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Jul 29, 2011 - Arable weeds in organically managed wheat fields foster carabid beetles by resource- and structure-mediated effects. Eva Diehl • Volkmar ...
Arthropod-Plant Interactions (2012) 6:75–82 DOI 10.1007/s11829-011-9153-4

ORIGINAL PAPER

Arable weeds in organically managed wheat fields foster carabid beetles by resource- and structure-mediated effects Eva Diehl • Volkmar Wolters • Klaus Birkhofer

Received: 15 March 2011 / Accepted: 7 July 2011 / Published online: 29 July 2011 Ó Springer Science+Business Media B.V. 2011

Abstract Arable weeds in organically managed fields may foster arthropod generalist predators by the provision of shelter and favorable microclimate (structure-mediated effects) and the provision of additional animal and floral food resources (resource-mediated effects). In three organically managed winter wheat fields in Central Germany, we investigated the impact of weed removal and introduction of artificial weed-like structure on the activity density and species richness of carabid beetles with respect to trophic groups, microclimatic conditions, and densities of potential prey. Removal of weeds reduced both carabid activity density and species richness but did not affect trophic group composition. The decline in carabid activity density was dampened by the addition of artificial structure. Mean daily surface temperature and light intensity were significantly lower under weeds and artificial plants than under wheat plants alone. Weed removal reduced the abundance of leafhoppers and true bugs, but the response was inconsistent across fields. We conclude that the presence of arable weeds in organically managed wheat fields fosters carabid activity density and species richness via resource-mediated effects, such as a higher availability of weed-borne resources (e.g. seeds and pollen) and herbivorous prey. Structure-mediated effects (altering the microclimate) add to this positive effect. The presence of

Handling editor: Robert Glinwood.

Electronic supplementary material The online version of this article (doi:10.1007/s11829-011-9153-4) contains supplementary material, which is available to authorized users. E. Diehl (&)  V. Wolters  K. Birkhofer Department of Animal Ecology, Justus Liebig University, Heinrich-Buff-Ring 26-32, 35392 Giessen, Germany e-mail: [email protected]

weeds in organically managed wheat fields enhances carabid activity density and diversity and needs to be integrated into future management strategies for natural enemy conservation. Keywords Carabidae  Organic farming  Biodiversity  Trophic interactions  Habitat complexity  Biological control

Introduction Organic farming systems have been suggested to counteract the severe loss of biodiversity that has been caused by agricultural intensification over the past 50 years (Stoate et al. 2001). In fact, organic farming has successfully fostered biodiversity, with up to 30% higher species richness and 50% higher abundances of animals and plants in arable fields compared to conventional farming systems (Bengtsson et al. 2005). The higher plant diversity in organically managed cereal fields is among the most obvious consequences of organic farming practices (Gabriel et al. 2006). Although the presence of weeds is often accompanied by yield losses (Zimdahl 2004), arable weeds are currently regarded as desirable ecological goods because of their aesthetic value and their positive effects on associated animal populations (Marshall et al. 2003). A high plant diversity, e.g. in non-crop plant strips within agricultural fields, fosters the abundance and diversity of arthropods (Asteraki et al. 2004). Nevertheless, the specific mechanisms that link weeds and surface-dwelling arthropods in arable fields have rarely been investigated in manipulative field experiments. Ground beetles (Coleoptera: Carabidae) are good model organisms for studying these links, as carabids have specific microhabitat needs that are affected

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by weed growth and further utilize plant-borne resources and feed on weed-attracted prey (Holland et al. 2002). Weeds may therefore foster carabid communities via two non-exclusive mechanisms (Norris and Kogan 2000); we refer to these links as structure- or resource-mediated effects (see also Birkhofer et al. 2008). Microclimatic conditions in agricultural fields are mainly determined by vegetation cover (Ekschmitt et al. 1997). Concerning structure-mediated effects, a denser vegetation cover due to the presence of weeds modifies the microclimate, such as ground temperature, and may provide shelter from physical disturbances, e.g. unfavorable weather conditions (e.g. Honek 1997). The presence of weeds in crop monocultures further increases the structural complexity of these habitats, defined as the absolute abundance of individual structural components per unit area (McCoy and Bell 1991; Woodcock et al. 2007). In complex-structured habitats, the abundance of predatory arthropods such as carnivorous carabids is known to be higher, as rates of intraguild predation and cannibalism are reduced under such conditions (Langellotto and Denno 2004). Several authors have highlighted the strong impact of these structure-mediated effects of weeds on arthropod populations (e.g. Booij and Noorlander 1992; Marshall et al. 2003). Most carabid beetles are generalist predators and prey on a variety of herbivores (e.g. aphids) and detritivores (e.g. collembolans) (Holland et al. 2002). Carabid beetles may hence contribute to a reduction in crop plant damage and an increase in yields by consuming large numbers of ¨ stman et al. 2003). Concerning resourcepest insects (O mediated effects, weeds and weed litter serve as food sources for herbivorous and detritivorous carabid species, and weeds may attract additional prey for generalist predators (Scheu 2001; Birkhofer et al. 2008). Several omnivorous carabid species further utilize weeds by consuming pollen or nectar (e.g. Lo¨vei and Sunderland 1996). Species from the genus Amara, for example, primarily feed on seeds, and such phytophagous or omnivorous carabid species may hence benefit directly from weed-borne resources (e.g. Honek et al. 2003). We investigated the impact of weed removal and introduction of artificial structure on carabid activity density and species richness in organically managed winter wheat fields. The introduction of artificial structure simulated structural characteristics of weeds and provided an opportunity to analyze the impact of structure-mediated effects independently of resource-mediated effects (Fig. 1; cf. Birkhofer et al. 2008). We assumed that carabid populations would synergistically be fostered by structure- and resource-mediated effects of weeds. Thus, we hypothesized that (1) the removal of weeds would reduce carabid activity density and species richness within fields, (2) the simulation of structural

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characteristics of weeds by artificial structure would dampen this negative effect of weed removal, and (3) the combination of weeds and artificial structure would enhance carabid activity density and species richness. To relate results on carabid populations to structure- and resource-mediated effects, we investigated microclimatic conditions, densities of herbivorous and detritivorous prey, and composition of trophic groups within carabids.

Materials and methods Study site The experiment was conducted in 2008 in three organically managed winter wheat fields (Triticum aestivum L. var. Lona, Poales: Poaceae) in the Wetterau Ecoregion (50°130 21.9400 N, 8°470 25.1500 E; Hesse, Germany). All fields had been under organic management since 1994, i.e. operating without pesticides, herbicides, and inorganic fertilizers, and were managed with identical crop rotation (alfalfa, winter wheat, potatoes, spelt, rye) and tillage (plowing depth 25 cm). Wheat plants were sown in 27-cmwide lines. In each field, weeds were recorded from eight 2.25-m2 large experimental plots in which weeds were left unmanipulated during the experiment (n = 24; see experimental design) and determined to species. Experimental Design In each of the three winter wheat fields, we established 16 unfenced plots with a size of 2.25 m2 and removed weeds from half of these plots while introducing artificial structure to half of the plots in a fully crossed design (n = 48 for all fields). The full factorial design resulted in four treatments replicated four times per field: (1) weeds removed, no artificial structure added (‘‘bare-ground’’

Fig. 1 Conceptual drawing of structure- and resource-mediated effects of arable weeds on carabid beetles. Simulation of structural characteristics of weeds by artificial structure makes it possible to study structure-mediated effects (left side, dotted box) independently of resource-mediated effects (right side)

Arable weeds in organically managed wheat fields foster carabid beetles

treatment; to test for the absence of structure- and resourcemediated effects of weeds), (2) weeds removed, artificial structure added (‘‘artificial structure’’ treatment; to test for the absence of weed-associated resource-mediated effects, but the presence of structure-mediated effects), (3) weeds unmanipulated, no artificial structure added (‘‘control’’ treatment; to test for the presence of structure- and resource-mediated effects of weeds), and (4) weeds unmanipulated, artificial structure added (‘‘additional structure’’ treatment; to test for a possible amplification of structure-mediated effects through additional structure). All weeds and their roots were removed manually at the beginning of the experiment, and re-grown weeds were removed weekly during the experiment. Treatment plots that included weeds were disturbed by walking through them and simulating disturbance to the soil to control for side effects of our weed manipulation. Artificial structure consisted of plastic plants with three different leaf types (Flora-Seta GmbH, Nu¨rtingen, Germany) to simulate the structural diversity of arable weed assemblages. Plastic plants were 30 cm high and covered a surface radius of approximately 20 cm per plant with 10–12 branches, resembling weed species that were present in all fields (e.g. Matricaria chamomilla L.). To reflect natural weed cover (estimated prior to treatment establishment), six plastic plants with varying leaf types were positioned per plot in a standardized arrangement between wheat stands. We are aware that plastic plants solely simulate structural characteristics but do not simulate any biochemical components of weed species that were originally present in the fields. The treatments were established from 13 June to 11 July 2008. In a randomized block design, four blocks per field were established with four experimental plots per block (5 m minimum distance of all blocks from the field edge, 12 m minimum distance between blocks, and 5 m distance of plots within a block). Sampling The activity density and species richness of carabids and the activity density of an abundant, surface-active detritivore group (epedaphic Collembola) were estimated using pitfall traps (14 cm depth, 8.5 cm diameter, ethylene glycol–water solution with the detergent Dowfax 2A1). Each experimental plot was sampled for 10 days prior to the end of the experiment with one central pitfall trap. Carabid species were categorized into trophic groups (carnivorous, phytophagous, and omnivorous) according to specifications in the literature (Lindroth 1985/86; Koch 1989; Marggi 1992; Luff 1998; Ribera et al. 1999; Ribera et al. 2001; Toft and Bilde 2002; Freude et al. 2004; Purtauf et al. 2005). Collembola were counted and determined to family level. The abundance of sap-sucking herbivores was

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estimated by suction-sampling all plots at the end of the experiment (16 subsamples per plot, 5 s per subsample, see Brook et al. 2008) under dry weather conditions using a motor-driven suction sampler with a sampling nozzle adapted to the height of wheat plants (Stihl SH85, Waiblingen). Cicadina, Aphidina, and Heteroptera were counted. To identify microclimatic differences, we measured ground temperature (°C) and light intensity (lux) under natural weed, artificial and wheat vegetation during the experiment with three data loggers per field (HOBOÒ Pendant temperature/light data logger, Onsent Computer Corporation, Bourne, USA). Water content (% dw) was measured from soil samples of all experimental plots at the end of the experiment (VDLUFA 1991). Statistical analysis Effects of the factors ‘‘Weed’’ (2 levels: unmanipulated or removed), ‘‘Artificial structure’’ (2 levels: artificial structure introduced and no artificial structure introduced), ‘‘Block’’ (4 levels), and ‘‘Field’’ (3 levels) on arthropods were analyzed by permutational analysis of variance (Anderson 2001; McArdle and Anderson 2001). The factors ‘‘Weed’’ and ‘‘Artificial structure’’ were included in the model as fixed factors, whereas ‘‘Block’’ and ‘‘Field’’ were included as random factors with ‘‘Block’’ nested in ‘‘Field.’’ All interaction terms of these factors up to the third order were included in the model. The highest-order interaction term was excluded from our analyses, as randomized block designs typically lack replication of treatments within blocks (Anderson et al. 2008). All response variables were square root transformed prior to analyses. Resemblance matrices for permutational ANOVA were based on Bray–Curtis distances (Bray and Curtis 1957) and were analyzed performing 9999 permutations with the permutation method ‘‘Permutation of residuals under a reduced model’’ (Anderson et al. 2008). Monte Carlo P-values were used to evaluate statistical significance for main effects of factors ‘‘Weed’’ and ‘‘Artificial structure,’’ as the number of unique permutational runs was lower than 100 (Anderson et al. 2008). In figures, mean values are given with standard errors. For a description of responses, percentage values were calculated as proportions of the mean value in the focused treatment compared to the control treatment (= 100%). In a second series of permutational ANOVA models, we analyzed the effects of the factor ‘‘Vegetation type’’ (3 levels: weed, artificial, or wheat vegetation) on mean daily surface temperatures and mean daily light intensities measured during the daytime (7 AM–7 PM). ‘‘Vegetation type’’ was included in the model as fixed factor, and ‘‘Field’’ was included as random factor. As the design lacks replication for factor ‘‘Field,’’ the interaction term was excluded from

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our analyses (Anderson et al. 2008). Data were normalized prior to analysis by subtracting the mean from each entry of a single variable and dividing by the standard deviation for that variable, as temperatures and light intensities were not measured on identical scales (Clarke and Gorley 2006). Resemblance matrices were based on Euclidean distances, as recommended for environmental data (e.g. Clarke and Gorley 2006). Data were analyzed performing 9999 permutations with the permutation method ‘‘Permutation of residuals under a reduced model’’ (Anderson et al. 2008). Differences in soil water content between fields were analyzed separately, but with the same settings in a one-way permutational ANOVA (only factor ‘‘Field’’). All statistical analyses were performed with PRIMER version 6.1.11 with the PERMANOVA ? add-on version 1.0.1 (PRIMER-E, Plymouth, UK).

Results We identified 12 weed species in two of the fields and 13 in one field. Out of a total of 18 identified species, 7 were common in all fields: Alopecurus myosuroides (Hudson), Apera spica-venti ([L.] Palisot de Beauvois), Convolvulus arvensis L., Galium aparine L., Matricaria chamomilla L., Myosotis arvensis ([L.] Hill), and Papaver rhoeas L. (a list of all weed species is given in Online Resource 1). Table 1 Results of permutational analysis of variance for response of carabid activity density and species richness and densities of potential prey (abundance of sap-sucking herbivores and activity density of collembolan detritivores) to removal of weeds (‘‘Weed’’), Source

df

A total of 3887 carabid beetles from 28 species were sampled in 48 experimental plots (a list of carabid species with feeding modes is given in Online Resource 2). Out of these 28 species, 13 species were carnivorous, accounting for 61.4% of the trapped individuals, 7 species were omnivorous, accounting for 37.6% of individuals, and 8 were phytophagous, accounting for 1% of individuals. The carnivorous Pterostichus melanarius (Illiger) and the omnivorous Harpalus rufipes (Degeer) were the most abundant carabid species. Weed removal significantly affected the activity density of carabids, but the response depended on the presence of artificial structure (Table 1; ‘‘Weed’’ x ‘‘Artificial structure’’). The mean activity density of carabids was highest in unmanipulated, weed-covered control plots with 105.6 ± 17.0 individuals per trap (Fig. 2). When weeds were removed, mean activity density of carabids was 41% lower in bare-ground plots and 28% lower in artificial structure plots compared to control plots. In plots where artificial structure was introduced in addition to natural weeds, mean activity density was 24% lower in comparison with natural weed plots. Our experimental treatments consistently affected carabid populations, despite significant spatial variability of carabid activity density among fields (Table 1; ‘‘Field’’). Species richness of carabids was significantly affected by the removal of weeds (Table 1; ‘‘Weed’’), with no significant effect of artificial structure introduction of artificial structure (‘‘Artificial structure’’), block identity in a randomized block design (‘‘Block’’), and field identity (‘‘Field’’) in three winter wheat fields

Carabid

Carabid

Herbivore

Detritivore

activity density

species richness

abundance

activity density

Pseudo-F

P

Pseudo-F

Pseudo-F

P

P

Pseudo-F

P

Weed

1

2.93

0.193

12.89

0.048*

1.45

0.332

0.30

0.603

Artificial structure

1

1.02

0.429

0.76

0.483

1.63

0.300

3.65

0.078

Block (Field)

9

0.70

0.764

0.27

0.972

1.54

0.171

2.17

0.109

Field

2

16.99

0.000*

4.65

0.056

1.82

0.121

12.38

0.003*

Weed 9 Artificial structure

1

21.69

0.015*

0.54

0.635

0.35

0.618

1.14

0.123

Weed 9 Block (Field)

9

0.72

0.718

0.91

0.559

1.21

0.350

0.51

0.941

Weed 9 Field

2

0.84

0.486

0.07

0.957

1.97

0.156

1.88

0.155

Artificial structure 9 Block (Field)

9

0.67

0.755

0.52

0.834

0.55

0.878

0.43

0.980

Artificial structure 9 Field Field 9 Weed 9 Artificial structure

2 2

0.85 0.11

0.471 0.974

0.71 0.06

0.529 0.969

0.48 3.32

0.688 0.036*

1.02 0.51

0.374 0.960

Residual Total

9 47

Data were square root transformed prior to analysis. Treatment factors (Weed, Artificial structure) refer to the presence/absence of weeds and artificial structure, respectively. Block was nested in Field as indicated by parentheses; x indicates interaction between variables; P-values refer to unique permutational runs, except for main effects of factors ‘‘Weed’’ and ‘‘Artificial structure,’’ where Monte Carlo P-values were used; * indicates significant effects (P \ 0.05)

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Arable weeds in organically managed wheat fields foster carabid beetles

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artificial structure. Mean daily surface temperatures and light intensities did not vary among fields (permutational ANOVA; Pseudo-F2,4 = 1.75, P = 0.279). Average soil water content varied from 21.20 to 27.90% dw (permutational ANOVA; Pseudo- F2,45 = 55.39, P \ 0.001) between the three winter wheat fields.

Discussion

Fig. 2 Mean activity density of carabids (with standard error bars) in experimental treatments as estimated by pitfall traps (n = 48). Treatments include plots with weeds removed or weeds present and without artificial structure (filled triangle) or with artificial structure (filled circle)

Our results suggest that the observed positive link between arable weeds and carabid populations in organically managed wheat fields is partly driven by resource-mediated effects, including a higher availability of weed-borne resources and herbivorous prey in weed-covered plots. Structure-mediated effects, including changes in microclimate, further affect carabid activity density. Carabid activity density

(Table 1; ‘‘Artificial structure’’). We found 7.4 ± 0.5 carabid species in experimental plots with weeds, whereas weed removal led on average to 11% lower species richness. The composition of trophic groups with respect to total activity densities and species richness of carnivorous, phytophagous, and omnivorous carabid species, respectively, was not affected by experimental manipulations but varied among fields (permutational ANOVA; activity density: Pseudo-F2,47 = 25.01, P \ 0.001; species richness: Pseudo-F2,47 = 24.28, P = 0.006). A total of 520 sap-sucking herbivores (Rynchota: 208 Cicadina, 187 Aphidina, and 125 Heteroptera) were collected at the end of the experiment. Removal of weeds significantly affected the abundance of sap-sucking herbivores, but the response depended on the presence of artificial structure, and treatment effects varied spatially across fields (Table 1; ‘‘Weed’’ x ‘‘Artificial structure’’ x ‘‘Field’’). When weeds were removed, mean abundance of leafhoppers and bugs in two of the fields was on average 50% lower than in plots with weeds. In one of the fields, our treatments did not affect leafhopper or bug abundance. Aphid abundance generally showed no consistent response to our treatments across the three fields. A total of 6580 epedaphic collembolans (Collembola: 6389 Entomobryidae, 191 Isotomidae) were sampled with pitfall traps. Activity density of collembolans varied spatially among fields (Table 1; ‘‘Field’’) but was not significantly affected by our experimental treatments (Table 1; e.g. ‘‘Weed’’ or ‘‘Artificial structure’’). Mean daily temperature and light intensity differed significantly between vegetation types (permutational ANOVA; Pseudo-F2,4 = 13.82, P = 0.034). Under wheat stands alone the mean daily temperature was on average 3.3°C higher and light intensity was 29005 lux higher in comparison with the average values under weeds and under

Carabid activity density was highest in control plots with natural crop plants and weeds only. In bare-ground plots, i.e. with crop plants only, mean activity density was 41% lower than in weed-covered control plots, supporting our first hypothesis. Yardim and Edwards (2002) found significantly lower activity densities of carabids in weed-free plots established by herbicide application when compared to unmanipulated plots with high weed biomasses in tomato agroecosystems. Reduced weed densities established by weed removal negatively affected grounddwelling arthropod predators in a soybean field (Balfour and Rypstra 1998), whereas increased weediness enhanced the activity density of the most common carabid species in a manipulative experiment in a maize field (Hough-Goldstein et al. 2004). The complex effects of structural properties and weed-associated food resources on natural enemies were emphasized by Honek and Jarosik (2000). In their study, carabid populations in agricultural fields were primarily affected by the density of crop stands, the presence of aphids and seeds of crops and weeds on the ground. However, in former studies, structure- and resource-mediated effects were not analyzed individually. The simulation of weed structure in our experiment was hypothesized to dampen the negative effect of weed removal on carabid activity density. This hypothesis was confirmed, as weed removal reduced activity density by 28% when artificial structure was present and by 41% when neither artificial structure nor natural weeds were present compared to the control treatment. The addition of artificial weed structure reduced temperature and light intensity significantly and to the same extent as natural weed vegetation compared to bare-ground plots. The two dominant species in our study, P. melanarius and H. rufipes, prefer vegetation-covered

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habitats over bare-ground areas (Armstrong and McKinlay 1997; Shearin et al. 2007). In addition to providing favorable microclimatic conditions, one structure-mediated effect of weeds on carabids may have been the provision of shelter from unfavorable weather conditions. Pavuk et al. (1997) observed that the presence of broad-leaved weeds enhanced carabid activity density in years with regular rainfall, whereas activity density was not affected by weed presence when rainfall was sparse. It is further known that increased habitat structural complexity affects predator– predator interactions by creating refuges for intraguild prey and thereby reduces the strength of intraguild predation, resulting in higher predator densities (reviewed by Janssen et al. 2007). Such changes in predator–predator interactions in artificial structure plots and natural weed plots may also have contributed to structure-mediated effects on activity density of carnivorous and omnivorous carabids, which altogether accounted for 99% of the trapped individuals in our experiment. In field experiments, artificial structure has rarely been used to simulate structure-mediated effects of weeds on natural enemies (McCoy and Bell 1991). Birkhofer et al. (2008) used plastic plants to simulate the structural characteristics of weeds in a conventionally managed wheat field. Contrary to our study, the presence of artificial structure had no significant effect on the activity density of carabids. Mathews et al. (2004) simulated structural characteristics of a mulch layer on the ground of apple orchards using polyester fiberfill mulch but observed that simulated mulch did not enhance the activity density of generalist predators compared to compost mulch. Both studies (Mathews et al. 2004, Birkhofer et al. 2008) concluded that resource-mediated effects of weeds or mulch, i.e. enhancement of herbivorous or detritivorous prey, were likely to affect generalist predators to a larger extent than structure-mediated effects. Our results support this observation for carabids in organically managed winter wheat fields but also show that structural characteristics (e.g. microclimatic conditions) add to the positive effect of weeds on carabid activity density. In order to improve our understanding of resourcemediated effects, we investigated the effect of the presence of natural weeds on herbivorous and detritivorous prey and on trophic groups within carabid populations. While there was no significant effect on activity densities and species richness of trophic groups, the removal of weeds reduced the abundance of leafhoppers and true bugs in two fields. The presence of weeds in cotton fields was shown to lead to higher densities in 9 out of 11 herbivorous taxa compared to weed-free cotton stands (Showler and Greenberg 2003). The inconsistent response of herbivores in our study may reflect the complex interactions of factors that determine the local abundance of herbivores in cereal fields. Such factors include the activity of natural enemies, patch size,

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stand density, and the nutritional status of host plants (Denno and Roderick 1991). The activity density of epedaphic collembolans was not affected by the removal of weeds or introduction of artificial structure but varied spatially among fields. As soil water content varied significantly between fields, a possible explanation for the observed spatial variation in collembolan activity density is the strong impact of local habitat conditions on Collembola abundance (e.g. Pflug and Wolters 2001). The positive response of carabid activity density to weed presence suggests that resource-mediated effects of weeds may partly act via the enhancement of plant sap-sucking prey for predatory carabids, but that due to inconsistent response of sap-sucking prey, the provision of additional plant food resources such as nectar, pollen, or seeds may be a more important resource-mediated effect of weeds on carabids in organically managed cereal fields. In addition, carabids may benefit from a positive interaction between weeds and prey taxa that were not sampled in our study (e.g. earthworms; Symondson et al. 2000). All trophic groups of carabids may thus benefit from this holistic weed effect, which may explain why our experiment did not affect trophic group composition of carabid populations. Despite this positive effect of weed resources on carabid activity density and contrary to our third hypothesis, the introduction of artificial structure in addition to natural weeds reduced carabid activity density by 24% when compared to weed-covered control plots. An artificial enhancement of structural complexity above the natural level may thus not enhance but rather reduce carabid activity density. In contrast, replacement of weeds by artificial structure reduced carabid activity density similarly, although weed-associated food resources were absent in these plots with artificial structure only. We suggest that short-term addition of artificial structure to already established weed communities may not enhance local carabid populations. Instead, such experimental disturbance may even reduce carabid numbers below the natural level, as highly complex-structured habitats increase the search time for prey by natural enemies (e.g. Meiners and Obermaier 2004), which may ultimately lead to a reduced attractiveness of structurally rich patches. Carabid species richness The species richness of carabids was reduced by the removal of naturally growing weeds, as predicted by our first hypothesis, but was not affected by the introduction of artificial structure, contrary to our second and third hypothesis. We thus attribute the observed positive effect of weeds on carabid diversity primarily to resource-mediated effects. Carnivorous, phytophagous, and omnivorous carabid species may have benefited from diverse weed

Arable weeds in organically managed wheat fields foster carabid beetles

communities in organically managed winter wheat fields. Phytophagous and omnivorous carabids often consume weed-borne resources, and many seed-consuming carabid species have preferences for seeds of particular weed species (Honek et al. 2007). Sasakawa (2010) observed close species-to-species links between plant-feeding carabids and weeds, and such relationships likely contributed to the observed beneficial effect of weed presence on carabid species richness in our study. Similarly, several carnivorous carabid species show preference for prey species based on the differences in their nutritional quality (Mundy et al. 2000). The assumption that all trophic groups within the investigated carabid populations benefited from holistic resource-mediated weed effects is partly supported by the fact that our manipulations affected overall species richness, but not the diversity of individual trophic groups. Weed presence in crop monocultures further enhances the diversity of structural elements and available microhabitats for carabid species, e.g. for oviposition (Lawton 1983; McCoy and Bell 1991). Carabus clatratus individuals select specific microhabitats for oviposition in laboratory experiments (Huk and Ku¨hne 1999). In the field, such preferences may be linked to small-scale plant structure, as P. melanarius prefers barley plants as egglaying sites over Brussels sprout plants (Trefas and van Lenteren 2008). The diverse plant community in organically managed fields provides a range of microhabitats and supports preferences of different carabid species.

Conclusions The presence of arable weeds in organically managed wheat fields fosters carabid activity density and species richness via resource-mediated effects. Resource-mediated effects of weeds may partly be related to the attraction of herbivorous prey, but the provision of plant-borne resources or soil-living prey may be more important. Carabid activity density is also affected by structure-mediated effects, and these effects are most likely caused by the provision of a favorable microclimate. Thus, the presence of weeds in organically managed wheat fields enhances carabid activity density and diversity and needs to be integrated into future management strategies for natural enemy conservation. However, our results do not suggest that the positive relationship between weeds and carabids necessarily leads to improved pest suppression, as weed-borne resources may distract carabids from target pests (see also Birkhofer et al. 2008; Straub et al. 2008). Further research should focus on the particular trophic links among dominant weeds, natural enemies, and their prey and may thereby help to improve management strategies that try to strengthen conservation biological control in organically managed fields (Zehnder et al. 2007).

81 Acknowledgments We thank two anonymous referees for their helpful comments on an earlier version of this manuscript. We are very grateful to the farmers, the Mager family, for permitting us to conduct our experiments on their fields. Thanks are due to Sascha Behr, Sergej Sereda, Janine Groh, and Kerstin Birkhofer for their assistance with the fieldwork, Sabine Wamser and Dennis Baulechner for assistance with sample determination, and Chistine Tandler, Susanne Vesper, Sabine Rauch, and Martin Kro¨ckel for technical support. This study was carried out within the BIOPLEX project (BIOLOG Europe) funded by the German Federal Ministry of Education and Research (BMBF).

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