Higher aphid infestation in the alleys of organic apple orchards compared to IPM during fruit setting in eastern Germany

Higher aphid infestation in the alleys of organic apple orchards compared to IPM during fruit setting in eastern Germany | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Higher aphid infestation in the alleys of organic apple orchards compared to IPM during fruit setting in eastern Germany Ingrid Aline Bapfubusa Niyibizi, Benjamin Schnerch, El Aziz Djoudi, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5783229/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Apple is a major fruit crop worldwide and the most produced fruit in Germany. However, apple orchards face persistent threats from aphid infestations, which can severely compromise fruit yields. In this study we compared aphid infestation levels in commercial apple orchards under organic and Integrated Pest Management (IPM) at three stages of the apple growing season: fruit-setting, fruit-growing and post-harvest, and in two habitats. We sampled eight organic and eight IPM apple orchards in eastern Germany using standardised canopy beating of apple trees and suction sampling in the orchard alleys. Our results indicate no significant differences in canopy aphid infestation between organic and IPM orchards. However, aphid communities in the tree canopy of organic orchards exhibited greater evenness across species compared to IPM orchards. Eriosoma lanigerum consistently dominated the aphid community of the tree canopies in both management systems, highlighting the need for targeted management practices for this pest. Aphid community structure varied significantly across sampling periods in the canopy and orchard alleys. Differences between organic and IPM orchards were observed during the fruit-setting phase in orchard alleys, with higher levels of infestation in organic orchards. Species such as Macrosiphum euphorbiae , Dysaphis spp., Aphis spiraecola , and Rhopalosiphum insertum contributed to these differences. Our findings provide a better understanding of the temporal dynamics of aphid communities in commercial apple orchards and highlight the importance of pest management strategies that consider different habitats and periods. Agricultural pest Aphidoidea Apple production Habitats Seasonality Species composition Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Introduction Around 60 phytophagous arthropod species are considered pests of apples in Europe, with aphids being one of the economically most important pest groups in orchards (Jenser et al. 1999 ). Aphids are particularly problematic due to their high reproductive rates and ability to cause extensive damage to fruit trees (Blommers et al. 2004 ; Dedryver et al. 2010 ). More than 20 aphid species have been recorded feeding on apples in Europe, but only six are considered harmful to apple production: the rosy apple aphid ( Dysaphis plantaginea Passerini) and the rosy leaf curling aphid ( Dysaphis devecta Walker) from the Dysaphis genus, the woolly apple aphid ( Eriosoma lanigerum Hausmann), the green apple aphid ( Aphis pomi De Geer), the apple-grass aphid ( Rhopalosiphum insertum Walker), and the polyphagous spirea aphid ( Aphis spiraecola Patch) (Hullé et al. 2006 ; Rousselin et al. 2017 ). Infestations by major apple aphid pests are often linked to specific phenological stages of apple trees (Miñarro and Dapena, 2007; Simon et al., 2011). Moreover, aphid populations show seasonal fluctuations, with population peaks influenced by environmental conditions, species interactions and the species composition of the local aphid community (Andreev et al., 2007 ; Dib et al., 2010 ; Nagy et al., 2013 ). Aphids have piercing-sucking mouthparts consisting of long, flexible, perforating stylets that allow them to penetrate plant tissues and reach the sieve tube bundles of the phloem, from which they extract the elaborated sap (Will et al. 2013 ). This feeding behaviour causes severe leaf curling and deformation to their host plant, leading to reduced photosynthesis, stunted growth, gall formation, secondary infection by fungal pathogens, premature fruit drop, reduced fruit size, and poor yields (Brown et al. 1995 ; De Berardinis et al. 1994 ; Graf et al. 1985 ). Infested trees often produce apple fruits that are unsuitable for the fresh fruit market (Alhmedi et al. 2022 ). Without adequate pest management measures for example, the species D. plantaginea can be responsible for up to 80% damage in commercial apple orchards (Qubbaj et al. 2005 ). Management of aphid pests is critical in apple orchards due to their very low abundance threshold to cause economic damage, resulting in a correspondingly low treatment threshold, which requires prompt pesticide application under integrated pest management (IPM) once aphids are detected (Barbagallo et al. 2007 ). European apple orchards typically receive 5–15 insecticide applications per year, making apples one of the most treated fruit crops in the region (Cross et al. 2007 ). Due to concerns about the risks associated with pesticide use and the growing public demand for environmentally friendly food products, there has been an increasing interest in developing sustainable solutions for pest control in the past decades (Bostanian et al. 2004 ). Consequently, aphids in commercial apple orchards in the European Union (EU) are typically managed using either organic or IPM practices (Dib et al. 2016 ). Integrated pest management is an important part of the concept of integrated production in apple orchards, which is defined as a production system that uses natural resources and regulating measures to reduce chemical agricultural inputs and minimises external costs through a balanced combination of chemical, technological and biological tools (Boller et al. 2004 ; Malavolta and Cross 2009 ). Organic management, in contrast, is defined as a sustainable farming system with a stronger focus on environmental protection. When agrochemicals such as insecticides are used, they are based on mineral or organic substances, and the use of synthetic products requires a special permit in the absence of suitable alternatives (EU 2012; Seufert et al. 2017). Organic management practices tend to be more expensive and labour intensive (Seufert and Ramankutty 2017 ), and differ from IPM mainly in terms of soil management; soil tillage being mostly used in organic orchards, while herbicides are more common in IPM orchards (EU 2008). Research conducted in orchards has established that management practices in organic and IPM-based production systems have a significant impact on the composition of orchard arthropod communities (Batáry et al. 2017 ; Bogya et al. 2000 ; Shaw et al. 2021 ). For example, the use of herbicides has been shown to significantly alter ground cover, which in turn affects arthropods whose habitat is determined by the plant community in the orchard alleys (Altieri and Nichols 2004 ; Fernández et al. 2008 ). Moreover, many apple aphids have a holocyclic-heteroecious life cycle, often using common agricultural weeds as secondary hosts (Rousselin et al. 2017 ). Synthetic insecticide applications can significantly reduce aphid populations, but they also deter beneficial arthropods that contribute to pest control (Shaw and Wallis 2008 ). This disruption of natural ecological processes can lead to resistance, pest resurgence or outbreaks of non-target pests, which can significantly influence the effectiveness of aphid management strategies in apple orchards (Dutcher 2007 ). Due to the increasing consumer demand for eco-friendly food products, there has been a growing emphasis on promoting sustainable agricultural practices in Europe (Directive 2009/128/EC; Feliciano, 2022 ). Previous studies have investigated the influence of pest management strategies on apple aphid populations (Dib et al. 2016 ; Porcel et al. 2018 ; Shaw et al. 2021 ), but there is limited knowledge on how organic and IPM systems impact aphid populations when considering seasonal variation and different orchard habitats, especially in continental temperate climates. Supporting a more sustainable production of apples as a fruit crop requires a better understanding of the factors influencing aphid populations in orchards. Our aim in this study was to evaluate aphid infestations in organic and IPM systems according to the sampling period and in two major orchard habitats. We hypothesise that 1.) the overall aphid abundance in both habitats is lower in IPM compared to organic apple orchards, 2.) that such patterns depend on the sampling period for individual species and that 3.) the species composition of aphid communities is more homogeneous in IPM than in organic orchards. Material and methods Study sites The study was conducted in 16 commercial apple orchards located in eastern Germany in the states of Brandenburg, Saxony-Anhalt and Saxony. Eight orchards were organically managed, while the other eight were under IPM (Fig. 1 ). In the IPM orchards, growers used synthetic fertilisers, pheromone traps, synthetic pesticides when necessary (e.g. acetamiprid, chlorantraniliprole, flonicamid) and herbicides twice a year. Organic growers used various methods to control pest populations. These included organic pesticides (e.g. azadirachtin, Quassia amara extract, Bacillus thuringiensis ) and pheromone traps. Organic orchards were all licensed by the European and national legislation (Council Regulation (EC) No 834/2007). Apple trees in organic orchards were 4 to 20 years old and the orchard size ranged from 2.8 to 13 ha. Apple trees in IPM orchards were about 5 to 22 years old and the orchard size ranged from 3.6 to 21.5 ha. Different apple varieties were present in both management systems, but only Jonagold and related cultivars such as Red Jonaprince were sampled. Orchard alleys were covered with plants belonging to common agricultural weed families such as Fabaceae, Polygonaceae, Asteracea, Caryophyllaceae, Compositae, Brassicacea, Lamiaceae, Equisitaceae, and Poaceae. Sampling Two plots of 20 × 20 m were delimited for sampling in each of the 16 orchards. The distance between the two plots within an orchard ranged from 20 to 25 m. In each plot, arthropods were collected using two different methods: canopy beating and suction sampling in the orchard alleys. All sampling was carried out during three different sampling periods (between June to November 2021) corresponding to key stages of apple tree phenology: fruit-setting, fruit-growth, and post-harvest. For canopy beating of apple trees, 10 trees were randomly selected within each plot and five branches from each tree were randomly beaten once. Beat sampling was carried out using a tray consisting of a 72 cm of diameter metal frame with a handle supporting a disc-shaped funnel cloth sloping towards the centre into a bottle containing 70% ethanol. Arthropods dislodged from the branches were collected in the ethanol bottle by shaking the tray after beating each branch. For suction sampling in the orchard alleys, three alleys were randomly selected in each plot. Suction sampling was conducted in an area of 0.25 m² within each selected orchard alley using a D-Vac suction sampler for two minutes per alley. Arthropods were collected in a short stocking placed at the inlet of the suction sampler and transferred to cups containing 70% ethanol. In total, two beating samples and six suction samples were collected per orchard, resulting in 16 beating samples and 48 suction samples per sampling period for each management system (organic and IPM). All arthropod groups collected were sorted to order and family level, and aphids were identified to genus (for Dysaphis spp. and Euceraphis sp.) or species level (21 other species). Data analysis To evaluate the differences between aphid communities in the tree canopy and in the orchard alleys according to the pest management system and sampling period, we used permutational analyses of variance models (PERMANOVA) with pest management (two levels: organic or IPM) and sampling period (three levels: fruit-setting, fruit growing, post-harvest) as fixed factors, and orchard name (sixteen levels) as a random factor. All models also included interaction terms between fixed factors. Permutation analysis of variance models have the advantage that there is no assumption of normality of residuals or homoscedasticity, which is important when handling count data. As recommended by Anderson et al. ( 2008 ), all models were based on 9999 permutations of the residuals. In the first PERMANOVA model for the canopy data, we tested whether the species composition of aphid communities (based on the abundances of each species) significantly varied according to pest management systems and sampling periods. The abundance and species composition of aphid communities were analysed based on a multivariate matrix of log(X + 1)-transformed numbers of individuals in each species in each sampled plot, which was then transformed into a similarity matrix based on Bray-Curtis similarities. Bray-Curtis similarity is a standard measure to calculate resemblances for count-based community data. A dummy variable of 0.1 was added to the Bray-Curtis matrix to deal with unresolved resemblance if two samples had zero aphids. A logarithmic transformation (log(X + 1)) was performed prior to analyses to reduce the impact of very abundant species compared to less abundant species on the results of the analyses (Clarke and Green 1988). In the second PERMANOVA model for the orchard alley, we tested whether the species composition of aphid communities varied significantly according to pest management systems and sampling period. We followed the same procedure as in the model for the canopy data, but when the interaction term between pest management system and sampling period was significant, we further analysed its effect on the species composition. In such cases, differences between the three levels of the fixed factor “sampling period”, were tested for each pest management system (organic or IPM) separately with a pairwise post hoc PERMANOVA, as well as differences between the two levels of the fixed factor management for each sampling period. A similarity percentage analysis (SIMPER; Clarke and Gorley 2015 ) was then performed to determine which species were responsible for the dissimilarity between organic and IPM orchards in terms of aphid species composition. A non-parametric Mantel test was performed to test for differences in the species composition between habitats (orchard alley and tree canopy) based on the Bray-Curtis similarities used in the two PERMANOVA models. In addition to this procedure for multivariate species composition data, both the overall abundance of aphids and the Gini-Simpson diversity index adjusted for small sample sizes (1-λ′) were calculated for all samples and separately for each habitat. The index is a measure of evenness for each community which corresponds to the probability that two randomly sampled individuals in a community belong to different species without replacement rather than with replacement. To analyse how the overall abundance and this index varied between aphid communities, a similarity matrix was constructed based on Euclidean distances, with samples with zero values considered as outliers and thus excluded from the subsequent PERMANOVA comparing aphid diversity between pest management systems and sampling periods for each habitst. A mean plot and a dominance plot were created to further illustrate the evenness of aphid communities between organic and IPM systems. All statistical analyses were conducted using PRIMER version 7 software with the PERMANOVA add-on (PRIMER-e, Quest Research Limited, Auckland, New Zealand). Results During the three sampling periods in organic and IPM apple orchards in eastern Germany, we collected 13475 individuals belonging to 23 aphid species, with a total of 9673 individuals collected in the orchard alleys and 3802 in the tree canopy. Aphids in the tree canopy We collected 19 aphid species in the tree canopy (see Table 1 of Appendix 1), with overall aphid abundances varying significantly across sampling periods (Pseudo-F 2,47 = 17.65, P = 0.0002) (Fig. 2 A). The orchard management system had no significant effect on overall aphid abundance (Pseudo-F 1,47 = 0.44, P = 0.529), and no significant interaction was found between the management system and the sampling period (Pseudo-F 2,47 = 0.43, P = 0.658). The abundance of major pest aphids in apple orchards, such as E. lanigerum , Dysaphis spp., and R. insertum accounted for 79.69%, 8.36% and 5.81% respectively of all collected aphids during the study period and their average abundances varied considerably across sampling periods (Fig. 2 B). The Gini-Simpson diversity index of aphid communities in the tree canopy differed significantly between organic and IPM orchards (Pseudo-F 1,43 = 5.40, P = 0.034). However, there was no significant effect of sampling period (Pseudo-F 2,43 = 2.38, P = 0.107) and the interaction between management and sampling period was not significant (Pseudo-F 2,43 = 1.58, P = 0.227). The Gini-Simpson diversity index of the aphid community in organic orchards (mean = 0.46 ± 0.07) was 1.6 times higher than in IPM orchards (mean = 0.29 ± 0.06). The species composition of aphid communities in the tree canopy differed significantly between sampling periods (Pseudo-F 2,47 = 9.82, P = 0.0001), with no significant effect of the orchard management system (Pseudo-F 1,47 = 1.55 P = 0.201) or interaction between management systems and sampling periods (Pseudo-F 2,47 = 1.58, P = 0.123). Aphid communities in the tree canopy of IPM orchards were dominated by the woolly apple aphid, E. lanigerum , which accounted for more than 87% of all individuals sampled (Fig. 3 ), whereas in the organic orchards this cumulative dominance percentage was only reached jointly by the three most dominant species together ( E. lanigerum (69.93%), Dysaphis spp. (13.97%) and R. insertum (7.67%)). Aphids in the orchard alleys We collected 16 aphid species in the orchard alleys (see Table 2 of Appendix 1), and the overall abundance of aphids varied according to the sampling period (Pseudo-F 2,47 = 12.82, P = 0.0002) (Fig. 4 A). There was no significant effect of the orchard management system on overall aphid abundance (Pseudo-F 1,47 = 0.94, P = 0.348), and no significant interaction between management and sampling period was found (Pseudo-F 2,47 = 0.16, P = 0.859). Figure 4 B shows the averaged abundance of major aphid pests of apple such as Dysaphis spp., R. insertum and E. lanigerum according to the sampling period. The abundances of Dysaphis spp., R. insertum and E. lanigerum accounted for 57.12%, 10.40%, and 3.02%, respectively, of all collected aphids during the study period. The Gini-Simpson diversity index of aphid communities in the orchard alleys did not differ significantly between sampling periods (Pseudo-F 2,46 = 2.79, P = 0.081) or orchard management systems (Pseudo-F 2,46 = 0.26, P = 0.626), and the interaction term between management and period was not significant (Pseudo-F 2,46 = 1.03, P = 0.374). The species composition of aphid communities in the orchard alleys differed significantly between the sampling periods (Pseudo-F 2,47 = 7.96, P = 0.0001) but not between management systems (Pseudo-F 1,47 = 1.18, P = 0.336). Pest management systems significantly affected the species composition of aphid communities in the orchard alleys depending on the sampling period (Pseudo-F 2,47 = 1.91, P = 0.037). Pairwise post-hoc tests between sampling periods conducted within either organic or IPM orchards revealed significant differences in species composition between all sampling periods (Table 1 ). Pairwise post-hoc tests conducted between management systems within each sampling period revealed significant differences in species composition only during the fruit-setting period, with 2.2 times higher overall aphid abundances observed in organic orchards (27.10 ± 3.94) compared to IPM (12.38 ± 2.54) (Table 2 ). Table 1 Differences in species composition between the sampling periods in each management system Sampling period IPM Organic t P t P Fruit-growing vs. Fruit-setting 2.02 0.020 2.135 0.008 Fruit-growing vs. Post-harvest 2.57 0.009 2.380 0.013 Fruit-setting vs. Post-harvest 1.90 0.016 2.520 0.006 Table 2 Differences in species composition between pest management systems in each of the three sampling periods Management Fruit-setting Fruit-growing Post-harvest t P t P t P Organic vs. IPM 1.55 0.032 1.043 0.335 1.108 0.303 Macrosiphum euphorbiae showed the most pronounced difference in average abundance between management systems during the fruit-setting stage (Fig. 5 ), followed by Dysaphis spp., Aphis spiraecola , and Rhopalosiphum insertum in decreasing order (Table 5). Table 3 Aphid species which contributed to at least 70% of the dissimilarity in aphid communities in alleys between organic and IPM orchards during the fruit-setting period with log(X + 1) transformed mean abundances in both management systems, individual contributions and cumulative contribution to community dissimilarity. IPM Organic Species Mean Abundance Mean Abundance Contribution % Cumulative % Macrosiphum euphorbiae 0.50 1.92 27.40 27.40 Dysaphis spp. 1.50 2.12 24.45 51.85 Aphis spiraecola 0.79 0.42 13.00 64.85 Ropalosiphum insertum 0.88 1.18 13.00 77.85 A comparison of the compositional similarity between aphid communities in the canopy to communities in the orchard alley of the same plot at the same sampling period indicates that the two communities in different habitats were not significantly related (non-parametric Mantel test ρ = 0.01, P = 0.425). Discussion The species composition of aphid communities in the canopy did not differ significantly between organic and IPM orchards, but communities in organic orchards had a greater evenness compared to IPM orchards. Seasonality on the other hand had a significant effect on aphid community structure across sampling periods both in the tree canopy and the orchard alleys. The species composition of aphid communities in the alley differed significantly between organic and IPM orchards, but only in the fruit-setting period. These results highlight the importance of considering seasonality and habitats when comparing pest management systems, as both affect the composition of aphid communities, which may affect the effectiveness of management practices. The overall abundance of all aphids and the species composition of aphid communities in the canopy of apple trees were mainly influenced by seasonality, regardless of orchard management system. Aphid populations are known to fluctuate significantly over time due to factors such as climate, host plant phenology and aphid biology (Dixon 2003; Llewellyn et al. 2003; Sheppard et al. 2016 ). Indeed, the phenological stages of the host plant can influence the availability of resources for aphids, further affecting their population dynamics (Dedryver et al. 2010 ). We observed relatively low abundances of Dysaphis spp. during the fruit-setting and throughout the fruit-growing period in the tree canopy, but a significant increase in Dysaphis spp. populations after harvest. This can be explained by the fact that D. plantaginea , which is the most common species of the Dysaphis group on apple trees, migrates to its alternative host Plantago spp. (plantain) in summer (fruit-setting period onward), where it continues its life cycle until returning to apple trees in autumn (post-harvest period) to deposit overwintering eggs (Blommers et al. 2004 ). Similar observations have been made for R. insertum , which is known to migrate to grasses in late summer and autumn (Petrović-Obradović 2022 ). Moreover, control of R. insertum and D. plantaginea populations in apple orchards often involves early insecticide applications, consisting of sprays in March-June for D. plantaginea control which has a relatively low action threshold level for insecticide application compared to other pests of apple (Cooke et al. 1976 ; Barbagallo et al. 2017 ; Cahenzli et al. 2017 ; Lefebvre et al. 2017 ). This early spraying could further explain the low abundances of these pests in the canopy at the beginning of our sampling campaign in IPM orchards. On the other hand, the abundance of the monoecious species E. lanigerum in the tree canopy increased throughout the growing season. Eriosoma lanigerum is known to thrive particularly well on Jonagold apple trees and their related varieties (Hao et al. 2020; Tan et al. 2021 ). Due to recurrent infestations, treatments to control this aphid are usually applied multiple times throughout the season (Madsen and Bailey 1958 ; Shaw and Wallis 2009 ). Apart from the known apple pests ( Dysaphis spp., E. lanigerum , R. insertum , A. pomi , A. spiraecola ) and polyphagous aphid species such as Myzus persicae , M. ornatus , Macrosiphum euphorbiae , M. rosae , Aphis fabae , Therioaphis trifolii , Brachycaudus helichrysi , and Hyperomyzus lactucae , other aphid species found in the tree canopy can be considered as random occurrences. In this study, aphid abundances and the species composition of aphid communities in the tree canopy were not significantly influenced by the orchard pest management system. The absence of a significant effect could be attributed to the wide range of practices within organic and IPM orchards in Europe (Hatteland et al. 2023). In a study across several European countries, Happe et al. ( 2018 ) reported that factors such as adjacent woody habitat and landscape characteristics had a significant effect on aphid populations, while the orchard management system (IPM vs. organic) did not consistently affect aphid abundance. This highlights the importance of the agroecosystem context as a whole, rather than only considering the local orchard management system. However, in this study, several apple orchards were located in close proximity to each other, which limited our ability to conduct landscape analyses and assess the influence of landscape characteristics on aphid infestation across management systems. In contrast to overall abundance or species composition, the evenness of canopy aphid communities was significantly influenced by the orchard pest management system. Aphid communities showed greater evenness in organic orchards compared to IPM orchards, but the evenness did not vary significantly across different sampling periods- This result suggests, that the orchard management system plays a more important role in shaping the dominance structure in the tree canopy than the apple growth stage. Brown and Adler ( 1989 ) reported that the evenness of aphid communities was significantly greater in abandoned and organic orchards compared to conventionally managed orchards. Although IPM practices are often more environmentally friendly than conventional methods, they involve the use of selective synthetic pesticides (Damos et al. 2015 ). This can result in lower evenness in IPM orchards as some species are more susceptible to pesticides than others, allowing a few species to dominate the sprayed habitat (Hole et al. 2005 ). Higher evenness in organic orchards can potentially contribute to more effective natural pest control, as more even aphid communities may support a more diverse range of natural enemies in different seasons, reducing the risk of pest outbreaks through facilitating complex food webs (Landis et al. 2000 ; Lundgren and Fausti 2015 ). The woolly apple aphid Eriosoma lanigerum , was the most dominant aphid species in both organic and IPM apple orchards in the tree canopy. Previous studies have shown that E. lanigerum forms dense colonies on apple trees in summer, making it a major pest of apple under different orchard management practices (Heunis and Pringle 2006 ; Stokwe and Malan 2016 ). In addition, Jonagold apple trees and their related varieties are known to be particularly susceptible to E. lanigerum infestation (Tan et al. 2021 ). The high dominance of E. lanigerum populations in IPM orchards may be attributed to lower predation pressure compared to organic orchards, which often support more robust populations of natural enemies, such as earwigs (Happe et al. 2018 ). Furthermore, synthetic insecticides on which commercial IPM systems mostly rely, have been found to be less effective in reaching and controlling woolly apple aphid colonies on the roots, which can serve as a persistent source of re-infestation for the above-ground parts of the tree (Nicholas et al. 2003 ). In the orchard alleys, the significant variation in aphid abundance and species composition of aphid communities between sampling periods may be attributed to the nature of aphid life cycles (Harrington et al., 2007 ). Many species, such as D. plantaginea and R. insertum , have heteroecious life cycles, alternating between apple trees and other host plants, including agricultural weeds found in orchard alleys (Blommers et al. 2004 ; Petrović-Obradović 2022 ). These weeds provide habitats for aphids at different stages of their life cycle and support aphid populations as they migrate away from apple trees. Despite its monoecious life cycle, the presence of E. lanigerum in orchard alleys can be explained by movements between root and canopy populations of E. lanigerum (Heunis and Pringle 2006 ; Orpet et al. 2019 ). Orpet et al. ( 2019 ) found that managing these movements through soil amendments (sandy soils, mulching) can help in preventing E. lanigerum root feeding. However, we did not find a significant relationship between the species composition of aphid communities in the canopy and orchard alleys in our study. The species composition of aphid communities differed significantly between organic and IPM orchards in the orchard alley during the fruit-setting. This result highlights the importance of tailoring management strategies to the temporal dynamics of aphid populations. A study by Hull and VanStarner ( 1983 ) demonstrated that early insecticide applications, timed to the hatching of overwintering eggs, were more effective in successfully controlling aphid populations than later applications. In addition, management practices such as mechanical weed control underneath the trees in organic orchards and herbicide use in IPM orchards further influence aphid dynamics (Happe et al. 2018 ). Markó et al. (2013) found that different ground cover treatments, such as flowering plants and mowed grass, can significantly impact aphid infestation and the diversity of beneficial insects. Fréchette et al. (2008) further demonstrated that different systems of ground cover influence the abundance and performance of aphid predators. The results of the SIMPER analyses indicated that M. euphorbiae , Dysaphis spp., A. spiraecola , and R. insertum contributed to the differences in the species composition of aphid communities between organic and IPM orchards during the fruit-setting period. This suggests that management practices in organic and IPM systems influence aphid communities in the orchard alleys differently, possibly due to variations in pesticide usage (Malagnoux et al. 2015 ), natural enemy populations (Dib et al. 2016 ), and habitat structure within the orchards (Markó et al. 2012 ). These differences are particularly significant during the fruit-setting period (early summer), when plants in the orchard alleys are still green and providing favourable developmental conditions for aphids. The polyphagous A. spiraecola , was the only species that had a higher abundance in the orchard alley of IPM orchards compared to organically managed orchards. This could be due to its known resistance to synthetic insecticides classes such as neonicotinoids and organophosphates (Lowery et al. 2005 ; Smirle et al. 2010 ). Conclusion Our study shows that overall aphid numbers and species composition in in the tree canopy do not differ significantly between organic and IPM orchards. However, the greater evenness of aphid communities in organic orchards suggests a more balanced species distribution, which could be beneficial in maintaining natural biological control in orchards. Eriosoma lanigerum was the most dominant species in both orchard systems, with a particularly high dominance in IPM orchards, which highlights the need for specific management strategies to control this pest in orchards with susceptible apple varieties such as Jonagold. The species composition and presence of pest species such as M. euphorbiae , Dysaphis spp., A. spiraecola and R. insertum varied significantly across different stages of the apple growing season, with notable differences between organic and IPM orchards during the fruit-setting period in the orchard alleys. Our results stress the importance of considering both seasonality and differences between habitats when assessing aphid infestations in orchards. Consequently, we conclude that tailored pest management strategies, which account for the dynamics of aphid populations in orchard habitats and throughout different stages of the apple growing season, are essential to optimise pest management practices. Implementing these strategies can significantly reduce aphid infestations, ultimately leading to improved yields and quality. Statements and Declarations Acknowledgments The authors wish to thank Mohammad Hossain for his assistance during fieldwork, and all apple growers who participated in this study. This work was supported by a scholarship to Ingrid Aline Bapfubusa Niyibizi from the German Academic Exchange Service (Deutscher Akademischer Austauschdienst, DAAD) and by funding from the Graduate Research School of the Brandenburg University of Technology Cottbus-Senftenberg to Benjamin Schnerch. Funding This work was supported by a scholarship to Ingrid Aline Bapfubusa Niyibizi from the German Academic Exchange Service (Deutscher Akademischer Austauschdienst, DAAD) and by funding from the Graduate Research School of the Brandenburg University of Technology Cottbus-Senftenberg to Benjamin Schnerch. Competing Interests The authors have no relevant financial or non-financial interests to disclose. Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Author Contributions KB and BS contributed to the study conception and design. Material preparation, data collection and analysis were performed by IABN, BS and KB. The first draft of the manuscript was written by IABN. EAD and all other authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Data availability statement The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request. References Alhmedi, A., Bylemans, D., Bangels, E., & Beliën, T. (2022). Cultivar-mediated effects on apple–Dysaphis plantaginea interaction. Journal of Pest Science, 95(1303-1315). https://doi.org/10.1007/s10340-021-01460-6 Altieri, M. A., & Nichols, C. I. (2004). Biodiversity and pest management in agroecosystems (2nd ed.). Binghamton, NY: The Haworth Press Inc. Anderson, M. J., Gorley, R. N., & Clarke, K. R. (2008). PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK. Andreev, R., Rasheva, D., & Kutinkova, H. (2007). Aphids in apple orchards in Central-South Bulgaria. Journal of Plant Protection Research, 47(1), 87–90. Barbagallo, S., Bosio, G., & Pansa, M. G. (2017). The aphid species in Italian apple orchards and their phenology. Bulletin of Insectology, 70(1), 77-87. Barbagallo, S., Cocuzza, G., Cravedi, P., & Komazaki, S. (2007). IPM case studies: Deciduous fruit trees. In Harrington, R. (Ed.), Van Emden, H. F. (Ed.), Aphids as crop pests (pp. 651–661). CABI. https://doi.org/10.1079/9780851998190.0651 Batáry, P., Gallé, R., Riesch, F., Fischer, C., Dormann, C. F., Mußhoff, O., Császár, P., Fusaro, S., Gayer, C., Happe, A.-K., Kurucz, K., Molnár, D., Rösch, V., Wietzke, A., & Tscharntke, T. (2017). The former Iron Curtain still drives biodiversity–profit tradeoffs in German agriculture. Nature Ecology & Evolution, 1(1279–1284). https://doi.org/10.1038/s41559-017-0272-x Blommers, L., Helsen, H., & Vaal, F. (2004). Life history data of the rosy apple aphid Dysaphis plantaginea (Pass.) (Homopt. Aphididae) on plantain and as migrant to apple. Journal of Pest Science, 77, 155-163. https://doi.org/10.1007/s10340-004-0046-5 Bogya, S., Marko, V., & Szinetar, C. S. (2000). Effect of pest management systems on foliage- and grass-dwelling spider communities in an apple orchard in Hungary. International Journal of Pest Management, 46(4), 241-250. https://doi.org/10.1080/09670870050206000 Boller, E. F., Avilla, J., Joerg, E., Malavolta, C., Wijnands, F. G., & Esbjerg, P. (2004). Integrated production - principles and technical guidelines. IOBC/wprs Bulletin, 27, 1–49. Bostanian, N. J., Goulet, H., O’Hara, J., Masner, L., & Racette, G. (2004). Towards insecticide-free apple orchards: Flowering plants to attract beneficial arthropods. Biocontrol Science & Technology, 14, 25–37. Brown, M., & Glenn, D. (1999). Ground cover plants and selective insecticides as pest management tools in apple orchards. Journal of Economic Entomology, 92, 899-905. https://doi.org/10.1093/JEE/92.4.899 Brown, M. W., & Adler, C. R. L. (1989). Community structure of phytophagous arthropods on apple. Environmental Entomology, 18(4), 600-607. Brown, M. W., Schmitt, J. J., Ranger, S., & Hogmire, H. W. (1995). Yield reduction in apple by edaphic woolly apple aphid (Holnoptera: Aphididae) populations. Journal of Economic Entomology, 88(1), 127-133. https://doi.org/10.1093/jee/88.1.127 Cahenzli, F., Pfiffner, L., & Daniel, C. (2017). Reduced crop damage by self-regulation of aphids in an ecologically enriched insecticide-free apple orchard. Agronomy for Sustainable Development, 37, Article 65. https://doi.org/10.1007/s13593-017-0476-0 Clarke, K. R., & Gorley, R. N. (2015). PRIMER v7: User Manual/Tutorial. PRIMER-E, Plymouth, UK. Cooke, B., Herrington, P., Jones, K., & Morgan, N. (1976). Pest and disease control with low doses of pesticides in low and ultralow volumes applied to intensive apple trees. Pesticide Science, 7, 30-34. https://doi.org/10.1002/PS.2780070105 Cross, J. V., Cubison, S., Harris, A., & Harrington, R. (2007). Autumn control of rosy apple aphid Dysaphis plantaginea (Passerini) with aphicides. Crop Protection, 26, 1140–1149. Crowder, D. W., Northfield, T. D., Strand, M. R., & Snyder, W. E. (2010). Organic agriculture promotes evenness and natural pest control. Nature, 466(7302), 109-112. Damos, P., Escudero Colomar, L.-A., & Ioriatti, C. (2015). Integrated fruit production and pest management in Europe: The apple case study and how far we are from the original concept? Insects, 6 (3), 626–657. https://doi.org/10.3390/insects6030626 De Berardinis, E., Baronio, P., & Baumgärtner, J. (1994). The effect of aphid (Dysaphis plantaginea Pass. Hom.Aphididae) feeding on apple fruit growth. Ecological Modelling, 72, 115–127. Dedryver, C. A., Le Ralec, A., & Fabre, F. (2010). The conflicting relationships between aphids and men: A review of aphid damage and control strategies. Comptes Rendus Biologies, 333(6-7), 539-553. Dib, H., Sauphanor, B., & Capowiez, Y. (2016). Effect of management strategies on arthropod communities in the colonies of rosy apple aphid Dysaphis plantaginea Passerini (Hemiptera: Aphididae) in south-eastern France. Agriculture, Ecosystems & Environment, 216. Dib, H., Simon, S., Sauphanor, B., & Capowiez, Y. (2010). The role of natural enemies on the population dynamics of the rosy apple aphid Dysaphis plantaginea Passerini (Hemiptera: Aphididae) in organic apple orchards in south-eastern France. Biological Control, 55, 97-109. https://doi.org/10.1016/J.BIOCONTROL.2010.07.005 Dutcher, J. D. (2007). A review of resurgence and replacement causing pest outbreaks in IPM. In A. Ciancio & K. G. Mukerji (Eds.), General concepts in integrated pest and disease management (Vol. 1, pp. 27-43). Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6061-8_2 EC Directive. (2009). EC Directive 2009/128/EC of the European parliament and of the council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides. Official Journal of the European Union, 309:71–86. El Jaouhari, M., Damour, G., Tixier, P., & Coulis, M. (2023). Glyphosate reduces the biodiversity of soil macrofauna and benefits exotic over native species in a tropical agroecosystem. Basic and Applied Ecology, 73, 18-26. Feliciano, D. (2022). Factors influencing the adoption of sustainable agricultural practices in the UK. Sustainability , 14 (12), 7123. https://doi.org/10.3390/su14127123 Fernández, D. E., Cichón, L. I., Sánchez, E. E., Garrido, S. A., & Gittins, C. (2008). Effect of different cover crops on the presence of arthropods in an organic apple (Malus domestica Borkh) orchard. Journal of Sustainable Agriculture, 32(2), 197–211. https://doi.org/10.1080/10440040802170624 Frechette, B., Cormier, D., Chouinard, G., Vanoosthuyse, F., & Lucas, E. (2008). Apple aphid Aphis spp. (Hemiptera: Aphididae) and predator populations in an apple orchard at the non-bearing stage: The impact of ground cover and cultivar. European Journal of Entomology, 105, 521-529. https://doi.org/10.14411/eje.2008.069 Graf, B., Baumgärtner, J., & Delucchi, V. (1985). Simulation models for the dynamics of three apple aphids Dysaphis plantaginea, Rhopalosiphum insertum, and Aphis pomi (Homoptera: Aphididae) in a Swiss apple orchard. Journal of Applied Entomology, 99(1-5), 453-465. Happe, A., Roquer‐Beni, L., Bosch, J., Alins, G., & Mody, K. (2018). Earwigs and woolly apple aphids in integrated and organic apple orchards: Responses of a generalist predator and a pest prey to local and landscape factors. Agriculture, Ecosystems & Environment, 256, 59-65. https://doi.org/10.1016/J.AGEE.2018.09.004 Harrington, R., Fleming, R. A., & Woiwod, I. P. (2007). Climate change impacts on insect management and conservation in temperate regions: Can they be predicted? Agricultural and Forest Entomology, 9(3), 233-240. Heunis, J., & Pringle, K. (2006). Field biology of woolly apple aphid Eriosoma lanigerum (Hausmann) and its natural enemy Aphelinus mali (Haldeman) in apple orchards in the Western Cape Province. African Entomology, 14, 77-86. Hole, D. G., Perkins, A. J., Wilson, J. D., Alexander, I. H., Grice, P. V., & Evans, A. D. (2005). Does organic farming benefit biodiversity? Biological Conservation, 122(1), 113-130. https://doi.org/10.1016/j.biocon.2004.07.018 Hull, L., & VanStarner, R. (1983). Effectiveness of insecticide applications timed to correspond with the development of rosy apple aphid (Homoptera: Aphididae) on apple. Journal of Economic Entomology, 76, 594-598. https://doi.org/10.1093/JEE/76.3.594 Hullé, M., Turpeau, E., & Chaubet, B. (2006). Encyclop'aphid. INRA. https://www6.inra.fr/encyclopedie-pucerons Jeffs, C., & Leather, S. (2014). Effects of extreme fluctuating temperature events on life history traits of the grain aphid Sitobion avenae. Entomologia Experimentalis et Applicata, 150, 89-99. https://doi.org/10.1111/eea.12160 Jenser, G., Balázs, K., Erdélyi, C., Haltrich, A., Kádár, F., Kozár, F., Markó, V., & Rácz, V. (1999). Changes in arthropod population composition in IPM apple orchards under continental climatic conditions in Hungary. Agriculture, Ecosystems & Environment, 73(2), 141-154. https://doi.org/10.1016/S0167-8809(99)00023-7 Landis, D. A., Wratten, S. D., & Gurr, G. M. (2000). Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology, 45(1), 175-201. Lefebvre, M., Franck, P., Olivares, J., Ricard, J., Mandrin, J., & Lavigne, C. (2017). Spider predation on rosy apple aphid in conventional, organic, and insecticide-free orchards and its impact on aphid populations. Biological Control, 104, 57-65. https://doi.org/10.1016/J.BIOCONTROL.2016.10.009 Lowery, D., Smirle, M., Foottit, R., Zurowski, C., & Peryea, E. (2005). Baseline susceptibilities to imidacloprid for green apple aphid and spirea aphid (Homoptera: Aphididae) collected from apple in the Pacific Northwest. Journal of Economic Entomology, 98, 188 - 194. https://doi.org/10.1603/0022-0493-98.1.188 Lundgren, J. G., & Fausti, S. W. (2015). Trading biodiversity for pest problems. Science Advances, 1 (6), e1500558. https://doi.org/10.1126/sciadv.1500558 Madsen, H., & Bailey, J. (1958). Woolly and green apple aphids: Field trials with new materials in orchard near Watsonville indicate same timing of spray treatment controls both pests. California Agriculture, 12, 14-16. Malagnoux, L., Marliac, G., Simon, S., & Rault, M. (2015). Management strategies in apple orchards influence earwig community. Chemosphere, 124, 156–162. https://doi.org/10.1016/j.chemosphere.2014.12.024 Malavolta, C., & Cross, J. (2009). Guidelines for integrated production of pome fruits in Europe. IOBC Technical Guideline III, 4th edition. IOBC/wprs Bulletin, 47, 1–12. Markó, V., Jenser, G., Kondorosy, E., Ábrahám, L., & Balázs, K. (2012). Flowers for better pest control? The effects of apple orchard ground cover management on green apple aphids (Aphis spp.) (Hemiptera: Aphididae), their predators, and the canopy insect community. Biocontrol Science and Technology, 23(2), 126–145. https://doi.org/10.1080/09583157.2012.743972 Moss, D., & Pollard, E. (1993). Calculation of collated indices of abundance of butterflies based on monitored sites. Ecological Entomology, 18, 211-222. https://doi.org/10.1111/j.1365-2311.1993.tb01083.x Nagy, C., Cross, J., & Markó, V. (2013). Sugar feeding of the common black ant, Lasius niger (L.), as a possible indirect method for reducing aphid populations on apple by disturbing ant-aphid mutualism. Biological Control, 65 (1), 24–36. Nicholas, A., Spooner-Hart, R., & Vickers, R. (2003). Control of woolly aphid Eriosoma lanigerum (Hausmann) (Hemiptera: Pemphigidae) on mature apple trees using insecticide soil-root drenches. Australian Journal of Entomology, 42, 6-11. https://doi.org/10.1046/J.1440-6055.2003.00336.X Orpet, R., Jones, V., Reganold, J., & Crowder, D. (2019). Effects of restricting movement between root and canopy populations of woolly apple aphid. PLoS ONE, 14. https://doi.org/10.1371/journal.pone.0216424 Petrović-Obradović, O. (2022). Aphid species (Hemiptera: Aphididae) – pests of apple. Plant Doctor, 50, 542–552. Porcel, M., Andersson, G., Pålsson, J., & Tasin, M. (2018). Organic management in apple orchards: Higher impacts on biological control than on pollination. Journal of Applied Ecology. https://doi.org/10.1111/1365-2664.13247 Pretty, J., & Bharucha, Z. P. (2014). Sustainable intensification in agricultural systems. Annals of Botany, 114, 1571–1596. https://doi.org/10.1093/aob/mcu205 Qubbaj, T., Reineke, A., & Zebitz, C. P. W. (2005). Molecular interactions between rosy apple aphids Dysaphis plantaginea and resistant and susceptible cultivars of its primary host Malus domestica. Entomologia Experimentalis et Applicata, 115(1), 145-152. https://doi.org/10.1111/j.1570-7458.2005.00255.x Rousselin, A., Bevacqua, D., Sauge, M. H., & others. (2017). Harnessing the aphid life cycle to reduce insecticide reliance in apple and peach orchards: A review. Agronomy for Sustainable Development, 37, 38. https://doi.org/10.1007/s13593-017-0444-8 Senior, V. L., Evans, L. C., Leather, S. R., Oliver, T. H., & Evans, K. L. (2020). Phenological responses in a sycamore–aphid–parasitoid system and consequences for aphid population dynamics: A 20-year case study. Global Change Biology, 26(5), 2814–2828. https://doi.org/10.1111/gcb.15015 Seufert, V., & Ramankutty, N. (2017). Many shades of gray– the context-dependent performance of organic agriculture. Science Advances, 3, e1602638. https://doi.org/10.1126/sciadv.1602638 Shaw, P. W., & Wallis, D. (2008). Biocontrol of pests in apples under integrated fruit production. New Zealand Plant Protection, 61, 333–337. Shaw, P., & Wallis, D. (2009). Early-season use of insecticides for management of woolly apple aphid ( Eriosoma lanigerum ) in Nelson apple orchards. New Zealand Plant Protection, 62, 291-295. https://doi.org/10.30843/NZPP.2009.62.4819 Shaw, B., Nagy, C., & Fountain, M. T. (2021). Organic control strategies for use in IPM of invertebrate pests in apple and pear orchards. Insects, 12(12), 1106. https://doi.org/10.3390/insects12121106 Sheppard, L., Bell, J., Harrington, R., & Reuman, D. (2016). Changes in large-scale climate alter spatial synchrony of aphid pests. Nature Climate Change, 6, 610-613. https://doi.org/10.1038/NCLIMATE2881 Smirle, M., Zurowski, C., Lowery, D., & Foottit, R. (2010). Relationship of insecticide tolerance to esterase enzyme activity in Aphis pomi and Aphis spiraecola (Hemiptera: Aphididae). Journal of Economic Entomology, 103, 374 - 378. https://doi.org/10.1603/EC09275 Stokwe, N., & Malan, A. (2016). Woolly apple aphid Eriosoma lanigerum (Hausmann) in South Africa: Biology and management practices with focus on the potential use of entomopathogenic nematodes and fungi. African Entomology, 24, 267 - 278. https://doi.org/10.4001/003.024.0267 Tan, X., Yang, Z., Zhou, H., Yang, Q., & Zhou, H. (2021). Resistance performance of four principal apple cultivars to woolly apple aphid Eriosoma lanigerum (Hemiptera: Pemphigidae) by simulated seasonal temperature in northern China. Arthropod-Plant Interactions, 15, 59 - 69. https://doi.org/10.1007/s11829-020-09797-y Tilman, D., Lehman, C. L., & Thomson, K. T. (1997). Plant diversity and ecosystem productivity: Theoretical considerations. Proceedings of the National Academy of Sciences, 94(5), 1857-1861. Will, T., Furch, A., & Zimmermann, M. (2013). How phloem-feeding insects face the challenge of phloem-located defenses. Frontiers in Plant Science, 4. https://doi.org/10.3389/fpls.2013.00336 Additional Declarations No competing interests reported. Supplementary Files Appendix1.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-5783229","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":400000044,"identity":"9210da96-3518-4e29-adb8-53d717b27ad7","order_by":0,"name":"Ingrid Aline Bapfubusa Niyibizi","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAyElEQVRIiWNgGAWjYBACAyD+ACL5JcB8ZqK0MM4AkZIzGBgbSNACYtwgVos5+9mDzTwFd+w2325gf8zDYC1HUItlT15iM4/Bs+Rtdw4wNvMwpBsTdtiBHPPHPAaHk81u5H8Eajmc2EBQy/k3hs0gLcYzEkC2HK4nrOVGDliLnYEEREsCYb/MeJfYOMfgcIIE0C8z5xikGxK0xZw/92DDmz+H7flnNzB8eFNhLU/QFgYGHjAJ9bUBERpgWuyJUjsKRsEoGAUjEwAAnQM873+SMXMAAAAASUVORK5CYII=","orcid":"","institution":"Brandenburg University of Technology Cottbus-Senftenberg","correspondingAuthor":true,"prefix":"","firstName":"Ingrid","middleName":"Aline Bapfubusa","lastName":"Niyibizi","suffix":""},{"id":400000046,"identity":"54aaeddf-718d-4432-8ff8-12a52917708e","order_by":1,"name":"Benjamin Schnerch","email":"","orcid":"","institution":"Brandenburg University of Technology Cottbus-Senftenberg","correspondingAuthor":false,"prefix":"","firstName":"Benjamin","middleName":"","lastName":"Schnerch","suffix":""},{"id":400000047,"identity":"067648e1-98e7-4244-8c05-53dea5391270","order_by":2,"name":"El Aziz Djoudi","email":"","orcid":"","institution":"Brandenburg University of Technology Cottbus-Senftenberg","correspondingAuthor":false,"prefix":"","firstName":"El","middleName":"Aziz","lastName":"Djoudi","suffix":""},{"id":400000048,"identity":"e8a10141-bf32-4ec4-90f7-2ee44b2cfb4a","order_by":3,"name":"Klaus Birkhofer","email":"","orcid":"","institution":"Brandenburg University of Technology Cottbus-Senftenberg","correspondingAuthor":false,"prefix":"","firstName":"Klaus","middleName":"","lastName":"Birkhofer","suffix":""}],"badges":[],"createdAt":"2025-01-07 17:08:05","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5783229/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5783229/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":73644758,"identity":"4f4866c0-7501-4203-bebd-a8647fbd473a","added_by":"auto","created_at":"2025-01-13 08:43:26","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":64770,"visible":true,"origin":"","legend":"\u003cp\u003eMap of orchards under organic and integrated pest management\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-5783229/v1/b28c42b43a941acf9b2a08f6.png"},{"id":73645360,"identity":"c717a23c-bcb0-4d65-873f-aa2b0031c7a7","added_by":"auto","created_at":"2025-01-13 08:51:26","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":89366,"visible":true,"origin":"","legend":"\u003cp\u003eAverage abundance of A) all aphids and B) the three major aphid pest species at different sampling periods in the tree canopy. F.-S. = Fruit-setting, F.-G. = Fruit-growing, P.-H. = Post-harvest. Error bars are standard errors of the mean\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-5783229/v1/25879dded45c5ddcd0186051.png"},{"id":73646970,"identity":"50292eee-414d-4397-8a93-98c3ef7e830a","added_by":"auto","created_at":"2025-01-13 08:59:26","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":37980,"visible":true,"origin":"","legend":"\u003cp\u003eCumulative dominance curve of aphid species in the tree canopy of IPM (▲) and organic (■) apple orchards\u003c/p\u003e","description":"","filename":"3.png","url":"https://assets-eu.researchsquare.com/files/rs-5783229/v1/681046dffe63cb420326aaac.png"},{"id":73645362,"identity":"e8691f8d-f4c6-4f76-b3fa-b1a3f1eb5d40","added_by":"auto","created_at":"2025-01-13 08:51:26","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":107963,"visible":true,"origin":"","legend":"\u003cp\u003eAverage abundance of A) all aphids and B) the three major aphid pest species at different sampling periods in the orchard alleys. F.-S. = Fruit-setting, F.-G. = Fruit-growing, P.-H. = Post-harvest. Error bars are standard errors of the mean.\u003c/p\u003e","description":"","filename":"4.png","url":"https://assets-eu.researchsquare.com/files/rs-5783229/v1/1006b48cb8b7ad059f231172.png"},{"id":73646972,"identity":"14ef2dd8-5159-46a4-be52-dc47ef03c90e","added_by":"auto","created_at":"2025-01-13 08:59:26","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":103194,"visible":true,"origin":"","legend":"\u003cp\u003eAbundance patterns of main aphid species contributing to dissimilarities between organic and IPM apple orchards during the fruit-setting stage\u003c/p\u003e","description":"","filename":"5.png","url":"https://assets-eu.researchsquare.com/files/rs-5783229/v1/c08b4a961bfb54ec3290e027.png"},{"id":74284350,"identity":"5dd9941f-01b1-4366-958d-229901b550ac","added_by":"auto","created_at":"2025-01-20 16:01:51","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":992258,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5783229/v1/a359e342-f4d2-45c9-bb72-77fe5ea00b76.pdf"},{"id":73645359,"identity":"9e9077a8-3fc9-4935-a31e-ab64217b189a","added_by":"auto","created_at":"2025-01-13 08:51:26","extension":"docx","order_by":0,"title":"","display":"","copyAsset":false,"role":"supplement","size":21763,"visible":true,"origin":"","legend":"","description":"","filename":"Appendix1.docx","url":"https://assets-eu.researchsquare.com/files/rs-5783229/v1/4b389f0ddc2e5e25744f0bdf.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Higher aphid infestation in the alleys of organic apple orchards compared to IPM during fruit setting in eastern Germany","fulltext":[{"header":"Introduction","content":"\u003cp\u003eAround 60 phytophagous arthropod species are considered pests of apples in Europe, with aphids being one of the economically most important pest groups in orchards (Jenser et al. \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e1999\u003c/span\u003e). Aphids are particularly problematic due to their high reproductive rates and ability to cause extensive damage to fruit trees (Blommers et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Dedryver et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2010\u003c/span\u003e). More than 20 aphid species have been recorded feeding on apples in Europe, but only six are considered harmful to apple production: the rosy apple aphid (\u003cem\u003eDysaphis plantaginea\u003c/em\u003e Passerini) and the rosy leaf curling aphid (\u003cem\u003eDysaphis devecta\u003c/em\u003e Walker) from the \u003cem\u003eDysaphis\u003c/em\u003e genus, the woolly apple aphid (\u003cem\u003eEriosoma lanigerum\u003c/em\u003e Hausmann), the green apple aphid (\u003cem\u003eAphis pomi\u003c/em\u003e De Geer), the apple-grass aphid (\u003cem\u003eRhopalosiphum insertum\u003c/em\u003e Walker), and the polyphagous spirea aphid (\u003cem\u003eAphis spiraecola\u003c/em\u003e Patch) (Hull\u0026eacute; et al. \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Rousselin et al. \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Infestations by major apple aphid pests are often linked to specific phenological stages of apple trees (Mi\u0026ntilde;arro and Dapena, 2007; Simon et al., 2011). Moreover, aphid populations show seasonal fluctuations, with population peaks influenced by environmental conditions, species interactions and the species composition of the local aphid community (Andreev et al., \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Dib et al., \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Nagy et al., \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2013\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAphids have piercing-sucking mouthparts consisting of long, flexible, perforating stylets that allow them to penetrate plant tissues and reach the sieve tube bundles of the phloem, from which they extract the elaborated sap (Will et al. \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). This feeding behaviour causes severe leaf curling and deformation to their host plant, leading to reduced photosynthesis, stunted growth, gall formation, secondary infection by fungal pathogens, premature fruit drop, reduced fruit size, and poor yields (Brown et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e1995\u003c/span\u003e; De Berardinis et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Graf et al. \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e1985\u003c/span\u003e). Infested trees often produce apple fruits that are unsuitable for the fresh fruit market (Alhmedi et al. \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Without adequate pest management measures for example, the species \u003cem\u003eD. plantaginea\u003c/em\u003e can be responsible for up to 80% damage in commercial apple orchards (Qubbaj et al. \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2005\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eManagement of aphid pests is critical in apple orchards due to their very low abundance threshold to cause economic damage, resulting in a correspondingly low treatment threshold, which requires prompt pesticide application under integrated pest management (IPM) once aphids are detected (Barbagallo et al. \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). European apple orchards typically receive 5\u0026ndash;15 insecticide applications per year, making apples one of the most treated fruit crops in the region (Cross et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). Due to concerns about the risks associated with pesticide use and the growing public demand for environmentally friendly food products, there has been an increasing interest in developing sustainable solutions for pest control in the past decades (Bostanian et al. \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). Consequently, aphids in commercial apple orchards in the European Union (EU) are typically managed using either organic or IPM practices (Dib et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2016\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIntegrated pest management is an important part of the concept of integrated production in apple orchards, which is defined as a production system that uses natural resources and regulating measures to reduce chemical agricultural inputs and minimises external costs through a balanced combination of chemical, technological and biological tools (Boller et al. \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Malavolta and Cross \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). Organic management, in contrast, is defined as a sustainable farming system with a stronger focus on environmental protection. When agrochemicals such as insecticides are used, they are based on mineral or organic substances, and the use of synthetic products requires a special permit in the absence of suitable alternatives (EU 2012; Seufert et al. 2017). Organic management practices tend to be more expensive and labour intensive (Seufert and Ramankutty \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), and differ from IPM mainly in terms of soil management; soil tillage being mostly used in organic orchards, while herbicides are more common in IPM orchards (EU 2008).\u003c/p\u003e \u003cp\u003eResearch conducted in orchards has established that management practices in organic and IPM-based production systems have a significant impact on the composition of orchard arthropod communities (Bat\u0026aacute;ry et al. \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Bogya et al. \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Shaw et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). For example, the use of herbicides has been shown to significantly alter ground cover, which in turn affects arthropods whose habitat is determined by the plant community in the orchard alleys (Altieri and Nichols \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Fern\u0026aacute;ndez et al. \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). Moreover, many apple aphids have a holocyclic-heteroecious life cycle, often using common agricultural weeds as secondary hosts (Rousselin et al. \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Synthetic insecticide applications can significantly reduce aphid populations, but they also deter beneficial arthropods that contribute to pest control (Shaw and Wallis \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2008\u003c/span\u003e). This disruption of natural ecological processes can lead to resistance, pest resurgence or outbreaks of non-target pests, which can significantly influence the effectiveness of aphid management strategies in apple orchards (Dutcher \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2007\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eDue to the increasing consumer demand for eco-friendly food products, there has been a growing emphasis on promoting sustainable agricultural practices in Europe (Directive 2009/128/EC; Feliciano, \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Previous studies have investigated the influence of pest management strategies on apple aphid populations (Dib et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Porcel et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Shaw et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), but there is limited knowledge on how organic and IPM systems impact aphid populations when considering seasonal variation and different orchard habitats, especially in continental temperate climates.\u003c/p\u003e \u003cp\u003eSupporting a more sustainable production of apples as a fruit crop requires a better understanding of the factors influencing aphid populations in orchards. Our aim in this study was to evaluate aphid infestations in organic and IPM systems according to the sampling period and in two major orchard habitats. We hypothesise that 1.) the overall aphid abundance in both habitats is lower in IPM compared to organic apple orchards, 2.) that such patterns depend on the sampling period for individual species and that 3.) the species composition of aphid communities is more homogeneous in IPM than in organic orchards.\u003c/p\u003e"},{"header":"Material and methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eStudy sites\u003c/h2\u003e \u003cp\u003eThe study was conducted in 16 commercial apple orchards located in eastern Germany in the states of Brandenburg, Saxony-Anhalt and Saxony. Eight orchards were organically managed, while the other eight were under IPM (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). In the IPM orchards, growers used synthetic fertilisers, pheromone traps, synthetic pesticides when necessary (e.g. acetamiprid, chlorantraniliprole, flonicamid) and herbicides twice a year. Organic growers used various methods to control pest populations. These included organic pesticides (e.g. azadirachtin, \u003cem\u003eQuassia amara\u003c/em\u003e extract, \u003cem\u003eBacillus thuringiensis\u003c/em\u003e) and pheromone traps. Organic orchards were all licensed by the European and national legislation (Council Regulation (EC) No 834/2007). Apple trees in organic orchards were 4 to 20 years old and the orchard size ranged from 2.8 to 13 ha. Apple trees in IPM orchards were about 5 to 22 years old and the orchard size ranged from 3.6 to 21.5 ha. Different apple varieties were present in both management systems, but only Jonagold and related cultivars such as Red Jonaprince were sampled. Orchard alleys were covered with plants belonging to common agricultural weed families such as Fabaceae, Polygonaceae, Asteracea, Caryophyllaceae, Compositae, Brassicacea, Lamiaceae, Equisitaceae, and Poaceae.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003eSampling\u003c/h3\u003e\n\u003cp\u003eTwo plots of 20 \u0026times; 20 m were delimited for sampling in each of the 16 orchards. The distance between the two plots within an orchard ranged from 20 to 25 m. In each plot, arthropods were collected using two different methods: canopy beating and suction sampling in the orchard alleys. All sampling was carried out during three different sampling periods (between June to November 2021) corresponding to key stages of apple tree phenology: fruit-setting, fruit-growth, and post-harvest. For canopy beating of apple trees, 10 trees were randomly selected within each plot and five branches from each tree were randomly beaten once. Beat sampling was carried out using a tray consisting of a 72 cm of diameter metal frame with a handle supporting a disc-shaped funnel cloth sloping towards the centre into a bottle containing 70% ethanol. Arthropods dislodged from the branches were collected in the ethanol bottle by shaking the tray after beating each branch. For suction sampling in the orchard alleys, three alleys were randomly selected in each plot. Suction sampling was conducted in an area of 0.25 m\u0026sup2; within each selected orchard alley using a D-Vac suction sampler for two minutes per alley. Arthropods were collected in a short stocking placed at the inlet of the suction sampler and transferred to cups containing 70% ethanol. In total, two beating samples and six suction samples were collected per orchard, resulting in 16 beating samples and 48 suction samples per sampling period for each management system (organic and IPM). All arthropod groups collected were sorted to order and family level, and aphids were identified to genus (for \u003cem\u003eDysaphis\u003c/em\u003e spp. and \u003cem\u003eEuceraphis\u003c/em\u003e sp.) or species level (21 other species).\u003c/p\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cp\u003eTo evaluate the differences between aphid communities in the tree canopy and in the orchard alleys according to the pest management system and sampling period, we used permutational analyses of variance models (PERMANOVA) with pest management (two levels: organic or IPM) and sampling period (three levels: fruit-setting, fruit growing, post-harvest) as fixed factors, and orchard name (sixteen levels) as a random factor. All models also included interaction terms between fixed factors. Permutation analysis of variance models have the advantage that there is no assumption of normality of residuals or homoscedasticity, which is important when handling count data. As recommended by Anderson et al. (\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2008\u003c/span\u003e), all models were based on 9999 permutations of the residuals.\u003c/p\u003e \u003cp\u003eIn the first PERMANOVA model for the canopy data, we tested whether the species composition of aphid communities (based on the abundances of each species) significantly varied according to pest management systems and sampling periods. The abundance and species composition of aphid communities were analysed based on a multivariate matrix of log(X\u0026thinsp;+\u0026thinsp;1)-transformed numbers of individuals in each species in each sampled plot, which was then transformed into a similarity matrix based on Bray-Curtis similarities. Bray-Curtis similarity is a standard measure to calculate resemblances for count-based community data. A dummy variable of 0.1 was added to the Bray-Curtis matrix to deal with unresolved resemblance if two samples had zero aphids. A logarithmic transformation (log(X\u0026thinsp;+\u0026thinsp;1)) was performed prior to analyses to reduce the impact of very abundant species compared to less abundant species on the results of the analyses (Clarke and Green 1988). In the second PERMANOVA model for the orchard alley, we tested whether the species composition of aphid communities varied significantly according to pest management systems and sampling period. We followed the same procedure as in the model for the canopy data, but when the interaction term between pest management system and sampling period was significant, we further analysed its effect on the species composition. In such cases, differences between the three levels of the fixed factor \u0026ldquo;sampling period\u0026rdquo;, were tested for each pest management system (organic or IPM) separately with a pairwise post hoc PERMANOVA, as well as differences between the two levels of the fixed factor management for each sampling period. A similarity percentage analysis (SIMPER; Clarke and Gorley \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2015\u003c/span\u003e) was then performed to determine which species were responsible for the dissimilarity between organic and IPM orchards in terms of aphid species composition. A non-parametric Mantel test was performed to test for differences in the species composition between habitats (orchard alley and tree canopy) based on the Bray-Curtis similarities used in the two PERMANOVA models.\u003c/p\u003e \u003cp\u003eIn addition to this procedure for multivariate species composition data, both the overall abundance of aphids and the Gini-Simpson diversity index adjusted for small sample sizes (1-λ\u0026prime;) were calculated for all samples and separately for each habitat. The index is a measure of evenness for each community which corresponds to the probability that two randomly sampled individuals in a community belong to different species without replacement rather than with replacement. To analyse how the overall abundance and this index varied between aphid communities, a similarity matrix was constructed based on Euclidean distances, with samples with zero values considered as outliers and thus excluded from the subsequent PERMANOVA comparing aphid diversity between pest management systems and sampling periods for each habitst. A mean plot and a dominance plot were created to further illustrate the evenness of aphid communities between organic and IPM systems.\u003c/p\u003e \u003cp\u003eAll statistical analyses were conducted using PRIMER version 7 software with the PERMANOVA add-on (PRIMER-e, Quest Research Limited, Auckland, New Zealand).\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003eDuring the three sampling periods in organic and IPM apple orchards in eastern Germany, we collected 13475 individuals belonging to 23 aphid species, with a total of 9673 individuals collected in the orchard alleys and 3802 in the tree canopy.\u003c/p\u003e\n\u003ch3\u003eAphids in the tree canopy\u003c/h3\u003e\n\u003cp\u003eWe collected 19 aphid species in the tree canopy (see Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e of Appendix 1), with overall aphid abundances varying significantly across sampling periods (Pseudo-F\u003csub\u003e2,47\u003c/sub\u003e = 17.65, P\u0026thinsp;=\u0026thinsp;0.0002) (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eA). The orchard management system had no significant effect on overall aphid abundance (Pseudo-F\u003csub\u003e1,47\u003c/sub\u003e = 0.44, P\u0026thinsp;=\u0026thinsp;0.529), and no significant interaction was found between the management system and the sampling period (Pseudo-F\u003csub\u003e2,47\u003c/sub\u003e = 0.43, P\u0026thinsp;=\u0026thinsp;0.658). The abundance of major pest aphids in apple orchards, such as \u003cem\u003eE. lanigerum\u003c/em\u003e, \u003cem\u003eDysaphis\u003c/em\u003e spp., and \u003cem\u003eR. insertum\u003c/em\u003e accounted for 79.69%, 8.36% and 5.81% respectively of all collected aphids during the study period and their average abundances varied considerably across sampling periods (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003eB).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe Gini-Simpson diversity index of aphid communities in the tree canopy differed significantly between organic and IPM orchards (Pseudo-F\u003csub\u003e1,43\u003c/sub\u003e = 5.40, P\u0026thinsp;=\u0026thinsp;0.034). However, there was no significant effect of sampling period (Pseudo-F\u003csub\u003e2,43\u003c/sub\u003e = 2.38, P\u0026thinsp;=\u0026thinsp;0.107) and the interaction between management and sampling period was not significant (Pseudo-F\u003csub\u003e2,43\u003c/sub\u003e = 1.58, P\u0026thinsp;=\u0026thinsp;0.227). The Gini-Simpson diversity index of the aphid community in organic orchards (mean\u0026thinsp;=\u0026thinsp;0.46\u0026thinsp;\u0026plusmn;\u0026thinsp;0.07) was 1.6 times higher than in IPM orchards (mean\u0026thinsp;=\u0026thinsp;0.29\u0026thinsp;\u0026plusmn;\u0026thinsp;0.06).\u003c/p\u003e \u003cp\u003eThe species composition of aphid communities in the tree canopy differed significantly between sampling periods (Pseudo-F\u003csub\u003e2,47\u003c/sub\u003e = 9.82, P\u0026thinsp;=\u0026thinsp;0.0001), with no significant effect of the orchard management system (Pseudo-F\u003csub\u003e1,47\u003c/sub\u003e = 1.55 P\u0026thinsp;=\u0026thinsp;0.201) or interaction between management systems and sampling periods (Pseudo-F\u003csub\u003e2,47\u003c/sub\u003e = 1.58, P\u0026thinsp;=\u0026thinsp;0.123).\u003c/p\u003e \u003cp\u003eAphid communities in the tree canopy of IPM orchards were dominated by the woolly apple aphid, \u003cem\u003eE. lanigerum\u003c/em\u003e, which accounted for more than 87% of all individuals sampled (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e), whereas in the organic orchards this cumulative dominance percentage was only reached jointly by the three most dominant species together (\u003cem\u003eE. lanigerum\u003c/em\u003e (69.93%), \u003cem\u003eDysaphis\u003c/em\u003e spp. (13.97%) and \u003cem\u003eR. insertum\u003c/em\u003e (7.67%)).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eAphids in the orchard alleys\u003c/h2\u003e \u003cp\u003eWe collected 16 aphid species in the orchard alleys (see Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e of Appendix 1), and the overall abundance of aphids varied according to the sampling period (Pseudo-F\u003csub\u003e2,47\u003c/sub\u003e = 12.82, P\u0026thinsp;=\u0026thinsp;0.0002) (Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003eA). There was no significant effect of the orchard management system on overall aphid abundance (Pseudo-F\u003csub\u003e1,47\u003c/sub\u003e = 0.94, P\u0026thinsp;=\u0026thinsp;0.348), and no significant interaction between management and sampling period was found (Pseudo-F\u003csub\u003e2,47\u003c/sub\u003e = 0.16, P\u0026thinsp;=\u0026thinsp;0.859). Figure\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003eB shows the averaged abundance of major aphid pests of apple such as \u003cem\u003eDysaphis\u003c/em\u003e spp., \u003cem\u003eR. insertum\u003c/em\u003e and \u003cem\u003eE. lanigerum\u003c/em\u003e according to the sampling period. The abundances of \u003cem\u003eDysaphis\u003c/em\u003e spp., \u003cem\u003eR. insertum\u003c/em\u003e and \u003cem\u003eE. lanigerum\u003c/em\u003e accounted for 57.12%, 10.40%, and 3.02%, respectively, of all collected aphids during the study period.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe Gini-Simpson diversity index of aphid communities in the orchard alleys did not differ significantly between sampling periods (Pseudo-F\u003csub\u003e2,46\u003c/sub\u003e = 2.79, P\u0026thinsp;=\u0026thinsp;0.081) or orchard management systems (Pseudo-F\u003csub\u003e2,46\u003c/sub\u003e = 0.26, P\u0026thinsp;=\u0026thinsp;0.626), and the interaction term between management and period was not significant (Pseudo-F\u003csub\u003e2,46\u003c/sub\u003e = 1.03, P\u0026thinsp;=\u0026thinsp;0.374).\u003c/p\u003e \u003cp\u003eThe species composition of aphid communities in the orchard alleys differed significantly between the sampling periods (Pseudo-F\u003csub\u003e2,47\u003c/sub\u003e = 7.96, P\u0026thinsp;=\u0026thinsp;0.0001) but not between management systems (Pseudo-F\u003csub\u003e1,47\u003c/sub\u003e = 1.18, P\u0026thinsp;=\u0026thinsp;0.336). Pest management systems significantly affected the species composition of aphid communities in the orchard alleys depending on the sampling period (Pseudo-F\u003csub\u003e2,47\u003c/sub\u003e = 1.91, P\u0026thinsp;=\u0026thinsp;0.037). Pairwise post-hoc tests between sampling periods conducted within either organic or IPM orchards revealed significant differences in species composition between all sampling periods (Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Pairwise post-hoc tests conducted between management systems within each sampling period revealed significant differences in species composition only during the fruit-setting period, with 2.2 times higher overall aphid abundances observed in organic orchards (27.10\u0026thinsp;\u0026plusmn;\u0026thinsp;3.94) compared to IPM (12.38\u0026thinsp;\u0026plusmn;\u0026thinsp;2.54) (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eDifferences in species composition between the sampling periods in each management system\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"6\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eSampling period\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eIPM\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c6\" namest=\"c5\"\u003e \u003cp\u003eOrganic\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003et\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eP\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003et\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eP\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFruit-growing vs. Fruit-setting\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2.02\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.020\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e2.135\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0.008\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFruit-growing vs. Post-harvest\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e2.57\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.009\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e2.380\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0.013\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFruit-setting vs. Post-harvest\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1.90\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.016\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e2.520\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0.006\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eDifferences in species composition between pest management systems in each of the three sampling periods\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"9\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c6\" colnum=\"6\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c7\" colnum=\"7\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c8\" colnum=\"8\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c9\" colnum=\"9\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003eManagement\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c3\" namest=\"c2\"\u003e \u003cp\u003eFruit-setting\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c6\" namest=\"c5\"\u003e \u003cp\u003eFruit-growing\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colspan=\"2\" nameend=\"c9\" namest=\"c8\"\u003e \u003cp\u003ePost-harvest\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003et\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eP\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003et\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c6\"\u003e \u003cp\u003eP\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c8\"\u003e \u003cp\u003et\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c9\"\u003e \u003cp\u003eP\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eOrganic vs. IPM\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1.55\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.032\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c5\"\u003e \u003cp\u003e1.043\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c6\"\u003e \u003cp\u003e0.335\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c7\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c8\"\u003e \u003cp\u003e1.108\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c9\"\u003e \u003cp\u003e0.303\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003cem\u003eMacrosiphum euphorbiae\u003c/em\u003e showed the most pronounced difference in average abundance between management systems during the fruit-setting stage (Fig.\u0026nbsp;\u003cspan refid=\"Fig5\" class=\"InternalRef\"\u003e5\u003c/span\u003e), followed by \u003cem\u003eDysaphis\u003c/em\u003e spp., \u003cem\u003eAphis spiraecola\u003c/em\u003e, and \u003cem\u003eRhopalosiphum insertum\u003c/em\u003e in decreasing order (Table\u0026nbsp;5).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eAphid species which contributed to at least 70% of the dissimilarity in aphid communities in alleys between organic and IPM orchards during the fruit-setting period with log(X\u0026thinsp;+\u0026thinsp;1) transformed mean abundances in both management systems, individual contributions and cumulative contribution to community dissimilarity.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"5\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eIPM\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eOrganic\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e\u0026nbsp;\u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eSpecies\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003eMean Abundance\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003eMean Abundance\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003eContribution %\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003eCumulative %\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMacrosiphum euphorbiae\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1.92\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e27.40\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e27.40\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eDysaphis\u003c/em\u003e spp.\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1.50\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e2.12\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e24.45\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e51.85\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAphis spiraecola\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.79\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.42\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e13.00\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e64.85\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eRopalosiphum insertum\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.88\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1.18\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e \u003cp\u003e13.00\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c5\"\u003e \u003cp\u003e77.85\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eA comparison of the compositional similarity between aphid communities in the canopy to communities in the orchard alley of the same plot at the same sampling period indicates that the two communities in different habitats were not significantly related (non-parametric Mantel test ρ\u0026thinsp;=\u0026thinsp;0.01, P\u0026thinsp;=\u0026thinsp;0.425).\u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eThe species composition of aphid communities in the canopy did not differ significantly between organic and IPM orchards, but communities in organic orchards had a greater evenness compared to IPM orchards. Seasonality on the other hand had a significant effect on aphid community structure across sampling periods both in the tree canopy and the orchard alleys. The species composition of aphid communities in the alley differed significantly between organic and IPM orchards, but only in the fruit-setting period. These results highlight the importance of considering seasonality and habitats when comparing pest management systems, as both affect the composition of aphid communities, which may affect the effectiveness of management practices.\u003c/p\u003e \u003cp\u003eThe overall abundance of all aphids and the species composition of aphid communities in the canopy of apple trees were mainly influenced by seasonality, regardless of orchard management system. Aphid populations are known to fluctuate significantly over time due to factors such as climate, host plant phenology and aphid biology (Dixon 2003; Llewellyn et al. 2003; Sheppard et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). Indeed, the phenological stages of the host plant can influence the availability of resources for aphids, further affecting their population dynamics (Dedryver et al. \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2010\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eWe observed relatively low abundances of \u003cem\u003eDysaphis\u003c/em\u003e spp. during the fruit-setting and throughout the fruit-growing period in the tree canopy, but a significant increase in \u003cem\u003eDysaphis\u003c/em\u003e spp. populations after harvest. This can be explained by the fact that \u003cem\u003eD. plantaginea\u003c/em\u003e, which is the most common species of the \u003cem\u003eDysaphis\u003c/em\u003e group on apple trees, migrates to its alternative host \u003cem\u003ePlantago\u003c/em\u003e spp. (plantain) in summer (fruit-setting period onward), where it continues its life cycle until returning to apple trees in autumn (post-harvest period) to deposit overwintering eggs (Blommers et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). Similar observations have been made for \u003cem\u003eR. insertum\u003c/em\u003e, which is known to migrate to grasses in late summer and autumn (Petrović-Obradović \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Moreover, control of \u003cem\u003eR. insertum\u003c/em\u003e and \u003cem\u003eD. plantaginea\u003c/em\u003e populations in apple orchards often involves early insecticide applications, consisting of sprays in March-June for \u003cem\u003eD. plantaginea\u003c/em\u003e control which has a relatively low action threshold level for insecticide application compared to other pests of apple (Cooke et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e1976\u003c/span\u003e; Barbagallo et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Cahenzli et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Lefebvre et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). This early spraying could further explain the low abundances of these pests in the canopy at the beginning of our sampling campaign in IPM orchards. On the other hand, the abundance of the monoecious species \u003cem\u003eE. lanigerum\u003c/em\u003e in the tree canopy increased throughout the growing season. \u003cem\u003eEriosoma lanigerum\u003c/em\u003e is known to thrive particularly well on Jonagold apple trees and their related varieties (Hao et al. 2020; Tan et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Due to recurrent infestations, treatments to control this aphid are usually applied multiple times throughout the season (Madsen and Bailey \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e1958\u003c/span\u003e; Shaw and Wallis \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2009\u003c/span\u003e). Apart from the known apple pests (\u003cem\u003eDysaphis\u003c/em\u003e spp., \u003cem\u003eE. lanigerum\u003c/em\u003e, \u003cem\u003eR. insertum\u003c/em\u003e, \u003cem\u003eA. pomi\u003c/em\u003e, \u003cem\u003eA. spiraecola\u003c/em\u003e) and polyphagous aphid species such as \u003cem\u003eMyzus persicae\u003c/em\u003e, \u003cem\u003eM. ornatus\u003c/em\u003e, \u003cem\u003eMacrosiphum euphorbiae\u003c/em\u003e, \u003cem\u003eM. rosae\u003c/em\u003e, \u003cem\u003eAphis fabae\u003c/em\u003e, \u003cem\u003eTherioaphis trifolii\u003c/em\u003e, \u003cem\u003eBrachycaudus helichrysi\u003c/em\u003e, and \u003cem\u003eHyperomyzus lactucae\u003c/em\u003e, other aphid species found in the tree canopy can be considered as random occurrences.\u003c/p\u003e \u003cp\u003eIn this study, aphid abundances and the species composition of aphid communities in the tree canopy were not significantly influenced by the orchard pest management system. The absence of a significant effect could be attributed to the wide range of practices within organic and IPM orchards in Europe (Hatteland et al. 2023). In a study across several European countries, Happe et al. (\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2018\u003c/span\u003e) reported that factors such as adjacent woody habitat and landscape characteristics had a significant effect on aphid populations, while the orchard management system (IPM vs. organic) did not consistently affect aphid abundance. This highlights the importance of the agroecosystem context as a whole, rather than only considering the local orchard management system. However, in this study, several apple orchards were located in close proximity to each other, which limited our ability to conduct landscape analyses and assess the influence of landscape characteristics on aphid infestation across management systems.\u003c/p\u003e \u003cp\u003eIn contrast to overall abundance or species composition, the evenness of canopy aphid communities was significantly influenced by the orchard pest management system. Aphid communities showed greater evenness in organic orchards compared to IPM orchards, but the evenness did not vary significantly across different sampling periods- This result suggests, that the orchard management system plays a more important role in shaping the dominance structure in the tree canopy than the apple growth stage. Brown and Adler (\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e1989\u003c/span\u003e) reported that the evenness of aphid communities was significantly greater in abandoned and organic orchards compared to conventionally managed orchards. Although IPM practices are often more environmentally friendly than conventional methods, they involve the use of selective synthetic pesticides (Damos et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). This can result in lower evenness in IPM orchards as some species are more susceptible to pesticides than others, allowing a few species to dominate the sprayed habitat (Hole et al. \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). Higher evenness in organic orchards can potentially contribute to more effective natural pest control, as more even aphid communities may support a more diverse range of natural enemies in different seasons, reducing the risk of pest outbreaks through facilitating complex food webs (Landis et al. \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2000\u003c/span\u003e; Lundgren and Fausti \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2015\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe woolly apple aphid \u003cem\u003eEriosoma lanigerum\u003c/em\u003e, was the most dominant aphid species in both organic and IPM apple orchards in the tree canopy. Previous studies have shown that \u003cem\u003eE. lanigerum\u003c/em\u003e forms dense colonies on apple trees in summer, making it a major pest of apple under different orchard management practices (Heunis and Pringle \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Stokwe and Malan \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). In addition, Jonagold apple trees and their related varieties are known to be particularly susceptible to \u003cem\u003eE. lanigerum\u003c/em\u003e infestation (Tan et al. \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The high dominance of \u003cem\u003eE. lanigerum\u003c/em\u003e populations in IPM orchards may be attributed to lower predation pressure compared to organic orchards, which often support more robust populations of natural enemies, such as earwigs (Happe et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Furthermore, synthetic insecticides on which commercial IPM systems mostly rely, have been found to be less effective in reaching and controlling woolly apple aphid colonies on the roots, which can serve as a persistent source of re-infestation for the above-ground parts of the tree (Nicholas et al. \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2003\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eIn the orchard alleys, the significant variation in aphid abundance and species composition of aphid communities between sampling periods may be attributed to the nature of aphid life cycles (Harrington et al., \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). Many species, such as \u003cem\u003eD. plantaginea\u003c/em\u003e and \u003cem\u003eR. insertum\u003c/em\u003e, have heteroecious life cycles, alternating between apple trees and other host plants, including agricultural weeds found in orchard alleys (Blommers et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Petrović-Obradović \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). These weeds provide habitats for aphids at different stages of their life cycle and support aphid populations as they migrate away from apple trees. Despite its monoecious life cycle, the presence of \u003cem\u003eE. lanigerum\u003c/em\u003e in orchard alleys can be explained by movements between root and canopy populations of \u003cem\u003eE. lanigerum\u003c/em\u003e (Heunis and Pringle \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Orpet et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Orpet et al. (\u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2019\u003c/span\u003e) found that managing these movements through soil amendments (sandy soils, mulching) can help in preventing \u003cem\u003eE. lanigerum\u003c/em\u003e root feeding. However, we did not find a significant relationship between the species composition of aphid communities in the canopy and orchard alleys in our study.\u003c/p\u003e \u003cp\u003eThe species composition of aphid communities differed significantly between organic and IPM orchards in the orchard alley during the fruit-setting. This result highlights the importance of tailoring management strategies to the temporal dynamics of aphid populations. A study by Hull and VanStarner (\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e1983\u003c/span\u003e) demonstrated that early insecticide applications, timed to the hatching of overwintering eggs, were more effective in successfully controlling aphid populations than later applications. In addition, management practices such as mechanical weed control underneath the trees in organic orchards and herbicide use in IPM orchards further influence aphid dynamics (Happe et al. \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Mark\u0026oacute; et al. (2013) found that different ground cover treatments, such as flowering plants and mowed grass, can significantly impact aphid infestation and the diversity of beneficial insects. Fr\u0026eacute;chette et al. (2008) further demonstrated that different systems of ground cover influence the abundance and performance of aphid predators. The results of the SIMPER analyses indicated that \u003cem\u003eM. euphorbiae\u003c/em\u003e, \u003cem\u003eDysaphis\u003c/em\u003e spp., \u003cem\u003eA. spiraecola\u003c/em\u003e, and \u003cem\u003eR. insertum\u003c/em\u003e contributed to the differences in the species composition of aphid communities between organic and IPM orchards during the fruit-setting period. This suggests that management practices in organic and IPM systems influence aphid communities in the orchard alleys differently, possibly due to variations in pesticide usage (Malagnoux et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), natural enemy populations (Dib et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2016\u003c/span\u003e), and habitat structure within the orchards (Mark\u0026oacute; et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). These differences are particularly significant during the fruit-setting period (early summer), when plants in the orchard alleys are still green and providing favourable developmental conditions for aphids. The polyphagous \u003cem\u003eA. spiraecola\u003c/em\u003e, was the only species that had a higher abundance in the orchard alley of IPM orchards compared to organically managed orchards. This could be due to its known resistance to synthetic insecticides classes such as neonicotinoids and organophosphates (Lowery et al. \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Smirle et al. \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2010\u003c/span\u003e).\u003c/p\u003e"},{"header":"Conclusion","content":"\u003cp\u003eOur study shows that overall aphid numbers and species composition in in the tree canopy do not differ significantly between organic and IPM orchards. However, the greater evenness of aphid communities in organic orchards suggests a more balanced species distribution, which could be beneficial in maintaining natural biological control in orchards. \u003cem\u003eEriosoma lanigerum\u003c/em\u003e was the most dominant species in both orchard systems, with a particularly high dominance in IPM orchards, which highlights the need for specific management strategies to control this pest in orchards with susceptible apple varieties such as Jonagold. The species composition and presence of pest species such as \u003cem\u003eM. euphorbiae\u003c/em\u003e, \u003cem\u003eDysaphis\u003c/em\u003e spp., \u003cem\u003eA. spiraecola\u003c/em\u003e and \u003cem\u003eR. insertum\u003c/em\u003e varied significantly across different stages of the apple growing season, with notable differences between organic and IPM orchards during the fruit-setting period in the orchard alleys. Our results stress the importance of considering both seasonality and differences between habitats when assessing aphid infestations in orchards. Consequently, we conclude that tailored pest management strategies, which account for the dynamics of aphid populations in orchard habitats and throughout different stages of the apple growing season, are essential to optimise pest management practices. Implementing these strategies can significantly reduce aphid infestations, ultimately leading to improved yields and quality.\u003c/p\u003e"},{"header":"Statements and Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgments\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors wish to thank Mohammad Hossain for his assistance during fieldwork, and all apple growers who participated in this study. This work was supported by a scholarship to Ingrid Aline Bapfubusa Niyibizi from the German Academic Exchange Service (Deutscher Akademischer Austauschdienst, DAAD) and by funding from the Graduate Research School of the Brandenburg University of Technology Cottbus-Senftenberg to Benjamin Schnerch.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis work was supported by a scholarship to Ingrid Aline Bapfubusa Niyibizi from the German Academic Exchange Service (Deutscher Akademischer Austauschdienst, DAAD) and by funding from the Graduate Research School of the Brandenburg University of Technology Cottbus-Senftenberg to Benjamin Schnerch.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting Interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors have no relevant financial or non-financial interests to disclose.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eDeclaration of competing interest\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor Contributions\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eKB and BS contributed to the study conception and design. Material preparation, data collection and analysis were performed by IABN, BS and KB. The first draft of the manuscript was written by IABN. EAD and all other authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eData availability statement\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n \u003cli\u003eAlhmedi, A., Bylemans, D., Bangels, E., \u0026amp; Beli\u0026euml;n, T. (2022). Cultivar-mediated effects on apple\u0026ndash;Dysaphis plantaginea interaction. Journal of Pest Science, 95(1303-1315). https://doi.org/10.1007/s10340-021-01460-6\u003c/li\u003e\n \u003cli\u003eAltieri, M. A., \u0026amp; Nichols, C. I. (2004). Biodiversity and pest management in agroecosystems (2nd ed.). Binghamton, NY: The Haworth Press Inc.\u003c/li\u003e\n \u003cli\u003eAnderson, M. J., Gorley, R. N., \u0026amp; Clarke, K. R. (2008). PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK.\u003c/li\u003e\n \u003cli\u003eAndreev, R., Rasheva, D., \u0026amp; Kutinkova, H. (2007). Aphids in apple orchards in Central-South Bulgaria. Journal of Plant Protection Research, 47(1), 87\u0026ndash;90.\u003c/li\u003e\n \u003cli\u003eBarbagallo, S., Bosio, G., \u0026amp; Pansa, M. G. (2017). The aphid species in Italian apple orchards and their phenology. Bulletin of Insectology, 70(1), 77-87.\u003c/li\u003e\n \u003cli\u003eBarbagallo, S., Cocuzza, G., Cravedi, P., \u0026amp; Komazaki, S. (2007). IPM case studies: Deciduous fruit trees. In Harrington, R. (Ed.), Van Emden, H. F. (Ed.), Aphids as crop pests (pp. 651\u0026ndash;661). CABI. https://doi.org/10.1079/9780851998190.0651\u003c/li\u003e\n \u003cli\u003eBat\u0026aacute;ry, P., Gall\u0026eacute;, R., Riesch, F., Fischer, C., Dormann, C. F., Mu\u0026szlig;hoff, O., Cs\u0026aacute;sz\u0026aacute;r, P., Fusaro, S., Gayer, C., Happe, A.-K., Kurucz, K., Moln\u0026aacute;r, D., R\u0026ouml;sch, V., Wietzke, A., \u0026amp; Tscharntke, T. (2017). The former Iron Curtain still drives biodiversity\u0026ndash;profit tradeoffs in German agriculture. Nature Ecology \u0026amp; Evolution, 1(1279\u0026ndash;1284). https://doi.org/10.1038/s41559-017-0272-x\u003c/li\u003e\n \u003cli\u003eBlommers, L., Helsen, H., \u0026amp; Vaal, F. (2004). Life history data of the rosy apple aphid Dysaphis plantaginea (Pass.) (Homopt. Aphididae) on plantain and as migrant to apple. Journal of Pest Science, 77, 155-163. https://doi.org/10.1007/s10340-004-0046-5\u003c/li\u003e\n \u003cli\u003eBogya, S., Marko, V., \u0026amp; Szinetar, C. S. (2000). Effect of pest management systems on foliage- and grass-dwelling spider communities in an apple orchard in Hungary. International Journal of Pest Management, 46(4), 241-250. https://doi.org/10.1080/09670870050206000\u003c/li\u003e\n \u003cli\u003eBoller, E. F., Avilla, J., Joerg, E., Malavolta, C., Wijnands, F. G., \u0026amp; Esbjerg, P. (2004). Integrated production - principles and technical guidelines. IOBC/wprs Bulletin, 27, 1\u0026ndash;49.\u003c/li\u003e\n \u003cli\u003eBostanian, N. J., Goulet, H., O\u0026rsquo;Hara, J., Masner, L., \u0026amp; Racette, G. (2004). Towards insecticide-free apple orchards: Flowering plants to attract beneficial arthropods. Biocontrol Science \u0026amp; Technology, 14, 25\u0026ndash;37.\u003c/li\u003e\n \u003cli\u003eBrown, M., \u0026amp; Glenn, D. (1999). Ground cover plants and selective insecticides as pest management tools in apple orchards. Journal of Economic Entomology, 92, 899-905. https://doi.org/10.1093/JEE/92.4.899\u003c/li\u003e\n \u003cli\u003eBrown, M. W., \u0026amp; Adler, C. R. L. (1989). Community structure of phytophagous arthropods on apple. Environmental Entomology, 18(4), 600-607.\u003c/li\u003e\n \u003cli\u003eBrown, M. W., Schmitt, J. J., Ranger, S., \u0026amp; Hogmire, H. W. (1995). Yield reduction in apple by edaphic woolly apple aphid (Holnoptera: Aphididae) populations. Journal of Economic Entomology, 88(1), 127-133. https://doi.org/10.1093/jee/88.1.127\u003c/li\u003e\n \u003cli\u003eCahenzli, F., Pfiffner, L., \u0026amp; Daniel, C. (2017). Reduced crop damage by self-regulation of aphids in an ecologically enriched insecticide-free apple orchard. Agronomy for Sustainable Development, 37, Article 65. https://doi.org/10.1007/s13593-017-0476-0\u003c/li\u003e\n \u003cli\u003eClarke, K. R., \u0026amp; Gorley, R. N. (2015). PRIMER v7: User Manual/Tutorial. PRIMER-E, Plymouth, UK.\u003c/li\u003e\n \u003cli\u003eCooke, B., Herrington, P., Jones, K., \u0026amp; Morgan, N. (1976). Pest and disease control with low doses of pesticides in low and ultralow volumes applied to intensive apple trees. Pesticide Science, 7, 30-34. https://doi.org/10.1002/PS.2780070105\u003c/li\u003e\n \u003cli\u003eCross, J. V., Cubison, S., Harris, A., \u0026amp; Harrington, R. (2007). Autumn control of rosy apple aphid Dysaphis plantaginea (Passerini) with aphicides. Crop Protection, 26, 1140\u0026ndash;1149.\u003c/li\u003e\n \u003cli\u003eCrowder, D. W., Northfield, T. D., Strand, M. R., \u0026amp; Snyder, W. E. (2010). Organic agriculture promotes evenness and natural pest control. Nature, 466(7302), 109-112.\u003c/li\u003e\n \u003cli\u003eDamos, P., Escudero Colomar, L.-A., \u0026amp; Ioriatti, C. (2015). Integrated fruit production and pest management in Europe: The apple case study and how far we are from the original concept? \u003cem\u003eInsects, 6\u003c/em\u003e(3), 626\u0026ndash;657. https://doi.org/10.3390/insects6030626\u003c/li\u003e\n \u003cli\u003eDe Berardinis, E., Baronio, P., \u0026amp; Baumg\u0026auml;rtner, J. (1994). The effect of aphid (Dysaphis plantaginea Pass. Hom.Aphididae) feeding on apple fruit growth. Ecological Modelling, 72, 115\u0026ndash;127.\u003c/li\u003e\n \u003cli\u003eDedryver, C. A., Le Ralec, A., \u0026amp; Fabre, F. (2010). The conflicting relationships between aphids and men: A review of aphid damage and control strategies. Comptes Rendus Biologies, 333(6-7), 539-553.\u003c/li\u003e\n \u003cli\u003eDib, H., Sauphanor, B., \u0026amp; Capowiez, Y. (2016). Effect of management strategies on arthropod communities in the colonies of rosy apple aphid Dysaphis plantaginea Passerini (Hemiptera: Aphididae) in south-eastern France. Agriculture, Ecosystems \u0026amp; Environment, 216.\u003c/li\u003e\n \u003cli\u003eDib, H., Simon, S., Sauphanor, B., \u0026amp; Capowiez, Y. (2010). The role of natural enemies on the population dynamics of the rosy apple aphid Dysaphis plantaginea Passerini (Hemiptera: Aphididae) in organic apple orchards in south-eastern France. Biological Control, 55, 97-109. https://doi.org/10.1016/J.BIOCONTROL.2010.07.005\u003c/li\u003e\n \u003cli\u003eDutcher, J. D. (2007). A review of resurgence and replacement causing pest outbreaks in IPM. In A. Ciancio \u0026amp; K. G. Mukerji (Eds.), General concepts in integrated pest and disease management (Vol. 1, pp. 27-43). Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6061-8_2\u003c/li\u003e\n \u003cli\u003eEC Directive. (2009). EC Directive 2009/128/EC of the European parliament and of the council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides. Official Journal of the European Union, 309:71\u0026ndash;86.\u003c/li\u003e\n \u003cli\u003eEl Jaouhari, M., Damour, G., Tixier, P., \u0026amp; Coulis, M. (2023). Glyphosate reduces the biodiversity of soil macrofauna and benefits exotic over native species in a tropical agroecosystem. Basic and Applied Ecology, 73, 18-26.\u003c/li\u003e\n \u003cli\u003eFeliciano, D. (2022). Factors influencing the adoption of sustainable agricultural practices in the UK. \u003cem\u003eSustainability\u003c/em\u003e, \u003cem\u003e14\u003c/em\u003e(12), 7123. https://doi.org/10.3390/su14127123\u003c/li\u003e\n \u003cli\u003eFern\u0026aacute;ndez, D. E., Cich\u0026oacute;n, L. I., S\u0026aacute;nchez, E. E., Garrido, S. A., \u0026amp; Gittins, C. (2008). Effect of different cover crops on the presence of arthropods in an organic apple (Malus domestica Borkh) orchard. Journal of Sustainable Agriculture, 32(2), 197\u0026ndash;211. https://doi.org/10.1080/10440040802170624\u003c/li\u003e\n \u003cli\u003eFrechette, B., Cormier, D., Chouinard, G., Vanoosthuyse, F., \u0026amp; Lucas, E. (2008). Apple aphid Aphis spp. (Hemiptera: Aphididae) and predator populations in an apple orchard at the non-bearing stage: The impact of ground cover and cultivar. European Journal of Entomology, 105, 521-529. https://doi.org/10.14411/eje.2008.069\u003c/li\u003e\n \u003cli\u003eGraf, B., Baumg\u0026auml;rtner, J., \u0026amp; Delucchi, V. (1985). Simulation models for the dynamics of three apple aphids Dysaphis plantaginea, Rhopalosiphum insertum, and Aphis pomi (Homoptera: Aphididae) in a Swiss apple orchard. Journal of Applied Entomology, 99(1-5), 453-465.\u003c/li\u003e\n \u003cli\u003eHappe, A., Roquer‐Beni, L., Bosch, J., Alins, G., \u0026amp; Mody, K. (2018). Earwigs and woolly apple aphids in integrated and organic apple orchards: Responses of a generalist predator and a pest prey to local and landscape factors. Agriculture, Ecosystems \u0026amp; Environment, 256, 59-65. https://doi.org/10.1016/J.AGEE.2018.09.004\u003c/li\u003e\n \u003cli\u003eHarrington, R., Fleming, R. A., \u0026amp; Woiwod, I. P. (2007). Climate change impacts on insect management and conservation in temperate regions: Can they be predicted? Agricultural and Forest Entomology, 9(3), 233-240.\u003c/li\u003e\n \u003cli\u003eHeunis, J., \u0026amp; Pringle, K. (2006). Field biology of woolly apple aphid Eriosoma lanigerum (Hausmann) and its natural enemy Aphelinus mali (Haldeman) in apple orchards in the Western Cape Province. African Entomology, 14, 77-86.\u003c/li\u003e\n \u003cli\u003eHole, D. G., Perkins, A. J., Wilson, J. D., Alexander, I. H., Grice, P. V., \u0026amp; Evans, A. D. (2005). Does organic farming benefit biodiversity? Biological Conservation, 122(1), 113-130. https://doi.org/10.1016/j.biocon.2004.07.018\u003c/li\u003e\n \u003cli\u003eHull, L., \u0026amp; VanStarner, R. (1983). Effectiveness of insecticide applications timed to correspond with the development of rosy apple aphid (Homoptera: Aphididae) on apple. Journal of Economic Entomology, 76, 594-598. https://doi.org/10.1093/JEE/76.3.594\u003c/li\u003e\n \u003cli\u003eHull\u0026eacute;, M., Turpeau, E., \u0026amp; Chaubet, B. (2006). Encyclop\u0026apos;aphid. INRA. https://www6.inra.fr/encyclopedie-pucerons\u003c/li\u003e\n \u003cli\u003eJeffs, C., \u0026amp; Leather, S. (2014). Effects of extreme fluctuating temperature events on life history traits of the grain aphid Sitobion avenae. Entomologia Experimentalis et Applicata, 150, 89-99. https://doi.org/10.1111/eea.12160\u003c/li\u003e\n \u003cli\u003eJenser, G., Bal\u0026aacute;zs, K., Erd\u0026eacute;lyi, C., Haltrich, A., K\u0026aacute;d\u0026aacute;r, F., Koz\u0026aacute;r, F., Mark\u0026oacute;, V., \u0026amp; R\u0026aacute;cz, V. (1999). Changes in arthropod population composition in IPM apple orchards under continental climatic conditions in Hungary. Agriculture, Ecosystems \u0026amp; Environment, 73(2), 141-154. https://doi.org/10.1016/S0167-8809(99)00023-7\u003c/li\u003e\n \u003cli\u003eLandis, D. A., Wratten, S. D., \u0026amp; Gurr, G. M. (2000). Habitat management to conserve natural enemies of arthropod pests in agriculture. Annual Review of Entomology, 45(1), 175-201.\u003c/li\u003e\n \u003cli\u003eLefebvre, M., Franck, P., Olivares, J., Ricard, J., Mandrin, J., \u0026amp; Lavigne, C. (2017). Spider predation on rosy apple aphid in conventional, organic, and insecticide-free orchards and its impact on aphid populations. Biological Control, 104, 57-65. https://doi.org/10.1016/J.BIOCONTROL.2016.10.009\u003c/li\u003e\n \u003cli\u003eLowery, D., Smirle, M., Foottit, R., Zurowski, C., \u0026amp; Peryea, E. (2005). Baseline susceptibilities to imidacloprid for green apple aphid and spirea aphid (Homoptera: Aphididae) collected from apple in the Pacific Northwest. Journal of Economic Entomology, 98, 188 - 194. https://doi.org/10.1603/0022-0493-98.1.188\u003c/li\u003e\n \u003cli\u003eLundgren, J. G., \u0026amp; Fausti, S. W. (2015). Trading biodiversity for pest problems. \u003cem\u003eScience Advances, 1\u003c/em\u003e(6), e1500558. https://doi.org/10.1126/sciadv.1500558\u003c/li\u003e\n \u003cli\u003eMadsen, H., \u0026amp; Bailey, J. (1958). Woolly and green apple aphids: Field trials with new materials in orchard near Watsonville indicate same timing of spray treatment controls both pests. California Agriculture, 12, 14-16.\u003c/li\u003e\n \u003cli\u003eMalagnoux, L., Marliac, G., Simon, S., \u0026amp; Rault, M. (2015). Management strategies in apple orchards influence earwig community. Chemosphere, 124, 156\u0026ndash;162. https://doi.org/10.1016/j.chemosphere.2014.12.024\u003c/li\u003e\n \u003cli\u003eMalavolta, C., \u0026amp; Cross, J. (2009). Guidelines for integrated production of pome fruits in Europe. IOBC Technical Guideline III, 4th edition. IOBC/wprs Bulletin, 47, 1\u0026ndash;12.\u003c/li\u003e\n \u003cli\u003eMark\u0026oacute;, V., Jenser, G., Kondorosy, E., \u0026Aacute;brah\u0026aacute;m, L., \u0026amp; Bal\u0026aacute;zs, K. (2012). Flowers for better pest control? The effects of apple orchard ground cover management on green apple aphids (Aphis spp.) (Hemiptera: Aphididae), their predators, and the canopy insect community. Biocontrol Science and Technology, 23(2), 126\u0026ndash;145. https://doi.org/10.1080/09583157.2012.743972\u003c/li\u003e\n \u003cli\u003eMoss, D., \u0026amp; Pollard, E. (1993). Calculation of collated indices of abundance of butterflies based on monitored sites. Ecological Entomology, 18, 211-222. https://doi.org/10.1111/j.1365-2311.1993.tb01083.x\u003c/li\u003e\n \u003cli\u003eNagy, C., Cross, J., \u0026amp; Mark\u0026oacute;, V. (2013). Sugar feeding of the common black ant, \u003cem\u003eLasius niger\u003c/em\u003e (L.), as a possible indirect method for reducing aphid populations on apple by disturbing ant-aphid mutualism. \u003cem\u003eBiological Control, 65\u003c/em\u003e(1), 24\u0026ndash;36.\u003c/li\u003e\n \u003cli\u003eNicholas, A., Spooner-Hart, R., \u0026amp; Vickers, R. (2003). Control of woolly aphid \u003cem\u003eEriosoma lanigerum\u003c/em\u003e (Hausmann) (Hemiptera: Pemphigidae) on mature apple trees using insecticide soil-root drenches. Australian Journal of Entomology, 42, 6-11. https://doi.org/10.1046/J.1440-6055.2003.00336.X\u003c/li\u003e\n \u003cli\u003eOrpet, R., Jones, V., Reganold, J., \u0026amp; Crowder, D. (2019). Effects of restricting movement between root and canopy populations of woolly apple aphid. PLoS ONE, 14. https://doi.org/10.1371/journal.pone.0216424\u003c/li\u003e\n \u003cli\u003ePetrović-Obradović, O. (2022). Aphid species (Hemiptera: Aphididae) \u0026ndash; pests of apple. Plant Doctor, 50, 542\u0026ndash;552.\u003c/li\u003e\n \u003cli\u003ePorcel, M., Andersson, G., P\u0026aring;lsson, J., \u0026amp; Tasin, M. (2018). Organic management in apple orchards: Higher impacts on biological control than on pollination. Journal of Applied Ecology. https://doi.org/10.1111/1365-2664.13247\u003c/li\u003e\n \u003cli\u003ePretty, J., \u0026amp; Bharucha, Z. P. (2014). Sustainable intensification in agricultural systems. Annals of Botany, 114, 1571\u0026ndash;1596. https://doi.org/10.1093/aob/mcu205\u003c/li\u003e\n \u003cli\u003eQubbaj, T., Reineke, A., \u0026amp; Zebitz, C. P. W. (2005). Molecular interactions between rosy apple aphids \u003cem\u003eDysaphis plantaginea\u003c/em\u003e and resistant and susceptible cultivars of its primary host Malus domestica. Entomologia Experimentalis et Applicata, 115(1), 145-152. https://doi.org/10.1111/j.1570-7458.2005.00255.x\u003c/li\u003e\n \u003cli\u003eRousselin, A., Bevacqua, D., Sauge, M. H., \u0026amp; others. (2017). Harnessing the aphid life cycle to reduce insecticide reliance in apple and peach orchards: A review. Agronomy for Sustainable Development, 37, 38. https://doi.org/10.1007/s13593-017-0444-8\u003c/li\u003e\n \u003cli\u003eSenior, V. L., Evans, L. C., Leather, S. R., Oliver, T. H., \u0026amp; Evans, K. L. (2020). Phenological responses in a sycamore\u0026ndash;aphid\u0026ndash;parasitoid system and consequences for aphid population dynamics: A 20-year case study. Global Change Biology, 26(5), 2814\u0026ndash;2828. https://doi.org/10.1111/gcb.15015\u003c/li\u003e\n \u003cli\u003eSeufert, V., \u0026amp; Ramankutty, N. (2017). Many shades of gray\u0026ndash; the context-dependent performance of organic agriculture. Science Advances, 3, e1602638. https://doi.org/10.1126/sciadv.1602638\u003c/li\u003e\n \u003cli\u003eShaw, P. W., \u0026amp; Wallis, D. (2008). Biocontrol of pests in apples under integrated fruit production. New Zealand Plant Protection, 61, 333\u0026ndash;337.\u003c/li\u003e\n \u003cli\u003eShaw, P., \u0026amp; Wallis, D. (2009). Early-season use of insecticides for management of woolly apple aphid (\u003cem\u003eEriosoma lanigerum\u003c/em\u003e) in Nelson apple orchards. New Zealand Plant Protection, 62, 291-295. https://doi.org/10.30843/NZPP.2009.62.4819\u003c/li\u003e\n \u003cli\u003eShaw, B., Nagy, C., \u0026amp; Fountain, M. T. (2021). Organic control strategies for use in IPM of invertebrate pests in apple and pear orchards. Insects, 12(12), 1106. https://doi.org/10.3390/insects12121106\u003c/li\u003e\n \u003cli\u003eSheppard, L., Bell, J., Harrington, R., \u0026amp; Reuman, D. (2016). Changes in large-scale climate alter spatial synchrony of aphid pests. Nature Climate Change, 6, 610-613. https://doi.org/10.1038/NCLIMATE2881\u003c/li\u003e\n \u003cli\u003eSmirle, M., Zurowski, C., Lowery, D., \u0026amp; Foottit, R. (2010). Relationship of insecticide tolerance to esterase enzyme activity in \u003cem\u003eAphis pomi\u003c/em\u003e and \u003cem\u003eAphis spiraecola\u003c/em\u003e (Hemiptera: Aphididae). Journal of Economic Entomology, 103, 374 - 378. https://doi.org/10.1603/EC09275\u003c/li\u003e\n \u003cli\u003eStokwe, N., \u0026amp; Malan, A. (2016). Woolly apple aphid \u003cem\u003eEriosoma lanigerum\u003c/em\u003e (Hausmann) in South Africa: Biology and management practices with focus on the potential use of entomopathogenic nematodes and fungi. African Entomology, 24, 267 - 278. https://doi.org/10.4001/003.024.0267\u003c/li\u003e\n \u003cli\u003eTan, X., Yang, Z., Zhou, H., Yang, Q., \u0026amp; Zhou, H. (2021). Resistance performance of four principal apple cultivars to woolly apple aphid \u003cem\u003eEriosoma lanigerum\u003c/em\u003e (Hemiptera: Pemphigidae) by simulated seasonal temperature in northern China. Arthropod-Plant Interactions, 15, 59 - 69. https://doi.org/10.1007/s11829-020-09797-y\u003c/li\u003e\n \u003cli\u003eTilman, D., Lehman, C. L., \u0026amp; Thomson, K. T. (1997). Plant diversity and ecosystem productivity: Theoretical considerations. Proceedings of the National Academy of Sciences, 94(5), 1857-1861.\u003c/li\u003e\n \u003cli\u003eWill, T., Furch, A., \u0026amp; Zimmermann, M. (2013). How phloem-feeding insects face the challenge of phloem-located defenses. Frontiers in Plant Science, 4. https://doi.org/10.3389/fpls.2013.00336\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Agricultural pest, Aphidoidea, Apple production, Habitats, Seasonality, Species composition","lastPublishedDoi":"10.21203/rs.3.rs-5783229/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5783229/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eApple is a major fruit crop worldwide and the most produced fruit in Germany. However, apple orchards face persistent threats from aphid infestations, which can severely compromise fruit yields. In this study we compared aphid infestation levels in commercial apple orchards under organic and Integrated Pest Management (IPM) at three stages of the apple growing season: fruit-setting, fruit-growing and post-harvest, and in two habitats. We sampled eight organic and eight IPM apple orchards in eastern Germany using standardised canopy beating of apple trees and suction sampling in the orchard alleys. Our results indicate no significant differences in canopy aphid infestation between organic and IPM orchards. However, aphid communities in the tree canopy of organic orchards exhibited greater evenness across species compared to IPM orchards. \u003cem\u003eEriosoma lanigerum\u003c/em\u003e consistently dominated the aphid community of the tree canopies in both management systems, highlighting the need for targeted management practices for this pest. Aphid community structure varied significantly across sampling periods in the canopy and orchard alleys. Differences between organic and IPM orchards were observed during the fruit-setting phase in orchard alleys, with higher levels of infestation in organic orchards. Species such as \u003cem\u003eMacrosiphum euphorbiae\u003c/em\u003e, \u003cem\u003eDysaphis\u003c/em\u003e spp., \u003cem\u003eAphis spiraecola\u003c/em\u003e, and \u003cem\u003eRhopalosiphum insertum\u003c/em\u003e contributed to these differences. Our findings provide a better understanding of the temporal dynamics of aphid communities in commercial apple orchards and highlight the importance of pest management strategies that consider different habitats and periods.\u003c/p\u003e","manuscriptTitle":"Higher aphid infestation in the alleys of organic apple orchards compared to IPM during fruit setting in eastern Germany","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2025-01-13 08:43:21","doi":"10.21203/rs.3.rs-5783229/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"e2e6f9d6-3a25-454e-8a34-9d9330a6ccdc","owner":[],"postedDate":"January 13th, 2025","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2025-01-20T15:53:44+00:00","versionOfRecord":[],"versionCreatedAt":"2025-01-13 08:43:21","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-5783229","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5783229","identity":"rs-5783229","version":["v1"]},"buildId":"XKTyCvWXoU3ODBz1xrDgd","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}