi ie-pl rhrs egrw icesdteRA infestation RAA the increased Hedgerows orchards. cider-apple in dynamics rm n niet fet u t mdfctos n h RA neatos network interactions RAA the in modifications to due effect indirect an from Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Ps. (ootr, piia) n ugra ape rhrs I: orh Internat Fourth In: orchards. apple bulgarian in Aphididae) (Homoptera, Pass., ) D. plantaginea D. “ Agrosym 2013Agrosym 0006) and to the “Verger Cidricole de Demain” CASDAR project. CASDAR Demain” de Cidricole the to “Verger and 0006) Comment citer cedocument: ̻ 43. 43. ̻ 115. 115. . Again it could result from indirect effect due to an increase in increase an to due effect indirect from result could it Again . . Litter-twig dwelling ant species richness and predation potential potential predation and richness species ant dwelling Litter-twig . ” 268:

Acknowledgments Acknowledgments References Cited Te yais f ooiig rhoo cmuiis t the at communities arthropod colonizing of dynamics The . ̻ 274. 274. . Predators of rosy apple aphyd ( This project is linked to the PEERLESS PEERLESS the to linked is project This D. plantaginea dynamics. dynamics. ecological infrastructure. infrastructure. ecological level. This could result result could This level. with other arthropods. arthropods. other with wed us to access their their access to us wed and habitats. Agric. Agric. and habitats. of this manuscript. ty in Mexico. Agric. y, we confirmed a confirmed we y, trips appeared appeared trips . plantagineaD. crease in RAA RAA in crease

Dysaphis Dysaphis natural natural ional ional 15

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Adalia bipunctataAdalia . Costs and benefits of ant attendance to the drepanosiphid drepanosiphid the to attendance ant of benefits and Costs . ̻ 10. 10. , on the abundance of the rosy apple aphid, aphid, apple the rosy of abundance the on , . Effects of augmentative releases ̻ 173. 173. 23 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3), 528-537 . DOI : 10.1093/ee/nvx054 Infrastructures on the Dynamics of Dysaphis plantaginea (Hemiptera: Aphididae) and ItsNatural Enemies in insecticides used in each orchard each year ineach ( each orchard used insecticides during applied of each Quotient insecticide Environmental Impact The (EIQ) Table 1: Main characteristics of the 14 studied cider-apple orchards. orchards. cider-apple studied 14 the of characteristics Main 1: Table TABLE

(referred (referred by number). In each orchard, 3 cider-apple cultivars were planted EIQ EIQ Number ofmonitored trees (plantingdistance between in (for each in(for apple each in(for apple Albert, L.,Franck, P., Gilles, Plantegenest, M.(2017). Impact of Agroecological rows*plantingdistance bynumber oftrees/ha field field Densityofplanting cultivar) cultivar) Yearofplanting

userating userating withinrows) Location Orchard 2015 2014 DDA DDA DDA DAB DAB DAB JUD JUD

Comment citercedocument : (5.5*2.3) 2010 2010 0.67 0.67 0.67 0.61 0.61 0.61 198 774 1a 1a 1 (5.5*2.3)

2010 2010 6.61 6.61 6.61 6.61 5.58 5.58 5.58 198 774 1b 1b EIQ (6.5*3) 2012 2012 field field use rating 153 495 2a 2a 0 0 0 0 0 0 2 (5.5*2.3) 2012 2012 1.20 1.20 1.20 153 774 ). *: only 63 trees monitored in 2014; **:only 425 trees monitored in 2014. *: ). in only 425 in 63 monitored 2014. monitored trees trees 2014; **:only 2b 2b 0 0 0 (5.5*2.3) 2011 2011 0.35 0.35 0.35 162 774 3a 3a 0 0 0 (DDA = 3 Two contiguous orchards (referred by (referred orchards contiguous Two (5.5*2.3) the onthe presence RAA to used the toxicity apple the was cumulative trees assess 2011 2011 2.80 1.60 2.80 0.35 0.35 0.35 162 774 3b 3b Douce Douce de l’Avent (6.5*3) 2012 2012 117* 495 4a 4a 0 0 0 0 0 0 4 (5.5*2.3) 2012 2012 117* 1.16 1.16 1.16 774 4b 4b 0 0 0 cov cultivar, DAB = Dabinett cultivar and JUD= Judor cultivar). (5.3*2) 0.087 0.087 0.087 1000 1000 2011 234 NA NA NA 5a 5a 5 (5.3*2) 1000 1000 2011 a 0.33 0.33 0.33 234 NA NA NA 5b 5b or b ) have been monitored in each location location each in monitored been have ) (5.5*2,3) 2011 2011 279 774 NA NA NA 6a 6a 0 0 0 6 (5.5*2.3) 2011 2011 4.67 6.81 6.61 NA means Not means Applicable. NA 279 774 NA NA NA 6b 6b (5.5*2.3) 270** 2010 2010 774 7a 7a 0 0 0 0 0 0 7 (5.5*2.3) 270** 2010 2010 0.35 0.24 2.09 0.29 0.35 774 7b 7b 0 24 of Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3), 528-537 . DOI : 10.1093/ee/nvx054 Infrastructures on the Dynamics of Dysaphis plantaginea (Hemiptera: Aphididae) and ItsNatural Enemies in

trees tothetrees closest tothetrees closest flowerstrip(in m) (accordingtothe (accordingtothe (+SD)oforchard (+SD)oforchard hedgerow m) (in Albert, L.,Franck, P., Gilles, Plantegenest, M.(2017). Impact of Agroecological Meandistance Meandistance year) year) 2015 2015 2014 2015 2014 Comment citercedocument : 0 (0) 0(0) 0(0) (7.2) (7.2) (7.2) 16.9 16.0

(14.2) (11.8) (11.8) (14.2) 21.3 21.3 21.3 34.5 34.5 (12.9) (12.9) 23.9 23.9 (0) (0) (0) (0) 0 0

(10.4) (11.3) (11.3) (10.4) 20.7 38.9 38.9 20.7 (11.0) (11.0) 21.3 21.3 (0) (0) (0) (0) 1 1

(11.0) (12.0) (12.0) (11.0) 21.3 43.6 43.6 21.3 (10.4) (6.0) (6.0) 15.5 20.8 (0) (0) (0) (0) 2 2

(4.64) (8.6) (8.6) (4.6) (8.2) (8.2) 13.8 31.8 24.9 18.3 (6.6) (6.6) (6.2) 14.3 10.8 NA NA (12.9) (6.5) (6.5) 15.2 27.0 NA NA (14.1) (6.9) (6.9) 27.6 27.6 11.9 NA NA

(14.1) (14.8) 27.6 36.9 NA NA

(12.7) (11.3) 23.7 21.5 1.5 1.5 (0) (0) (0) (0)

(12.7) (12.9) (11.9) (13.2) 23.7 28.1 33.4 39.8 25 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin tree per observation in one studied orchard) by taxonomic group, life stage and year. year. and stage life group, taxonomic by orchard) studied inone observation tree per

Table 2 Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Coleoptera Hemiptera Diptera Order Family Life stage Life Family Order : Total number observations number Total of (date*orchard) Total Total number of observed arthropods (and range of mean the number f

Number of studied of orchards Number Coccinellidae Anthocoridae Cantharidae Syrphidae Nabidae Miridae Comment citer cedocument:

Larvae Larvae Adults Adults Adults Eggs Eggs All All - - -

(from 1.0^(from 5.6^(from (from 6.6^(from (from 6.3^(from (from 0 to (from 1.0^- (from 0 to (from 2.4^- 0 to (from 1.2^- 0 to (from 4.5^- 0 to (from 1.2^- 0 to 2.7^- (from 0 to (from 4.7^- (6.3^- (from 5 to (from 10) 1083 1083 2014 1500 1500 3 to 0.79) to 3 408 739 141 533 35 10 67 37 34 17 65 2) 9 9 -2 to to -2 - - -

2 to 0.50) to 2 2 to 0.71) to 2 3 to 8.8^- to 3

0.47) 2) 1) 2) 2) 2) 1) 1)

Year (from 3.0^-(from (from 2.9^-(from (from 6.0^-(from (from 0 to (from 5.3^-2) (from 0 to (from 1.7^-1) 0 to (from 5.0^-2) 0 to (from 4.1^-2) 0 to (from 3.8^-1) 0 to (from 3.8^-1) (from 0 to (from 6.4) 0 to (from 5.2) (from 5 to (from 11) (from 0 to (from 0) or one monitored 1122 1122 2015 1829 1829 1325 1602 429 114 161 343 92 51 57 14 68 0 0

2 to 0.51) to 2 2 to 1.7) to 2 2 to 2.3) to 2

26 2568 2568 1858 3103 2205 Total 153 126 226 484 838 103 67 85 60

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin

enemies Number RAA of Number Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Ratio (Ratio

Hymenoptera Dermaptera Neuroptera Araneae AllNE AllNE Total number of observations (date*orchard) observations number Total of Ants natural

per RAA)per

Number studied of Number orchards

Chrysopidae Forficulidae Comment citer cedocument:

Juveniles+Adults Juveniles+adults

Mummies Larvae Adults Adults Eggs All All

(from 5.0^(from (from 2.4^(from (from 0.77 0.77 95.5)to (from (from 0.10 0.10 1.45) to (from (from 0 to (from 1.2^- 0 to (from 1.2^- (from 0 to (from 6.5^- 0 to (from 3.2^- 0 to (from 3.2^- (from 0 to (from 0.36) (from 0 to (from 0.16) (from 5 to (from 10) (from 0 to (from 0) 0 to (from 0) 206195 0.016 0.016 2014 2014 9279 9279 3326 582 296 35 10 45 12 33 9 9 0 0 9 -

- 4 to 0.18) to 4 2 to 3.8) to 2

2) 2) 2) 2) 2) 2) 2)

Year (from 2.4^-(from 2.9^-(from (from 21.0 21.0 182.4)to (from (from 4.7^-(from (from 0.30 0.30 7.4)to (from (from 0 to (from 6.0^-3) 0 to (from 2.3^-3) 0 to (from 6.0^-3) (from 0 to (from 5.7^-2) 0 to (from 1.9^-2) (from 0 to (from 0.16) (from 0 5.4^-2)(from (from 5 to (from 11) (from 0 to (from 0) 554230 15578 15578 0.009 0.009 2015 2015 5025 5025 742 440 133 108 57 14 25 5 5 3 2 0

3 to 0.21) to 3 0.60) to 3 2 to 7.1) to 2

27 760425 0.0109 24857 24857 8355 8355 1324 Total 737 178 141 103 37 14 3 2 9

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin

( PA Distance the to Distance the to Distance EIQ closest flower closest hedgerow / logAUC Cultivar closest closest field RAA strip strip

Table 3: significantly influence the variable. NA: not applicable. See Appendix A for detail. A for Appendix See applicable. not NA: variable. the influence significantly aibe ( variable infrastructure. For the cultivar factor factor cultivar the For infrastructure. (resp. (resp. “ For arthropods. considered the to unfavourable) (resp. favourable is factor the that

use ratinguse Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological / PD

- ) “) “) indicates that the arthropods are more (resp. less) present in the vicinity

Synthetic Synthetic overview of the Generalized Linear Mixed models results: PA , Ü logAUC RAA / NA Ü + 0 + - 0 0 + + 0 0 - + 0 + - - - + + + + 0 - - 0 + + + + - / Ü

or or Comment citer cedocument: PD) PD) Ü o a lat n atrpd tg. idcts ht h fco dd not did factor the that indicates 0 stage. arthropod one least at for AllNE AllNE / Ü + + - - / Ü “

Ü

” means that cultivar has a significant effect on effect significant a has cultivar that means ” Syrphidae Syrphidae Ü /0/ + + - - Ü

Coccinellidae Coccinellidae Ü / Ü + + - - / Ü

Forficulidae Forficulidae Ü /0/0 “+” “+” (resp. “

+ + - - of the agroecological

the distance, a “+” a distance, the the response response the Araneae Araneae - Ü “) “) indicates /0/0 /0/0 + + - - 28 Ü Ants /0/0 + + - - Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin

dotted line with square mark) per monitored apple tree in aphid colonies in 2014 (A) and 2015 (B) 2015 and (A) 2014 in aphid colonies in tree apple per monitored mark) with square line dotted Cocc of and mark) triangle with line dotted (grey stages) (all Syrphidae of Fig. Fig. 2. in 2015. studied locations the are dots 2015. Grey and 2014 in both studied

1. Fig. FIGURE LEGENDS Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Mean number (+ SE) of RAA (black dot), of all natural enemies (grey dotted l Map of the seven studied locations (two orchards per location). Black dots are dots Black location). per orchards (two locations studied seven the of Map Comment citer cedocument:

inellidae (all stages) (grey (grey stages) (all inellidae ine ine with circle mark), the locations locations the .

29 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin

Fig. 1 Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Comment citer cedocument:

30 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin

Fig. 2 B A

Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological Comment citer cedocument:

31 Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin Appendix A: Results of Generalized Linear Models obtained for each arthropod ( arthropod each for obtained Models Linear Generalized of Results A: Appendix Appendix B: Sum of arthropods observed per orchard each studied year (2014 and (2014 year studied each orchard per observed arthropods of Sum B: Appendix a Contents [email protected] c [email protected] FRANCE, Cedex, Rennes b ALBERTLaurence France Northwestern in Orchards Apple in Enemies Natural its plantaginea Dysaphis Impact of Agroecological Infrastructures on the Dynamics of and each variable. variable. each and aphid apple with rosy infected per tree date sampling arthropods per of number [email protected]; [email protected] [email protected] [email protected]; INRA Plantes & Systèmes de culture Horticoles, F-84914 AVIGNON Cedex 9, 9, Cedex AVIGNON F-84914 Horticoles, culture de Systèmes & Plantes INRA nttt rnas e Poutos ircls L Rné Cenl 650 és F Sées, 61500 Chesnel, Rangée La Cidricoles, Productions des Français Institut M14 IEP IR/goapsOetUiest Rne 1 6 re e an Biu, 35 Brieuc, Saint de rue 65 1, Rennes INRA/Agrocampus-Ouest/Université IGEPP, UMR1349 Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological

a , Pierre FRANCK , Pierre Comment citer cedocument: Supplementary Material c Passerini (Hemiptera: Aphididae) and (Hemiptera: Passerini , Yann GILLESYann ,

a , Manuel PLANTEGENESTManuel , b

by taxon and stage) stage) and taxon by 2015) and mean mean and 2015) FRANCE, FRANCE, RANCE, RANCE, 042 042 32 Version preprint Appendix A: Results of Generalized Linear Models obtained for each arthropod (by taxon and stage) and stage) taxon (by arthropod each for obtained Models Linear Generalized of Results A: Appendix first line is the pvalue of the variable, when inferior to 0.05, the second line is second the 0.05, to inferior when variable, the of line pvalue is the first cultivar of Douce de l’Avent de Douce cultivar of DDA Dabinett, of cultivar means DAB Curve. the Under Area AUC mean Quotient. Impact Environmental means Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 Globalnatural Coccinellidae Coccinellidae plantaginea Syrphidae Syrphidae Larvae of Larvae of Dysaphis Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin enemies Eggs of Eggs of

(binomialdistribution) (binomialdistribution) (binomialdistribution) (binomialdistribution) (binomialdistribution) (binomialdistribution) (Gammadistribution) (Gammadistribution) (Gammadistribution) (Gammadistribution) (Gammadistribution) Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological (normal distribution)(normal (normal distribution)(normal distribution)(normal distribution)(normal distribution)(normal Log(AreaUnder the Log(AreaUnder the Log(AreaUnder the Log(AreaUnder the Log(AreaUnder the Log(AreaUnder the Presenceduration Presenceduration Presenceduration Presenceduration Presenceduration

Probabilityof Probabilityof Probabilityof Probabilityof Probabilityof Probabilityof presence presence presence presence presence presence Curve) Curve) Curve) Curve) Curve) Curve) cov and JUD means cultivar of Judor. Judor. of cultivar means JUD and LogAUCof *** 0.0009433 Comment citer cedocument: *** 8.057e-07*** 1.125e-07*** *** 4.961e-06 7.458e-08*** 2.894e-11*** *** < 2.2e-16< *** 2.2e-16< *** ***<2.2e-16 2.2e-16***< 2.2e-16***< NS 0.06483NS plantaginea NS 0.6864NS * 0.02581* 0.0376 0.0422 0.0535 0.122 0.285 0.219 0.117 0.286 0.122 0.185 0.194 0.277

D.

Distance the to *** 0.0001546*** *** <2.2^-16*** ** 0.005793** **0.002537 NS 0.8587NS 0.7486NS 0.1892NS 0.4274NS 0.3227NS NS 0.4644NS 0.3697 NS 0.1241NS 0.8032NS 0.8352NS ** 0.00516** hedgerow *0.04781 -0.00536 NS 0.75NS -0.0058 -0.0057 -0.0171 -0.0034 0.0162

Distance the to flower Variablesstudied *** 7.867e-16 *** 6.688e-05 *** < 2.2e-16< *** ***3.266e-06 *** 0.000528*** ** 0.001588** ** 0.002112** **0.001459 NS 0.1266NS NS 0.4144NS 0.3969NS 0.1016NS 0.4155NS the coefficient. NS means no- means NS coefficient. the * 0.03901* *0.03814 -0.00091 -0.00452 -0.00787 * 0.0366* 0.02953 -0.0029 -0.0048 -0.0078 -0.0082 -0.0044 0.0022 0.0063 0.0111 -0.011 -0.010 strips DAB

significant. EIQ significant. 33 means means *** *** 4.617e-05*** *** 8.676e-13 *** 7.166e-05 ** 0.006066** NS 0.4914NS 0.3095NS 0.8945NS 0.6054NS 0.4199NS 0.1041NS 0.2187NS 0.7999NS NS 0.294NS 0.005526 *0.03559 0.01154 -0.0586 0.0008589 0.0225 -0.364 -0.090 -0.051 -0.091 -0.019 -0.057 field usefield rating

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3),528-537 .DOI :10.1093/ee/nvx054 (Juvenilesand (Juvenilesand Coccinellidae Forficulidae Infrastructures onthe Dynamics ofDysaphis plantaginea (Hemiptera: Aphididae) andItsNatural Enemiesin Adults ofAdults Araneae adults) adults) Ants

(binomialdistribution) (binomialdistribution) (binomialdistribution) (binomialdistribution) (Gammadistribution) (Gammadistribution) (Gammadistribution) (Gammadistribution) (Gammadistribution) Albert, L., Franck,P., Gilles, Plantegenest, M.(2017). ImpactofAgroecological (normal distribution)(normal distribution)(normal (normal distribution)(normal distribution)(normal distribution)(normal Log(AreaUnder the Log(AreaUnder the Log(AreaUnder the Log(AreaUnder the Presenceduration Presenceduration Presenceduration Presenceduration Presenceduration Probabilityof Probabilityof Probabilityof Probabilityof presence presence presence presence Curve) Curve) Curve) Curve) Comment citer cedocument: *** 4.533e-12 *** 7.437e-15 *** < 2.2e-16*** < 2.2e-16*** < 2.2e-16*** < 2.2e-16*** < ** 0.001888** NS 0.1252NS 0.3479NS 0.8494NS 0.1201NS NS 0.491NS *0.03107 0.0304 0.0892 0.152 0.509 0.405 0.146 0.223 0.246

*** 0.000344 NS 0.9254NS 0.2126NS 0.1346NS 0.9295NS 0.5724NS 0.1347NS 0.6654NS NS 0.1676NS 0.5379NS 0.5216NS 0.9367NS * 0.03643* -0.0146 0.0057

** 0.005847** NS 0.1275NS 0.8388NS 0.6548NS 0.4651NS 0.7773NS NS 0.8688NS 0.8873NS 0.4528NS 0.3193NS NS 0.895NS 0.008168 -0.00534 0.04627 0.0068 -0.005 DAB

34 * * * 0.006257* * NS 0.08618NS 0.09964NS 0.07431NS ** 0.001295** **0.0006422 NS 0.2145NS 0.8418NS 0.1281NS 0.9349NS 0.2327NS 0.4131NS 0.5245NS -0.049 -0.059 -0.097

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3), 528-537 . DOI : 10.1093/ee/nvx054 Infrastructures on the Dynamics of Dysaphis plantaginea (Hemiptera: Aphididae) and ItsNatural Enemies in AppendixofSumarthropods B: observed per orchard eachstudied year (2014 and 2015 infected withinfected rosyapple aphid

Orchard

3b 3b 1b 2b 2b 3a 3a 2a 1a

Albert, L.,Franck, P., Gilles, Plantegenest, M.(2017). Impact of Agroecological

Sampling 04 810 2014 810 2014 1377 2014 1980 2014 1980 2014 2014 05 972 2015 972 2015 1683 2015 1683 2015 2574 2015 2574 2015 year

monitored tree per Sum ofSum 1377 year

Comment citercedocument : Eggs 0.13 0.05 1.79 0.06 0.02 0.19 0.09 0.50 0.04 0.29 0.43 0.26

282 234 246 148 235 294 16 19 21 13 23 43

Larvae 0.21 0.10 0.17 0.01 0.51 0.01 0.15 0.11 0.14 0.03 0.01 0.09 119 102 23 67 39 84 36 21 11 63 3 3 3 Syrphidae

Diptera

Adults 3.9^- 1.4^- 4.4^- 0.05 0 0 0 0 0 0 0 0 7 0 0 1 0 0 0 0 0 0 1 0 0 3 3 3 3

Total 0.37 2.35 0.31 0.71 0.31 0.53 0.33 0.06 0.08 0.21 0.23 0.09 309 360 348 232 401 245 53 65 44 19 22 59

Eggs 0.04 1.68 0.05 0.28 0.04 0.21 0.46 0.01 221 126 260 41 15 32 53 13 0 0 0 0 0 0 0 0 0

Larvae 2.1^- 5.3^- 3.6^- 1.4^- 0.28 0.38 0.02 0.13 0.07 125 51 51 15 35 43 Coccinellidae 0 0 0 0 0 2 0 0 5 5 1 1 1 Coleoptera

3 3 3 3

7.5^ Adults 6.7^ 8.4^ 6.3^ 5.8^ 0.02 0.01 0.01 0.01 0.28 0.02 0.01 37 37 7 7 6 6 7 5 5 9 8 4 4 4 5 5 - - - - - 3 3 3 3 3

6.3^- Total 0.02 0.01 0.05 0.08 0.06 0.37 0.01 0.02 2.35 0.59 0.55 309 258 312 53 53 22 22 52 93 10 18 4 4 5 5

3

Dermaptera Forficulidae +adults Nymph 9.1^-3 0.01 0.10 0.01 0.01 0.19 0.18 0.03 0.36 0.22 0.19 0.60 337 211 156 411 31 31 24 18 5 5 3 4 8 4 ) and meannumberand of) arthropods per sampling date per tree Mummies 2.6^-3 1.7^-3 3.2^-3 0.01 0.03 Hymenoptera 5 5 0 0 0 0 0 2 9 0 0 0 0 0 1 3 3 0 0 0 0 0 0 0 - 6.8^ 2.1^ adults 0.01 3 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 2 2 0 0 0 0 - - 3 3

Araneae Juvenile +Adults 7.0^-3 0.10 0.04 0.03 0.04 0.08 0.01 0.02 0.04 0.11 105 81 81 12 12 14 14 39 46 46 19 19 29 0 0 0 2 2 0 0 3 3 -

All NE 0.54 0.84 5.27 0.10 0.87 0.40 0.17 1.45 0.55 0.54 1.23 0.91 403 212 691 382 382 821 425 836 850 31 31 48 48 89 89 - - - 6712 2461 3915 3580 Ants 0.32 1.82 0.04 0.02 7.11 3.14 5.77 3.85 1.21 0.07 0.60 0.35 245 239 528 342 12 12 20 20 57 57 7 7 -

Number 53,95% 13,47% 14,91% 35,18% 36,63% 39,54% 26,34% 46,91% 25,90% 33,82% 40,95% 16,56% of tree with RAA 743 131 251 285 943 783 678 929 436 274 564 161

infected Number per tree 158824 123724 by RAA 182.48 of RAA 22047 57232 32682 20977 16194 29953 62291 168.2 131.2 43.98 28.71 168.4 38.25 67.05 8388 0.95 0.77 83.5 52.0 263 222 35

NE/RAA 6.6^-3 2.4^-3 6.7^-3 Ratio 0.03 0.18 0.01 0.01 0.05 0.01 0.01 0.01 0.13

Version preprint Apple Orchards in Northwestern France. Environmental Entomology, 46 (3), 528-537 . DOI : 10.1093/ee/nvx054 Infrastructures on the Dynamics of Dysaphis plantaginea (Hemiptera: Aphididae) and ItsNatural Enemies in

4b 4b 7b 7b 2790 2015 2574 6b 2015 5b 4a 4a 7a 7a 2790 2015 2574 6a 2015 5a Albert, L.,Franck, P., Gilles, Plantegenest, M.(2017). Impact of Agroecological 04 378 2014 378 2014 04 1875 2014 1875 2014 05 2700 2015 2700 2015 819 2015 819 2015 Comment citercedocument : 0.07 0.12 0.17 0.17 0.12 0.05 0.19 0.10 0.35 0.16 0.65 0.03 206 109 11 47 58 26 24 28 34 6 6 8 8 8 8

0.11 0.09 0.08 0.45 0.03 0.06 0.04 0.09 0.02 0.03 0.11 24 33 18 42 13 66 52 2 2 9 0 0 0 5 2

6.7^- 3.8^- 2.8^- 6.9^- 0.019 0.01 0.02 0.10 0.05 0.01 11 11 7 7 4 1 0 0 1 0 0 1 1 6 1 3 6 6 3 3 3 3

0.26 0.15 0.44 0.22 0.24 0.54 0.03 0.09 0.65 0.19 0.71 0.18 279 165 34 37 93 81 50 51 14 40 13 15

0.025 0.10 5.58 0.47 4.75 0.24 0.24 0.25 0.20 108 441 247 27 32 19 85 24 89 0 0 0 0 0 0 0

3.9^- 1.9^- 9.3^- 0.06 0.44 0.23 0.28 0.26 0.03 0.27 72 72 35 16 15 21 12 12 26 0 0 0 0 0 1 2 2 4 4 3 3 3

5.7^ 3.9^ 0.024 0.088 0.025 0.05 0.02 0.04 0.39 0.38 27 27 31 20 11 11 6 6 6 4 8 8 4 1 0 0 0 0 0 - - 3 3

7.8^- 0.03 0.79 0.55 0.58 0.12 6.41 5.43 0.29 0.24 136 507 282 105 104 33 33 54 44 54 54 0 0 0 0 0 2

3

8.5^-3 3.9^-3 2.3^-3 0.05 0.07 0.10 0.01 0.10 0.01 0.12 17 17 15 13 13 43 43 9 9 0 0 7 1 0 0 1 1 1 1 2.3^-3 0.03 0.01 0.01 0.02 0.03 0.05 0.05 24 24 11 11 57 57 20 20 0 0 0 1 0 0 0 0 0 0 0 0 3 3 1 1 1 9.1^ 8.4^ 4.7^ 2.8^ 0.03 0.01 0.01 0.01 0 0 0 3 3 3 3 3 3 0 0 0 1 0 0 0 0 0 5 5 3 3 3 3 3 3 - - - - 3 3 3 3

0.16 0.02 0.01 0.03 0.03 0.01 0.16 0.08 0.01 0.16 0.09 0.11 117 70 70 13 13 41 41 99 7 7 5 7 3 1 6 6 1 1 0.57 0.37 0.75 1.23 6.80 0.36 1.16 7.43 1.35 0.62 0.30 0.35 245 122 267 115 354 587 651 368 76 76 92 92 92 92 79 79 1251 1.49 1.88 2.07 2.81 0.90 0.02 1.19 1.01 0.04 3.13 0.54 641 619 733 262 187 845 570 80 80 0 0 0 2 2 3 3

15,37% 12,18% 18,82% 20,89% 17,98% 40,71% 40,55% 6.34% 4,96% 9.64% 7.66% 9.13% 1048 1044 429 329 353 207 255 52 52 93 93 79 79 79 79 68 68

26913 17173 10105 16913 20844 61721 23252 81.80 48.64 48.81 66.32 48.58 58.89 22.27 21.02 19.25 30.51 8889 1661 1309 1629 2411 95.5 31.3 36

4.5^-3 7.5^-3 4.6^-3 0.01 0.01 0.01 0.01 0.01 0.35 0.07 0.21 0.03