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Ground beetles (Coleoptera, Carabidae) in an intensively managed vegetable crop landscape in eastern England
Agriculture, Ecosystems and Environment 131 (2009) 340–346
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Ground beetles (Coleoptera, Carabidae) in an intensively managed vegetable crop landscape in eastern England M.D. Eyre a,*, D. Labanowska-Bury b, J.G. Avayanos a, R. White c, C. Leifert a a
Nafferton Ecological Farming Group, University of Newcastle upon Tyne, Nafferton Farm, Stocksfield, Northumberland, NE43 7XD, UK Department of Applied Entomology, Warsaw University of Life Sciences- SGGW, Ul. Nowoursynowska 159, 02-787 Warsaw, Poland c Westhorpe Flower & Plants Ltd, Westhorpe House, West End, Benington, Boston, Lincolnshire, PE22 0EL, UK b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 16 December 2008 Received in revised form 4 February 2009 Accepted 24 February 2009
Four fields (three organic and one conventionally managed) in an intensive vegetable producing landscape in eastern England were sampled for ground beetles in 2005 and 2006, using pitfall traps, to investigate species activity and species assemblage distribution within five crop and three field margin types. In addition, non-crop ditch sites were also sampled. Three species assemblages in the fields were strongly related to crop type, with two others consisting of non-crop sites, one dominated by field margins, the other by ditch sites. Species activity and richness in fields were also strongly, and significantly, associated with crop type, with most in organic Brassica crops (cauliflower, cabbage, broccoli), less in organic leeks and least in conventional calabrese. Some species were significantly more active in weedier fields but others preferred more open ground. Considerably more species were recorded from first-year planted field margins, with fewest species active in unplanted margins. Activity was also relatively low in densely vegetated second-year margins. There appeared to be little relationship between species activity in the margins and that in the crop fields. Ground beetle species are important for the predation of cabbage root fly eggs in Brassica crops, especially in organic fields. In order to enhance and maximise appropriate ground beetle species activity and predation within vegetable fields, it is likely that management within both fields and margins would be required, as well as some method for increasing movement of predators from margins into fields. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Ground beetles Beneficial invertebrates Organic farming Brassicas Leeks Field margins
1. Introduction Increasing the activity of generalist invertebrate predators, important pest control agents in arable crops (Symondson et al., 2002), especially ground beetles (Carabidae) (Holland et al., 2005), has been attempted by providing areas such as beetle banks and planted field margins (Landis et al., 2000). This has become more important with the increase in organic food consumption and production, generally a result of concerns about food quality (Leifert et al., 2007), and there is a need to change management practices in organic systems to increase natural enemy effectiveness (Gurr et al., 2003). Planted field margins have usually been sown with a mixture of wildflower seeds (Marshall and Moonen, 2002), which have proven to be much more effective than unsown margins (Meek et al., 2002). In addition to increasing beneficial invertebrate activity by providing appropriate field margins, a number of measures within
* Corresponding author. Tel.: +44 1661 830222; fax: +44 1661 831006. E-mail addresses: [email protected], [email protected] (M.D. Eyre). 0167-8809/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2009.02.006
the crop have also been employed. Weed strips in cereals (Lys et al., 1994) and intercropping with clover in cabbage (Booij et al., 1997) have both been used to increase the activity of ground beetles. Weed cover in fields has also been shown to increase the activity of some ground beetle species in organic potato (O’Sullivan and Gormally, 2002) and cabbage (Armstrong and McKinlay, 1997). The cessation of chemical spray application in organic systems means greater reliance on natural enemies, and in the case of Brassica crops, controlling the major pest, cabbage root fly (Delia radicum L.) (Langer, 1996). Ground beetle species have long been known to be predators of cabbage root fly eggs and there have been laboratory assessments of consumption efficacy (Finch and Elliott, 1992; Finch, 1996). Medium-sized ground beetle species were found to eat more than small species, whilst large species ate few eggs. However, although Prasad and Snyder (2004, 2006) confirmed predation of eggs by small ground beetle species in the field, they also observed small ground beetles being predated by large ground beetle species, which did not eat eggs. In order to provide baseline information on the activity and distribution of ground beetle species and assemblages in an intensively managed landscape used primarily for vegetable
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production, a survey of four (three organic, one conventional) fields was carried out in 2005 and 2006. Activity of ground beetle species in leeks and four different Brassica crops was assessed using pitfall traps. In 2005 two organic fields of cauliflower were sampled and these fields were re-sampled again in 2006, when they were used to grow leeks. In addition, in 2006 an organic field with cabbage and broccoli and a conventional field of calabrese were also surveyed. Field margins and ditch sites were also sampled to cover the major habitat types present. The relationship of both species and assemblage distribution in these non-crop habitats to those in the crop fields was investigated, as they are likely to be the source of a number of pest control species. Management of both crops and field margins, in the context of increasing pest control, is discussed. 2. Methods 2.1. Study area The survey was carried out in three organic fields and one conventionally managed field near Benington, Boston, Lincolnshire in eastern England (national grid reference TF4637). The organic fields were converted to certified organic status in 2004 after being sown with grass and clover for two years. Two organic fields (both 320 m long, 90 m wide) were planted with cauliflower (var Delfino) in the first week of May 2005 and the same fields were planted with leeks (var Shelton) in the middle of May 2006. In the other organic field (300 m long 110 m wide), one-third was planted with cabbage (var Sunta) and two-thirds with broccoli (var Bordeaux) in the middle of May 2006, whilst in the last week of April 2006 calabrese (var Iron) was planted in the conventional field (280 m long, 90 m wide). These fields were in a flat landscape used for intensive vegetable production, with few trees and hedges and fields split by roads or drainage ditches. The conventional field was treated with inorganic fertiliser (N22, P4, K14) at 500 kg ha 1 and a number of pesticide sprays (trifluralin 1 l ha 1; metazachlor 1.5 l ha 1; aphox 420 g ha 1; hallmark 100 ml ha 1; silwet 220 ml ha 1). No fertiliser was applied to the organic fields whilst weeding was mechanical with a spring-tined weeder. To satisfy organic regulations, 4 m wide field margins were established on two sides of the organic fields in September 2004. They were planted with a wild flower mixture containing Achillea millefolium L. (yarrow), Lotus corniculatus L. (birdsfoot trefoil), Silene dioica (L.) (red campion), Papaver rhoeas L. (poppy), Anthriscus sylvestris Hoffm. (cow parsley), Knautia arvensis (L.) (field scabious), Matricaria recutita L. (scented mayweed), Daucus carota L. (wild carrot), Onobrychis viciifolia Scop. (sainfoin) and Galium verum L. (lady’s bedstraw). Redidual Trifolium repens L. (white clover) and Lolium perenne L. (ryegrass) were also present. Development during the 2005 crop season involved these margins (first-year margins) becoming more densely vegetated, with less bare ground with time. By the 2006 crop season (second-year margins), there was dense vegetation cover and no bare ground. The 4 m edge of the conventional field was unplanted, and bare, at the time the calabrese crop was planted but developed vegetation with time. There were drainage ditches, with unmanaged vegetation, next to one edge of the cauliflower and leek fields, on both long edges of the cabbage and broccoli field and next to the field margin of the calabrese field. Historical records held by the UK Meterological Office (www.metoffice.gov.uk) show that there were differences in weather parameters in 2005 and 2006. The mean monthly temperatures for stations in eastern England were 11.6, 16.0, 17.1 and 16.9 8C for May, June, July and August 2005 respectively, with means of 12.5, 16.8, 20.7 and 16.7 8C for the same months in 2006. Monthly precipitation was 38, 54, 47 and 74 mm in May, June, July and August 2005 and 74, 16, 43 and 84 mm for the same months in 2006.
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2.2. Sampling Sampling for ground beetles was carried out using pitfall traps (8.5 cm diameter 10 cm deep) part-filled with saturated salt (NaCl) solution with a little strong detergent as preservative. There were 24 sampling points in each field, with five pitfall traps (0.5 m apart in a star shape), in a grid in the central part of the fields. Eight lines of three sample points, 20 m apart, were employed across the fields at 15, 30 and 45 m intervals away from one field margin in the cauliflower, leek and calabrese fields. Four lines of six sampling points, also at 15, 30 and 45 m from both long field margins, were used in the broccoli (16 sampling points) and cabbage (8 sampling points) field. The traps were set out in the fields just after transplanting of crop plants. In the six planted field margins of the three organic fields, five pitfall traps were set at four 30 m intervals, opposite the area sampled in the crop. In the conventional calabrese field only one margin was sampled, with 8 sampling points opposite the 3 lines of traps in the crop. In addition, the tops of ditches adjacent to the fields were also sampled, in the same pattern as the field margin sites. The two ditches bordering the cauliflower and leek fields (8 sampling points) were sampled in 2005 and 2006, with ditches by the cabbage and broccoli and the calabrese fields (both 8 sampling points) also sampled in 2006. Four samples were taken, at four-week intervals throughout crop development, with the last sample taken in August. All ground beetles were taken from the pitfall traps at each sampling point and counted. Nomenclature follows Luff (2007). At each sampling time an assessment of weed cover in the crops was made. Coverage of weeds was estimated to the nearest 10% and the four estimates were meaned to provide a value for analyses. A similar estimate was made for vegetation cover around the field margin sites at sampling times. 2.3. Data analysis The total number of each ground beetle species recorded throughout the total sampling period were used in analyses concentrating on investigating the effect of crop type on activity and differences in activity between the planted margins (first- and second-year), the unplanted margins and the ditch sites. Linear mixed-effects models (Pinheiro and Bates, 2000) were used to assess activity differences, using the number recorded transformed by log10 n + 1 (Crawley, 2007) as a measure of activity. Analysis of variance was generated using models with crop and margin type and ditches as fixed factors and management (organic or conventional) as the random factor. The effects of weed cover in the fields and vegetation cover in the margins were assessed using Spearman’s rank correlations. In addition, analyses were carried out using ground beetle species richness as a variable. The mixedeffects models and correlations were carried out in the R statistical environment (R Development Core Team, 2007). Multivariate techniques were also applied to the data. The ground beetle species assemblage data, from all sites, was first classified using fuzzy set clustering (Bezdek, 1981), based on a DECORANA ordination (Hill, 1979), as in Eyre et al. (2006). The site scores on the first two axes of the ordination were used for the classification. Constrained ordination, using canonical correspondence analysis (CANOCO) was used to investigate the relationship between the ground beetle assemblages and the crop and margin types (CANOCO Version 4— Ter Braak and Sˇmilauer, 1998). Automatic forward selection of nine agronomic variables within CANOCO was employed and significance calculated using Monte Carlo permutation tests. 3. Results The effect of crop type on the activity of ground beetle species, and on species richness, is shown in Table 1, with means of the
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Table 1 The mean number (one or more) of each ground beetle species and of species richness, standard error, recorded from sites in each crop type, together with the F-ratios, probabilities and significances (n.s. not significant; *P < 0.05; **P < 0.01; ***P < 0.001) generated by the linear mixed-effects models (degrees of freedom 4, 138) comparing activity in each crop. Species
F-ratio
Probability
Significance
Cauliflower
Leek
Broccoli
Cabbage
Calabrese
Acupalpus meridianus Amara apricaria Amara familiaris Amara similata Anchomenus dorsalis Bembidion aeneum Bembidion guttula Bembidion lampros Bembidion obtusum Bembidion quadrimaculatum Bembidion tetracolum Clivina fossor Harpalus affinis Harpalus rufipes Loricera pilicornis Nebria brevicollis Notiophilus biguttatus Pterostichus melanarius Pterostichus niger Pterostichus strenuus Trechus quadristriatus Species richness
2.5 57.4 16.6 22.4 36.4 16.4 6.1 48.8 28.0 2.1 91.5 27.5 6.9 27.3 5.5 90.1 8.5 89.0 13.5 4.9 83.3 9.3
0.042 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.78 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.001 <0.001 <0.001
* *** *** *** *** *** *** *** *** n.s. *** *** *** *** *** *** *** *** *** ** *** ***
1 0.1 6 0.6 1 0.2 2 0.4 13 1.2 1 0.3 – 67 4.3 2 0.3 3 0.4 13 1.1 – – 12 1.1 2 0.4 – 2 0.2 54 4.6 1 0.2 – 3 0.4 14 0.3
– 1 0.2 – – 3 0.6 5 0.5 1 0.2 23 1.4 1 0.2 3 0.4 43 2.3 – 1 0.1 19 1.1 1 0.2 – 1 0.1 67 3.6 3 0.3 – 5 0.7 12 0.3
– – 4 0.7 3 0.6 4 0.7 5 0.7 1 0.5 62 6.5 9 1.1 2 0.5 107 11.0 2 0.8 2 0.3 10 1.3 1 0.2 5 0.8 2 0.4 308 17.4 1 0.4 1 0.2 116 15.4 15 0.3
– – 1 0.4 – 3 0.4 3 0.8 – 39 5.3 5 0.9 2 0.3 92 8.5 4 0.7 2 0.5 6 1.0 – 7 1.6 1 0.4 282 12.2 2 0.4 – 56 16.2 14 1.0
– – – – 2 0.4 2 0.4 – 5 0.8 1 0.3 1 0.3 30 2.5 2 0.3 – 1 0.2 – 8 0.9 2 0.3 77 4.5 1 0.3 – 9 1.3 11 0.5
numbers recorded from sites in the five crops and the F-ratio, probabilities and significances derived from the linear mixedeffect models. Most species generated very highly significant models, with only Bembidion quadrimaculatum activity not significantly affected by crop type and with two species having low activity (Acupalpus meridianus, Pterostichus strenuus) producing less significant models. A number of species were most active in the cauliflower crop (Amara apricaria, Anchomenus dorsalis, Bembidion lampros), but there was generally less activity in the following leek crop. Harpalus rufipes was most active in leeks but the majority of abundant species were most active in the broccoli crop (Bembidion obtusum, Bembidion tetracolum, Pterostichus melanarius, Trechus quadristriatus) and these species also tended to be active in cabbage. In general, species activity was less in calabrese, with Nebria brevicollis the only species most active in this crop. Ground beetle species richness was also highly significantly influenced by crop type and there was greater activity, and more species, in cauliflower, broccoli and cabbage than in leek and calabrese. The mean number of each species recorded from the three field margin types and the ditches, and of species richness, is given in Table 2, together with F-ratios, probabilities and significances from the mixed-effect models. A number of species with low activity produced non-significant models but there were significant differences in activity with most species and with species richness. There was far more overall activity in the first-year field margins than in any other margin type or in the ditches, especially for the more abundant species (A. dorsalis, B. lampros, B. tetracolum, H. rufipes, Loricera pilicornis, P. melanarius). In general, there was more activity in the second-year margins than in the unplanted margins. Some species had most activity in the ditches (N. brevicollis, Ophonus rufibarbis, Pterostichus niger). Mean species richness was significantly greater in the first-year margins, similar in second-year and unplanted margins and lowest in ditches. Weed cover was greatest in the cauliflower crop, which was badly affected by cabbage root fly, less in cabbage and broccoli and least in leek and calabrese, a result of efficient mechanical weeding and spraying respectively. Table 3 shows the coefficients,
probabilities and significances derived from the rank correlation of the ground beetle species activity, and species richness, in the crop sites and the mean weed cover. Most species gave significant correlations but there were conflicting preferences. Three Bemdidion species (B. aeneum, B. guttula, B. tetracolum) were significantly negatively related to weed cover whilst three others (B. lampros, B. obtusum, B. quadrimaculatum) significantly preferred weeds in the crop. Other species with a significant liking for less weedy fields were Clivina fossor, N. brevicollis, P. melanarius, P. niger and T. quadristriatus. Two Amara species (A. apricaria, A. similata), A. meridianus, A. dorsalis, L. pilicornis and Notiophilus biguttatus were significantly associated with increasing weed cover. Two Harpalus species (H. affinis, H. rufipes), Amara familaris and P. strenuus were not significantly related to weed cover. Higher species richness was also significantly related to increasing weed cover. Table 3 also shows the coefficients, probabilities and significances derived from the rank correlation of the crop ground beetle species activity in the field margins, and of species richness, and mean vegetation cover. Most species were not significantly correlated with vegetation cover but where there were significant correlations, they were mostly negative with more species activity in less vegetated margins. These included three Bembidion species (B. lampros, B. obtusum, B. quadrimaculatum), Amara similata, N. brevicollis, N. biguttatus and T. quadristriatus with only two Pterostichus species (P. niger, P. strenuus) significantly more active in densely vegetated margins. The significant relationship between species richness and vegetation cover indicated that as margin vegetation developed, the fewer species were recorded. The classification of the species assemblage data, based on an ordination of all the data, produced five groups. The mean number of each species recorded from sites in the five groups is shown in Table 4. Group 1 was restricted to the 48 sites in the two cauliflower fields, with B. lampros and P. melanarius the two most active species. The 48 sites in the leek fields and 2 sites in the broccoli crop were in group 2. P. melanarius was again the most active species but there was more B. tetracolum and less B. lampros than in group 1. The remaining 22 sites in the broccoli and cabbage fields and 23 sites in the calabrese were in group 3. Sites in this
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Table 2 The mean number (one or more) of each ground beetle species and of species richness, standard error, recorded from sites in field margins and ditches, together with the Fratios, probabilities and significances (n.s. not significant; *P < 0.05; **P < 0.01; ***P < 0.001) generated by the linear mixed-effects models (degrees of freedom 3, 75) comparing activity in margins and ditches. Species
F-ratio
Probability
Significance
First-year
Second-year
Unplanted
Ditches
Acupalpus meridianus Amara aenea Amara apricaria Amara communis Amara familiaris Amara lunicollis Amara plebeja Amara similata Anchomenus dorsalis Asaphidion flavipes Badister bullatus Bembidion aeneum Bembidion lampros Bembidion lunulatum Bembidion obtusum Bembidion quadrimaculatum Bembidion tetracolum Calathus rotundicollis Clivina fossor Demetrias atricapillus Harpalus affinis Harpalus rufipes Leistus spinibarbis Loricera pilicornis Nebria brevicollis Notiophilus biguttatus Notiophilus substriatus Ophonus rufibarbis Poecilus cupreus Pterostichus madidus Pterostichus melanarius Pterostichus niger Pterostichus strenuus Stomis pumicatus Trechus quadristriatus Species richness
4.9 9.2 13.7 2.6 0.3 1.9 11.3 26.9 4.4 53.3 2.5 53.2 23.9 115.1 20.9 3.7 20.5 27.7 2.5 5.4 9.4 13.7 27.6 23.5 13.2 8.5 12.6 19.9 6.4 0.1 5.1 9.9 3.5 2.7 5.6 49.9
0.004 <0.001 <0.001 0.062 0.863 0.132 <0.001 <0.001 0.006 <0.001 0.066 <0.001 <0.001 <0.001 <0.001 0.016 <0.001 <0.001 0.064 0.002 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.983 0.003 <0.001 0.019 0.055 0.002 <0.001
** *** *** n.s. n.s. n.s. *** *** ** *** n.s. *** *** *** *** * *** *** n.s. ** *** *** *** *** *** *** *** *** *** n.s. ** *** * n.s. ** ***
1 0.3 2 0.5 4 1.2 1 0.4 1 0.3 – 7 1.2 17 2.9 96 8.1 17 4.1 – 12 2.2 38 6.6 4 0.7 2 0.6 1 0.4 37 4.1 – 1 0.2 1 0.3 3 0.8 62 6.5 – 42 4.8 8 1.9 4 0.6 2 0.4 7 2.7 1 0.4 – 215 19.0 5 1.0 1 0.4 1 0.3 5 1.9 24 0.6
– – – 2 0.5 1 0.3 1 0.7 4 1.4 1 0.4 47 4.0 – – 1 0.3 4 0.7 – – – 32 6.4 – 1 0.2 – 1 0.4 36 5.9 – 21 3.5 8 2.3 1 0.2 – 2 0.6 1 0.2 – 142 18.7 10 1.5 6 1.5 – 1 0.3 15 0.5
– – – – 1 0.4 – 1 0.3 7 3.1 31 9.5 – – – 5 0.8 – – – 17 1.8 – – – 1 0.3 15 2.5 – 2 0.7 10 1.4 2 0.7 – 1 0.3 – 15 2.2 126 27.2 5 0.9 – – 2 0.4 15 1.0
– – 1 0.3 1 0.3 1 0.2 – 1 0.2 3 1.0 66 11.3 1 0.3 1 0.2 – 8 2.7 – – – 8 1.5 1 0.2 – – 1 0.5 13 1.9 1 0.5 5 1.0 24 8.9 2 0.3 – 15 2.5 – 4 1.6 113 16.1 13 2.0 2 0.6 – 2 0.4 13 0.6
group had considerably more activity of T. quadristriatus, B. tetracolum and P. melanarius than sites in groups 1 and 2 but fewer H. rufipes. 38 of the 46 sites in group 4 were planted field margins (14 first-year, 16 second-year, 8 unplanted) together with seven
ditch sites and one site from the calabrese field. These sites had the most species, with considerable numbers of P. melanarius, H. rufipes, L. pilicornis and A. dorsalis. Group 5 had 35 sites of which 25 were ditches and 10 field margins (two first-year, eight second-
Table 3 Spearman rank correlation coefficients (rs), probabilities and significances (n.s. not significant; *P < 0.05; **P < 0.01; ***P < 0.001) derived from analyses relating the activity of crop ground beetle species and of species richness to mean weed cover and to vegetation cover in the margins. Species
Acupalpus meridianus Amara apricaria Amara familiaris Amara similata Anchomenus dorsalis Bembidion aeneum Bembidion guttula Bembidion lampros Bembidion obtusum Bembidion quadrimaculatum Bembidion tetracolum Clivina fossor Harpalus affinis Harpalus rufipes Loricera pilicornis Nebria brevicollis Notiophilus biguttatus Pterostichus melanarius Pterostichus niger Pterostichus strenuus Trechus quadristriatus Species richness
Weed cover in crop
Vegetation cover margins
rs
Probability
Significance
rs
Probability
Significance
0.27 0.65 0.15 0.46 0.62 0.26 0.30 0.76 0.33 0.20 0.43 0.18 0.03 0.05 0.28 0.28 0.23 0.19 0.40 0.09 0.20 0.30
0.002 <0.001 0.070 <0.001 <0.001 0.002 <0.001 <0.001 <0.001 0.014 <0.001 0.026 0.748 0.535 <0.001 <0.001 0.005 0.025 <0.001 0.307 0.018 <0.001
** *** n.s. *** *** ** *** *** *** * *** * n.s. n.s. *** *** ** * *** n.s. * ***
0.23 0.24 0.06 0.52 0.16 0.21 0.01 0.53 0.38 0.40 0.06 0.03 0.08 0.03 0.05 0.32 0.36 0.01 0.35 0.39 0.35 0.32
0.117 0.010 0.687 <0.001 0.276 0.151 0.986 <0.001 0.007 0.004 0.671 0.862 0.596 0.849 0.743 0.024 0.012 0.974 0.016 0.006 0.016 0.026
n.s. n.s. n.s. *** n.s. n.s. n.s. *** ** ** n.s. n.s. n.s. n.s. n.s. * * n.s. * ** * *
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Table 4 Mean number of species (one or more in one group) found in sites in the five groups derived from the classification of ground beetle species assemblages. Species order is as axis 1 of the ordination. Species
Trechus quadristriatus Bembidion quadrimaculatum Bembidion obtusum Bembidion lampros Acupalpus meridianus Bembidion tetracolum Bembidion guttula Clivina fossor Bembidion aeneum Amara familiaris Pterostichus melanarius Amara apricaria Notiophilus biguttatus Poecilus cupreus Harpalus rufipes Harpalus affinis Notiophilus substriatus Amara similata Bembidion lunulatum Loricera pilicornis Amara plebeja Anchomenus dorsalis Asaphidion flavipes Badister bullatus Amara aenea Pterostichus niger Amara communis Amara lunicollis Ophonus rufibarbis Pterostichus strenuus Nebria brevicollis Pterostichus madidus Leistus spinibarbis
Group 1
2
3
4
5
3 3 2 67 1 13 – – 1 1 54 6 2 – 12 – – 2 – 2 – 13 – – – 1 – – – – – – –
7 3 2 22 – 49 1 – 4 – 76 1 1 – 18 1 – – – 1 – 2 – – – 3 – – – – – – –
54 1 4 29 – 67 1 2 3 1 190 – 2
3 – 1 16 – 33 – 1 5 1 195 2 2 1 43 2 1 6 1 23 4 60 5 – – 8 1 1 4 1 6 3 –
1 – – 7 – 9 – – – 1 73 1 2 – 12 1 – 5 – 9 2 64 2 1 1 12 1 1 13 5 26 4 1
5 1 – 1 – – – 3 – – – 2 – – – – 7 – –
year). A group again with a lot of species, mostly at low levels of activity, but with the most A. dorsalis, P. niger and N. brevicollis. The relationship between the sites in the five groups and the crop, margin and ditch variables is shown as a biplot derived from the CANOCO analysis (Fig. 1). Group centroids and vectors show the relative importance of the agronomic variables. Axis 1 (eigenvalue 0.262) split the margin and ditch sites in groups 4 and 5 away from the crop sites in the other three groups, with sites in groups 1, 2 and 3 along axis 2 (eigenvalue 0.170). The corresponding distribution of the 20 most abundant species (Fig. 2) shows that many more species were associated with ditch and margin sites, opposite to species in the genera Bembidion and Trechus, which preferred crop sites. Within Bembidion, activity was strongly associated with crop type, with B. lampros and B. quadrimaculatum favouring cauliflower, B. obtusum the leek crop and B. tetracolum the broccoli crop. H. rufipes was associated with the first-year field margins whilst P. melanarius and N. biguttatus were not strongly related to any of the agronomic variables. The vectors in the two figures indicate that the ditch sites were having the most influence along the positive axis 1, with the first- and second-year margins more influential than the unplanted margins. Along axis 2, the cauliflower and broccoli crop types were exerting the most influence. The results of the Monte Carlo permutations showed that the cauliflower crop explained most additional variance (F = 29.73), with ditches (F = 26.80), first-year margins (F = 23.67), second-year margins (F = 22.22), unplanted margins (F = 13.52), leeks (F = 13.22) and broccoli (F = 5.02) also significant (all P = 0.002) in explaining the distribution of species assemblages.
Fig. 1. Biplot showing the relationship of the five group centroids (‘spokes’ indicate standard deviations along axes) derived from the classification to the five crop types, three field margin types and ditches.
Fig. 2. Biplot showing the relationship of the 20 most abundant ground beetle species to the five crop types, three field margin types and ditches.
4. Discussion Considerable differences in the activity of ground beetle species were observed within and between crop fields and field margins, and between the assemblages present. Fewer species were recorded in crop fields than in margins and ditches and most species were found at a fairly low level of activity, with few abundant species. The classification produced three groups with assemblages dominated by sites in particular crop types, indicating that sampling point position within fields had no effect. However, the picture in the margins and ditches was not as clear. The mixing of margin and ditch sites in groups 4 and 5 indicated that the ground beetle species assemblages were signalling variation in the margins and ditches, probably related to vegetation cover. Crop type has been shown to affect ground beetle activity (Booij and Noorlander, 1992) and Hummel et al. (2003) reported that the different ground cover produced by a number of vegetable crops influenced the activity of most invertebrates. In the agricultural landscape vegetation structure is known to affect ground beetle species distribution (Cole et al., 2002; Eyre, 2006) and in the vegetable fields surveyed here it also appears to be affecting species activity in both crop and non-crop habitats. These differences were considerable and the CANOCO analyses showed that three crop types, all three field margin types and ditches significantly affected species assemblage distribution. The species assemblages in the cabbage and broccoli field were
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similar to that in the calabrese field but the conventionally managed field had fewer species and less activity. There is a possibility that differences in vegetation density may have affected pitfall trapping efficiency (Spence and Niemela¨, 1994) but the fewest beetles and species were trapped in the crops (leek and calabrese) and margins (calabrese field) with the least vegetation. Another potential factor that may have influenced pitfall trap catches was the weather, given that sampling was carried out in two different years. The monthly temperature records showed that it was warmer in May and June of 2006 than in 2005 and considerably hotter in July 2006 than in 2005. These higher temperatures may have influenced beetle catches but there was no obvious relationship between the number of beetles caught and temperature. Since both the greatest (cabbage and broccoli) and fewest (leek and calabrese) number of beetles were recorded from 2006 crops, it appears that crop type had considerably more influence than any weather parameter. There was a noticeable reduction in ground beetle species activity in the leek fields, in comparison to the previous cauliflower crop. The cauliflower crops had the most weeds whilst the leeks had the fewest because of efficient mechanical weeding, known to have a detrimental effect on beneficial invertebrates (Thorbek and Bilde, 2004). Weed strips have been used to increase ground beetle activity in cereals (Lys et al., 1994) and Navntoft et al. (2006) reported that weed cover increased ground beetle activity in wheat except for species typical of open ground such as those in the genus Bembidion. The results from the vegetable fields gave a much more complex picture with a split between species preference for weed cover. This was especially apparent in the case of the genus Bembidion where there was increased activity of three species with increasing weed cover and decreased activity with three other species. The three species with greater activity in weedier crops showed reduced activity in the densely vegetated field margins, indicating that for some species vegetation cover between the two extremes was optimal for maximum activity. The results indicated that crop type, weeds and vegetation cover affected both species activity and assemblage distribution in the vegetable fields surveyed. This has considerable implications for maximising predator activity and abundance for pest control (Bianchi et al., 2006). This is especially important in organic Brassica fields where the major pest is cabbage root fly and with ground beetles known to be egg predators. B. lampros is a known egg predator (Finch and Elliott, 1992; Humphreys and Mowat, 1994) whilst Finch (1996) listed 20 species of medium-sized ground beetle species as being consumers of cabbage root fly eggs in the laboratory. However, only three of these medium-sized species occurred in any numbers in the fields and margins surveyed. Whilst P. strenuus was only recorded in relatively low numbers, B. tetracolum was abundant in one field and active in the planted field margins and A. dorsalis was far more abundant in the field margins than in the crop fields. B. lampros was abundant in crop fields and this species, A. dorsalis and B. tetracolum appear to be the major potential cabbage fly egg predators. However, they had different weed and vegetation cover preferences. A. dorsalis and B. lampros were most active in the weediest fields whilst B. tetracolum was more active in fields with fewer weeds. A. dorsalis did not have a preference for field margin type but B. lampros and B. tetracolum were most active in the first-year field margins. Whilst both Bembidion species were active in crop fields, A. dorsalis was far more active in field margins and there was no obvious relationship between the numbers of this species recorded from margins and those trapped in fields. To maximise beneficial invertebrate activity in crops, especially of ground beetles in organic fields, it is likely that some management of both crop fields and field margins will be needed. In Brassica fields there is a requirement to optimise the activity of a
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number of ground beetle species to predate cabbage root fly eggs, most of which were more active with some weed cover. The use of planted field margins to increase predator activity appeared to be most effective when vegetation cover was not too dense but care will be needed to make sure that this was not an artefact of the trapping method. However, margins may need some management input, such as regular thinning and or mowing with removal of cut material. It is also likely that some management procedure should be devised to increase the movement of appropriate species from the field margins into the crop fields. Acknowledgements This work was supported by the European Union Integrated Project QualityLowInputFood (EU FP6 Contract CT-2003-506358.). We thank Philip Effingham of Marshall’s, Butterwick, Lincolnshire for assistance in carrying out the work and a referee for constructive ideas and criticism. References Armstrong, G., McKinlay, R.G., 1997. The effect of undersowing cabbages with clover on the activity of carabid beetles. Biol. Agric. Hortic. 15, 269–277. Bezdek, J.C., 1981. Pattern Recognition with Fuzzy Objective Algorithms. Plenum Press, New York. Bianchi, F.J.J.A., Booij, C.J.H., Tscharntke, T., 2006. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc. R. Soc. B 273, 1715–1727. Booij, C.J.H., Noorlander, J., 1992. Farming systems and insect predators. Agric. Ecosyst. Environ. 40, 125–135. Booij, C.J.H., Noorlander, J., Theunissen, J., 1997. Intercropping cabbage with clover: effects on ground beetles. Biol. Agric. Hortic. 15, 261–268. Cole, L.J., McCracken, D.I., Dennis, P., Downie, I.S., Griffin, A.L., Foster, G.N., Murphy, K.J., Waterhouse, T., 2002. Relationships between agricultural management and ecological groups of ground beetles (Coleoptera:Carabidae) on Scottish farmland. Agric. Ecosyst. Environ. 93, 323–336. Crawley, M.J., 2007. The R Book. John Wiley & Sons Ltd., Chichester, UK. Eyre, M.D., 2006. A strategic interpretation of beetle (Coleoptera) assemblages, biotopes, habitats and distribution, and the conservation implications. J. Insect Conserv. 10, 151–160. Eyre, M.D., Foster, G.N., Luff, M.L., Rushton, S.P., 2006. The definition of British water beetle species pools (Coleoptera) and their relationship to altitude, temperature, precipitation and land cover variables. Hydrobiologia 560, 121–131. Finch, S., 1996. Effect of beetle size on predation of cabbage root fly eggs by ground beetles. Entomol. Exp. Appl. 81, 199–206. Finch, S., Elliott, M.S., 1992. Carabidae as potential biological agents for controlling infestations of the cabbage root fly. Phytoparasitica 20, S67–S70. Gurr, G.M., Wratten, S.D., Luna, J.M., 2003. Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl. Ecol. 4, 107–116. Hill, M.O., 1979. DECORANA—a FORTRAN program for detrended correspondence analysis and reciprocal averaging. In: Ecology and Systematics, Cornell University, Ithaca, New York. Holland, J.M., Thomas, C.F.G., Birkett, T., Southway, S., Oaten, H., 2005. Farm-scale spatiotemporal dynamics of predatory beetles in arable crops. J. Appl. Ecol. 42, 1140–1152. Hummel, R.L., Walgenbach, J.F., Hoyt, G.D., Kennedy, G.G., 2003. Effects of vegetable production system on epigeal arthropod populations. Agric. Ecosyst. Environ. 93, 177–188. Humphreys, I.C., Mowat, D.J., 1994. Effects of some organic treatments on predators (Coleoptera, Carabidae) of cabbage root fly, Delia radicum (L.) (Diptera, Anthomyiidae) and on alternative prey species. Pedobiologia 38, 513–518. Landis, D.A., Wratten, S.D., Gurr, G.M., 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Ann. Rev. Entomol. 45, 175– 201. Langer, V., 1996. Insect-crop interactions in a diversified cropping system: parasitism by Aleochara bilineata and Trybliographa rapae of the cabbage root fly, Delia radicum, on cabbage in the presence of white clover. Entomol. Exp. Appl. 80, 365–374. Leifert, C., Rembialkowska, E., Nielson, J.H., Cooper, J.M., Butler, G., Lueck, L., 2007. Effects of organic and ‘low input’ production methods on food quality and safety. In: Niggli, U., Leifert, C., Alfo¨ldi, T., Lu¨ck, L., Willer, H. (Eds.), Improving Sustainability in Organic and Low Input Food Production Systems. Research Institute of Organic Farming FiBL, Frick, Switzerland, pp. 75–95. Luff, M.L., 2007. The Carabidae (ground beetles) of Britain and Ireland, Handb. Ident. Br. Insects, 2nd edition, vol. 4 (2). pp. 1–247. Lys, J.A., Zimmermann, M., Nentwig, W., 1994. Increase in activity density and species number of carabid beetles in cereals as a result of strip management. Entomol. Exp. Appl. 73, 1–9. Marshall, E.J.R., Moonen, A.C., 2002. Field margins in northern Europe: their functions and interactions with agriculture. Agric. Ecosyst. Environ. 89, 5–21.
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Meek, B., Loxton, D., Sparks, T., Pywell, R., Pickett, H., Nowakowski, M., 2002. The effect of arable field margin composition on invertebrate biodiversity. Biol. Conserv. 106, 259–271. Navntoft, S., Esbjerg, P., Riedel, W., 2006. Effects of reduced pesticide dosages on carabids (Coleoptera:Carabidae) in winter wheat. Agric. Forest Entomol. 8, 57– 62. O’Sullivan, C.M., Gormally, M.J., 2002. A comparison of ground beetle (Carabidae:Coleoptera) communities in an organic and conventional potato crop. Biol. Agric. Hortic. 20, 99–110. Pinheiro, J.C., Bates, D.M., 2000. Mixed-effects models in S and S-PLUS. Springer, New York. Prasad, R.P., Snyder, W.E., 2004. Predator interference limits fly egg biological control by a guild of ground-active beetles. Biol. Control 31, 428–437.
Prasad, R.P., Snyder, W.E., 2006. Polyphagy complicates conservation biological control that targets generalist predators. J. Appl. Ecol. 43, 343–352. R Development Core Team, 2007. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Spence, J.R., Niemela¨, J.K., 1994. Sampling carabid assemblages with pitfall traps— the madness and the method. Can. Entomol. 126, 881–894. Symondson, W.O.C., Sunderland, K.D., Greenstone, M.H., 2002. Can generalist predators be effective biocontrol agents? Ann. Rev. Entomol. 47, 561–594. Ter Braak, C.J.F., Sˇmilauer, P., 1998. CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination, version 4. Centre for Biometry, Wageningen. Thorbek, P., Bilde, T., 2004. Reduced numbers of generalist arthropod predators after crop management. J. Appl. Ecol. 41, 526–538.
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Ground beetles (Coleoptera, Carabidae) in an intensively managed vegetable crop landscape in eastern England M.D. Eyre a,*, D. Labanowska-Bury b, J.G. Avayanos a, R. White c, C. Leifert a a
Nafferton Ecological Farming Group, University of Newcastle upon Tyne, Nafferton Farm, Stocksfield, Northumberland, NE43 7XD, UK Department of Applied Entomology, Warsaw University of Life Sciences- SGGW, Ul. Nowoursynowska 159, 02-787 Warsaw, Poland c Westhorpe Flower & Plants Ltd, Westhorpe House, West End, Benington, Boston, Lincolnshire, PE22 0EL, UK b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 16 December 2008 Received in revised form 4 February 2009 Accepted 24 February 2009
Four fields (three organic and one conventionally managed) in an intensive vegetable producing landscape in eastern England were sampled for ground beetles in 2005 and 2006, using pitfall traps, to investigate species activity and species assemblage distribution within five crop and three field margin types. In addition, non-crop ditch sites were also sampled. Three species assemblages in the fields were strongly related to crop type, with two others consisting of non-crop sites, one dominated by field margins, the other by ditch sites. Species activity and richness in fields were also strongly, and significantly, associated with crop type, with most in organic Brassica crops (cauliflower, cabbage, broccoli), less in organic leeks and least in conventional calabrese. Some species were significantly more active in weedier fields but others preferred more open ground. Considerably more species were recorded from first-year planted field margins, with fewest species active in unplanted margins. Activity was also relatively low in densely vegetated second-year margins. There appeared to be little relationship between species activity in the margins and that in the crop fields. Ground beetle species are important for the predation of cabbage root fly eggs in Brassica crops, especially in organic fields. In order to enhance and maximise appropriate ground beetle species activity and predation within vegetable fields, it is likely that management within both fields and margins would be required, as well as some method for increasing movement of predators from margins into fields. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Ground beetles Beneficial invertebrates Organic farming Brassicas Leeks Field margins
1. Introduction Increasing the activity of generalist invertebrate predators, important pest control agents in arable crops (Symondson et al., 2002), especially ground beetles (Carabidae) (Holland et al., 2005), has been attempted by providing areas such as beetle banks and planted field margins (Landis et al., 2000). This has become more important with the increase in organic food consumption and production, generally a result of concerns about food quality (Leifert et al., 2007), and there is a need to change management practices in organic systems to increase natural enemy effectiveness (Gurr et al., 2003). Planted field margins have usually been sown with a mixture of wildflower seeds (Marshall and Moonen, 2002), which have proven to be much more effective than unsown margins (Meek et al., 2002). In addition to increasing beneficial invertebrate activity by providing appropriate field margins, a number of measures within
* Corresponding author. Tel.: +44 1661 830222; fax: +44 1661 831006. E-mail addresses: [email protected], [email protected] (M.D. Eyre). 0167-8809/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2009.02.006
the crop have also been employed. Weed strips in cereals (Lys et al., 1994) and intercropping with clover in cabbage (Booij et al., 1997) have both been used to increase the activity of ground beetles. Weed cover in fields has also been shown to increase the activity of some ground beetle species in organic potato (O’Sullivan and Gormally, 2002) and cabbage (Armstrong and McKinlay, 1997). The cessation of chemical spray application in organic systems means greater reliance on natural enemies, and in the case of Brassica crops, controlling the major pest, cabbage root fly (Delia radicum L.) (Langer, 1996). Ground beetle species have long been known to be predators of cabbage root fly eggs and there have been laboratory assessments of consumption efficacy (Finch and Elliott, 1992; Finch, 1996). Medium-sized ground beetle species were found to eat more than small species, whilst large species ate few eggs. However, although Prasad and Snyder (2004, 2006) confirmed predation of eggs by small ground beetle species in the field, they also observed small ground beetles being predated by large ground beetle species, which did not eat eggs. In order to provide baseline information on the activity and distribution of ground beetle species and assemblages in an intensively managed landscape used primarily for vegetable
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production, a survey of four (three organic, one conventional) fields was carried out in 2005 and 2006. Activity of ground beetle species in leeks and four different Brassica crops was assessed using pitfall traps. In 2005 two organic fields of cauliflower were sampled and these fields were re-sampled again in 2006, when they were used to grow leeks. In addition, in 2006 an organic field with cabbage and broccoli and a conventional field of calabrese were also surveyed. Field margins and ditch sites were also sampled to cover the major habitat types present. The relationship of both species and assemblage distribution in these non-crop habitats to those in the crop fields was investigated, as they are likely to be the source of a number of pest control species. Management of both crops and field margins, in the context of increasing pest control, is discussed. 2. Methods 2.1. Study area The survey was carried out in three organic fields and one conventionally managed field near Benington, Boston, Lincolnshire in eastern England (national grid reference TF4637). The organic fields were converted to certified organic status in 2004 after being sown with grass and clover for two years. Two organic fields (both 320 m long, 90 m wide) were planted with cauliflower (var Delfino) in the first week of May 2005 and the same fields were planted with leeks (var Shelton) in the middle of May 2006. In the other organic field (300 m long 110 m wide), one-third was planted with cabbage (var Sunta) and two-thirds with broccoli (var Bordeaux) in the middle of May 2006, whilst in the last week of April 2006 calabrese (var Iron) was planted in the conventional field (280 m long, 90 m wide). These fields were in a flat landscape used for intensive vegetable production, with few trees and hedges and fields split by roads or drainage ditches. The conventional field was treated with inorganic fertiliser (N22, P4, K14) at 500 kg ha 1 and a number of pesticide sprays (trifluralin 1 l ha 1; metazachlor 1.5 l ha 1; aphox 420 g ha 1; hallmark 100 ml ha 1; silwet 220 ml ha 1). No fertiliser was applied to the organic fields whilst weeding was mechanical with a spring-tined weeder. To satisfy organic regulations, 4 m wide field margins were established on two sides of the organic fields in September 2004. They were planted with a wild flower mixture containing Achillea millefolium L. (yarrow), Lotus corniculatus L. (birdsfoot trefoil), Silene dioica (L.) (red campion), Papaver rhoeas L. (poppy), Anthriscus sylvestris Hoffm. (cow parsley), Knautia arvensis (L.) (field scabious), Matricaria recutita L. (scented mayweed), Daucus carota L. (wild carrot), Onobrychis viciifolia Scop. (sainfoin) and Galium verum L. (lady’s bedstraw). Redidual Trifolium repens L. (white clover) and Lolium perenne L. (ryegrass) were also present. Development during the 2005 crop season involved these margins (first-year margins) becoming more densely vegetated, with less bare ground with time. By the 2006 crop season (second-year margins), there was dense vegetation cover and no bare ground. The 4 m edge of the conventional field was unplanted, and bare, at the time the calabrese crop was planted but developed vegetation with time. There were drainage ditches, with unmanaged vegetation, next to one edge of the cauliflower and leek fields, on both long edges of the cabbage and broccoli field and next to the field margin of the calabrese field. Historical records held by the UK Meterological Office (www.metoffice.gov.uk) show that there were differences in weather parameters in 2005 and 2006. The mean monthly temperatures for stations in eastern England were 11.6, 16.0, 17.1 and 16.9 8C for May, June, July and August 2005 respectively, with means of 12.5, 16.8, 20.7 and 16.7 8C for the same months in 2006. Monthly precipitation was 38, 54, 47 and 74 mm in May, June, July and August 2005 and 74, 16, 43 and 84 mm for the same months in 2006.
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2.2. Sampling Sampling for ground beetles was carried out using pitfall traps (8.5 cm diameter 10 cm deep) part-filled with saturated salt (NaCl) solution with a little strong detergent as preservative. There were 24 sampling points in each field, with five pitfall traps (0.5 m apart in a star shape), in a grid in the central part of the fields. Eight lines of three sample points, 20 m apart, were employed across the fields at 15, 30 and 45 m intervals away from one field margin in the cauliflower, leek and calabrese fields. Four lines of six sampling points, also at 15, 30 and 45 m from both long field margins, were used in the broccoli (16 sampling points) and cabbage (8 sampling points) field. The traps were set out in the fields just after transplanting of crop plants. In the six planted field margins of the three organic fields, five pitfall traps were set at four 30 m intervals, opposite the area sampled in the crop. In the conventional calabrese field only one margin was sampled, with 8 sampling points opposite the 3 lines of traps in the crop. In addition, the tops of ditches adjacent to the fields were also sampled, in the same pattern as the field margin sites. The two ditches bordering the cauliflower and leek fields (8 sampling points) were sampled in 2005 and 2006, with ditches by the cabbage and broccoli and the calabrese fields (both 8 sampling points) also sampled in 2006. Four samples were taken, at four-week intervals throughout crop development, with the last sample taken in August. All ground beetles were taken from the pitfall traps at each sampling point and counted. Nomenclature follows Luff (2007). At each sampling time an assessment of weed cover in the crops was made. Coverage of weeds was estimated to the nearest 10% and the four estimates were meaned to provide a value for analyses. A similar estimate was made for vegetation cover around the field margin sites at sampling times. 2.3. Data analysis The total number of each ground beetle species recorded throughout the total sampling period were used in analyses concentrating on investigating the effect of crop type on activity and differences in activity between the planted margins (first- and second-year), the unplanted margins and the ditch sites. Linear mixed-effects models (Pinheiro and Bates, 2000) were used to assess activity differences, using the number recorded transformed by log10 n + 1 (Crawley, 2007) as a measure of activity. Analysis of variance was generated using models with crop and margin type and ditches as fixed factors and management (organic or conventional) as the random factor. The effects of weed cover in the fields and vegetation cover in the margins were assessed using Spearman’s rank correlations. In addition, analyses were carried out using ground beetle species richness as a variable. The mixedeffects models and correlations were carried out in the R statistical environment (R Development Core Team, 2007). Multivariate techniques were also applied to the data. The ground beetle species assemblage data, from all sites, was first classified using fuzzy set clustering (Bezdek, 1981), based on a DECORANA ordination (Hill, 1979), as in Eyre et al. (2006). The site scores on the first two axes of the ordination were used for the classification. Constrained ordination, using canonical correspondence analysis (CANOCO) was used to investigate the relationship between the ground beetle assemblages and the crop and margin types (CANOCO Version 4— Ter Braak and Sˇmilauer, 1998). Automatic forward selection of nine agronomic variables within CANOCO was employed and significance calculated using Monte Carlo permutation tests. 3. Results The effect of crop type on the activity of ground beetle species, and on species richness, is shown in Table 1, with means of the
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Table 1 The mean number (one or more) of each ground beetle species and of species richness, standard error, recorded from sites in each crop type, together with the F-ratios, probabilities and significances (n.s. not significant; *P < 0.05; **P < 0.01; ***P < 0.001) generated by the linear mixed-effects models (degrees of freedom 4, 138) comparing activity in each crop. Species
F-ratio
Probability
Significance
Cauliflower
Leek
Broccoli
Cabbage
Calabrese
Acupalpus meridianus Amara apricaria Amara familiaris Amara similata Anchomenus dorsalis Bembidion aeneum Bembidion guttula Bembidion lampros Bembidion obtusum Bembidion quadrimaculatum Bembidion tetracolum Clivina fossor Harpalus affinis Harpalus rufipes Loricera pilicornis Nebria brevicollis Notiophilus biguttatus Pterostichus melanarius Pterostichus niger Pterostichus strenuus Trechus quadristriatus Species richness
2.5 57.4 16.6 22.4 36.4 16.4 6.1 48.8 28.0 2.1 91.5 27.5 6.9 27.3 5.5 90.1 8.5 89.0 13.5 4.9 83.3 9.3
0.042 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.78 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.001 <0.001 <0.001
* *** *** *** *** *** *** *** *** n.s. *** *** *** *** *** *** *** *** *** ** *** ***
1 0.1 6 0.6 1 0.2 2 0.4 13 1.2 1 0.3 – 67 4.3 2 0.3 3 0.4 13 1.1 – – 12 1.1 2 0.4 – 2 0.2 54 4.6 1 0.2 – 3 0.4 14 0.3
– 1 0.2 – – 3 0.6 5 0.5 1 0.2 23 1.4 1 0.2 3 0.4 43 2.3 – 1 0.1 19 1.1 1 0.2 – 1 0.1 67 3.6 3 0.3 – 5 0.7 12 0.3
– – 4 0.7 3 0.6 4 0.7 5 0.7 1 0.5 62 6.5 9 1.1 2 0.5 107 11.0 2 0.8 2 0.3 10 1.3 1 0.2 5 0.8 2 0.4 308 17.4 1 0.4 1 0.2 116 15.4 15 0.3
– – 1 0.4 – 3 0.4 3 0.8 – 39 5.3 5 0.9 2 0.3 92 8.5 4 0.7 2 0.5 6 1.0 – 7 1.6 1 0.4 282 12.2 2 0.4 – 56 16.2 14 1.0
– – – – 2 0.4 2 0.4 – 5 0.8 1 0.3 1 0.3 30 2.5 2 0.3 – 1 0.2 – 8 0.9 2 0.3 77 4.5 1 0.3 – 9 1.3 11 0.5
numbers recorded from sites in the five crops and the F-ratio, probabilities and significances derived from the linear mixedeffect models. Most species generated very highly significant models, with only Bembidion quadrimaculatum activity not significantly affected by crop type and with two species having low activity (Acupalpus meridianus, Pterostichus strenuus) producing less significant models. A number of species were most active in the cauliflower crop (Amara apricaria, Anchomenus dorsalis, Bembidion lampros), but there was generally less activity in the following leek crop. Harpalus rufipes was most active in leeks but the majority of abundant species were most active in the broccoli crop (Bembidion obtusum, Bembidion tetracolum, Pterostichus melanarius, Trechus quadristriatus) and these species also tended to be active in cabbage. In general, species activity was less in calabrese, with Nebria brevicollis the only species most active in this crop. Ground beetle species richness was also highly significantly influenced by crop type and there was greater activity, and more species, in cauliflower, broccoli and cabbage than in leek and calabrese. The mean number of each species recorded from the three field margin types and the ditches, and of species richness, is given in Table 2, together with F-ratios, probabilities and significances from the mixed-effect models. A number of species with low activity produced non-significant models but there were significant differences in activity with most species and with species richness. There was far more overall activity in the first-year field margins than in any other margin type or in the ditches, especially for the more abundant species (A. dorsalis, B. lampros, B. tetracolum, H. rufipes, Loricera pilicornis, P. melanarius). In general, there was more activity in the second-year margins than in the unplanted margins. Some species had most activity in the ditches (N. brevicollis, Ophonus rufibarbis, Pterostichus niger). Mean species richness was significantly greater in the first-year margins, similar in second-year and unplanted margins and lowest in ditches. Weed cover was greatest in the cauliflower crop, which was badly affected by cabbage root fly, less in cabbage and broccoli and least in leek and calabrese, a result of efficient mechanical weeding and spraying respectively. Table 3 shows the coefficients,
probabilities and significances derived from the rank correlation of the ground beetle species activity, and species richness, in the crop sites and the mean weed cover. Most species gave significant correlations but there were conflicting preferences. Three Bemdidion species (B. aeneum, B. guttula, B. tetracolum) were significantly negatively related to weed cover whilst three others (B. lampros, B. obtusum, B. quadrimaculatum) significantly preferred weeds in the crop. Other species with a significant liking for less weedy fields were Clivina fossor, N. brevicollis, P. melanarius, P. niger and T. quadristriatus. Two Amara species (A. apricaria, A. similata), A. meridianus, A. dorsalis, L. pilicornis and Notiophilus biguttatus were significantly associated with increasing weed cover. Two Harpalus species (H. affinis, H. rufipes), Amara familaris and P. strenuus were not significantly related to weed cover. Higher species richness was also significantly related to increasing weed cover. Table 3 also shows the coefficients, probabilities and significances derived from the rank correlation of the crop ground beetle species activity in the field margins, and of species richness, and mean vegetation cover. Most species were not significantly correlated with vegetation cover but where there were significant correlations, they were mostly negative with more species activity in less vegetated margins. These included three Bembidion species (B. lampros, B. obtusum, B. quadrimaculatum), Amara similata, N. brevicollis, N. biguttatus and T. quadristriatus with only two Pterostichus species (P. niger, P. strenuus) significantly more active in densely vegetated margins. The significant relationship between species richness and vegetation cover indicated that as margin vegetation developed, the fewer species were recorded. The classification of the species assemblage data, based on an ordination of all the data, produced five groups. The mean number of each species recorded from sites in the five groups is shown in Table 4. Group 1 was restricted to the 48 sites in the two cauliflower fields, with B. lampros and P. melanarius the two most active species. The 48 sites in the leek fields and 2 sites in the broccoli crop were in group 2. P. melanarius was again the most active species but there was more B. tetracolum and less B. lampros than in group 1. The remaining 22 sites in the broccoli and cabbage fields and 23 sites in the calabrese were in group 3. Sites in this
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Table 2 The mean number (one or more) of each ground beetle species and of species richness, standard error, recorded from sites in field margins and ditches, together with the Fratios, probabilities and significances (n.s. not significant; *P < 0.05; **P < 0.01; ***P < 0.001) generated by the linear mixed-effects models (degrees of freedom 3, 75) comparing activity in margins and ditches. Species
F-ratio
Probability
Significance
First-year
Second-year
Unplanted
Ditches
Acupalpus meridianus Amara aenea Amara apricaria Amara communis Amara familiaris Amara lunicollis Amara plebeja Amara similata Anchomenus dorsalis Asaphidion flavipes Badister bullatus Bembidion aeneum Bembidion lampros Bembidion lunulatum Bembidion obtusum Bembidion quadrimaculatum Bembidion tetracolum Calathus rotundicollis Clivina fossor Demetrias atricapillus Harpalus affinis Harpalus rufipes Leistus spinibarbis Loricera pilicornis Nebria brevicollis Notiophilus biguttatus Notiophilus substriatus Ophonus rufibarbis Poecilus cupreus Pterostichus madidus Pterostichus melanarius Pterostichus niger Pterostichus strenuus Stomis pumicatus Trechus quadristriatus Species richness
4.9 9.2 13.7 2.6 0.3 1.9 11.3 26.9 4.4 53.3 2.5 53.2 23.9 115.1 20.9 3.7 20.5 27.7 2.5 5.4 9.4 13.7 27.6 23.5 13.2 8.5 12.6 19.9 6.4 0.1 5.1 9.9 3.5 2.7 5.6 49.9
0.004 <0.001 <0.001 0.062 0.863 0.132 <0.001 <0.001 0.006 <0.001 0.066 <0.001 <0.001 <0.001 <0.001 0.016 <0.001 <0.001 0.064 0.002 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 0.983 0.003 <0.001 0.019 0.055 0.002 <0.001
** *** *** n.s. n.s. n.s. *** *** ** *** n.s. *** *** *** *** * *** *** n.s. ** *** *** *** *** *** *** *** *** *** n.s. ** *** * n.s. ** ***
1 0.3 2 0.5 4 1.2 1 0.4 1 0.3 – 7 1.2 17 2.9 96 8.1 17 4.1 – 12 2.2 38 6.6 4 0.7 2 0.6 1 0.4 37 4.1 – 1 0.2 1 0.3 3 0.8 62 6.5 – 42 4.8 8 1.9 4 0.6 2 0.4 7 2.7 1 0.4 – 215 19.0 5 1.0 1 0.4 1 0.3 5 1.9 24 0.6
– – – 2 0.5 1 0.3 1 0.7 4 1.4 1 0.4 47 4.0 – – 1 0.3 4 0.7 – – – 32 6.4 – 1 0.2 – 1 0.4 36 5.9 – 21 3.5 8 2.3 1 0.2 – 2 0.6 1 0.2 – 142 18.7 10 1.5 6 1.5 – 1 0.3 15 0.5
– – – – 1 0.4 – 1 0.3 7 3.1 31 9.5 – – – 5 0.8 – – – 17 1.8 – – – 1 0.3 15 2.5 – 2 0.7 10 1.4 2 0.7 – 1 0.3 – 15 2.2 126 27.2 5 0.9 – – 2 0.4 15 1.0
– – 1 0.3 1 0.3 1 0.2 – 1 0.2 3 1.0 66 11.3 1 0.3 1 0.2 – 8 2.7 – – – 8 1.5 1 0.2 – – 1 0.5 13 1.9 1 0.5 5 1.0 24 8.9 2 0.3 – 15 2.5 – 4 1.6 113 16.1 13 2.0 2 0.6 – 2 0.4 13 0.6
group had considerably more activity of T. quadristriatus, B. tetracolum and P. melanarius than sites in groups 1 and 2 but fewer H. rufipes. 38 of the 46 sites in group 4 were planted field margins (14 first-year, 16 second-year, 8 unplanted) together with seven
ditch sites and one site from the calabrese field. These sites had the most species, with considerable numbers of P. melanarius, H. rufipes, L. pilicornis and A. dorsalis. Group 5 had 35 sites of which 25 were ditches and 10 field margins (two first-year, eight second-
Table 3 Spearman rank correlation coefficients (rs), probabilities and significances (n.s. not significant; *P < 0.05; **P < 0.01; ***P < 0.001) derived from analyses relating the activity of crop ground beetle species and of species richness to mean weed cover and to vegetation cover in the margins. Species
Acupalpus meridianus Amara apricaria Amara familiaris Amara similata Anchomenus dorsalis Bembidion aeneum Bembidion guttula Bembidion lampros Bembidion obtusum Bembidion quadrimaculatum Bembidion tetracolum Clivina fossor Harpalus affinis Harpalus rufipes Loricera pilicornis Nebria brevicollis Notiophilus biguttatus Pterostichus melanarius Pterostichus niger Pterostichus strenuus Trechus quadristriatus Species richness
Weed cover in crop
Vegetation cover margins
rs
Probability
Significance
rs
Probability
Significance
0.27 0.65 0.15 0.46 0.62 0.26 0.30 0.76 0.33 0.20 0.43 0.18 0.03 0.05 0.28 0.28 0.23 0.19 0.40 0.09 0.20 0.30
0.002 <0.001 0.070 <0.001 <0.001 0.002 <0.001 <0.001 <0.001 0.014 <0.001 0.026 0.748 0.535 <0.001 <0.001 0.005 0.025 <0.001 0.307 0.018 <0.001
** *** n.s. *** *** ** *** *** *** * *** * n.s. n.s. *** *** ** * *** n.s. * ***
0.23 0.24 0.06 0.52 0.16 0.21 0.01 0.53 0.38 0.40 0.06 0.03 0.08 0.03 0.05 0.32 0.36 0.01 0.35 0.39 0.35 0.32
0.117 0.010 0.687 <0.001 0.276 0.151 0.986 <0.001 0.007 0.004 0.671 0.862 0.596 0.849 0.743 0.024 0.012 0.974 0.016 0.006 0.016 0.026
n.s. n.s. n.s. *** n.s. n.s. n.s. *** ** ** n.s. n.s. n.s. n.s. n.s. * * n.s. * ** * *
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Table 4 Mean number of species (one or more in one group) found in sites in the five groups derived from the classification of ground beetle species assemblages. Species order is as axis 1 of the ordination. Species
Trechus quadristriatus Bembidion quadrimaculatum Bembidion obtusum Bembidion lampros Acupalpus meridianus Bembidion tetracolum Bembidion guttula Clivina fossor Bembidion aeneum Amara familiaris Pterostichus melanarius Amara apricaria Notiophilus biguttatus Poecilus cupreus Harpalus rufipes Harpalus affinis Notiophilus substriatus Amara similata Bembidion lunulatum Loricera pilicornis Amara plebeja Anchomenus dorsalis Asaphidion flavipes Badister bullatus Amara aenea Pterostichus niger Amara communis Amara lunicollis Ophonus rufibarbis Pterostichus strenuus Nebria brevicollis Pterostichus madidus Leistus spinibarbis
Group 1
2
3
4
5
3 3 2 67 1 13 – – 1 1 54 6 2 – 12 – – 2 – 2 – 13 – – – 1 – – – – – – –
7 3 2 22 – 49 1 – 4 – 76 1 1 – 18 1 – – – 1 – 2 – – – 3 – – – – – – –
54 1 4 29 – 67 1 2 3 1 190 – 2
3 – 1 16 – 33 – 1 5 1 195 2 2 1 43 2 1 6 1 23 4 60 5 – – 8 1 1 4 1 6 3 –
1 – – 7 – 9 – – – 1 73 1 2 – 12 1 – 5 – 9 2 64 2 1 1 12 1 1 13 5 26 4 1
5 1 – 1 – – – 3 – – – 2 – – – – 7 – –
year). A group again with a lot of species, mostly at low levels of activity, but with the most A. dorsalis, P. niger and N. brevicollis. The relationship between the sites in the five groups and the crop, margin and ditch variables is shown as a biplot derived from the CANOCO analysis (Fig. 1). Group centroids and vectors show the relative importance of the agronomic variables. Axis 1 (eigenvalue 0.262) split the margin and ditch sites in groups 4 and 5 away from the crop sites in the other three groups, with sites in groups 1, 2 and 3 along axis 2 (eigenvalue 0.170). The corresponding distribution of the 20 most abundant species (Fig. 2) shows that many more species were associated with ditch and margin sites, opposite to species in the genera Bembidion and Trechus, which preferred crop sites. Within Bembidion, activity was strongly associated with crop type, with B. lampros and B. quadrimaculatum favouring cauliflower, B. obtusum the leek crop and B. tetracolum the broccoli crop. H. rufipes was associated with the first-year field margins whilst P. melanarius and N. biguttatus were not strongly related to any of the agronomic variables. The vectors in the two figures indicate that the ditch sites were having the most influence along the positive axis 1, with the first- and second-year margins more influential than the unplanted margins. Along axis 2, the cauliflower and broccoli crop types were exerting the most influence. The results of the Monte Carlo permutations showed that the cauliflower crop explained most additional variance (F = 29.73), with ditches (F = 26.80), first-year margins (F = 23.67), second-year margins (F = 22.22), unplanted margins (F = 13.52), leeks (F = 13.22) and broccoli (F = 5.02) also significant (all P = 0.002) in explaining the distribution of species assemblages.
Fig. 1. Biplot showing the relationship of the five group centroids (‘spokes’ indicate standard deviations along axes) derived from the classification to the five crop types, three field margin types and ditches.
Fig. 2. Biplot showing the relationship of the 20 most abundant ground beetle species to the five crop types, three field margin types and ditches.
4. Discussion Considerable differences in the activity of ground beetle species were observed within and between crop fields and field margins, and between the assemblages present. Fewer species were recorded in crop fields than in margins and ditches and most species were found at a fairly low level of activity, with few abundant species. The classification produced three groups with assemblages dominated by sites in particular crop types, indicating that sampling point position within fields had no effect. However, the picture in the margins and ditches was not as clear. The mixing of margin and ditch sites in groups 4 and 5 indicated that the ground beetle species assemblages were signalling variation in the margins and ditches, probably related to vegetation cover. Crop type has been shown to affect ground beetle activity (Booij and Noorlander, 1992) and Hummel et al. (2003) reported that the different ground cover produced by a number of vegetable crops influenced the activity of most invertebrates. In the agricultural landscape vegetation structure is known to affect ground beetle species distribution (Cole et al., 2002; Eyre, 2006) and in the vegetable fields surveyed here it also appears to be affecting species activity in both crop and non-crop habitats. These differences were considerable and the CANOCO analyses showed that three crop types, all three field margin types and ditches significantly affected species assemblage distribution. The species assemblages in the cabbage and broccoli field were
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similar to that in the calabrese field but the conventionally managed field had fewer species and less activity. There is a possibility that differences in vegetation density may have affected pitfall trapping efficiency (Spence and Niemela¨, 1994) but the fewest beetles and species were trapped in the crops (leek and calabrese) and margins (calabrese field) with the least vegetation. Another potential factor that may have influenced pitfall trap catches was the weather, given that sampling was carried out in two different years. The monthly temperature records showed that it was warmer in May and June of 2006 than in 2005 and considerably hotter in July 2006 than in 2005. These higher temperatures may have influenced beetle catches but there was no obvious relationship between the number of beetles caught and temperature. Since both the greatest (cabbage and broccoli) and fewest (leek and calabrese) number of beetles were recorded from 2006 crops, it appears that crop type had considerably more influence than any weather parameter. There was a noticeable reduction in ground beetle species activity in the leek fields, in comparison to the previous cauliflower crop. The cauliflower crops had the most weeds whilst the leeks had the fewest because of efficient mechanical weeding, known to have a detrimental effect on beneficial invertebrates (Thorbek and Bilde, 2004). Weed strips have been used to increase ground beetle activity in cereals (Lys et al., 1994) and Navntoft et al. (2006) reported that weed cover increased ground beetle activity in wheat except for species typical of open ground such as those in the genus Bembidion. The results from the vegetable fields gave a much more complex picture with a split between species preference for weed cover. This was especially apparent in the case of the genus Bembidion where there was increased activity of three species with increasing weed cover and decreased activity with three other species. The three species with greater activity in weedier crops showed reduced activity in the densely vegetated field margins, indicating that for some species vegetation cover between the two extremes was optimal for maximum activity. The results indicated that crop type, weeds and vegetation cover affected both species activity and assemblage distribution in the vegetable fields surveyed. This has considerable implications for maximising predator activity and abundance for pest control (Bianchi et al., 2006). This is especially important in organic Brassica fields where the major pest is cabbage root fly and with ground beetles known to be egg predators. B. lampros is a known egg predator (Finch and Elliott, 1992; Humphreys and Mowat, 1994) whilst Finch (1996) listed 20 species of medium-sized ground beetle species as being consumers of cabbage root fly eggs in the laboratory. However, only three of these medium-sized species occurred in any numbers in the fields and margins surveyed. Whilst P. strenuus was only recorded in relatively low numbers, B. tetracolum was abundant in one field and active in the planted field margins and A. dorsalis was far more abundant in the field margins than in the crop fields. B. lampros was abundant in crop fields and this species, A. dorsalis and B. tetracolum appear to be the major potential cabbage fly egg predators. However, they had different weed and vegetation cover preferences. A. dorsalis and B. lampros were most active in the weediest fields whilst B. tetracolum was more active in fields with fewer weeds. A. dorsalis did not have a preference for field margin type but B. lampros and B. tetracolum were most active in the first-year field margins. Whilst both Bembidion species were active in crop fields, A. dorsalis was far more active in field margins and there was no obvious relationship between the numbers of this species recorded from margins and those trapped in fields. To maximise beneficial invertebrate activity in crops, especially of ground beetles in organic fields, it is likely that some management of both crop fields and field margins will be needed. In Brassica fields there is a requirement to optimise the activity of a
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number of ground beetle species to predate cabbage root fly eggs, most of which were more active with some weed cover. The use of planted field margins to increase predator activity appeared to be most effective when vegetation cover was not too dense but care will be needed to make sure that this was not an artefact of the trapping method. However, margins may need some management input, such as regular thinning and or mowing with removal of cut material. It is also likely that some management procedure should be devised to increase the movement of appropriate species from the field margins into the crop fields. Acknowledgements This work was supported by the European Union Integrated Project QualityLowInputFood (EU FP6 Contract CT-2003-506358.). We thank Philip Effingham of Marshall’s, Butterwick, Lincolnshire for assistance in carrying out the work and a referee for constructive ideas and criticism. References Armstrong, G., McKinlay, R.G., 1997. The effect of undersowing cabbages with clover on the activity of carabid beetles. Biol. Agric. Hortic. 15, 269–277. Bezdek, J.C., 1981. Pattern Recognition with Fuzzy Objective Algorithms. Plenum Press, New York. Bianchi, F.J.J.A., Booij, C.J.H., Tscharntke, T., 2006. Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. Proc. R. Soc. B 273, 1715–1727. Booij, C.J.H., Noorlander, J., 1992. Farming systems and insect predators. Agric. Ecosyst. Environ. 40, 125–135. Booij, C.J.H., Noorlander, J., Theunissen, J., 1997. Intercropping cabbage with clover: effects on ground beetles. Biol. Agric. Hortic. 15, 261–268. Cole, L.J., McCracken, D.I., Dennis, P., Downie, I.S., Griffin, A.L., Foster, G.N., Murphy, K.J., Waterhouse, T., 2002. Relationships between agricultural management and ecological groups of ground beetles (Coleoptera:Carabidae) on Scottish farmland. Agric. Ecosyst. Environ. 93, 323–336. Crawley, M.J., 2007. The R Book. John Wiley & Sons Ltd., Chichester, UK. Eyre, M.D., 2006. A strategic interpretation of beetle (Coleoptera) assemblages, biotopes, habitats and distribution, and the conservation implications. J. Insect Conserv. 10, 151–160. Eyre, M.D., Foster, G.N., Luff, M.L., Rushton, S.P., 2006. The definition of British water beetle species pools (Coleoptera) and their relationship to altitude, temperature, precipitation and land cover variables. Hydrobiologia 560, 121–131. Finch, S., 1996. Effect of beetle size on predation of cabbage root fly eggs by ground beetles. Entomol. Exp. Appl. 81, 199–206. Finch, S., Elliott, M.S., 1992. Carabidae as potential biological agents for controlling infestations of the cabbage root fly. Phytoparasitica 20, S67–S70. Gurr, G.M., Wratten, S.D., Luna, J.M., 2003. Multi-function agricultural biodiversity: pest management and other benefits. Basic Appl. Ecol. 4, 107–116. Hill, M.O., 1979. DECORANA—a FORTRAN program for detrended correspondence analysis and reciprocal averaging. In: Ecology and Systematics, Cornell University, Ithaca, New York. Holland, J.M., Thomas, C.F.G., Birkett, T., Southway, S., Oaten, H., 2005. Farm-scale spatiotemporal dynamics of predatory beetles in arable crops. J. Appl. Ecol. 42, 1140–1152. Hummel, R.L., Walgenbach, J.F., Hoyt, G.D., Kennedy, G.G., 2003. Effects of vegetable production system on epigeal arthropod populations. Agric. Ecosyst. Environ. 93, 177–188. Humphreys, I.C., Mowat, D.J., 1994. Effects of some organic treatments on predators (Coleoptera, Carabidae) of cabbage root fly, Delia radicum (L.) (Diptera, Anthomyiidae) and on alternative prey species. Pedobiologia 38, 513–518. Landis, D.A., Wratten, S.D., Gurr, G.M., 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Ann. Rev. Entomol. 45, 175– 201. Langer, V., 1996. Insect-crop interactions in a diversified cropping system: parasitism by Aleochara bilineata and Trybliographa rapae of the cabbage root fly, Delia radicum, on cabbage in the presence of white clover. Entomol. Exp. Appl. 80, 365–374. Leifert, C., Rembialkowska, E., Nielson, J.H., Cooper, J.M., Butler, G., Lueck, L., 2007. Effects of organic and ‘low input’ production methods on food quality and safety. In: Niggli, U., Leifert, C., Alfo¨ldi, T., Lu¨ck, L., Willer, H. (Eds.), Improving Sustainability in Organic and Low Input Food Production Systems. Research Institute of Organic Farming FiBL, Frick, Switzerland, pp. 75–95. Luff, M.L., 2007. The Carabidae (ground beetles) of Britain and Ireland, Handb. Ident. Br. Insects, 2nd edition, vol. 4 (2). pp. 1–247. Lys, J.A., Zimmermann, M., Nentwig, W., 1994. Increase in activity density and species number of carabid beetles in cereals as a result of strip management. Entomol. Exp. Appl. 73, 1–9. Marshall, E.J.R., Moonen, A.C., 2002. Field margins in northern Europe: their functions and interactions with agriculture. Agric. Ecosyst. Environ. 89, 5–21.
346
M.D. Eyre et al. / Agriculture, Ecosystems and Environment 131 (2009) 340–346
Meek, B., Loxton, D., Sparks, T., Pywell, R., Pickett, H., Nowakowski, M., 2002. The effect of arable field margin composition on invertebrate biodiversity. Biol. Conserv. 106, 259–271. Navntoft, S., Esbjerg, P., Riedel, W., 2006. Effects of reduced pesticide dosages on carabids (Coleoptera:Carabidae) in winter wheat. Agric. Forest Entomol. 8, 57– 62. O’Sullivan, C.M., Gormally, M.J., 2002. A comparison of ground beetle (Carabidae:Coleoptera) communities in an organic and conventional potato crop. Biol. Agric. Hortic. 20, 99–110. Pinheiro, J.C., Bates, D.M., 2000. Mixed-effects models in S and S-PLUS. Springer, New York. Prasad, R.P., Snyder, W.E., 2004. Predator interference limits fly egg biological control by a guild of ground-active beetles. Biol. Control 31, 428–437.
Prasad, R.P., Snyder, W.E., 2006. Polyphagy complicates conservation biological control that targets generalist predators. J. Appl. Ecol. 43, 343–352. R Development Core Team, 2007. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. Spence, J.R., Niemela¨, J.K., 1994. Sampling carabid assemblages with pitfall traps— the madness and the method. Can. Entomol. 126, 881–894. Symondson, W.O.C., Sunderland, K.D., Greenstone, M.H., 2002. Can generalist predators be effective biocontrol agents? Ann. Rev. Entomol. 47, 561–594. Ter Braak, C.J.F., Sˇmilauer, P., 1998. CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination, version 4. Centre for Biometry, Wageningen. Thorbek, P., Bilde, T., 2004. Reduced numbers of generalist arthropod predators after crop management. J. Appl. Ecol. 41, 526–538.