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Agriculture, Ecosystems and Environment 140 (2011) 62–67

Contents lists available at ScienceDirect

Agriculture, Ecosystems and Environment

journa l homepage: www.e lsev ier .com/ locate /agee

cological restoration on farmland can drive beneficial functionalesponses in plant and invertebrate communities

ichard F. Pywell a,∗, William R. Meeka, R.G. Loxtona, Marek Nowakowskib,laire Carvell a, Ben A. Woodcocka

NERC Centre for Ecology & Hydrology, Maclean Building, Wallingford, Oxfordshire, OX10 8BB, UKWildlife Farming Company, Chesterwood, Alchester Road, Chesterton, Oxon, OX26 1UN, UK

r t i c l e i n f o

rticle history:eceived 26 July 2010eceived in revised form5 November 2010ccepted 16 November 2010vailable online 14 December 2010

a b s t r a c t

This study contrasted the effects of the most widely implemented, low cost restoration prescriptions pro-moted by the English AES with more demanding and costly options on plant and invertebrate communitycomposition, and their functional traits. In all cases these prescriptions were compared to intensive cropmanagement. The plant community regenerating from the seed bank was species-poor, highly dynamicand had a high proportion of undesirable crop weeds. Sowing a low-cost, simple mix of tall grassesresulted in a stable community dominated by competitive grasses. Creation of these habitats resultedin negligible shifts in the functional composition of the associated invertebrate community. Sowing a

eywords:gri-environment schemeseneficial arthropodscosystem servicesield margin stripsollinatorseed addition

diverse mix of wildflowers resulted in a stable, perennial vegetation community with both legumes andregulating hemi-parasitic plants that supported significantly more pollinator and herbivore species, aswell as higher abundances of beneficial arthropod predators. There were no measured synergies when amix of tall grass and wildflower habitats were created adjacent to each other on the same margin. Theresults confirm the value of ecological restoration as a potentially useful means of enhancing ecosystemfunction within intensive farmland systems.

ustainable agriculture

. Introduction

There is growing evidence that ecological restoration of appro-riate habitats on farmland increases habitat heterogeneity andan mitigate some of these damaging effects (Tscharntke et al.,005; Wade et al., 2008; Rey Benayas et al., 2009). In the contextf this study we refer to restoration as the creation of habitats ofncreased floristic and faunistic diversity on land that had been pre-iously used for crop production. The European agri-environmentalchemes (AES) are voluntary agreements with farmers whicheward environmentally-sensitive land management often associ-ted with traditional, extensive farming practices (Ovenden et al.,998). They are increasingly seen as a means of planning and

mplementing the large-scale ecological restoration required toeliver sustainable agriculture and ensure the continued provisionf ecosystem services. However, the effectiveness of these policies

emains poorly monitored (Kleijn and Sutherland, 2003). In 2005 aew agri-environment scheme (Environmental Stewardship) was

aunched in England (Natural England, 2010). The key componentf this is the Entry Level Scheme (ELS) which is voluntary and aims

∗ Corresponding author. Tel.: +44 1491 692356; fax: +44 1491 692424.E-mail address: rfp@ceh.ac.uk (R.F. Pywell).

167-8809/$ – see front matter © 2010 Elsevier B.V. All rights reserved.oi:10.1016/j.agee.2010.11.012

© 2010 Elsevier B.V. All rights reserved.

to deliver simple and effective environmental benefits over largeareas. The ELS currently covers 5 million ha (55% of the utilisablefarmland with a target of 70% by 2011) and has an annual budgetof D193 million (Natural England, 2010). The scheme has a broadrange of objectives including conservation of biodiversity, protec-tion of resources, climate change adaptation and mitigation, andincreasingly, the delivery of ecosystem services. To receive sup-port payments participating farms are encouraged to both managecropped land more extensively, and remove marginal areas fromproduction for the creation of wildlife habitat.

Previous studies have focused primarily on the benefits of habi-tat restoration as part of the agri-environment schemes for theconservation and enhancement of biodiversity (e.g. Pywell et al.,2004, 2006; Carvell et al., 2006; Marshall and Moonen, 2002). How-ever, considerably less is known about the effectiveness of theserestoration prescriptions in promoting key ecosystem functionsand services, and enhancing the stability of agro-ecosystems. Apragmatic approach to this problem would be to classify speciesassemblages in terms of their functional traits which more closely

reflect their potential role in determining and regulating ecosys-tem processes, and through this the provision of agro-ecosystemservices (Balvanera et al., 2006; Moonen and Bàrberi, 2008). Thispaper describes a multi-trophic study examining the effects of arange of habitat restoration strategies (differing in both cost and

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omplexity) on plant and invertebrate functional traits. It contrastshe observed effects to those recorded in an intensively managedrop treatment. It specifically focuses on the agro-ecosystem ser-ices for production provided by functional groups, namely foodeb services and gene flow services (pollination) (after Moonen

nd Bàrberi, 2008).Using this approach the following hypotheses were addressed:

H1: removing areas from agricultural production causes largeshifts in the functional composition of plant and invertebrate com-munities that have the potential to benefit food web and gene flow(pollination) services;H2: creating two contrasting habitat types on the same fieldmargin enhances the potential for multi-functionality by havingcomplementary beneficial effects on traits associated with agro-ecosystem services for production.

. Materials and methods

The experiment was carried out at Manor Farm, Eddlethorpe,ear Malton, UK (000◦49′W 54◦05′N). This is an intensively man-ged arable enterprise of 164 ha growing cereals, oilseed rape andeans on clay and loam soil. In September 1999, five field marginanagement treatments were applied at random to contiguous

lots within one of three replicate blocks. Each field margin plotas 6 m × 72 m. The treatments were:

1) Intensively managed crop with conventional inputs of pesticideand fertiliser (control; see Supplementary Table 1 for details ofmanagement);

2) Natural regeneration following a final autumn cultivation (nat-ural regeneration);

3) Tall grass seed mixture comprising five grass species sown at20 kg ha−1 (tall grass);

4) 3 m tall grass margin adjacent to hedge and 3 m wildflowermargin (see 5 below) adjacent to crop (split margin);

5) Wildflower mixture comprising eight grass and 17 forb speciessown at 37 kg ha−1 (wildflower).

The treatments were replicated on the margins of three separateelds (blocks) with the crop treatment assigned randomly to eithernd of each replicate to enable farming operations. Details of theeed mixtures are given in Supplementary Table 2. In year 1 andthe crop treatment and the rest of the field was winter wheat

Triticum aestivum L.) for all replicates. In year 2, two replicatesere winter oilseed rape (Brassica napus L. ssp. oleifera), and the

ther winter wheat. The wildflower vegetation was managed byutting and removal of the biomass in May and August of year 1,nd in late August of each subsequent year according to the schemeuidelines (Natural England, 2010). The other non-crop treatmentsere left unmanaged as per guidelines.

.1. Monitoring

Vegetation composition was recorded in July each year2000–2002) from six randomly located 1 m × 1 m quadrats locatedithin each treatment plot. The percentage cover of all vascu-

ar plants, bare ground, litter and bryophytes was estimated as aertical projection. Litter and bryophyte cover were a very smallomponent of the vegetation and so was not reported further.

Transects were walked through the centre of each plot (72 m)o record the abundance and species richness of butterfly andumblebee (Bombus spp.) species using a modified version of theutterfly Monitoring Scheme (BMS) methodology (temperaturebove 13 ◦C with at least 60% clear sky, or 17 ◦C in any sky con-

and Environment 140 (2011) 62–67 63

ditions) (Pywell et al., 2006). Butterfly transects were walked on15 occasions between May and August in 2000, on 14 occasionsin 2001 and 13 times in 2002. Bumblebees were recorded on 12occasions in 2000, on 10 occasions in 2001 and 11 times in 2002. Pit-fall traps were used to sample surface active epigeal invertebrates.Pitfall traps (diameter 8 cm, depth 11 cm) were placed in lines ofeight along the centreline of each plot, 5 m apart. Each trap washalf filled with a 50% solution of propylene glycol (antifreeze) andwater, combined with a small volume of detergent to reduce sur-face tension. Propylene glycol was used as a preservative (insteadof the more commonly used ethylene glycol) as it is less poi-sonous to badgers (Meles meles) and foxes (Vulpes vulpes) which areattracted to the traps. The traps were open for a four week periodfrom late April to late May in each year from 2000 to 2002. Thecontents of the traps were emptied after a two week period andthen again at the end of the trapping period. The entire contentsof all pitfall traps was retained for subsequent identification andsummed within an individual year for a particular treatment. Alladult individuals collected within the pitfall traps were identifiedto the level of species. This included spiders (Araneae), harvest-men (Opiliones), beetles (Coleoptera), true bugs (Heteroptera), ants(Formicidae), centipedes (Chilopoda), millipedes (Diplopoda) andwoodlice (Isopoda). To sample the complementary fauna of canopydwelling arthropods, sweep netting on a single occasion in earlyJuly of each year was undertaken. A standard sweep net of 0.5 mdiameter with a 0.7 m handle was used. One sample unit comprisedall material collected from a single plot by sweeping vigorouslyfrom side to side through the canopy while walking a standard-ised, figure-of-eight transect (length 90 m), keeping the speed andspatial extent of sweeping as constant as possible. All sweeping wascarried out by the same person during warm, dry weather (>15◦ C)between the hours of 10.00 and 16.00. Species identification wastaken to the same resolution as described for pitfall traps.

Finally, overwintering invertebrates were sampled in each habi-tat with the exception of the split tall grass and wildflowermargin. Twelve randomly positioned soil cores, each measuring16 cm × 16 cm and 12 cm deep, were collected at equal intervalsalong the centre line of each plot in January 2002. Each samplewas placed in a sealed and labelled polythene bag, and stored in acold room at 4◦ C. Batches of samples were removed to a room atbetween 18 and 22◦ C for 24 h prior to sorting. This was to encour-age invertebrate activity and therefore increase the probabilityof catching individuals by hand sorting. Each sample was brokenup by hand and thoroughly searched for invertebrates for a fixedperiod of 10 min (Pywell et al., 2005). Adults and larvae of the orderColeoptera (with the exception of the Staphylinidae from the sub-family Aleocharinae) were identified to species level. Finally, larvaeof the orders Diptera and Thysanoptera, and adult Hymenopterawere counted, but not identified to species.

2.2. Classification into guilds and functional groups

Following Blondel (2003) sown and unsown plant specieswere classified into the following ecological guilds to describehow they share resources and for explaining the structure of thecommunities: grasses (27 species), forbs (77), legumes (6) andhemi-parasites (1). The single hemi-parasitic plant species (Rhinan-thus minor) was included as it is well known to have an importantrole in the regulation and maintenance of plant diversity throughthe reduction of competitive species (Bullock and Pywell, 2005).It also attained a high (>30%) cover in some plots. In addition, we

applied a further economic and cultural classification based on thepotential to reduce the yield of crops and the undesirability ofspecies (weeds: 9 species). This group included serious weeds ofagriculture (e.g. Alopecurus myosuroides) and species that must becontrolled by law under the UK Injurious Weeds Act of 1959 (e.g.

64 R.F. Pywell et al. / Agriculture, Ecosystems and Environment 140 (2011) 62–67

Table 1ANOVA F values for the response of plant cover abundance, species richness and functional trait scores to field margin management prescription.

Year (F2,19) Treatment (F4,8) Year × treatment (F8,19)

CoverGrasses 3.98* 11.31** NSLegumes 4.47* 9.11** NSHemi-parasites 5.21* 8.87** NSOther forbs NS 5.49* 3.46*

Weeds/undesirable species 7.99** 9.63** NSSpecies richness

Grasses 29.88*** 29.44*** 3.43*

Legumes NS 15.88*** 2.55*

Hemi-parasites NS 16.71*** NSOther forbs 30.39*** 14.72*** 7.31***

Weeds/undesirable species 21.26*** 19.84*** NSFunctional traits

Ruderal 9.47** 14.51*** 7.91***

Competitor NS 5.02* 10.08***

Stress-tolerator 46.89*** 76.47*** NSSeed size (axis length mm) NS 5.11* NSSeed weight (g per shoot) 12.17*** 30.37*** 6.65***

Seed energy per shoot (kJ per shoot) 15.84*** 79.37*** NS

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irsium arvense and Senecio jacobaea), the latter being poisonouso livestock. Plants were also classified into functional groupsccording to their life history strategies based on the CSR modelcompetitor, stress-tolerator, ruderal) (Grime, 1979). In addition,unctional traits describing the food web service of seed productionnd energy value were obtained from the LEDA database (Knevelt al., 2005).

All adult individuals collected within the pitfall traps and sweepet samples were classified into functional groups responsible for

ood web and gene flow (pollination) services, namely herbivorous170 species) (BRC, 2009) or predominantly predatory (73 species)e.g. Hoffmann, 1950–1958; Southwood and Leston, 1959; Roberts,985–1993; Douget, 1994; Bohac, 1999; Ribera et al., 1999), andollinators (23 species). While pollinators are not a trophic leveler se, they are functionally distinct from other herbivore arthro-ods that are characterized by feeding directly on plant structures,.g. foliage eaten by leaf beetles (Douget, 1994), and as such theyill be considered within this paper as a fourth ‘pseudo’ trophic

evel. Finally, species were also classified as detritivores (16 species)Snyder and Hendrix, 2008), partly responsible for the key regulat-ng service of nutrient cycling. Full details of the composition ofach functional group are given in Supplementary Table 3.

.3. Statistical analysis

Mean arc sine transformed cover values were calculated for eachlant guild and functional grouping. In addition, cover-weightedalues for seed production and life-history strategy were calcu-ated for each plot. As pitfall traps and sweep nets sample differentpatial components of the same community the abundances ofndividual species collected by these two sampling methods weremalgamated. Based on summed values for individual plots in aarticular year the abundance (loge N + 1) and summed species rich-ess were calculated separately for the detritivores, herbivores,redatory and pollinator groupings. The response of each of thesearameters to the explanatory variables of treatment, year, and the

nteraction treatment × year were tested using analysis of varianceANOVA) models with repeated measures in Genstat 9.0. Values offor adjustment of degrees of freedom according to the amount byhich the population covariance matrix departs from homogene-

ty were calculated using the Geisser–Greenhouse method. Post

hoc Tukey’s pairwise comparisons were used, where necessary, todetermine differences among individual treatments.

3. Results

3.1. Vegetation

There were large and consistent significant differences in the cover and richnessof plant guilds and functional groups between treatments (Table 1). These trendsgenerally strengthened with time. Overall species number (richness) was signifi-cantly higher in the wildflower and split treatments than the tall grass and crop.This trend was strongest for forbs. In the intensively managed crop total speciesnumber increased from 5.0 ± 2.9 m−2 in year 1 to 6.3 ± 2.1 m−2 in year 2 reflectingthe broad-leaved break crop, and declining in year 3 to 3.8 ± 1.1 m−2. In contrast,there were sharp declines in species number after year 1 in all non-crop treatments.Cover of grasses was significantly higher in the tall grass and natural regenerationtreatments than wildflower and the crop. Cover of grasses increased significantlywith time in all treatments. Cover of forbs was significantly higher in the wildflowertreatment than the natural regeneration and the tall grass margins. The significantyear × treatment interaction reflected the sharp decline in forb cover in the tall grassmargin after year 1.

Cover of legumes (particularly Lotus corniculatus, Lathyrus pratensis) was sig-nificantly higher in margins sown with wildflowers than all others and this trendincreased with time. Legume species richness increased with time in the split mar-gin and was more stable in the wildflower treatment. Similarly, cover of regulatinghemi-parasitic plants (R. minor) was significantly higher in the wildflower treat-ment than all others except the split treatment, and increased rapidly after year 1(reaching up to 30% in some plots). Finally, cover of undesirable and injurious weedspecies was significantly higher in the natural regeneration treatment than all oth-ers. Species richness of weeds was significantly higher in the natural regenerationtreatment than all others. However, cover and number of weed species declined inall treatments with time.

The cover weighted scores for plant ruderality, competitiveness and stress-tolerance all showed significant responses to the main treatments. The abundanceweighted ruderal score was significantly higher in the crop than all other treatmentsexcept natural regeneration (Table 1). Ruderality fell over time in all treatmentswith the exception of the crop. Species with a competitive life history were moreabundant in the natural regeneration treatment than the crop. Finally, stress-tolerators were more abundant in the treatments sown with the wildflower seedmix than either the crop or natural regeneration. The stress-tolerator score increasedwith time across all treatments. Trait-estimated mean seed size (axis length mm)responded significantly to the effects of margin treatment, with higher valuesrecorded where natural regeneration had been used to establish the margins, asopposed to the sowing wildflowers (Table 1). This reflected the abundance of vol-

unteer cereals in this treatment in year 1, followed by the colonisation of relativelylarge-seeded grasses, such as Elytrigia repens and Anisantha sterilis. Mean seedweight (g per shoot) was significantly higher in the crop than all other treatments(Fig. 1). Seed weight fell by over 50% in the crop when a break crop of oilseed rapewas grown in year 2. Estimated energy (KJ per shoot) of the seed produced was sig-nificantly higher in the crop than all other treatments. Seed energy in the natural

R.F. Pywell et al. / Agriculture, Ecosystems and Environment 140 (2011) 62–67 65

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egeneration treatment was higher than that of the sown field margin vegetation.eed energy produced declined in most treatments between year 1 and 2.

.2. Invertebrates

A total of 6481 detritivores, 24,463 herbivores, 29,518 predators and 3655 pol-inators were collected during the study. There were strong and consistent effectsf field margin management prescription on the key invertebrate functional groupsssociated with food web and gene flow services (Table 2; Fig. 2). Many of theseffects strengthened with time. However, there were no significant treatment × yearnteractions. Abundance and species richness of detritivore arthropods did notespond significantly to either treatment. However, there were significant increasesn abundance and richness across all treatments over the three years as vegeta-ion communities matured. Herbivore abundance was significantly higher in theildflower and split margins than the crop, and abundance of this group increased

ignificantly with time. Herbivore species richness was also significantly higher inhe wildflower margin than the crop and tall grass margin. Similarly, abundancef predatory arthropods was significantly higher in the wildflower and split treat-ents than the crop and tall grass. Abundance of predators increased significantly

o a peak in year 2 and then declined. Richness of predators was highest in the wild-ower treatment, but this was not significant (ANOVA F4,8 = 1.79, P > 0.05). Pollinatorbundance and species richness were both significantly higher in the wildflower andplit treatments than the crop and tall grass margin. In addition, species richnessas significantly higher in the naturally regenerated margin than the crop. Both

bundance and richness of pollinating insects showed significant trends with time,ncreasing to a peak in year 2.

The limited study of overwintering invertebrates showed a greater species rich-ess of detritivores in the non-crop treatments compared to the crop (Table 3). Thereere no significant effects of treatment on any measure of overwintering herbivore

bundance or richness. In contrast, there were a large number of significant effectsf overwinter habitat on predatory arthropods. Abundance of predators was sig-

ificantly higher in the wildflower and natural regeneration treatments than therop. Finally, species richness of predators was significantly higher in all non-cropreatments than the crop.

able 2NOVA F values for the response of abundance and species richness of invertebrate

unctional groups to field margin management prescription.

Year (F2,19) Treatment (F4,8) Year × treatment (F8,19)

Abundance (loge N + 1)Detritivores 26.15*** NS NSHerbivores 12.32*** 9.74** NSPredators 3.82* 8.12** NSPollinators 4.51* 32.23*** NS

Species richnessDetritivores 17.16*** NS NSHerbivores NS 7.23** NSPredators NS NS NSPollinators 12.10** 33.29*** NS

S: not significant (p > 0.05).* p < 0.05.

** p < 0.01.*** p < 0.001.

Fig. 2. Treatment effects on mean (±SE) arthropod (a) abundance and (b) speciesrichness averaged across years (2000–2002).

4. Discussion

non-crop habitats emphasised the highly detrimental effects ofmodern, intensive agriculture on the abundance and diversityof many plant and invertebrate functional groups, particularly

Table 3ANOVA F values for the response of abundance and species richness of overwinter-ing invertebrate functional groups to field margin management prescription (thesewere sampled only in 2002 therefore year was not included in the model).

Treatment (F3,5)

Abundance (loge N + 1)Detritivores NSHerbivores NSPredatory 9.38*

Species richnessDetritivores 35.17***

Herbivores NSPredatory 16.11**

Total 32.41***

NS: not significant (p > 0.05).* p < 0.05.

** p < 0.01.*** p < 0.001.

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ollinators and predatory arthropods (Carvell et al., 2007). Theifferences between crop and non-crop habitat appeared to beagnified in the winter, emphasising the importance of refuge

abitat for many farmland invertebrates. Many of the most effectiveredators are known to overwinter in field boundaries and disperse

nto the crop in the spring (Wratten, 1988). Maximising overwin-er survival is therefore an important constraint on effective pestontrol services. However, it is important to note that intensiverop management resulted in highly effective control of undesir-ble weed species, and produced the greatest abundance of foodor auxiliary biota, such as farmland birds, in terms of seed yieldnd total seed calorific value. Indeed, the English agri-environmentchemes fund farmers to leave strips of unharvested cereal as anverwinter food resource for birds (Henderson et al., 2004).

The conversion of arable field margins to non-crop habitatesulted in rapid and marked beneficial shifts in the abundancef many functional groups likely to enhance the provision ofood web and gene flow ecosystem services (e.g. Collins et al.,001; Ricketts et al., 2008). The concurrent increase in diversityf ‘insurance species’ within these functional groups is also likelyo increase the stability and resilience of these services to extremelimatic events and other environmental stresses (Balvanera et al.,006). The removal of small parcels of land from production toreate a heterogeneous mix of habitats at the landscape scale isonsidered important to the ‘wildlife-friendly farming’ strategy foruccessfully integrating agriculture and biodiversity conservationFischer et al., 2008), and for the provision of ecosystem servicesBrosi et al., 2008).

.1. Magnitude of changes in relation to the choice of perennialsown

The rate and magnitude of responses of plant and invertebrateuilds and functional groups varied considerably between treat-ents. Allowing perennial vegetation to colonise ex-arable land

rom the seed bank and hedge base is one of the most popu-ar management prescriptions under the English agri-environmentchemes (Stevenson, 2007). This highly dynamic plant communityas initially dominated by competitive-ruderal crop weeds (e.g. A.

terilis), and reflected the severe seed limitation of natural coloni-ation on fertile ex-arable soils (Pywell et al., 2002). However, afterhree years the resultant community was structurally complex, butominated by a small number of perennial grasses (e.g. Poa trivialis)nd tall, undesirable forbs (e.g. C. arvense) (Critchley et al., 2006).his unmanaged habitat was second only to the crop in terms ofhe provision of seed resources for higher trophic levels, notablyeed-feeding invertebrates, small mammals and birds (Marshallnd Moonen, 2002). This restoration prescription also resulted inoderate beneficial effects on invertebrate functional groups after

hree years, particularly the abundance of pollinators and herbi-ores as a potential food source for higher trophic levels. This is alsoikely to reflect colonisation by Cirsium spp. (Pywell et al., 2006).

The alternative strategy of sowing simple, low-cost tall grasseseed mixes is also a popular prescription in the agri-environmentchemes, costing as little as D91 ha−1 which equates to a stripm wide and 1600 m long. Rapid establishment of tall, competi-

ive grasses was effective in excluding undesirable weed speciesCritchley et al., 2006). This species poor-vegetation resulted inelatively small functional shifts in the invertebrate community.owever, the dense, sheltered vegetation provided an effectivehysical barrier against pesticide and fertiliser drift into any adja-

ent water courses or wildlife habitats (Miller and Lane, 1999). Itlso provides habitat for small mammals (Shore et al., 2005), andesting bumblebees (Lye et al., 2009).

Sowing a complex mixture of perennial wildflower speciesncreased significantly the cost of ecological restoration

nd Environment 140 (2011) 62–67

(D1186 ha−1) and there were additional management require-ments of annual cutting to maintain this diverse vegetation onfertile soils. However, subsequent research has shown that costscan be reduced significantly to as little as D266 ha−1 by decreasingthe ratio of forbs to grasses (Pywell et al., 2010). Creation of diversevegetation using this approach resulted in the largest positiveshifts in the functional composition and diversity of both theplant and invertebrate communities. Functionally important plantgroups, such as legumes and hemi-parasites, are only likely toestablish on land taken out of intensive farming where they areintroduced as seed (Pywell et al., 2002).

Associated with the restoration of diverse field margin vege-tation were potentially beneficial increases in the abundance anddiversity of herbivorous insects (Woodcock et al., 2008). Theseprovide both and important food source for auxiliary biota (e.g.farmland birds; Wilson et al., 1999), and play a potentially impor-tant role in regulation of the vegetation community (Scherber et al.,2006). Similarly, there were significant increases in diversity andabundance of pollinators reflecting the establishment of key for-age plants in the wildflower habitat (Carvell et al., 2006). Thereis evidence that conserving and enhancing native pollinator com-munities in this way may have beneficial spill over effects on thepollination of adjacent crops and wildflowers (Ricketts et al., 2008).Finally, the greater abundance of arthropod predators in this habitatmay also serve an important regulatory function for the ecosystem,and may have beneficial spill over effects for the control of pests inthe adjacent crop (e.g. Collins et al., 2001).

4.2. Creation of contrasting habitats and enhancement ofbeneficial effects

The creation of two complementary habitat types on the samefield margin (tall grass adjacent wildflower) did not result in mea-sured synergistic effects on functional composition of plant andinvertebrate communities. This probably reflected the overwhelm-ing, large beneficial effects of creating wildflower habitat comparedwith tall grass on plants and invertebrates. Nevertheless, the pro-vision of shelter and nesting sites by the tall grass vegetation, notconsidered by this study, is likely to be complementary to the wild-flower habitat (Luff, 1966). This space-efficient approach to wildlifehabitat creation may become more important given predicted pres-sure to increase food production from finite resources of productiveland (Godfray et al., 2010).

To conclude, it is widely acknowledged that there are posi-tive relationships between biodiversity, ecosystem function andthe provision of ecosystem services (Balvanera et al., 2006), andthat for degraded systems these relationships can be significantlyenhanced by ecological restoration (Rey Benayas et al., 2009). Herewe have assessed responses of both plant and invertebrate commu-nity composition in terms of functional groups and their associatedtraits in order to investigate the potential contribution of habitatcreation in providing ecosystem services in agro-ecosystems. How-ever, it is important to understand that these services are deliveredat a range of spatial and temporal scales (Hooper et al., 2005) bya variety of component habitats, and species assemblages depen-dent upon them. Moreover, the inferred measures of ecosystemfunction reported in this paper cannot replace direct measures ofthe services themselves where they are possible and practical. Nev-ertheless, we believe that this paper does provide valuable insightsinto the potential contribution ecological restoration of appropri-ate habitats could make to the delivery and stability of ecosystem

services within intensively managed agro-ecosystems.

This study demonstrated that it is possible to achieve large pos-itive shifts in abundance and diversity of key function groups ofplants and invertebrates on small areas of productive land usingappropriate ecological restoration. However, no single crop or non-

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rop habitat is likely to provide all the ecosystem services required.deally policy should seek to create a wide range of complementaryabitat types to maximise habitat heterogeneity at the field scalend deliver the greatest number of positive shifts in function oflant and invertebrate communities. The creation of diverse vege-ation communities by sowing seed mixtures resulted in the largestositive shifts in function, though this was the most costly andemanding approach. Further research is required to guide agri-nvironmental policy as to the optimal type, proportion and spatialrrangement of non-crop habitats required at the farm and land-cape scale to ensure future agro-ecosystems deliver the requiredncreases in food production, but at the same time are biologicallyustainable and resilient to environmental change.

cknowledgements

The authors would like to thank Richard Brown for hosting thexperiment and Matt Heard for compiling data on seed yield. Were grateful to the anonymous referees for constructive commentsn an earlier draft of the manuscript.

ppendix A. Supplementary data

Supplementary data associated with this article can be found, inhe online version, at doi:10.1016/j.agee.2010.11.012.

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