Arthropod ecosystem services in apple orchards ... - Wiley Online Library

Ecological Entomology (2015), 40 (Suppl. 1), 82–96

DOI: 10.1111/een.12234

I N S E C T S A N D E C O S Y S T E M S E RV I C E S S P E C I A L I S S U E

Arthropod ecosystem services in apple orchards and their economic beneﬁts J E R R Y C R O S S, 1 M I C H E L L E F O U N T A I N, 1 V I K T O R M A R K Ó 2 and C S A B A N A G Y 1,2 1 East Malling Research, East Malling, U.K. and 2 Department of Entomology, Corvinus University of Budapest, Budapest, Hungary

Abstract. Apple is grown as a long-term perennial crop and orchards provide relatively stable ecological habitats. Only a small proportion of the diverse fauna of arthropods that can inhabit the orchard ecosystem are important pests, the majority of species being minor pests, beneficial or benign. In this paper, the interacting ecosystem services provided by five contrasting naturally occurring arthropod groups in cool temperate apple orchards are reviewed, and their economic benefits broadly quantified. These are: •

The roles of bees and other insects in apple pollination increasing yields and fruit quality, the economic value of which may be significantly underestimated. • Naturally occurring, pesticide-resistant phytoseiid predatory mites and their role in regulating phytophagous mites. They eliminate the need for 1–2 acaricide sprays per annum and the risk of acaricide resistance. • The earwig Forficula auricularia L. and its role in regulating several important apple pests. There is great variability in populations between orchards for reasons not fully understood. It is estimated that F. auricularia reduces insecticide applications by 2–3 per annum and reduces pest damage. • Mutualism between the common black ant Lasius niger (L.) and important pest aphids, the roles of competitors, natural and artificial food sources, and ant exclusion in disrupting mutualism which can foster biocontrol of aphids by generalist predators so greatly reducing the need for sprays. • Beneficial epigeic arthropods and their role in predating the soil dwelling life stages of insect pests. These contribute to the control of pest populations although the level of suppression is not consistent depending on several ecological factors. Key words. Biocontrol, natural enemy, pollination, pollinator, predation, predator.

Introduction Apple is grown as a long-term perennial crop, orchard duration being typically 15–30 years (Nix, 2013). The tree canopy is semi-permanent and apple orchards, thus, provide relatively stable ecological habitats that support a rich and diverse fauna of arthropods. The apple trees in modern orchards are grown on dwarfing rootstocks for productivity, ease of management, and harvesting. They are sensitive to competition from weeds for soil moisture and nutrients, so a weed-free strip with no or sparse herbage is maintained under the trees, in conventional orchards by use of herbicides, to minimise weed competition. Thus, the soil is generally undisturbed by cultivation. Correspondence: Jerry Cross, East Malling Research, New Road, East Malling, Kent ME19 6BJJ, U.K. E-mail: [email protected] 82

Ground herbage (predominantly grass) is usually maintained in the inter-row alleys, usually kept short by regular mowing. Thus, in conventional orchards the soil is largely undisturbed. Additionally, orchards are usually surrounded and often contain hedgerows and/or purpose-planted windbreaks. The plant composition of these ranges from single species [e.g. in England Italian Alder (Alnus cordata Desf.) is widely used for windbreaks] to very diverse, comprising a wide range of woody and herbaceous, often native, species. Species composition of hedgerows and windbreaks varies with region. Unsprayed apple trees support a large fauna of > 2000 arthropod species. Approximately 20% of the total British Auchenorrhyncha and Heteroptera fauna were collected by foliar sampling in three apple orchards in South-East England (Bleicher et al., 2010; Kondorosy et al., 2010) and more than © 2015 The Royal Entomological Society

Arthropod ecosystem services in apple orchards 2500 arthropod species have been reported from apple orchards in Hungary (Mészáros et al., 1984; Markó et al., 1995; Bogya & Markó, 1999; Bogya et al., 2000; Balog et al., 2003; Kutasi et al., 2004; Bleicher et al., 2006; Szabó et al., 2014). About a quarter of the arthropod fauna are pests, a quarter are natural enemies of pests, and the remaining half are benign to the trees, although they are an important part of the food web of other animals including other arthropods (Milaire et al., 1974; H. Steiner, pers. comm.). However, even a small number of sprays of broad-spectrum insecticides are likely to reduce greatly this fauna. The apple is a member of the Rosaceae which has many closely related tree and shrub species [hawthorn (Crataegus sp.), rose (Rosa sp.), rowan (Sorbus sp.) etc.] that are common in the wider environment. Many apple pests occur on other Rosaceae, which provide a source of infestation for apple orchards. Also, some apple pest species may be host alternating, moving to other woody hosts or forbs at various times of the year. Fortunately, only a small proportion of the arthropods that feed on apple are important (key) pests including those that attack the fruit directly, frequently causing damage at low population densities. They are often not effectively regulated by their natural enemies to prevent economic damage and tend to reoccur after control with insecticides [e.g. codling moth (Cydia pomonella (L.)) and rosy apple aphid (Dysaphis plantaginea Passerini)]. A second important pest group are the secondary pests, which are not effectively regulated by their natural enemies after spraying. Outbreaks are caused by natural enemy disturbance. They have a tendency to develop strains resistant to insecticides and are difficult to control chemically [e.g. the fruit tree red spider mite (Panonychus ulmi (Koch))]. The preservation of natural enemies of secondary pests is a crucial part of successful intergrated pest management (IPM). Most other pests are categorised as minor pests that do not cause a reduction in fruit yield or quality, are very localised or sporadic in their occurrence or are easily controlled with insecticides. Successful IPM in apple orchards needs a range of effective methods to control the pests without harming important natural enemies of secondary pests, and having effective and non-disruptive management methods for the myriad of minor pests that can become troublesome from time to time (Cross & Berrie, 2009). In this paper, the interacting ecosystem services provided by five contrasting naturally occurring arthropod groups that are important in cooler temperate apple production regions (England, northern Europe, north America, and New Zealand) are reviewed and their economic benefits broadly quantified in the framework of the economic performance of apple production including the losses caused by pests and the costs of spray programmes used for controlling them. The particular five groups have been chosen because of their importance, the rapidly growing literature about them in the last 5–10 years (pollinators, F. auricularia), the development of pesticide-resistant strains (phytoseiids), and because they differ considerably in their nature and value and the degree to which they are understood, valued and implemented by growers. Further, the roles of disruption of Lasius niger (L.)–aphid mutualism and epigeic predators in apple orchards have been understudied and not previously reviewed.

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General factors and economic performance Economic performance of apple orchards The economic performance of apple orchards varies greatly. In the UK in 2013, for instance, yields usually fell in the range 15–55 t ha−1 and prices varied between €618 and 1051 t−1 giving projected gross outputs ranging from €9270 to 57 784 ha−1 for the worst to the best performing orchards (Nix, 2013) (Table 1). Variable costs from €7882 to 38 532 ha−1 resulted in gross margins of €1388–19 252 ha−1 . The wide range in the economic performance of UK orchards is probably typical of apple orchards worldwide, although the global range is likely to be considerably greater. In any event, losses in yield or quality owing to pests which both decrease gross output (in direct proportion to yield and price reduction) and increase variable costs, can clearly have a severe adverse effect on the economic performance of apple orchards. Reductions owing to pests in the proportion of fruits harvested and graded that meet the Class I quality grade are particularly detrimental as the prices of Class II and juice fruit are usually very low.

Potential losses caused by pests in unsprayed and sprayed apple orchards If uncontrolled, insect pests cause substantial losses in yield and quality in apple production. For example, in a large-scale, 5-year replicated orchard experiment between 2000 and 2004 in the UK, losses as a result of pests in the untreated control plots averaged 43% over 5 years (range 23–57%) reducing the net margin from €7246 to 1596 ha−1 on average [from Cross et al. (2005) using a currency conversion factor of £1.0 = €1.2]. In a further large-scale, 6-year replicated orchard experiment between 2001 and 2006 in the UK, losses as a result of pests in untreated plot averaged 52% over 6 years (range 19–85%) (Berrie & Cross, 2004, 2007). The extent of losses and the pests that caused them varied greatly, but they demonstrate that on average losses owing to pests exceeding 20% can be expected if no effort is made to control them. Commercial orchards are sprayed with insecticides to minimise losses as a result of pests. Most pests of the apple can be controlled very effectively but the degree of control actually achieved depends on many factors including the number of applications and types of insecticides applied and the skill of the grower. In the Berrie and Cross (2004, 2007) study, losses owing to pests in the conventionally managed plots averaged 7% per year over 6 years (range 4–10%).

Spray programmes and costs There is great variability between apple-producing regions of the world in the average number of insecticide applications per season. A survey of pesticide use in commercial apple orchards in the UK in 2012 showed that, on average, apple orchards receive five insecticide sprays per annum (Garthwaite et al., 2012). Another survey of pesticide use on seven commercial

© 2015 The Royal Entomological Society, Ecological Entomology, 40 (Suppl. 1), 82–96

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Table 1. Apple orchard performance and economic factors applied in this paper∗. Economic performance of dessert apple orchards in the UK 2014∗ Low (t ha−1 )

Yield Price (€ t−1 ) Gross output (€ ha−1 year−1 ) Variable costs (€ ha−1 year−1 ) Orchard depreciation Fertilisers/sprays Crop sundries Harvesting Grading packing Packaging Transport Commission/levies Total variable costs (€ ha−1 year−1 ) Gross margin (€ ha−1 year−1 )

High

Reference

15 618 9270

55 1051 57 784

Nix (2013)

301 1046 186 1112 2387 918 1108 816 7882 1388

1978 1745 742 4079 8752 10 098 6089 5052 38 532 19 252

Potential losses caused by pests if orchards are unsprayed with insecticides Unsprayed Plots in organic IPM orchard Robertsbridge 2000–2004 Untreated plots in IPDM trial at EMR 2001–2006 Average expected losses in unsprayed orchards

Routinely sprayed

Reference

43% (23–57%)

–

Cross et al. (2005)

52% (19–85% in different years)

7% (4–10% in different years)

Berrie and Cross (2004, 2007)

>20%

7%

–

Spray programmes No. of insecticide sprays per annum UK Cost of insecticide spray per hectare at full rate. Average dose used (% of label recommended) Cost of a spray application (labour, fuel, tractor) per hectare Cost of a typical insecticide spray programme including application costs

5 €60 (2.34–89.4) 70% (10–100%) €20 €400

Garthwaite et al. (2012) Cross & Walklate (2014)

∗The figures indicate a range within which the performance of most (established) orchards falls. The gross margin is calculated as lower yields less lower costs/higher yields less higher costs. In practice yields are not necessarily so directly linked to costs. A conversion rate of £1.0 = €1.2 has been applied.

apple farms in the U.K. in 2012–2013 showed that the application of pesticides at reduced doses is common, the average dose actually applied being 76% of the full recommended dose on average (Cross & Walklate, 2014). In southern Europe where C. pomonella has up to three generations per annum and is often resistant to insecticides, the number of insecticide applications is greatly affected by whether or not sex pheromone-mating disruption is used for its control. Sauphanor et al. (2009) indicate that in France 5–15 yearly insecticide applications are made in conventional orchards with a 50% decrease in orchards under mating disruption. In contrast, in apple-producing regions where the brown marmorated stink bug Halyomorpha halys Stal. has invaded, very high numbers of insecticide applications (>10 per annum) may be applied (G Krawzyck, pers. comm.). In the U.K., the cost of an application pesticide per hectare (at the full recommended dose) varied greatly between products (permethrin €2.34 ha−1 - chlorantraniliprole €89.4 ha−1 , average estimated to be €60 ha−1 ) (Cross & Walklate, 2014). Spray applications typically take 35 min ha−1 (including 25 min spraying time at 6 km h−1 on a 4 m row spacing) and cost typically ∼€20 ha−1

including labour, fuel, and depreciation on tractor and spray machinery and taking into account that more than one pesticide is included in most spray applications. Thus, a typical U.K. insecticide programme of five sprays/annum costs the grower an estimated €400 ha−1 per annum. Note that this does not include the cost of regular (normally fortnightly) monitoring orchards for pests and diseases. The cost of provision of these services by an experienced agronomist under contract is currently €100–120 ha−1 per season in the U.K.

Ecosystem services provided by different arthropod taxa and their economic value The role of wild and managed insects in providing apple pollination services Pollination underpins the sustainable production of apple, but most apple varieties are self-incompatible, all varieties do not bloom in unison and, therefore, insect pollinators are needed to move adequately pollen from variety to variety (Thomson


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& Goodell, 2001). Managed honeybees and bumblebees, and native, wild bees play a key role in the delivery of pollination services to the fruit industry (Delaplane & Mayer, 2000; Klein et al., 2007).

2009; Andersson et al., 2013; Morandin & Kremen, 2013). This provision will increase the diversity and numbers of wild cross-pollinated flowers and encourage other beneficial insects including parasitoids, hoverflies, Orius, and anthocorids into the orchards. Insect pollinators of apple (primarily bees) need;

Abundance. In recent years, pollinating insects have declined (Biesmeijer et al., 2006; Potts et al., 2010; Fox et al., 2011; Carvalheiro et al., 2013); the causes of which are likely a consequence of multiple anthropogenic pressures (Vanbergen, 2013), including disease and parasites (Morse & Flottum, 1997; Fürst et al., 2014). Wild bees, dominated by Andrenidae, make up to two-thirds of apple blossom visitors (Gardner & Ascher, 2006; Fountain, 2011; Garratt et al., 2013) and probably make a significant contribution to apple pollination (Klein et al., 2007). Conversely, honeybees can be less effective pollinators in some crops (e.g. Willmer et al., 1994; Thomson & Goodell, 2001; Westerkamp, 2005). In comparison to solitary bees, honeybees can exhibit lower activity in adverse weather conditions (Vicens & Bosch, 2000a), different foraging behaviour (sometimes focused on nectar rather than pollen collection), and dissimilar anatomy for pollen collection [pollen in corbicula rather than in dense hairs (scopae) where the pollen may be more accessible to the stigma]. However, increasing the numbers of foraging honeybees in apple can improve cross-pollination (Stern et al., 2001). Solitary bees can promote seed-set, reducing misshapen fruits (Ladurner et al., 2004), and they forage for shorter distances (Greenleaf et al., 2007) than bumblebees and honeybees (Zurbuchen et al., 2010). For this reason, they may be more influenced by orchard management practices, surroundings, and nearby habitat resources.

1 2 3 4 5

Ecosystem services. Pollinating insects provide a key ecosystem service pollinating flowering plants, ensuring seed and/or fruit set and safeguarding flowering plant success, providing resources for other animals (Potts et al., 2003). Pollinators are an important part of food webs, as prey or hosts for other organisms. Some pollinators, e.g. hoverflies, may also play a role in predation at the larval stage. A reduction of the diversity of pollinating insects can reduce the resilience (Brittain et al., 2013) of pollinating communities and hence the pollination services they deliver. Increasing the intensification of modern apple orchards could put a strain on these services as more apple blossoms are produced in a given area to provide higher yields. In Asia, the use of sprays of pollen in pear orchards has been practiced (e.g. Sakamoto et al., 2009) and is now used commercially to achieve an adequate pear fruit set in poor weather conditions in the Netherlands. Enhancement of populations. Some orchard management practices, e.g. narrow mown headlands of grass with minimal forage and poor diversity hedgerows, do not deliver the food resource needed to increase pollinator abundance and diversity. Flower-rich field margins, restoring species-rich grassland, functional hedgerows, and farm heterogeneity can enhance wild pollinators in the crop (e.g. Ricketts et al., 2008; Potts et al.,

somewhere to nest undisturbed, plentiful and diverse forage throughout the lifecycle, undisturbed areas for overwintering, connectivity of populations and the minimised use of insecticides.

Susceptibility to insecticides. As a result of the high water volumes and air-assisted spray equipment used to obtain adequate spray coverage in orchards, insecticide residues will be present over the whole cropping area, including the alleyways. The effects of some major insecticides on non-target species in ecosystems, such as bees, is under scrutiny and has been reviewed in a recent publication by Pisa et al. (2015). Insecticide effects have impacts at the population and sublethal level (Cresswell, 2011), but there is a major knowledge gap regarding impacts and many of the test protocols have been considered inadequate (Pisa et al., 2015). Research on this subject continues, but realistic large-scale field trials with long-range foraging bees continue to be a challenge, and very little data exists currently for insecticide effects on wild solitary bees in orchards. Rundlöf et al. (2015) have recently demonstrated that the neonicotinoid insecticide clothianidin and the non-systemic pyrethroid 𝛽-cyfluthrin, applied as a seed treatment to oilseed rape seeds, reduces wild bee density, solitary bee nesting, and bumblebee colony growth and reproduction under field conditions. Further research is needed into the possible effects on wild bees of neonicotinoid insecticides that are or may be used as foliar sprays in apple orchards (acetamiprid, imidacloprid, thiacloprid and thiamethoxam). Honeybee toxic insecticides from other chemical groups are currently approved for use as foliar sprays in many countries (e.g. the organophosphorus (OP) chlorpyrifos and the juvenile hormone analogue Insect Growth Regulator fenoxycarb are currently approved in the U.K.). Use of such insecticides is prohibited during flowering but use at other times may pose a significant risk to wild bees in apple orchards e.g. because they are foraging on flowering ground herbage or honeydew excreted by insects in the orchard or its surrounds.

Economic value of the ecosystem services provided in orchards. Differences in bee species functional traits result in greater pollinator richness improving the quantity and quality of pollination (Blüthgen & Klein, 2011); increasing the proportion seed or fruit set and product quality (e.g. fruit size and shape) (Garibaldi et al., 2014). There is evidence that fruit quality (e.g. sugar and mineral content) is highly dependent on adequate levels of pollination (e.g. Wei et al., 2002; Buccheri & Di Vaio, 2004; Blazek & Hlusickova, 2006). The seed number affects the apple shape, and weight (Buccheri & Di Vaio, 2004; Garratt et al., 2013), and the incidence of misshapen fruits is higher when the seed number is low.


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More recent estimates for the pollination service provided by insects to the U.K. fruit industry were >€240 M per annum (NEA, 2011). However, by enhancing the yield of high-value crops, this could be increased by €516–612 M per annum (Breeze et al., 2011). The apple has a market value of €122 M per annum in the U.K. with insect pollinators contributing ∼€104 M per annum (NEA, 2011). Using field trials, a more refined estimate of crop economic value was made by Garratt et al. (2014). In this study, the effect of insect pollination on the quality of cv. Gala and Cox apples were assessed. The estimated value that insects contributed to these varieties (yield and quality) was €44 M per annum for U.K. cropping; equating to a deficit of >€7.2 M which could, potentially, be realised by better pollination. The results were variety specific with less pronounced effects on cv. Cox quality compared with cv. Gala. By encouraging and enhancing insect pollination in apple orchards, it may be possible to raise standards for apple quality and ensure enhanced yields.

Key knowledge gaps. A greater understanding of crop management practices on wild solitary bees would help mitigation procedures to be put into practice. This would benefit wild insect pollinators of apple and ensure reliable crop pollination from year to year.

Phytoseiid predatory mites Phytoseiid predatory mites are very important predators of phytophagous mites in apple orchards and there have been several extensive reviews of their role (van de Vrie, 1985; Solomon et al., 2000; Gregory et al., 2013). Several species occur on unsprayed apple trees, but in selectively sprayed orchards in temperate north and central Europe Typhlodromus pyri Scheuten predominates though recently Amblyseius andersoni Chant has become dominant in many regions e.g. in France (Tixier et al., 2014) and Hungary (Szabó et al., 2014). In spring and summer, phytoseiids are mainly present on the undersides of leaves often tucked under the side of the main leaf vein where it meets a secondary vein. There are 3–4 generations per year. The nymphal and adult stages are active predators of mites, including phytophagous species. After mating in the autumn, females overwinter, in diapause, in deep crevices in the bark of trees, emerging in April or early May.

Abundance. Phytoseiid mite populations are very variable but generally in the range of 0.1–5 per leaf in commercial orchards where phytophagous pest mite populations are low. Much higher populations can occur in response to outbreaks of pest mites. Populations and relative species abundance are affected by many factors e.g. when dense ground vegetation is present in the alleys T. pyri gradually replaces A. andersoni (probably because of wind-borne pollen on the leaves) and the abundance of phytoseiid mites in spring and autumn becomes higher than in the apple orchard plots with bare ground (Markó et al., 2013).

Ecosystem services provided by phytoseiid predatory mites. On unsprayed trees, phytophagous mites including the fruit tree red spider mite P. ulmi and the apple rust mite Aculus schlechtendali (Nalepa) are under continuous predation by phytoseiid mites but also a range of other insect predators. Outbreaks of phytophagous mites are caused by the disturbance of the phytoseiid predatory mite populations. Panonychus ulmi, potentially one of the most destructive pests of apple, was unknown as a pest until the advent of dormant season sprays of tar oil and DNOC to control overwintering insect pests which virtually eradicated overwintering phytoseiid mites but has little effect on the overwintering eggs of P. ulmi (Massee, 1929).

Susceptibility of phytoseiids to pesticides and enhancement of populations in orchards. These subjects have recently been reviewed by Gregory et al. (2013) and discussed by Duso et al. (2014) and Wearing (2014). The natural development of pesticide resistance in phytoseiid populations, notably to commonly used OP insecticides, was crucial to their emergence as key natural enemies in orchards (Hoy, 2011). Populations often remain susceptible to synthetic pyrethroids, the use of which is disruptive causing outbreaks of phytophagous mites. Phytoseiids are usually absent on nursery trees owing to the intensive use of fungicides and insecticides in the nursery. However, they normally colonise orchards naturally (Szabó et al., 2014). They have been successfully introduced into new orchards on summer prunings.

Economic value of the ecosystem services provided by phytoseiid predatory mites. One of the main success stories of apple IPM has been the realisation of the crucial importance of OP-resistant strains of T. pyri. Up to the 1980s, insecticides and fungicides harmful to the predatory mite were extensively used and phytophagous mites, which rapidly developed resistance to new acaricides, were the most troublesome orchard pests. For many years, it was almost routine practice to spray pirimiphos-methyl in spring for apple rust mite (A. schlechtendali) and cyhexatin after flowering for P. ulmi. In the 1980s, once the importance of the orchard predatory mite had been realised, growers stopped using pesticides harmful to it (e.g. synthetic pyrethroids, pirimiphos-methyl, dinocap etc.). The predatory mite re-colonised most commercial orchards, and the phytophagous mites ceased to be a problem. There are many fruit farms in the U.K. where acaricide treatment has not been necessary for ≥30 years. If phytoseiid predators were not present, we estimate that at least two acaricide treatments per season would be needed costing approximately €200–250 ha−1 , depending on the materials chosen. Such a response would be only partially effective (A. schlechtendali is difficult to control with acaricides) and would have negative unquantifiable consequences for the long-term sustainability of apple production as spider mite populations often resurge after treatment when no phytoseiid predators are present and rapidly develop resistance to acaricides. If acaricide treatment could not be resorted to, catastrophic losses (>50%) are likely to result making apple production uneconomic.


Arthropod ecosystem services in apple orchards Key knowledge gaps. Greater knowledge of susceptibility of naturally occurring phytoseiids to pesticides and development of resistance, especially insecticides used to control alien invasive pests (e.g. H. halys), is important to avoid serious future disruption of IPM.

The common European earwig The common European earwig Forficula auricularia L. has been extensively studied [for recent studies which see Burnip et al. (2002), Suckling et al. (2006), Gobin et al. (2008a,2008b) and Moerkens et al. (2009)]. In brief, F. auricularia overwinters as an adult, mostly in subterranean nests, where females oviposit towards the end of the winter. During this nesting phase, the adults, and later the adult female and her nymphs, may forage outside at night. From the second instar onwards, nymphs forage and shelter outside including in fruit trees. They forage at night and seek shelter during the day. Populations may be single or double-brooded. Abundance. Forficula auricularia is very common in many though by no means all, apple orchards. Helsen et al. (2004) surveyed the abundance of F. auricularia in orchards in the Netherlands using refuges. Over half the IPM orchards had 0 or < 1 F. auricularia per refuge while < 10% of IPM orchards had over five per refuge, the reasons for the variability in abundance being unclear. A similar survey conducted in SE England for two successive years (2013–2014) similarly showed enormous variation in the abundance of F. auricularia (J. Cross East Malling Research unpublished). Over half the 26 apple orchards had no or virtually no F. auricularia, with numbers varying up to 80 per refuge in the others. Numbers were considerably greater in pear orchards. Patterns of use of insecticides known to be harmful to F. auricularia (especially chlorpyrifos) and orchard age accounted for a significant part but by no means all variability. Moerkens (2010) investigated the causes of the orchard-to-orchard variability in F. auricularia abundance and found no proof that predation or cannibalism actually regulated the population. He concluded that earwig populations were passively limited by the environment to support all individuals. Food and natural shelters were refuted as key limiting resources, the real driving factors in population variation remaining unknown (Moerkens, 2010; Moerkens et al., 2012). Ecosystem services provided by F. auricularia. Forficula auricularia is an important predator of many orchard pests including codling moth C. pomonella (Jones et al., 2012; Sauphanor et al., 2012), apple leaf-curling midge Dasineura mali Kieffer (He et al., 2008), scale insects (Hill et al., 2005; Logan et al., 2007), the leafroller Epiphyas postvittana Walker (Suckling et al., 2006; Frank et al., 2007), aphids such as woolly apple aphid (WAA) Eriosoma lanigerum Hausmann (Ravensberg, 1981; Noppert et al., 1987; Mueller et al., 1988; Solomon et al., 1999; Nicholas et al., 2005), rosy apple aphid (RAA) D. plantaginea (Brown & Mathews, 2007; Dib et al., 2010), green apple aphid Aphis pomi DeGeer (Carroll & Hoyt, 1984; Hagley

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& Allen, 1990), and psyllids including pear psyllid Cacopsylla pyri L. (Lenfant et al., 1994; Sauphanor et al., 1994; Höhn et al., 2007). Experiments show that excluding F. auricularia from E. lanigerum or psyllid infested trees leads to a proliferation of the pests (Mueller et al., 1988; Nicholas et al., 2005; Gobin et al., 2008a). The benefits of F. auricularia as voracious predators of these pests with high prey consumption rates, and the vital part they play in naturally regulating populations of several key pests is now widely recognised. Ravensberg (1981) was the first to connect outbreaks of the woolly apple aphid in plots repeatedly treated with diflubenzuron, with the low numbers of earwigs in these plots. Mueller et al. (1988) and Mols (1996) demonstrated the relationship between the earwig density in the trees and the extermination of woolly apple aphid colonies. Assessments of the abundance of pests and F. auricularia in the 40 apple and pear orchards in SE England in 2013–2014 showed that the orchards that had the highest numbers of codling moth, woolly aphid, and pear psylla all had zero or virtually zero F. auricularia (J. Cross East Malling Research, unpublished). Although other orchards that had zero or virtually zero F. auricularia did not necessarily have high pest levels, none of the orchards with high F. auricularia numbers had high pest levels. It should be noted that F. auricularia is omnivorous and can cause economic damage to some crops (see e.g. Huth et al., 2011), particularly those with a thin or soft skin (e.g. peaches and strawberries) It was once considered to be an important pest of apple which growers attempted to control with sprays of pesticides but damage to fruits is now generally considered to be only secondary, at points where the skin has already been damaged. Feeding on leaves and blossoms is common but of minor importance.

Enhancement of F. auricularia populations. Avoiding the use of insecticides harmful to F. auricularia is an important first step in increasing its abundance (see below). Given that F. auricularia is an important natural enemy of apple pests, their promotion through the use of additional shelters or artificial refuges has been assessed in apple, pear, and kiwifruit orchards (Solomon et al., 1999; Gobin et al., 2006; Logan et al., 2011). However, it has not yet been demonstrated that provision of shelters causes long-term increases in F. auricularia populations or increases in pest predation. Theoretically it would be possible to use shelters to transfer F. auricularia from orchards where they are abundant to orchards where populations are low. This practice could be beneficial in newly planted orchards where F. auricularia populations take the time to establish and where the trees have smooth bark providing few natural shelters.

Susceptibility of F. auricularia to pesticides. Earwigs are susceptible to some common pesticides (Markó et al., 2008; Colvin & Cranshaw, 2010; Vogt et al., 2010; Belien et al., 2013; Fountain et al., 2013). The OP chlorpyrifos and synthetic pyrethroids have strong, lasting direct toxic effects but some other pesticides, including indoxacarb, spinosad, thiacloprid, have less obvious effects but adversely affect feeding and reproduction. Therefore, insecticide spray programmes can have


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long-lasting repercussions on populations (Gobin et al., 2006; Peusens & Gobin, 2008; Peusens et al., 2010).

Economic value of the ecosystem services provided by F. auricularia. None of the above studies have directly quantified the impact of F. auricularia on the economic performance of orchards and although a few provide insights as a basis for speculation into what those benefits may be. If earwigs were absent from apple orchards, many pests would be more abundant, some substantially so, including very damaging pests such as codling moth and woolly aphid. Controlling these pests chemically, where there is no insecticide resistance, might require an additional 2–3 insecticide sprays per annum costing perhaps €160–240 ha−1 including application costs, and depending on the materials chosen. Such a response, though effective in the short term, would lead to an increased dependency on pesticides and have negative economic and ecological unquantifiable consequences for the long-term sustainability of apple production. If the increased incidence of serious pests were not tackled by increased insecticide use or other effective measures, a substantive increase in pest damage to fruit would occur. Every 10% of the crop losses would cause economic losses to gross output in the range of €928–5778 ha−1 . Fixed costs would remain unaffected or perhaps increase marginally because of increased picking costs. A 10% loss in yield would reduce gross margins by 67% to 30% to €461–13 474 ha−1 , for the least and most productive orchards, respectively.

Key knowledge gaps. Greater understanding of the reasons for orchard-to-orchard variation in F. auricularia populations and means of enhancing and stabilising populations in orchards where their numbers are low and in new orchards is the highest priority. A greater knowledge of the harmful effects of pesticides on F. auricularia is also needed so these can be avoided or minimised.

Mutualism between the common black ant Lasius niger and pest aphids, interactions with grass root aphids and competing ant species and manipulations to foster biocontrol of aphids by generalist predators Apple orchards provide suitable habitats and nesting sites for the common black ant L. niger and its main competitor the yellow meadow ant, Lasius flavus (Fabricius). Lasius niger is one of the commonest European ant species, and builds its nests in the ground, often under stones and the workers often occur in the canopy (Markó et al., 2013). This species is an aphidicolous and carnivorous, quite aggressive ant which protects food sources within its foraging area. It feeds in all biocoenotic strata: in the soil (tending root aphids), on the soil surface, in the herb layer and tree canopies. Lasius flavus is abundant in North Europe, occurring in meadows and the periphery of woodlands where it builds big soil mounds. This species is hypogoeic, seldom occurs above ground, feeding mainly on the honeydew of subterranean root aphids and on

small insects and never climbs up to tree canopies (Collingwood, 1979; Seifert, 1992; Czechowski et al., 2012). Various honeydew-producing homopterans have complex mutualistic relationships with ants (Way, 1963; Buckley, 1987; Stadler & Dixon, 2005) which reciprocally and positively affect the partners (Stadler & Dixon, 2005). Aphids feed on phloem sap, which is typically rich in sugars but poor in nitrogen, so aphids have to ingest large volumes of phloem sap and the surplus sugars are excreted as honeydew (Dixon, 1998, 2005). This mutualism has benefits and costs for both partners, which are well described in several reviews (Way, 1963; Buckley, 1987; Stadler & Dixon, 1998, 1999, 2005; Yao et al., 2000; Katayama & Suzuki, 2002), so in this review we focus on the most important ecological costs and benefits. Ants provide increased colony hygiene and improved defence against natural enemies and fungal infection for aphid colonies (Stadler & Dixon, 1999, 2005). In contrast, some specialised predators and parasitoids exploit ant-attended aphids (Völkl, 1992; Stadler & Dixon, 1999; Kaneko, 2002, 2003) and ants also prey on their homopteran partners (Sakata, 1994; Offenberg, 2001).

Abundance of L. niger and L. flavus. Lasius niger is the dominant ant species in most apple orchards in Europe, although abundance is very variable between locations (Stewart-Jones et al., 2008; Miñarro et al., 2010; Nagy et al., 2013). Seifert (1992) found a mean of 22 nests and a maximum of 108 nests per 100 m2 in plots of variable habitat structure. Lasius flavus is one of the most abundant ant species in North Europe, and can be quite common in some apple orchards where the alleys have grass, because this species depends on their subterranean root aphid partners (Seifert, 1992).

Ecosystem effects of L. niger. Ants have great effects in many habitats (Way & Khoo, 1992). As predators of pests, they may be useful in pest management and some ants are important in pollination, soil improvement, and nutrient cycling (Gotwald, 1986). In contrast, some feed on or disturb plants and can be vectors of plant diseases, benefit damaging Homoptera, and attack or irritate humans, domestic animals, and other beneficial organisms (Vinson, 1986; Vander Meer et al., 1990). All species that prey on pests also have some potential disadvantages (Way & Khoo, 1992). On apple trees some of the most important pest aphid species [D. plantaginea, A. pomi, Aphis spiraecola Patch, and Rhopalosiphum insertum (Walker)] are involved in facultative mutualistic relationship with L. niger (Stewart-Jones et al., 2008; Miñarro et al., 2010). Experimental studies showed that L. niger workers attacked and carried off or drove away larvae of Syrphidae and Adalia bipunctata (L.) from aphid colonies. Adult Coccinellidae, larvae of Chrysoperla carnea Stephens and larval and adult Anthocoridae were also attacked by them (El-Ziady & Kennedy, 1956; Banks, 1962; Jiggins et al., 1993). Occasionally ants also attacked adults of the parasitoid Aphidius sp. but did not harm syrphid or coccinellid


Arthropod ecosystem services in apple orchards eggs (El-Ziady & Kennedy, 1956). Banks (1962) found opposite results. He observed that ants removed syrphid and coccinellid eggs but ignored aphid parasites. Evidence for the negative effects of L. niger on herbivores can be found on other plants (Suzuki et al., 2004), but such data are very rare from the apple. Manipulation of L. niger and its interactions to foster biocontrol. Given that L. niger is a crucial factor in promoting aphid populations on apple trees, there is no motivation to enhance its abundance. To the contrary, a reduction by physical exclusion, by provision of alternative sugar sources, with supporting populations of grass root aphids or promotion of their competitor L. flavus may result in lower levels of aphid damage in apple orchards. As various studies previously reported, the exclusion of ants from tree canopies can decrease aphid attack in apple orchards (Wyss et al., 1999; Stewart-Jones et al., 2008; Miñarro et al., 2010; Nagy et al., 2013) where aphid pests are ant-tended. These studies reported that applying sticky barriers on the bark of the trees is a possible method for excluding ants from tree canopies, and through this, reducing aphid populations. However, Stewart-Jones et al. (2008) and Piñol et al. (2009) mentioned that this method, as a side effect, can also exclude important natural enemies such as F. auricularia from the tree canopies, and may result in an increase in aphid populations (Piñol et al., 2009; Miñarro et al., 2010). Furthermore, ant exclusion using sticky barriers also has some practical problems. Alternative ways are thus required to exclude ants from tree canopies. In laboratory experiments Offenberg (2001) demonstrated that offering sugar to L. niger workers can change the interaction with aphids from mutualism to exploitation owing to decreased ant-tending and increased predation, causing a significant reduction in aphid populations. Nagy et al. (2013) demonstrated that offering artificial sugar sources (honey solution) to ants in the field can decrease the level of ant attendance on colonies of D. plantaginea and A. pomi, and so indirectly can reduce aphid damage in apple orchards without disturbing predators which move between the tree canopy and ground surface. Special sucrose solution bottle feeders also showed very promising results (Nagy et al., 2014). Susceptibility to insecticides. There is a very little information about the susceptibility of L. niger to insecticides in general, yet alone in apple orchards. It is assumed that L. niger will be killed by direct interception by sprays of broad-spectrum insecticides such as chlorpyrifos or synthetic pyrethroids and that sprays of specific aphicides such as flonicamid, pirimicarb or pymetrozine are likely to kill aphid pests, thus depriving ants of important food sources. The residual effects of insecticide applications on the ant–aphid mutualism are worthy of further study. Economic value of ecosystem services. Some of the above studies have directly quantified the impact of L. niger on the economic performance of apple orchards (Stewart-Jones et al.,

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2008) and although a few provide insights as a basis for speculation into what those benefits may be. If L. niger were absent from apple orchards, myrmecophilic aphid pests would be less abundant, and in many instances insecticide control of these aphids probably would not be necessary at all. Most commercial apple orchards receive 1–2 insecticide treatments for aphids per annum caused indirectly by the presence of L. niger. Lasius niger causes increased costs (i.e. has a negative economic benefit) within the orchard of €80–160 ha per season. If insecticides could not be resorted to, L. niger would probably indirectly cause crop losses of >10% per annum (i.e. losses of >€928–5778 ha−1 ) owing to aphid damage. Thus, L. niger is a good example provider of an ecosystem disservice. Key knowledge gaps. A greater understanding of the reasons for orchard-to-orchard variation in L. niger populations is an important challenge. A greater knowledge of susceptibility of L. niger to pesticides, the development of resistance, and the long-term effects of pesticides on L. niger is also needed. Further studies are necessary to determine on which pests L. niger preys in apple orchards, and also to quantify its impact on the population development of these pests. Furthermore, studying the long-term effects of sugar feeding of L. niger, promotion of its competitor L. flavus or supporting populations of grass root aphids on the levels of aphid damage in apple orchards are important research directions for the future.

Beneficial epigeic arthropods including carabids, staphylinids, and Araneae and their role in predating the soil dwelling life stages of insect pests Ground beetles (family Carabidae) belong to the one of the most species-rich Coleoptera families. Adults live on the soil surface (epigeic) and are highly mobile, whereas larvae live in the soil, and a have lower dispersal ability (Kromp, 1999). The majority of the species are generalist predators although even these species might be omnivorous. Other species have a restricted variety of prey or are predominantly herbivores (e.g. Amara and Harpalus spp.) (Kromp, 1999). Rove beetles (Staphylinidae) typically occur on the ground or in the soil, leaf litter, on fungi, carrion, and dung. The majority of the species are predacious (Bohac, 1999). Spiders (order Araneae) are the most abundant predacious macro-arthropods in terrestrial ecosystems in temperate geographical regions. All species are carnivorous feeding mainly on insects. Based on methods of prey capture and other ecological characteristics, spiders can be classified into two main guilds, hunting and web-building spiders. Some spider groups are ground-dwellers or epigeic, others show preference to different vegetation layers (Marc et al., 1999). Diversity and abundance of carabids, staphylinids, and spiders in apple orchards. Apple orchards harbour diverse and abundant epigeic predator communities. The species richness of an apple orchard carabid community, at high sampling effort, is usually 30–60 species (Hagley & Allen, 1988; Riddick &


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Mills, 1995; Epstein et al., 2000; Kutasi et al., 2004; Smith et al., 2004; Markó & Kádár, 2005; Miñarro et al., 2009). However, the composition of the carabid communities varies greatly among different areas. In Western Europe and North America, the predominant species in apple orchards are primarily carnivorous (Pterostichus spp.) whereas in a Mediterranean climate and Central and Eastern Europe, the carabid species with a mixed diet (animal and vegetal, e.g. Harpalus spp.) are more common. Samples collected from the canopy and trunk of apple trees showed that epigeic carabids only occasionally climb on the trees (Markó et al., 1995; Kutasi et al., 2004). Little is known about the diversity and abundance of staphylinids in apple orchards. Compared in the same orchards, their species richness is usually higher, and the relative abundance of the most common (dominant) species is lower than those of carabids. In Great Britain (Kent, East Malling), 54 species (V. Markó et al., unpublished), in Czech Republic 28 species, and in Spain 46 species were collected in the studied orchards (Miñarro et al., 2009; Honˇek et al., 2012). In Hungary, 23–100 (typically 50–80) species per orchard, altogether 241 species were found (Balog et al., 2003). Staphylinids were rarely found on the apple trees both in Great Britain (East Malling) (V. Markó et al., unpublished) and Hungary (Markó et al., 1995). The species richness of spiders on the ground surface of apple orchards in Europe vary between 40 and 90 species per orchard; Great Britain (East Malling): 62 (V. Markó et al., unpublished), Czech Republic: 89 (Pekár, 2003), Hungary: 37–86 species (Bogya & Markó, 1999; V. Markó and B. Keresztes, unpublished). The spider communities on the ground surface and in grass and canopy layers differ considerably in their composition, and the species common in the ground do not climb on the trees (Bogya et al., 2000). One exception is Xysticus kochi Thor., the adults of which are active on the ground, but juveniles colonise the canopy (Markó & Keresztes, 2014). The most abundant species on the ground surface belong to families Lycosidae, Thomisidae, Gnaphosidae, and Linyphiidae [see references above and Samu and Lövei (1995); Bogya and Markó (1999); Miñarro et al. (2009) and Miliczky et al. (2000) for species].

Ecosystem services provided. As most of the epigeic predators in orchards are generalists, they are potentially able to attack and consume various apple orchard pests that occur on the ground surface and thus suppress their numbers and damage. Codling moth (C. pomonella), oriental fruit moth [Grapholita molesta (Busck)], light brown apple moth (E. postvittana), tufted apple bud moth [Platynota idaeusalis (Walker)], apple maggot fly [Rhagoletis pomonella (Walsh)], apple leaf midge (D. mali), plum curculio [Conotrachelus nenuphar (Herbst)], cockchafers (Melolontha spp.), Japanese beetle (Popillia japonica Newman), apple fruit rhynchites [Tatianaerhynchites aequatus (L.)], apple sawfly [Hoplocampa testudinea (Klug)], and woolly apple aphid (E. lanigerum) spend a part of their life cycles in soil or leaf litter around the trees, and, therefore, might be exposed to predators hunting on these layers. The most well-documented example of biocontrol of apple pests by epigeic predators concerns codling moth. Laboratory studies

showed that adults of several Pterostichus species, but also other carabids attack fifth-instar codling moth larvae with high success (Jaynes & Marucci, 1947; Hagley et al., 1982; Riddick & Mills, 1994; Epstein et al., 2001). Other carabid species [typically the ones with mixed feeding habit, e.g. Amara aenea (DeGeer), Harpalus affinis Schr.,] were found to be less effective (Hagley et al., 1982; Riddick & Mills, 1994). Open field studies revealed that codling moth larvae which have left the trees or fallen fruits seeking for suitable pupation sites are actively attacked by carabids and spiders (Glen, 1982; Hagley & Allen, 1988; Boreau de Roincé et al., 2012). According to serological tests, the proportion of Pterostichus melanarius (Illig.) adults preying on larvae might be as high as 63% in some apple orchards in Canada (Wearing & Skilling, 1975; Hagley & Allen, 1988). However, in apple orchards in south-eastern France, where Pterostichus spp. were absent, the most important carabid predator of the codling moth (but also of G. molesta) was Harpalus (Pseudophonus) rufipes (Deg.), with 8% of codling moth predation as a maximum (Boreau de Roincé et al., 2012). In this study, the most active codling moth predators beside carabids were wolf spiders (Lycosidae, less than 8% preying on codling moth larvae) (Boreau de Roincé et al., 2012). Further, ants, active on the ground surface, also appear to contribute to the overall predation on the fifth-instar larvae greatly (Jaynes & Marucci, 1947; Mathews et al., 2004). So far, most studies have focused on epigeic predators, with only a few attempts to quantify their impact on codling moth populations. In a small study, 34–81% of the sentinel fourth and fifth-instar codling moth larvae were attacked on the ground of an apple orchard (Mathews et al., 2004), although in natural conditions this predation rate should be lower as codling moth larvae try to find shelter as soon as possible. In the laboratory, P. melanarius, H. affinis, Anisodactylus sanctaecrucis F., and, to a lesser extent, other carabid species actively preyed on apple maggot pupae (Hagley et al., 1982). Some species were able to dig up the maggot pupae from the soil (Monteith, 1971, 1975). In orchards, the most active predators of apple maggot pupae were staphylinids (mainly Philonthus spp., the highest proportion of seropositive individuals: 30%), the carabids (29%), gryllids (23%), spiders (16%), and ants (10%) (Allen & Hagley, 1990). The mortality caused by ground-dwelling predators might probably be as high as in the case of Mediterranean fruit fly pupae in citrus orchards, 53–76% (Urbaneja et al., 2006). Alternative prey decreased the apple maggot predation in the laboratory and a similar effect on open field predation is highly probable (Hagley et al., 1982; Renkema et al., 2012). Various ant species were responsible for 60% mortality of plum curculio larvae on the apple orchard ground surface and in non-apple agricultural systems ants, larvae, adults of staphylinids (Philonthus spp.) and carabids caused substantial mortality in eggs and young larvae of scarabs, e.g. Japanese beetle (Terry et al., 1993; Jenkins et al., 2006; Juen & Traugott, 2007). At last, epigeic predators might also prey on apple pests falling from the trees, for example on green apple aphids or young larvae of Spodoptera littoralis (Boisd.) (Mansour et al., 1981; Hagley & Allen, 1990).


Arthropod ecosystem services in apple orchards Enhancement of populations. Natural ground cover vegetation could enhance the carabids in the soil of apple orchards compared with tilled plots (Holliday & Hagley, 1984; Kromp, 1999). However, this positive effect of the understory vegetation often diminishes when the activity-abundance of carabids is measured on the ground surface (Holliday & Hagley, 1984; Miñarro & Dapena, 2003; Markó & Kádár, 2005). While different carabid species respond differently, the abundance of epigeic spiders is usually increased considerably in the orchard habitats with dense herbaceous vegetation (Bogya & Markó, 1999; Miñarro & Dapena, 2003; Markó & Kádár, 2005; Funayama, 2014). Plastic (polyethylene sheets) and straw mulch affect negatively the carabid and spider abundances (Miñarro & Dapena, 2003; Miñarro et al., 2009) while compost mulch provides alternative prey and, therefore, increases the abundance of the epigeic predator communities especially staphylinids (Mathews et al., 2004). However, the alternative prey could also reduce the effectiveness of carabids in pest suppression by decreasing their propensity to attack codling moth larvae (Riddick & Mills, 1994; Mathews et al., 2004).

Susceptibility to insecticides. Applications of broadspectrum insecticides such as pyrethroids and organophosphates is detrimental to epigeic predators in apple orchards (Epstein et al., 2000; Markó & Kádár, 2005; Funayama, 2011), although this negative effect on natural enemies is often less pronounced on the ground than in the canopy (Bogya & Markó, 1999; Bogya et al., 2000; Miliczky et al., 2000). The selective insecticides applied in IPM and organic apple orchards are less toxic to carabids and spiders and their abundances showed no difference between these two pest management systems (Hedde et al., 2015; Mazzia et al., 2015).

Economic value. Epigeic predators might be important limiting factors to codling moth in intensive orchards where the young apple trees have smooth bark, and in the absence of suitable cocooning sites a high proportion of codling moth larvae pupate on the ground (Wearing & Skilling, 1975; Causse, 1976; but see Blomefield & Giliomee, 2012). They might also contribute significantly to the control of other apple pest populations although the level of suppression is not consistent and depends on several ecological factors.

Key knowledge gaps. Further studies are necessary to determine not only which epigeic and below-ground arthropod species prey commonly on pests in apple orchards, but also to quantify their impact on the population development of apple pests.

Perspectives The ecosystem services and economic benefits provided by five arthropod groups are overviewed in this paper which, although wide ranging, is far from comprehensive: Important services provided by several other arthropod groups, notably parasitoids

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and several groups of specialised and generalist predators, are not covered. The five groups have been chosen because they differ considerably in their nature and value and the degree to which they are understood, valued, and implemented by growers. Implementation into commercial practice ranges from easy modification of commercial practices to special measures taken to conserve or enhance them. Pesticide-resistant phytoseiid predatory mites have clear benefits in naturally regulating important pest mites. These benefits are well understood by growers and practices to conserve them, the avoidance of using pesticides harmful to them, are implemented almost universally. Forficula auricularia has an important role in regulating several important apple pests, but for many pests (e.g. C. pomonella) the benefits have not been quantified. The full range of benefits of F. auricularia is not widely appreciated by growers and require further study. Growers in western Europe are starting avoid using pesticides harmful to them where they can and in some orchards refuges to stabilise populations are deployed. Lasius niger causes aphid pest outbreaks, but these are modulated naturally by competition from L. flavus where it is present and by the presence of alternative natural food sources, especially grass root aphids. The negative impact of L. niger could be greatly reduced by providing artificial alternative food sources, but suitable formulations, and ways of applying them have yet to be identified and implemented in commercial practice. Several groups of managed and wild insects provide pollination services in the orchard and the wider environment and have a clear benefit in maximising apple yield and quality. Many, although not all, growers provide honey bee hives in orchards for pollination and spraying pesticides harmful to bees during flowering is avoided. Wildflower areas as forage for bees are provided on some farms. Epigeic predators are the least well studied and understood of these five groups and growers do not in general adopt practices, such as ground herbage management, to exploit them. It should be noted that the economic benefits are context-specific. The costs, context, and pest damage risk presented here are based on those in the U.K. and similar cool temperate apple production regions. The arthropods groups reviewed here provide diverse and valuable ecosystem services in apple orchards that have substantive economic and many other benefits. There is still an overreliance on the use of pesticides for pest control in orchards, which have adverse effects on arthropods that provide these valuable ecosystem services. There are many opportunities to reduce pesticide reliance by exploiting and enhancing arthropod ecosystem services including opportunities to improve the design of orchards towards more sustainable systems. Acknowledgements The authors wish to acknowledge funding support from the Worshipful Company of Fruiterers, U.K., and ÖMKi and Hungarian Scientific Research Fund (K112743), Hungary. References Allen, W.R. & Hagley, E.A.C. (1990) Epigeal arthropods as predators of mature larvae and pupae of the apple maggot (Diptera: Tephritidae). Environmental Entomology, 19, 309–312.


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