PURE – Deliverable D10.5

Funded by the European Union

PURE Pesticide Use-and-risk Reduction in European farming systems with Integrated Pest Management

Grant agreement number: FP7-265865 Collaborative Project SEVENTH FRAMEWORK PROGRAMME

D10.5 Recommendation of manipulation of field margins

Due date of deliverable: M 48

Actual submission date: M 48

Start date of the project: March 1st, 2011 Duration: 48 months

Workpackage concerned: WP 10

Concerned workpackage leader: Graham Begg

Organisation name of lead contractor: AU

Project co-funded by the European Commission within the Seventh Framework Programme (2007 - 2013) Dissemination Level PU Public PU PP Restricted to other programme participants (including the Commission Services) RE Restricted to a group specified by the consortium (including the Commission Services) CO Confidential, only for members of the consortium (including the Commission Services)

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Table of contents

1. Summary ______3 2. Objectives ______3 3. Deliverable procedure ______3 3.1 Experiments in Denmark ______3 3.1.1. Arthropod sampling methods ______4 3.1.2. Quantifying predation intensity ______4 3.2. Experiments in the U.K. ______5 3.2.1. Pitfall trapping – ground active arthropods ______7 3.2.2. Vortis suction sampling- aerial arthropods ______7 3.2.3. Aphid counts ______7 3.2.4. Exclusion cage experiment ______7 3.2.5. Assessment of parasitism activity in oilseed rape ______8 4. Results summary ______8 5. Conclusions ______10

Appendix 1 Poster presented at the PURE conference IPM Innovation in Europe 2015 ___ 11 Appendix 2 Abstract of Poster presentation at the PURE conference2015 ______12 Appendix 3 Abstract of the oral presentation at the PURE conference 2015 ______13 Appendix 4 Report on work done at Rothamsted Research, UK for the PURE project (Draft paper)______14

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1. Summary

We reported the results of two-years work aimed to evaluate the effectiveness of margin manipulation using flowering mixture to enhance biological control. The experiment included complementary sampling methods of the natural enemies and of the predation service provided by it. Results suggest that with differences related to the predatory guilds, margin manipulation may enhance predation rate, especially of specialist natural enemies. Although there are potential benefits of the inclusion of brassicas in field margins, the brassica species or varieties selected should be chosen carefully, and combinations with the longest possible flowering period should be used to maximise the availability of floral resources and extend the window over which specialist pest larvae are available as prey or hosts.

2. Objectives Manipulating field margins have been suggested as a method to increase the beneficial services, especially of natural enemies, to suppress pest populations in cultivated fields. Planting flowering crops and/or flowers is the most often recommended method to achieve this, especially due to the additional alternative food provide to natural enemies (nectar, pollen), and the shelter function. We tested the effect of plant cruciferous flowering crops on the natural enemies and on predation rate to make recommendations concerning this method.

3. Deliverable procedure The project was carried out over two years in Denmark and the UK using complementary (as far as possible) experimental arrangements.

3.1 Experiments in Denmark

In Flakkebjerg (Zealand, Denmark), during the field season 2013, a flowering mixture composed of two cruciferous plants (Brassica rapa var. rapa and Raphanus sativus var. oleiformis) was planted along the edges of respectively two winter wheat (Triticum aestivum), and three oil seed rape (Brassica napus) fields. Natural enemies were collected, counted, and identified to the broad taxonomic level (order or family), using directional pitfall traps (30 July - 6 August, 14-21 August, 28 August- 4 September) and vacuum sampling (2nd, 15th, 28th August). Moreover, predation rate was measured using artificial sentinel prey (30th July, 15th August, 29th August) made of plasticine as for 2014 (see below for details). Sampling took place in flowering and grassy adjacent margins of fifteen meters long each. In 2014 the same flower mix was planted along the edges of five winter wheat fields (6.7 ±3.3 ha). Each field was bordered by a natural grass strip ca. 1m wide and in the opposite side by a 50m long and 2.5m wide flowering margin, excluding one field where only the grass margin was used for logistic reasons. Only the central 15m of the margin were used for the experiments. The grass strips were selected to ensure they were distant from other flowering areas and regularly cut, to avoid additional flower resources in the control margin. Associated with each margin (edge part), a strip of crop of equal size and located 10m away from the margin (inner part) was investigated in order to compare the effect of the margin on the arthropod composition and their activity. The flowering strip was established on 10 April 2014 and started to flower on the beginning of June 2014. When the wheat was harvested at the end of July 2014, the flowering was over.

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3.1.1. Arthropod sampling methods The arthropod composition of the natural enemy guild was determined by using two complementary sampling methods. Epigeal predators were collected using directional pitfall traps (two single pitfall traps, 500ml volume and 10cm diameter, filled with 100ml ethylene glycol 70%, connected asymmetrically by 1m long plastic barriers). This arrangement formed two funnels, causing one of the pitfalls to catch mostly arthropods moving into the field, while the other captured mostly arthropods intending to emigrate from the field. For each field, two groups of directional pitfall traps 5m distant from each other were arranged in the inner part of each plot, for a total of 40 single traps. Each trap was covered by a square cover made of galvanized iron (10×10cm), in order to reduce the by-catch. The traps were collected fortnightly on four dates in 2014 (21-28 May, 3-10 June, 18-25 June, 2-9 July). A total of 144 samples were collected by this method. Vegetation dwelling arthropods were collected using a suction device made of a converted and modified portable leaf blower (Husqvarna® 125BVx). The vacuum tube measured 85cm long and 12.5cm of diameter. The collection bag made of a fine cotton mesh (20×30cm) was held in place by a ring collar stuck between the two parts of the vacuum tube. Sampling was made by walking along a 15m transect in both the inner and edge part of the margins. Sampling occurred fortnightly on three dates in 2014 (3rd June, 16th June, and 1st July), for a total of 54 samples. Vacuum samples were stored at -20°C overnight before sorting. All the collected arthropods were identified to the order level or, in the case of beetles (Coleoptera), to family using identification keys of Choate (1999) and Unwin (1984). 3.1.2. Quantifying predation intensity Predation pressure was quantified in each margin using two methods: exclusion cages containing the grain aphids (Sitobion avenae) acting as real sentinel prey; and artificial sentinel prey made of plasticine. Exclusions cages consisted in three different types (open, partially closed and totally closed) placed in a random sequence in the inner part of the field, arranging each at 5m from the next. Cages were cylindrical and made of solid plastic (31.5cm diameter, 50cm height). The open cage was fully uncovered, the partially closed cage was covered by a plastic mesh 2x2cm size and uncovered at the bottom, and the total exclusion cage was fully covered with a muslin mesh and hence used as control. To ensure that no predators could enter the total exclusion cage, a first muslin mesh was placed on the cage and glued to the frame and a second muslin mesh was placed on the ground and ridden up to overlap with the first mesh. The open cage allowed the access both to invertebrate and small vertebrate predators, while the partially closed only to invertebrate. In each cage, a pot containing several 10cm tall winter wheat plants was infested by ten grain aphids of mixed age classes (nymph and adult), and placed to soil level (except for the total exclusion cages, where the pot was put on the bottom mesh).The fate of these aphid colonies was followed during the flowering period of the flower margin, with nondestructive counting twice a week. If a population of aphids went extinct in the total exclusion cage or in either the open or partially closed cage, the experiment was re-installed and restarted for the whole field. In total we concluded 24 experiments from 7 June to 7 July 2014. In order to determine how the provision of the biological control service was affected by the treatments (flowery or grassy margins), relative aphid suppression was calculated in each margin by expressing the change in aphid numbers in open and partially exclusive cages as a proportion of aphid abundance with respect to numbers reached in the absence of predators (given by the total exclusion cages). The resulting Biocontrol Service Index (BSI) ranged from 0 to 1, with values

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PURE – Deliverable D10.5 increasing as the level of aphid predation increases:

(A − A ) BSI = c o Ac where Ac is the number of aphids on the caged plant (total exclusion cage) after 2 or 5 days from inoculation, Ao is the number of aphids on the open plant (open or partially exclusive cage) on day 2 or day 5. Cases with negative BSI values indicated a lack of effective biocontrol. Artificial sentinel prey consisted in green light plasticine (Smeedi plus, V. nr. 776609, Denmark), “caterpillars” 15mm length and 0.3mm diameter, produced using a modified garlic press. Sentinel prey were glued on a stick of reed or bamboo, and placed at the ground level for 24h after which were collected and checked in order to record eventual predation attempts. The basic advantages of using dummy sentinel prey are the logistic aspects (ease of production, cheapness), and the informative ones (artificial sentinel prey allows the identification of the predators, although to a certain taxonomic level). For each sampling event we placed fifteen caterpillars in each part (edge and inner) of both flower and grass margins, for a total of sixty caterpillars per field (excluding that where for logistic reason contained only one margin type). Artificial caterpillars were arranged weekly (26th May, 04th June, 12th June, 18th June, 25th June, 3rd July), covering the period where the pitfall traps were active.

3.2. Experiments in the U.K. Brassica margins (3m wide) containing a 50:50 mixture of Fodder radish (Raphanus sativus cv. Apoll) and Tyfon (hybridized Brassica rapa Rapifera x B. rapa Pekinesis) were established alongside existing grass margins (3m) at the borders of wheat (Triticum aestivum) and oilseed rape (Brassica napus) crops. The composition of these margins was informed by previous (but as yet unpublished) studies (Skellern et al, submitted; Final report of Defra project IF0139). Crops with a grass margin but no brassica margin (3m bare ground at the field edge) served as controls (Figure 1). Six fields of wheat and six fields of oilseed rape (OSR) were drilled on Rothamsted farm in Autumn 2012. All fields had long-established 3m wide grass margins on all sides. Brassica field margins were drilled in autumn 2012 on one side of each of three of the wheat fields adjacent to the existing grass margin, and three of the oilseed rape fields also adjacent to the existing grass margin. The direction of the margins were positioned carefully to provide three pairs of fields in each crop type where there were either just grass margins (control) or grass margins and an additional brassica margin (Fig. 2). Surrounding landscape features such as hedgerows and tree-lines at the borders were standardized as much as possible within pairs. In 2013 the experiment was repeated using the same fields but the rotation changed such that fields containing wheat contained OSR and vice-versa.

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Figure 1. Experimental design for field experiments in the U.K.

Figure 2. Field experimental set up at RRes 2013. Six fields of oilseed rape (OSR, highlighted in pink) and 6 fields of wheat (highlighted yellow) were established. Red lines indicate positions of the borders; B = grass + Brassica border; C = Control grass border only. Roman numerals indicate treatment pairs such that Brassica and control borders were orientated in a similar direction.

To assess the arthropod community structure in the two margin treatments and their effects on the arthropod community and biocontrol potential in the crop we conducted pitfall trapping and Vortis suction sampling to assess ground-dwelling and aerial arthropods, respectively. Page 6 of 33

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This was carried out on two occasions in both years between May - July to correspond with the period prior to ear emergence and during grain ripening of the wheat crop. Direct counts of aphid populations within-wheat fields were carried out in 2013. To assess the relative effects of ground-dwelling and aerial predators, an exclusion cage experiment was carried out in 2013 and parasitism of oilseed rape pests were also assessed (2013).

3.2.1. Pitfall trapping – ground active arthropods Pitfall traps consisted of plastic cups 150 ml volume and 7cm diameter, filled with 100 ml ethylene glycol. Plastic covers, supported by metal pins prevented by-catch of aerial arthropods. The pitfall traps were placed in all fields; three traps were placed 18.75m apart within the grass margin and the brassica margin (or the bare ground in the same position in the Control treatments) and at 5m, 10m, 20m and 40m into the crop parallel to the margin. The traps were left in place for one week on two occasions in May and June 2013 and June & July 2014. Pitfall trap samples were returned to the laboratory and stored at -5°C prior to processing and identification of the insects to species level wherever possible. Directional pitfalls, with a plastic barrier bisecting the trap with a 2 cm barrier extending over the lip of the trap were placed parallel to the crop/margin interface and were used to gain a ‘snap-shot’ of movement towards the margins or away from them along those placed 5m into the crop. ANOVA was used to analyse differences in the activity-abundance of captured species or groups between the two margin treatments. For the comparisons of the arthropod communities caught in the different components of the margin treatments (grass margin, brassica margin or field edge) a nested ANOVA was used with random effects blocking for year, field and margin component. Activity-abundance of species or groups caught within field were analysed by REML with margin treatment*distance into the crop as fixed effects and year/field pair/field/position as random effects. All analyses were done using GenStat GenStat, version 15 (VSN International, Hemel Hempstead, UK).

3.2.2. Vortis suction sampling- aerial arthropods A vortis suction sampler (Burkard, UK; see Arnold, 1994) was used. Samples were taken at the start and again at the end of the pitfalling period along the transects marked by the pitfall traps in the grass and brassica margins, and at 5m, 10m, 20m and 40m into the crop. Samples were returned to the laboratory and stored at -5°C prior to processing and identification of the insects to species level wherever possible. Analyses were conducted for within margin comparisons and within field effects as described above.

3.2.3. Aphid counts Ten wheat plants were sampled along each transect 5, 10, 20 and 40m into each wheat crop. Aphids infesting each plant were counted and identified and numbers of any parasitized aphids (mummies) were also recorded. Data were analysed by REML as described above.

3.2.4. Exclusion cage experiment To provide a ‘snapshot’ so that natural enemy activity could be measured against similar populations of aphids in each of the treatments, an experiment was carried out in June 2013 using insectary-reared sentinel Metopolophium dirhodum aphids on potted glasshouse-reared wheat plants. Six plant potted plants were sunk into the ground on each of 2 wheat fields with a brassica margin and 2 control sites with just the grass margin. Pots were placed 10m apart along a transect within the crop 5m from the margin. Half of the plants were covered with perforated bread bags to exclude natural enemies while the remainder was uncovered and susceptible to natural enemies. After 24h all plants were returned to the laboratory and

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PURE – Deliverable D10.5 remaining aphids were counted and placed on to fresh plants and incubated for 7 days. The number of parasitized aphids were counted.

3.2.5. Assessment of parasitism activity in oilseed rape In crops of oilseed rape, 100 pods were selected from each sampling site at the pod ripening phase. They were dissected in the laboratory and the numbers of pest larvae (seed weevil (Ceutorhynchus assimilis) and brassica pod midge (Dasineura brassicae)) were recorded along with % parasitism. Data were analysed using ANOVA (GenStat, version 15 (VSN International, Hemel Hempstead, UK)).

4. Results summary Although within-field effects of the margin treatments were fairly elusive, the inclusion of brassicas in field margins clearly has some benefits, particularly for the natural enemies of specialist pests. In margins next to oilseed rape crops, specialist parasitoids of oilseed rape pests were more abundant in the brassica-containing margins than in those without, and although this was also true for the pests themselves, within-field pest abundance was unaffected. Few parasitoids of brassica pests, however, were sampled from the brassica- containing margins that were situated next to wheat crops. Thus it is probable that brassica- containing margins would continue to support these insects throughout phases of the crop rotation where oilseed rape crops are absent. In the margins of wheat fields, the inclusion of brassicas also appeared to benefit populations of specialist aphid predators, and this may be due to the provision of nectar, or additional aphid resources.

In the U.K. site, generalist predators appeared less responsive to the margin treatments than specialists, although the predatory empid flies were an exception, being particularly associated with the presence of margin brassicas. The pitfall trap results were difficult to interpret, but there was evidence of within-field effects of the margin treatments on the abundance of some individual carabid species in oilseed rape, with two species more frequently and one species less frequently trapped in the fields next to brassica-containing margins, respectively. Interestingly, the greater carabid abundance and species richness within the brassica component of margins that were spatially separated from the oilseed rape crops (i.e. those next to wheat) may illustrate the potential importance of brassica strips in supporting communities of carabid species that are usually associated with oilseed rape, at points in the rotation when the crop is absent.

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Table.1 Summary results of the natural enemies abundance measured using directional pitfall traps and vacuum sampling and of the predation rate of generalist predators measured using artificial caterpillars in flowery and grassy margins in Flakkebjerg, (Denmark), during the field season 2013.

Total no. of natural enemies captured by pitfall traps Flowery margin Grassy margin Immigration Emigration Immigration Emigration 3930 4373 4150 4107

Total no. of natural enemies captured by vaccum sampler Flowery Grassy Edge Inner Edge Inner 1025 26 781 45

Predation on artificial caterpillars, % Flowery Grassy Edge Inner Edge Inner 42.1 56.9 48.2 58.9

Table.2 Summary results of the natural enemies abundance measured using directional pitfall traps and vacuum sampling and of the predation rate measured using aphid cages and artificial caterpillars in flowery and grassy margins in Flakkebjerg, (Denmark), during the field season 2014.

Total no. of natural enemies captured by pitfall traps Flowery margin Grassy margin Immigration Emigration Immigration Emigration 2007 2219 2801 2613

Total no. of natural enemies captured by vaccum sampler Flowery Grassy Edge Inner Edge Inner 582 311 537 445

Predation on artificial caterpillars, % Flowery Grassy Edge Inner Edge Inner 30.6 30.9 57.6 40.1

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In Denmark, our results did not support the hypothesis that flowering margins attract in the field a significant higher number of generalist natural enemies (Araneae, Carabidae, Staphylinidae; Table.1, Table.2). However, specialist predators were significantly more abundant in the field´s edge when enhanced with flowers rather than without. This observation, together with the significantly lower lifetime of aphid colonies in flowery margins (Table.2), suggested that biological control may be increased by this practice. Although in 2013 we did not find any striking difference (Table.1), the following year generalist predators seemed to prefer grassy margins, maybe due to its vegetative structure and the consequent microclimatic conditions. Both generalist predator abundance and their predation rate quantified using artificial caterpillars supported this evidence. Considering that colonization time by generalist and specialist predators differ along the crop season, and that both may be essential in pest regulation, we recommend that the agro-environment would be managed as a mosaic of different habitats, including cruciferous flowering margins, in order to provide abiotic and biotic resources to the whole natural enemies community.

5. Conclusions There are potential benefits of the inclusion of brassicas in field margins, however, the brassica species or varieties selected should be chosen carefully, and combinations with the longest possible flowering period should be used to maximise the availability of floral resources and extend the window over which specialist pest larvae are available as prey or hosts. Care must also be taken to select brassicas that favour parasitoid production over the production of pests. Due to the ruderal nature of these plants, their maintenance within field margins from year to year is likely to be difficult, without regular soil disturbance and / or re- seeding, and the additional costs of these activities for farmers will need to be weighed against the pest control benefits.

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Appendix 1 Poster presented at the PURE conference on IPM Innovationin Europe, Poznan, Poland, January 14-16 2015

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Appendix 2

Abstract of the poster (see Appendix 1) for the PURE conference on IPM Innovationin Europe, Poznan, Poland, January 14-16 2015

Manipulating field margins to increase predation intensity in winter wheat (Triticum eastivum) fields in Denmark.

Agathe MANSION-VAQUIÉ, Marco FERRANTE, Gabor L. LÖVEI Aarhus University, Department of Agroecology, Flakkebjerg Research Center, Forgøsvej 1, DK4200 Slagelse, Denmark.

Habitat manipulation is a well-known practice in conservation biological control in order to enhance natural enemy density, and is a valid alternative to pesticide use. However, due to the striking differences in their ecology, generalist and specialist predators may show different response to habitat manipulation interventions. Moreover, clear evidence that to higher density of predators correspond higher density of predation may be not easy to find, due to possible undesired effects (i.e. intraguild predation, cannibalism, hyperparasithism). Additionally, quantitative estimations of predation rate are difficult to obtain, as predation may remain undetectable (i.e. hidden, night). We recorded the composition of predatory arthropod guild and predation rate within and along the edges of winter wheat (Triticum aestivum) fields surrounded by flowery or grassy strips from May to July 2014 in Denmark. Predators were collected using pitfalls traps and a suction sampler, while predation rate was measured using aphids cages (open, partially open, and closed as control), and sentinel prey made of plasticine, that allows the identification of the predator marks. Ground beetles (Carabidae), rove beetles (Staphylinidae), spiders (Aranea), and parasitoid and predatory wasps (Hymenoptera) were the most common natural enemies during the experiment. We found significantly lower number of generalist predators (but not specialists) in flowery vs grassy margins (p<0.05) from the suction samples. Activity density recorded using pitfall traps did not show significant difference in flowery vs. grassy margins for either specialist or generalist predators. Mean survival time of in-field aphid colonies was shorter (5.8 days) near flowery vs. grassy (9.9 days) edges. However, the Biological Control Index was not different. Forty-six % (n=756/1637) of the sentinel prey were attacked after 24 h mostly by chewing insects (88%, n=665/756 of the bites), followed by small mammals (13.2%, n=100/756), and birds (1.3%, n=10/756). Predation rate by chewing insects was higher in grass than flowery margins (48.9%, n=436/892 vs. 30.7%, n=229/745), and also higher in the edge than within field (45.3%, n=371/819 vs. 35.9%, n=294/818). In the flowery strips, predation was slightly higher within the field than in the edge (30.9%, n=115/372 vs. 30.6%, n=114/373, respectively), while in grassy ones, it was higher in the edge than within field (57.6%, n=257/446 vs. 40.1% n=179/446). Our preliminary results suggested that flowery strips enhance specialist but not generalist predator abundance in the field edges.

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Appendix 3

Abstract of the oral presentation for the PURE conference on IPM Innovationin Europe, Poznan, Poland, January 14-16 2015

Designing multifunctional margins for biocontrol in wheat-oilseed rape rotations

Samantha M. Cook1, Matthew P. Skellern1, Lucy Nevard1, Gabor Lövei2, & Judith K. Pell1,3

1Department of AgroEcology, Rothamsted Research, Harpenden, Hertfordshire, UK 2Department of Agroecology, Aarhus University, Flakkebjerg Research Centre, Forsoegsvej 1, DK-4200 Slagelse, Denmark 3J.K. Pell Consulting, Luton, Bedfordshire, UK

Agricultural intensification has led to fragmentation of semi-natural habitats within the farmed landscape resulting in a loss of biodiversity and concern about the deterioration of important ecosystem services. Managed field margins that deliver multiple ecosystem services and take account of agronomic practicality could help to redress the balance and are essential if ‘land-sharing’ agri-environmental schemes are to be optimized. Provision for birds and pollinators has been a primary driver for field margin design to date and the value of margins for biocontrol of crop pests has been less well studied. A number of studies have shown the potential of grassy margins which support cereal aphids and their natural enemies for improved biocontrol in cereal crops. However, most arable rotations in Europe include oilseed rape (Brassica napus) and we have shown that margins that do not contain brassicas do not support well the specialist natural enemies important in the biocontrol of oilseed rape pests. Our work has focussed on designing field margins to increase the abundance of natural enemies and to provide biocontrol across the wheat-oilseed rape crop rotation. We tested a range of brassicas as potential ‘banker plants’ to provide resources for specialist natural enemies of oilseed rape pests. In the PURE project we assessed the value of field margins containing brassicas for invertebrate biodiversity in general and biocontrol in cereal and oilseed rape crops specifically. Our initial results suggest that while the brassica margins did increase the abundance and diversity of natural enemies found in field margins, there were limited positive effects on biocontrol in the crop or on yield. It seems that getting biocontrol agents into the open field remains one of the greatest challenges in delivering crop protection via conservation biocontrol.

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Appendix 4

Report on work done at Rothamsted Research, UK for the PURE project (Draft paper).

Effect of brassica field margins on arthropod biodiversity and biocontrol in a wheat-oilseed rape rotation

Sam M. Cook1, Matthew P. Skellern1, Martin Torrance1, Lucy Nevard1, Nigel P. Watts1, Suzanne J. Clark2 & Judith K. Pell3 1AgroEcology Department, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK. 2 Computational and Systems Biology Department, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK. 3J.K. Pell Consulting, 74 Wardown Crescent, Luton, Bedfordshire, LU2 7JT, UK.

Introduction

The objective of Task 10.2 was to investigate the biocontrol potential of non-cropped reservoir habitats in the farmed landscape, focusing on the ecological process underlying the functioning of these reservoirs, establishing the impact they can make on natural enemy densities and pest control, and how to manipulate these reservoir habitats to improve their biocontrol function. Task 10.2 pursued two approaches to address this objective: (i) on-station experiments testing the biocontrol response to field margin treatments and (ii) a review of the biological control literature. Here we present results from part (i); analyses from Rothamsted Research of a 2- year experiment, collaboratively conducted at two sites (Flakkebjerg, Denmark (AU) and Rothamsted Research, UK (RRes)) using complementary approaches. In recent years, field margins have become an important part of European agri-environment schemes. So far, field margin seed mixtures have tended to be designed for a specific purpose, for example to encourage pollinators or to support farmland birds. From a natural pest control perspective, grassy margins, which support cereal aphids and their natural enemies, have become an important area of study. The need to design multi-functional margins, however, has now been recognised and field margins which do not contain brassicas do not support the specialist natural enemies of oilseed rape, the second most important crop in most arable rotations (Skellern et al., submitted; see also Baverstock et al., 2014). The experiments were designed to assess the biodiversity of natural enemies inhabiting field margins containing brassicas, and estimate the effects of these natural enemies, supported by the margins, on biocontrol in adjacent crops within the wheat-oilseed rape rotation.

Materials & Methods

Brassica margins (3m wide) containing a 50:50 mixture of Fodder radish (Raphanus sativus cv. Apoll) and Tyfon (hybridized Brassica rapa Rapifera x B. rapa Pekinesis) were established alongside existing grass margins (3m) at the borders of wheat (Triticum aestivum) and oilseed rape (Brassica napus) crops. The composition of these margins was informed by previous (but as yet unpublished) studies (Skellern et al, submitted; Final report of Defra project IF0139). Crops with a grass margin but no brassica margin (3m bare ground at the field edge) served as controls (Figure 1).

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Figure 1. Experimental design for field experiments

Six fields of wheat and six fields of oilseed rape (OSR) were drilled on Rothamsted farm in autumn 2012. All fields had long-established 3m wide grass margins on all sides. Brassica field margins were drilled in autumn 2012 on one side of each of three of the wheat fields and three of the oilseed rape fields, adjacent to the existing grass margins. The orientation of the margins was selected carefully to provide three pairs of fields in each crop type with margins running in an equivalent direction; each pair had either just grass margins (control) or grass margins and an additional brassica margin (Fig. 2). Surrounding landscape features such as hedgerows and tree-lines at the borders were standardized as much as possible within pairs. In 2013 the experiment was set up for a second year using the same fields but, with crop rotation, fields previously containing wheat contained OSR and vice-versa. The grass margins were the same and brassica margins re-drilled.

To assess the arthropod communities in the two margin treatments and their effects on community structure and biocontrol potential in the crop, we conducted pitfall trapping and Vortis suction sampling for ground-dwelling and aerial arthropods, respectively. Both sampling methods were carried out in the wheat crops on two occasions in each year (June and July), to correspond with the ear emergence and grain ripening stages of the crop. In oilseed rape, sampling was also done on two occasions during each year, between mid-April and early June, to correspond with the flowering and pod development stages. Direct counts of aphid populations within wheat fields were made in 2013. To assess the relative effects of ground-dwelling and aerial predators, an exclusion cage experiment was carried out in 2013 and parasitism of oilseed rape pests was also assessed (2013).

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Figure 2. Field experimental set up at RRes 2013. Six fields of oilseed rape (OSR, highlighted in pink) and 6 fields of wheat (highlighted in yellow) were established. Red lines indicate positions of the borders; B = grass + brassica border; C = control grass border only. Roman numerals indicate treatment pairs such that brassica and control borders were orientated in a similar direction.

Pitfall trapping – ground active arthropods Pitfall traps consisted of plastic cups 150 ml volume and 7cm diameter, filled with 100 ml ethylene glycol. Plastic covers, supported by metal pins prevented by-catch of aerial arthropods. The pitfall traps were placed in all fields; three traps were placed 18.75m apart within the grass margin and the brassica margin (or the bare ground in the same position in the Control treatments) and at 5m, 10m, 20m and 40m into the crop parallel to the margin. The traps were left in place for one week on each sampling occasion. Samples were returned to the laboratory and stored at −5°C prior to identification of the arthropods present, to species level wherever possible. In 2014, directional pitfalls, with a plastic barrier bisecting the trap and extending 2 cm beyond the lip of the trap were placed 5m into the crop parallel to the crop/margin interface and used to gain a ‘snap-shot’ of movement towards, or away from, the margins.

Data were pooled from the three pitfall traps taken from each of the margin components and from each of the distances into the crop. For within-margin and within-field comparisons, season totals (over the two sample dates within each year) were analysed. Multi-stratum analysis of variance (ANOVA), with nested strata corresponding to years, fields and margin components, was used to compare activity-abundance of species, or groups, caught in the two margin treatments. Nested treatment contrasts were incorporated to additionally compare the arthropod communities caught in the different components of the margin treatments (i.e. grass margin compared with brassica margin or field edge). A nested ANOVA was also used to compare the 2014 directional trap catches (trap direction nested within treatment), using field/direction as random effects. Activity-abundance of species, or groups, caught within the field were analysed using a linear mixed model (LMM) fitted using residual maximum likelihood (REML). Nested random effects included were years, fields and within-field

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PURE – Deliverable D10.5 positions, plus an autocorrelation term to allow for changes in correlation with distance into each field. Fixed effects were the factorial set of treatments defined by margin treatment and distance into the crop. All analyses were done using GenStat, version 17 (VSN International, Hemel Hempstead, UK).

Vortis suction sampling- aerial arthropods A vortis suction sampler (Burkard, UK; see Arnold, 1994) was used. Samples were taken where possible to correspond with the pitfall sampling period, along transects marked by the pitfall traps in the grass and brassica margins, and at 5m, 10m, 20m and 40m into the crop. Samples were returned to the laboratory and stored at −5°C prior to processing and identification of the arthropods present, to species level wherever possible. Analyses of within-margin and within-field effects were done as described above.

Aphid counts Ten wheat plants were sampled along each transect 5, 10, 20 and 40m into each wheat crop. Aphids infesting each plant were counted and identified in situ and numbers of any parasitized aphids (mummies) were also recorded. Data were analysed as a LMM using REML as described above.

Exclusion cage experiment To provide a ‘snapshot’ of natural enemy activity against similar populations of aphids in each of the treatments, an exclusion experiment was done in June 2013 using insectary-reared sentinel Metopolophium dirhodum aphids on potted glasshouse-reared wheat plants following the principals of Gardiner et al. (2009). Pots containing six plants were sunk into the ground on each of two wheat fields with a brassica margin and two control wheat fields with just the grass margin. Pots were placed 10m apart along a transect parallel to the margin and 5m into the crop. Half of the plants were covered with perforated bread bags to exclude natural enemies while the rest remained uncovered and accessible to natural enemies. After 24h all plants were returned to the laboratory; remaining aphids were counted and placed on to fresh plants and incubated for 7 days. The number of aphids that had become parasitized, as determined by the number of parasitoid cocoons that formed, was recorded.

Assessment of parasitoid activity in oilseed rape In crops of oilseed rape, 100 pods were selected from each sampling site at the pod ripening phase. They were dissected in the laboratory and the numbers of pest larvae (seed weevil [Ceutorhynchus assimilis] and brassica pod midge [Dasineura brassicae]) and % parasitism were recorded. Data were analysed using ANOVA (GenStat, version 15 (VSN International, Hemel Hempstead, UK)).

Results and Discussion

Pitfall trapping within field margins The total number of carabids and their species richness was not significantly different in the brassica+grass and field edge+grass treatments (Tables 1 and 2). Differences were apparent, however, between individual margin components. Within field edge+grass margins next to both crops, total carabid numbers were c. 4-fold higher, and species richness significantly greater in the bare field edge plots than in adjacent grassy strips. It is important to recognise though, that these differences may largely be due to variation in pitfall sampling efficiency between the vegetation types; fast-moving beetles running over sparsely vegetated ground are

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PURE – Deliverable D10.5 more likely to be trapped than those whose movement is impeded by dense grassy vegetation (Thomas, Brown & Kendall, 2006), and thus direct comparisons of pitfall-trapped beetle abundance between different vegetation types should be treated with caution. Within the brassica+grass margins next to wheat crops, however, carabid numbers and species richness were higher in the brassica component than in the grass strips (Table 1), but this effect was not apparent for margins next to oilseed rape crops (Table 2), where no differences existed between the two vegetation types. These differences in response to margin components between crop types cannot be explained by vegetation-related sampling efficiency effects, but may be related to landscape concentration and dilution effects, which have previously been shown to influence local insect abundance (e.g. Haenke et al., 2009). In particular, the carabid species that tend to form communities within brassica crops may become more concentrated within isolated brassica strips (i.e. those next to wheat) than within those that are next to large areas of oilseed rape crops which may act to dilute populations locally.

On an individual species basis, only Nebria salina and Pterostichus melanarius showed statistically significant differences in their abundance between the main margin treatments (Tables 1 and 2). Nebria salina was consistently more abundant in the field edge+grass margins of both crop types than in the brassica+grass treatment. Pterostichus melanarius followed a similar pattern in margins next to wheat (borderline statistical significance), but conversely this species was more abundant in the brassica+grass margins when they were next to oilseed rape crops. Several species showed statistically significant or borderline- significant responses to individual margin components: for both crops, Nebria salina was more frequently trapped in field edge plots than in the adjacent grassy strips, and this pattern of responses was also shown by Amara ovata in margins next to oilseed rape. Within the brassica+grass margins next to oilseed rape crops, A. ovata was more abundant in the brassica component, while in those next to wheat Harpalus rufipes, A. ovata and P. melanarius all followed this pattern. Amara ovata was the only species to be consistent in this response within brassica+grass margins next to both crops, and this species has previously been shown to be typical of carabid communities associated with brassicas (more specifically, oilseed rape; Brooks et al., 2008).

With the exception of Pterostichus madidus in margins next to oilseed rape, no other carabid species were found to be more abundant in traps from the grassy strips than in those from either the brassica or field edge components; this observation most likely reflects the low efficiency of the traps placed in grassy vegetation.

When sampled from within the margins of either crop, no between-treatment differences were observed for other generalist predators caught in the pitfall traps (staphylinids and spiders). In the margins next to oilseed rape crops however, significantly more oilseed rape pests were trapped in the brassica and field edge components than in the grassy strips. Too few brassica specialist pests were sampled from margins next to wheat (even from the brassica component) to allow meaningful analysis. This most likely reflects the later timing of the sampling of the wheat margins, which was directed to coincide more with cereal aphid phenology than brassica pest phenology.

Within-crop pitfall trapping No significant effects of the margin treatments were found for overall carabid abundance or species richness within either the wheat or the oilseed rape crops (Tables 3 and 4). Three individual carabid species, however, showed significant within-field responses, but only in the oilseed rape crops. While Leistus spinibarbis and Bembidion lampros were more frequently

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PURE – Deliverable D10.5 trapped in oilseed rape fields next to brassica-containing margins, N. salina activity-density resonated with the within-margin results for this species, and was higher in fields next to margins where brassicas were absent. Interestingly, two of these species, B. lampros and N. salina, were also the only ones to show distance effects (Table 5). In oilseed rape B. lampros was edge-distributed, while N. salina tended to be most and least frequently trapped at 10m and 20m into the field, respectively. Edge distribution has previously been observed for B. lampros (Holland, Perry & Winder, 1999; Thomas et al., 2001), and perhaps it is more likely that edge distributed species would respond to the margin treatments than typically more widely dispersed species.

It is known that the activity of satiated beetles can be reduced and that well-resourced individuals may be less likely to be caught in pitfall traps than those that are under-resourced (Fournier & Loreau, 2001). The differential responses to treatment shown by B. lampros, L. spinibarbis and N. salina, however, are difficult to interpret in the light of this, but may be due to differences in life histories. On one hand, lower activity-density in fields next to brassica-containing margins, as in the case of N. salina, could indicate more satiated beetles as a result of better resource access, but this explanation would not apply to L. spinibarbis and B. lampros. On the other hand, the higher catches of L. spinibarbis and B. lampros in fields next to brassica-containing margins could be interpreted as representing higher densities of these species, as a result of better resource access, but on this basis it is difficult to see why N. salina densities should be lower (as opposed to not different or higher) in fields next to the brassica margins, where food resource availability (pest larval prey) is expected to be higher. Furthermore, the response to treatment of Leistus spinibarbis is also surprising as this species is considered a collembola-feeding specialist (Hengeveld, 1979).

Spiders and staphylinids showed no significant treatment effects in either crop, and oilseed rape pests (within the oilseed rape crops) were unaffected by the margin treatments. Interestingly, however, despite the lack of an overall treatment effect in wheat, both total staphylinids and Tachyporus spp. showed significant treatment x distance interactions (Table 6). In wheat fields next to brassica-containing margins, their abundance tended to decrease from the inner crop towards the edge, while in fields next to margins without brassicas, abundance increased towards the edge of the field. These results are again difficult to interpret; reduced activity due to more abundant food resources close to the brassica- containing margins could, at least in part, explain this interaction.

Directional pitfall trapping Within oilseed rape crops next to both margin treatments, no differences in carabid, spider or staphylinid abundance were observed between edge- and inner field-facing pitfall traps (Table 7). However, during June, in the wheat crops with brassica-containing margins only, significantly more carabids were found in the field-facing traps than in those facing the margins. Rather than reflecting a net movement out of the field, which would be unlikely at a time of year when cereal aphid populations should be building up, this result may reflect reduced beetle activity around the traps facing the brassica margins due to their provision of additional food resources (specialist pest larvae).

By the time of the July sample, carabid numbers no longer differed between field- and edge- facing traps in either treatment, and this may reflect a later-season reduction in larval prey resource provision by the brassica margins, leading to more equalised carabid activity around both field- and edge-facing traps. In contrast, in July Staphylinids were more abundant in edge-facing traps than in those facing the centres of the fields next to brassica-containing

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PURE – Deliverable D10.5 margins, but numbers did not differ between trap directions for those traps next to margins without brassicas; perhaps this could represent a movement of these insects into the field as resources previously provided by the brassica margins became unavailable.

Suction sampling within field margins In field margins next to oilseed rape crops the abundance of oilseed rape pests was significantly greater in the brassica+grass treatment than in the control (Table 8). Comparisons of individual margin components revealed that, as might be expected, these brassica specialists were more abundant within the brassica strips than within the adjacent grassy areas. These patterns were repeated for pollen beetles, when analysed individually, and also for stem weevil parasitoids, seed weevil parasitoids, and total numbers of specialist natural enemies of oilseed rape pests. Pollen beetle parasitoid abundance, however, was greater within the brassica plots than within the adjacent grassy strips, but did not differ overall between the brassica+grass and field edge+grass treatments. No differences were detected between margins or margin components for aphids or their specialist predators and parasitoids. Total numbers of all specialist natural enemies (brassica pest and aphid specialists), however, did differ between treatments and margin components, reflecting the general trends described above for the brassica specialist natural enemies alone.

When analysed in aggregate, the generalist natural enemies sampled from margins next to oilseed rape fields did not differ between the main margin treatments, but within the grass+field edge treatment, more individuals were found in the grassy strips than in the field edge plots; this pattern of results was also reflected in both spider (borderline significance) and staphylinid numbers. In addition, however, within the brassica+grass treatment the staphylinids were also found to be more abundant in the grassy strips than in the brassica plots. The predatory empid flies were an exception to the overall trends for generalists, and were more abundant within the brassica+grass treatment than in the field edge+grass margins, and were also more frequently caught within the brassica strips than in the adjacent grassy areas.

In field margins next to the wheat crops (Table 9), pollen beetle numbers did not differ overall between the brassica+grass and control treatments, but within the control field edge+grass treatment beetle abundance was higher in the grassy strips. These results contrast with those for pollen beetles in margins next to oilseed rape, but the differences can be attributed to the later sampling time in wheat; by the time the wheat margins were sampled in June and July, the majority of beetles may have moved off the brassica strips to feed on other flowers such as some of those likely to be found in grassy areas.

In terms of wheat pests and their natural enemies, no differences between margin treatments were found for aphids, aphid parasitoids, or orange wheat blossom midge. Within the brassica+grass treatment, however, gout fly numbers were found to be higher in the grassy areas. Interestingly, the abundance of specialist aphid predators (lacewings, ladybirds and hoverflies) was found to be significantly higher in the brassica+grass treatment than in the control margins.

None of the generalist natural enemies sampled from wheat margins differed between the treatments, but within brassica+grass, spiders were more frequently found in the grassy strips, and this result was also reflected in the results for generalist natural enemies in aggregate.

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Within-field suction sampling The presence of brassicas within field margins next to both wheat and oilseed rape crops did not significantly influence numbers of any of the pests and specialist or generalist natural enemies sampled from within-field (Tables 10 and 11). In wheat crops however, orange wheat blossom midge numbers showed a borderline-significant trend of higher numbers in the fields next to brassica-containing margins (Table 11). The dolichopods, when sampled from wheat, were the only group from either crop to show significant distance effects, tending to be edge- distributed (Table 12).

Aphid counts Aphid counts within the wheat fields (conducted in 2013 only) showed no significant treatment effects for total cereal aphids or for parasitised aphid mummies (Table 13).

Exclusion cage experiment There was no significant difference between the number of aphids found on the plants retrieved (estimate of predation) from fields adjacent to either of the margin treatments (with/without brassica margin) regardless of whether they were with or without the exclusion cage. After incubation, not a single aphid was found to be parasitized. An exclusion cage experiment adapted from this trial was conducted at Flakkebjerg, Denmark (AU) in 2014.

Assessment of parasitism activity in oilseed rape The numbers of pest larvae that had been parasitized, were too few to analyse (only two parasitoid eggs were found from a total of 400 pods assessed). The numbers of pod midge larvae (pest) were too low for meaningful analysis. For seed weevil larvae (pest), the power in the analysis between margin treatments was too low to be meaningful. There was no effect of distance or interaction with margin treatment and distance (F3,6 = 0.54; P = 0.67 and F3,6 = 0.45 P = 0.73, respectively).

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Table 1. Results from analyses of variance (ANOVA) of pitfall trap data (season totals) collected from within brassica-containing and control field margins adjacent to wheat fields. The first entry for each species or group represents comparisons between margin treatments (brassica+grass vs. field edge+grass; n.d.f.=1, d.d.f.=9); the second and third entries represent nested comparisons of individual margin components within these treatments (n.d.f.=1, d.d.f.=10). Grass BR and Grass FE represent grass strips next to brassica and field edge strips, respectively. With the exception of carabid species richness, means are on log10(y+1) scale, and back- transformed values are given in brackets. Statistically significant or borderline-significant comparisons are shown in bold typeface Margin treatment / component Species/ Brassica + Field edge + s.e.d. F P Group Grass / Grass / Brassica Grass BR Field edge Grass FE Carabids Leistus 0.158 (0.4) - 0.151 (0.4) - 0.151 0.00 0.963 spinibarbis 0.186 (0.5) 0.130 (0.3) - - 0.114 0.24 0.634 - - 0.050 (0.1) 0.251 (0.8) 0.114 3.10 0.109 Nebria 0.223 (0.7) - 0.310 (1.0) - 0.099 0.76 0.407 brevicollis 0.330 (1.1) 0.116 (0.3) - - 0.144 2.20 0.169 - - 0.410 (1.6) 0.209 (0.6) 0.144 1.94 0.194

Nebria 0.144 (0.4) - 0.457 (1.9) - 0.133 5.48 0.044 salina 0.289 (0.9) 0.00 (0.0) - - 0.182 2.52 0.143 - - 0.633 (3.3) 0.280 (0.9) 0.182 3.77 0.081 Pterostichus 0.542 (2.5) - 0.672 (3.7) - 0.237 0.30 0.598 madidus 0.626 (3.2) 0.458 (1.9) - - 0.169 0.99 0.344 - - 0.837 (5.9) 0.506 (2.2) 0.169 3.86 0.078

Pterostichus 0.395 (1.5) - 0.763 (4.8) - 0.198 3.45 0.096 melanarius 0.581 (2.8) 0.209 (0.6) - - 0.183 4.13 0.070 - - 1.100 (11.6) 0.426 (1.7) 0.183 13.57 0.004 Amara ovata 0.376 (1.4) - 0.125 (0.3) - 0.152 2.71 0.134 0.753 (4.7) 0.00 (0.0) - - 0.167 20.30 0.001 - - 0.201 (0.6) 0.050 (0.1) 0.167 0.81 0.389 Harpalus 0.237 (0.7) - 0.280 (0.9) - 0.095 0.21 0.659 rufipes 0.474 (2.0) 0.00 (0.0) - - 0.167 8.06 0.018 - - 0.360 (1.3) 0.201 (0.6) 0.167 0.91 0.363 Total 1.202 (14.9) - 1.340 (20.9) - 0.137 1.03 0.337 Carabids 1.487 (29.7) 0.916 (7.24) - - 0.177 10.47 0.009 - - 1.639 (42.6) 1.041 (10.0) 0.177 11.48 0.007

Carabid 6.17 - 7.50 - 0.981 1.85 0.207 species 7.83 4.50 - - 1.174 8.06 0.018 richness - - 8.83 6.17 1.174 5.16 0.046 Other generalist predators Total 0.824 (5.7) - 1.017 (9.4) - 0.132 2.13 0.178 Staphylinids 0.691 (3.9) 0.957 (8.1) - - 0.157 2.86 0.122 - - 0.983 (8.6) 1.051 (10.2) 0.157 0.18 0.677 Araneae 1.633 (42.0) - 1.746 (54.7) - 0.081 1.96 0.195 1.528 (32.7) 1.738 (53.7) - - 0.134 2.46 0.148 - - 1.762 (56.8) 1.730 (52.7) 0.134 0.06 0.814

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Table 2. Results from analyses of variance (ANOVA) of pitfall trap data (season totals) collected from within brassica- containing and control field margins adjacent to oilseed rape fields (see Table 1 legend for further explanation). Margin treatment / component Species/ Brassica + Field edge + s.e.d. F P Group Grass / Grass / Brassica Grass BR Field edge Grass FE Carabids Leistus 0.357 (1.3) - 0.286 (0.9) - 0.148 0.23 0.643 spinibarbis 0.397 (1.5) 0.317 (1.1) - - 0.169 0.22 0.648 - - 0.230 (0.7) 0.342 (1.2) 0.169 0.44 0.524 Nebria 0.392 (1.5) - 0.321 (1.1) - 0.197 0.13 0.727 brevicollis 0.410 (1.6) 0.374 (1.4) - - 0.200 0.03 0.862 - - 0.441 (1.8) 0.201 (0.6) 0.200 1.45 0.257

Nebria 0.184 (0.5) - 0.774 (4.9) - 0.204 8.34 0.018 salina 0.151 (0.4) 0.217 (0.6) - - 0.139 0.23 0.643 - - 1.158 (13.4) 0.389 (1.5) 0.139 30.71 <0.001 Pterostichus 0.583 (2.8) - 0.475 (2.0) - 0.224 0.23 0.640 madidus 0.379 (1.4) 0.787 (5.1) - - 0.176 5.33 0.044 - - 0.489 (2.1) 0.460 (1.9) 0.176 0.03 0.871 Pterostichus 0.345 (1.2) - 0.125 (0.3) - 0.082 7.16 0.025 melanarius 0.330 (1.1) 0.360 (1.3) - - 0.100 0.09 0.775 - - 0.100 (0.3) 0.151 (0.4) 0.100 0.25 0.627 Poecilus 0.325 (1.1) - 0.265 (0.8) - 0.181 0.11 0.748 cupreus 0.483 (2.0) 0.167 (0.5) - - 0.210 2.28 0.162 - - 0.401 (1.5) 0.130 (0.3) 0.210 1.67 0.226 Amara ovata 0.338 (1.2) - 0.302 (1.0) - 0.110 0.05 0.822 0.546 (2.5) 0.130 (0.3) - - 0.116 6.44 0.029 - - 0.554 (2.6) 0.050 (0.1) 0.116 9.42 0.012 Total 1.297 (18.8) - 1.370 (22.4) - 0.312 0.31 0.589 Carabids 1.279 (18.0) 1.314 (19.6) - - 0.166 0.05 0.835 - - 1.659 (44.6) 1.081 (11.0) 0.166 12.11 0.006 Carabid spp. 7.25 - 6.83 - 0.991 0.18 0.684 Richness 7.67 6.83 - - 1.726 0.23 0.640 - - 8.83 4.83 1.726 5.37 0.043 Other generalist predators Total 0.942 (7.7) - 0.691 (3.9) - 0.105 2.86 0.125 Staphylinids 0.903 (7.0) 0.982 (8.6) - - 0.167 0.11 0.745 - - 0.524 (2.3) 0.858 (6.2) 0.167 2.00 0.187

Araneae 1.802 (62.4) - 1.789 (60.5) - 0.142 0.01 0.931 1.744 (54.5) 1.861 (71.6) - - 0.130 0.81 0.389 - - 1.749 (55.1) 1.830 (66.6) 0.130 0.39 0.549 Oilseed rape pests Phyllotreta 0.160 (0.4) - 0.182 (0.5) - 0.111 0.04 0.847 spp. 0.321 (1.1) 0.00 (0.0) - - 0.182 3.12 0.108 - - 0.314 (1.1) 0.05 (0.1) 0.182 2.12 0.176 OSR pests 0.282 (0.9) - 0.354 (1.3) - 0.116 0.39 0.550 0.484 (2.0) 0.080 (0.2) - - 0.158 6.57 0.028 - - 0.527 (2.4) 0.180 (0.5) 0.158 4.85 0.052

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Table 3. Results from linear mixed model analyses (using REML) of pitfall trap data (season totals) collected from wheat fields next to either brassica-containing or control field margins. With the exception of carabid species richness, means are on log10(y+1) scale, and back-transformed values are given in brackets. Statistically significant or borderline-significant terms are shown in bold typeface.

Species / group Brassica + Field edge + s.e.d. F (1,9) P grass margin grass margin

Carabids Nebria brevicollis 0.161 (0.4) 0.187 (0.5) 0.105 0.06 0.806 Nebria salina 0.133 (0.4) 0.321 (1.1) 0.121 2.40 0.152 Loricera pilicornis 0.133 (0.4) 0.128 (0.3) 0.050 0.01 0.919 Pterostichus madidus 0.953 (8.0) 0.888 (6.7) 0.294 0.05 0.830

Pterostichus melanarius 1.197 (14.7) 1.216 (15.4) 0.225 0.00 1.000

Poecilus cupreus 0.243 (0.7) 0.160 (0.4) 0.146 0.29 0.605

Anchomenus dorsalis 0.283 (0.9) 0.310 (1.0) 0.139 0.04 0.848

Harpalus rufipes 0.255 (0.8) 0.266 (0.8) 0.112 0.01 0.919

Demetrias atricapillus 0.218 (0.7) 0.134 (0.4) 0.109 0.60 0.460

Trechus quadristriatus 0.305 (1.0) 0.371 (1.4) 0.209 0.10 0.757

Total Carabids 1.646 (43.3) 1.691 (48.1) 0.120 0.14 0.713

Carabid richness 6.750 7.083 1.214 0.11 0.752

Other generalist predators

Tachyporus spp. 0.476 (2.0) 0.390 (1.5) 0.089 0.93 0.359

Total Staphylinids 1.110 (11.9) 1.004 (9.1) 0.163 0.44 0.525

Total Araneae 1.651 (43.8) 1.710 (50.3) 0.118 0.23 0.645

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Table 4. Results from REML analyses of pitfall trap data (season totals) collected from oilseed rape fields next to either brassica-containing or control field margins (see Table 3 legend for further explanation).

Species / group Brassica + grass Field edge + s.e.d. F (1,9) P margin grass margin Carabids

Leistus spinibarbis 0.336 (1.2) 0.135 (0.4) 0.069 7.71 0.019

Nebria brevicollis 0.162 (0.5) 0.388 (1.4) 0.227 0.99 0.347

Nebria salina 0.227 (0.7) 0.859 (6.2) 0.247 6.54 0.031 Loricera pilicornis 0.081 (0.2) 0.184 (0.5) 0.082 1.57 0.241 Pterostichus madidus 0.180 (0.5) 0.288 (0.9) 0.076 2.11 0.180 Pterostichus melanarius 0.257 (0.8) 0.140 (0.4) 0.131 0.50 0.495

Poecilus cupreus 0.853 (6.1) 0.383 (1.4) 0.275 2.37 0.155

Amara ovata 0.394 (1.5) 0.552 (2.6) 0.187 0.99 0.346

Amara similata 0.240 (0.7) 0.450 (1.8) 0.151 2.20 0.167

Notiophilus biguttatus 0.107 (0.3) 0.124 (0.3) 0.052 0.12 0.739

Anchomenus dorsalis 0.384 (1.4) 0.239 (0.7) 0.123 1.44 0.264 Harpalus rufipes 0.133 (0.4) 0.050 (0.1) 0.071 1.36 0.273 Demetrias atricapillus 0.138 (0.4) 0.133 (0.4) 0.059 0.01 0.931 Bembidion lampros 0.318 (1.1) 0.132 (0.4) 0.057 10.51 0.012 Total Carabids 1.377 (22.8) 1.500 (30.6) 0.180 0.52 0.490

Carabid sp. richness 7.375 8.167 1.343 0.59 0.462

Other generalist predators Total Staphylinids 0.900 (6.9) 1.152 (13.2) 0.160 3.00 0.120 Total Araneae 1.531 (33.0) 1.368 (22.3) 0.138 1.29 0.287 Pests All OSR pests 0.694 (3.9) 0.634 (3.3) 0.152 0.23 0.644

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Table 5. Results from REML analyses of pitfall trap data (season totals) collected from oilseed rape fields next to either brassica-containing or control field margins: distance effects (only statistically significant relationships shown) (see Table 3 legend for further explanation).

Species / Distance into crop s.e.d. F (3,30) P group 5 10 20 40 Nebria salina 0.536 (2.4) 0.655 (3.5) 0.400 (1.5) 0.581 (2.8) 0.075 4.06 0.016 Bembidion lampros 0.408 (1.6) 0.225 (0.7) 0.190 (0.5) 0.075 (0.2) 0.080 5.90 0.004

Table 6. Results from REML analyses of pitfall trap data (season totals) collected from wheat fields next to either brassica-containing or control field margins: treatment x distance effects (only statistically significant relationships shown) (see Table 3 legend for further explanation).

Species / Treatment Distance into crop F P group 5 10 20 40 s.e.d. (3,30) Tachyporus Grass + 0.339 0.381 0.659 0.526 0.154 3.94 0.017 spp. brassica (1.2) (1.4) (3.6) (2.4) Grass + 0.620 0.351 0.230 0.358

field edge (3.2) (1.2) (0.7) (1.3) Total Grass + 0.860 1.085 1.213 1.283 0.140 9.12 <0.001 Staphylinids brassica (6.2) (11.2) (15.3) (18.2) Grass + 1.258 1.039 0.735 0.983

field edge (17.1) (9.9) (4.4) (8.6)

Table 7. Results from analyses of variance (ANOVA) of data from directional pitfall traps collected on two different dates in 2014 from within wheat and oilseed rape fields adjacent to either brassica-containing or control field margins. Traps were set 5m from the edge of the margin, within the cropped area. The first entry for each species or group represents comparisons of 5m trap catches between main margin treatments (brassica+grass vs. field edge+grass), and the second and third entries represent nested comparisons of inner field- vs. edge-facing traps within each of these treatments. Means are on log10(y+1) scale, and back-transformed values are given in brackets. Statistically significant or borderline-significant relationships are shown in bold typeface.

Species/ Brassica + Grass Field edge + Grass s.e.d. F(1,4) P Group Field-facing Edge-facing Field-facing Edge-facing Oilseed Rape (April) Total 0.614 (3.1) - 0.704 (4.1) - 0.132 0.47 0.530 Araneae 0.634 (3.3) 0.593 (2.9) - - 0.133 0.10 0.770 - - 0.693 (3.9) 0.715 (4.2) 0.133 0.03 0.875 All 0.722 (4.3) - 0.782 (5.1) - 0.167 0.14 0.729 Generalists 0.702 (4.0) 0.742 (4.5) - - 0.082 0.23 0.657 - - 0.748 (4.6) 0.816 (5.5) 0.082 0.69 0.454 Oilseed Rape (May) Poecilus 0.400 (1.5) - 0.191 (0.6) - 0.302 0.48 0.527 cupreus 0.360 (1.3) 0.441 (1.8) - - 0.133 0.37 0.576 - - 0.282 (0.9) 0.100 (0.3) 0.133 1.85 0.245

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Total 0.706 (4.1) - 0.818 (5.6) - 0.121 0.86 0.405 Carabids 0.796 (5.3) 0.615 (3.1) - - 0.187 0.94 0.388 - - 0.725 (4.3) 0.911 (7.1) 0.187 0.98 0.378 Total 0.535 (2.4) - 0.809 (5.4) - 0.243 1.27 0.322 Staphylinid 0.651 (3.5) 0.418 (1.6) - - 0.235 0.99 0.377 s - - 0.864 (6.3) 0.753 (4.7) 0.235 0.22 0.661 Total 0.750 (4.6) - 0.983 (8.6) - 0.120 3.79 0.123 Araneae 0.725 (4.3) 0.774 (4.9) - - 0.182 0.07 0.802 - - 0.994 (8.9) 0.973 (8.4) 0.182 0.01 0.914 All 1.111 (11.9) - 1.342 (21.0) - 0.140 2.71 0.175 generalists 1.192 (14.6) 1.030 (9.7) - - 0.146 1.22 0.331 - - 1.335 (20.6) 1.349 (21.3) 0.146 0.01 0.929 Wheat (June) Pterostichus 0.337 (1.2) - 0.796 (5.3) - 0.361 1.62 0.272 melanarius 0.441 (1.8) 0.233 (0.7) - - 0.170 1.49 0.290 - - 0.752 (4.64) 0.840 (5.9) 0.170 0.27 0.634 Total 0.626 (3.2) - 1.157 (13.4) - 0.327 2.63 0.180 Carabids 0.711 (4.1) 0.541 (2.5) - - 0.051 11.27 0.028 - - 1.208 (15.1) 1.106 (11.8) 0.051 4.06 0.114 Total 0.606 (3.0) - 0.992 (8.8) - 0.172 5.02 0.089 Staphylinid 0.651 (3.5) 0.560 (2.6) - - 0.100 0.84 0.412 s - - 1.079 (11.0) 0.905 (7.0) 0.100 3.05 0.155 Total 0.976 (8.5) - 1.181 (14.2) - 0.295 0.48 0.525 Araneae 1.071 (10.8) 0.881 (6.6) - - 0.093 4.16 0.111 - - 1.212 (15.3) 1.149 (13.1) 0.093 0.45 0.539 All 1.22 (15.4) - 1.579 (36.9) - 0.273 1.79 0.252 generalists 1.317 (19.7) 1.113 (12.0) - - 0.079 6.62 0.062 - - 1.638 (42.5) 1.521 (32.2) 0.079 2.17 0.215 Wheat (July) Pterostichus 0.347 (1.2) - 0.617 (3.1) - 0.255 1.12 0.349 melanarius 0.259 (0.8) 0.434 (1.7) - - 0.205 0.72 0.444 - - 0.460 (1.9) 0.774 (4.9) 0.205 2.34 0.201 Total 0.491 (2.1) - 0.823 (5.7) - 0.240 1.91 0.240 Carabids 0.382 (1.4) 0.600 (3.0) - - 0.241 0.82 0.417 - - 0.719 (4.2) 0.926 (7.4) 0.241 0.74 0.439 Total 0.460 (1.9) - 0.808 (5.4) - 0.231 2.26 0.207 Staphylinid 0.318 (1.1) 0.602 (3.0) - - 0.078 13.20 0.022 s - - 0.842 (6.0) 0.774 (4.9) 0.078 0.76 0.433 Total 1.112 (11.9) - 1.289 (18.5) - 0.327 0.30 0.616 Araneae 0.970 (8.3) 1.253 (16.9) - - 0.209 1.84 0.247 - - 1.315 (19.7) 1.263 (17.3) 0.209 0.06 0.815 All 1.346 (21.2) - 1.510 (31.4) - 0.195 0.71 0.446 generalists 1.231 (16.0) 1.460 (27.8) - - 0.160 2.05 0.225 - - 1.518 (32.0) 1.502 (30.8) 0.160 0.01 0.922

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Table 8. Results from analyses of variance (ANOVA) of suction sample data (season totals) collected from within brassica- containing or control field margins next to oilseed rape crops (see Table 1 legend for further explanation). Species/ Brassica + Field edge + s.e.d. F P Group Grass / Grass / Brassica Grass BR Field edge Grass FE Pests Pollen 0.709 (4.1) - 0.257 (0.8) - 0.105 18.48 0.002 beetles 1.238 (16.3) 0.180 (0.5) - - 0.189 31.34 <0.001 - - 0.167 (0.5) 0.347 (1.2) 0.189 0.91 0.364 OSR pests 0.846 (6.0) - 0.332 (1.1) - 0.114 20.52 0.001 1.404 (24.4) 0.289 (0.9) - - 0.223 25.03 <0.001 - - 0.259 (0.8) 0.405 (1.5) 0.223 0.43 0.528

Aphids 0.234 (0.7) - 0.402 (1.5) - 0.144 1.35 0.275 0.201 (0.6) 0.267 (0.8) - - 0.184 0.13 0.726 - - 0.246 (0.8) 0.557 (2.6) 0.184 2.86 0.122 Specialist natural enemies Pollen beetle 0.474 (2.0) - 0.195 (0.6) - 0.164 2.92 0.122 parasitoids 0.848 (6.0) 0.100 (0.3) - - 0.217 11.85 0.006 - - 0.224 (0.7) 0.167 (0.5) 0.217 0.07 0.798

Stem weevil 0.527 (2.4) - 0.00 (0.0) - 0.030 305.61 <0.001 parasitoids 0.953 (8.0) 0.100 (0.3) - - 0.093 83.50 <0.001 - - 0.00 (0.0) 0.00 (0.0) 0.093 0.00 1.000 Seed weevil 0.275 (0.9) - 0.140 (0.4) - 0.056 5.80 0.039 parasitoids 0.551 (2.6) 0.000 (0.0) - - 0.120 21.20 <0.001 - - 0.151 (0.4) 0.13 (0.3) 0.120 0.03 0.865

All specialist 0.744 (4.5) - 0.303 (1.0) - 0.107 16.95 0.003 natural 1.308 (19.3) 0.180 (0.5) - - 0.208 29.52 <0.001 enemies of - - 0.310 (1.0) 0.296 (1.0) 0.208 0.00 0.951 OSR pests

Aphid 0.215 (0.6) - 0.100 (0.3) - 0.069 2.82 0.127 predators & 0.230 (0.7) 0.201 (0.6) - - 0.182 0.03 0.875 parasitoids - - 0.050 (0.1) 0.151 (0.4) 0.182 0.30 0.594

All specialist 0.915 (7.2) - 0.484 (2.0) - 0.109 15.50 0.003 natural 1.383 (23.2) 0.447 (1.8) - - 0.206 20.69 0.001 enemies - - 0.492 (2.1) 0.476 (2.0) 0.206 0.01 0.939

Generalist natural enemies Staphylinids 0.369 (1.3) - 0.453 (1.8) - 0.072 1.38 0.271 0.100 (0.3) 0.638 (3.3) - - 0.159 11.43 0.007 - - 0.251 (0.8) 0.656 (3.5) 0.159 6.50 0.029 Empids 0.338 (1.2) - 0.125 (0.3) - 0.070 9.41 0.013 0.577 (2.8) 0.100 (0.3) - - 0.092 26.87 <0.001 - - 0.100 (0.3) 0.151 (0.4) 0.092 0.30 0.597

Araneae 0.499 (2.2) - 0.420 (1.6) - 0.088 0.82 0.388 0.410 (1.6) 0.589 (2.9) - - 0.109 2.71 0.131 - - 0.318 (1.1) 0.52 (2.3) 0.109 3.50 0.091 All generalist 0.878 (6.6) - 0.754 (4.7) - 0.083 2.25 0.168 natural 0.811 (5.5) 0.945 (7.8) - - 0.165 0.65 0.437 enemies - - 0.547 (2.5) 0.960 (8.1) 0.165 6.26 0.031

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Table 9. Results from analyses of variance (ANOVA) of suction sample data (season totals) collected from within brassica-containing or control field margins next to wheat crops (see Table 1 legend for further explanation).

Species/ Brassica + Field edge + s.e.d. F P Group Grass / Grass / Brassica Grass BR Field edge Grass FE Pests Pollen 0.714 (4.2) - 0.581 (2.8) - 0.229 0.34 0.574 beetles 0.852 (6.1) 0.576 (2.8) - - 0.264 1.10 0.320 - - 0.286 (0.9) 0.879 (6.51) 0.264 4.99 0.050 Aphids 0.486 (2.1) - 0.612 (3.1) - 0.104 1.48 0.255 0.418 (1.6) 0.554 (2.6) - - 0.174 0.60 0.456 - - 0.551 (2.6) 0.674 (3.72) 0.174 0.50 0.495

Gout fly 0.188 (0.5) - 0.257 (0.8) - 0.153 0.21 0.660 0.000 (0.0) 0.376 (1.4) - - 0.148 6.49 0.029 - - 0.180 (0.5) 0.335 (1.2) 0.148 1.10 0.319 Orange 0.531 (2.4) - 0.549 (2.5) - 0.180 0.01 0.924 wheat 0.442 (1.8) 0.621 (3.2) - - 0.176 1.04 0.332 midge - - 0.437 (1.7) 0.661 (3.6) 0.176 1.62 0.232 Specialist natural enemies Aphid 0.691 (3.9) - 0.880 (6.6) - 0.195 0.93 0.359 parasitoids 0.712 (4.2) 0.671 (3.7) - - 0.109 0.14 0.712 - - 0.893 (6.8) 0.866 (6.3) 0.109 0.06 0.810 Aphid 0.195 (0.6) - 0.025 (0.1) - 0.054 9.93 0.012 specialist 0.230 (0.7) 0.159 (0.4) - - 0.109 0.42 0.530 predators - - 0.000 (0.0) 0.050 (0.1) 0.109 0.21 0.655 Specialist Too few enemies of OSR pests All specialist 0.813 (5.5) - 0.963 (8.2) - 0.132 0.65 0.440 natural 0.884 (6.7) 0.741 (4.5) - - 0.070 2.07 0.181 enemies - - 0.987 (8.7) 0.940 (7.7) 0.070 0.23 0.644 Generalist natural enemies Empids 0.286 (0.9) - 0.274 (0.9) - 0.139 0.01 0.934 0.130 (0.3) 0.442 (1.8) - - 0.190 2.70 0.131 - - 0.259 (0.8) 0.289 (0.9) 0.190 0.02 0.880 Dolichopods 0.215 (0.6) - 0.386 (1.4) - 0.122 1.98 0.193 0.280 (0.9) 0.151 (0.4) - - 0.100 1.67 0.226 - - 0.410 (1.6) 0.363 (1.3) 0.100 0.22 0.648 Spiders 0.520 (2.3) - 0.517 (2.3) - 0.094 0.00 0.977 0.376 (1.4) 0.665 (3.6) - - 0.094 9.39 0.012 - - 0.559 (2.6) 0.476 (2.0) 0.094 0.77 0.402

All generalist 0.906 (7.1) - 0.973 (8.4) - 0.088 0.29 0.603 natural 0.736 (4.4) 1.076 (10.9) - - 0.093 6.68 0.027 enemies - - 0.979 (8.5) 0.967 (8.3) 0.093 0.01 0.928

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Table 10. Results from REML analyses of suction sample data (season totals) collected from oilseed rape fields next to either brassica-containing or control field margins (see Table 3 legend for further explanation).

Species / group Brassica + Field edge + s.e.d. F (1,9) P grass margin grass margin

Pests

Pollen beetles 1.149 (13.1) 1.012 (9.3) 0.169 0.66 0.438

Seed weevils 0.422 (1.6) 0.411 (1.6) 0.107 0.18 0.678

All OSR pests 1.398 (24.0) 1.310 (19.4) 0.117 0.57 0.467

Specialist natural enemies

Pollen beetle parasitoids 0.741 (4.5) 0.755 (4.7) 0.154 0.01 0.929

Seed weevil parasitoids 0.366 (1.3) 0.462 (1.9) 0.113 0.72 0.419

Stem weevil parasitoids 0.719 (4.2) 0.657 (3.5) 0.158 0.32 0.589 All specialist enemies of 1.103 (11.7) 1.078 (11.0) 0.132 0.05 0.830 OSR pests Aphid natural enemies 0.113 (0.3) 0.204 (0.6) 0.080 1.30 0.280 (predators & parasitoids) All specialist natural 1.193 (14.59) 1.179 (14.1) 0.105 0.02 0.884 enemies Generalist natural enemies

Empidae 0.260 (0.8) 0.235 (0.7) 0.098 0.06 0.820 All generalist natural 0.353 (1.3) 0.412 (1.6) 0.083 0.12 0.582 enemies

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Table 11. Results from REML analyses of suction sample data (season totals) collected from wheat fields next to either brassica-containing or control field margins (see Table 3 legend for further explanation).

Species / group Brassica + Field edge + s.e.d. F (1,9) P grass margin grass margin

Wheat pests Cereal aphids 1.189 (14.5) 1.138 (12.7) 0.111 0.22 0.653 Orange wheat blossom 0.946 (7.9) 0.719 (4.2) 0.121 3.54 0.093 midge Specialist natural enemies Aphid parasitoids 1.357 (21.8) 1.371 (22.5) 0.064 0.05 0.834

Aphid specialist predators 0.245 (0.8) 0.190 (0.5) 0.049 1.24 0.295 All specialist natural 1.410 (24.7) 1.412 (24.8) 0.059 0.00 0.974 enemies Generalist natural enemies Soldier beetles 0.198 (0.6) 0.075 (0.2) 0.118 1.08 0.328

Empids 0.702 (4.0) 0.608 (3.1) 0.157 0.36 0.560

Dolichopods 0.309 (1.0) 0.343 (1.2) 0.108 0.10 0.761

Spiders 0.720 (4.2) 0.773 (4.9) 0.103 0.27 0.617 All generalist natural 1.252 (16.9) 1.234 (16.1) 0.086 0.05 0.835 enemies

Table 12. Results from REML analyses of suction sample data (season totals) collected from wheat fields next to either brassica-containing or control field margins: distance effects (only statistically significant relationships shown) (see Table 3 legend for further explanation).

Species / Distance into crop s.e.d. F (3,30) P group 5 10 20 40 Dolichopods 0.436 (1.7) 0.305 (1.0) 0.391 (1.5) 0.173 (0.5) 0.077 4.47 0.010

Table 13. Results from REML analyses of aphid count data from wheat fields next to either brassica-containing or control field margins. Means are on log10(y+1) scale, and back-transformed values are given in brackets.

Species / group Brassica + Field edge + s.e.d. F (1,4) P grass margin grass margin

Sitobian avenae 0.765 (4.8) 0.922 (7.3) 0.150 1.08 0.357

Metopolophium dirhodum 0.388 (1.4) 0.345 (1.2) 0.180 0.06 0.822 Total cereal aphids 0.889 (6.7) 1.032 (9.8) 0.160 0.80 0.421 Parasitised aphid 0.447 (1.8) 0.466 (1.9) 0.242 0.01 0.943 mummies

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Conclusions and Management recommendations

Although within-field effects of the margin treatments were fairly elusive, the inclusion of brassicas in field margins clearly has some benefits, particularly for the natural enemies of specialist pests. In margins next to oilseed rape crops, specialist parasitoids of oilseed rape pests were more abundant in the brassica-containing margins than in those without, and although this was also true for the pests themselves, within-field pest abundance was unaffected. Few parasitoids of brassica pests, however, were sampled from the brassica- containing margins that were situated next to wheat crops, but this was most likely due to later sampling of the wheat margins (in June and July and towards the usual end of the window of activity for these insects). Thus it is probable that brassica-containing margins would continue to support these insects throughout phases of the crop rotation where oilseed rape crops are absent. In the margins of wheat fields, the inclusion of brassicas also appeared to benefit populations of specialist aphid predators, and this may be due to the provision of nectar, or additional aphid resources.

Overall, generalist predators appeared less responsive to the margin treatments than specialists, although the predatory empid flies were an exception, being particularly associated with the presence of margin brassicas. The pitfall trap results were difficult to interpret, but there was evidence of within-field effects of the margin treatments on the abundance of some individual carabid species in oilseed rape, with two species more frequently and one species less frequently trapped in the fields next to brassica-containing margins, respectively. Interestingly, the greater carabid abundance and species richness within the brassica component of margins that were spatially separated from the oilseed rape crops (i.e. those next to wheat) may illustrate the potential importance of brassica strips in supporting communities of carabid species that are usually associated with oilseed rape, at points in the rotation when the crop is absent.

Although there are potential benefits of the inclusion of brassicas in field margins, the brassica species or varieties selected should be chosen carefully, and combinations with the longest possible flowering period should be used to maximise the availability of floral resources and extend the window over which specialist pest larvae are available as prey or hosts. Care must also be taken to select brassicas that favour parasitoid production over the production of pests, as species such as Raphanus sativus have been shown to fit these criteria for pollen beetles, but to promote seed weevil populations (Skellern et al., submitted; Defra Project IF0139 Final report). Due to the ruderal nature of these plants, their maintenance within field margins from year to year is likely to be difficult, without regular soil disturbance and / or re-seeding, and the additional costs of these activities for farmers will need to be weighed against the pest control benefits.

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References

Baverstock, J., Pell, J.K., Storkey, J., Torrance, M.T. & Cook, S.M. (2014) Field margins for biocontrol and biodiversity across crop rotations: Overview of the aims and approaches of Defra project IF01122. Landscape Management for Functional Biodiversity, Bulletin IOBC/WPRS, 100, 29-33. Brooks, D., Perry, J., Clark, S., Heard, M., Firbank, L., Holdgate, R., Mason, N., Shortall, C., Skellern, M. & Woiwod, I. (2008) National-scale metacommunity dynamics of carabid beetles in UK farmland. Journal of Animal Ecology, 77, 265-274. Fournier, E. & Loreau, M. (2001) Activity and satiation state in Pterostichus melanarius: an experiment in different agricultural habitats. Ecological Entomology, 26, 235-244. Gardiner, M.M., Landis, D.A., Gratton, C., DiFonzo, C.D., O’Neal, M., Chacon, J.M., Wayo, M.T., Schmidt, N.P., Mueller, E.E. and Heimpel, G.E. (2009) Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecological Applications, 19, 143-154. Haenke, S., Scheid, B., Schaefer, M., Tscharntke, T. & Thies, C. (2009) Increasing syrphid fly diversity and density in sown flower strips within simple vs. complex landscapes. Journal of Applied Ecology, 46, 1106-1114. Hengeveld, R. (1979) Polyphagy, Oligophagy and Food Specialization in Ground Beetles (Coleoptera, Carabidae). Netherlands Journal of Zoology, 30, 564-584. Holland, J.M., Perry, J.N. & Winder, L. (1999) The within-field spatial and temporal distribution of arthropods in winter wheat. Bulletin of Entomological Research, 89, 499-513. Skellern, M.P., Clark, S.J., Ferguson, A.W., Watts, N.P. & Cook, S.M. Banker plant bonuses? The benefits and risks of including Brassia plants in field margins to promote conservation biocontrol of specialist pests (submitted) Thomas, C.F.G., Brown, N.J. & Kendall, D.A. (2006) Carabid movement and vegetation density: Implications for interpreting pitfall trap data from split fields. Agriculture Ecosystems & Environment, 113, 51-61. Thomas, C.F.G., Parkinson, L., Griffiths, G.J.K., Fernandez Garcia, A. & Marshall, E.J.P. (2001) Aggregation and temporal stability of carabid distributions in field and hedgerow habitats. Journal of Applied Ecology, 38, 100-116.

Acknowledgements We are grateful to Rothamsted Farm staff for management of the field sites; special thanks to Garry Talbot for helping to site the experimental pairs. This work was funded by the European Union Seventh Framework Programme (FP7/ 2007-2013) under the grant agreement n°265865- PURE. Rothamsted Research is a national institute of bioscience strategically funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC).

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